Fifty Years of Citrus Developmental Research: A Perspective

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  • 1 Institute of Plant Sciences and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel

An overview of the conceptual and methodological changes in citrus developmental research during the past half century is provided. Beginning with the hormonal era, the extensive use of plant growth regulators (PGRs) is described and the presumed role of gibberellins in various stages of the reproductive processes is emphasized. Introduction of the source-sink concept opened the way for alternative, carbohydrate-mediated explanations of productivity and alternate bearing. The potential role of ethylene in citrus abscission and fruit ripening is reviewed. The recent adoption of genetic–molecular approaches paves the way for deeper understanding of citrus developmental enigmas.

Abstract

An overview of the conceptual and methodological changes in citrus developmental research during the past half century is provided. Beginning with the hormonal era, the extensive use of plant growth regulators (PGRs) is described and the presumed role of gibberellins in various stages of the reproductive processes is emphasized. Introduction of the source-sink concept opened the way for alternative, carbohydrate-mediated explanations of productivity and alternate bearing. The potential role of ethylene in citrus abscission and fruit ripening is reviewed. The recent adoption of genetic–molecular approaches paves the way for deeper understanding of citrus developmental enigmas.

For a long time, morphological observations, microscopes, and simple chemical analyses were fruit tree researchers’ major tools. However, then, toward the middle of the 20th century, horticulturists were enchanted by the plant hormone concept. The hormonal thinking dominated citrus developmental physiology for a long time; rooting, vegetative growth, flowering, fruit development, ripening, and abscission were all attributed to one specific plant hormone or to the perplexing “hormonal balance” concept. Synthetic growth regulators were exploited in every possible way to solve practical problems. The emergence of the source-sink concept (≈1980) partially replaced the hormonal hypothesis. The source-sink hypothesis claims that carbohydrate levels control the major stages of the fruiting process—flowering, fruit set, and fruit enlargement—and are, therefore, responsible also for the “alternate bearing” syndrome. Although the effects of girdling and fruit thinning seem to support the source-sink concept, direct control of flowering and fruit set by carbohydrate levels has not been unequivocally demonstrated. However, then, rather soon, came the molecular–genetic era, forcing us all to acquire a new language and follow its logic. We can now identify the genes responsible for developmental phenomena. Citrus research is still a few steps behind Arabidopsis but here we are, still doing our best to solve the remaining mysteries of citrus.

The purpose of the present article is to provide an overview of the conceptual changes that took place in the area of Citrus developmental physiology during the recent half century or so and highlight major achievements. Corresponding changes must have taken place in other fruit tree crops. In the background of this specific area are the far-reaching developments in biological theory and, of no lesser significance, the emergence of new techniques and methodologies. While plant physiological research gradually adopted the new experimental tools, the acquisition of new methodologies by horticulturists was a slow, painstaking process. A schematic illustration of these conceptual changes is provided in Figure 1. Please note that the “source-sink” concept “invades” the scenery but does not fully replace the “hormonal paradigm.” The elliptic “genetic–molecular era” is wider than the circle of the “hormonal paradigm,” indicating its broader biological significance.

Fig. 1.
Fig. 1.

Conceptual trends during the recent 50 years of citrus developmental research.

Citation: HortScience horts 48, 7; 10.21273/HORTSCI.48.7.820

The Hormonal Era

The dawn of this half century period roughly coincides with the emergence of the “hormonal paradigm,” which appeared to provide an explanation for all plant developmental phenomena. The hormonal concept, which had been developed with a few model systems (Avena coleoptiles, pea seedlings), was rapidly adopted by horticulturists. It is quite amazing that although so little was actually known about plant hormones, the hormonal theory became so dominant, pushing aside alternative explanations such as nutritional carbon/nitrogen ratios (Zheng, 2009). The introduction of synthetic PGRs opened the way for a multitude of horticultural treatments in an attempt to solve every developmental problem and cure every physiological disorder. The implementation of PGRs in citriculture began very soon after the adoption of the hormonal paradigm. In fact, the American physiologist W.C. Cooper was the first to demonstrate that treating woody cuttings with a synthetic auxin promoted root formation; these early experiments with lemon cuttings (Cooper, 1935) initiated the use of synthetic auxins as universal rooting agents. The pioneering work of C.W. Coggins, Jr., and his team in California laid the foundation of a range of still prevailing citrus pre- and post-harvest PGR treatments (Coggins and Hield, 1968; Lovatt, 2012).

