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Some factors affecting longevity of cut lilacs
Postharvest Biology and Technology 111 (2016) 247–255
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Postharvest Biology and Technology journal homepage: www.elsevier.com/locate/postharvbio
Some factors affecting longevity of cut lilacs Agata Je˛drzejuk* , Julita Rabiza-Swider, Ewa Skutnik, Aleksandra Łukaszewska Department of Ornamental Plants, Faculty of Horticulture, Biotechnology and Landscape Architecture, Warsaw University of Life Sciences, Nowoursynowska 166, 02-787 Warsaw, Poland
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 May 2015 Received in revised form 3 September 2015 Accepted 12 September 2015 Available online xxx
Short vase life of cut lilac stems limits its commercial potential. Rapid wilting of cut lilac inflorescences is probably caused by blockage of water transport in stems. The purpose of this study was to recognize the nature of the occlusions blocking xylem vessels in cut stems of common lilac and to identify a relationship, if any, between the type of a holding solution, xylem blockages and vase life of lilacs flowering under different environmental conditions. The stems of the white flowering cultivar “Mme Florent Stepman” were harvested in Nov/Dec from shrubs forced from the beginning of November by a standard procedure involving treatment with 37 C, in January from shrubs forced from the beginning of November under 15 C, and in May from control shrubs, i.e., flowering naturally in the field. Cut stems were placed in distilled water, 8-HQC, a standard preservative composed of 8-HQC + 2% sucrose, nanosilver and nanosilver + 2% sucrose. Tyloses were observed in stem xylem vessels while practically no microorganisms were detectable. The incidence of blockage formation in the stems depended on the flowering date and the biocide used. The longest vase life was observed in January with 8-HQC or 8-HQC + S, but in all flowering periods the least xylem blockages were formed when NS was used as the biocide. Therefore, formation of tyloses does not appear to be directly related to the postharvest life of lilac and its vase life can be extended by standard florists’ preservatives irrespective of their effect of the xylem physical obstructions. ã 2015 Elsevier B.V. All rights reserved.
Keywords: Tyloses Vessel blockage Senescence Syringa vulgaris
1. Introduction Unobstructed water uptake is indispensable for proper flower bud opening and proper water balance in cut stems; hence it is crucial for the postharvest longevity of cut flowers (Reid and Evans, 1986). The main agent limiting water uptake by cut flowers may be the obstruction of xylem vessels which develops during the vase life. This may be a consequence of microbial growth, deposition of materials in the lumen of xylem vessels, presence of air emboli in the vascular system and formation of tyloses (van Doorn, 1997; Twumasi et al., 2005). It has been demonstrated (Twumasi et al., 2005) that hydraulic properties and dimensions of stem xylem vessels directly affect the vase life and quality of cut flowers. Tyloses are outgrowths of parenchyma cells through the vessel parenchyma pit pairs and into the lumen of the treachery elements (Esau, 1977; Zimmermann, 1983; Sun et al., 2006). Tyloses form in a wide range of species (Saitoh et al., 1993) and genetic variation in
Abbreviations: 8-HQC, 8-hydroxyquinoline citrate; NS, nanosilver; S, sucrose; WU, water uptake; RFW, relative fresh weight. * Corresponding author. E-mail address: [email protected] (A. Je˛drzejuk). http://dx.doi.org/10.1016/j.postharvbio.2015.09.018 0925-5214/ ã 2015 Elsevier B.V. All rights reserved.
the propensity to form tyloses has been reported in some genera (e.g., Quercus and Robinia) (Biggs, 1987; Saitoh et al., 1993). Formation of tyloses is a well known response to infection by pathogens (Canny, 1997) and tyloses appear at the site of stem wounding (Clerivet et al., 2001). During the postharvest life, probably as a consequence of mechanic injury at harvest, xylem vessels at the basal stem parts may become blocked by microorganisms and tyloses, but in several woody cut flowers such as roses, physiological blockages by gels and gums may also form at the interface between water and air (van Doorn, 1997). In the context of handling cut stems of ornamental plants, biocides must be used in pulsing and vase solutions in order to exploit the full postharvest longevity inherent in cut flowers (Damunupola and Joyce, 2008). The most popular and effective biocides are esters of hydroxyquinoline (HQ) and silver ions. The effectiveness of HQ as an apparent biocide in cut flower handling solutions has been known for decades (van Doorn, 1997; Damunupola and Joyce, 2008). Sulphate (HQS) and citrate (HQC) forms of HQ are most commonly used in flower handling. They may also increase flower longevity by acidifying the vase solution and by acting as antitranspirants thus limiting water losses (Halevy and Mayak, 1981; Damunupola and Joyce, 2008). Pure colloidal silver
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nano particles (nano-Ag or NS) are potent and broad spectrum antimicrobial agents (Lok et al., 2006). The mechanism of the antibacterial action of NS is not fully understood (Pal et al., 2007), however, interaction between the particles and bacterial membranes may cause structural damage leading to bacterial cell death (Sondi and Salopek-Sondi, 2004; Damunupola and Joyce, 2008). The quality of cut flowers is also affected by a range of environmental factors. These variables include plant maturity, the stage of bud opening or the season of planting and harvesting (Manning, 1995; Pompodakis et al., 2005; Rafdi et al., 2014). According to Jones (2002), poor postharvest handling may cause up to 30% loss of floriculture products. Thus, it is important to understand the diverse causes of quality loss with a view to extend the vase life of cut flowers and foliage (Rafdi et al., 2014). Common lilac (Syringa vulgaris L.) is a popular ornamental shrub. Under natural conditions of the temperate zone it blooms in May. Its flowering period is relatively short and is usually completed by the end of the month. Properly applied forcing procedures induce lilac flowering any time between November and May, filling a niche in the cut flower market when the supply of naturally flowering plants is low. Overcoming periodicity and prolonging plant flowering beyond the natural period has always been a point of interest to scientists and growers (Dale et al., 1999). Forcing is commonly used to induce flowering independently of the natural blooming date in many bulbous plants but also in ornamental shrubs and trees; it requires overcoming endodormancy. The temperatures required to begin the forcing cycle of lilac range from 37 C in November to 16 C in March. The studies on the relationship between temperature and the length of the forcing cycle have shown that forcing lilac at 15 C in November is also effective, but it requires 49 days as compared to 23 days for the standard 37 C used by most growers. However, panicles produced at 15 C are completely filled with flowers, hence more decorative, while panicles produced by the standard high temperature treatment tend to be floppy and their flowers are not completely open (Je˛drzejuk and Łukaszewska, 2008c). Flowering stems of lilac, even when placed in water immediately after harvest, quickly develop symptoms of wilting (van Doorn et al., 1991). This short vase life is probably caused by blockage of water transport in the stems (Sytsema-Kalkman, 1991; Je˛drzejuk and Zakrzewski, 2009). The purpose of this study was to identify the nature of occlusions blocking xylem vessels in cut stems of common lilac depending on flowering conditions and treatments with two common biocide solutions, and to identify a relationship, if any, between holding solution, formation of such blockages and the vase life of lilac flowering under different environmental conditions. 2. Material and methods 2.1. Plant material and conditions The experimental materials were flowering stems of common lilac (Syringa vulgaris L.) of the white cv. “Mme Florent Stepman”. Plants for the experiments were kindly provided by Mr. Michał Łyczko in Grodzisk Mazowiecki (Central Poland). Stems were cut from 6–8-year old shrubs, maintained as semi standard, each with several strong flowering stems and well developed root balls 35–40 cm in diameter. Shrubs for the experiments were dug up at the beginning of October and left in the field with their root balls exposed to low ambient temperatures. The forcing procedures started at the beginning of November: one part of shrubs were forced according to the standard procedure involving the 37 C treatment which assured flowering in late November and early December (Je˛drzejuk and Szlachetka, 2003), and the other part was forced under mild temperature of 15 C during the entire
forcing period and flowered in January (alternative forcing). Shrubs blooming naturally in the field in May were used as a control. Flowering stems were harvested when one third of florets in panicles were open, immediately transferred to the laboratory and trimmed to 50 cm. Stems were placed in distilled water (control treatment), 200 mg L1 8-HQC, standard preservative containing 200 mg L1 8-HQC with 2% sucrose, 1 mg L1 NS, and 1 mg L1 NS with 2% sucrose. The solutions were prepared in distilled water. They were not exchanged during the experiments but their depletions were supplemented to maintain steady levels, and the mouths of vases were covered with parafilm to minimize evaporation from the solution surface. There were ten stems in each treatment, individually tagged and treated as separate replications. The experiments were conducted at a constant temperature of 18–20 C and 12 h photoperiod, under luminescence light with the quantum irradiance of 25 mmol m2 s1. The relative air humidity was maintained at 60%. Lilac vase life was regarded as terminated if 30% of the florets wilted, dried up and/or turned brown. 2.2. Bacterial counts To determine bacterial populations in holding solutions, 0.5 mL aliquots were taken in triplicate from each holding solution on the last day of the lilac’s vase life. Samples were serially diluted with 0.9% sterile normal saline (NaCl). The 0.1 mL aliquots were spread over agar plates and incubated at 30 C for 24 h.Colony counts were expressed as colony forming units per ml (CFU mL1). 2.3. Relative fresh weight The fresh weights of cut stems were measured daily. The relative fresh weight (RFW) of stems was calculated using the formula: RFW (%) = (FWt/FWt = 0) 100; where FWt is the fresh weight of stem (g) at t = days 0, 1, 2, etc., and FWt = 0 is the fresh weight of stem (g) at t = day 0 (He et al., 2006). 2.4. Water uptake The average daily water uptake (WU) was calculated using the following formula: WU (g stem1 d1) = (St 1 St), where St is the weight vase of solution (g) at t = days 1, 2, 3, etc., and St1 is the weight of holding solution (g) on the previous day (day 0) (He et al., 2006). 2.5. Microscopic observations The material for microscopy was sampled immediately after harvest (the basal part) and later from all treatments when 1/3 of panicles on stems held in water were wilted and/or dry. The specimen were boiled for 4 h in distilled water, fixed in 5% glutaraldehyde and 4% paraformaldehyde solution in 0.1 M sodium cacodylate buffer (pH 7.2–7.3) at 0.8 atm at room temperature and rinsed with the same buffer. Next, samples were dehydrated by graded ethanol series (30, 50, 70, 80, 90, 100%), and dried at RT for 24 h. Observations were made under a scanning electron microscope (SEM) FEI QUANTA 200 ESEM with digital camera EDS EDAX, at the Analytical Centre, Warsaw University of Life Sciences. The samples were not dried to the critical point. Basal segments 1 cm long from each of ten stems from each treatment were examined. 2.6. Statistical analyses Data were analyzed by the General Linear Model program of the IBM SPSS Statistics Data Editor (Softonic, Poland), and means were compared by the Tukey–Kramer multiple range test.
