Sources of vase life variation in cut roses: A review

Postharvest Biology and Technology 78 (2013) 1–15

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Review

Sources of vase life variation in cut roses: A review Dimitrios Fanourakis a,∗ , Roland Pieruschka a , Andreas Savvides b,c , Andrew J. Macnish d , Vaia Sarlikioti e , Ernst J. Woltering b,f a

Plant Sciences (IBG-2), Forschungszentrum Jülich, D-52425 Jülich, Germany Wageningen University, Horticultural Supply Chains Group, P.O. Box 630, 6700AP Wageningen, The Netherlands Wageningen UR Greenhouse Horticulture, P.O. Box 644, 6700AP Wageningen, The Netherlands d Horticulture and Forestry Science, Department of Agriculture, Fisheries and Forestry, Maroochy Research Facility, 47 Mayers Road, Nambour, Qld 4560, Australia e INRA Centre d’Avignon, UR 1115, PSH, Site Agroparc, 84914 Avignon cedex 9, France f Food and Biobased Research, Wageningen University and Research Centre, P.O. Box 17, 6700 AA Wageningen, The Netherlands b c

a r t i c l e

i n f o

Article history: Received 1 October 2012 Accepted 6 December 2012 Keywords: Carbohydrate status Postharvest Preharvest Rosa hybrida Stomatal responsiveness Vase life evaluation protocol

a b s t r a c t In determining vase life (VL), it is often not considered that the measured VL in a particular experiment may greatly depend on both the preharvest and evaluation environmental conditions. This makes the comparison between studies difficult and may lead to erroneous interpretation of results. In this review, we critically discuss the effect of the growth environment on the VL of cut roses. This effect is mainly related to changes in stomatal responsiveness, regulating water loss, whereas cut flower carbohydrate status appears less critical. When comparing cultivars, postharvest water loss and VL often show no correlation, indicating that components such as variation in the tissue resistance to cavitate and/or collapse at low water potential play an important role in the incidence of water stress symptoms. The effect of the growth environment on these components remains unknown. Botrytis cinerea sporulation and infection, as well as cut rose susceptibility to the pathogen are also affected by the growth environment, with the latter being largely unexplored. A huge variability in the choices made with respect to the experimental setup (harvest/conditioning methods, test room conditions and VL terminating symptoms) is reported. We highlight that these decisions, though frequently overlooked, influence the outcome of the study. Specifications for each of these factors are proposed as necessary to achieve a common VL protocol. Documentation of both preharvest conditions and a number of postharvest factors, including the test room conditions, is recommended not only for assisting comparisons between studies, but also to identify factors with major effects on VL. © 2012 Elsevier B.V. All rights reserved.

1. Introduction The vase life (VL) of cut flowers refers to the duration from placement of stems in a vase solution to the loss of visible ornamental value, and is synonymous with display life, keeping or lasting quality (Halevy and Mayak, 1981). It is an important measure to select genotypes in breeding programs, to determine the effects of storage and distribution conditions, as well as to design optimal packaging and chemical treatment solutions. The VL terminating criteria are mainly either water stress symptoms (van Doorn, 1997, 2012) or Botrytis cinerea infection symptoms (van Meeteren, 2007; Macnish et al., 2010b). The VL is determined by the phenotype × postharvest

Abbreviations: AL, supplemental assimilation light; gs , stomatal conductance; RH, relative air humidity; Tair , air temperature; v, air velocity; VL, vase life; VPD, vapour pressure deficit;  , water potential. ∗ Corresponding author. Tel.: +49 2461 614411; fax: +49 2461 612492. E-mail address: [email protected] (D. Fanourakis). 0925-5214/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.postharvbio.2012.12.001

conditions interaction, while phenotype is the result of the interaction between genotype and growth environment (Fig. 1). For the past decades, an increasing number of studies has been devoted to quantifying the VL of different genotypes grown (preharvest) and tested (postharvest) under a range of conditions. The inherent variability and rudimentary description of the pre- and postharvest conditions observed among the different studies limit the application of these resources in horticulture and constrain progress of our understanding of the underlying processes. Therefore, a systematic revision of the known effects of the pre- and postharvest conditions on VL is essential to both draw attention to the need for a more complete documentation of the experimental conditions and establish common standards for VL analysis. In this review, we firstly survey the effect of abiotic factors [i.e. light (intensity, quality, and period), (air and soil) temperature, carbon dioxide, air humidity, air velocity, and nutrition], and their interactions during plant growth with the VL of cut roses. The effects of the growth environment on B. cinerea sporulation and infection, as well as on the cut flower susceptibility to the pathogen,

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Growth environment

Genotype

Postharvest factors

Phenotype

Vase life

Fig. 1. Factors determining vase life.

are also considered. Secondly, we discuss the genetic component, which has very prominent effects on VL. Scattered information in the literature about factors determining cultivar differences in VL is collectively examined. Thirdly, we illustrate how the experimental setup (harvest/conditioning methods, test room conditions, and VL terminating symptoms), influences the measurements. Finally, we suggest standardization for these factors (i.e. harvest and conditioning methods, as well as terminating symptoms) and the need for their documentation in VL experiments together with test room conditions. The cases (and references) presented in this review refer to cut rose, which has been studied most extensively, as compared to other cut flowers. However, most concepts addressed here are equally applicable to other cut flowers as well. 2. Preharvest factors For many years research has mainly focused on maximizing VL during the postharvest period. However, the physiological and anatomical characteristics that ultimately determine the VL potential of the cut flower are formed during the preharvest period (genotype × growth environment interaction; van Meeteren et al., 2005; Fanourakis et al., 2012b) (Fig. 1). Understanding how the growth environment affects the VL potential and its interaction with the genetic background would contribute to the efficient utilization of an optimal combination of growth conditions and genotype, with the aim of maximizing the postharvest performance of cut flowers. 2.1. Environmental factors Marissen and Benninga (2001) sampled the cv. First Red from 35 growers in The Netherlands, and found a considerable variation in VL (up to 70%) when examined under identical postharvest conditions. Since both the genetic component and the postharvest conditions can be excluded, this variation in VL was caused solely by the growth environment. To this end, the phenotype is not very informative about the genotype without taking into account the environmental conditions during growth. Below we address the effect of important environmental factors during growth on the VL of cut roses, and we then touch upon the seasonal effects. 2.1.1. Air humidity Relative air humidity (RH) is the ratio of the amount of water vapour in the air relative to the amount of water vapour that would be present at saturation, and it is routinely measured in many greenhouses. RH depends on both the amount of moisture available and air temperature (Tair ). Vapour pressure deficit (VPD) combines the effects of both RH and temperature, and is the difference between saturation vapour pressure and actual air vapour pressure. VPD characterizes the evaporative demand of air, and it is one of the key drivers of transpiration. However, RH remains the commonly used measure in horticulture, and it is also used in the relevant literature. High RH is common in greenhouses especially during the winter, mainly due to low ventilation (Mortensen and Fjeld, 1995; Kittas and Bartzanas, 2007; Max et al., 2009). Elevated RH (≥85%) exerts a

minor effect on the growth and visual quality of cut roses (Torre and Fjeld, 2001), though it often results in decreased (9–80%, depending on the cultivar) VL and reduced (3–27%, depending on the cultivar) flower diameter (Mortensen and Gislerød, 2005; Fanourakis et al., 2012a). High RH-grown roses had higher rates of water loss, compared to roses grown at moderate RH, as a result of less responsive stomata to both water stress and darkness (Fanourakis et al., 2012a). The stomatal malfunctioning was related to the lower foliar abscisic acid content (Rezaei Nejad and van Meeteren, 2008; Arve et al., 2013). Sensitive cultivars whose stomatal functionality was more impaired by high RH during growth, had a lower level of endogenous leaf abscisic acid content, as compared to tolerant cultivars (personal communication: H.G. Gebraegziabher). A decrease in stomatal responsiveness is induced when the RH levels during leaf expansion are high for a large part of the day (12 h day−1 , Ottosen et al., 2002; >12 h day−1 , In et al., 2006; >18 h day−1 , Mortensen and Gislerød, 2005). Stomatal responsiveness can be improved by adjusting the humidity level (i.e. hours of moderate RH per day as indicated above) either during the day or night (In et al., 2006). An alternative approach is an increase in Tair (by 10 ◦ C), instead of a decrease in RH for the same period, which has been suggested to be equally effective in improving stomatal responsiveness (Mortensen and Gislerød, 2011), a step which may not be favoured by horticulturalists because of increased costs for heating the greenhouses. An increase in the transpiration rate during growth may be induced by increasing the air velocity (v), which in turn enhances the boundary layer conductance (discussed in detail below). The effect of v on stomatal functionality at high RH environments was tested in two experiments, where no effect was observed (Mortensen and Gislerød, 1997; In et al., 2006). Over a longer time period (days), elevated RH during the last phase of leaf expansion (≥2 days at 19 ◦ C) has been shown to be the most decisive for stomatal closing ability (Fanourakis et al., 2011). Unlike other species (Phaseolus vulgaris, Pospisilova, 1996; Tradescantia virginiana, Rezaei Nejad and van Meeteren, 2008), alterations in ambient humidity after complete leaf expansion have no effect on the stomatal response characteristics in rose (Mortensen and Gislerød, 2000; Fanourakis et al., 2010, 2011). High RH has been shown to affect neither stem hydraulic conductivity nor its recovery after artificial induction of air emboli at the cut surface (Fanourakis et al., 2012a). Torre et al. (2003) reported that leaves of high RH-grown plants show reduced density of vascular tissue (expected to increase leaf hydraulic resistance; Sack and Holbrook, 2006; Nardini et al., 2012), and increased intercellular air spaces (expected to decrease leaf hydraulic resistance; Cochard et al., 2004; Sack and Holbrook, 2006). However, the degree and the relative importance of these responses have as yet not been quantified. Leaf hydraulic resistance data will yield a deeper understanding of the consequences of a more humid environment on the leaf water balance. Environmental factors or cultivation practices that effectively counteract the negative effect of long-term cultivation at high RH on VL of cut roses, without decreasing the VPD, have been rarely reported. In a growth chamber experiment, Terfa et al. (2012) studied the stomatal responsiveness of roses grown at high RH and either using high pressure sodium lamps or light emitting diodes (red and blue) having 5 and 20% blue light, respectively. It was found that rose leaves developed under light emitting diodes had more responsive stomata, compared to leaves grown under high pressure sodium lamps. It is well known that blue light affects stomatal properties (Shimazaki et al., 2007; Hogewoning et al., 2010b), but the interaction of the blue light effect with elevated RH on determining stomatal closing ability, and whether VL is affected under these conditions have not been studied in detail so far. Mortensen and Gislerød (2005) showed that severe drought stress during growth at high RH increased the VL in rose (16–120%, depending

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on the cultivar), but its alleviating effect on VL was at the expense of growth. The authors attributed this positive effect of drought stress on VL of high RH-grown roses to the stimulation of stomatal functionality. A more hydrosensitive leaf water potential ( ; Auge et al., 1986) and a higher stem resistance to air emboli [shown for Zinnia elegans (Twumasi et al., 2005), and chrysanthemum (van Meeteren et al., 2005)] might also have been involved. Partial root drying, an irrigation technique where a part of the root system is exposed to wet and the other part to dry soil, intensifies the root-toshoot abscisic acid signalling without a strong yield penalty (Stoll et al., 2000). Partial root drying was found to enhance stomatal responsiveness in rose plants grown at moderate RH, but it was not successful in plants grown at high RH due to a very slow rate of decrease in soil moisture content and, thus, a dry cycle that is too long (D. Fanourakis, S.M.P. Carvalho, and E. Heuvelink, unpublished results). Future endeavours should, therefore, focus on the whole root zone. Regulated deficit irrigation, where the irrigation is decreased during specific periods of the crop cycle (Wakrim et al., 2005), or increased salinity (Hwang and Morris, 1994), might be tested as alternatives. 2.1.2. Botrytis cinerea B. cinerea is a ubiquitous pathogen (Dean et al., 2012) and its spores can enter the greenhouse through ventilation openings, on people, or through the propagation material (Dik and Wubben, 2004). The pathogen can then spread throughout the crop by air circulation, water, or insects (Jarvis, 1980). B. cinerea can survive between crop cycles on plant debris for up to 1 year (Araújo et al., 2005). On plants, B. cinerea can be present either as conidia (Salinas et al., 1989), or as a latent infection, which is asymptomatic (Elad, 1988). In the presence of condensation, B. cinerea conidia can germinate within 5 h and symptoms of disease become visible within 1 day (Salinas et al., 1989). B. cinerea is the only biotic factor affecting VL, while its infection symptoms represent a major VL terminating criterion (van Meeteren, 2007; Macnish et al., 2010b). The environmental conditions during growth may not only affect the sporulation and infection of B. cinerea, but also the cut rose susceptibility to the pathogen, as surveyed below. 2.1.2.1. Sporulation and infection. The number of B. cinerea infections in cut roses during the postharvest period has been positively correlated with the spore density in glasshouses (Kerssies et al., 1994). Spore density, in turn, increases with sporulation. Free water on the tissue surface (at least 4 h) is a prerequisite for sporulation (Sirjusingh and Sutton, 1996). The optimum in vitro temperature for sporulation ranged between 17 and 18 ◦ C, while temperatures above or below this range decreased sporulation (Sosa-Alvarez et al., 1995). Limited sporulation can take place at 25 ◦ C, while no sporulation was observed at 30 ◦ C. Very high (50 mmol mol−1 ) carbon dioxide levels reduced sporulation of B. cinerea (Svircev et al., 1984), but such levels are not realized in commercial practice. Sporulation can also be influenced by light quality, where near ultraviolet light is the most effective wavelength in inducing sporulation (Honda and Yunoki, 1978; West et al., 2000). Spore density in glasshouses has also been found to be dependent on the presence of plant debris, being a primary inoculum source of B. cinerea (Yunis and Elad, 1989). Elevated RH levels during crop growth resulted in an increased number of B. cinerea infections (Kerssies et al., 1994). Under high RH, the dew point is reached with a small decrease in Tair leading to condensation, which results in infection (Salinas et al., 1989). Very high RH levels (94%) may also stimulate infections in the absence of free water (Williamson et al., 1995).

