Physiological and molecular basis of alternate bearing in perennial fruit crops

Scientia Horticulturae 243 (2019) 214–225

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Review

Physiological and molecular basis of alternate bearing in perennial fruit crops

T

⁎

Nimisha Sharmaa, , Sanjay Kumar Singha, Ajay Kumar Mahatob, Hutchappa Ravishankarc, Anil K. Dubeya, Nagendra Kumar Singhb a

Division of Fruits and Horticultural Technology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India National Research Centre on Plant Biotechnology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India c Ex-Director, ICAR-Central Institute for Subtropical Horticulture, Lucknow, UP, 227107, India b

A R T I C LE I N FO

A B S T R A C T

Keywords: Alternate bearing Flowering Perennial fruit crops Gene expression analysis On-off phases

In perennial fruit crops, reproductive success and productivity are principally governed by the core event, regular flowering. However, this feature bearing can be influenced by different factors viz. environmental conditions, germplasm, rootstocks, and cultural operations. The phenomenon of irregular bearing is more dominant in perennial fruit crops. In order to ensure regular and quality fruit production it is therefore, imperative to regulate the flowering phenology. The comparative studies conducted by the researchers for understanding the physiological and molecular aspects associated with regular and irregular bearing phenomenon in perennial fruit crops are helpful to understand the crux of flowering, discover the regulatory factors for regularity in bearing. Further, differential gene expression studies allow the identification of key genes related with the regular bearing feature. The identified candidate genes in this regard could be harnessed for selection of desirable parents, hybrids in early nursery stage, thus facilitating the plant breeders through precision breeding approaches. This paper reviews the current understanding of the physiological and molecular basis associated with the flowering phenology along with the impact of different factors on alternate bearing in perennial fruit crops.

1. Introduction Globally, countries possess and maintain the genetic diversity of different fruit crops important to nutrition and health of mankind. However, their relative contribution to the total production has been decreasing. Different factors appear responsible for this trend decline viz., dynamics of climate change, incidence of pests and diseases, lack of efficient rootstocks, irregular bearing etc., impacting sustainable livelihoods of growers through alternate bearing problem. Perennial fruit crops, in their phyto-gerantology, manifest two major multiannual reproductive strategies, 1) heavy fruit load (‘On’ crop) in one year, and 2) low fruit load (‘Off’ crop) in the following year. This phenomenon is prominently known as alternate bearing (AB) (Goldschmidt, 2013; Sharma et al., 2015). Some orange and grapefruit cultivars produce sufficient fruits in the first year, followed by a good amount of

vegetative growth simultaneously. This results in profuse flowering during the following year also. Moreover, these crops possess efficient mechanism(s) to control the surplus fruit production. An index was given by Hoblyn et al. (1936) that estimated the intensity of deviation in yield during consecutive years. Then Wilcox (1944), named this index as the Biennial Bearing Index (BBI). The BBI has been widely used to study the tendency of fruit yields over orchards, individual trees, or branches (Wilcox, 1944; Jonkers, 1979). The BBI has been used in various fruit crops like in apple (Barritt et al., 1997), mango (Reddy et al., 2003), coffee (Cilas et al., 2011), citrus (Smith et al., 2004), pecan (Wood et al., 2004), and pistachio (Rosenstock et al., 2010). This index is calculated by dividing the sum of the individual tree yields to the differences in successive years. For an adult tree, generally three years are enough for the evaluation of the alternative bearing. If the index value is higher then it means higher alternation. However, Racsko

Abbreviations: ABI, alternate bearing index; ABA, abscisic acid; AFL2, apple floricula/lfy; AP, apetala; BBI, biennial bearing index; BFT, brothers of ft; CiFT, citrus flowering locus T; CO, constans; DEGs, differentially expressed genes; FI, flower induction; FLC, flowering locus c; FUL, fruitful; GAs, gibberellins; LFY, leafy; MABI, modified alternate bearing index; miRNA, micro RNA; SoC1, suppressor of over expression of constants; SPL5, squamosa promoter binding; SVP, short vegetative phase; TFL1, terminal flower1 ⁎ Corresponding author. E-mail address: [email protected] (N. Sharma). https://doi.org/10.1016/j.scienta.2018.08.021 Received 28 April 2018; Received in revised form 10 August 2018; Accepted 10 August 2018 0304-4238/ © 2018 Elsevier B.V. All rights reserved.

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Fig. 1. Impact of various factors on bearing habit of perennial fruit crops.

mature buds responsive to floral induction and floral initiation, so it seems to be the main factor governing the flowering and fruit yield in the following year in olive'. In light of the above, the foregoing explains how different factors affect the bearing tendencies in perennial fruit crops.

(2008) reported that a fluctuation in yield is not sufficient for calculation of the alternate bearing. Then, researcher developed a new index so called “Modified Alternate Bearing Index” (MABI), which includes cultivar flower production to define alternate bearing. A significance test for biennial bearing was given by Huff (2001). Moreover, understanding the major events along with different environmental cues and molecular mechanisms that regulate the flower initiation, emerging of inflorescences, flower and fruit formation and effect of factors on existing fruit producing regions will be more useful (Khan et al., 2014). Extensive genomic and transcriptomic studies pave the way to discover the entire gene set, the subsets of genes mainly involved in the regulatory mechanism, various signal transduction systems, and the related metabolic pathways, focusing the identification of potential candidate genes to interpret the biological functions (Sharma et al., 2017).