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Table 1 Longevity of cut lilacs ‘Mme Florent Stepman’ as affected by a flowering date and a holding solution. Longevity (days)
Distilled water 200 mg L1 8-HQC 200 mg L1 8-HQC + 2% sucrose 1 mg L1 NS 1 mg L1 NS + 2% sucrose
November standard forcing (blooming in November/ December)
November alternative forcing (blooming in January)
Natural flowering in May
2.4 a 6.2 e 6.8 f
9.2 j 11.3 m 12.0 n
5.0 b 7.9 g 8.0 h
5.2 c 5.8 d
10.4 k 10.7 l
8.0 h 8.5 i
Means followed by the same letter do not differ significantly at a = 0.05. P < 0.001.
3. Results 3.1. Vase life, relative fresh weight and water uptake of lilacs harvested on different dates and held in different solutions The inflorescences on stems kept in distilled water and blooming in Nov/Dec wilted after 2.4 days, those blooming in January—after 9.2 days while those taken from shrubs flowering
outdoors in May after 5.0 days (Table 1). The longevity of stems from the same flowering dates but kept in 8-HQC was 6.2 days, 11.3 and almost 8 days, respectively. For the NS and NS with + S solutions, the corresponding longevities were 5.2 and 5.8 days, 10.4 and 10.7 days, and 8 and 8.5 days. In all cases, stems from shrubs flowering in January had the highest longevity. The relative fresh weight of stems, after a brief initial increase, showed a steady reduction over the duration of the experiment,
Fig. 1. Relative fresh weight of cut common lilac stems flowering under different conditions and held in various solutions. (a) November standard forcing (blooming in November/December). (b) November alternative forcing (blooming in January). (c) Natural flowering in May. Means of 10 replicates Standard Deviation.
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but at different rates depending on the flowering date and keeping solutions. For stems kept in distilled water, the relative fresh weight for the November/December flowering dropped to ca 44% of the initial weight (Fig. 1a). In this treatment, the water uptake increased only on the second day of observations, and then it kept decreasing to reach 0.1 g g1 of the initial FW between the 9th and the last day of observations (Fig. 2a). In stems collected from the January flowering kept in water the relative fresh weight dropped to 52% on the last day of observations (Fig. 1b). Here, the water uptake increased between the 2nd and the 6th day, and then dropped to 0.1 g g1 of the initial FW on the last day of observations (Fig. 2b). In stems collected from shrubs blooming in May the
relative fresh weight in stems kept in distilled water was 47% on the last day of observations (Fig. 1c). In this treatment, the water uptake was similar to that observed in stems blooming in January (Fig. 2c). For all flowering dates, the curves of RFW and WU for stems kept in 8-HQC and 8-HQC + S were similar (Figs. 1 a–c and 2 a–c). The drop in the fresh weight was slower and less dramatic than for stems kept in water, and it reached ca 80% on the last day of observations. The daily water uptake kept increasing until days 4–6, reaching the maximum of 0.32–0.62 g g1 while on the last day it dropped to 0.18–0.27 g g1 of the initial FW. In stems held in the two silver solutions (with or without sucrose) the curves for
Fig. 2. Water uptake of cut common lilac stems flowering under different conditions and held in various solutions. (a) November standard forcing (blooming in November/ December). (b) November alternative forcing (blooming in January). (c) Natural flowering in May. Means of 10 replicates Standard Deviation.
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Table 2 Number of bacteria in holding solution. Number of bacteria
Distilled water 200 mg L1 8-HQC 200 mg L1 8-HQC + 2% sucrose 1 mg L1 NS 1 mg L1 NS + 2% sucrose
November standard forcing (blooming in November/ December) (CFU mL1)
November alternative forcing (blooming in January) (CFU mL1)
Natural flowering in May (CFU mL1)
4.8 105 e 3.8 104 c 3.8 104 c
4.8 105 e 3.8 104 c 3.8 104 c
5.1 105 f 3.8 104 c 3.9 104 d
3.5 104 a 3.5 104 a
3.5 104 a 3.5 104 a
3.6 104 b 3.6 104 b
Means followed by the same letter do not differ significantly at p = 0.05.
the relative fresh weight and water uptake were similar to those for the 8-HQC solutions (Figs. 1 a–c and 2 a–c). On the last observation day the stems from all flowering dates had their fresh weight at the 78–85% of the initial level. In stems blooming in Nov/Dec, the water uptake increased to 0.32 g g1 of the initial FW on the 4th day of observations, and dropped to 0.18 g g1 of the initial FW on the last day of observations (Fig. 2a). In stems blooming in January, the initial water uptake was 0.35 g g1 of the initial FW, and on the 6th day of observations it reached 0.62 g g1 of the initial FW (Fig. 2b). For the May bloom, the initial and the highest values of water uptake were equal to those observed in flowers blooming in January (Fig. 2c). 3.2. Bacteria counts in holding solutions and in stem ends Generally, the number of bacteria in holding solutions was low. The highest number was found in distilled water in May flowering, reaching 5.1 105 CFU mL1 on the last day of observations. The most effective media arresting bacteria populations were NS and NS + S which reduced bacteria numbers to 3.5 104 CFU mL1 in November/December and January, and to 3.6 104 CFU mL1 in May (Table 2). Some bacteria in tracheary elements were found only in lilacs kept in distilled water and only on the last sampling dates (Fig. 3). No traces of microorganisms were detected on any sampling date in stems placed in the holding solutions tested in the experiment. 3.3. Blockage in cut stems The stems collected from forced shrubs and analyzed immediately after harvest had nearly all vessels free of any detectable blockage (Fig. 4a and b). Surprisingly, 9% of the freshly harvested
stems from shrubs flowering outdoors in May (the unforced controls) were filled with tyloses (Fig. 4c). However, those tyloses did not completely obstruct the vessel lumina, making the water flow possible. On the last day of the vase life, 60% of stems held in distilled water and blooming in Nov/Dec had identifiable tyloses in vessels of the basal stem segments. Those tyloses obstructed the entire lumen of the vessel (Fig. 4d and Table 3), especially in the outer part of the stem. In January, the basal xylem vessels were obstructed in 35% (Fig. 4e and Table 3) and the incidence of blockage in the outer and inner sections tested were similar. Tyloses filled the entire vessel lumen. In May, only 12% of vessels in the basal parts of stems held in distilled water had identifiable tyloses (Fig. 4f and Table 3). In this treatment, other occlusions composed of unidentified microbiological material were also observed (Fig. 3a,b). In the Nov/Dec flowering, nearly 80% vessels in stems held in 200 g L1 8-HQC were blocked by tyloses on the day when the control lilacs wilted (Fig. 4g and Table 3). Blocked vessels were present both in the outer and in inner parts of the stems, but most tyloses blocked only about one half of the vessel lumen, leaving openings for water flow. In January, ca 50% of vessels were blocked by tyloses and these were present mostly in the outer parts of the stems (Fig. 4h and Table 3). Similarly to the stems collected from the Nov/Dec flowering, the tyloses blocked only parts of the vessel lumen. In May, the basal stem segments had 86% of their vessels blocked by tyloses which still did not fill the entire xylem lumen (Fig. 4i and Table 3). Blocked vessels were present equally in the outer as in the inner parts of the stems.In stems from the standard November forcing held in 200 g L1 8-HQC + 2% sucrose, ca 40% vessels were blocked by tyloses (Fig. 4j and Table 3), both in the outer and in inner parts of the stem, but most tyloses blocked only about one half of the vessel lumen, leaving openings for water
Fig. 3. Evidence of bacteria presence in stem ends of lilac held in distilled water on the last day of observations. (a) in vessels.
