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The miR166-SIHB15A regulatory module controls ovule development and parthenocarpic fruit set under adverse temperatures in tomato

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Molecular Plant 2021年第7期14卷 1185-1198页

作者： Christian Clepet Ravi Sureshbhai Devani Rachid Boumlik Yanwei Hao Halima Morin Fabien Marcel Marion Verdenaud Brahim Mania Gwilherm Brisou Sylvie Citerne Gregory Mouille Jean-Christophe Lepeltier Shai Koussevitzky Adnane Boualem Abdelhafid Bendahmane Institute of Plant Sciences Paris-Saclay INRAECNRSUniversite Paris-SaclayOrsay 91405France HM Clause Mas Saint-PierreQuartier La GalineSaint-Remy de Provence 13210France Hazera Seeds Ltd Berurim M.P.Shikmim 7983700Israel lnstitut Jean-Pierre Bourgin INRAEVersaillesFrance Present address:Key Laboratory of Horticultural Crop Biology and Germplasm Innovation in South China College of HorticultureSouth China Agricultural UniversityGuangzhou 510642China

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.

关键词： parthenocarpy dosage sensitivity HD-Ziplll miRNA166 heat stress cold stress

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