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2.1.2.2. Rose susceptibility. Marois et al. (1988) reported that high VPD during the preharvest period, caused by a combination of higher Tair and lower RH, was correlated with lower cut rose susceptibility to infections by B. cinerea. Whereas, Hammer and Evensen (1996) did not find an effect of Tair , RH, or VPD on cut rose susceptibility in both greenhouse and growth chamber experiments. Additionally, they showed that high RH during production increased latent infections (symptomless at harvest). In the same study, it was reported that flowers grown under high v (0.55 m s−1 ) were significantly more susceptible to infection than flowers grown under low v (0.18 m s−1 ). Calcium deficiency increased the susceptibility to B. cinerea (Baas et al., 2000), while higher cut flower calcium content, as a result of higher calcium concentration in the nutrient solution, decreased the susceptibility to B. cinerea (Volpin and Elad, 1991; Bar-Tal et al., 2001). Interestingly, de Capdeville et al. (2005) showed that spraying roses with calcium sulphate (10 mM) one day before harvest decreased the infections by B. cinerea and significantly prolonged VL for at least 30%. In addition, tissue mechanical damage, for instance as a result of cultivation or harvesting practices, has been shown to increase the susceptibility to the pathogen (Verhoeff, 1980). 2.1.3. Light conditions Supplemental assimilation light (AL) is frequently used to control both the photoperiod and light intensity in greenhouses in northern Europe (Heuvelink et al., 2006; Hemming, 2011). It is often applied in horticulture to enhance productivity, but also to reduce the visual variation in flower quality throughout the year (Fjeld et al., 1994). A number of different AL sources is commercially available such as fluorescent tubes, high pressure sodium lamps and more recently light emitting diodes that differ in the light quality they emit (Hogewoning et al., 2010a; Savvides et al., 2012). High pressure sodium lamps are the most commonly used AL sources in protected cultivation, due to their highest energy efficiency (van Ieperen and Trouwborst, 2008), while light emitting diodes are currently gaining importance (van Ieperen, 2012). The number of crops, where AL is applied, is increasing, and the applied light levels are reportedly higher compared to five years ago (Heuvelink et al., 2006). Additionally, higher light intensities are realized in modern greenhouses through newly introduced designs (less constructional elements resulting in less shading), cover materials with higher light permeability and materials increasing light transmission inside the greenhouse (e.g. white ground cover; Hemming, 2011; Max et al., 2012). Another emerging trend in horticulture is greenhouse cover materials that influence the directional quality of light, by scattering it, without reducing its intensity (Hemming et al., 2008). Diffuse light penetrates deeper into the canopy (i.e. more uniform vertical distribution of light) as compared to direct light, enhancing production in various ornamental crops (Hemming et al., 2008; Markvart et al., 2010), including roses (Victoria et al., 2012). 2.1.3.1. Photoperiod. Continuous light (i.e. 24 h light period) induces visible injuries (e.g. chlorosis and necrosis) in several plant species such as tomato and eggplant, while in others, including roses, it does not lead to injuries but enhances productivity (Velez-Ramirez et al., 2011). Due to its yield promoting effect, it is sometimes applied in cut rose crops (Mortensen and Gislerød, 1999). Mortensen and Fjeld (1998) showed that extending the photoperiod from 16 to 20 h did not affect the VL of cut roses. However, a further extension of the photoperiod to continuous light resulted in a shorter VL (5–47%, depending on the cultivar). An increase of the photoperiod from 12 through 16 to 20 h did not affect night time stomatal conductance (gs ), indicating no effect on stomatal

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responsiveness (Blom-Zandstra et al., 1995; Mortensen and Fjeld, 1998). A further increase of the photoperiod to 24 h resulted in significantly higher gs , compared to roses grown at shorter photoperiods, due to less responsive stomata (Mortensen and Fjeld, 1998; Mortensen and Gislerød, 1999). The impaired ability of stomata to respond to closing stimuli, as a result of continuous light, was related to the depletion of foliar abscisic acid (Arve et al., 2013). Contrary to the findings of Mortensen and co-workers, Slootweg and van Meeteren (1991) reported that winter roses grown under AL (for 20 h day−1 ) showed higher rates of water loss during the postharvest phase, compared to roses grown under natural light alone (about 10 h day−1 ), due to less responsive stomata. Mortensen and Fjeld (1998) proposed that this discrepancy was probably due to increased greenhouse RH (not recorded in the study of Slootweg and van Meeteren, 1991), but such an interpretation implies that the RH was elevated only in the AL treatment. Slootweg (1997) studied the effect of AL on stem hydraulic conductivity of cut roses. In that study, roses grown under AL (for 20 h day−1 ) showed a slower rehydration rate, following a 2 h dehydration event, compared to those grown under natural light. Differences in the rehydration rate were attributed to the lower stem hydraulic conductivity of roses grown under AL. The amount of light received per day can be increased by extending the photoperiod and/or increasing the light intensity. Increasing the light intensity per se does not negatively affect VL at shorter photoperiods than continuous light. The effect of continuous light has been discussed by Velez-Ramirez et al. (2011) showing that it induces different levels of injury in various species, excluding roses. This effect depends on the light intensity (less injury at lower intensity), light quality (e.g. less injury when using solar light) and Tair (e.g. less injury at lower or fluctuating Tair ). Future studies are required to investigate the role of these factors on the continuous light-induced attenuation of stomatal closing ability. 2.1.3.2. Light intensity. A limited number of studies has reported a negative effect of increasing light intensity on VL (0.3–2.5 days less) depending on the cultivar (Fjeld et al., 1992) and the nitrogen levels applied to the crop (Armitage and Tsujita, 1979). In a later study, Fjeld et al. (1994) showed that increasing the intensity of the AL from 130 to 370 ␮mol m−2 s−1 to the background illumination enhanced the VL of cut roses by 9–30%, depending on the cultivar, and proposed that improved carbohydrate status mediates this effect. This hypothesis is supported by the observations that the addition of sugar (sucrose, 44 mM) to the vase solution of roses grown without AL increased their VL to the level of roses grown under AL. However, Marissen (2001) found that while AL (by adding 100 ␮mol m−2 s−1 to the background illumination) increased the leaf and flower bud carbohydrate content in all four studied cultivars, it significantly increased (30%) VL in one of them. No effect of increased cut flower carbohydrate content, as a result of AL, on VL was also reported by Vogelezang et al. (2000). Other studies where AL was added, but carbohydrate content was not assessed, found no increase in VL (Särkkä and Rita, 1997; Bredmose, 1998; Särkkä, 2002). Thus, although the current data are not conclusive, the effect of increasing light intensity and carbohydrate content is likely to be small. Defined light conditions in future studies are needed to unravel the effect of light intensity on VL. The effect of light intensity on the control of water loss in rose has been investigated in a study by Blom-Zandstra et al. (1995). It was shown that increasing light intensity from 50 to 150 ␮mol m−2 s−1 increased the transpiration rate during the light period, but did not affect the gs during the dark period, indicating that stomatal closure was not impaired by higher light intensities. 2.1.3.3. Light (directional and spectral) quality. Roses grown under diffuse light (by using diffuse glass greenhouse cover), showed the

same VL with flower stalks grown under direct light (by using clear glass greenhouse cover; Victoria et al., 2012). Growing roses under high pressure sodium lamps (for 24 h day−1 ) slightly increased (by 1.1 days; Garello et al., 1995) or had no effect (Roberts et al., 1993) on their VL, compared to roses grown under metal halide lamps. Similarly, no difference in the VL was recorded when roses were grown under either high pressure sodium lamps or fluorescent tubes for 20 h per day (Mortensen and Fjeld, 1998). Also, gs at different times of the photoperiod was not significantly different in roses grown under either high pressure sodium lamps or fluorescent tubes (Mortensen and Fjeld, 1998). Similarly, stomatal responsiveness was comparable in rose plants grown under either high pressure sodium lamps or light emitting diodes (20% blue, 80% red; Terfa et al., 2012). In a growth chamber experiment, Blom-Zandstra et al. (1995) extended the photoperiod with different AL sources. It was reported that orange light during that period resulted in higher gs in both light and dark periods, compared to plants receiving blue or white light during the photoperiodic extension, in one of the two cultivars tested. In conclusion, the difference in light quality of currently used AL sources has most likely a negligible effect on VL. The application of light emitting diodes, as potential AL source, is becoming increasingly important, opening new opportunities to control and to study the light quality effect on roses in protected cultivation systems in more detail (van Ieperen, 2012). 2.1.4. Additional environmental factors and seasonality 2.1.4.1. Temperature. The optimum Tair during rose flower production for maximum VL varies from 21 to 24 ◦ C. A lower Tair down to 12 ◦ C or higher up to 27 ◦ C resulted in shorter VL (39 and 34%, respectively; Moe, 1975). Later studies confirmed these findings (Mortensen and Gislerød, 1996; Marissen, 2001). Lower preharvest Tair has been suggested to enhance flower bud opening during VL (Marissen, 2001; Marissen and Benninga, 2001), whereas Gudin (1992) showed that the enhancement of the opening takes place when the flower bud is harvested at an earlier stage than recommended. Additionally, it was shown that a short period of low Tair (12 ◦ C) might also decrease (5–37%) VL depending on the stage of the crop (Moe, 1975). Contrary to this, Tair diel fluctuations, when the mean diel Tair is kept constant, have no effect on VL (Vogelezang et al., 2000; Bredmose and Nielsen, 2004). Moe (1975) showed that increasing Tair stepwise from 15 to 24 ◦ C increased the cut flower water uptake during VL, while roses grown under 21 ◦ C Tair maintained higher water uptake for a longer (postharvest) period compared to roses grown under higher Tair . There is only one study on the effect of root temperature on the VL of cut roses, where VL increased (25%) when root temperature decreased from 22 to 12 ◦ C (Mortensen and Gislerød, 1996). In commercial practice, Tair is generally set to optimize visual quality and production. Therefore, temperatures that would potentially decrease VL, are generally avoided. Less emphasis has been placed on root temperature, which may affect VL. Such information may be directly translated into commercial practice, where nutrient tanks are often outside the greenhouse, and their temperature deviates from greenhouse Tair (e.g. low solution temperature during winter). 2.1.4.2. Carbon dioxide. Carbon dioxide enrichment is a common practice in commercial greenhouses at high altitudes, and is usually combined with decreased ventilation to attain the target CO2 concentration (Dik and Wubben, 2004). Mattson and Widmer (1971) reported a slightly longer (7%) VL, as a result of CO2 enrichment (2000 ␮mol mol−1 ), in one out of four studied cultivars. Mortensen and Gislerød (1996) also found no significant effect of CO2 enrichment (800 ␮mol mol−1 ) on VL, whereas Urban et al. (2002) reported

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a longer VL (21–33%, depending on the cultivar) in roses grown at high CO2 concentration (700 ␮mol mol−1 ). In the latter study, it was concluded that this positive effect of elevated CO2 on the VL of cut roses was due to both more hydrosensitive stomata (i.e. closing at higher  ) and lower minimum gs . Although not assessed in the above-mentioned studies, carbon dioxide enrichment is expected to improve cut flower carbohydrate status. Similarly to increasing light intensity, which also enhances carbohydrate content, carbon dioxide fertilization showed generally limited effects on VL. The three studies conducted on the influence of CO2 enrichment on VL, observed a positive effect in specific cultivars. To our knowledge, respective studies in newly introduced cultivars are currently lacking. 2.1.4.3. Air velocity. Low v (0.08 m s−1 ) during growth resulted in considerably shorter VL (38–108%, depending on the cultivar), compared to roses grown at higher v (≥0.21 m s−1 ; Mortensen and Gislerød, 1997). Such low v levels resulted in low transpiration rates during growth due to a decreased boundary layer conductance (discussed in detail below). Under these conditions, humidity accumulates within the boundary layer and may be substantially higher than the ambient RH, inducing stomatal malfunctioning similar to plants grown under high RH levels. Thus, the negative effect of low v on VL of cut roses was related to disturbed water balance due to less responsive stomata (Mortensen and Gislerød, 1997). Increasing the air circulation on the other hand, by blowing air, resulted in a (22%) longer VL, compared to the VL of flower stalks grown without any air circulation (In et al., 2006). RH within the boundary layer was reduced in the elevated v treatment, stimulating stomatal functioning. Increasing v at elevated RH environments, however, is not likely to improve stomatal responsiveness. Under elevated ambient RH and high v (i.e. high boundary layer conductance), the humidity within the boundary layer will be close to ambient RH, which (still) impairs stomatal closing ability. Although only two studies have been conducted on the effect of v on VL (at moderate RH levels), they illustrate the need for further work. A comprehensive analysis of stomatal responsiveness under varying v has not yet been performed. However, accumulation of humidity in the boundary layer may be the major driver of stomatal functioning under varying v. Further experiments are needed to test whether the stomatal functioning under low v is similar to that at elevated RH. Although low v conditions may not appear in growth chambers with (strong) air circulation systems, they might be particularly relevant within dense rose canopies. 2.1.4.4. Nutrition. In general, increasing the EC level of the irrigation solution up to about 5 m S cm−1 either by increasing macronutrients’ concentration (Gislerød et al., 1993; Urban et al., 1995; Sonneveld et al., 1999) or by adding sodium chloride (Sonneveld et al., 1999) exerted a very small effect on VL, compared to normal EC levels (about 2 m S cm−1 ). Specifically, an increase of nitrogen concentration in the nutrient solution decreased VL of rose flowers by 0.3–2.5 days (Armitage and Tsujita, 1979; Menard et al., 1996). This decrease of VL due to a higher nitrogen concentration in the nutrient solution was not found in the study of Gislerød et al. (1993), though the nitrogen levels were similar with the study of Menard et al. (1996). Lowering the nutrient concentrations (to 40%), decreased VL of cut roses by about 1 day, due to an inadequate regulation of the water balance (Gorbe, 2009). Khoshgoftarmanesh et al. (2008) evaluated different concentrations of Fe, Zn, Mn, and Cu in the nutrient solution on VL of three cut rose cultivars. They showed that increasing the Zn concentration prolonged the VL (5–100%, depending on the cultivar) in the tested cultivars, whereas the other micronutrients did not have a consistent effect.