– extracellular polysaccharides, (b) ! – bacteria located
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Fig. 4. Xylem structure in stems of common lilac ‘Mme Florent Stepman’. (a–c) Freshly harvested stems in: November standard forcing and flowering in November/December (a), November alternative forcing and flowering in January (b), natural flowering in May (c); v – vessel, - – tylose. (d–f) Stems kept in distilled water. November standard forcing and flowering in November/December (d), November alternative forcing and flowering in January (e), natural flowering in May (f); – tylose. (g–i) Stems kept in 200 mg L1 8HQC. November standard forcing and flowering in November/December (g), November alternative forcing and flowering in January (h), natural flowering in May
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Table 3 Frequency of vessel blockage (%) and the blockage severity in the basal stem parts in cut lilac ‘Mme Florent Stepman’ as affected by a flowering date and a holding solution (evaluated on a day when the control flowers wilted). Frequency of vessel blockage (%) and the blockage severity
Distilled water 200 mg L1 8-HQC 200 mg L1 8-HQC + 2% sucrose 1 mg L1 NS 1 mg L1 NS + 2% sucrose
November standard forcing (blooming in November/ December)
November alternative forcing (blooming in January)
Natural flowering in May
60.0 k * 80.8 l 40.0 i
35.0 h * 49.7 j 28.0 g
12.0 c * 86.2 m 40.0 i
21.2 f 5.0 a
18.6 d 5.0 a
17.8 e 11.0 b
Means followed by the same letter do not differ significantly at p = 0.05. * – Vessel completely blocked.
flow. In lilacs flowering in January after alternative forcing, 28% of vessels in the stems were filled with tyloses occurring equally in the outer and inner part of the stem (Fig. 4k and Table 3). In May, the basal stem segments had 40% of their vessels blocked by tyloses which, however, did not fill the whole xylem lumen (Fig. 4l and Table 3). Blocked vessels were present equally in the outer as in the inner parts of the stem. In lilacs flowering in Nov/Dec held in 1 g L1 NS21% of vessels in stems held in the NS solution were blocked by tyloses (Fig. 4m and Table 3). Blocked vessels were present both in the outer and in inner parts of the stem, but most tyloses blocked only about half of the vessel lumen, leaving openings for water flow. In January, almost 19% of vessels were blocked by tyloses, equally distributed in the outer and inner part of the stem (Fig. 4n and Table 3). In May, ca 18% of vessels were blocked by tyloses which did not fill the whole xylem lumen (Fig. 4o and Table 3). Blocked vessels were present equally in the outer as in the inner parts of the stem. On the day the control stems wilted, the stems held in 1 g L1 NS with 2% sucrose had only few vessels blocked and this was true for all flowering dates. Tyloses blocked ca 5% of vessels in stems after forcing (Fig. 3p and r and Table 2) and 11% in stems harvested from naturally flowering shrubs in May (Fig. 4s and Table 3). 4. Discussion 4.1. Longevity of cut lilacs depending on the flowering date A long vase life is a prerequisite for commercialization of cut flowers (Rafdi et al., 2014; Lim-Camacho, 2006). The quality of cut flowers is affected by a range of environmental factors and management practices throughout the marketing chain (Manning, 1995; Pompodakis et al., 2005; Rafdi et al., 2014). One of the significant factors determining the postharvest life of cut ornamentals is the season of flowering, and thus flowering conditions and the physiological state of plants at harvest. In Acacia holoserica, stems blooming from winter to spring had an average vase life of 4.8 1.1 days while for summer and autumn it was significantly prolonged, to 7.3 1.4 (Rafdi et al., 2014). Postharvest floral longevity of miniature cut roses was 14.3 days during their growth under long day and high temperature, while under short day and low temperature, it was reduced to 9.9 days (Kyalo et al., 1996). In the current experiment the shortest vase life was observed in lilacs forced in November by the standard method and flowering in Nov/Dec; the longest vase life was in flowers forced by the alternative method, and blooming in January, while inflorescences from shrubs growing outdoors under natural conditions had an
– Vessel partly blocked.
intermediate longevity. Reduction of the vase life in lilacs blooming in Nov/Dec may be due to the negative effect of high temperatures involved in the forcing procedure. Negative effects of high temperatures on the generative flower parts were earlier revealed in lilacs forced in November by the standard method (Je˛drzejuk, 2005; Je˛drzejuk and Łukaszewska, 2008a,b,c) while no such effects were observed in lilacs gently forced under constant temperature of 15 C (to be published). It is, therefore, not surprising that the postharvest longevity of flowers produced following a gentle procedure was so high. Somewhat surprising was the intermediate position of the flowers produced on shrubs growing under natural conditions and flowering in May. Perhaps those shrubs had been exposed to some changes in ambient temperatures that adversely affected their longevity. 4.2. Longevity of cut lilac stems depending on the biocide Both biocides – used alone or combined with sucrose – significantly prolonged the vase life of lilacs in all seasons. The best results were obtained for inflorescences on stems blooming in January and kept in 8-HQC and 8-HQC + S: they lasted for 11.3 and 12 days, respectively, longer than any other treatment or the controls. Similar observations were earlier made by Skolimowska et al. (2011) on the same cultivar. Esters of HQ are commonly used in the flower preservatives (Halevy and Mayak, 1981). Nanosilver releases silver ions (Ag+), which accounts for its antibacterial effect (Rai et al., 2009; Marambio-Jones and Hoek, 2010; Li et al., 2012). In this study, NS at 1 mg L1 was used. This concentration was chosen after preliminary trials to find the optimal concentration of NS for cut lilacs. On all three flowering dates tested, addition of NS to water or to the 2% sucrose solution significantly prolonged the vase life relative to distilled water, to over 10 days in lilacs blooming in January. However, this was still belowthe 8-HQC solutions. The solutions containing different NS concentrations are commonly used for cut ornamentals. Liu et al. (2009) demonstrated that pulsing with 5 mg L1 NS, prolonged cut gerbera longevity from 3.6 to 9 days; the vase life of roses was prolonged to 22 days by a 24 h pulse treatment with 10 g L1 NS plus 5% sucrose followed by holding the flowers in 0.5 mg dm3 NS plus 2% sucrose. In A. holoserica, stems in 0.5–1 g L1 of NS kept up to 9.2–9.9 days (Liu et al., 2012). 4.3. Frequency of stem blockage depending on the flowering date Physiological blockage in stem vessels of cut ornamentals may be caused by the formation of tyloses. This phenomenon is defined as uncontrolled growth of cells into the vessel lumen forming balloonlike protrusions. These ’balloons’, commonly referred to as ‘tyloses’,
(i); – tylose. (j–l) stems kept in 200 mg L1 8HQC + 2% sucrose. November standard forcing and flowering in November/December (j), November alternative forcing and flowering in January (k), natural flowering in May (l); – tylose. (m–o) Stems kept in 1 mg L1 NS. November standard forcing and flowering in November/December (m), November alternative forcing and flowering in January (n), natural flowering in May (o); – tylose. (p–s) Stems kept in 1 mg L1 NS + 2% sucrose. November standard forcing and flowering in November/December (p), November alternative forcing and flowering in January (r), natural flowering in May (s); – tylose.
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do not occur in sufficient numbers to explain the blockage of water transport towards the flowers but their formation is accompanied by the production of the high molecular weight substances which reduced water fluidity (Van Doorn, 1999; da Silva Vieira et al., 2013). In common lilac, tyloses are the main type of xylem occlusions, as shown earlier by Je˛drzejuk and Zakrzewski (2009) in the violet flowering cultivar ‘Andenken an Ludwig Spaeth’ and now also in a white-flowering cultivar. Practically, no microflora was detected in xylemvessels although some kind of an amorphous substance was at times observed to block water flow in stems. 4.4. Frequency of stem blockage depending on the biocide According to van Doorn et al. (1991), stems of common lilac kept in distilled water wilt after 4–6 days, but those placed in the antibacterial 8-HQC can last up to 20 days. In this study, the average longevity of cut lilacs in distilled water was 2.4 days for those flowering in November and up to 9.2 days for those flowering in January. A possible explanation for such a short vase life for the November bloom in distilled water is poor quality of the panicles and a very low water uptake, which was probably impaired by tyloses and bacteria in stem vessels.This study also tested the 8-HQC solutions, either alone or with sucrose. In Nov/Dec the incidence of blockages in the stems was 80% and 40%, respectively, in January it was 50% and 28% and in May it increased back to the levels observed in Nov/Dec. However, the tyloses did not block vessels completely making the water flow possible, so on all three dates both solutions increased the lilac vase life relative to the respective controls. Similar effects were observed in cut Clematis vitalba stems where the standard preservative increased the vase life but did not limit the blockage incidence although – similarly to lilac – the vessels were only partially blocked and were able to conduct water (Je˛drzejuk et al., 2012). According to van Doorn et al. (1991), 8-HQC is capable of prolonging the vase life of cut lilacs for up to 20 days; in this study it was prolonged up to 12 days in plants flowering in January with a sucrose supplement. This difference may be a result of a relatively high number of tyloses partialy blocking vascular vessels (28% in the stems of plants flowering in January and kept in a solution of 8-HQC + S and up to 86% in stems flowering in May and kept in 8-HQC without sucrose). van Doorn et al. (1991), did not observe bacteria in the 8-HQC solution nor in the stem ends; here, no bacteria were visible in stem ends, but some were present in the holding solution: 3.8–3.9 104 CFU mL1. This is much lower than the critical value of 107 CFU mL1 found to cause blockages and premature wilting of cut roses (Put, 1989). The absence of bacteria in stem ends is definitely a result of the antibacterial properties of the HQC esters and retardation of bacteria development that for the relatively short vase-life of cut lilac stems, were unable to spread into the stem vessels. Addition of NS and, especially, of NS + S, almost completely prevented the tylose formation in the stems. For all three harvest dates held in the solution of 1 mg L1 NS with 2% sucrose the numbers of blocked vessels ranged between 5% and 11%. As the nanosilver particles are becoming increasingly popular as components of cut flower preservatives, it is now clear that NS can also be successfully used for cut lilacs. According to van Doorn et al. (1991), in the solution of STS bacteria were present in stem ends, while in current study no bacteria were observed in stem vessels, though on the last day of observations the number of bacteria in the NS solution was: 3.5–3.6 104 CFU mL1. Such a low count may also be attributed to the strong antibacterial effect of nanosilver that delayed bacteria propagation.