The review of El-Otmani et al. (2000), although not completely up to date, demonstrates the extensive, worldwide use of PGRs in citriculture. It also contains references to a large number of experimental field studies conducted in Israel, Spain, the United States, Brazil, Japan, and elsewhere to define the specific chemicals, concentrations, and conditions for optimal orchard treatments. Figure 2 summarizes major, most commonly used PGR treatments along the sequence of the fruiting process. Synthetic auxins, gibberellic acid (GA), and ethylene (or ethephon) are the most frequently used orchard and packing house PGRs. GA antagonists, in particular paclobutrazole, have been used experimentally (Greenberg et al., 1993; Harty and van Staden, 1988) but are not currently in commercial use. Cytokinins have been used mainly in tissue culture operations. Abscisic acid and the more recent members of the plant hormone club have not yet become part of the regular orchard management systems.

Fig. 2.
Fig. 2.

Major plant growth regulators (PGRs) treatments during stages of citrus fruiting processes.

Citation: HortScience horts 48, 7; 10.21273/HORTSCI.48.7.820

The Productivity Complex

It is not easy to distinguish among the physiological problems of flowering, fruit set, and tree productivity because they are so closely intertwined. Flowering of Citrus is a subbranch of the general flower induction enigma. The work of Monselise and Halevy (1964) was one of the first to show that GA inhibited the flowering of citrus, whereas GA antagonists promoted it (Monselise et al., 1966). Gibberellins were assumed therefore to play an inhibitory role in the natural regulation of citrus flowering; the environmental cues, drought and cool temperatures, presumably interfere with the biosynthesis of gibberellins, thereby enabling the formation of flower buds (Goldschmidt and Monselise, 1972; Monselise, 1985).

Closely related to the regulation of flowering is the shoot type/inflorescence phenology. Following various attempts to define citrus shoot types (Lenz, 1966; Sauer, 1951), the distinction among the three shoot types—vegetative, mixed-type, and reproductive (Goldschmidt and Monselise, 1972)—became widely accepted. GA and GA antagonists can modify the shoot type distribution toward the vegetative or the reproductive end, respectively (Goldschmidt and Monselise, 1972; Greenberg et al., 1993). Furthermore, fruit set follow-ups invariably showed that most fruit are borne on mixed-type inflorescences, suggesting a role (nutritional, hormonal, or water transport; Erner et al., 2000) for inflorescence leaves in the fruit set process (Moss et al., 1972). Initial set was found to be high on leafless inflorescences (especially after fall girdling; Erner, 1988), but during the subsequent fruit drop period, the proportion of fruit on leafless inflorescences decreased in favor of the mixed-type inflorescences (Goldschmidt and Monselise, 1977). The importance of GA became evident also in another reproductive event. Quite early, Soost and Burnett (1961) showed that GA could replace the pollinator trees in ‘Clementine’ orchards, opening the way for the current use of GA as an inducer of parthenocarpic, seedless fruit in numerous Citrus reticulata cultivars (El-Otmani et al., 2000). A more general, as yet insufficiently resolved problem is alternate bearing, which is widespread among mandarins and their hybrids (Monselise and Goldschmidt, 1982).

It might be appropriate to point out that notwithstanding the impressive progress in citrus developmental physiology, there are a few neglected areas where too little has been accomplished. Citrus root systems and the regulation of their development is one striking example (Bevington and Castle, 1985; Kosola and Eisenstat, 1994). The early differentiation of citrus fruits' unique internal tissues, juice vesicles in particular, is another little explored case.

