Freezing stress can seriously affect plant growth and development,but the mechanisms of these effects and plant responses to freezing stress require further exploration.Here,we identified a NAM,ATAF1/2,and CUC2(NAC)-f...Freezing stress can seriously affect plant growth and development,but the mechanisms of these effects and plant responses to freezing stress require further exploration.Here,we identified a NAM,ATAF1/2,and CUC2(NAC)-family transcription factor(TF),NAC056,that can promote freezing tolerance in Arabidopsis.NAC056 mRNA levels are strongly induced by freezing stress in roots,and the nac056 mutant exhibits compromised freezing tolerance.NAC056 acts positively in response to freezing by directly promoting key C-repeat-binding factor(CBF)pathway genes.Interestingly,we found that CBF1 regulates nitrate assimilation by regulating the nitrate reductase gene NIA1 in plants;therefore,NAC056–CBF1–NIA1 form a regulatory module for the assimilation of nitrate and the growth of roots under freezing stress.In addition,35S::NAC056 transgenic plants show enhanced freezing tolerance,which is partially reversed in the cbfs triple mutant.Thus,NAC056 confers freezing tolerance through the CBF pathway,mediating plant responses to balance growth and freezing stress tolerance.展开更多
Cold acclimation in Arabidopsis thaliana triggers a significant transcriptional reprogramming altering the expression patterns of thousands of cold-responsive(COR) genes. Essential to this process is the C-repeat bind...Cold acclimation in Arabidopsis thaliana triggers a significant transcriptional reprogramming altering the expression patterns of thousands of cold-responsive(COR) genes. Essential to this process is the C-repeat binding factor(CBF)-dependent pathway, involving the activity of AP2/ERF(APETALA2/ethylene-responsive factor)-type CBF transcription factors required for plant cold acclimation. In this study, we performed chromatin immunoprecipitation assays followed by deep sequencing(ChIP-seq) to determine the genomewide binding sites of the CBF transcription factors. Cold-induced CBF proteins specifically bind to the conserved C-repeat(CRT)/dehydrationresponsive elements(CRT/DRE;G/ACCGAC) of their target genes. A Gene Ontology enrichment analysis showed that 1,012 genes are targeted by all three CBFs. Combined with a transcriptional analysis of the cbf1,2,3 triple mutant, we define 146 CBF regulons as direct CBF targets. In addition, the CBF-target genes are significantly enriched in functions associated with hormone, light,and circadian rhythm signaling, suggesting that the CBFs act as key integrators of endogenous and external environmental cues. Our findings not only define the genome-wide binding patterns of the CBFs during the early cold response, but also provide insights into the role of the CBFs in regulating multiple biological processes of plants.展开更多
The C-repeat binding factors/dehydrationresponsive element binding protein 1 s(CBFs/DREB1 s)have been identified as major regulators of cold acclimation in many angiosperm plants.However,their origin and evolutionary ...The C-repeat binding factors/dehydrationresponsive element binding protein 1 s(CBFs/DREB1 s)have been identified as major regulators of cold acclimation in many angiosperm plants.However,their origin and evolutionary process associated to cold responsiveness are still lacking.By integrating multi-omics data of genomes,transcriptomes,and CBFs/DREB1 s genome-wide binding profiles,we unveil the origin and evolution of CBFs/DREB1 s and their regulatory network.Gene collinearity and phylogeny analyses show that CBF/DREB1 is an innovation evolved from tandem duplication-derived DREBⅢgene.A subsequent event of e-whole genome duplication led to two CBF/DREB1 archetypes(CladesⅠandⅡ)in ancient angiosperms.In contrast to cold-insensitivity of Clade I and their parent DREBⅢgenes,CladeⅡevolved a further innovation in cold-sensitive response and was stepwise expanded in eudicots and monocots by independent duplications.In geological time,the duplication events were mainly enriched around the Cretaceous-Paleogene(K-Pg)boundary and/or in the Late Cenozoic Ice Age,when the global average temperature significantly decreased.Consequently,the duplicated CBF/DREB1 genes contributed to the rewiring of CBFs/DREB1 s-regulatory network for cold tolerance.Altogether,our results highlight an origin and convergent evolution of CBFs/DREB1 s and their regulatory network probably for angiosperms adaptation to global cooling.展开更多
基金supported by the National Natural Science Foundation of China(grant nos.32371293,32171232,31500236,and 31570859)the Natural Science Foundation of Shanghai(grant no.22ZR1469500).