4.5. Incidence of blockages and the lilac vase life There was a close relationship between the flowering date, holding solution, blockage incidence and the lilac postharvest longevity (Tables 1 and 2). The vase life was always the shortest for straight water while each holding solution increased it, and the increase was evident on each observation date. As to the flowering date, the vase life was the shortest in inflorescences subjected to the standard forcing procedure and blooming in Nov/Dec and the longest in January. The average percentage of blocked vessels was also the highest in the Nov/Dec-flowering stems while the lowest in those flowering in January. One might thus jump to a conclusion that the lower percentage of blocked vessels the longer would be a vase life of cut lilacs. However, a closer examination of the effects of holding solutions on both the vase life and blockage incidence implies that the lilac vase life was not directly related to the severity of xylem obstructions by tyloses near the cutting surface. Stems kept in water had their vessels blocked by 60% and lasted barely 2.4 days while those kept in the 8-HQC solution were blocked by over 80% and lasted more than 2.5 times longer. The NS-containing solutions drastically limited the tylose development but were less effective in prolonging the flower vase life than the 8-HQC solutions where the tylose development was more pronounced than in the silver treated stems. Both biocides tested (8-HQC and NS) prolonged the vase life of cut lilacs. The surprising fact is that the numbers of tyloses blocking xylem vessels dropped with the addition of 2% sucrose. Perhaps sucrose served as a supplementary respiration substrate and contributed to the increased water uptake thus limiting the water stress which may stimulate tylose formation. The longest vase life of lilacs was observed in the stems gently forced by the alternative method. This can perhaps be explained by the best panicle quality as well as the highest uptake of the holding solution. These stems formed the least number of tyloses. In stems kept in distilled water, the direct reason for the drastically short vase life in November and May was the complete blockage of the xylem vessels by tyloses and bacteria. However, no direct relationship between the number of tyloses in cut lilac stems and their vase life has been found. 5. Conclusions 1. The flowering date of cut lilac stems in the white cultivar “Mme Florent Stepman” affected the inflorescence longevity, and that longevity could be prolonged by a holding solution. 2. Practically no bacteria were detectable in lilac tracheary elements while their low amounts were found in the holding solutions. 3. Formation of tyloses was the main cause of vascular obstruction in cut lilac stems although their incidence did not appear to be directly related to their vase life. Lilac vase life can be prolonged by the florists’ preservatives irrespective of their effect of the tylose formation.
Acknowledgements This research was partly supported by Grant of Ministry of Science and Higher Education No. 0893/B/P01/2009/36. The authors would like to thank Prof. Adam J. Łukaszewski (University of California, Riverside, Department of Botany and Plant Sciences) for linguistic corrections of the manuscript.
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References Biggs, A.R., 1987. Occurrence and location of suberin in wound reaction zones in xylem of 17 tree species. Phytopathol 77, 718–725. Canny, M.J., 1997. Tyloses and the maintenance of transpiration. Ann. Bot. 80, 565–570. Clerivet, A., Deon, V., Alami, I., Lopez, F., Geiger, J.P., Nicole, M., 2001. Tyloses and gels associated with cellulose accumulation in vessels are responses of plane tree seedlings (Platanus x acerifolia) to the vascular fungus Ceratocystis fimbriata f. sp. platani. Trees 15, 25–31. da Silva Vieira, M.R., Santos, C.M.G., Vacaro de Souza, A., de Alencar Paes, R., Ferreira da Silva, L., 2013. Physiological blockage in plants in response to postharvest stress. Afr. J. Biotechnol. 12 (11), 1168–1170. Dale, A., Sample, A., King, E., 1999. Breaking dormancy in red raspberries for greenhouse production. Hortic. Sci. 38 (4), 515–519. Damunupola, J.W., Joyce, D.C., 2008. When is a vase solution biocide not, or not only, antimicrobial? J. Jpn. Soc. Hortic. Sci. 77 (3), 211–228. Esau, K., 1977. Anatomy of Seed Plants, 2nd ed. Wiley, New York, USA. Halevy, A.H., Mayak, S., 1981. Senescence and postharvest physiology of cut flowers—part 2. Hortic. Rev. 3, 59–141. He, S., Joyce, D.C., Irving, D.E., Faragher, J.D., 2006. Stem end blockage in cut Grevillea ‘Crimson Yul-lo’ inflorescences. Postharvest Biol. Technol. 41, 78–84. doi:http:// dx.doi.org/10.1016/j.postharvbio.2006.03.002. Je˛drzejuk, A., 2005. Ultrastructure of pollen grains from forced and unforced shrubs in common lilac. J. Plant Growth Regul. 24, 1–10. Je˛drzejuk, A., Łukaszewska, A., 2008a. High temperatures applied at fall forcing disturb ovule development in Syringa vulgaris L. Mme Florent Stepman. Acta Physiol. Plant 30, 673–678. Je˛drzejuk, A., Łukaszewska, A., 2008b. Winter forcing affects anther development in common lilac (Syringa vulgaris L.). Floric. Ornam. Biotechnol. 2 (2), 39–43. Je˛drzejuk, A., Łukaszewska, A., 2008c. Wpływ temperatury na fazy fenologiczne i jakos c kwiatostanów lilaka podczas pe˛dzenia listopadowego [influence of the temperature on phenological phases and panicle quality in Syringa vulgaris L. shrubs during November forcing]. Zeszyty Problemowe Poste˛pów Nauk Rolniczych 525, 189–195. Je˛drzejuk, A., Szlachetka, W., 2003. Effect of forcing term on morphology of flower buds and quality of panicles in lilac (Syringa vulgaris L.) Mme Florent Stepman. Ann. Warsaw Agric. Univ. SGGW Hortic. Landscape Archit. 24, 41–49. Je˛drzejuk, A., Zakrzewski, J., 2009. Xylem occlusions in the stems of common lilac during postharvest life. Acta Physiol. Plant 31, 1147–1153. Je˛drzejuk, A., Rochala, J., Zakrzewski, J., Rabiza-Swider, J., 2012. Identification of xylem occlusions occurring in cut clematis (Clematis L., fam. Ranunculaceae Juss.) stems during their vase life. Sci. World J. 1–12. doi:http://dx.doi.org/ 10.1100/2012/749281 Article ID 749281. Jones, M.L., 2002. Postproduction care and handling. Ohio Florists’ Assoc. 872, 15–16. Kyalo, T.M., Pemberton, H.B., Zajicek, J.M., 1996. Seasonal growing environment affects quality characteristics and postproduction longevity of potted miniature roses. Hortic. Sci. 31 (1), 120–121. Li, H., Huanga, X., Li, J., Liua, J., Joyce, D., Hea, S., 2012. Efficacy of nano-silver in alleviating bacteria-related blockage in cut rose cv. Movie Star stems. Postharvest Biol. Technol. 74, 36–41. Lim-Camacho, L., 2006. Australian Native Flowers in the Japanese Market: A Compendium of Market Research Results. The Centre for Native Floriculture, The University of Queensland, Gatton, Australia.
255
Liu, J., Zhang, Z., He, S., Cao, J., Lu, P., Joyce, D.C., 2009. Effects of postharvest nano silver treatments on cut flowers. Acta Hortic. 847, 245–250. Liu, J., Ratnayake, K., Joyce, D.C., He, S., Zhang, Z., 2012. Effects of three different nano-silver formulations on cut Acacia holosericea vase life. Postharvest Biol. Technol. 66, 8–15. Lok, C.N., Ho, C.M., Chen, R., He, Q.Y., Yu, W.Y., Sun, H.Z., Tam, P.K.H., Chiu, J.F., Che, C. M., 2006. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J. Proteome Res. 5, 916–924. Manning, L.E., 1995. Genetic and environmental influences on the vase life of Chamelaucium spp.. Masters Thesis. The University of Western Australia, Australia. Marambio-Jones, C., Hoek, E.M.V., 2010. A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J. Nanopart. Res. 12, 1531–1551. Pal, S., Tak, K.Y., Song, J.M., 2007. Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gramnegative bacterium Esherichia coli. Appl. Environ. Microbiol. 73, 1712–1720. Pompodakis, N.E., Terry, L.A., Joyce, D.C., Lydakis, D.E., Papadimitriou, M.D., 2005. Effect of seasonal variation and storage temperature on leaf chlorophyll fluorescence and vase life of cut roses. Postharvest Biol. Technol. 36, 1–8. Put, H.M.C., 1989. The effects on the vase life of cut rosa cultivar ‘Sonia’ of bacteria added to the vase water. Sci. Hortic. 39, 167–179. Rafdi, H.H.M., Joyce, D.C., Lisleb, A., Lib, X., Irvingd, D.E., Gupta, M., 2014. A retrospective study of vase life determinants for cut Acacia holosericea foliage. Sci. Hortic. 180, 254–261. Rai, M., Yadav, A., Gade, A., 2009. Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27, 76–83. Reid, M.S., Evans, R.Y., 1986. Control of cut flowers opening. Acta Hortic. 181, 45–54. Saitoh, T.J., Ohtani, J., Fukazawa, K., 1993. The occurrence and morphology of tyloses and gums in the vessels of Japanese hardwoods. Int. Assoc. Wood Anat. J. 14, 359–371. Skolimowska, K., Lukaszewska, A., Adamczyk, D., Rochala, J., 2011. Postharvest performance of forced cut lilacs Mme Florent Stepman as affected by harvest date and preservatives. Ann. Warsaw. Univ. Life Sci. SGGW Hortic. Landscape Archit. 32, 43–51. Sondi, I., Salopek-Sondi, B., 2004. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J. Colloid Interface Sci. 275, 177–182. Sun, Q.S., Rost, T.L., Matthews, M.A., 2006. Pruning-induced tylose development in stems of current-year shoots of Vitis vinifera (Vitaceae). Am. J. Bot. 93, 1567–1576. Sytsema-Kalkman, E.C., 1991. Post-harvest studies on Syringa vulgaris. Acta Hortic. 298, 127–134. 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, 303–311. van Doorn, W., Harkema, H., Otma, E., 1991. Is vascular blockage in stems of cut lilac flowers mediated by ethylene? Acta Hortic. 298, 177–182. van Doorn, W., 1997. Water relations of cut flowers. Hortic. Rev. 18, 1–85. Van Doorn, W.G., 1999. Vascular occlusion in cut flowers. I. General principles and recent advances. Acta Hortic. 482, 59–64. Zimmermann, M.H., 1983. Xylem Structure and the Ascent of Sap. Springer-Verlag, Berlin.