Source-sink Regulation of Developmental Events

It is difficult to pinpoint the emergence of the source-sink hypothesis of plant development (deWitt, 1986; Wareing and Patrick, 1975). The concept that was initially applied to annual crops became very soon popular with horticultural crops, including citrus. The source-sink hypothesis claims that carbohydrate levels control the major stages of tree fruiting—flowering, fruit set, and fruit enlargement. Although the hypothesis initially emphasized quantitative supply of photosynthate, the more recent feast/famine version (Koch, 1996) takes into account specific sugar/gene regulation cascades (Li et al., 2003a, 2003b). The rapidly spreading source-sink concept seemed to replace, or at least complement, the hormonal explanation of developmental processes.

Although the importance of photosynthate supply (= dry matter, energy) for all plant life processes is obvious, its role as a limiting factor for developmental events needs to be unequivocally demonstrated. Two most common horticultural practices were considered in this context, girdling and fruit thinning. Girdling invariably brings about accumulation of carbohydrates above the girdle (Goren et al., 2004). Fall girdling of citrus trees promoted flowering, elevated the percentage of leafy inflorescences (Garcia-Luis et al., 1995; Goldschmidt et al., 1985), and increased the number of fruit per tree, resulting in higher yields (Erner, 1988). This evidence suggests that the promotion of flowering was brought about by the girdling-induced upsurge of carbohydrates. However, according to Erner (1988), Garcia-Luis et al. (1995), and Monerri et al. (2011), this kind of correlative evidence is not sufficiently convincing; girdling might have other, perhaps hormonal effects on flowering. The role of carbohydrates in fruit set is also controversial; carbohydrate supply might be the limiting factor in some cases but not in others (Garcia-Luis et al., 1988; Goldschmidt, 1999).

Fruit thinning reduces the number of fruit per unit leaf area per tree, thereby enabling each fruit to increase its size, presumably as a result of improved supply of photosynthate. The intensity of fruit thinning is negatively correlated with fruit size (Goldschmidt and Monselise, 1977). Thus, fruit enlargement is most closely dependent on the supply of photosynthate (Goldschmidt, 1999). Most orange and grapefruit cultivars have an effective self-thinning mechanism that adjusts the number of remaining fruit to a tree’s fruit bearing potential. The natural thinning mechanism, i.e., fruitlet abscission, appears to be induced by a shortage of carbohydrates (Garcia-Luis et al., 1988; Mehouachi et al., 1995).

As already mentioned, alternate bearing is common in mandarins and mandarin hybrid cultivars. In extreme cases, trees collapse after a heavy crop (“on”) year; this collapse is clearly associated with severe depletion of carbohydrate reserves, particularly in roots (Goldschmidt and Golomb, 1982; Smith, 1976). Carbohydrates seem therefore to play a role in the alternate bearing syndrome (Li et al., 2003a; Monselise and Goldschmidt, 1982), but other nutritional and hormonal factors are certainly involved.

The source-sink hypothesis of citrus productivity is schematically presented in Figure 3. Carbohydrate levels seem to play a role in floral induction, fruit set, fruitlet abscission, and fruit enlargement but they are not the sole factor and direct evidence for their involvement in some of these stages is still missing. The interplay of plant hormones and carbohydrates, in particular, requires further study. There is a general understanding that plant hormones and source-sink mechanisms must interact in the execution of plant performance. However, how this is accomplished is still debatable (Baker, 2000; Peleg et al., 2011; Wardlaw and Moncur, 1976).

Fig. 3.
Fig. 3.

The source-sink hypothesis: annual course of carbohydrate levels in high crop (“on”) and low crop (“off”) citrus trees. Based on data of mandarin cultivars (Goldschmidt and Golomb, 1982; Li et al., 2003b).

