Abstract
Improving yield by increasing the size of produce is an important selection criterion during the domestication of fruit and vegetable crops. Genes controlling meristem organization and organ formation work in concert to regulate the size of reproductive organs. In tomato, lc and fas control locule number, which often leads to enlarged fruits compared to the wild progenitors. LC is encoded by the tomato ortholog of WUSCHEL (WUS), whereas FAS is encoded by the tomato ortholog of CLAVATA3 (CLV3). The critical role of the WUS‐CLV3 feedback loop in meristem organization has been demonstrated in several plant species. We show that mutant alleles for both loci in tomato led to an expansion of the SlWUS expression domain in young floral buds 2–3 days after initiation. Single and double mutant alleles of lc and fas maintain higher SlWUS expression during the development of the carpel primordia in the floral bud. This augmentation and altered spatial expression of SlWUS provided a mechanistic basis for the formation of multilocular and large fruits. Our results indicated that lc and fas are gain‐of‐function and partially loss‐of‐function alleles, respectively, while both mutations positively affect the size of tomato floral meristems. In addition, expression profiling showed that lc and fas affected the expression of several genes in biological processes including those involved in meristem/flower development, patterning, microtubule binding activity, and sterol biosynthesis. Several differentially expressed genes co‐expressed with SlWUS have been identified, and they are enriched for functions in meristem regulation. Our results provide new insights into the transcriptional regulation of genes that modulate meristem maintenance and floral organ determinacy in tomato.
Highlights
To develop varieties with improved characteristics, breeders exploit the genetic variation of important agronomic traits such as fruit weight, grain yield, and overall plant architecture
With the advent of Quantitative Trait Loci (QTL) mapping and cloning methods in past decades, many genes contributing to the increase in fruit weight and crop yield have been identified (Bommert, Nagasawa, & Jackson, 2013; Chakrabarti et al, 2013; Frary et al, 2000; Li et al, 2011; Song et al, 2007)
Our findings indicate a close conservation between tomato LC-FAS and Arabidopsis WUS-CLV3 regulatory loops
Summary
To develop varieties with improved characteristics, breeders exploit the genetic variation of important agronomic traits such as fruit weight, grain yield, and overall plant architecture. In contrast to genes co-expressed with SlWUS, the expression of the sterol biosynthesis pathway genes increased with the floral development stages These genes were expressed at lower levels in fas and lc/fas compared to WT across different developmental stages, implying the negative roles of these genes in meristem maintenance. Cluster 6 was enriched with genes encoding microtubule motor proteins, including putative homologs of Arabidopsis KINESIN 1 (ATK1) (Solyc g005250), PHRAGMOPLAST-ASSOCIATED KINESINRELATED PROTEIN 1 (PAKRP1) (Solyc g097860), TETRASPORE (TES) (Solyc g042560) and ZWICHEL (ZWI) (Solyc g082730) These genes were expressed at higher levels at 2 dpi, indicating that their expression might be positively regulated by genes mediating outer whorl initiation. Kinesins might play a role in organelle movement (Zhu & Dixit, 2012), the co-expressed pattern of these kinesin genes with putative tomato Cyclin B2;3 and Cellulose Synthase-Like gene suggested that they were more likely involved in cytokinesis (Hunter et al, 2012; Tank & Thaker, 2011)
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