Contents lists available at ScienceDirect
Postharvest Biology and Technology journal homepage: www.elsevier.com/locate/postharvbio
Some factors affecting longevity of cut lilacs Agata Je˛drzejuk* , Julita Rabiza-Swider, Ewa Skutnik, Aleksandra Łukaszewska Department of Ornamental Plants, Faculty of Horticulture, Biotechnology and Landscape Architecture, Warsaw University of Life Sciences, Nowoursynowska 166, 02-787 Warsaw, Poland
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 May 2015 Received in revised form 3 September 2015 Accepted 12 September 2015 Available online xxx
Short vase life of cut lilac stems limits its commercial potential. Rapid wilting of cut lilac inflorescences is probably caused by blockage of water transport in stems. The purpose of this study was to recognize the nature of the occlusions blocking xylem vessels in cut stems of common lilac and to identify a relationship, if any, between the type of a holding solution, xylem blockages and vase life of lilacs flowering under different environmental conditions. The stems of the white flowering cultivar “Mme Florent Stepman” were harvested in Nov/Dec from shrubs forced from the beginning of November by a standard procedure involving treatment with 37 C, in January from shrubs forced from the beginning of November under 15 C, and in May from control shrubs, i.e., flowering naturally in the field. Cut stems were placed in distilled water, 8-HQC, a standard preservative composed of 8-HQC + 2% sucrose, nanosilver and nanosilver + 2% sucrose. Tyloses were observed in stem xylem vessels while practically no microorganisms were detectable. The incidence of blockage formation in the stems depended on the flowering date and the biocide used. The longest vase life was observed in January with 8-HQC or 8-HQC + S, but in all flowering periods the least xylem blockages were formed when NS was used as the biocide. Therefore, formation of tyloses does not appear to be directly related to the postharvest life of lilac and its vase life can be extended by standard florists’ preservatives irrespective of their effect of the xylem physical obstructions. ã 2015 Elsevier B.V. All rights reserved.
Keywords: Tyloses Vessel blockage Senescence Syringa vulgaris
1. Introduction Unobstructed water uptake is indispensable for proper flower bud opening and proper water balance in cut stems; hence it is crucial for the postharvest longevity of cut flowers (Reid and Evans, 1986). The main agent limiting water uptake by cut flowers may be the obstruction of xylem vessels which develops during the vase life. This may be a consequence of microbial growth, deposition of materials in the lumen of xylem vessels, presence of air emboli in the vascular system and formation of tyloses (van Doorn, 1997; Twumasi et al., 2005). It has been demonstrated (Twumasi et al., 2005) that hydraulic properties and dimensions of stem xylem vessels directly affect the vase life and quality of cut flowers. Tyloses are outgrowths of parenchyma cells through the vessel parenchyma pit pairs and into the lumen of the treachery elements (Esau, 1977; Zimmermann, 1983; Sun et al., 2006). Tyloses form in a wide range of species (Saitoh et al., 1993) and genetic variation in
Abbreviations: 8-HQC, 8-hydroxyquinoline citrate; NS, nanosilver; S, sucrose; WU, water uptake; RFW, relative fresh weight. * Corresponding author. E-mail address: [email protected] (A. Je˛drzejuk). http://dx.doi.org/10.1016/j.postharvbio.2015.09.018 0925-5214/ ã 2015 Elsevier B.V. All rights reserved.
the propensity to form tyloses has been reported in some genera (e.g., Quercus and Robinia) (Biggs, 1987; Saitoh et al., 1993). Formation of tyloses is a well known response to infection by pathogens (Canny, 1997) and tyloses appear at the site of stem wounding (Clerivet et al., 2001). During the postharvest life, probably as a consequence of mechanic injury at harvest, xylem vessels at the basal stem parts may become blocked by microorganisms and tyloses, but in several woody cut flowers such as roses, physiological blockages by gels and gums may also form at the interface between water and air (van Doorn, 1997). In the context of handling cut stems of ornamental plants, biocides must be used in pulsing and vase solutions in order to exploit the full postharvest longevity inherent in cut flowers (Damunupola and Joyce, 2008). The most popular and effective biocides are esters of hydroxyquinoline (HQ) and silver ions. The effectiveness of HQ as an apparent biocide in cut flower handling solutions has been known for decades (van Doorn, 1997; Damunupola and Joyce, 2008). Sulphate (HQS) and citrate (HQC) forms of HQ are most commonly used in flower handling. They may also increase flower longevity by acidifying the vase solution and by acting as antitranspirants thus limiting water losses (Halevy and Mayak, 1981; Damunupola and Joyce, 2008). Pure colloidal silver
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nano particles (nano-Ag or NS) are potent and broad spectrum antimicrobial agents (Lok et al., 2006). The mechanism of the antibacterial action of NS is not fully understood (Pal et al., 2007), however, interaction between the particles and bacterial membranes may cause structural damage leading to bacterial cell death (Sondi and Salopek-Sondi, 2004; Damunupola and Joyce, 2008). The quality of cut flowers is also affected by a range of environmental factors. These variables include plant maturity, the stage of bud opening or the season of planting and harvesting (Manning, 1995; Pompodakis et al., 2005; Rafdi et al., 2014). According to Jones (2002), poor postharvest handling may cause up to 30% loss of floriculture products. Thus, it is important to understand the diverse causes of quality loss with a view to extend the vase life of cut flowers and foliage (Rafdi et al., 2014). Common lilac (Syringa vulgaris L.) is a popular ornamental shrub. Under natural conditions of the temperate zone it blooms in May. Its flowering period is relatively short and is usually completed by the end of the month. Properly applied forcing procedures induce lilac flowering any time between November and May, filling a niche in the cut flower market when the supply of naturally flowering plants is low. Overcoming periodicity and prolonging plant flowering beyond the natural period has always been a point of interest to scientists and growers (Dale et al., 1999). Forcing is commonly used to induce flowering independently of the natural blooming date in many bulbous plants but also in ornamental shrubs and trees; it requires overcoming endodormancy. The temperatures required to begin the forcing cycle of lilac range from 37 C in November to 16 C in March. The studies on the relationship between temperature and the length of the forcing cycle have shown that forcing lilac at 15 C in November is also effective, but it requires 49 days as compared to 23 days for the standard 37 C used by most growers. However, panicles produced at 15 C are completely filled with flowers, hence more decorative, while panicles produced by the standard high temperature treatment tend to be floppy and their flowers are not completely open (Je˛drzejuk and Łukaszewska, 2008c). Flowering stems of lilac, even when placed in water immediately after harvest, quickly develop symptoms of wilting (van Doorn et al., 1991). This short vase life is probably caused by blockage of water transport in the stems (Sytsema-Kalkman, 1991; Je˛drzejuk and Zakrzewski, 2009). The purpose of this study was to identify the nature of occlusions blocking xylem vessels in cut stems of common lilac depending on flowering conditions and treatments with two common biocide solutions, and to identify a relationship, if any, between holding solution, formation of such blockages and the vase life of lilac flowering under different environmental conditions. 2. Material and methods 2.1. Plant material and conditions The experimental materials were flowering stems of common lilac (Syringa vulgaris L.) of the white cv. “Mme Florent Stepman”. Plants for the experiments were kindly provided by Mr. Michał Łyczko in Grodzisk Mazowiecki (Central Poland). Stems were cut from 6–8-year old shrubs, maintained as semi standard, each with several strong flowering stems and well developed root balls 35–40 cm in diameter. Shrubs for the experiments were dug up at the beginning of October and left in the field with their root balls exposed to low ambient temperatures. The forcing procedures started at the beginning of November: one part of shrubs were forced according to the standard procedure involving the 37 C treatment which assured flowering in late November and early December (Je˛drzejuk and Szlachetka, 2003), and the other part was forced under mild temperature of 15 C during the entire
forcing period and flowered in January (alternative forcing). Shrubs blooming naturally in the field in May were used as a control. Flowering stems were harvested when one third of florets in panicles were open, immediately transferred to the laboratory and trimmed to 50 cm. Stems were placed in distilled water (control treatment), 200 mg L1 8-HQC, standard preservative containing 200 mg L1 8-HQC with 2% sucrose, 1 mg L1 NS, and 1 mg L1 NS with 2% sucrose. The solutions were prepared in distilled water. They were not exchanged during the experiments but their depletions were supplemented to maintain steady levels, and the mouths of vases were covered with parafilm to minimize evaporation from the solution surface. There were ten stems in each treatment, individually tagged and treated as separate replications. The experiments were conducted at a constant temperature of 18–20 C and 12 h photoperiod, under luminescence light with the quantum irradiance of 25 mmol m2 s1. The relative air humidity was maintained at 60%. Lilac vase life was regarded as terminated if 30% of the florets wilted, dried up and/or turned brown. 2.2. Bacterial counts To determine bacterial populations in holding solutions, 0.5 mL aliquots were taken in triplicate from each holding solution on the last day of the lilac’s vase life. Samples were serially diluted with 0.9% sterile normal saline (NaCl). The 0.1 mL aliquots were spread over agar plates and incubated at 30 C for 24 h.Colony counts were expressed as colony forming units per ml (CFU mL1). 2.3. Relative fresh weight The fresh weights of cut stems were measured daily. The relative fresh weight (RFW) of stems was calculated using the formula: RFW (%) = (FWt/FWt = 0) 100; where FWt is the fresh weight of stem (g) at t = days 0, 1, 2, etc., and FWt = 0 is the fresh weight of stem (g) at t = day 0 (He et al., 2006). 2.4. Water uptake The average daily water uptake (WU) was calculated using the following formula: WU (g stem1 d1) = (St 1 St), where St is the weight vase of solution (g) at t = days 1, 2, 3, etc., and St1 is the weight of holding solution (g) on the previous day (day 0) (He et al., 2006). 2.5. Microscopic observations The material for microscopy was sampled immediately after harvest (the basal part) and later from all treatments when 1/3 of panicles on stems held in water were wilted and/or dry. The specimen were boiled for 4 h in distilled water, fixed in 5% glutaraldehyde and 4% paraformaldehyde solution in 0.1 M sodium cacodylate buffer (pH 7.2–7.3) at 0.8 atm at room temperature and rinsed with the same buffer. Next, samples were dehydrated by graded ethanol series (30, 50, 70, 80, 90, 100%), and dried at RT for 24 h. Observations were made under a scanning electron microscope (SEM) FEI QUANTA 200 ESEM with digital camera EDS EDAX, at the Analytical Centre, Warsaw University of Life Sciences. The samples were not dried to the critical point. Basal segments 1 cm long from each of ten stems from each treatment were examined. 2.6. Statistical analyses Data were analyzed by the General Linear Model program of the IBM SPSS Statistics Data Editor (Softonic, Poland), and means were compared by the Tukey–Kramer multiple range test.
