The miR166-SlHB15A regulatory module controls ovule development and parthenocarpic fruit set under adverse temperatures in tomato.

Fruit set is inhibited by adverse temperatures, with consequences on yield. We isolated a tomato mutant producing fruits under non-permissive hot temperatures and identified the causal gene as SlHB15A, belonging to class III homeodomain leucine-zipper transcription factors. SlHB15A loss-of-function mutants display aberrant ovule development that mimics transcriptional changes occurring in fertilized ovules and leads to parthenocarpic fruit set under optimal and non-permissive temperatures, in field and greenhouse conditions. Under cold growing conditions, SlHB15A is subjected to conditional haploinsufficiency and recessive dosage sensitivity controlled by microRNA 166 (miR166). Knockdown of SlHB15A alleles by miR166 leads to a continuum of aberrant ovules correlating with parthenocarpic fruit set. Consistent with this, plants harboring an Slhb15a-miRNA166-resistant allele developed normal ovules and were unable to set parthenocarpic fruit under cold conditions. DNA affinity purification sequencing and RNA-sequencing analyses revealed that SlHB15A is a bifunctional transcription factor expressed in the ovule integument. SlHB15A binds to the promoters of auxin-related genes to repress auxin signaling and to the promoters of ethylene-related genes to activate their expression. A survey of tomato genetic biodiversity identified pat and pat-1, two historical parthenocarpic mutants, as alleles of SlHB15A. Taken together, our findings demonstrate the role of SlHB15A as a sentinel to prevent fruit set in the absence of fertilization and provide a mean to enhance fruiting under extreme temperatures.

The gynoecious CmWIP1 transcription factor interacts with CmbZIP48 to inhibit carpel development.

In angiosperms, sex determination leads to development of unisexual flowers. In Cucumis melo, development of unisexual male flowers results from the expression of the sex determination gene, CmWIP1, in carpel primordia. To bring new insight on the molecular mechanisms through which CmWIP1 leads to carpel abortion in male flowers, we used the yeast two-hybrid approach to look for CmWIP1-interacting proteins. We found that CmWIP1 physically interacts with an S2 bZIP transcription factor, CmbZIP48. We further determined the region mediating the interaction and showed that it involves the N-terminal part of CmWIP1. Using laser capture microdissection coupled with quantitative real-time gene expression analysis, we demonstrated that CmWIP1 and CmbZIP48 share a similar spatiotemporal expression pattern, providing the plant organ context for the CmWIP1-CmbZIP48 protein interaction. Using sex transition mutants, we demonstrated that the expression of the male promoting gene CmWIP1 correlates with the expression of CmbZIP48. Altogether, our data support a model in which the coexpression and the physical interaction of CmWIP1 and CmbZIP48 trigger carpel primordia abortion, leading to the development of unisexual male flowers.