2.1. Cultivars/varieties Cultivars within a given species vary in the bearing tendencies; some are regular bearers while others are alternate. For example, apple varieties show variable bearing tendencies with varieties like ‘Gala’, ‘Jonagold’, ‘Granny Smith’ and ‘Idared’ possess low alternate bearing index while, ‘Golden Delicious’ and ‘Fuji manifest’ high alternate bearing index. Haberman et al., 2016 have compared the regular and alternate (spur) type of Delicious varieties. Atay et al. (2013) studied the modified alternate bearing index (MABI) and classified the varieties into four relative classes. Varieties ‘Braeburn’ and ‘Jersey Mac’ come under no susceptible group; ‘Topaz’, ‘Granny Smith’, ‘Mondial Gala’, ‘Jonagold’, ‘Starkrimson Delicious’ and ‘Clear Red’ grouped into medium alternate whereas, ‘Kassel 37’, ‘Golden Reinders’ and ‘Kassel 41’ as showing highest level of alteration. The conceptual fact in this regard, is that varieties had the major impact on alternate bearing (Guitton et al., 2012; Smith and Samach, 2013). Earlier Crassweller et al. (2005) evaluated 20 apple varieties viz. ‘Arlet’, ‘Braeburn’, ‘Fuji’ and ‘Golden Delicious’ in order to know the extent of alternate bearing in the United States. Similarly, it was determined that variety ‘Golden Delicious’ and its strains had higher tendency to alternate bearing than the strains of ‘Delicious’. Spur-type Delicious cultivars such as ‘Starkrimson’ Delicious and ‘Red chief’ Delicious generally have alternate bearing behavior in respect of flowering and fruiting (Lauri et al., 2009). Like apple, in mango research findings have clearly attributed this phenomenon to the varietal differences. Varieties with axillary fruit bearing habit possessed less alternate bearing tendencies than the terminal bearing ones. ‘Dashehari’, ‘Langra’ and ‘Chausa’ important choice cultivars of north India are alternate bearers. While south Indian varieties like ‘Totapuri Red Small’, ‘Bangalora’, and ‘Neelum’ are known to be regular bearers (Schnell and Knight, 1992). Response of mango varieties at different height of grafting on rootstock was studied by

2. Impact of different factors on alternate bearing Flowering is governed either autonomously or by different external and internal factors and their interactions affect the flower formation in perennial fruit crops (Blázquez, 2000). Details of these factors are given in Fig. 1, Tables 1 and 2. For example, external factors like photoperiod, temperature, and water stress etc. and internal factors viz.: carbon-nitrogen ratio, hormones and interaction with other organs affect the flower formation in different fruit crops (Hanke et al., 2007; Bangerth, 2009; Takeno, 2016). For example flower set variability in apple due to the negative association between fruit development and flower bud differentiation (Foster et al., 2003) has been documented. Biennial bearing is also influenced by the number of seed per fruit or per bourse (Neilsen and Dennis, 2000). Mainly three important factors have been investigated for the alternate bearing phenomenon in perennial fruit crops (Goldschmidt, 2005). They include, i) reproductive and vegetative organs show the competition for the site of the flowering (Monselise and Goldschmidt, 1981); ii) differential amounts of nutrients during the ‘Off’ year (Rosecrance et al., 1998); and iii) endogenous phyto-hormonal control (Achard et al., 2006). Variable amounts of certain growth hormones in many fruit crops are considered core regulators for alternate bearing phenomenon (Baktir et al., 2004). Dag et al. (2010) showed that developing fruits appear to primarily depress vegetative growth and consequently the number of new and 215

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Table 1 Impact of genetic factors on bearing habit in fruit crops. Fruit Crop Apple

Effect Differentially expressed factors like GDE tempranillo (TEM), flower transition at meristem(FTM1) and squamosa • promoter binding protein-like (SPL) were identified. MdGA20ox1a andMdGA3ox-like-b on LG1 and MdGA2ox8a

• • • Citrus

Olive

Mango

Reference

• • • • • • • • • • • •

on LG10 transcripts were involved in the GA biosynthesis pathway and identified in QTL cluster intervals that control tree production and alternation. Flowering locus t (FTL) genes of apple, MdFT and MdTFL1 genes were characterized. During first years of apple production genetic value of F1 progenies play an important role in irregular bearing.This is helpful to know the bearing behavior during the first years of tree maturity and to capture genetic variations. iTRAQ-based investigation of M. prunifolia was carried out. Leaves of on and off trees were significantly differing in their proteome and metabolic content. Finally 667 differentially expressed proteins were identified that regulate the various biochemical pathways. Citrus orthologue of FT(CiFT) Differentially expressed protein in mandarins. In citrus AP3, SOC1 and WUS were functionally characterized. In citrus constitutive expression of Arabidopsis LEAFY or APETALA1 genes reduces their generation time. LEAFY and APETALA1 homologues were isolated and characterized from Citrus sinensis. MiR156-regulated SPL5 showed an increased level of mRNA in off crop buds. Further act as an inducer for flowering in citrus trees. Flowering regulator genes like FT, LFY, AP1, TFL, and miR156-regulated SPL5 in leaves and buds of citrus were differentially expressed due to the fruit load. Gene expression profiling using olive array showed the relationship with the alternate bearing in olive tree. Deep sequencing of olive tree samples at different developmental phases was carried out to study the alternate bearing. A subtractive cDNA library identified a differentially expressed gene (jat) that regulated the transition from juvenile to adult phase of the olive tree. In Olea europaea L. cv. Ayvalık, expression analysis of cDNAs has shown the association with the alternate bearing. Differential expression of flowering control genes like FT,LFY, AP1, TFL, and miR156-regulated SPL5 were seen due to the affect of fruit load in leaves and buds of mango.

