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 (HD-ZipIII). 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 glasshouse conditions. Under cold growing condition, 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 SlHB15A-miRNA166 resistant allele developed normal ovules and were unable to set parthenocarpic fruit under cold condition. DNA affinity purification sequencing (DAP-seq) and RNAseq analyses revealed SlHB15A is a bifunctional transcription factor, expressing in the ovule integument. SlHB15A binds to the promoters of auxin genes to repress auxin signaling and to ethylene genes to activate their expression. Survey of tomato genetic biodiversity identified pat and pat-1, two historical parthenocarpic mutants, as alleles of SlHB15A. Our finding demonstrates the role of SlHB15A as a sentinel to prevent fruit set in the absence of fertilization and provides a mean to enhance fruiting under extreme temperatures.