Physiology of citrus fruiting - SciELO

1 Braz. J. Plant Physiol., 19(4):333-362, 2007 REVIEWP hysiology of citrus fruitingDomingo J. Iglesias, Manuel Cerc s, Jos M. Colmenero-Flores, Miguel A. Naranjo, GabinoR os, Esther Carrera, Omar Ruiz-Rivero, Ignacio Lliso, Raphael Morillon1, Francisco R. Tadeoand Manuel Talon*Centro de Gen mica, Instituto Valenciano de Investigaciones Agrarias, Apdo. Oficial, 46113 Moncada, Valencia, de Coop ration Internationale en Recherche Agronomique pour le D velopement (CIRAD), SanGiuliano (Corse), F-20230, France. *Corresponding author: 31 October 2007; Accepted: 02 November 2007 citrus is the main fruit tree crop in the world and therefore has a tremendous economical, social and cultural impact in oursociety. In recent years, our knowledge on plant reproductive biology has increased considerably mostly because of thework developed in model plants. However, the information generated in these species cannot always be applied tocitrus, predominantly because citrus is a perennial tree crop that exhibits a very peculiar and unusual reproductivebiology.

2 Regulation of fruit growth and development in citrus is an intricate phenomenon depending upon many internaland external factors that may operate both sequentially and simultaneously. The elements and mechanisms wherebyendogenous and environmental stimuli affect fruit growth are being interpreted and this knowledge may help to providetools that allow optimizing production and fruit with enhanced nutritional value, the ultimate goal of the citrus article will review the progress that has taken place in the Physiology of citrus fruiting during recent years andpresent the current status of major research topics in this words: abiotic stresses, abscission, color break, flowering, fruit set, ripeningFisiologia da frutifica o em citrus . citrus a principal fruteira no mundo, tendo, portanto, profundos impactosecon micos, sociais e culturais em nossa sociedade. Nos ltimos anos, o conhecimento sobre a biologia reprodutiva deplantas tem aumentado consideravelmente, principalmente em fun o de trabalhos desenvolvidos com , a informa o produzida nessas esp cies nem sempre pode ser aplicada a citrus , fundamentalmente porque citrus uma cultura arb rea perene com uma biologia reprodutiva muito peculiar e incomum.

3 A regula o do crescimento edesenvolvimento do fruto em citrus um fen meno complexo e dependente de muitos fatores externos e internos quepodem operar tanto seq encialmente como simultaneamente. Os elementos e mecanismos pelos quais est mulos ambientese end genos afetam o crescimento do fruto v m sendo interpretados, e esse conhecimento pode auxiliar a proverferramentas que permitiriam otimizar a produ o per se, al m da obten o de frutos com maior valor nutricional, o objetivoprec puo da Industria de citrus . Neste artigo, revisam-se os avan os que v m ocorrendo na fisiologia da frutifica ode citrus durante os ltimos anos; apresenta-se, tamb m, o status atual de pesquisas mais relevantes nessa : estresses abi ticos, flora o, matura o, vingamento de frutosINTRODUCTIONF ruit have been a matter of extensive research inrecent years because of their importance to agricultureand the human diet.

4 However, research on fleshy fruit hasfocused primarily on climacteric fruits such as tomatowhile other fruit models are not so well known. In thisrevision, we will review our understanding of citrus fruitdevelopment and will present it as a plausible model fortree and woody perennials. We will focus on thephysiology of citrus fruiting , an area that complementsthe information presented in two upcoming reviewsdealing with the generation of genomic tools andresources (Talon and Gmitter, 2008) and the progress inmolecular biology and genetics of development (Tadeo et334 Braz. J. Plant Physiol., 19(4):333-362, IGLESIAS et , 2008) in the genus citrus . The focus chosen for thisreview is on major physiological factors regulating fruitgrowth including flowering, hormones, carbohydratesand abiotic constrains. Also revised are majorbiochemical aspects of the ripening processes that maybe important for fruit quality.

5 A central part of the reviewconcentrates on the hormonal and metabolic control offruit set and development and documents progress in theunderstanding of abscission and social relevance: citrus is the mosteconomically important fruit crop in the world, is grown indeveloped and developing countries and certainlyconstitutes one of the main sources of vitamin C. There isalso an increasing demand of high quality fresh citrus driven by World Health Organization contain the largest number of carotenoids found inany fruit and an extensive array of secondary compoundswith pivotal nutritional properties such as vitamin E, pro-vitamin A, flavonoids, limonoids, polysaccharides,lignin, fiber, phenolic compounds, essential oils substances greatly contribute to the supply ofanticancer agents and other nutraceutical compoundswith anti-oxidant, inflammatory, cholesterol and allergicactivities, all of them essential to prevent cardiovascularand degenerative diseases, thrombosis, cancer,atherosclerosis and obesity.