Guitton et al. (2012, 2016) Kotoda et al. (2010), Tränkner et al. (2010), Mimida et al. (2011) Durand et al. (2013), Fan et al. (2016)

Endo et al. (2005), Munoz-Fambuena et al. (2013) Tan and Swain (2007) Pẽna et al. (2001) Pillitteri et al. (2004a, 2004b) Shalom et al. (2012, 2014) Muñoz-Fambuena et al. (2011, 2012), Shalom et al. (2012) Turktas et al. (2013), Yanik et al. (2013), Fernández-Ocaña et al. (2010) Dündar et al. (2013)

Nakagawa et al. (2012)

increased synthesis of photosynthetic proteins and higher CO2 assimilation, however cannot be excluded (Shalom et al., 2012). Physiological studies on alternate bearing in different mango varieties indicated that leaves of regular bearing mango varieties possessed more number of uniform mesophyll cells highly efficient in CO2 utilization (Singh, 2002). Studies of Singh and Sharma (2008) on the promotive effects of Paclobutrazol on sugar and protein contents can be attributed to its flower regulatory role in mango. During the ‘Off’ years, pistachio trees required low amounts of carbohydrates however, accumulated some starch (Rosecrance et al., 1998). Baninasab and Rahemi (2006) analyzed carbohydrates content in different tissues like flower buds, leaves, fruits, current shoots in pistachio (Pistacia vera L.). Similar amounts of soluble sugars and starch were found in ‘Off’ and ‘On’ trees until 70 days after bloom. Thereafter, in ‘On’ trees, many organs showed decreased amounts of soluble sugars and starch. However, different organs of ‘Off’ trees began to accumulate greater concentration of soluble sugars and starch subsequently, suggestive of emerging sink demands. A significant negative correlation however, was found between bud, leaf and root sucrose, fruit glucose and flower bud abscission signifying source-sink relationships. Thus, soluble sugars played an important role in alternate bearing in pistachio. Moreover, Spann et al. (2008) found carbohydrate storage and mobilization patterns were different in bearing and non-bearing pistachio trees. A similar carbohydrate accumulation pattern is also seen in citrus (Goldschmidt and Golomb, 1982a, 1982b). Ulger et al. (2004) showed the effect of carbohydrates and mineral nutrients on flower bud formation in the olive trees. Additionally, carbohydrates and mineral contents were significantly different in the leaves of both ‘On’ and ‘Off’ year olive trees (Stutte and Martin, 1986; Fernandez-Escobar et al., 1999; Erel et al., 2008). However, Bustan et al. (2011) suggested that the status of carbohydrate reserves in the olive trees is mainly involved in the survival rather than reflecting the alternate bearing tendencies. Further, Yanik et al. (2013) elucidated the role of miRNA regulating the minerals, carbohydrate biosynthesis and transport genes in olive tree. These genes were down regulated during the bearing year of the crop. Therefore, the available data showed that storage of nutrition during

Pandey (1989). Similarly, effects of clonal rootstocks on Hass avocado on alternate bearing has been elucidated by Mickelbart et al. (2007). 2.2. Carbohydrate metabolism It is fairly well recognized now that when a perennial fruit tree produces bumper crops in one season, it gets exhausted nutritionally and fails to put forth new flushes attributable to growth correlations, leading to either less or no yields in the following season. During ‘On’ year’s crop, carbohydrate and nitrogen reserves get depleted and its effect can be seen in the following season’s crop (Singh, 2002). A nutritional concept given by Goldschmidt et al., 1985; Goldschmidt, 1999. This theory explained how the developing fruit provides a strong sink for photo-assimilates and further explains the mechanism of depletion of photo-assimilates, especially carbohydrates from the bud that prevents flower induction. In Arabidopsis, sucrose is shown a key regulator controlling flowering phenomenon (Eriksson et al., 2006). Trehalose metabolic pathway is also shown important to regulate the flowering in Arabidopsis (van Dijken et al., 2004; Wahl et al., 2013). But how these sugars played a regulatory role in flower induction under varying crop loads in perennial fruit trees has not been answered sufficiently for many years (Jones et al., 1974; Goldschmidt and Golomb, 1982a, 1982b; Li et al., 2003). In ‘Off’ year crops, trehalose metabolism associated genes in buds were found up-regulated (Shalom et al., 2012). Majority of leaf nitrogen present mainly in the form of proteins of the photosynthetic machinery (Evans, 1989) appears to play crucial role. Therefore, high rate of photosynthesis seen in ‘Off’ year leaves could evidence the existence of such a mechanism. However, no net changes in photosynthesis between leaves of ‘On’ and ‘Off’ phase crop trees as reported by many authors (Roper et al., 1988; Monerri et al., 2011, Nebauer et al.,2013) need further appraisal. Some findings highlighting increased photosynthetic rate in ‘On’ year as compared to ‘Off’ year phases (Iglesias et al., 2002; Syvertsen et al., 2003; Urban et al., 2004) is suggestive of higher demands of ensuing vegetative phenophase. In the scheme of lower leaf photosynthesis in ‘Off’ year crop trees resulting in reduced flow of photo-assimilates into the bud region, leading to 216