Citation: HortScience horts 48, 7; 10.21273/HORTSCI.48.7.820

Abscission, Ripening, and Senescence

Although the previous section had GA as its hormone champion, ethylene is the major player, although not the only one, in the present section. Ethylene has been used as a citrus and banana degreening agent since the 1920s but its general function as a plant hormone was discovered much later. Abscission of plant organs is a natural process, regulated by a complex interaction between auxin that delays abscission and ethylene that promotes it (Taiz and Zeiger, 1998). In citriculture we need means to regulate abscission in both opposite directions; the natural shedding of young fruitlets must sometimes be amplified (= fruit thinning) but excessive fruit drop may cause up to total loss of the crop. With mature fruit too, there is a need to prevent preharvest drop, for which 2,4-D is commonly used (El-Otmani et al., 2000) but, on the other hand, we want to “loosen” the fruit to facilitate mechanical harvesting. Following the early work of Addicott et al. (1949) who developed the citrus explant system, Goren and coworkers conducted thorough physiological studies of citrus leaf and fruitlet abscission, elucidating the anatomical, hormonal, and enzymatic aspects of the process (Goren, 1993). A unique event is the abscission of the style, which occurs in all citrus fruits shortly after fruit set, except for certain cultivars of citron (Citrus medica L.). The synthetic auxin, Picloram (4-amino-3,5,6-trichloro-picolinic acid), prevents style abscission (Goldschmidt and Leshem, 1971), a treatment used in Israel to ensure the persistence of the style in citron fruits used for the feast of Tabernacles (Nicolosi et al., 2005). A tremendous amount of work was invested in the calibration and fine-tuning of fruit thinning treatments for each cultivar and growth area. Various synthetic auxins that bring about evolution of ethylene are most commonly used (El-Otmani et al., 2000). Synthetic auxins are also used to increase fruit size in C. reticulata hybrid cultivars. Such treatments must be applied within a narrow time window, when the fruit thinning capacity has already faded away but the fruit is still growth-responsive to exogenous, synthetic auxins. Endless efforts have been invested, mainly in Florida, in screening and adoption of fruit-loosening chemicals. Recent research by Burns and coworkers has focused on CMNP (5-chloro-3-methyl-4-nitro-1H-pyrazole) as a promising fruit-loosening agent (Alferez et al., 2007). High concentrations of 2,4-D are applied in the packing house, often together with GA, to avoid loss of the calyx (which is also an abscission process), maintain rind firmness, and reduce postharvest decay (El-Otmani et al., 2000).

Citrus fruits have a unique pattern of ripening, often called “maturation” (Spiegel-Roy and Goldschmidt, 1996). According to classic definitions citrus, fruits are “non-climacteric,” revealing a slow decline in respiration and a gradual increase in sugar/acid ratio, not promoted by ethylene. On the other hand, the degreening response to exogenous ethylene suggests that ethylene is somehow involved in the maturation process. Evidence accumulated during the last decades (Aharoni, 1968; Goldschmidt et al., 1993; Katz et al., 2004) enforces the view that the extremely low amounts of endogenous ethylene evolved by citrus fruits have nonetheless a significant physiological role in fruit maturation. This conclusion is in line with a recent review that questions the classic distinction between climacteric and non-climacteric fruits (Paul et al., 2012).

During citrus fruit maturation, rind and pulp behave in most respects as separate entities (Iglesias et al., 2007; Monselise, 1977). The flavedo, which was up to now a green photosynthetic tissue, undergoes senescence; the chlorophyll is degraded and the chloroplasts are transformed into carotenoid-rich chromoplasts. This is a partially reversible environmentally, nutritionally, and hormonally controlled process (Goldschmidt, 1988), which involves ethylene-induced upregulation of chlorophyllase (Azoulay-Shemer et al., 2008) and carotenoid build-up as well as other molecular events. These changes are reversed by the senescence antagonists GA and cytokinins; such an antagonism was also demonstrated with other fruits (Goldschmidt et al., 1977).The degreening–regreening events of citrus fruit peel and the regulatory systems involved are illustrated in Figure 4. Maturation of the pulp, on the other hand, consists primarily of the developmentally regulated decline in acid and accumulation of sugars, processes that are barely affected by ethylene or other PGRs and are still insufficiently understood (Katz et al., 2011). The profound difference between peel and pulp can best be demonstrated by the differential regulation of the same biochemical process: carotenoid biosynthesis. Ethylene has a dramatic effect on peel carotenoid biosynthesis (Rodrigo and Zacarias, 2007) but its effect on pulp carotenoids is negligible (Matsumoto et al., 2009). Also, peel and pulp carotene genesis respond differently to temperature regimes (Tao et al., 2012).