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Although in general, nutrient availability seems to have limited effects on VL, the potential of specific micronutrients (e.g. Zn) to prolong VL should be exploited, and a better understanding of the process underlying this effect is required. 2.1.4.5. Seasonality. A large number of studies reported seasonal differences in VL of cut roses (Fjeld et al., 1994; Urban et al., 1995, 2002; Cross, 2000; Gorbe, 2009). In these studies, roses harvested during the winter season have a shorter VL, compared to roses harvested during the summer. The reduced VL of winter-produced roses may be explained by the following two factors. At first, they show increased susceptibility to B. cinerea (Marois et al., 1988; but see Hammer and Evensen, 1996). More importantly, stomata of roses produced during winter months are less responsive, compared to roses produced during other seasons, resulting in higher rates of water loss (Markhart and Harper, 1995; Slootweg et al., 2001). Roses grown during winter are often exposed to (i) lower light intensity (Fjeld et al., 1994), (ii) shorter photoperiod (Slootweg and van Meeteren, 1991), (iii) lower Tair (Moe, 1975), (iv) higher CO2 concentration (Gislerød et al., 1993), and (v) elevated RH (Mortensen and Gislerød, 1999; Fanourakis et al., 2010), as compared to summer-cultivated roses. As previously discussed, shorter photoperiod and higher CO2 concentration are not likely to induce large effects on VL, and thus cannot explain the reported seasonal effects. The lower light intensity might slightly decrease VL. The VL of roses grown during the winter remained lower than the VL of roses harvested during the summer, even when the light intensity during the winter increased to the level of the summer period by using AL (Gislerød et al., 1993; Fjeld et al., 1994). Moe (1975) proposed that the lower Tair might explain part of the VL decrease of the winter-grown roses. This might be true in many circumstances, though a number of studies conducted in experimental greenhouses, where the Tair was kept close to the optimum during the winter, still reports significantly lower VL during this period (Gislerød et al., 1993; Fjeld et al., 1994). Marissen (2001) as well as Marissen and Benninga (2001) discussed that lower Tair during the winter is also accompanied by higher RH, so the shorter VL during the winter is most likely the effect of high RH. We suggest that lower light intensity and Tair contribute only little to the shorter VL of winter roses, while elevated RH at lower Tair , is the major player reducing VL. 2.1.5. Concluding remarks and outlook Preharvest conditions affect VL through an effect on water balance components. Studies conducted so far have been mostly focused on environmental factors that negatively affect VL. For instance, preharvest conditions (elevated RH, low v, and continuous light) that disturb stomatal functioning result in higher rates of water loss during the postharvest phase, and consequently lead to shorter VL. Greater emphasis should be placed on the deregulation of water balance by low nutrient concentrations (Gorbe, 2009), as well as on the beneficial effect of increasing Tair (when lower than 21 ◦ C) or decreasing root temperature on VL. Only recently, it was shown that vertical gradients in root temperature induced substantial differences in growth and development of barley, as compared to plants exposed to uniform root temperatures (Füllner et al., 2012), while it remains to be seen whether such effects hold in rose and stimulate VL enhancement. Another area that has received no attention is the role of air pollutants, such as ozone, sulfur dioxide and nitrate oxides, which may appear in relatively elevated levels in greenhouses (Likas et al., 2001; Wetzstein and Law, 2006). As by-products of combustion, they often originate from furnace or carbon dioxide generators within the greenhouse (Mortensen, 1987; Blom, 1998), but also from external sources (Fowler et al., 1999). Exposure to these pollutants has been shown to impair

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stomatal responsiveness of several species, such as Dactylis glomerata and Leontodon hispidus, within days (Robinson et al., 1997; Mills et al., 2009; Wilkinson and Davies, 2009), while no studies have been conducted so far in rose. Preharvest treatments that increase the VL of cut roses have been rarely reported. It is our opinion that treatments that stimulate stomatal responsiveness such as partial root drying, regulated deficit irrigation, and increased salinity (>6 m S cm−1 ) have the potential of increasing VL. Although an improvement of VL is often associated with the addition of a carbohydrate (e.g. sucrose, glucose) in vase water for selected species including rose (van Doorn et al., 1991b; Van Doorn, 2001), preharvest conditions that affect the carbohydrate status of a cut rose exert negligible effects on VL. Therefore higher light intensity, carbon dioxide enrichment, higher day than night Tair , as well as lower plant density (Bredmose, 1998; Bredmose and Nielsen, 2004) that increase the amount of carbohydrates prior to harvest, do not necessarily exert a positive effect on VL. Despite the demonstrated importance of environmental conditions during growth on VL (summarized in Table 1), these factors have received little or no attention in postharvest studies. The incorporation of a detailed description of the growth environment in scientific studies may thus greatly help not only in achieving a higher degree of reproducibility, but also to identify hidden factors with major effects on the postharvest performance of cut flowers. Moreover, the effects of postharvest treatments on the VL, such as storage conditions, packaging types, and all other measures taken to optimize the chain and prolong the storage period, are often studied without having in mind that there may be quite some effect of growing conditions. Being more conscious about the effect of growth environment on the postharvest behaviour will strongly facilitate these procedures. 2.2. Genetic factors The genetic make up of a cultivar exerts a pronounced effect on VL. Large differences in VL have been observed among cultivars that were grown and tested under identical conditions (Mortensen and Gislerød, 1999; Marissen, 2001; Särkkä and Rita, 2002; Fanourakis et al., 2012b). For instance, in the study of Marissen (2001) VL ranged between 13 and 24 days depending on the cultivar. A large number of studies examining genotypic variation in VL, by comparing different cultivars grown under different environmental conditions, showed considerable differences (Ichimura et al., 2002; Macnish et al., 2010a; Borda et al., 2011). However, the genetic and/or environmental factors that account for these differences cannot be distinguished. The reasons underlying genotypic variation in VL are not fully understood. A different response of stomata to closing stimuli (e.g. low  , light/dark transition) has been shown to account for cultivar differences in VL (Mayak et al., 1974). The water loss of detached leaves (a measure of stomatal opening in response to dehydration) has been proposed as a quick method to predict reduced VL (Mortensen and Gislerød, 1997; Slootweg et al., 2001; Fanourakis et al., 2012b). The control of water loss can alternatively be tested on stems with leaves (van Doorn and Reid, 1995). To standardize the assessment, Spinarova and Hendriks (2007) introduced a terminology to rank cultivars based on the dehydration resistance (defined as the percentage of weight loss within a certain period of rose cultivars with similar leaf areas), and the dehydration speed (defined as the time for a certain weight loss of rose cultivars with similar leaf areas). These authors reported that cultivars with high dehydration resistance or slow dehydration speed also showed longer VL. Although stomatal functioning certainly has a key role in VL, the correlation between control of water loss and VL between cultivars is not always significant (Mortensen and Gislerød, 1999; Fanourakis et al.,

2012b). This might be taken to indicate that overlooked components such as  at which significant cavitation events take place, and tissue resistance (pedicel; see below) to collapse at low  contribute to the genotypic variation. The  , at which a high rate of cavitations takes place, can range over a factor of two, depending on the cultivar (van Doorn and Suiro, 1996). That means that at the same  , the water uptake in one cultivar might be significantly impaired, while in another there is no effect. Another example of genotypic variation in the inhibition of water uptake was shown by van Doorn and D‘Hont (1994). These authors left stems of four rose cultivars dry (i.e. induced cavitation in the xylem vessels opened by cutting as well as in the medium part of the stem), and subsequently placed them in vase water with varying bacterial populations (i.e. physically blocked xylem vessels in the basal part of the stem to various degrees). It was shown that the decrease in VL, as a result of the above-mentioned treatments, strongly depended on the cultivar. Differences between cultivars have also been observed in rehydration performance meaning their ability to increase fresh weight upon rehydration (discussed as rehydration rate by Slootweg, 1997), but also in the cativation profiles during both de- and rehydration cycles (Spinarova and Hendriks, 2007). It was observed that cultivars with a better rehydration performance or specific cavitation profiles during the above-mentioned cycles had a longer VL. These processes are particularly relevant when the effect of transport is studied, often containing a period, where the flower stalks are not placed in water (the so-called “dry storage”) (Hu et al., 1998; Leonard et al., 2011). Cultivars judged to be superior (or inferior) with regard to VL, when placed directly in the vase, may very well be ranked differently following a “transport treatment”. Cultivar differences occur also with respect to the tissue resistance to collapse at low  . For instance, both the position of the bending zone and the occurrence of pedicel bending strongly depended on the cultivar (Zieslin et al., 1989b). Although different rates of water loss among cultivars contributed to this variation, there were also other factors involved. This was because even under similar water loss rates, genotypic variation in the resistance to bending persisted (Zieslin et al., 1978). The peduncle lignin content affected its mechanical strength, and thus its resistance to bending. This positive effect of higher lignin content to peduncle mechanical strength is not linear (Parups and Voisey, 1976). Although there was evidence that cultivar differences in the peduncle lignin content contributed to genotypic variation in the resistance to bending (Zieslin et al., 1989a), this requires additional investigation. Genotypic variation in the susceptibility of cut roses to B. cinerea incidence has also been reported (Hammer and Evensen, 1994; Hazendonk et al., 1995; Vrind, 2005). Lower susceptibility to B. cinerea in certain cultivars has been related to the reduction of infective hyphal growth in the petal (Pie and Brouwer, 1993). A thicker petal cuticle may slow down the hyphae from penetrating the petal and decrease susceptibility to the pathogen, though cultivar differences in susceptibility were not consistently related to cuticular thickness (Hammer and Evensen, 1994). Cultivar differences in B. cinerea resistance were not also related with the antioxidant level (Friedman et al., 2010). Most of the modern cut rose cultivars are devoid of a distinct fragrance (Zuker et al., 1998), while at the same time there is an increasing interest on its incorporation in the breeding programs (Bent, 2007). Although the specific causes of the lack of fragrance in modern cultivars are not known (Guterman et al., 2002), the notion that fragrant cultivars last less in the vase is prevailing in both the horticultural (Barletta, 1995; Spiller et al., 2010) and breeding (Bent, 2007; Bergougnoux et al., 2007) communities. However in a

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Table 1 Effect of environmental conditions during growth on the vase life (VL) and the susceptibility to Botrytis cinerea of cut roses. Data are a compilation of the literature. Factor

Change

Effect on VL

Susceptibility to B. cinerea

Air humidity B. cinerea spore density B. cinerea latent infections Photoperiod

≥85% ↑ ↑ ↑ (≤20 h) 24 h ↑ = / sources, directional quality ↑ (<21 ◦ C) ↑ (>24 ◦ C) ↑ (12 ≤T <22 ◦ C) ↑ ↑ ↑ (2 < EC < 5 mS cm−1 ) Winter

↓ ↓ ↓ × ↓ ×/↑ × ↑ ↓ ↓ ×/↑ ↑ × ↓

?

Light intensity Light quality Air temperature Root temperature Carbon dioxide Air velocity Nutrition Season

recent study by Borda et al. (2011), no relation was demonstrated between VL and volatile emission. Under natural conditions (i.e. in the virtual absence of exogenous ethylene), cut roses biosynthesize ethylene in the course of senescence (Mayak et al., 1972; Chamani et al., 2005), with large differences (up to ten-fold) in ethylene production between cultivars (Müller et al., 1998; Tan et al., 2006). Although it has been suggested that the produced ethylene amount may negatively correlate with VL in ethylene-free environments (Mayak et al., 1972), recent work indicates that the amount of biosynthesized ethylene among various cultivars was not related to variation in VL (Borda et al., 2011). Consequently, genotypic variation in ethylene production is not related to cultivar differences in VL in ethylene-free environments. Under specific circumstances, cut roses may be exposed to exogenous ethylene. Exposure to exogenous ethylene has been shown to stimulate ethylene biosynthesis (Müller et al., 2001; Xue et al., 2008). Enhanced production of endogenous ethylene has also been found in response to stress (e.g. low Tair ; Mor et al., 1989; Müller et al., 2000). Brief exposure (24 h) to low levels (1 ␮mol mol−1 ) of ethylene decreased (16–90%) the VL of most studied rose cultivars, while in some cultivars the VL was not affected (Macnish et al., 2010a; Borda et al., 2011). However, neither the amount of ethylene produced by the cut roses nor the (temporal) pattern of its biosynthesis was related to tolerance to ethylene exposure (Borda et al., 2011). In conclusion, tolerance to ethylene is critical for a long VL in ethylene-rich environments, though the mechanism(s) underlying tolerance has as yet not been elucidated. Ichimura et al. (2005) assessed the petal content of both soluble carbohydrates (glucose, fructose and sucrose) and starch at harvest in two cultivars with a factor of two difference in VL. It was shown that the cultivar with longer VL had higher soluble carbohydrate concentration in petals, compared to the cultivar with shorter VL. Instead, starch concentration in petals was lower in the cultivar with longer VL. Based on these findings, Ichimura et al. (2005) proposed that the concentration of soluble carbohydrates in petals accounts for the difference in VL between the two cultivars studied. However, this hypothesis is still under debate. Nabigol et al. (2010) supported Ichimura’s hypothesis by showing that in ten cultivars petal soluble carbohydrate content underlay variation in VL, whereas Marissen (2001) found that variation in VL was not related to differences in petal carbohydrate content of the four studied cultivars. Based on the VL termination criteria of Ichimura et al. (2005) and Nabigol et al. (2010), we assume that water stress symptoms were responsible for ending VL in these studies. Van Doorn (2001) proposed that the incidence of water stress symptoms may be delayed by increasing the endogenous sugar level, though experimental evidence to support this statement is currently lacking. Additional work will help to better understand whether cultivar

? ?