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Table 2 Impact of hormones, carbohydrate metabolism and crop load on alternate bearing in fruit crops. Factors

Fruit Crop

Hormone

Apple Citrus

Mango

Olive

Pistachio

Litchi

Carbohydrate Metabolism

Apple Citrus

Summary

Reference

initiation in apple inhibits by GA. After full bloom application • Floral of cytokinin initiate the flowering. and fruit set in citrus is regulated by phtohormones. • Abscission • Both floral induction and evocation in citrus inhibited by GA. GA pathways play an important role in both biennial • Autonomous bearing and flowering control in mango. study • Hormonal bearing in olive trees affected by seasonal changes in • Alternate endogenous plant hormones. and hormonal control had remarkable impact on the • Nutritional alternate bearing in olive. bearing in olive. • Biennial of alternate bearing intensity. • Evaluation endogenous growth regulators in pistachio (Pistacia vera L.) • Free effect of nitrogen in preventing of alternate-bearing of • Physiological pistachio.

induction in litchi and longan is controlled by • Flower phytohormones. temperature difference also regulate flowering. • Diurnal and non-fruiting apple trees compared by seasonal change • Fruiting in photosynthetic rate. reserves, flower formation and photosynthetic rate • Carbohydrate regulate the alternate bearing in ‘Salustiana’ Sweet Orange (Citrus sinensis L.).

Pistachio

Olive

Dates

metabolic pathway was induced in ‘off’crop buds in citrus • Trehalose and related with alternate bearing. in pistachio is controlled by nutritional factors. • Flowering sugars in the many part of tree could be related to the • Soluble alternate bearing in pistachio. had trivial influence on the flower bud formation. • Carbohydrates mobilization might have an effect on the alternate bearing. • Carbon • Leaf nutrient content have effect on alternate bearing. palm, an off tree could be possibly identified by lower levels • Inof date leaf boron, thus highlighting the role of mineral elements

Harley et al., (1942), Tromp (1982), McLaughlin and Greene (1984), Bertelsen et al. (2002), Schmidt et al. (2010) Shalom et al. (2014) Monselise and Halevy (1964), Goldschmidt et al. (1985), GarciaLuis et al. (1986), Inoue (1989a, 1989b), Ogata et al. (1996), Koshita et al. (1999), Koshita and Takahara (2004) Nakagawa et al (2012) Tongumpai et al. (1991), Nunez-Elisea and Davenport (1998), Blaikie et al. (2004) Fernández-Escobar et al. (1999), Baktir et al. (2004), Ulger et al. (2004), Al-Shdiefat and Qrunfleh (2008) Turktas et al. (2013) Lavee (2007) Esmailpour (2005), Rosenstock et al. (2010) Johnson and Weinbaum (1987), Kallsen et al. (2007) Picchioni et al. (1997), Spann et al. (2008), Vemmos (2010), Okay et al. (2011), Amiri (2009), Todd et al. (2010) Batten and McConchie (1995) Menzel et al. (2000), Ying and Davenport (2004), Hegele et al. (2010) Fujii and Kennedy (1985) Monerri et al. (2011), Goldschmidt (1999), Garcia-Luis et al. (1995, 1998), Goldschmidt and Golomb (1982), Li et al. (2003) Monselise and Goldschmidt (1981) Shalom et al. (2012) Rosecrance et al. (1998) Baninasab and Rahemi (2006) Ulger et al. (2004); Nejad and Niroomand (2007), Bustan et al. (2011). Stutte and Martin (1986), Spann et al. (2008) (Fernández-Escobar et al. (1999); Erel et al. (2008) Pillay et al. (2005)

controlling flowering.

Mango

Crop Load

Citrus

changes in the leaf of bearing and nonbearing trees of • Biochemical some mango (Mangifera indica L.). on changes in carbohydrate metabolism in regular bearing • Studies and “Off” season bearing cultivars of mango during flowering. effect of crop load on bud break influences return bloom in • The alternate bearing ‘Pixie’ Mandarin. load induces changes in global gene expression and in abscisic • Fruit acid (ABA) and indole acetic acid (IAA) homeostasis. of fruit removal on photosynthesis, stomatal conductance and • Effects ABA level in the leaves of vegetative shoots in relation to flowering

Jyothi et al. (2000) Shivu Prasad et al. (2014)

Verreynne and Lovatt (2009), Chao et al. (2011) Shalom et al. (2014) Garcia-Luis et al. (1986), Iwasaki (1959); Okuda et al. (1996). Garcia-Luis et al. (1995), Goldschmidt et al. (1985), MartínezFuentes et al. (2010); Nishikawa et al. (2012)

of satsuma mandarin.

Olive

Avocado

load study • Fruit Inhibition of floral development at the level of gene expression of • putative OeFT, preventing the meristems of lateral buds from

•

becoming determined in all but a small pool of buds on nonbearing shoots of on-crop trees, resulting in few inflorescences, an increased number of lateral vegetative shoots, and significant number of inactive buds. Fruit-load might affect flowering by repressing the expression of PaFT in the leaves and increasedPaFT expression during late autumn leads to flower induction.

the ‘Off’ year is a critical factor for further utilization in the reproductive phenophase in the ensuing year. Importance of root signals in circulation of metabolites, their assimilation partitioning patterns and interplay and interpolation of hormones in regulating flowering phenology in this regard appeared crucial (Ravishankar, 1987).