Fig. 4.
Fig. 4.

Citrus fruit peel degreening and regreening: Chloroplast–chromoplast transformations and the relevant regulatory systems.

Citation: HortScience horts 48, 7; 10.21273/HORTSCI.48.7.820

Both acceleration of peel coloration by ethylene and delay of peel senescence by GA are used extensively in citriculture, pre- and post-harvest (El-Otmani et al., 2000). GA also reduces albedo apoptosis phenomena such as creasing (Embleton et al., 1973; Monselise et al., 1976). Synthetic auxins reduce creasing as well (Greenberg et al., 2006).

The Genetic–molecular Era

Establishing a causal relationship between an endogenous hormonal factor and a presumably related morphological or physiological process proved to be difficult since the early years of the hormonal era (Jacobs, 1959) and became increasingly so with the expanding list of plant hormones and their interactions. Indirect, correlative evidence was the most one could attain in physiological experiments. One type of evidence required according to Jacobs (1959) was called “excision”—“Remove the source of the chemical and demonstrate subsequent absence of formation of the structure… The chemical is sometimes removed by selecting genetic mutants.” Indeed, mutants became eventually a major tool in plant hormone studies; gibberellin research, in particular, was based from the outset on mutants, which enabled the deciphering of gibberellins’ biosynthetic pathway and physiological activity (Ross et al., 1997). With the growing consent that all plant developmental events are genetically programmed, there was but a short step from the use of mutants in physiological studies to their implementation in molecular–genetic studies. Furthermore, genetic engineering techniques enabled the design of new types of mutants, which became indispensable for deeper, direct understanding of the underlying developmental and metabolic mechanisms. The main drawback from the point of view of a citrus physiologist was that most if not all of this impressive progress has been achieved with model plants, primarily Arabidopsis.

Although the biological principles were formulated during the 1960s, it took a long time until the genetic–molecular language was adopted by plant scientists and even longer until the molecular approaches were applied to crop plants. Fruit trees, including citrus, were probably the last to enter the molecular era; heterozygosity, scarcity of point mutations, difficulties in transformation, and lack of genetic maps delayed and restricted progress in this field of research. Yet, during the last decade or so, there has been an increasing number of studies aimed at elucidation of the distinct molecular basis for citrus developmental phenomena; flowering, fruit set, alternate bearing, fruit maturation, pigment changes, and flavonoid biosynthesis are all currently under molecular scrutiny. Some progress has been achieved using peel color mutants (Alos et al., 2008). Transformed citrus plants revealed reduced juvenility (Pena et al., 2001) and transgenic plants were used to demonstrate the role of gibberellins in citrus stem elongation, similarly to that previously shown in model plants (Fagoaga et al., 2007). The molecular evolution of citrus carotenoids (Alquezar et al., 2009) and flavonoids (Frydman et al., 2013) has been elucidated in detail; these are just a few examples. The recent deciphering of most if not all of the citrus genome (Talon and Gmitter, 2008) provides the basis for more advanced molecular studies of citrus development in the near future. Extensive review of this research is beyond the scope of the present article. It must be realized, however, that current molecular–genetic research does not negate the earlier physiological work. Rather, the genetic evidence is imposed on top of the hormonal findings, providing them with explicit molecular explanations. As an example, the long known inhibition of citrus flowering by GA is still valid, but now a molecular explanation of this phenomenon can be sought (Albrigo and Chica, 2012; Goldberg-Moeller et al., 2013). Thus, past, present, and future citrus research efforts form a continuum, reflecting the endless human quest for knowledge and comprehension.