↑ √ (Ca2+ ) √

differences in petal carbohydrate status may partly account for genotypic variation in VL. 2.2.1. Interactions between genetic and environmental factors Cultivars respond very differently to environmental conditions affecting VL. Consequently, one way to manipulate the effect of growth environment on VL is to select the appropriate cultivars. Although this approach alone is not always a satisfactory answer to growth environment-induced reductions in VL (e.g. high RH combined with continuous light; see below), it does highlight that breeding shows promise as a successful strategy to cope with short VL. It also suggests that cultivar development will be benefited by incorporating traits related to long VL. Extensive research has been conducted on VL cultivar differences in response to elevated RH and continuous light (Mortensen and Gislerød, 1999, 2005; Fanourakis et al., 2012a,b), whereas less emphasis has been placed on low v (Mortensen and Gislerød, 1997) and low Tair (Marissen, 2001). Cultivars showing tolerance to elevated RH and continuous light were found when these factors were applied one at a time. However, when these factors were applied simultaneously the VL decreased considerably (at least 34%) in all examined cultivars, as compared to roses grown under lower RH (75%) and shorter photoperiod (18 h) (Mortensen and Gislerød, 1999). During our survey of the literature, we found that the effect of growth environment on VL has been mainly approached by studying the stomatal responsiveness, whereas there have been limited efforts to assess a comprehensive set of cultivar traits such as resistance of the tissue to cavitate or collapse (Fig. 2), as well as cut rose susceptibility to B. cinerea infection. Despite a well-documented interaction between genetic and environmental factors on determining stomatal responsiveness, other important traits such as tissue resistance to cavitate or collapse, and susceptibility to B. cinerea (Figs. 2 and 3) also depend largely on the genotype × environment interactions Growth environment

Genotype

Water uptake

Water loss

Resistance to collapse

Water balance

Water stress symptoms

Fig. 2. Factors involved in the incidence of water stress symptoms.

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Genotype

Growth environment

Suscepbility to B. cinerea

B. cinerea spore density

B. cinerea latent infecons

be identified for a given postharvest scenario. This one-dimensional breeding strategy carries the risk that the selected genotypes may perform less well in other circumstances that may come across the postharvest chain. An alternative approach, carrying the pitfall of higher complexity, is to target a combination of these characteristics, which will undoubtedly lead to improved cultivars with longer VL under a wider range of postharvest conditions. 3. Postharvest factors

B. cinerea symptoms Fig. 3. Factors involved in the appearance of Botrytis cinerea symptoms.

underlining the need for trait characterization and environmental monitoring. 2.2.2. Concluding remarks and outlook Considering the importance of a long VL to the horticultural industry, the selection of associated traits is necessary. More concentrated efforts are needed to screen not only for cultivars with a better ability to control water loss, but also for desirable traits related to the remaining factors leading to the incidence of water stress symptoms (Fig. 2). The positive effect of these traits on VL is strongly associated with the postharvest scenario under assessment. For instance, tolerance (or sensitivity) to bacterial occlusion of the xylem vessels (which will decrease water uptake) will be masked by an effective biocide, while tolerance (or sensitivity) to air emboli in the vessels near the cut surface will not be observed when stems are kept in water throughout the (postharvest) chain. Similarly, resistance (or susceptibility) to B. cinerea will be of limited interest, when the pathogen is absent (Fig. 3) or under conditions unfavourable to infection. Therefore, the VL promoting effect of each trait may be maximized under severe circumstances (e.g. pronounced bacterial colonization in the vase solution or high B. cinerea spore density), while it may remain undetected under favourable conditions. To this end, the positive effect of a specific trait has a non-deterministic component related to the variability in the postharvest conditions and/or unaccounted situations. Which trait(s) may be selected? In breeding activities for the release of cultivars with longer VL, the postharvest chain conditions ought to be considered. The most relevant trait(s) for long VL can

Fig. 4. The vase life of cut rose cv. Frisco grown under similar conditions (temperature = 20 ◦ C, relative air humidity of about 75%, and light intensity of 100 or 220 ± 20 ␮mol m−2 s−1 ) in different studies. Data were taken from literature. The vase life terminating criteria were pedicel bending (Fjeld et al., 1994; Särkkä and Rita, 1997; Mortensen and Gislerød, 1999), natural flower senescence (Mortensen and Gislerød, 1999), severe wilting or drying of leaves or petals (Fjeld et al., 1994), as well as wilting and drying of the petals (Särkkä and Rita, 1997). In the study of Marissen (2001), the terminating symptoms were not stated.

Despite the simplicity of measuring VL, the interpretation of the data can (and does) become complex depending on the design and execution of the experiment. For example, the VL of cv. Frisco, grown under similar environmental conditions, varied over a factor of two between studies (Fig. 4), indicating that postharvest factors may exert a considerable effect on the VL. Postharvest factors refer to harvest and beyond, and will be here grouped into (a) harvest factors, (b) cutting and conditioning methods, (c) test room conditions, and (d) VL terminating symptoms. Although not always adopted, recommendations on the test room conditions have previously been provided (Reid and Kofranek, 1980). The choices concerning the other postharvest conditions greatly depend on the laboratory tradition and experience. Variation in these factors may introduce a number of secondary effects outlined in detail below. 3.1. Harvest factors The flower developmental stage at harvest is well established as exerting a pronounced effect on both flower opening (Marissen and Benninga, 2001) and length of the VL (Moe, 1975). However, our survey of the literature has revealed that the flower developmental stage at harvest often varies depending on the studied cultivar (Särkkä and Rita, 2002), or was either not reported (Mortensen and Fjeld, 1998; Sonneveld et al., 1999; Gorbe, 2009), or not clearly defined. For instance, floral developmental stages have been described as flowering stage (Mortensen and Gislerød, 1999, 2011; Khoshgoftarmanesh et al., 2008), commercial cutting stage (Slootweg and van Meeteren, 1991; Borda et al., 2011; Lü et al., 2011; Victoria et al., 2012), as well as optimum stage (Ferreira and de Swardt, 1981). It is recommended to document the flower stage at harvest by utilizing published phenological scales [e.g. van Doorn et al. (1991b), Kuiper et al. (1996), and the Association of Dutch Flower Auctions (VBN, 2005)]. The time of the day at which harvest occurs is also generally not stated in postharvest studies except for a limited number of studies (Garello et al., 1995; Marissen, 2001; Urban et al., 2002; Xie et al., 2008; Ahmad et al., 2011; Borda et al., 2011; Fanourakis et al., 2012b). In greenhouse as well as growth chamber experiments, the time of the day at which the harvest takes place, exerts an effect on VL. For greenhouse experiments, the light conditions at the day of harvest may also exert an effect (Cross, 2000). Temporal variation in  and stem hydraulic conductivity at least partly explains the heterogeneity in VL introduced by the time of harvest.  decreased in the course of the day (Fanourakis et al., 2011), and caused higher uptake of air into the xylem conduits that were opened by cutting (van Ieperen et al., 2001). Moreover, on sunny days the number of cavitations on stems attached on the plant (before cut) was higher at midday, which resulted in reduced water uptake depending on the cultivar (van Doorn and Suiro, 1996). Because of these reasons, we consider it appropriate to plan the harvest at the beginning of the light period at a suitably short time interval, and report it. 3.2. Cutting and conditioning methods Vase life experiments are typically conducted with stems of varying lengths. Cut flowers have been tested either at the stem

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length of harvest (Gislerød et al., 1993; Fjeld et al., 1994; Mortensen and Fjeld, 1998; Mortensen and Gislerød, 1999; Särkkä and Rita, 2002) or upon re-cutting at arrival in the laboratory to a predefined value. The predefined stem length varied between as little as 12 cm to as much as 75 cm (Armitage and Tsujita, 1979; Roberts et al., 1993; Garello et al., 1995; Mortensen and Fjeld, 1998; Badiyan et al., 2004; Gorbe, 2009), and it was sometimes different between tested cultivars (Särkkä and Eriksson, 2003; Fanourakis et al., 2012a). In studies in which the leaf number was not normalized (Fjeld et al., 1994; Mortensen and Fjeld, 1998; Mortensen and Gislerød, 1999; Särkkä and Rita, 2002), a longer stem length may also have resulted in higher number of leaves. In studies in which normalization in the number of leaves took place, longer stem increased the length of the water transport path, and VL may be negatively affected. Särkkä and co-authors reported that stem length either did not affect (Särkkä, 2002) or reduced the VL (Särkkä and Rita, 2002) depending on the cultivar. A significant negative correlation between VL and stem length has been reported (Mortensen and Gislerød, 1999), while shortening stem length has been shown to delay the occurrence of cavitation events (Spinarova and Hendriks, 2005). Leaf number was normalized in most studies to a predefined value (besides Fjeld et al., 1994; Mortensen and Fjeld, 1998; Mortensen and Gislerød, 1999; Särkkä and Rita, 2002), although this normalization did not necessarily result in the same leaf area, which finally determined the water loss on cut flower basis (cut flower water loss = transpiration rate × leaf area). Like stem length, the normalization ranged considerably depending on the study. Vase life experiments were conducted with cut roses having one (Roberts et al., 1993), two (Armitage and Tsujita, 1979; Garello et al., 1995), three (Ichimura et al., 1999), four or five (Fanourakis et al., 2012a,b), up to six (Urban et al., 2002) leaves. Higher number of leaves, resulting in greater leaf area, is expected to increase water loss (in cut flower basis) and may thus decrease the VL. Ferreira and de Swardt (1981) as well as In et al. (2010) showed that roses lasted longer when two instead of four leaves were present. In agreement, Särkkä and Rita (2002) reported that a larger leaf area was negatively correlated with VL, though this effect was cultivar dependent. A strong relationship between cavitation occurrence and transpiration rate has been reported during the VL (Spinarova et al., 2007), while larger leaf area increased the cavitation events (Spinarova and Hendriks, 2005). Short stems (i.e. short water transport path) and/or less leaves (i.e. lower water loss in cut flower basis) would decrease the chance of developing a negative water balance leading to a longer VL. In addition, the effect of a treatment that negatively affects VL through the water balance (e.g. high RH or continuous light) would be underestimated or overlooked (i.e. interaction phenotype × conditioning factors). We recommend, whenever possible, to consider using test cut flowers of about 40 cm long (i.e. close to the length used in the majority of studies) and bearing four leaves. Following harvest and transport to the laboratory, the flowers were rehydrated in cold water (3–5 ◦ C) in a number of studies. Commercial hydration preservatives have occasionally been added in the water (Bredmose, 1998; Slootweg et al., 2001; Macnish et al., 2010a,b; Leonard et al., 2011; Victoria et al., 2012), the effect of which may not be assessed (see below). The rehydration period varied from a few hours (3–4 h; Slootweg and van Meeteren, 1991; Vogelezang et al., 2000) through overnight (Armitage and Tsujita, 1979; Garello et al., 1995; Marissen, 2001; Särkkä, 2002; Borda et al., 2011; Victoria et al., 2012) up to days (1–3 days, Gudin, 1992; Roberts et al., 1993; Särkkä and Rita, 2002; Leonard et al., 2011). The duration of this pre-treatment was usually not added to the length of VL, though exceptions do exist (Faragher et al., 1984). The effect of the above-mentioned cold treatment on the subsequent VL has not been studied, and the introduced variation cannot be assessed. Water balance is benefited by cold treatment by improvement of

9

water uptake (air bubbles in the stems are more easily dissolved at low vase water temperature), while cold pre-treatment may also exert a negative effect on VL (Faragher et al., 1984). The accumulation of microorganisms, especially bacteria, in the xylem conduits close to the cut edge may be an important cause of VL termination (Woltering, 1987; Put and Jansen, 1989), as a result of water stress symptoms due to decreased water uptake (de Witte and van Doorn, 1988; van Doorn and de Witte, 1991a). The bacterial population within the basal part of the stem depends on the cut flower handling during and after harvest. Initial contamination of the cut edge may be caused by the use of non-sanitized harvesting equipment (e.g. shears; van Doorn and de Witte, 1997), and contaminated water for temporary storage or rehydration (van Doorn and de Witte, 1991b). Tap water has also been shown to act as a source of bacteria (van Doorn and de Witte, 1997). Different bacterial strains similarly decreased water uptake, indicating that bacterial population rather than species is the determining factor (de Witte and van Doorn, 1988), though different genera vary in their multiplication rate (Put, 1990; van Doorn et al., 1991a). Enhanced cut rose wounding, as a result of defoliation, increased the bacterial accumulation due to higher amount of growth substrate leaking out of the stem (Woltering, 1987). Moreover, increasing Tair significantly stimulated bacterial growth (van Doorn and de Witte, 1991b). Consequently, variability in the handling of the cut flower will induce differences in the bacterial population in the basal part of the stem, and this will introduce variation in the VL. A commonly applied practice to control bacterial growth is the addition of biocides in the vase water. Several antimicrobial compounds have been found to be effective biocides and their addition substantially prolonged VL (reviewed by Damunupola and Joyce, 2008). To ensure that obtained data are informative, care needs to be taken with the selection of the vase solution biocide, since these often not only influence microbial growth, but also other processes (e.g. Ag+ is a stomatal closing stimulus and an ethylene inhibitor; Damunupola and Joyce, 2008; van Doorn, 2012). Commercial preservatives (the so-called “flower food”), containing biocides, are sometimes used in VL experiments (Bredmose, 1998; Macnish et al., 2010a,b; Leonard et al., 2011). Their use often makes the interpretation of the results difficult, since the composition and concentration of these preservatives, including biocides and other compounds (e.g. sugars and/or surfactants), is usually unknown. Despite attempts to introduce a common vase solution (Reid and Kofranek, 1980; Halevy and Mayak, 1981; van Meeteren et al., 1999), we are far from such a situation. Although seemingly trivial, the composition of the vase water influences the efficacy of holding solutions, but also has been shown to induce variation in VL (Halevy and Mayak, 1981; van Meeteren et al., 1999). An illustrative example is provided by the variable stability of free available chlorine, applied as a biocide, depending on the tap water source (Xie et al., 2008). In the majority of the studies vase water had been either tap water (e.g. Slootweg et al., 2001; Gorbe, 2009) or deionized/distilled water (i.e. water without minerals, pH of about 5.8) (e.g. Ichimura et al., 2002; Mortensen and Gislerød, 2011), whereas the vase solution proposed by van Meeteren et al. (1999; deionized water containing CuSO4 , CaCl2 and NaHCO3 at low concentrations) (e.g. Fanourakis et al., 2012a,b) has not been widely adopted. It is advisable to avoid using tap water as vase water, since its mineral composition, mineral content and pH vary depending on both the location and the season (Halevy and Mayak, 1981; van Meeteren et al., 1999; Xie et al., 2008). For instance, Ca2+ and Na+ contents varied by a factor of 40 and 56, respectively, between tap waters sampled by 21 north American cities (Azoulay et al., 2001). Regarding deionized water, van Meeteren et al. (1999) discussed that it is not only common at the consumer level, where tap water is regularly used as vase water, but also in planta, where xylem