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Table 1 Longevity of cut lilacs ‘Mme Florent Stepman’ as affected by a flowering date and a holding solution. Longevity (days)
Distilled water 200 mg L1 8-HQC 200 mg L1 8-HQC + 2% sucrose 1 mg L1 NS 1 mg L1 NS + 2% sucrose
November standard forcing (blooming in November/ December)
November alternative forcing (blooming in January)
Natural flowering in May
2.4 a 6.2 e 6.8 f
9.2 j 11.3 m 12.0 n
5.0 b 7.9 g 8.0 h
5.2 c 5.8 d
10.4 k 10.7 l
8.0 h 8.5 i
Means followed by the same letter do not differ significantly at a = 0.05. P < 0.001.
3. Results 3.1. Vase life, relative fresh weight and water uptake of lilacs harvested on different dates and held in different solutions The inflorescences on stems kept in distilled water and blooming in Nov/Dec wilted after 2.4 days, those blooming in January—after 9.2 days while those taken from shrubs flowering
outdoors in May after 5.0 days (Table 1). The longevity of stems from the same flowering dates but kept in 8-HQC was 6.2 days, 11.3 and almost 8 days, respectively. For the NS and NS with + S solutions, the corresponding longevities were 5.2 and 5.8 days, 10.4 and 10.7 days, and 8 and 8.5 days. In all cases, stems from shrubs flowering in January had the highest longevity. The relative fresh weight of stems, after a brief initial increase, showed a steady reduction over the duration of the experiment,
Fig. 1. Relative fresh weight of cut common lilac stems flowering under different conditions and held in various solutions. (a) November standard forcing (blooming in November/December). (b) November alternative forcing (blooming in January). (c) Natural flowering in May. Means of 10 replicates Standard Deviation.
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but at different rates depending on the flowering date and keeping solutions. For stems kept in distilled water, the relative fresh weight for the November/December flowering dropped to ca 44% of the initial weight (Fig. 1a). In this treatment, the water uptake increased only on the second day of observations, and then it kept decreasing to reach 0.1 g g1 of the initial FW between the 9th and the last day of observations (Fig. 2a). In stems collected from the January flowering kept in water the relative fresh weight dropped to 52% on the last day of observations (Fig. 1b). Here, the water uptake increased between the 2nd and the 6th day, and then dropped to 0.1 g g1 of the initial FW on the last day of observations (Fig. 2b). In stems collected from shrubs blooming in May the
relative fresh weight in stems kept in distilled water was 47% on the last day of observations (Fig. 1c). In this treatment, the water uptake was similar to that observed in stems blooming in January (Fig. 2c). For all flowering dates, the curves of RFW and WU for stems kept in 8-HQC and 8-HQC + S were similar (Figs. 1 a–c and 2 a–c). The drop in the fresh weight was slower and less dramatic than for stems kept in water, and it reached ca 80% on the last day of observations. The daily water uptake kept increasing until days 4–6, reaching the maximum of 0.32–0.62 g g1 while on the last day it dropped to 0.18–0.27 g g1 of the initial FW. In stems held in the two silver solutions (with or without sucrose) the curves for
Fig. 2. Water uptake of cut common lilac stems flowering under different conditions and held in various solutions. (a) November standard forcing (blooming in November/ December). (b) November alternative forcing (blooming in January). (c) Natural flowering in May. Means of 10 replicates Standard Deviation.
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Table 2 Number of bacteria in holding solution. Number of bacteria
Distilled water 200 mg L1 8-HQC 200 mg L1 8-HQC + 2% sucrose 1 mg L1 NS 1 mg L1 NS + 2% sucrose
November standard forcing (blooming in November/ December) (CFU mL1)
November alternative forcing (blooming in January) (CFU mL1)
Natural flowering in May (CFU mL1)
4.8 105 e 3.8 104 c 3.8 104 c
4.8 105 e 3.8 104 c 3.8 104 c
5.1 105 f 3.8 104 c 3.9 104 d
3.5 104 a 3.5 104 a
3.5 104 a 3.5 104 a
3.6 104 b 3.6 104 b
Means followed by the same letter do not differ significantly at p = 0.05.
the relative fresh weight and water uptake were similar to those for the 8-HQC solutions (Figs. 1 a–c and 2 a–c). On the last observation day the stems from all flowering dates had their fresh weight at the 78–85% of the initial level. In stems blooming in Nov/Dec, the water uptake increased to 0.32 g g1 of the initial FW on the 4th day of observations, and dropped to 0.18 g g1 of the initial FW on the last day of observations (Fig. 2a). In stems blooming in January, the initial water uptake was 0.35 g g1 of the initial FW, and on the 6th day of observations it reached 0.62 g g1 of the initial FW (Fig. 2b). For the May bloom, the initial and the highest values of water uptake were equal to those observed in flowers blooming in January (Fig. 2c). 3.2. Bacteria counts in holding solutions and in stem ends Generally, the number of bacteria in holding solutions was low. The highest number was found in distilled water in May flowering, reaching 5.1 105 CFU mL1 on the last day of observations. The most effective media arresting bacteria populations were NS and NS + S which reduced bacteria numbers to 3.5 104 CFU mL1 in November/December and January, and to 3.6 104 CFU mL1 in May (Table 2). Some bacteria in tracheary elements were found only in lilacs kept in distilled water and only on the last sampling dates (Fig. 3). No traces of microorganisms were detected on any sampling date in stems placed in the holding solutions tested in the experiment. 3.3. Blockage in cut stems The stems collected from forced shrubs and analyzed immediately after harvest had nearly all vessels free of any detectable blockage (Fig. 4a and b). Surprisingly, 9% of the freshly harvested
stems from shrubs flowering outdoors in May (the unforced controls) were filled with tyloses (Fig. 4c). However, those tyloses did not completely obstruct the vessel lumina, making the water flow possible. On the last day of the vase life, 60% of stems held in distilled water and blooming in Nov/Dec had identifiable tyloses in vessels of the basal stem segments. Those tyloses obstructed the entire lumen of the vessel (Fig. 4d and Table 3), especially in the outer part of the stem. In January, the basal xylem vessels were obstructed in 35% (Fig. 4e and Table 3) and the incidence of blockage in the outer and inner sections tested were similar. Tyloses filled the entire vessel lumen. In May, only 12% of vessels in the basal parts of stems held in distilled water had identifiable tyloses (Fig. 4f and Table 3). In this treatment, other occlusions composed of unidentified microbiological material were also observed (Fig. 3a,b). In the Nov/Dec flowering, nearly 80% vessels in stems held in 200 g L1 8-HQC were blocked by tyloses on the day when the control lilacs wilted (Fig. 4g and Table 3). Blocked vessels were present both in the outer and in inner parts of the stems, but most tyloses blocked only about one half of the vessel lumen, leaving openings for water flow. In January, ca 50% of vessels were blocked by tyloses and these were present mostly in the outer parts of the stems (Fig. 4h and Table 3). Similarly to the stems collected from the Nov/Dec flowering, the tyloses blocked only parts of the vessel lumen. In May, the basal stem segments had 86% of their vessels blocked by tyloses which still did not fill the entire xylem lumen (Fig. 4i and Table 3). Blocked vessels were present equally in the outer as in the inner parts of the stems.In stems from the standard November forcing held in 200 g L1 8-HQC + 2% sucrose, ca 40% vessels were blocked by tyloses (Fig. 4j and Table 3), both in the outer and in inner parts of the stem, but most tyloses blocked only about one half of the vessel lumen, leaving openings for water
Fig. 3. Evidence of bacteria presence in stem ends of lilac held in distilled water on the last day of observations. (a) in vessels.