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  • Monerri, C., Fortunato-Almeida, A., Molina, R.V., Nebauer, S.G., Garcia-Luis, A. & Guardiola, J.L. 2011 Relation of carbohydrate reserves with the forthcoming crop, flower formation and photosynthetic rate, in the alternate bearing ‘Salutiana’ sweet orange (Citrus sinensis L.) Sci. Hort. 129 71 78

    • Search Google Scholar
    • Export Citation
  • Monselise, S.P. 1977 Citrus fruit development: Endogenous systems and external regulation Proc. Intl. Soc. Citriculture 2 664 668

  • Monselise, S.P. 1985 Citrus, p. 275–294. In: Halevy, A.H. (ed.). Handbook of flowering. Vol. 2. CRC Press, Boca Raton, FL

  • Monselise, S.P. & Goldschmidt, E.E. 1982 Alternate bearing in fruit trees. A review Hort. Rev. 4 128 173

  • Monselise, S.P., Goren, R. & Halevy, A.H. 1966 Effects of B-nine, Cycocel and benzothiazoleoxyacetate on flower bud induction of lemon trees Proc. Amer. Soc. Hort. Sci. 89 195 200

    • Search Google Scholar
    • Export Citation
  • Monselise, S.P. & Halevy, A.H. 1964 Chemical inhibition and promotion of citrus flower bud induction Proc. Amer. Soc. Hort. Sci. 84 141 146

  • Monselise, S.P., Weiser, M., Shafir, N., Goren, R. & Goldschmidt, E.E. 1976 Creasing of orange peel—Physiology and control J. Hort. Sci. 51 341 351

  • Moss, G.I., Steer, B.T. & Kriedemann, P.E. 1972 The regulatory role of inflorescence leaves in fruit setting of sweet orange (Citrus sinensis) Physiol. Plant. 27 432 438

    • Search Google Scholar
    • Export Citation
  • Nicolosi, E., La Malfa, S., El-Otmani, M., Negbi, M. & Goldschmidt, E.E. 2005 The search for the authentic citron (Citrus medica L.): Historic and genetic analysis HortScience 40 1963 1968

    • Search Google Scholar
    • Export Citation
  • Paul, V., Pandey, R. & Srivastava, G.C. 2012 The fading distinctions between classical patterns of ripening in climacteric and non-climacteric fruit and the ubiquity of ethylene—An overview J. Food Sci. Technol. 49 1 21

    • Search Google Scholar
    • Export Citation
  • Peleg, Z., Reguera, M., Tumimbang, E., Walia, H. & Blumwald, E. 2011 Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress Plant Biotechnol. J. 9 747 758

    • Search Google Scholar
    • Export Citation
  • Pena, L., Martin-Trillo, M., Juarez, J., Pina, J.A., Navarro, L. & Martinez-Zapater, J.M. 2001 Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time Nat. Biotechnol. 19 263 267

    • Search Google Scholar
    • Export Citation
  • Rodrigo, M.J. & Zacarias, L. 2007 Effect of postharvest ethylene treatment on carotenoid accumulation and the expression of carotenoid biosynthetic genes in the flavedo of orange (Citrus sinensis L. Osbeck) fruit Postharvest Biol. Technol. 43 14 22

    • Search Google Scholar
    • Export Citation
  • Ross, J.J., Murfet, I.C. & Reid, J.B. 1997 Gibberellin mutants Physiol. Plant. 100 550 560

  • Sauer, M.R. 1951 Growth of orange shoots Austral. J. Agr. Res. 2 105 117

  • Smith, P. 1976 Collapse of ‘Murcott’ tangerine trees J. Amer. Soc. Hort. Sci. 101 23 25