6 In spite of these beneficialtraits there is still a major need to improve fruit quality tomeet current consumer s biology: From a scientific standpoint, citrus has proved to be valuable material for studyingmany biological questions because citrus combine anunusual mixture of reproductive characteristicsincluding, for example, non-climacteric development. Incontrast to climacteric fruits (reviewed in Giovannoni,2004), the mechanism of ripening in non-climacteric fruitsis basically unknown. citrus also exhibit a long juvenilityphase and nearly all important citrus species includingsweet oranges, mandarins, lemons and grapefruits showsome degree of apomixis. Furthermore, many of them areparthenocarpic, sterile or self-incompatible and/ordevelop defective pollen (Baldwin, 1993; Davies andAlbrigo, 1994). In seeded citrus cultivars, fruitdevelopment is linked to the presence of seeds and,therefore, it depends upon pollination and usually takes place in the unopened oropening flower, often allowing pollination beforeanthesis.

7 Cross-pollination occurs between plants ofdifferent genetic background by insect transport ofpollen. However, many current citrus cultivars are mostlyseedless varieties showing high parthenocarpy, in manyinstances due to gametic sterility. Generative sterility canbe relative or absolute. Relative gametic sterility may bedue to self-incompatibility as in Clementine and to cross-incompatibility. On the other hand, absolute gameticsterility is associated with pollen and/or embryo-sacsterility. Some cultivars such as Washington Naveloranges and Satsuma mandarins have both, althougheven in these two varieties a few embryo sacs may oftenreach fruits are also classified as hesperidiums,berries of very special organization characterized by ajuicy pulp made of vesicles within segments. Thus, thecombination of these characteristics suggests that thestudy of citrus fruit growth may reveal original regulationmechanisms based on specific molecular differences and/or even novel genes (Forment et al.)

8 , 2005; Cerc s et al.,2006; Terol et al., 2007). citrus fruits are particularly convenient models tostudy regulation, for example, of secondary metabolismor sugar and citric acid build-ups and although manyefforts have been certainly dedicated to comprehensivephysiological and biochemical descriptive studies (seeBaldwin, 1993) there is still an enormous unexploredpotential in the study of the regulation of the metabolitesassociated with citrus fruit FRUIT SET AND GROWTHF ruit growth and abscission: In general, fruit formationin citrus pursues a genetic developmental programexpressed over a relatively long period. In most speciesunder subtropical conditions flowering takes place inspring and the subsequent formation of fruit extendsuntil mid-winter. However, full ripening in early varietiesmay be reached as soon as September while in latespecies it can be prolonged until the onset of nextsummer.

9 Growth and development of citrus fruit follows atypical sigmoid growth curve, divided into three clear-cutstages (Bain, 1958). The initial phase, or phase I, is an335 Braz. J. Plant Physiol., 19(4):333-362, 2007 Physiology OF citrus fruiting approximately two-month interval of cell division andslow growth including the period between anthesis andJune drop. Thereafter, in the rapid growth period (phaseII) fruit experiences a huge increase in size by cellenlargement and water accumulation during four to sixmonths. Therefore, developing fruitlets are utilizationsinks during the cell division period and act rather asstorage sinks during phase II (Mehouachi et al., 1995).Finally, in phase III or ripening period growth is mostlyarrested and fruits undergo a non-climacteric bloom profusely and therefore also show highabscission of buds, flowers, fruitlets and fruits.

10 It isinteresting to note that although abscission ofreproductive organs is overall continuous during phase I,two waves of elevated abscission take place at the onsetof phase I and during the transition to phase II. Thus,bud, flower and ovary abscission occurs mostly at thebeginning of the cell division phase, whereas fall offruitlets and developing fruits is higher during the Junedrop. Generally, a small percentage of fruits overcome theJune drop and in general less than 1% reaches period in which fruit is liable to fall is referred to asfruit set and in this episode that can be extended alongthe whole phase I, several endogenous and exogenousfactors configure the decision of either setting oraborting growth. The end of the period of fruit set usuallycoincides with the metabolic transition from cell divisionto cell enlargement. During phase II and phase III fruitabscission is considerably reduced although in somespecies and under adverse environmental conditions ripefruits may show pre-harvest fall.