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sap contains minerals. In that study, it was also shown that deionized water decreased the VL of chrysanthemum, as compared to cut flowers placed in either the proposed vase solution or tap water. In a recent review, van Doorn (2012) provided several lines of argument in favour of deionized water as vase water for VL experiments. The jury is still out on this issue. Although it is a common practice to report the volume of the vase solution (ranging between 0.1 and 1 L; Hendriks et al., 2005; Gorbe, 2009), the length of the hydrostatic column that is created is more meaningful factor. This length depends on both the vase solution volume and the vase per se. The longer the hydrostatic column is, the higher the hydrostatic pressure applied to the cut end becomes (in the order of a few kPa), which in turn stimulates water uptake (Mensink and van Doorn, 2001; Valle et al., 2001). Although this effect is generally small, large differences in the hydrostatic column length ought to be avoided not only between studies, but also within experiments. For instance, the decrease of column length, as a result of cut flower transpiration, was much higher in cut roses grown at high RH as compared to moderate RH-grown roses (Fanourakis et al., 2012a), and this may easily go unnoticed. Finally, the flowers are often placed individually in vases, but also in many studies more flowers per vase were used (three to ten flowers per vase: Fjeld et al., 1994; Nell and Leonard, 2005; Mortensen and Fjeld, 1998; Mortensen and Gislerød, 1999, 2011; Ichimura et al., 2002; Pettersen et al., 2006; Macnish et al., 2010a; Leonard et al., 2011; Bayleyegn et al., 2012). Putting multiple stems per vase increases the risk of pronounced bacterial colonization, which in turn hampers water uptake. This effect, though, may be reduced, when an effective biocide is used (bear in mind that the concentration needs to be adjusted depending on the number of stems; see Xie et al., 2008). Placing more than one stem in a vase, indeed, resulted in lower VL, due to reduced water uptake (personal communication: J.M. Dole). Consequently, a higher number of stems per vase increases the relative importance of water balance and results in shorter VL. 3.3. Test room conditions The importance of keeping test room conditions uniform among studies, in order to facilitate comparisons, was addressed by Reid and Kofranek (1980). In their paper, they proposed a set of test room conditions, which were constant test room Tair of 18–22 ◦ C, 60–70% RH (still resulting in a VPD range of 0.62–1.05 kPa), photosynthetically active radiation of approximately 14 ␮mol m−2 s−1 (provided by fluorescent tubes), and 12 h photoperiod. Recommendations for ethylene concentration (<0.05 ␮mol mol−1 ), CO2 concentration (200–400 ␮mol mol−1 ) and v (<0.5 m s−1 ) were also presented. However, these conditions are frequently not met and/or monitored. There is considerable variation in the length of the photoperiod used for testing VL ranging from 8 h (Särkkä, 2002; Särkkä and Rita, 2002) through 16 h (Gudin, 1992; Heo et al., 2004; Robinson et al., 2009) up to continuous light (Armitage and Tsujita, 1979; Mortensen and Gislerød, 1997; Mortensen and Fjeld, 1998; de Capdeville et al., 2003, 2005; Bayleyegn et al., 2012). The same was true for light intensity where both very low (4–7 ␮mol m−2 s−1 : Kiyoshi et al., 1999; Sonneveld et al., 1999; Jowkar et al., 2012) and very high (30–50 ␮mol m−2 s−1 : Garello et al., 1995; Mortensen and Gislerød, 1997; Bredmose, 1998; Bredmose and Nielsen, 2004; 100–200 ␮mol m−2 s−1 : Gudin, 1992; Jin et al., 2006; < 500 ␮mol m−2 s−1 : Robinson et al., 2009) levels, compared to the recommended intensity, were used. Daylight (i.e. varying intensity) was also used (Bolívar et al., 1999; Elgimabi and Ahmed, 2009; Elgimabi, 2011; Hayat et al., 2012). In the majority of the studies, test room Tair was within the recommended limits (besides Zagory and Reid, 1986: 24 ◦ C; Heo et al.,

2004: 25 ◦ C). Huge variability in the test room RH was found, where lower (20–40%: Mortensen and Gislerød, 1997, 2011; Särkkä and Eriksson, 2003) or higher (≥80%: Bolívar et al., 1999; de Capdeville et al., 2003, 2005; Srilaong and Buanong, 2007; Ahmad et al., 2011) RHs, compared to the recommended values, were used. Ethylene concentration, CO2 concentration and v were not recorded in test rooms used for VL evaluation [with the exception of CO2 concentration and v measurements by Robinson et al. (2009) and Ahmad et al. (2011), respectively], and therefore variation in these conditions among VL studies cannot be assessed. Some laboratories use ethylene scrubbers to remove ethylene from incoming air (Borda, 2009), but this is also rarely stated in the materials and methods. As discussed, short-term (24 h) exposure to ethylene (1 ␮mol mol−1 ) negatively affected (16–90%) VL of selected cultivars (Macnish et al., 2010a; Borda et al., 2011), and it would be advisable to record ethylene concentration in VL experiments. Ambient carbon dioxide concentration is currently on the highest edge of the recommended range (390 ␮mol mol−1 ), and is increasing by 1–3 ␮mol mol−1 per year (Edenhofer et al., 2011). Carbon dioxide levels vary depending on the season and location, and are generally higher in a building than in the outside air (Poorter et al., 2012). However, no effect is to be expected by these differences in CO2 concentration, since cut flower photosynthesis is of minor importance for VL (see below). Air velocity is the most poorly-defined component influencing evaporative demand in VL experiments. A decline in v decreases the boundary layer conductance, which in turn reduces the transpiration rate. Model calculations indicated that under conditions of very low boundary layer conductance the rate of transpiration is independent of gs (Collatz et al., 1991). The dependence of the boundary layer conductance on v can be calculated using approaches commonly applied in ecosystems (Campbell and Norman, 1998). Using these calculations, we estimated that the transpiration rate is very low and is dominated by the large boundary layer (small conductance of vapour) at v lower than 0.1 m s−1 . Instead, at higher v (0.1–0.5 m s−1 ) the transpiration rate is elevated and largely determined by gs . Consequently, we suggest that very low v (<0.1 m s−1 ) should be avoided in test rooms used for VL experiments. Growth chambers, sometimes employed for determining VL (Teklic et al., 2003; Heo et al., 2004; de Capdeville et al., 2005; Ichimura et al., 2005; Robinson et al., 2009; Lü et al., 2010), have stronger air circulation systems and consequently higher v, compared to test rooms typical for VL evaluation. In such cases, adjustments in v have to be made for VL experiments. Variation in v between laboratories was assessed by the evaporation rate of beakers filled with distilled water under the conditions recommended for VL assessment. The evaporation rate of distilled water, under the same VPD and light conditions, varied over a factor of two (0.43–0.83 mmol H2 O m−2 s−1 ) between the test rooms of different laboratories, indicating considerable variation in v among them (data not shown). Hence, it is suggested to record v in the test rooms, and document it for all experiments. Note that from air exchange data (volume air h−1 ; Bredmose, 1998; Bredmose and Nielsen, 2004), v cannot be calculated. Under the proposed light intensity for VL assessment, light affects VL mostly via water relations. The recommended light level for VL evaluation is below the compensation point, which varies depending on growth environment mainly between 30 and 70 ␮mol m−2 s−1 photosynthetically active radiation (Zieslin and Mor, 1990). Under 14 ␮mol m−2 s−1 photosynthetically active radiation, leaves can be regarded as carbon sinks, since respiratory processes dominate, and photosynthesis can be neglected. Higher light intensity would fuel photosynthesis, which per se is expected to be of minor relevance to VL (Drüge, 2000). Test room conditions, other than recommended, can introduce a number of unintended effects. Shorter photoperiod (Halevy and

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Table 2 Recommendations for a number of factors for vase life (VL) evaluation, together with their effect on the VL of cut roses. Period

Factor

Recommended

Preharvest Postharvest Harvest factors

Environmental conditions

Documentationa

Bud stage at harvest Time of harvest Stem length Number of leaves Vase water

2b Beginning light period 40 cm 4 Deionized water/deionized water containing CuSO4 , CaCl2 and NaHCO3 10–12 cm 1 14 ␮mol m−2 s−1 Fluorescent 12 h 20 ± 2 ◦ C Ambient 60–70% 0.1 < v < 0.5 m s−1 <0.05 ␮mol mol−1

Cutting and conditioning methods

Test room conditions

Terminating symptoms a b

Hydrostatic column Number of flowers (vase)−1 Light intensity Light quality Photoperiod Air temperature Carbon dioxide Air humidity Air velocity Ethylene Criteria

Literature

Change

Effect on VL

↑ ↑ ↑ ↑

↓ ↓ ↓ ↓

↑ ↑ ↑

↑ ↓ ↓

↑ ↑

↓ ↓

↑ ↑ ↑

↑ ↓ ↓

Reid and Kofranek (1980)/van Meeteren et al. (1999)

Reid and Kofranek (1980) Reid and Kofranek (1980) Reid and Kofranek (1980) Reid and Kofranek (1980) Reid and Kofranek (1980) Reid and Kofranek (1980) VBN (2005)

An excellent outline of how to measure and report environmental conditions is provided by Poorter et al. (2012) According to the scale of VBN (2005).

Mayak, 1981; Spinarova and Hendriks, 2005), lower light intensity, lower test room Tair (Ichimura et al., 1999; Spinarova and Hendriks, 2005), lower v or higher RH (Slootweg et al., 2001) would all result in a lower water loss. A decreased water demand of the flower will probably mask the existence of factors related to the incidence of water stress symptoms (Fig. 2), such as decreased water uptake or increased water loss, which would otherwise decrease the VL. Under these favourable conditions, (a) the cultivar differences, (b) the (positive or negative) effect of growth environment, and (c) the (positive or negative) effect of postharvest treatments on VL will be underestimated or overlooked, because all roses will do well. Opposite effects (i.e. amplification of the differences/studied effect) are to be expected, when test room conditions increase water loss. Consequently, since the results obtained strongly depend on the test room conditions, caution must be exercised that these are correctly set and monitored. 3.4. Vase life terminating symptoms The final stage of VL evaluation is the rejection of the cut flowers based on visual, and thus merely subjective, criteria. Bending of the pedicel (the so-called “bent-neck”) may be the most acceptable criterion for ending VL (Armitage and Tsujita, 1979; Roberts et al., 1993; Garello et al., 1995; Mortensen and Gislerød, 1999, 2011; Särkkä and Rita, 2002). However, the flower angle from the vertical position was rarely reported, and this raises differences (e.g. 30◦ : Heo et al., 2004; 90◦ : Robinson et al., 2009; Fanourakis et al., 2012a). The next most common criterion seems to be petal blueing (Armitage and Tsujita, 1979; Roberts et al., 1993; Garello et al., 1995; Särkkä and Rita, 2002; Bredmose and Nielsen, 2004), which is applied by (subjective) visual judgement. Flower wilting (i.e. loss of petal turgor) was also used (Bredmose and Nielsen, 2004; Mortensen and Gislerød, 2011). Leaf drop was used as a VL termination criterion (Mortensen and Gislerød, 1997), whereas in other studies it did not end VL (Fjeld et al., 1994). The same stands for leaf wilting, where it did (Bredmose and Nielsen, 2004) or did not (Fjeld et al., 1994) terminate VL. Leaf wilting in certain studies needed to be severe (Slootweg et al., 2001), whereas in other studies signs of wilting (Tshwenyane and Bishop, 2009) were adequate to terminate the VL. A complicating factor is B. cinerea incidence, often used as a terminating symptom (Khoshgoftarmanesh et al., 2008; Macnish

et al., 2010a; Ahmad et al., 2011; Borda et al., 2011). Although the decorative value of the cut flower diminishes at a certain stage of B. cinerea infection, a subjective measure, this symptom is related to its susceptibility to the pathogen, spore density, latent infections (Fig. 3) as well as to the handling of the cut flower (e.g. presence of free water or very high RH), and not to the factors related to the appearance of water stress symptoms (e.g. water loss and water uptake; Fig. 2), which dominate the rest of the above-mentioned terminating criteria. Thus, short VL due to disease symptom appearance and the same VL due to flower wilting are due to completely different causal effects. Rejection due to the latter criterion has to do with the factors summarized in Fig. 2, while the former does not. A more objective criterion for the termination of VL such as a pre-defined percentage of cut flower weight loss (Ferreira and de Swardt, 1981; Chang et al., 1997) or when water balance becomes negative (Urban et al., 2002) would be highly desirable. However this seems not easy to use practically, since it varies considerably depending on the studied cultivar as well as the growth conditions (Ichimura et al., 1999, 2002; Fanourakis et al., 2012a). 3.5. Concluding remarks and outlook Choices made with regard to the experimental setup can affect the assessed VL (summarized in Table 2). Substantial variation was found on (i) harvest stage, (ii) cutting and conditioning methods, (iii) test room conditions, and (iv) VL terminating symptoms, while it was not possible to assess variation in a number of factors (e.g. time of harvest and v). Conditioning methods (e.g. smaller leaf area) and test room conditions (e.g. lower evaporative demand) that result in lower water loss also lead to longer VL, and may mask differences between cultivars and treatments that are related to either the water balance or the tissue resistance to collapse at low  . Additionally, the result obtained depends on the VL terminating criteria (e.g. first sign of wilting versus severe wilting). B. cinerea incidence, although deteriorates VL, is not directly linked to the water status of the cut flower, which dominates the rest of the given criteria. 4. Towards a standardized protocol Although the number of papers published on VL has increased rapidly during the last decades, the lack of a unified VL evaluation