  • Soost, R.K. & Burnett, R.H. 1961 Effects of gibberellin on yield and fruit characteristics of Clementine mandarin Proc. Amer. Soc. Hort. Sci. 77 194 201

    • Search Google Scholar
    • Export Citation
  • Spiegel-Roy, P. & Goldschmidt, E.E. 1996 The biology of citrus. Cambridge University Press, Cambridge, UK

  • Taiz, L. & Zeiger, E. 1998 Plant physiology. 2nd Ed. Sinauer Associates, Inc., Sunderland, MA

  • Talon, M. & Gmitter, F.G. Jr 2008 Citrus genomics Intl. J. Plant Genomics, Article ID 528361, 17 pages. DOI:10.1155/2008/528361

  • Tao, N., Wang, C., Xu, J. & Cheng, Y. 2012 Carotenoid accumulation in postharvest ‘Cara Cara’ navel orange (Citrus sinensis Osbeck) fruits stored at different temperatures was transcriptionally regulated in a tissue-dependent manner Plant Cell Rpt. 31 1667 1676

    • Search Google Scholar
    • Export Citation
  • Wardlaw, I.F. & Moncur, L. 1976 Source, sink and hormonal control of translocation in wheat Planta 128 93 100

  • Wareing, P.F. & Patrick, J. 1975 Source-sink relations and the partition of assimilate, p. 481–499. In: Cooper, J.P. (ed.). Photosynthesis and productivity in different environments. Cambridge University Press, Cambridge, U.K

  • Zheng, Z-L. 2009 Carbon and nitrogen nutrient balance signaling in plants Plant Signal. Behav. 4 584 591

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Contributor Notes

Thanks are due to Prof. Raffi Goren and Prof. Carol J. Lovatt for valuable comments on early versions of the article. The Editor-in-Chief and the reviewers are acknowledged for their help in improving and refining the manuscript.

To whom reprint requests should be addressed; e-mail eli.goldsmit@mail.huji.ac.il.

  • View in gallery

    Conceptual trends during the recent 50 years of citrus developmental research.

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    Major plant growth regulators (PGRs) treatments during stages of citrus fruiting processes.

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    The source-sink hypothesis: annual course of carbohydrate levels in high crop (“on”) and low crop (“off”) citrus trees. Based on data of mandarin cultivars (Goldschmidt and Golomb, 1982; Li et al., 2003b).

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    Citrus fruit peel degreening and regreening: Chloroplast–chromoplast transformations and the relevant regulatory systems.

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  • Monerri, C., Fortunato-Almeida, A., Molina, R.V., Nebauer, S.G., Garcia-Luis, A. & Guardiola, J.L. 2011 Relation of carbohydrate reserves with the forthcoming crop, flower formation and photosynthetic rate, in the alternate bearing ‘Salutiana’ sweet orange (Citrus sinensis L.) Sci. Hort. 129 71 78

    • Search Google Scholar
    • Export Citation
  • Monselise, S.P. 1977 Citrus fruit development: Endogenous systems and external regulation Proc. Intl. Soc. Citriculture 2 664 668

  • Monselise, S.P. 1985 Citrus, p. 275–294. In: Halevy, A.H. (ed.). Handbook of flowering. Vol. 2. CRC Press, Boca Raton, FL

  • Monselise, S.P. & Goldschmidt, E.E. 1982 Alternate bearing in fruit trees. A review Hort. Rev. 4 128 173

  • Monselise, S.P., Goren, R. & Halevy, A.H. 1966 Effects of B-nine, Cycocel and benzothiazoleoxyacetate on flower bud induction of lemon trees Proc. Amer. Soc. Hort. Sci. 89 195 200

    • Search Google Scholar
    • Export Citation
  • Monselise, S.P. & Halevy, A.H. 1964 Chemical inhibition and promotion of citrus flower bud induction Proc. Amer. Soc. Hort. Sci. 84 141 146