Sibbett (2000), Dag et al. (2010), (Martín-Vertedor et al. (2011), Fichtner and Lovatt (2013) Yi-Yun (2015).

Ziv et al. (2014)

2.3. Temperature Flower bud dormancy is an additional level of reproductive control in perennial fruit crops (Brunner et al., 2014). Floral transition and flowering happen almost simultaneously in annual plants, however, in perennials, an additional rest phase (i.e., bud dormancy) is also observed. It separated these two processes and enables the buds to survive 217

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flow into the bud that further, inhibits its transition to apical meristem. Moreover, it was shown that removal of fruits from ‘On’ year crop enhanced the return bloom (Shalom et al., 2014). This hypothesises, that if fruit load is more, then it blocks the recognition of flowering inductive signal (s). It prevents the emergence of inflorescence and bud break (Albrigo and Saúco, 2004; Verreynne and Lovatt, 2009). Different stages of flower development and bud break are also influenced by the fruit load in citrus (Verreynne and Lovatt, 2009). Moreover, fruit load had remarkable effects on expression of the key flower regulatory genes like FT, LFY,AP1, TFL, and miR156-regulated SQUAMOSA PROMOTER BINDING (SPL5) in leaves and buds of citrus (Muñoz-Fambuena et al., 2011, 2012; Shalom et al., 2012) as well as in mango and apple (Kotoda et al.,2010; Nakagawa et al., 2012).

in the winter season. Vernalization and chilling requirements is also seen in many annuals and perennials growing in the temperate regions. Actually, for these plants cool environment is required for flowering. Moreover, temperature is the most crucial factor that affects the flowering at different phases starting from flower bud differentiation, anthesis and development of parts of the flower. Cool temperatures are required to induce flowering in several tropical and subtropical perennial fruit trees including mango (Ravishankar et al., 1979; Sukhvibul et al., 1999), lychee, macadamia, avocado, orange and olive (Hackett and Hartmann, 1964) and citrus (Inoue, 1989a, 1989b; Valiente and Albrigo, 2004; Knauer et al., 2011). It is observed that flower induction is seen after bud release during cool environmental conditions in the subtropical trees like lychee, avocado, and macadamia (Olesen, 2005). In perennial fruit trees, suitable conditions are available for floral induction just prior to the shoot initiation (Davenport et al., 2006).Vegetative or generative shoots emergence are dependent on suitable environmental cues. A change in low to high temperature during shoot development in mango leads to the transition of shoots from reproductive to vegetative phase (Davenport, 2010). Flowering potential decreased due to the unusual warm temperatures during early flower bud differentiation. Different phase transition from vegetative (no flowers), to mixed (only flowers and leaves), to generative (leafless with at least one flower) were seen during inductive temperature conditions. Davenport (2007, 2008) showed in mango, temperatures and their duration mainly regulated the development of different types of shoots viz., totally vegetative, totally flowering, mixed panicles, two transition stages (vegetative to flower and flower to vegetative), and chimeral (flowers on one side and leaves on the other). Moreover, temperature can affect the intensity of floral initiation in temperate deciduous fruit trees (Chen and Huang, 2001). It is observed that flower induction is seen after bud release during cool environmental conditions in the subtropical trees like lychee, avocado, and macadamia (Olesen, 2005). It could be therefore, surmised that sufficient cool hours are required for optimal flowering density in perennial fruit crops. Though mango is a well acclimatized crop an otherwise hostile climatic situation can convert an ‘On year' into an ‘Off year' and mango grown under tropical and sub-tropical conditions exhibited different flowering behaviours (Davenport, 2007). Therefore, cool temperature is the main induction factor, which causes stress that is required for fruit bud differentiation (Ravishankar et al., 1979 and Davenport, 2007).The effect of another abiotic stresses like temperature and water on flowering of mango has also been studied by many researchers (Whiley, 1993; Kulkarni, 1991; Núñez-Elisea and Davenport, 1994; Sukhvibul et al., 1999; Davenport, 2003; Yeshitela et al., 2004; Davenport et al., 2006, Ramírez et al.,2010). Similarly, effects of temperature and water supply on flowering of tropical fruit trees are studied by Chaikiattiyos et al. (1994). Flowering and fruit set would be adversely influenced if profuse rains occur with cloudy weather and excessive dew during fruit bud differentiation. Flowering induction is triggered by dry and cool weather along with a day /night temperature around 15–20 °C during the winter season. In citrus, low temperatures during the autumn and winter are a key factor in inducing flowering (Valiente and Albrigo, 2004; Nishikawa et al., 2007, 2012, 2013; Wilkie et al., 2008; Knauer et al., 2011; Muñoz-Fambuena et al., 2011). Further, molecular basis of flowering in response to seasonal cues was studied by Searle and Coupland (2004) and Andrés and Coupland (2012). They explained how genetics of plant is helpful to understand the response due to changes in day length (photoperiod) or winter temperature (vernalization). Further, explained the diverse genetic mechanisms that enable plants to recognize winter, spring and autumn to initiate flower development.

