Plants are vulnerable to heat stress especially during reproductive development. HSR (Heat shock response) in cytosol and nucleus as well as UPR (Unfolded protein response) in ER (Endoplasmic reticulum) are two mechanisms that enable plants to survive heat stress. Excessive heat or ER stresses lead to cell death when UPR cannot repair stress damages, but how the outcome of being survival being death is determined is not clear. Here, we uncovered from GWAS (Genome-wide association study) that a gene cluster containing five IAN (Immune-associated nucleotide-binding protein) genes (IAN2 to IAN6) is responsible for heat tolerance variation on heat tolerance at reproductive stage in Arabidopsis thaliana. These IAN genes have both unique and overlapping function in negatively regulating heat tolerance as the loss of their functions, singly or combinatorically, confers an increased heat tolerance measured by a lower number of barren siliques and a higher seedling survival rate under heat. The loss of rice IAN1 gene function also leads to enhanced heat tolerance, suggesting a conserved function of plant IANs. Transcriptome analysis revealed an enhanced expression of HSR genes and UPR genes as well as reduced cell death under heat stress and ER stress in the mutant of IAN6, a major effect member in Arabidopsis. Furthermore, the IAN proteins are found to promote cell death induced by heat stress, ER stress and cell death inducing molecules. Thus the Arabidopsis IAN genes repress heat tolerance likely through HSR and UPR and by enhancing the cell death pathway. The IAN2 to IAN6 proteins are partially localized to ER, suggesting a direct role in UPR and UPR mediated cell death. In addition, a natural IAN6 variant from more heat tolerant Arabidopsis accessions confers a higher heat tolerance and induces less cell death compared to the natural variant from less heat tolerant accessions. The heat-tolerant IAN6 variant is associated with a higher maximum temperature of the warmest month at their collection sites than the heat-sensitive variant. Our results thus reveal an important role of Arabidopsis IAN2 to IAN6 genes in regulating HSR, UPR and cell death and suggest an adaptive value of their natural variations in heat tolerance.
Arabidopsis Immune-Associated Nucleotide-binding genes inhibit heat tolerance at reproductive stages via inhibiting unfolded protein response and promoting cell death.
Shan Lu,Tianquan Zhu,Zhixue Wang,Lilin Luo,Shuai Wang,Minghui Lu,Yongmei Cui,Baohong Zou,J. Hua
Published 2020 in Molecular Plant
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- Publication year
2020
- Venue
Molecular Plant
- Publication date
2020-11-19
- Fields of study
Biology, Medicine, Environmental Science
- Identifiers
- External record
- Source metadata
Semantic Scholar, PubMed
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