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protocol not only raises differences when comparing studies (Fig. 4) but also hampers the establishment of cause-and-effect relationships between morpho-physiological traits and long VL. The simplicity of measuring VL often contrasts with the interpretation of the results, depending on the experimental setup. A standardized protocol, therefore, ought to be considered. The last attempt for a VL evaluation protocol was proposed by Reid and Kofranek (1980). Although their protocol was restricted to optimizing the test room conditions, it is our belief that it should be extended to include information on the harvest and conditioning methods, as well as terminating symptoms. Table 2 provides an extended list of specifications. In the cases where these recommendations cannot be applied, the authors are advised to discuss the consequences of such deviations. Acknowledgement The authors wish to thank Dr. Fabio Fiorani for critically reviewing the manuscript. References Ahmad, I., Joyce, D.C., Faragher, J.D., 2011. Physical stem-end treatment effects on cut rose and acacia vase life and water relations. Postharvest Biol. Technol. 59, 258–264. Araújo, A.E., Maffia, L.A., Mizubuti, E.S.G., Alfenas, A.C., de Capdeville, G., Grossi, J.A.S., 2005. Survival of Botrytis cinerea as mycelium in rose crop debris and as sclerotia in soil. Fitopatol. Bras. 30, 516–521. Armitage, A.M., Tsujita, M.J., 1979. Supplemental lighting and nitrogen nutrition effects on yield and quality of ‘Forever Yours’ roses. Can. J. Plant Sci. 59, 343–350. Arve, L.E., Terfa, M.T., Gislerød, H.R., Olsen, J.E., Torre, S., 2013. High relative air humidity and continuous light reduce stomata functionality by affecting the ABA regulation in rose leaves. Plant Cell Environ. 36, 382–392. Auge, R.M., Schekel, K.A., Wample, R.L., 1986. Osmotic adjustment in leaves of VA mycorrhizal and nonmycorrhizal rose plants in response to drought stress. Plant Physiol. 82, 765–770. Azoulay, A., Garzon, P., Eisenberg, M.J., 2001. Comparison of the mineral content of tap water and bottled waters. J. Gen. Intern. Med. 16, 168–175. Baas, R., Marissen, N., Dik, A.J., 2000. Cut rose quality as affected by calcium supply and translocation. Acta Hortic. 518, 45–54. Badiyan, D., Wills, R.B.H., Bowyer, M.C., 2004. Use of a nitric oxide donor compound to extent the vase life of cut flowers. Hortscience 39, 1371–1372. Bar-Tal, A., Baas, R., Ganmore-Neumann, R., Dik, A., Marissen, N., Silber, A., Davidov, S., Hazan, A., Kirshner, B., Elad, Y., 2001. Rose flower production and quality as affected by Ca concentration in the petal. Agronomie 21, 393–402. Barletta, A., 1995. Scent makes a comeback. Florac 5, 23–25. Bayleyegn, A., Tesfaye, B., Workneh, T.S., 2012. Effects of pulsing solution, packaging material and passive refrigeration storage system on vase life and quality of cut rose flowers. Afr. J. Biotechnol. 11, 3800–3809. Bent, E., 2007. Fragrance is unpredictable, but breeders undeterred. In: Floraculture International, September, pp. 32–33. Bergougnoux, V., Caissard, J.-C., Jullien, F., Magnard, J.-L., Scalliet, G., Cock, J.M., Hugueney, P., Baudino, S., 2007. Both the adaxial and abaxial epidermal layers of the rose petal emit volatile scent compounds. Planta 226, 853–866. Blom, T.J., 1998. Air pollution in greenhouses. Regul. Hortic. 24, 1–5. Blom-Zandstra, M., Pot, C.S., Maas, F.M., Schapendonk, H.C.M., 1995. Effects of different light treatments on the nocturnal transpiration and dynamics of stomatal closure of two rose cultivars. Sci. Hortic. 61, 251–262. Bolívar, P., Fischer, G., Flórez, V.J., Mora, A., 1999. Effect of pre- and postharvest treatments on cut flower longevity of ‘Ariana’ cut roses. Acta Hortic. 482, 83–90. Borda, A.M., 2009. Studies on fragrance, vase life and ethylene regulation of volatile production in rose flowers. Ph.D. Thesis. University of Florida, USA, p. 156. Borda, A.M., Clark, D.G., Huber, D.J., Welt, B.A., Nell, T.A., 2011. Effects of ethylene on volatile emission and fragrance in cut roses: the relationship between fragrance and vase life. Postharvest Biol. Technol. 59, 245–252. Bredmose, N.B., 1998. Growth, flowering and postharvest performance of singlestemmed rose (Rosa hybrida L.) plants in response to light quantum integral and plant population density. J. Am. Soc. Hortic. Sci. 123, 569–576. Bredmose, N., Nielsen, J., 2004. Effect of thermoperiodicity and plant population density on stem and flower elongation, leaf development, and specific fresh weight in single stemmed rose (Rosa hybrida L.) plants. Sci. Hortic. 100, 169–182. Campbell, G.S., Norman, J.M., 1998. An Introduction to Environmental Biophysics. Springer-Verlag, New York, p. 286. Chamani, E., Khalighi, A., Joyce, D.C., Irving, D.E., Zamani, Z.A., Mostofi, Y., Kafi, M., 2005. Ethylene and anti-ethylene treatment effects on cut ‘first red’ rose. J. Appl. Hortic. 7, 3–7. Chang, A.Y., Gladon, R.J., Gleason, M.L., Parker, S.K., Agnew, N.H., Olson, D.G., 1997. Postharvest quality of cut roses following electron-beam irradiation. Hortscience 32, 698–701.

Cochard, H., Nardini, A., Coll, L., 2004. Hydraulic architecture of leaf blades: where is the main resistance? Plant Cell Environ. 27, 1257–1267. Collatz, G.J., Ball, J.T., Grivet, C., Berry, J.A., 1991. Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer. Agric. Forest Meteorol. 54, 107–136. Cross, M., 2000. Quality and postharvest performance of cut roses grown in root media containing coal bottom ash. Ph.D. Thesis. West Virginia University, USA, p. 128. Damunupola, J.W., Joyce, D.C., 2008. When is a vase solution biocide not, or not only, antimicrobial? Jpn. Soc. Hortic. Sci. 77, 211–228. de Capdeville, G., Maffia, L.A., Finger, F.L., Batista, U.G., 2003. Gray mold severity and vase life of rose buds after pulsing with citric acid, salicylic acid, calcium sulfate, sucrose and silver thiosulfate. Fitopatol. Bras. 28, 380–385. de Capdeville, G., Maffia, L.A., Finger, F.L., Batista, U.G., 2005. Pre-harvest calcium sulfate applications affect vase life and severity of gray mold in cut roses. Sci. Hortic. 103, 329–338. de Witte, Y., van Doorn, W.G., 1988. Identification of bacteria in the vase water of roses, and the effect of the isolated strains on water uptake. Sci. Hortic. 35, 285–291. Dean, R., van Kan, J.A.L., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Dickman, M., Kahmann, R., Ellis, J., Foster, G.D., 2012. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13, 414–430. Dik, A.J., Wubben, J.P., 2004. Epidemiology of Botrytis cinerea diseases in greenhouses. In: Elad, Y., Williamson, B., Tudzynski, P., Delen, N. (Eds.), Botrytis: Biology, Pathology and Control. Kluwer Academic Press, Dordrecht, The Netherlands, pp. 319–333. Drüge, U., 2000. Influence of pre-harvest nitrogen supply on post-harvest behaviour of ornamentals: importance of carbohydrate status, photosynthesis and plant hormones. Gartenbauwissenschaft 65, 52–64. Edenhofer, O., Pichs-Madruga, R., Sokona, Y., Seyboth, K., Matschoss, P., Kadner, S., Zwickel, T., Eickemeier, P., Hansen, G., Schlömer, S., von Stechow, C., 2011. IPCC Special Report on Renewable Energy Sources and Climate Change Mitigation. Cambridge University Press, Cambridge, United Kingdom/New York, USA, p. 1075. Elad, Y., 1988. Involvement of ethylene in the disease caused by Botrytis cinerea on rose and carnation flowers and the possibility of control. Ann. Appl. Biol. 113, 589–598. Elgimabi, M.E.N.E., 2011. Vase life extension of rose cut flowers (Rosa hybirida) as influenced by silver nitrate and sucrose pulsing. Am. J. Agric. Biol. Sci. 6, 128–133. Elgimabi, M.N., Ahmed, O.K., 2009. Effects of bactericides and sucrose-pulsing on vase life of rose cut flowers (Rosa hybrida). Bot. Res. Int. 2, 164–168. Fanourakis, D., Carvalho, S.M.P., Almeida, D.P.F., Heuvelink, E., 2011. Avoiding high relative air humidity during critical stages of leaf ontogeny is decisive for stomatal functioning. Physiol. Plant. 142, 274–286. Fanourakis, D., Carvalho, S.M.P., Almeida, D.P.F., van Kooten, O., van Doorn, W.G., Heuvelink, E., 2012a. Postharvest water relations in cut rose cultivars with contrasting sensitivity to high relative air humidity during growth. Postharvest Biol. Technol. 64, 64–73. Fanourakis, D., Carvalho, D.R.A., Gitonga, V.W., van Heusden, A.W., Almeida, D.P.F., Heuvelink, E., Carvalho, S.M.P., 2012b. Breeding cut roses for better keeping quality: first steps. Acta Hortic. 937, 875–882. Fanourakis, D., Matkaris, N., Carvalho, S.M.P., Heuvelink, E., 2010. Effect of relative air humidity on the stomatal functionality in fully developed leaves. Acta Hortic. 870, 83–88. Faragher, J.D., Mayak, S., Tirosh, T., Halevy, A.H., 1984. Cold storage of rose flowers: effects of cold storage and water loss on opening and vase life of ‘Mercedes’ roses. Sci. Hortic. 24, 369–378. Ferreira, D.I., de Swardt, G.H., 1981. The influence of the number of foliage leaves on the vase life of cut rose flowers in two media. Agroplantae 13, 73–76. Fjeld, T., Mortensen, L.M., Gislerød, H.R., Revhaug, V., 1992. Winter production of cut roses: effects on keeping quality. Norw. J. Agric. Sci. 6, 275–278. Fjeld, T., Gislerød, H.R., Revhaug, V., Mortensen, L.M., 1994. Keeping quality of cut roses as affected by high supplementary irradiation. Sci. Hortic. 57, 157–164. Fowler, D., Cape, J.N., Coyle, M., Smith, R.I., Hjellbrekke, A.G., Simpson, D., Derwent, R.G., Johnson, C.E., 1999. Modelling photochemical oxidant formation, transport, deposition and exposure of terrestrial ecosystems. Environ. Pollut. 100, 43–55. Friedman, H., Agami, O., Vinokur, Y., Droby, S., Cohen, L., Refaeli, G., Resnick, N., Umiel, N., 2010. Characterization of yield, sensitivity to Botrytis cinerea and antioxidant content of several rose species suitable for edible flowers. Sci. Hortic. 123, 395–401. Füllner, K., Temperton, V.M., Rascher, U., Jahnke, S., Rist, R., Schurr, U., Kuhn, A.J., 2012. Vertical gradient in soil temperature stimulates development and increases biomass accumulation in barley. Plant Cell Environ. 35, 884–892. Garello, G., Menard, C., Dansereau, B., Le Page-Degivry, M.T., 1995. The influence of light quality on rose flower senescence: involvement of abscisic acid. Plant Growth Regul. 16, 135–139. Gislerød, H.R., Fjeld, T., Mortensen, L.M., 1993. The effect of supplementary light and electrical conductivity on growth and quality of cut roses. Acta Hortic. 342, 51–60. Gorbe, E., 2009. Study of nutrient solution management in soilless rose cultivation, through the analysis of physiological parameters and nutrient absorption. Ph.D. Thesis. Polytechnic University of Valencia, Spain, p. 174. Gudin, S., 1992. Effect of preharvest growing temperatures on the development of cut roses. Postharvest Biol. Technol. 2, 155–161.