2.5. Phytohormones Flowering time is mainly influenced by important chemical constitutes like plant hormones (Davis, 2009; Domagalska et al., 2010). How hormones influence the plants, mainly governed by three core factors like i) time of release, ii) target tissue susceptibility, and iii) concentration of the hormone. Studying the mechanism of hormones influencing the flowering time and their interactions with the other plant metabolites is useful to infer the bearing phenomenon. Flower induction is prevented by an inhibitory signal due to the presence of the fruits (Bower et al., 1990; Talon et al., 1998). Exogenous application of plant hormones also has an impact on transition to flowering (Ionescu et al., 2016). 2.5.1. Auxin Smith and Samach (2013) studied the function of auxin in inhibition of flowering following an ‘On’ year crop. Basically, this mechanism is based on the ATA hypothesis (Caaejas and Bangerth, 1997; Bangerth, 2006). Bangerth (2006) inferred GA synthesis in the meristem could be due to the presence of auxin that acts as mobile signal signifying that both GA and auxin acted as FI-inhibiting signals. Gibberellin is the primary messenger that induces the formation and mobility of the second messenger auxin. Fruit thinning from ‘On’ year trees inducing the return bloom (Monselise and Goldschmidt, 1981) is attributed to the polar auxin transport through a dominant sink. It acts as a possible mobile signal which affects the flowering (Caaejas and Bangerth, 1997; Smith and Samach, 2013). Application of auxin polar transport inhibitors on flower induction in a number of fruit trees has been well studied (Ito et al., 2001, Blaikie et al.,2004; Bangerth, 2006). Further, ATA hypothesis explains that auxin export from the bud was prevented by the strong polar transport of auxin from the dominant sinks (i.e., the fruit or the seed). It clearly defined that why auxin levels in ‘Off’ buds and in buds following de-fruiting is lower than in ‘On’ buds. Hormone analyses also indicated that auxin levels decreased in these buds as compared to that of ‘On’ crop buds (Shalom et al., 2014). 2.5.2. Gibberellin In many perennial fruit crops, flowering is inhibited by gibberellins (GA) (Goldschmidt and Samach, 2004; Bangerth, 2009; MuñozFambuena et al., 2012 and Goldberg-Moeller et al., 2013). However, it has been shown that GA4 induces flowering in apple during ‘Off’ years (Looney et al., 1985). Indeed, application of GA7 has shown highest inhibitory effect on flower induction in apple (Tromp, 1982). Common horticultural practices and management involving the external application of GA during ‘Off’ years to prevent an excessive FI attenuated the biennial bearing cycle (Schmidt et al., 2010). It is assumed that bioactive GAs has an inhibitory effect on core flowering genes and pathways in apple. Thus, high GA3 levels inhibits the flower induction and various other growth regulators like GA4, ABA and cytokinins, elevated the levels of flower formation in the olive tree (Baktir et al., 2004).

2.4. Fruit load The precise mechanism, how flower induction is influenced by fruit load is still elusive. Presence of fruit produced an inhibitory signal that 218

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et al., 2002; Kotoda and Wada, 2005; Esumi et al., 2005; Kotoda et al., 2006, 2010). Gene synteny studies have shown that orthologues genes of apple like LFY, AFL1, and AFL2 (Wada et al., 2002), as well as MdMADS2 and MdMADS5 and orthologues of the Arabidopsis FUL and AP1, procreated and over expressed during early flowering in heterologous systems (Kotoda et al., 2002). In defiance, up-regulation of the TFL1 orthologue gene of apple, MdTFL1, in Arabidopsis postponed the flowering (Kotoda and Wada, 2005). In addition, Kotoda et al., (2006) observed transgenic Orion apple trees flowered 8 months after grafting due to down-regulation of MdTFL1 gene whereas, non-transformed Orion plants showed much delayed flowering nearly after 5 years of grafting. Branching intensity and spur extinction characters were found coordinated with biennial bearing tendency in apple (Lauri et al., 1995, 1997). Biennial bearing is an apparently genetic trait that is governed both by multigene as well as environmental cues and cultural factors (Guitton et al., 2011). Despite the fact, flowering genes may not directly regulate biennial bearing, their control by phytohormones might be one of the mechanisms leading to biennial bearing tendencies in perennial fruit crops. It has however been observed that MdFT and MdTFL1flowering genes in Malus, are not responsible for biennial bearing (Mimida et al., 2009; Kotoda et al., 2010). However, in biennial bearing mango trees FLOWERING LOCUS T-like and gibberellins metabolism genes were identified by Nakagawa et al. (2012). In disparity, other flowering genes such as MdBFTa, MdSOC1 and MdCOL1 were located within QTL intervals for inflorescence and fruit production mapping on LG1. In recent years, although QTL mapping is widely used it is difficult to determine the exact gene (s) among MdSOC1, MdBFTa, and MdCOL1 as causative for the LG1 QTL.

2.5.3. Abscisic acid The level of abscisic acid (ABA) and its isomer, t-ABA was higher in ‘On’ crop trees in comparison to ‘Off’ crop trees due to the stress imposed by the fruit overload (Jones et al., 1976; Goldschmidt, 1984). In Citrus unshiu bud sprouting and profuse flowering was inhibited by the application of ABA (Garcia-Luis et al., 1986). To the contrary, the possibility that flowering promotes ABA activity has been shown. Therefore, in leaves of ‘Off’ crop trees and following de-fruiting of ‘On’ crop trees have shown the increased ABA levels (Koshita et al., 1999; Okuda, 2000). Direct biochemical evidence showed the complete pathway where NCED3 (Cs5g14370) cleaved 9-cis-violaxanthin to form xanthoxin, a precursor of ABA (Kato et al., 2006). Further, its expression synchronized with ABA levels in the peel during cycles of drought and re-watering of leaves and fruit (Rodrigo et al., 2006, Agustí et al.,2007). Production of ABA is higher in ‘Off’ year than in ‘On’ year olive trees (Al-Shdiefat and Qrunfleh, 2008). In ‘Off’ crop trees, the translocation of ABA into the bud is blocked and it induces the expression of NCDE3 (Baktir et al., 2004). 3. Genomic and transcriptomics approach to study alternate bearing In plants phase transition from vegetative to reproductive is a complex mechanism (Huijser and Schmid, 2011). This leads to explore the regulatory mechanisms to understand the phase transitions. Recently, the development of next generation sequencing (NGS) tool, genomic and transcriptomic has contributed to a thorough understanding of the metabolic and molecular processes involved in floral biology.