  • Monselise, S.P., Weiser, M., Shafir, N., Goren, R. & Goldschmidt, E.E. 1976 Creasing of orange peel—Physiology and control J. Hort. Sci. 51 341 351

  • Moss, G.I., Steer, B.T. & Kriedemann, P.E. 1972 The regulatory role of inflorescence leaves in fruit setting of sweet orange (Citrus sinensis) Physiol. Plant. 27 432 438

    • Search Google Scholar
    • Export Citation
  • Nicolosi, E., La Malfa, S., El-Otmani, M., Negbi, M. & Goldschmidt, E.E. 2005 The search for the authentic citron (Citrus medica L.): Historic and genetic analysis HortScience 40 1963 1968

    • Search Google Scholar
    • Export Citation
  • Paul, V., Pandey, R. & Srivastava, G.C. 2012 The fading distinctions between classical patterns of ripening in climacteric and non-climacteric fruit and the ubiquity of ethylene—An overview J. Food Sci. Technol. 49 1 21

    • Search Google Scholar
    • Export Citation
  • Peleg, Z., Reguera, M., Tumimbang, E., Walia, H. & Blumwald, E. 2011 Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress Plant Biotechnol. J. 9 747 758

    • Search Google Scholar
    • Export Citation
  • Pena, L., Martin-Trillo, M., Juarez, J., Pina, J.A., Navarro, L. & Martinez-Zapater, J.M. 2001 Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time Nat. Biotechnol. 19 263 267

    • Search Google Scholar
    • Export Citation
  • Rodrigo, M.J. & Zacarias, L. 2007 Effect of postharvest ethylene treatment on carotenoid accumulation and the expression of carotenoid biosynthetic genes in the flavedo of orange (Citrus sinensis L. Osbeck) fruit Postharvest Biol. Technol. 43 14 22

    • Search Google Scholar
    • Export Citation
  • Ross, J.J., Murfet, I.C. & Reid, J.B. 1997 Gibberellin mutants Physiol. Plant. 100 550 560

  • Sauer, M.R. 1951 Growth of orange shoots Austral. J. Agr. Res. 2 105 117

  • Smith, P. 1976 Collapse of ‘Murcott’ tangerine trees J. Amer. Soc. Hort. Sci. 101 23 25

  • Soost, R.K. & Burnett, R.H. 1961 Effects of gibberellin on yield and fruit characteristics of Clementine mandarin Proc. Amer. Soc. Hort. Sci. 77 194 201

    • Search Google Scholar
    • Export Citation
  • Spiegel-Roy, P. & Goldschmidt, E.E. 1996 The biology of citrus. Cambridge University Press, Cambridge, UK

  • Taiz, L. & Zeiger, E. 1998 Plant physiology. 2nd Ed. Sinauer Associates, Inc., Sunderland, MA

  • Talon, M. & Gmitter, F.G. Jr 2008 Citrus genomics Intl. J. Plant Genomics, Article ID 528361, 17 pages. DOI:10.1155/2008/528361

  • Tao, N., Wang, C., Xu, J. & Cheng, Y. 2012 Carotenoid accumulation in postharvest ‘Cara Cara’ navel orange (Citrus sinensis Osbeck) fruits stored at different temperatures was transcriptionally regulated in a tissue-dependent manner Plant Cell Rpt. 31 1667 1676

    • Search Google Scholar
    • Export Citation
  • Wardlaw, I.F. & Moncur, L. 1976 Source, sink and hormonal control of translocation in wheat Planta 128 93 100

  • Wareing, P.F. & Patrick, J. 1975 Source-sink relations and the partition of assimilate, p. 481–499. In: Cooper, J.P. (ed.). Photosynthesis and productivity in different environments. Cambridge University Press, Cambridge, U.K

  • Zheng, Z-L. 2009 Carbon and nitrogen nutrient balance signaling in plants Plant Signal. Behav. 4 584 591

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