D. Fanourakis et al. / Postharvest Biology and Technology 78 (2013) 1–15 Guterman, I., Shalit, M., Menda, N., Piestun, D., Dafny-Yelin, M., Shalev, G., Bar, E., Davydov, O., Ovadis, M., Emanuel, M., Wang, J., Adam, Z., Pichersky, E., Lewinsohn, E., Zamir, D., Vainstein, A., Weiss, D., 2002. Rose scent: genomics approach to discovering novel floral fragrance-related genes. Plant Cell 14, 2325–2338. Halevy, A.H., Mayak, S., 1981. Senescence and postharvest physiology of cut flowers: part 2. Hortic. Rev. 3, 59–143. Hammer, P.E., Evensen, K.B., 1994. Differences between rose cultivars in susceptibility to infection by Botrytis cinerea. Phytopathology 84, 1305–1312. Hammer, P.E., Evensen, K.B., 1996. Effects of the production environment on the susceptibility of rose flowers to postharvest infection by Botrytis cinerea. J. Am. Soc. Hortic. Sci. 12, 314–320. Hayat, S., Amin, N.U., Khan, M.A., Soliman, T.M.A., Nan, M., Hayat, K., Ahmad, I., Kabir, M.R., Zhao, L., 2012. Impact of silver thiosulfate and sucrose solution on the vase life of rose cut flower cv. Cardinal. Adv. Environ. Biol. 6, 1643–1649. Hazendonk, H., ten Hoope, M., van der Wurff, T., 1995. Methods to test rose cultivars on their susceptibility to Botrytis cinerea during the postharvest stage. Acta Hortic. 405, 39–45. Hemming, S., 2011. Use of natural and artificial light in horticulture—interaction of plant and technology. Acta Hortic. 907, 25–36. Hemming, S., Dueck, T.A., Janse, J., van Noort, F.R., 2008. The effect of diffuse light on crops. Acta Hortic. 801, 1293–1300. Hendriks, L., Spinarova, S., Bormann, M., 2005. Acoustic emission profiles of cut roses as a prognosis component for vase life. Acta Hortic. 669, 35–42. Heo, J.W., Chakrabarty, D., Paek, K.Y., 2004. Longevity and quality of cut ‘Master’ carnation and ‘Red Sandra’ rose flowers as affected by red light. Plant Growth Regul. 42, 169–174. Heuvelink, E., Bakker, M.J., Hogendonk, L., Janse, J., Kaarsemaker, R., Maaswinkel, R., 2006. Horticultural lighting in The Netherlands: new developments. Acta Hortic. 711, 25–34. Hogewoning, S.W., Douwstra, P., Trouwborst, G., van Ieperen, W., Harbinson, J., 2010a. An artificial solar spectrum substantially alters plant development compared with usual climate room irradiance spectra. J. Exp. Bot. 61, 1267–1276. Hogewoning, S.W., Trouwborst, G., Maljaars, H., Poorter, H., van Ieperen, W., Harbinson, J., 2010b. Blue light dose-responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue light. J. Exp. Bot. 61, 3107–3117. Honda, Y., Yunoki, T., 1978. Action spectrum for photosprogenesis in Botrytis cinerea Pers. ex Fr. Plant Physiol. 61, 711–713. Hu, Y., Doi, M., Imanishi, D.H., 1998. Competitive water relations between leaves and flower buds during transport of cut roses. Jpn. Soc. Hortic. Sci. 67, 532–536. Hwang, Y.H., Morris, J.T., 1994. Whole-plant gas exchange responses of Spartina alterniflora (Poaceae) to a range of constant and transient salinities. Am. J. Bot. 81, 659–665. Ichimura, K., Kojima, K., Goto, R., 1999. Effect of temperature, 8-hydroxyquinoline sulphate and sucrose on the vase life of cut rose flowers. Postharvest Biol. Technol. 15, 33–40. Ichimura, K., Kawabata, Y., Kishimoto, M., Goto, R., Yamada, K., 2002. Variation with the cultivar in the vase life of cut rose flowers. Bull. Natl. Inst. Flor. Sci. 2, 9–20. Ichimura, K., Kishimoto, M., Norikoshi, R., Kawabata, Y., Yamada, K., 2005. Soluble carbohydrates and variation in vase-life of cut rose cultivars ‘Delilah’ and ‘Sonia’. J. Hortic. Sci. Biotechnol. 80, 280–286. In, B., Kiminobu, S., Katsuhiko, I., Motoaki, D., Gentaro, M., 2006. Effects of airblowing treatment on yield, transpiration and vase life of cut flowers in ‘Asami Red’ rose plant. Jpn. Soc. Hortic. Sci. 13, 64–69. In, B.C., Chang, M.K., Byoun, H.J., Son, K.C., 2010. Effect of vase water temperature and leaf number on water relations and senescence of cut roses. Kor. J. Hortic. Sci. Technol. 28, 609–617. Jarvis, W.R., 1980. Epidemiology. In: Coley-Smith, H.R., Verhoeff, K., Jarvis, W.R. (Eds.), The Biology of Botrytis. Academic Press, London, pp. 219–250. Jin, J., Shan, N., Ma, N., Bai, J., Gao, J., 2006. Regulation of ascorbate peroxidase at the transcript level is involved in tolerance to postharvest water deficit stress in the cut rose (Rosa hybrida L.) cv. Samantha. Postharvest Biol. Technol. 40, 236–243. Jowkar, M.M., Kafi, M., Khalighi, A., Hasanzadeh, N., 2012. Reconsideration in using citric acid as vase solution preservative for cut rose flowers. Curr. Res. J. Biol. Sci. 4, 427–436. Kerssies, A., Bosker-Van Zessen, A.I., Frinking, H.D., 1994. Influence of environmental conditions in a glasshouse on conidia of Botrytis cinerea and on post-harvest infection of rose flowers. Eur. J. Plant Pathol. 101, 201–216. Khoshgoftarmanesh, A.H., Khademi, H., Hosseini, F., Aghajani, R., 2008. Influence of additional micronutrient supply on growth, nutritional status and flower quality of three rose cultivars in a soilless culture. J. Plant Nutr. 31, 1543–1554. Kittas, C., Bartzanas, T., 2007. Greenhouse microclimate and dehumidification effectiveness under different ventilators configuration. Energ. Build. 42, 3774–3784. Kiyoshi, O., Kasahara, Y., Suh, J.N., 1999. Mobility and effects on vase life of silvercontaining compounds in cut rose flowers. Hortscience 34, 112–113. Kuiper, D., van Reenen, H.S., Ribot, S.A., 1996. Characterisation of flower bud opening is roses: a comparison of Madelon and Sonia roses. Postharvest Biol. Technol. 9, 75–86. Leonard, R.T., Alexander, A.M., Nell, T.A., 2011. Postharvest performance of selected Colombian cut flowers after three transport systems to the United States. Horttechnology 21, 435–442.

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Likas, C., Exarchou, V., Gourgoulianis, K., Giaglaras, P., Gemptos, T., Kittas, K., Molyvdas, P.A., 2001. Noxious gases in greenhouses. Ann. Agric. Environ. Med. 8, 99–101. Lü, P., He, S., Li, H., Cao, J., Xu, H.-L., 2010. Effects of nano-silver treatment on vase life of cut rose cv. Movie Star flowers. J. Food Agric. Enriron. 8, 1118–1122. Lü, P., Huang, X., Li, H., 2011. Continuous automatic measurement of water uptake and water loss of cut flower stems. Hortscience 46, 509–512. Macnish, A.J., Leonard, R.T., Borda, A.M., Nell, T.A., 2010a. Genotypic variation in the postharvest performance and ethylene sensitivity of cut rose flowers. Hortscience 45, 790–796. Macnish, A.J., Morris, K.L., de Theije, A., Mensink, M.G.J., Boerrigter, H.A.M., Reid, M.S., Jiang, C.-Z., Woltering, E.J., 2010b. Sodium hypochlorite: a promising agent for reducing Botrytis cinerea infection on rose flowers. Postharvest Biol. Technol. 58, 262–267. Marissen, N., 2001. Effects of pre-harvest light intensity and temperature on carbohydrate levels and vase life of cut roses. Acta Hortic. 543, 191–197. Marissen, N., Benninga, J., 2001. A nursery comparison on the vase life of the rose ‘First Red’: effects of growth circumstances. Acta Hortic. 543, 285–291. Markhart, A.H., Harper, M.S., 1995. Deleterious effects of sucrose in preservative solutions on leaves of cut roses. Hortscience 30, 1429–1432. Markvart, J., Rosenqvist, E., Aaslyng, J.M., Ottosen, C.O., 2010. How is canopy photosynthesis and growth of chrysanthemums affected by diffuse and direct light? Eur. J. Hortic. Sci. 75, 253–258. Marois, J.J., Redmond, J.C., MacDonald, J.D., 1988. Quantification of the impact of environment on the susceptibility of Rosa hybrida flowers to Botrytis cinerea. J. Am. Soc. Hort. Sci. 113, 842–845. Mattson, R.H., Widmer, R.E., 1971. Effects of carbon dioxide during growth on vase life of greenhouse roses (Rosa hybrida). J. Am. Soc. Hortic. Sci. 96, 284–285. Mayak, S., Halevy, A.H., Katz, M., 1972. Correlative changes in phytohormones in relation to senescence processes in rose petals. Physiol. Plant. 27, 1–4. Mayak, S., Halevy, A.H., Sagie, S., Bar-Yoseph, A., Bravdo, B., 1974. The water balance of cut rose flowers. Physiol. Plant. 31, 15–22. Max, J.F.J., Horst, W.J., Mutwiwa, U.N., Tantau, H.J., 2009. Effects of greenhouse cooling method on growth, fruit yield and quality of tomato (Solanum lycopersicum L.) in a tropical climate. Sci. Hortic. 122, 179–186. Max, J.F.J., Schurr, U., Tantau, H.J., Hofmann, T., Ulbrich, A., 2012. Greenhouse cover technology. Hortic. Rev. 40, 259–396. Menard, C., Dansereau, B., Garello, G., Le Page-Degivry, M.T., 1996. Influence of nitrogen supply on ABA levels and flower senescence in Rosa hybrida cv Royalty. Acta Hortic. 424, 151–155. Mensink, M.G.J., van Doorn, W.G., 2001. Small hydrostatic pressures overcome the occlusion by air emboli in cut rose stems. J. Plant Physiol. 158, 1495–1498. Mills, G., Hayes, F., Wilkinson, S., Davies, W.J., 2009. Chronic exposure to increasing background ozone impairs stomatal functioning in grassland species. Glob. Change Biol. 15, 1522–1533. Moe, R., 1975. The effect of growing temperature on keeping quality of cut roses. Acta Hortic. 41, 77–92. Mor, Y., Johnson, F., Faragher, J.D., 1989. Preserving the quality of cold-stored rose flowers with ethylene antagonists. Hortscience 24, 640–641. Mortensen, L.M., 1987. Review: CO2 enrichment in greenhouses. Crop responses. Sci. Hortic. 33, 1–25. Mortensen, L.M., Fjeld, T., 1995. High air humidity reduces the keeping quality of cut roses. Acta Hortic. 405, 148–155. Mortensen, L.M., Fjeld, T., 1998. Effects of air humidity, lighting period and lamp type on growth and vase life of roses. Sci. Hortic. 73, 229–237. Mortensen, L.M., Gislerød, R.H., 1996. The effect of root temperature on growth, flowering, and vase life of greenhouse roses grown at different air temperatures and CO2 concentrations. Gartenbauwissenschaft 61, 211–214. Mortensen, L.M., Gislerød, H.R., 1997. Effects of air humidity and air movement on the growth and keeping quality of roses. Gartenbauwissenschaft 62, 273–277. Mortensen, L.M., Gislerød, H.R., 1999. Influence of air humidity and lighting period on growth, vase life and water relations of 14 rose cultivars. Sci. Hortic. 82, 289–298. Mortensen, L.M., Gislerød, H.R., 2000. Effects of air humidity on growth, keeping quality, water relations and nutrient content of cut roses. Gartenbauwissenschaft 65, 40–44. Mortensen, L.M., Gislerød, H.R., 2005. Effect of air humidity variation on powdery mildew and keeping quality of cut roses. Sci. Hortic. 104, 49–55. Mortensen, L.M., Gislerød, H.R., 2011. Vase life: the influence of variation in air humidity, temperature and super-elevated CO2 concentration in roses grown under continuous light. Eur. J. Hortic. Sci. 76, 63–68. Müller, R., Anderson, A.S., Serek, M., 1998. Differences in display life of miniature potted roses (Rosa hybrida L.). Sci. Hortic. 76, 59–71. Müller, R., Sisler, E.C., Serek, M., 2000. Stress induced ethylene production, ethylene binding, and the response to the ethylene action inhibitor 1-mcp in miniature roses. Sci. Hortic. 83, 51–59. Müller, R., Stummann, B.M., Sisler, E.C., Serek, M., 2001. Cultivar differences in regulation of ethylene production in miniature rose flowers (Rosa hybrida L.). Gartenbauwissenschaft 66, 34–38. Nabigol, A., Naderi, R., Mostofi, Y., 2010. Variation in vase life of cut rose cultivars and soluble carbohydrates content. Acta Hortic. 858, 199–204. Nardini, A., Pedà, G., La Rocca, N., 2012. Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytol. 196, 788–798.

