The transcription factor ERF110 promotes cold tolerance by directly regulating sugar and sterol biosynthesis in citrus

Author:

Khan Madiha1,Dahro Bachar1,Wang Yue1,Wang Min2,Xiao Wei1,Qu Jing1,Zeng Yike1,Fang Tian1,Xiao Peng1,Xu Xiaoyong3,Li Chunlong14ORCID,Liu Ji‐Hong14ORCID

Affiliation:

1. National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Science Huazhong Agricultural University Wuhan 430070 China

2. College of Life Sciences Gannan Normal University Ganzhou 341000 China

3. College of Horticulture and Landscape Architecture Yangzhou University Yangzhou 225009 China

4. Hubei Hongshan Laboratory Wuhan 430070 China

Abstract

SUMMARYERFs (ethylene‐responsive factors) are known to play a key role in orchestrating cold stress signal transduction. However, the regulatory mechanisms and target genes of most ERFs are far from being well deciphered. In this study, we identified a cold‐induced ERF, designated as PtrERF110, from trifoliate orange (Poncirus trifoliata L. Raf., also known as Citrus trifoliata L.), an elite cold‐hardy plant. PtrERF110 is a nuclear protein with transcriptional activation activity. Overexpression of PtrERF110 remarkably enhanced cold tolerance in lemon (Citrus limon) and tobacco (Nicotiana tabacum), whereas VIGS (virus‐induced gene silencing)‐mediated knockdown of PtrERF110 drastically impaired the cold tolerance. RNA sequence analysis revealed that PtrERF110 overexpression resulted in global transcriptional reprogramming of a range of stress‐responsive genes. Three of the genes, including PtrERD6L16 (early responsive dehydration 6‐like transporters), PtrSPS4 (sucrose phosphate synthase 4), and PtrUGT80B1 (UDP‐glucose: sterol glycosyltransferases 80B1), were confirmed as direct targets of PtrERF110. Consistently, PtrERF110‐overexpressing plants exhibited higher levels of sugars and sterols compared to their wild type counterparts, whereas the VIGS plants had an opposite trend. Exogenous supply of sucrose restored the cold tolerance of PtrERF110‐silencing plants. In addition, knockdown of PtrSPS4, PtrERD6L16, and PtrUGT80B1 substantially impaired the cold tolerance of P. trifoliata. Taken together, our findings indicate that PtrERF110 positively modulates cold tolerance by directly regulating sugar and sterol synthesis through transcriptionally activating PtrERD6L16, PtrSPS4, and PtrUGT80B1. The regulatory modules (ERF110‐ERD6L16/SPS4/UGT80B1) unraveled in this study advance our understanding of the molecular mechanisms underlying sugar and sterol accumulation in plants subjected to cold stress.

Funder

National Natural Science Foundation of China

National Key Research and Development Program of China

Publisher

Wiley

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