3.2. Transcriptome studies 3.1. Flowering genes Gene regulation studies during vegetative to flowering and fruiting transition at transcription and post-translational level is required to understand the ‘On’ and ‘Off” mechanism operating in perennial fruit trees (Khan et al., 2014; Sharma et al., 2015). RNA profiling is required for both types of mRNAs and small regulatory RNAs in order to understand the bearing tendencies in perennial fruit crops (Yanik et al., 2013). Differentially expressed genes (DEGs) utilizing the microarray and RNA sequencing could solve the complex mechanisms that convert ‘On’ into ‘Off’ buds (Sharma et al., 2015). Crucial task of interpretation of the gene expression data is underscored to identify those genes whose patterns of expression are related to a particular phenotype of interest. MicroRNA (miRNA), play an important regulatory role in different physiological processes (Teotia and Tang, 2015). Earlier, miR156 is found in the regulation of flowering time (Wang, 2014). Ozdemir- Ozgenturk et al. (2010) synthesized the cDNA libraries from young olive tree leaves and immature fruits. Further 3,734 arbitrarily sequenced, expressed sequence tags (ESTs) were used to identify and annotate the functions of the genes by homologies to known genes. Donaire et al., 2011 sequenced miRNA from the juvenile and adult shoots to explore the microRNA (miRNA) associated with phase transition in the olive tree. Several miRNA like miR156, miR172 and miR390 were found involved in controlling the developmental transition. Besides that Fernandez-Ocana et al. (2010) have used subtractive cDNA libraries and found a differentially expressed gene (jat) involved in the juvenile-to-adult transition of the olive tree. Turktas et al. (2013) brought out, differential expression of one transcript GO243632_1 during flower development in olive tree. The expression of this transcript was two-folds higher in the ‘Off’ year leaves than that of ‘On’ year ones. Further, 246 differentially expressed genes were found between the ‘On’ and ‘Off’ year leaves, irrespective to their developmental stage. However, only 5.69% genes were functional in hormone regulation. Further, few more genes like genesh4_pg.C_scaffold_ 19987000001, eugene3.00160596, eugene3.00020895, eugene3.00170500 and FL683585_1were significantly expressed in the ‘On’ year leaves than ‘Off’ year ones. Yanik et al. (2013) have identified 135 conserved

Regulatory factors that govern flowering mechanism have been demystified in the annual model plant (Pajoro et al., 2014, Blümel et al.,2015). Likewise, most important core floral development regulatory genes have been identified in model plants, such as Antirrhinum majus and Arabidopsis thaliana (Bernier and Périlleux, 2005; Tan and Swain, 2006; Corbesier et al., 2007). In Arabidopsis, BFT functions like a TFL1and play role in inhibition of inflorescence meristem development (Yoo et al., 2010). In annual plants, SOC1 intensified FI in response to GAs (GA4) (Eriksson et al., 2006). Similarly, CO positively regulates the expression of two floral integrators, LFY and SOC1, via FT in Arabidopsis (Samach et al., 2000; Parcy, 2005). Studies on the flowering time associated genes in perennial fruit crops is scarce due to their long gestation cycle (Arora et al., 2003; Cooke et al., 2012, Abbott et al., 2015). Previous studies undertaken on flowering associated genes; gene expression analyses at different stages of flowering phenophase in perennial fruit crops allow the deciphering of targeted genes and then understand their relationships with reproductive processes. These comprise the flowering promoter gene (Lee et al., 2006) like flowering locus t (FT), that encodes a protein which is a key regulator of florigen (Kobayashi et al., 1999), floral meristem identity determinant genes like leafy (LFY) and apetala1 (AP1) genes (Yanofsky,1995). Besides that few others important genes like flowering locus c (FLC), terminal flower 1 (TFL1), brother of ft (BFT), and short vegetative phase (SVP) are also found. These genes act as repressors in floral pathway (Boss, 2004; Yoo et al., 2010). Flowering locus c (FLC) is a major repressor gene that effectively controls the flowering time. Substantially molecular biological and epigenetic approaches have been used to understand the function of FLC gene. However, regulation of FLC at post-translational level is yet to be inferred (Kwak et al., 2017). Gene synteny approach is widely used to understand the flowering gene functions. A set of apple genes with sequence similarity to genes tangled in floral meristem transition of Arabidopsis has been determined. Further it has been subjected to expression studies (Wada 219

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Fig. 2. Phylogenetic tree represents the evolutionary relationship among gene sequences of different alternate bearing fruit crops.