14

D. Fanourakis et al. / Postharvest Biology and Technology 78 (2013) 1–15

Nell, T.A., Leonard, R.T., 2005. The effect of storage temperatures on Colombian grown cut rose varieties. Acta Hortic. 669, 337–342. Ottosen, C.O., Mortensen, L.M., Gislerød, H.R., 2002. Effect of relative air humidity on gas exchange, stomatal conductance and nutrient uptake in miniature potted roses. Gartenbauwissenschaft 67, 143–147. Parups, E.V., Voisey, P.W., 1976. Lignin content and resistance to bending of the pedicel in greenhouse-grown roses. J. Hortic. Sci. 51, 253–259. Pettersen, R.I., Mortensen, L.M., Moe, R., Gislerød, H.R., 2006. Air humidity control essential for rose production under continuous lighting. Acta Hortic. 711, 323–331. Pie, K., Brouwer, Y.J.C.M., 1993. Susceptibility of cut rose flower cultivars to infections by different isolates of Botrytis cinerea. J. Phytopathol. 137, 233–244. Poorter, H., Fiorani, F., Stitt, M., Schurr, U., Finck, A., Gibon, Y., Usadel, B., Munns, R., Atkin, O.K., Tardieu, F., Pons, T.L., 2012. The art of growing plants for experimental purposes: a practical guide for the plant biologist. Funct. Plant Biol. 39, 821–838. Pospisilova, J., 1996. Effect of air humidity on the development of functional stomatal apparatus. Biol. Plant. 38, 197–204. Put, H.M.C., 1990. Micro-organisms from freshly harvested cut flower stems and developing during the vase life of chrysanthemum, gerbera and rose cultivars. Sci. Hortic. 43, 129–144. Put, H.M.C., Jansen, L., 1989. The effects on the vase life of cut Rosa cultivar ‘Sonia’ of bacteria added to the vase water. Sci. Hortic. 39, 167–179. Reid, M.S., Kofranek, A.M., 1980. Recommendations for standardized vase life evaluations. Acta Hortic. 113, 171–173. Rezaei Nejad, A., van Meeteren, U., 2008. Dynamics of adaptation of stomatal behaviour to moderate or high relative air humidity in Tradescantia virginiana. J. Exp. Bot. 59, 289–301. Roberts, G.L., Tsujita, M.J., Dansereau, B., 1993. Supplemental light quality affects bud break, yield, and vase life of cut roses. Hortscience 28, 621–622. Robinson, S., Graham, T., Dixon, M.A., Zheng, Y., 2009. Aqueous ozone can extend vase-life in cut rose. J. Hortic. Sci. Biotechnol. 84, 97–101. Robinson, M.F., Heath, J., Mansfield, T.A., 1997. Disturbances in stomatal behaviour caused by air pollutants. J. Exp. Bot. 49, 461–469. Sack, L., Holbrook, M., 2006. Leaf hydraulics. Annu. Rev. Plant Biol. 57, 361–381. Salinas, J., Glandorf, D.C.M., Picavet, F.D., Verhoeff, K., 1989. Effects of temperature, relative humidity and age of conidia on the incidence of spotting of gerbera flowers caused by Botrytis cinerea. Neth. J. Plant Pathol. 95, 51–64. Särkkä, L.E., 2002. Effects of rest period length and forcing temperature on yield, quality and vase life of cv. Mercedes roses. Acta Agric. Scand. B: Soil Plant Sci. 52, 36–42. Särkkä, L.E., Rita, H., 1997. Significance of plant type and age, shoot characteristics and yield on the vase life of cut roses grown in winter. Acta Agric. Scand. B: Soil Plant Sci. 47, 118–123. Särkkä, L.E., Rita, H., 2002. Effects of rest period length and forcing temperature on yield, quality and vase life of cv. Mercedes roses. Acta Agric. Scand. B: Soil Plant Sci. 52, 6–42. Särkkä, L.E., Eriksson, C., 2003. Effects of bending and harvesting height combinations on cut rose yield in a dense plantation with high intensity lighting. Sci. Hortic. 98, 433–447. Savvides, A., Fanourakis, D., van Ieperen, W., 2012. Coordination of hydraulic and stomatal conductances across light qualities in cucumber leaves. J. Exp. Bot. 63, 1135–1143. Shimazaki, K., Doi, M., Assmann, S.M., Kinoshita, T., 2007. Light regulation of stomatal movement. Annu. Rev. Plant Biol. 58, 219–247. Sirjusingh, C., Sutton, J.C., 1996. Effects of wetness duration and temperature on infection of geranium by Botrytis cinerea. Plant Dis. 80, 160–165. Slootweg, C., 1997. Post-harvest water uptake and stem conductance of cut roses cv. Sonia grown with supplementary lighting. Acta Hortic. 418, 107–110. Slootweg, C., ten Hoope, M.A., de Gelder, A., 2001. Seasonal changes in vase life, transpiration and leaf drying of cut roses. Acta Hortic. 543, 337–342. Slootweg, C., van Meeteren, U., 1991. Transpiration and stomatal conductance of roses cv. Sonia grown with supplementary lighting. Acta Hortic. 298, 119–125. Sonneveld, C., Baas, R., Nijssen, H.M.C., de Hoog, J., 1999. Salt tolerance of flower crops grown in soilless culture. J. Plant Nutr. 22, 1033–1048. Sosa-Alvarez, M., Madden, L.V., Ellis, M.A., 1995. Effects of temperature and wetness duration on sporulation of Botrytis cinerea on strawberry leaf residues. Plant Dis. 79, 609–615. Spiller, M., Berger, R.G., Debener, T., 2010. Genetic dissection of scent metabolic profiles in diploid rose populations. Theor. Appl. Genet. 120, 1461–1471. Spinarova, S., Hendriks, L., 2005. Factors influencing acoustic emission profiles of cut roses. Acta Hortic. 669, 63–69. Spinarova, S., Hendriks, L., 2007. Post-harvest water stress tolerance of various rose cultivars: screening and characterisation. Acta Hortic. 751, 423–430. Spinarova, S., Hendriks, L., Steinbacher, F., Schmid, O., Hauser, B., 2007. Cavitation and transpiration profiles of cut roses under water stress. Eur. J. Hortic. Sci. 72, 113–118. Srilaong, V., Buanong, M., 2007. Effect of chlorophenol and 8-hydroxyquinoline sulphate on vase life of cut rose ‘Rosa hybrida L.’. Acta Hortic. 755, 450–455. Stoll, M., Loveys, B., Dry, P., 2000. Hormonal changes induced by partial rootzone drying of irrigated grapevine. J. Exp. Bot. 51, 1627–1634. Svircev, A.M., McKeen, W.E., Berry, J.W., 1984. Sensitivity of Peronospora hyoscyami f. sp. tabacina to carbon dioxide compared to that of Botrytis cinerea and Aspergillus niger. Phytopathology 74, 445–447.

Tan, H., Liu, X., Ma, N., Xue, J., Lu, W., Bai, J., Gao, J., 2006. Ethylene-influnced flower opening and expression of genes encoding ETRs, and EIN3s in two cut rose cultivars. Postharvest Biol. Technol. 40, 97–105. Teklic, T., Paradzikovic, N., Vukadinovic, V., 2003. The influence of temperature on flower opening, vase life and transpiration of cut roses and carnations. Acta Hortic. 624, 405–411. Terfa, M.T., Poudel, M.S., Roro, A.G., Gislerød, H.R., Olsen, J.E., Torre, S., 2012. Light emitting diodes with a high proportion of blue light affects external and internal quality parameters of pot roses differently than the traditional high pressure sodium lamp. Acta Hortic. 956, 635–642. Torre, S., Fjeld, T., 2001. Water loss and postharvest characteristics of cut roses grown at high or moderate relative humidity. Sci. Hortic. 89, 217–226. Torre, S., Fjeld, T., Gislerød, H.R., Moe, R., 2003. Leaf anatomy and stomatal morphology of greenhouse roses grown at moderate or high air humidity. J. Amer. Soc. Hort. Sci. 128, 598–602. Tshwenyane, S.O., Bishop, C.F.H., 2009. The effect of uniform and fluctuating temperature on the respiration and vase life of ‘Akito’ roses. Acta Hortic 847, 265–268. Twumasi, P., van Ieperen, W., Woltering, E.J., Emons, A.M.C., Schel, J.H.N., Snel, J.F.H., van Meeteren, U., van Marwijk, D., 2005. Effects of water stress during growth on xylem anatomy, xylem functioning and vase life in three Zinnia elegans cultivars. Acta Hortic. 669, 303–312. Urban, I., Brun, R., Urban, L., 1995. Influence of electrical conductivity, relative humidity and seasonal variations on the behavior of cut roses produced in soilless culture. Acta Hortic. 482, 101–110. Urban, L., Six, S., Barthélémy, L., Bearez, P., 2002. Effect of elevated CO2 on leaf water relations, water balance and senescence of cut roses. J. Plant Physiol. 159, 717–723. Valle, R.E., Evans, R.Y., Bobroff, S., Reid, M.S., 2001. Magnetic resonance imaging investigation of the rehydration of cut roses. Acta Hortic. 553, 495–498. van Doorn, W.G., 1997. Water relations of cut flowers. Hortic. Rev. 18, 1–85. Van Doorn, W.G., 2001. Role of soluble carbohydrate in flower senescence. A survey. Acta Hortic. 543, 179–183. van Doorn, W.G., 2012. Water relations of cut flowers. An update. Hortic. Rev. 40, 55–106. van Doorn, W.G., D‘Hont, K., 1994. Interaction between the effects of bacteria and dry storage on the opening and water relations of cut rose flowers. J. Appl. Microbiol. 77, 644–649. van Doorn, W.G., de Stigter, H.C.M., de Witte, Y., Boekestein, A., 1991a. Microorganisms at the cut surface and in xylem vessels of rose stems. J. Appl. Microbiol. 70, 34–39. van Doorn, W.G., de Witte, Y., 1991a. Effect of bacterial suspensions on vascular occlusion in stems of cut rose flowers. J.Appl. Microbiol. 71, 119–123. van Doorn, W.G., de Witte, Y., 1991b. Effect of dry storage on bacterial counts in stems of cut rose flowers. Hortscience 26, 1521–1522. van Doorn, W.G., de Witte, Y., 1997. Sources of the bacteria involved in vascular occlusion of cut rose flowers. J. Am. Soc. Hortic. Sci. 122, 263–266. van Doorn, W.G., Groenewegen, G., van de Pol, P.A., Berkholst, C.E.M., 1991b. Effects of carbohydrate and water status on flower opening of cut Madelon roses. Postharvest Biol. Technol. 1, 47–57. van Doorn, W.G., Reid, M.S., 1995. Vascular occlusion in stems of cut rose flowers exposed to air. Role of xylem anatomy and rates of transpiration. Physiol. Plant. 93, 624–629. van Doorn, W.G., Suiro, V., 1996. Relationship between cavitation and water uptake in rose stems. Physiol. Plant. 96, 305–311. van Ieperen, W., 2012. Plant morphological and developmental responses to light quality in a horticultural context. Acta Hortic. 956, 131–140. van Ieperen, W., Nijsse, J., Keijzer, J., van Meeteren, U., 2001. Induction of air embolism in xylem conduits of pre-defined diameter. J. Exp. Bot. 52, 981–991. van Ieperen, W., Trouwborst, G., 2008. The application of LEDs as assimilation light source in greenhouse horticulture: a simulation study. Acta Hortic. 801, 1407–1414. van Meeteren, U., 2007. Why do we treat flowers the way we do? A system approach of the cut flower postharvest chain. Acta Hortic. 755, 61–73. van Meeteren, U., van Gelder, H., van Ieperen, W., 1999. Reconsideration of the use of deionized water as vase water in postharvest experiments on cut flowers. Postharvest Biol. Technol. 17, 175–187. van Meeteren, U., van Gelder, H., van Ieperen, W., 2005. Effect of growth conditions on post harvest rehydration ability of cut chrysanthemum flowers. Acta Hortic. 669, 287–296. VBN, 2005. Evaluation cards for cut flowers. VBN, Leiden, The Netherlands. Velez-Ramirez, A.I., van Ieperen, W., Vreugdenhil, D., Millenaar, F.F., 2011. Plants under continuous light. Trends Plant Sci. 16, 310–318. Verhoeff, K., 1980. Infection and host–pathogen interactions. In: Coley-Smith, J.R., Verhoeff, K., Jarvis, W.R. (Eds.), The Biology of Botrytis. Academic Press, London, pp. 158–180. Victoria, N.G., Kempkes, F.L.K., van Weel, P.A., Stanghellini, C., Dueck, T.A., Bruins, M.A., 2012. Effect of a diffuse glass greenhouse cover on rose production and quality. Acta Hortic. 952, 241–248. Vogelezang, J.V.M., de Hoog Jr., J., Marissen, N., 2000. Effects of diurnal temperature strategies on carbohydrate content and flower quality of greenhouse roses. Acta Hortic. 515, 111–118. Volpin, H., Elad, Y., 1991. Influence of calcium nutrition on susceptibility of rose flowers to Botrytis blight. Phytopathology 81, 1390–1394.

D. Fanourakis et al. / Postharvest Biology and Technology 78 (2013) 1–15 Vrind, T.A., 2005. The Botrytis problem in figures. Acta Hortic 669, 99–102. Yunis, H., Elad, Y., 1989. Survival of Botrytis cinerea in plant debris during summer in Israel. Phytoparasitica 17, 13–21. Zagory, D., Reid, M.S., 1986. Role of vase solution microorganisms in the life of cut flowers. J. Am. Soc. Hortic. Sci. 111, 154–158. Zieslin, N., Kohl, H.C., Kofranek, A.M., Halevy, A.H., 1978. Changes in the water status of cut roses and its relation to bent-neck phenomenon. J. Am. Soc. Hortic. Sci. 103, 176–179. Zieslin, N., Starkman, F., Zamski, E., 1989a. Bending of rose peduncles and the activity of phenylalamine ammonia lyase in the peduncle tissue. Plant Physiol. Biochem. 27, 431–436. Zieslin, N., Starkman, F., Zamski, E., 1989b. Growth of rose peduncles and effects of applied plant growth regulators. Plant Growth Regul. 8, 65–76. Zieslin, N., Mor, Y., 1990. Light on roses. A review. Sci. Hortic. 43, 1–14. Zuker, A., Tzfira, T., Vainstein, A., 1998. Cut-flower improvement using genetic engineering. Biotechnol. Adv. 16, 33–79. Wakrim, R., Wahbi, S., Tahi, H., Aganchich, B., Serraj, R., 2005. Comparative effects of partial root drying (PRD) and regulated deficit irrigation (RDI) on water relations and water use efficiency in common bean (Phaseolus vulgaris L.). Agric. Ecosyst. Environ. 106, 275–287.

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West, J.S., Pearson, S., Hadley, P., Wheldon, A.E., Davis, F.J., Gilbert, A., Henbest, R.G.C., 2000. Spectral filters for the control of Botrytis cinerea. Ann. Appl. Biol. 136, 115–120. Wetzstein, H.l.Y., Law, S.E., 2006. Measurements of ambient ozone concentrations show elevated levels within commercial greenhouses. Hortscience 41, 976. Wilkinson, S., Davies, W.J., 2009. Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylene-dependent mechanism. Plant Cell Environ. 32, 949–959. Williamson, B., Duncan, G.H., Harrison, J.G., Harding, L.A., Elad, Y., Zimand, G., 1995. Effect of humidity on infection of rose petals by dry-inoculated conidia of Botrytis cinerea. Mycol. Res. 99, 1303–1310. Woltering, E.J., 1987. The effects of leakage of substances from mechanically wounded rose stems on bacterial growth and flower quality. Sci. Hortic. 33, 129–136. Xie, L., Joyce, D.C., Irving, D.E., Eyre, J.X., 2008. Chlorine demand in cut flower vase solutions. Postharvest Biol. Technol. 47, 267–270. Xue, J.Q., Li, Y.H., Tan, H., Yang, F., Ma, N., Gao, J.P., 2008. Expression of ethylene biosynthetic and receptor genes in rose floral tissues during ethylene-enhanced flower opening. J. Exp. Bot. 59, 2161–2169.