Multispecies transcriptomes reveal core fruit development genes.

During angiosperm evolution there have been repeated transitions from an ancestral dry fruit to a derived fleshy fruit, often with dramatic ecological and economic consequences. Following the transition to fleshy fruits, domestication may also dramatically alter the fruit phenotype via artificial selection. Although the morphologies of these fruits are well documented, relatively less is known about the molecular basis of these developmental and evolutionary shifts. We generated RNA-seq libraries from pericarp tissue of desert tobacco and both cultivated and wild tomato species at common developmental time points and combined this with corresponding, publicly available data from Arabidopsis and melon. With this broadly sampled dataset consisting of dry/fleshy fruits and wild/domesticated species, we applied novel bioinformatic methods to investigate conserved and divergent patterns of gene expression during fruit development and evolution. A small set of 121 orthologous "core" fruit development genes show a common pattern of expression across all five species. These include key players in developmental patterning such as orthologs of KNOLLE, PERIANTHIA, and ARGONAUTE7. GO term enrichment suggests that these genes function in basic cell division processes, cell wall biosynthesis, and developmental patterning. We furthermore uncovered a number of "accessory" genes with conserved expression patterns within but not among fruit types, and whose functional enrichment highlights the conspicuous differences between these phenotypic classes. We observe striking conservation of gene expression patterns despite large evolutionary distances, and dramatic phenotypic shifts, suggesting a conserved function for a small subset of core fruit development genes.

New genomic resources and comparative analyses reveal differences in floral gene expression in selfing and outcrossing Collinsia sister species.

The evolutionary transition from outcross- to self-fertilization is one of the most common in angiosperms and is often associated with a parallel shift in floral morphological and developmental traits, such as reduced flower size and pollen to ovule ratios, known as the "selfing syndrome." How these convergent phenotypes arise, the extent to which they are shaped by selection, and the nature of their underlying genetic basis are unsettled questions in evolutionary biology. The genus Collinsia (Plantaginaceae) includes seven independent transitions from outcrossing or mixed mating to high selfing rates accompanied by selfing syndrome traits. Accordingly, Collinsia represents an ideal system for investigating this parallelism, but requires genomic resource development. We present a high quality de novo genome assembly for the highly selfing species Collinsia rattanii. To begin addressing the basis of selfing syndrome developmental shifts, we evaluate and contrast patterns of gene expression from floral transcriptomes across three stages of bud development for C. rattanii and its outcrossing sister species Collinsia linearis. Relative to C. linearis, total gene expression is less variable among individuals and bud stages in C. rattanii. In addition, there is a common pattern among differentially expressed genes: lower expression levels that are more constant across bud development in C. rattanii relative to C. linearis. Transcriptional regulation of enzymes involved in pollen formation specifically in early bud development may influence floral traits that distinguish selfing and outcrossing Collinsia species through pleiotropic functions. Future work will include additional Collinsia outcrossing-selfing species pairs to identify genomic signatures of parallel evolution.

Evolution and Diversification of FRUITFULL Genes in Solanaceae.

Ecologically and economically important fleshy edible fruits have evolved from dry fruit numerous times during angiosperm diversification. However, the molecular mechanisms that underlie these shifts are unknown. In the Solanaceae there has been a major shift to fleshy fruits in the subfamily Solanoideae. Evidence suggests that an ortholog of FRUITFULL (FUL), a transcription factor that regulates cell proliferation and limits the dehiscence zone in the silique of Arabidopsis, plays a similar role in dry-fruited Solanaceae. However, studies have shown that FUL orthologs have taken on new functions in fleshy fruit development, including regulating elements of tomato ripening such as pigment accumulation. FUL belongs to the core eudicot euFUL clade of the angiosperm AP1/FUL gene lineage. The euFUL genes fall into two paralogous clades, euFULI and euFULII. While most core eudicots have one gene in each clade, Solanaceae have two: FUL1 and FUL2 in the former, and MBP10 and MBP20 in the latter. We characterized the evolution of the euFUL genes to identify changes that might be correlated with the origin of fleshy fruit in Solanaceae. Our analyses revealed that the Solanaceae FUL1 and FUL2 clades probably originated through an early whole genome multiplication event. By contrast, the data suggest that the MBP10 and MBP20 clades are the result of a later tandem duplication event. MBP10 is expressed at weak to moderate levels, and its atypical short first intron lacks putative transcription factor binding sites, indicating possible pseudogenization. Consistent with this, our analyses show that MBP10 is evolving at a faster rate compared to MBP20. Our analyses found that Solanaceae euFUL gene duplications, evolutionary rates, and changes in protein residues and expression patterns are not correlated with the shift in fruit type. This suggests deeper analyses are needed to identify the mechanism underlying the change in FUL ortholog function.