– extracellular polysaccharides, (b) ! – bacteria located
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Fig. 4. Xylem structure in stems of common lilac ‘Mme Florent Stepman’. (a–c) Freshly harvested stems in: November standard forcing and flowering in November/December (a), November alternative forcing and flowering in January (b), natural flowering in May (c); v – vessel, - – tylose. (d–f) Stems kept in distilled water. November standard forcing and flowering in November/December (d), November alternative forcing and flowering in January (e), natural flowering in May (f); – tylose. (g–i) Stems kept in 200 mg L1 8HQC. November standard forcing and flowering in November/December (g), November alternative forcing and flowering in January (h), natural flowering in May
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Table 3 Frequency of vessel blockage (%) and the blockage severity in the basal stem parts in cut lilac ‘Mme Florent Stepman’ as affected by a flowering date and a holding solution (evaluated on a day when the control flowers wilted). Frequency of vessel blockage (%) and the blockage severity
Distilled water 200 mg L1 8-HQC 200 mg L1 8-HQC + 2% sucrose 1 mg L1 NS 1 mg L1 NS + 2% sucrose
November standard forcing (blooming in November/ December)
November alternative forcing (blooming in January)
Natural flowering in May
60.0 k * 80.8 l 40.0 i
35.0 h * 49.7 j 28.0 g
12.0 c * 86.2 m 40.0 i
21.2 f 5.0 a
18.6 d 5.0 a
17.8 e 11.0 b
Means followed by the same letter do not differ significantly at p = 0.05. * – Vessel completely blocked.
flow. In lilacs flowering in January after alternative forcing, 28% of vessels in the stems were filled with tyloses occurring equally in the outer and inner part of the stem (Fig. 4k and Table 3). In May, the basal stem segments had 40% of their vessels blocked by tyloses which, however, did not fill the whole xylem lumen (Fig. 4l and Table 3). Blocked vessels were present equally in the outer as in the inner parts of the stem. In lilacs flowering in Nov/Dec held in 1 g L1 NS21% of vessels in stems held in the NS solution were blocked by tyloses (Fig. 4m and Table 3). Blocked vessels were present both in the outer and in inner parts of the stem, but most tyloses blocked only about half of the vessel lumen, leaving openings for water flow. In January, almost 19% of vessels were blocked by tyloses, equally distributed in the outer and inner part of the stem (Fig. 4n and Table 3). In May, ca 18% of vessels were blocked by tyloses which did not fill the whole xylem lumen (Fig. 4o and Table 3). Blocked vessels were present equally in the outer as in the inner parts of the stem. On the day the control stems wilted, the stems held in 1 g L1 NS with 2% sucrose had only few vessels blocked and this was true for all flowering dates. Tyloses blocked ca 5% of vessels in stems after forcing (Fig. 3p and r and Table 2) and 11% in stems harvested from naturally flowering shrubs in May (Fig. 4s and Table 3). 4. Discussion 4.1. Longevity of cut lilacs depending on the flowering date A long vase life is a prerequisite for commercialization of cut flowers (Rafdi et al., 2014; Lim-Camacho, 2006). The quality of cut flowers is affected by a range of environmental factors and management practices throughout the marketing chain (Manning, 1995; Pompodakis et al., 2005; Rafdi et al., 2014). One of the significant factors determining the postharvest life of cut ornamentals is the season of flowering, and thus flowering conditions and the physiological state of plants at harvest. In Acacia holoserica, stems blooming from winter to spring had an average vase life of 4.8 1.1 days while for summer and autumn it was significantly prolonged, to 7.3 1.4 (Rafdi et al., 2014). Postharvest floral longevity of miniature cut roses was 14.3 days during their growth under long day and high temperature, while under short day and low temperature, it was reduced to 9.9 days (Kyalo et al., 1996). In the current experiment the shortest vase life was observed in lilacs forced in November by the standard method and flowering in Nov/Dec; the longest vase life was in flowers forced by the alternative method, and blooming in January, while inflorescences from shrubs growing outdoors under natural conditions had an
– Vessel partly blocked.
intermediate longevity. Reduction of the vase life in lilacs blooming in Nov/Dec may be due to the negative effect of high temperatures involved in the forcing procedure. Negative effects of high temperatures on the generative flower parts were earlier revealed in lilacs forced in November by the standard method (Je˛drzejuk, 2005; Je˛drzejuk and Łukaszewska, 2008a,b,c) while no such effects were observed in lilacs gently forced under constant temperature of 15 C (to be published). It is, therefore, not surprising that the postharvest longevity of flowers produced following a gentle procedure was so high. Somewhat surprising was the intermediate position of the flowers produced on shrubs growing under natural conditions and flowering in May. Perhaps those shrubs had been exposed to some changes in ambient temperatures that adversely affected their longevity. 4.2. Longevity of cut lilac stems depending on the biocide Both biocides – used alone or combined with sucrose – significantly prolonged the vase life of lilacs in all seasons. The best results were obtained for inflorescences on stems blooming in January and kept in 8-HQC and 8-HQC + S: they lasted for 11.3 and 12 days, respectively, longer than any other treatment or the controls. Similar observations were earlier made by Skolimowska et al. (2011) on the same cultivar. Esters of HQ are commonly used in the flower preservatives (Halevy and Mayak, 1981). Nanosilver releases silver ions (Ag+), which accounts for its antibacterial effect (Rai et al., 2009; Marambio-Jones and Hoek, 2010; Li et al., 2012). In this study, NS at 1 mg L1 was used. This concentration was chosen after preliminary trials to find the optimal concentration of NS for cut lilacs. On all three flowering dates tested, addition of NS to water or to the 2% sucrose solution significantly prolonged the vase life relative to distilled water, to over 10 days in lilacs blooming in January. However, this was still belowthe 8-HQC solutions. The solutions containing different NS concentrations are commonly used for cut ornamentals. Liu et al. (2009) demonstrated that pulsing with 5 mg L1 NS, prolonged cut gerbera longevity from 3.6 to 9 days; the vase life of roses was prolonged to 22 days by a 24 h pulse treatment with 10 g L1 NS plus 5% sucrose followed by holding the flowers in 0.5 mg dm3 NS plus 2% sucrose. In A. holoserica, stems in 0.5–1 g L1 of NS kept up to 9.2–9.9 days (Liu et al., 2012). 4.3. Frequency of stem blockage depending on the flowering date Physiological blockage in stem vessels of cut ornamentals may be caused by the formation of tyloses. This phenomenon is defined as uncontrolled growth of cells into the vessel lumen forming balloonlike protrusions. These ’balloons’, commonly referred to as ‘tyloses’,
(i); – tylose. (j–l) stems kept in 200 mg L1 8HQC + 2% sucrose. November standard forcing and flowering in November/December (j), November alternative forcing and flowering in January (k), natural flowering in May (l); – tylose. (m–o) Stems kept in 1 mg L1 NS. November standard forcing and flowering in November/December (m), November alternative forcing and flowering in January (n), natural flowering in May (o); – tylose. (p–s) Stems kept in 1 mg L1 NS + 2% sucrose. November standard forcing and flowering in November/December (p), November alternative forcing and flowering in January (r), natural flowering in May (s); – tylose.
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do not occur in sufficient numbers to explain the blockage of water transport towards the flowers but their formation is accompanied by the production of the high molecular weight substances which reduced water fluidity (Van Doorn, 1999; da Silva Vieira et al., 2013). In common lilac, tyloses are the main type of xylem occlusions, as shown earlier by Je˛drzejuk and Zakrzewski (2009) in the violet flowering cultivar ‘Andenken an Ludwig Spaeth’ and now also in a white-flowering cultivar. Practically, no microflora was detected in xylemvessels although some kind of an amorphous substance was at times observed to block water flow in stems. 4.4. Frequency of stem blockage depending on the biocide According to van Doorn et al. (1991), stems of common lilac kept in distilled water wilt after 4–6 days, but those placed in the antibacterial 8-HQC can last up to 20 days. In this study, the average longevity of cut lilacs in distilled water was 2.4 days for those flowering in November and up to 9.2 days for those flowering in January. A possible explanation for such a short vase life for the November bloom in distilled water is poor quality of the panicles and a very low water uptake, which was probably impaired by tyloses and bacteria in stem vessels.This study also tested the 8-HQC solutions, either alone or with sucrose. In Nov/Dec the incidence of blockages in the stems was 80% and 40%, respectively, in January it was 50% and 28% and in May it increased back to the levels observed in Nov/Dec. However, the tyloses did not block vessels completely making the water flow possible, so on all three dates both solutions increased the lilac vase life relative to the respective controls. Similar effects were observed in cut Clematis vitalba stems where the standard preservative increased the vase life but did not limit the blockage incidence although – similarly to lilac – the vessels were only partially blocked and were able to conduct water (Je˛drzejuk et al., 2012). According to van Doorn et al. (1991), 8-HQC is capable of prolonging the vase life of cut lilacs for up to 20 days; in this study it was prolonged up to 12 days in plants flowering in January with a sucrose supplement. This difference may be a result of a relatively high number of tyloses partialy blocking vascular vessels (28% in the stems of plants flowering in January and kept in a solution of 8-HQC + S and up to 86% in stems flowering in May and kept in 8-HQC without sucrose). van Doorn et al. (1991), did not observe bacteria in the 8-HQC solution nor in the stem ends; here, no bacteria were visible in stem ends, but some were present in the holding solution: 3.8–3.9 104 CFU mL1. This is much lower than the critical value of 107 CFU mL1 found to cause blockages and premature wilting of cut roses (Put, 1989). The absence of bacteria in stem ends is definitely a result of the antibacterial properties of the HQC esters and retardation of bacteria development that for the relatively short vase-life of cut lilac stems, were unable to spread into the stem vessels. Addition of NS and, especially, of NS + S, almost completely prevented the tylose formation in the stems. For all three harvest dates held in the solution of 1 mg L1 NS with 2% sucrose the numbers of blocked vessels ranged between 5% and 11%. As the nanosilver particles are becoming increasingly popular as components of cut flower preservatives, it is now clear that NS can also be successfully used for cut lilacs. According to van Doorn et al. (1991), in the solution of STS bacteria were present in stem ends, while in current study no bacteria were observed in stem vessels, though on the last day of observations the number of bacteria in the NS solution was: 3.5–3.6 104 CFU mL1. Such a low count may also be attributed to the strong antibacterial effect of nanosilver that delayed bacteria propagation.
