Histological,transcriptomic,and gene functional analyses reveal the regulatory events underlying gibberellin-induced parthenocarpy in tomato

Gibberellin(GA)is one of the major plant hormones that promote parthenocarpy,a highly valuable agronomic trait.Here,we demonstrated that exogenous GA3application triggered the formation of parthenocarpic fruits with smaller size but unchanged shape in tomato(Solanum lycopersicum).These fruits exhibited a thicker pericarp,undeveloped ovules,and few jelly tissues,leading to smaller locules with empty cavities.Histological investigation showed that GA treatment produced more cell layers with larger cells in the pericarp,suggesting its promotion in both cell division and expansion.Transcriptomic analyses between GA-3and mock-treated unpollinated ovaries/fruits identified a large number of differentially expressed genes related to hormones,cell division,cell expansion,and transcription factors,implying that they coordinately regulated parthenocarpy conferred by GA.In particular,the downregulation of five reported repressors of tomato parthenocarpy,including two auxin signaling components,AUXIN RESPONSE FACTOR5(SlARF5)and Sl ARF7,and three MADS-box genes,TOMATO APETALA3(TAP3),TOMATO PISTILLATA(TPI),and AGAMOUS-LIKE6(SlAGL6),after GA treatment might play a key role in this process.Furthermore,we found that the knockdown of a GA signaling factor SlMYB33,which was depressed by GA treatment,induced parthenocarpic fruit set in tomato,an effect that might have been achieved by enhancing GA biosynthesis and decreasing the expression of some repressors of tomato parthenocarpy.Thus,our results provide a basis for understanding the regulatory mechanism of GA in tomato parthenocarpy.

The miR166-SIHB15A 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 SIHB15A,belonging to classⅢhomeodomain leucine-zipper transcription factors.SIHB15A,loss-of-function mu-tants 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,SIHB15A is subjected to conditional haploinsufficiency and recessive dosage sensitivity controlled by microRNA 166(miR166).Knockdown of SIHB15A alleles by miR166 leads to a continuum of aberrant ovules correlating with parthenocarpic fruit set.Consistent with this,plants harboring an Slhb15a-miRNA166-resisiant allele developed normal ovules and were unable to set parthenocarpic fruit under cold conditions.DNA affinity purification sequencing and RNA-sequencing analyses revealed that SIHB15A is a bifunctional transcription factor expressed in the ovule integument.SIHB15A 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 SIHB15A.Taken together,our findings demonstrate the role of SIHB15A as a sentinel to prevent fruit set in the absence of fertilization and provide a mean to enhance fruiting under extreme temperatures.