Fruit ripening mutants yield insights into ripening control
Introduction
Fruit constitute important components of human and animal diets, and are organs and developmental systems that are unique to plants. As a result, considerable scientific study has focused on questions of fruit organogenesis, differentiation, development and maturation, in addition to the genetic basis of organoleptic and nutritional qualities (reviewed in [1, 2, 3, 4•]). Pioneering work on the genetic basis of fruit formation and development has emphasized the model system Arabidopsis [5], whereas investigations of organ expansion, maturity, ripening, shelf-life and nutritional quality have centered on the crop model tomato (Solanum lycopersicum) [2]. Tomato, the centerpiece of the Solanceae family, has emerged as a model of fleshy fruit development, primarily because this is the species for which the genetic and molecular toolkits are most advanced. Extensive germplasm collections, well-characterized mutant stocks, high-density genetic maps, immortalized mapping populations, efficient transient and stable transformation, deep expressed sequence tag (EST) resources, microarrays and an ongoing genome sequencing effort all contribute to the utility of this experimental system (see www.sgn.cornell.edu and www.tigr.org for links to these resources). Well-characterized ripening mutations, short generation time, a long history of physiological, biochemical and molecular investigations related to fruit development and maturation, and interest in the species as an important commodity crop, have fueled considerable effort on understanding ripening in tomato. Early molecular analyses of fruit ripening focused on the roles of cell-wall-metabolizing and structural proteins [6], and on the genetic basis of ethylene synthesis [7]. In recent years, the molecular biology of ripening has turned to genomics approaches to reveal insights into primary ripening control upstream of ethylene, ripening-related signal transduction systems and downstream metabolic networks. These advances have been facilitated by increasingly efficient positional cloning in tomato, by the development of a model for ethylene signal transduction from Arabidopsis (which could be tested in tomato) and by improved metabolic profiling technologies, respectively. The result has been the opening of a new frontier in ripening molecular biology that is focused on upstream transcriptional control and on the characterization of hormonal and environmental signaling mechanisms.
Section snippets
Revealing the secrets of ripening mutants
Deep screens for ripening mutants have been limited by the number of mature tomato plants that can be reasonably managed in field trials. For example, the screening of 10 000 tomato M2 families consisting of twenty individuals per family would require approximately 20 hectares (50 acres) of field space. A mutant screen on this scale has recently been performed, rendering numerous mutant lines available for genetic purification and analysis [8]. Previously characterized ripening mutants have
Insights into the transcriptional control of fruit ripening
The rin and Cnr mutations are recessive and dominant mutations, respectively, that effectively block the ripening process and result in mutant fruit that fail either to produce elevated ethylene or to respond to exogenous ethylene by ripening [9, 10••]. The rin mutation is additionally noteworthy because hybrids (rin/Rin) form the basis for most present-day production of slow-ripening, long shelf-life, fresh-market tomatoes. Both the rin [9] and Cnr [10••] loci encode putative transcription
The molecular basis of the ethylene response in fruit
Recent efforts related to the molecular biology of the ethylene response of ripening fruit have centered on the characterization of tomato homologs of Arabidopsis ethylene signal transduction genes. All of the analyzed components of the Arabidopsis ethylene signaling machinery are clearly conserved in tomato [16, 17, 18, 19, 20], but family sizes and expression profiles are differ between some Arabidopsis and tomato ethylene signaling genes. Tomato harbors six ethylene receptors compared to the
Genetics of fruit chemistry
Biochemical pathways that impact fruit quality and nutritional content have long been the focus of ripening biology. Indeed, many steps in carotenoid biosynthesis have been elucidated through the study of tomato mutations and genes [29, 30, 31, 32]. The genetics of downstream cleavage activities that result in signaling molecules, growth regulators and aroma volatiles that might serve as nutritional signals for seed-dispersing organisms have been reviewed recently [4•, 33]. Emerging metabolic
Conclusions
Physiologically characterized single gene tomato ripening mutants, which in some cases have been available for decades, have recently become accessible at the molecular level as the genomics infrastructure for tomato has expanded. Cloning of the RIN and CNR genes defined the first ripening-specific transcription factors and provided insight into ripening control upstream of ethylene. The Nr mutation revealed an ethylene receptor gene, and Gr has been found to encode a novel component of
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
Special thanks to Julia Vrebalov for critical review and comments. Ripening research in the Giovannoni laboratory was supported by grants from the National Science Foundation Plant Genome Program (05-01778, 06-05659, 06-06595), US Department of Agriculture – National Research Initiative Competitive Grants Program (2002-35304-12530) and the Binational Agricultural Research and Development fund (IS-3877-06CR).
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