4.5. Incidence of blockages and the lilac vase life There was a close relationship between the flowering date, holding solution, blockage incidence and the lilac postharvest longevity (Tables 1 and 2). The vase life was always the shortest for straight water while each holding solution increased it, and the increase was evident on each observation date. As to the flowering date, the vase life was the shortest in inflorescences subjected to the standard forcing procedure and blooming in Nov/Dec and the longest in January. The average percentage of blocked vessels was also the highest in the Nov/Dec-flowering stems while the lowest in those flowering in January. One might thus jump to a conclusion that the lower percentage of blocked vessels the longer would be a vase life of cut lilacs. However, a closer examination of the effects of holding solutions on both the vase life and blockage incidence implies that the lilac vase life was not directly related to the severity of xylem obstructions by tyloses near the cutting surface. Stems kept in water had their vessels blocked by 60% and lasted barely 2.4 days while those kept in the 8-HQC solution were blocked by over 80% and lasted more than 2.5 times longer. The NS-containing solutions drastically limited the tylose development but were less effective in prolonging the flower vase life than the 8-HQC solutions where the tylose development was more pronounced than in the silver treated stems. Both biocides tested (8-HQC and NS) prolonged the vase life of cut lilacs. The surprising fact is that the numbers of tyloses blocking xylem vessels dropped with the addition of 2% sucrose. Perhaps sucrose served as a supplementary respiration substrate and contributed to the increased water uptake thus limiting the water stress which may stimulate tylose formation. The longest vase life of lilacs was observed in the stems gently forced by the alternative method. This can perhaps be explained by the best panicle quality as well as the highest uptake of the holding solution. These stems formed the least number of tyloses. In stems kept in distilled water, the direct reason for the drastically short vase life in November and May was the complete blockage of the xylem vessels by tyloses and bacteria. However, no direct relationship between the number of tyloses in cut lilac stems and their vase life has been found. 5. Conclusions 1. The flowering date of cut lilac stems in the white cultivar “Mme Florent Stepman” affected the inflorescence longevity, and that longevity could be prolonged by a holding solution. 2. Practically no bacteria were detectable in lilac tracheary elements while their low amounts were found in the holding solutions. 3. Formation of tyloses was the main cause of vascular obstruction in cut lilac stems although their incidence did not appear to be directly related to their vase life. Lilac vase life can be prolonged by the florists’ preservatives irrespective of their effect of the tylose formation.
Acknowledgements This research was partly supported by Grant of Ministry of Science and Higher Education No. 0893/B/P01/2009/36. The authors would like to thank Prof. Adam J. Łukaszewski (University of California, Riverside, Department of Botany and Plant Sciences) for linguistic corrections of the manuscript.
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References Biggs, A.R., 1987. Occurrence and location of suberin in wound reaction zones in xylem of 17 tree species. Phytopathol 77, 718–725. Canny, M.J., 1997. Tyloses and the maintenance of transpiration. Ann. Bot. 80, 565–570. Clerivet, A., Deon, V., Alami, I., Lopez, F., Geiger, J.P., Nicole, M., 2001. Tyloses and gels associated with cellulose accumulation in vessels are responses of plane tree seedlings (Platanus x acerifolia) to the vascular fungus Ceratocystis fimbriata f. sp. platani. Trees 15, 25–31. da Silva Vieira, M.R., Santos, C.M.G., Vacaro de Souza, A., de Alencar Paes, R., Ferreira da Silva, L., 2013. Physiological blockage in plants in response to postharvest stress. Afr. J. Biotechnol. 12 (11), 1168–1170. Dale, A., Sample, A., King, E., 1999. Breaking dormancy in red raspberries for greenhouse production. Hortic. Sci. 38 (4), 515–519. Damunupola, J.W., Joyce, D.C., 2008. When is a vase solution biocide not, or not only, antimicrobial? J. Jpn. Soc. Hortic. Sci. 77 (3), 211–228. Esau, K., 1977. Anatomy of Seed Plants, 2nd ed. Wiley, New York, USA. Halevy, A.H., Mayak, S., 1981. Senescence and postharvest physiology of cut flowers—part 2. Hortic. Rev. 3, 59–141. He, S., Joyce, D.C., Irving, D.E., Faragher, J.D., 2006. Stem end blockage in cut Grevillea ‘Crimson Yul-lo’ inflorescences. Postharvest Biol. Technol. 41, 78–84. doi:http:// dx.doi.org/10.1016/j.postharvbio.2006.03.002. Je˛drzejuk, A., 2005. Ultrastructure of pollen grains from forced and unforced shrubs in common lilac. J. Plant Growth Regul. 24, 1–10. Je˛drzejuk, A., Łukaszewska, A., 2008a. High temperatures applied at fall forcing disturb ovule development in Syringa vulgaris L. Mme Florent Stepman. Acta Physiol. Plant 30, 673–678. Je˛drzejuk, A., Łukaszewska, A., 2008b. Winter forcing affects anther development in common lilac (Syringa vulgaris L.). Floric. Ornam. Biotechnol. 2 (2), 39–43. Je˛drzejuk, A., Łukaszewska, A., 2008c. Wpływ temperatury na fazy fenologiczne i jakos c kwiatostanów lilaka podczas pe˛dzenia listopadowego [influence of the temperature on phenological phases and panicle quality in Syringa vulgaris L. shrubs during November forcing]. Zeszyty Problemowe Poste˛pów Nauk Rolniczych 525, 189–195. Je˛drzejuk, A., Szlachetka, W., 2003. Effect of forcing term on morphology of flower buds and quality of panicles in lilac (Syringa vulgaris L.) Mme Florent Stepman. Ann. Warsaw Agric. Univ. SGGW Hortic. Landscape Archit. 24, 41–49. Je˛drzejuk, A., Zakrzewski, J., 2009. Xylem occlusions in the stems of common lilac during postharvest life. Acta Physiol. Plant 31, 1147–1153. Je˛drzejuk, A., Rochala, J., Zakrzewski, J., Rabiza-Swider, J., 2012. Identification of xylem occlusions occurring in cut clematis (Clematis L., fam. Ranunculaceae Juss.) stems during their vase life. Sci. World J. 1–12. doi:http://dx.doi.org/ 10.1100/2012/749281 Article ID 749281. Jones, M.L., 2002. Postproduction care and handling. Ohio Florists’ Assoc. 872, 15–16. Kyalo, T.M., Pemberton, H.B., Zajicek, J.M., 1996. Seasonal growing environment affects quality characteristics and postproduction longevity of potted miniature roses. Hortic. Sci. 31 (1), 120–121. Li, H., Huanga, X., Li, J., Liua, J., Joyce, D., Hea, S., 2012. Efficacy of nano-silver in alleviating bacteria-related blockage in cut rose cv. Movie Star stems. Postharvest Biol. Technol. 74, 36–41. Lim-Camacho, L., 2006. Australian Native Flowers in the Japanese Market: A Compendium of Market Research Results. The Centre for Native Floriculture, The University of Queensland, Gatton, Australia.
255
Liu, J., Zhang, Z., He, S., Cao, J., Lu, P., Joyce, D.C., 2009. Effects of postharvest nano silver treatments on cut flowers. Acta Hortic. 847, 245–250. Liu, J., Ratnayake, K., Joyce, D.C., He, S., Zhang, Z., 2012. Effects of three different nano-silver formulations on cut Acacia holosericea vase life. Postharvest Biol. Technol. 66, 8–15. Lok, C.N., Ho, C.M., Chen, R., He, Q.Y., Yu, W.Y., Sun, H.Z., Tam, P.K.H., Chiu, J.F., Che, C. M., 2006. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J. Proteome Res. 5, 916–924. Manning, L.E., 1995. Genetic and environmental influences on the vase life of Chamelaucium spp.. Masters Thesis. The University of Western Australia, Australia. Marambio-Jones, C., Hoek, E.M.V., 2010. A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J. Nanopart. Res. 12, 1531–1551. Pal, S., Tak, K.Y., Song, J.M., 2007. Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gramnegative bacterium Esherichia coli. Appl. Environ. Microbiol. 73, 1712–1720. Pompodakis, N.E., Terry, L.A., Joyce, D.C., Lydakis, D.E., Papadimitriou, M.D., 2005. Effect of seasonal variation and storage temperature on leaf chlorophyll fluorescence and vase life of cut roses. Postharvest Biol. Technol. 36, 1–8. Put, H.M.C., 1989. The effects on the vase life of cut rosa cultivar ‘Sonia’ of bacteria added to the vase water. Sci. Hortic. 39, 167–179. Rafdi, H.H.M., Joyce, D.C., Lisleb, A., Lib, X., Irvingd, D.E., Gupta, M., 2014. A retrospective study of vase life determinants for cut Acacia holosericea foliage. Sci. Hortic. 180, 254–261. Rai, M., Yadav, A., Gade, A., 2009. Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27, 76–83. Reid, M.S., Evans, R.Y., 1986. Control of cut flowers opening. Acta Hortic. 181, 45–54. Saitoh, T.J., Ohtani, J., Fukazawa, K., 1993. The occurrence and morphology of tyloses and gums in the vessels of Japanese hardwoods. Int. Assoc. Wood Anat. J. 14, 359–371. Skolimowska, K., Lukaszewska, A., Adamczyk, D., Rochala, J., 2011. Postharvest performance of forced cut lilacs Mme Florent Stepman as affected by harvest date and preservatives. Ann. Warsaw. Univ. Life Sci. SGGW Hortic. Landscape Archit. 32, 43–51. Sondi, I., Salopek-Sondi, B., 2004. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J. Colloid Interface Sci. 275, 177–182. Sun, Q.S., Rost, T.L., Matthews, M.A., 2006. Pruning-induced tylose development in stems of current-year shoots of Vitis vinifera (Vitaceae). Am. J. Bot. 93, 1567–1576. Sytsema-Kalkman, E.C., 1991. Post-harvest studies on Syringa vulgaris. Acta Hortic. 298, 127–134. 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, 303–311. van Doorn, W., Harkema, H., Otma, E., 1991. Is vascular blockage in stems of cut lilac flowers mediated by ethylene? Acta Hortic. 298, 177–182. van Doorn, W., 1997. Water relations of cut flowers. Hortic. Rev. 18, 1–85. Van Doorn, W.G., 1999. Vascular occlusion in cut flowers. I. General principles and recent advances. Acta Hortic. 482, 59–64. Zimmermann, M.H., 1983. Xylem Structure and the Ascent of Sap. Springer-Verlag, Berlin.