文摘Freezing stress can seriously affect plant growth and development,but the mechanisms of these effects and plant responses to freezing stress require further exploration.Here,we identified a NAM,ATAF1/2,and CUC2(NAC)-family transcription factor(TF),NAC056,that can promote freezing tolerance in Arabidopsis.NAC056 mRNA levels are strongly induced by freezing stress in roots,and the nac056 mutant exhibits compromised freezing tolerance.NAC056 acts positively in response to freezing by directly promoting key C-repeat-binding factor(CBF)pathway genes.Interestingly,we found that CBF1 regulates nitrate assimilation by regulating the nitrate reductase gene NIA1 in plants;therefore,NAC056–CBF1–NIA1 form a regulatory module for the assimilation of nitrate and the growth of roots under freezing stress.In addition,35S::NAC056 transgenic plants show enhanced freezing tolerance,which is partially reversed in the cbfs triple mutant.Thus,NAC056 confers freezing tolerance through the CBF pathway,mediating plant responses to balance growth and freezing stress tolerance.
基金This work was supported by the National Natural Sciences Foundation of China(31872658,32022008,31921001)。
文摘Cold acclimation in Arabidopsis thaliana triggers a significant transcriptional reprogramming altering the expression patterns of thousands of cold-responsive(COR) genes. Essential to this process is the C-repeat binding factor(CBF)-dependent pathway, involving the activity of AP2/ERF(APETALA2/ethylene-responsive factor)-type CBF transcription factors required for plant cold acclimation. In this study, we performed chromatin immunoprecipitation assays followed by deep sequencing(ChIP-seq) to determine the genomewide binding sites of the CBF transcription factors. Cold-induced CBF proteins specifically bind to the conserved C-repeat(CRT)/dehydrationresponsive elements(CRT/DRE;G/ACCGAC) of their target genes. A Gene Ontology enrichment analysis showed that 1,012 genes are targeted by all three CBFs. Combined with a transcriptional analysis of the cbf1,2,3 triple mutant, we define 146 CBF regulons as direct CBF targets. In addition, the CBF-target genes are significantly enriched in functions associated with hormone, light,and circadian rhythm signaling, suggesting that the CBFs act as key integrators of endogenous and external environmental cues. Our findings not only define the genome-wide binding patterns of the CBFs during the early cold response, but also provide insights into the role of the CBFs in regulating multiple biological processes of plants.
基金supported by National Key R&D Program of China(2018YFD1000604)National Natural Science Foundation of China(31871233)Natural Science Foundation of Zhejiang Province(LY22C160005)。
文摘The C-repeat binding factors/dehydrationresponsive element binding protein 1 s(CBFs/DREB1 s)have been identified as major regulators of cold acclimation in many angiosperm plants.However,their origin and evolutionary process associated to cold responsiveness are still lacking.By integrating multi-omics data of genomes,transcriptomes,and CBFs/DREB1 s genome-wide binding profiles,we unveil the origin and evolution of CBFs/DREB1 s and their regulatory network.Gene collinearity and phylogeny analyses show that CBF/DREB1 is an innovation evolved from tandem duplication-derived DREBⅢgene.A subsequent event of e-whole genome duplication led to two CBF/DREB1 archetypes(CladesⅠandⅡ)in ancient angiosperms.In contrast to cold-insensitivity of Clade I and their parent DREBⅢgenes,CladeⅡevolved a further innovation in cold-sensitive response and was stepwise expanded in eudicots and monocots by independent duplications.In geological time,the duplication events were mainly enriched around the Cretaceous-Paleogene(K-Pg)boundary and/or in the Late Cenozoic Ice Age,when the global average temperature significantly decreased.Consequently,the duplicated CBF/DREB1 genes contributed to the rewiring of CBFs/DREB1 s-regulatory network for cold tolerance.Altogether,our results highlight an origin and convergent evolution of CBFs/DREB1 s and their regulatory network probably for angiosperms adaptation to global cooling.
