Genetic Regulation of Fruit Development and Ripening

Abstract

Fruit development and ripening are unique to plants and represent an important component of human and animal diets. Recent discoveries have shed light on the molecular basis of developmental ripening control, suggested common regulators of climacteric and nonclimacteric ripening physiology, and defined a new role for MADS box genes in this late stage of floral development. Analyses of fruit-ripening mutants and ripening-related gene expression suggest higher levels of a developmental regulatory cascade that remain to be defined. Examination of the molecular basis of ethylene signaling in tomato has demonstrated conservation of the basic model defined in Arabidopsis, yet with modifications in gene family composition and expression that may represent adaptations to promote successful fruit development and seed dispersal. The role of light signaling in fruit carotenoid accumulation is being examined and may represent a target for practical manipulation of fruit pigmentation and nutrient content. The continuing development of genomics tools, including ESTs and cDNA microarrays, for important fruit crops should foster accelerated discovery in fruit development and ripening research. By anatomical definition, the fruit is a mature ovary and therefore typically includes carpel tissues in part or in whole. Many fleshy fruit species important to humans additionally develop mature fruit tissues, including extracarpellary floral components. Examples include strawberry, pineapple, mulberry, and pome fruit (apple, pear), in which the receptacle, bracts, calyx, and floral tube (the fused base of floral organs), respectively, constitute the majority of mature fruit tissue. Even species with fruit derived from carpel tissue exclusively can display a range of developmental programs, spanning the relatively uniform single expanded carpel or drupe of stone fruit to the differentiated carpel tissues giving rise to the peel (flavedo) and multicarpel flesh of citrus and banana. Evolutionary pressures have resulted in a variety of developmental manifestations of fruit tissues, resulting in structures that range in design and function from hardened fruit capsules or pods that forcefully expel seeds at maturation, to forms optimized for seed movement by wind, water, animal fur, or gravity, to those implementing developmental programs that yield succulent and flavorful tissues for organisms that consume and disperse the associated seed. Tanksley (this issue) discusses the impact of domestication on selection for fruit genes that influence size and shape early in fruit development in addition to discoveries regarding their underlying molecular functions. The focus here will be on recent advances in our understanding of developmental and signaling pathways that affect later fruit maturation and ripening. Although dehiscent and dry fruit types (e.g., cereals) represent the majority of plant species, fruit developmental studies to date have focused primarily on fleshy species because of their importance in the human diet. Particular emphasis has been placed on tomato as an especially tractable system for molecular genetic analysis of fleshy fruit development and ripening (Giovannoni, 2001). Arabidopsis also has proven exceptionally informative as a model system for floral development in general (Lohmann and Weigel, 2002) and gene identification and the subsequent functional analysis of carpel identity–, development-, and maturation-associated genes (Pinyopich et al., 2003, and references therein). In addition, the Arabidopsis silique is a dehiscent fruit characteristic of the legumes and thus represents another exceptionally important fruit type in terms of human and animal food. Other systems will be mentioned where appropriate, but the majority of this review will focus on Arabidopsis and tomato as the major systems underlying many recent discoveries in fruit development and ripening. Since the initial description of a requirement for the AGAMOUS (AG) protein for carpel and stamen determination (Bowman et al., 1989), a large family of Arabidopsis MADS box genes has been reported and in many cases functionally defined (Alvarez-Buylla et al., 2000, and references therein). For example, the redundant SEPALLATA genes (SEP1, SEP2, and SEP3) can be eliminated via mutation individually with minimal impact on floral development, yet the triple mutant results in the conversion of all floral organs to sepals, indicating roles in normal petal, stamen, and carpel development (Pelaz et al., 2000). Spatial constraint of AG expression via negative regulation by the APETALA2 (AP2) EREBP-like protein provided early evidence that additional transcription factors also play important roles in floral and carpel development, in part via the regulation of MADS box genes (Drews et al., 1991). Additional insight into the molecular basis of carpel determination in the developing flower came through the recent discovery that two previously described MADS box SH