expression was earlier than the flower induction period (Shalom et al., 2012). Therefore, the mRNA levels of CiFT2 and CiSPL5 were higher in ‘Off’ than in ‘On’ crop buds. However, LFY gene did not show any difference in its expression between buds of ‘On’ and ‘Off’ crop trees. Nonetheless, de-fruiting resulted in a 2-folds increase in its mRNA level. However, it drops to basal level 28 days after treatment. Previously, it was shown that the number of DEGs between ‘On’ and ‘Off’ crop buds was considerably lower in September than in May (Shalom et al., 2012). Shalom et al. (2014) had observed that de-fruiting resulted in relatively prompt changes in global gene expression. Cift (citrus flowering locus T) and Soc1 (suppressor of over expression of constants 1) genes were up-regulated during the ‘Off” year (Muñoz-Fambuena et al., 2011). Haberman et al. (2016) correlated the presence of adjacent fruit with re-accumulation of transcript encoding a potential flowering inhibitor, MdTFL1-2, in BS apices prior to inflorescence initiation. Fruit load and gibberellin (GA) application had similar effects on the expression of

miRNA that are important for alternate bearing processes. In addition, seven main pathways that had a noteworthy impact on the alternate bearing in olive tree were identified. Differential gene expression studies were carried out in various fruit crops for example in leaves of mango few genes viz; FT, AP1 and LFY were up-regulated during the flower induction period. As a principle, the expression of flower control genes in mango is induced in leaves, buds, and stems in coordinate with the onset of the flower induction period (November–December) in regular bearing varieties, and in alternate bearers during the ‘Off’ crop year, while GA treatment decreased their expression (Nishikawa et al., 2007, Muñoz-Fambuena et al.,2011, 2012; Shalom et al., 2012, Goldberg-Moeller et al.,2013). In mango, the availability of the draft genome sequence is expected to greatly assist the candidate gene approach to solve the mystery of alternate bearing at gene level (Singh et al., 2016). In case of citrus CiSPL5 exhibited higher response in buds (May – September) and CiFT2 220

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MdTFL1-2. These results will be implied for cultivar specific approaches to reach sustainable fruit production. Moreover, different experimental approaches have led to a staggering amount of data (Fornara et al., 2010; Prunet and Jack, 2014). This data could be utilized. Recently, Bouché and colleagues provided FLOR-ID, the flowering interactive database to the public domain, which is freely available at www.flor-id.org (Bouché et al., 2016). Interestingly, FLOR-ID is a simple and effective tool (UniProt, www. uniprot.org) and PubMed (www.ncbi.nlm.nik.gov/pubmed) database finder combined with information taken from other sources (Wellmer, 2017). Furthermore, orthologs and coorthologus detection was done to study the evolutionary relationship between alternate bearing genes of different fruit plant species like avocado, litchi, apple, mango, olive, pistacia, prunus etc. A total of 1282 nucleotide sequences were compared with all-against-all BLASTP utilizing the data from NCBI (ESM1) and phylogenetic tree (Fig. 2) was constructed using Mega (version 7.0, https://www.megasoftware.net) Kumar et al., 2016. OrthoMCL (http:// orthomcl.org/orthomcl/) detected 351 coorthologs (avocado: 13, litchi: 96, apple: 278, mango: 112, prunus: 183 and remaining in others species) and 362 orthologs (avocado: 8, litchi: 16, apple: 318, mango: 14, pistacia: 17, prunus: 319 and remaining in other plant species) within the eleven plant species utilizing the data from NCBI (ESM 2). Coorthologus and orthologus gene statistics have shown in Figs. 3 and 4, respectively. Moreover, status of the flowering gene is given in Table 3.

Fig. 4. Orthologs venn diagram among five major alternate bearing fruit species. Table 3 Current status of sequence information in NCBI database (2017) related to flowering gene in alternate bearing fruit crops.

4. Conclusions

NCBI database

Molecular mechanisms governing the flowering behavior has been sufficiently elucidated in model plants. A thorough understanding of the physiological and molecular basis of bearing tendencies in perennial fruit crops is useful to understand the mechanism of flower development process and regulatory elements which are responsible for differential expression. Further, this information will be helpful in selection of suitable recombinants and hybrids in early nursery stage itself overcoming the problem of long gestation periods and other economic constraints. A number of studies in perennial fruit crops systems signify prominent role of root signals /root dynamism in bringing out wide range of morphogenetic responses as influenced by environmental and cultural events which however, need to be further elucidated especially in light of up and down-regulation of genes in relation to switching on

S. No. 1 2 3 4 5 6 7 8

Fruit crop Avocado (Persea Americana) Citrus (Citrus spp.) Prunus (Prunus spp.) Pistachio (Pistacia vera) Litchi (Litchi chinensis) Mango (Mangifera indica L.) Olive (Olea europaea) Apple (Malus x domestica Borkh.)

Nucleotides 3 – 1059 1 6 82 16 126

Gene – 19 40 – – – – 45

EST – 323 – – – – – –

and off mechanisms at the onset of specific phenological cues in perennial fruit tree systems. Differential gene expression studies during different phenophase may provide a clear understanding of the complex phenomenon of alternate bearing in perennial fruit crops. The exact environmental cues and the positive and negative regulatory genes however, still elude identification in perennial fruit plants like mango. Systematic studies on computational biology and genomics could hold key options to regulate the function of key genes/proteins associated in alternate bearing mechanism in perennial fruit crops by identifying interactive factors.

Funding This work was supported by Department of Science and TechnologySERB, New Delhi, India [grant numbers YSS/2015/001302].

Declarations of interest None.

Acknowledgements Authors are thankful to Director ICAR-IARI, New Delhi for research facilities.

Fig. 3. Coorthologus flowering gene statistics in different alternate bearing fruit crops. 221

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Appendix A. Supplementary data

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