UC Davis

Fruit ripening is a complex developmental process in which fruit undergo physiological and biochemical changes, transforming fruit into nutritious and flavorful foods. Fruit quality traits, such as flavor and aroma, texture, and color, are essential for product marketability and increase during ripening. The characteristic changes in fruit physiology and biochemical composition during ripening result from extensive transcriptional reprogramming. While some regulatory mechanisms governing ripening have been identified, such as, transcription factors (TFs), plant hormones, and post-transcriptional and epigeneticfactors, the genetic factors regulating fruit quality are not fully understood.

The overarching goal of this Ph.D. dissertation was to explain the physiological and genetic events determining fruit quality traits during ripening. First, I assessed the current knowledge of ripening regulators of fruit quality traits across diverse fruit species(Chapter 1). Five main categories emerged—color, flavor, nutrition, texture, and shelf life. Transcription factor regulators can act in a pathway-specific manner or as “master” regulators of multiple pathways. Pathway-specific regulators are promising targets for improving fruit quality because they cause fewer unwanted effects on other traits (Chapter 1). In contrast, manipulations to master regulators impact multiple quality attributes causing pleiotropic effects (Chapter 1, Chapter 2). Plant hormones act with transcription factors and are often non-specific to quality traits (Chapter 1).

I employed multiple approaches to provide a system-wide understanding of ripening regulation and events associated with fruit quality in two economically important crops for California, tomato (Solanum lycopersicum) and pistachio (Pistacia vera). In both studies (Chapters 2 and 3), fruit physiological parameters were measured in field conditions to provide evidence of physical changes occurring in the fruit through ripening. Biochemical measurements provided further evidence of the specific compounds being altered in each crop. Then, the information was integrated with genome-wide expression analysis to identify underlying molecular mechanisms for each study.

In Chapter 2, I studied the impact of mutations in ripening-related transcription factors (NOR, RIN, and CNR) on tomato fruit quality through trait phenotyping, transcriptional profiling, and hormone measurements over multiple field seasons. I hypothesized each mutant had distinct defects in fruit quality attributes. I determined that ripening in two mutants (nor and rin) is not entirely inhibited; instead, some ripening processes are delayed. I also demonstrate that the Cnr mutation affects fruit development long before the onset of ripening. We also generated homozygous double mutants of these genotypes for the first time to study the combined effect of the mutations on development and ripening. This study contributed new knowledge regarding the tomato ripening mutants, which have been employed to understand fruit ripening for at least the past two decades.Also, given the importance of both rin and nor in breeding, quality trait data from these mutants are of high value.

In Chapter 3, I applied the knowledge gained in the model system of tomato to investigate a nut crop, pistachio, in which ripening had not been previously described. With collaborators, we generated critical genomic resources to study pistachio ripening:a complete genome assembly for P. vera (c.v. Kerman) and a large transcriptomic study expanding 15 weeks of pistachio growth and development and three different fruit tissues (hull, shell, kernel). I also performed a multiyear multi-location analysis of pistachio phenology, allowing me to model multiple fruit physiological measurements across the growing season. The molecular and physiological data allowed me to determine four distinct stages of pistachio development, with Stage IV corresponding to fruit ripening and kernel maturation. I then hypothesize that transcriptional changes at Stage IV are critical for gaining and establishing nut quality traits. I identified hormones associated with fruit ripening and downstream genetic pathways that can explain the physiological changes observed in the nut. I gave particular attention to genes and pathways related to key quality attributes in pistachio, hull softening, shell hardening, and kernel fat composition.Overall, this work ascertained a complete characterization of pistachio development for the first time, generated valuable genetic resources for future nut research, and providednovel insights into the genetic programs governing pistachio ripening.

The results of this dissertation improve the understanding of the molecular basis of fruit quality traits. My research provides new knowledge about transcriptional regulation required for tomato fruit quality and the implications for better utilizing ripening mutants in breeding for hybrids with extended shelf-life. The genetic resources created for pistachio development will be a basis for continued research in pistachio and other nut tree crops. Further, identifying the timing and mechanisms of ripening in pistachio involved in hull softening and color changes will help develop management strategies for harvest time.