title: Proteasome-mediated degradation of FRIGIDA modulates flowering time in Arabidopsis during vernalization.
abstract: Winter-annual accessions of Arabidopsis thaliana require either exposure to cold stress or vernalization to initiate flowering via FRIGIDA (FRI). FRI acts as a scaffold protein to recruit several chromatin modifiers that epigenetically modify flowering genes. Here, we report that proteasome-mediated FRI degradation regulates flowering during vernalization in Arabidopsis. Our genetic and biochemical experiments demonstrate that FRI directly interacts with the BTB (Bric-a-Brac/Tramtrack/Broad Complex) proteins LIGHT-RESPONSE BTB1 (LRB1) and LRB2 as well as the CULLIN3A (CUL3A) ubiquitin-E3 ligase in vitro and in vivo, leading to proteasomal degradation of FRI during vernalization. The degradation of FRI is accompanied by an increase in the levels of the long noncoding RNA ColdAIR, which reduces the level of histone H3Lys4 trimethylation (H3K4me3) in FLOWERING LOCUS C chromatin to promote flowering. Furthermore, we found that the cold-induced WRKY34 transcription factor binds to the W-box in the promoter region of CUL3A to modulate CUL3A expression. Deficiency of WRKY34 suppressed CUL3A transcription to enhance FRI protein stability and led to late flowering after vernalization. Conversely, overexpression of WRK34 promoted FRI degradation and early flowering through inducing CUL3A accumulation. Together, these data suggest that WRKY34-induced and CUL3A-dependent proteolysis of FRI modulate flowering in response to vernalization.
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100101, China huxiangyang@mail.kib.ac.cn.
authors.forename: Xiangyang
authors.identifier: http://orcid.org/0000-0002-6830-2107
authors.initials: X
authors.lastname: Hu
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100101, China.
authors.forename: Xiangxiang
authors.initials: X
authors.lastname: Kong
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100101, China.
authors.forename: Chuntao
authors.initials: C
authors.lastname: Wang
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China University of the Chinese Academy of Sciences, Beijing 100049, China.
authors.forename: Lan
authors.initials: L
authors.lastname: Ma
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China University of the Chinese Academy of Sciences, Beijing 100049, China.
authors.forename: Jinjie
authors.initials: J
authors.lastname: Zhao
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China University of the Chinese Academy of Sciences, Beijing 100049, China.
authors.forename: Jingjing
authors.initials: J
authors.lastname: Wei
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China University of the Chinese Academy of Sciences, Beijing 100049, China.
authors.forename: Xiaoming
authors.initials: X
authors.lastname: Zhang
authors.affiliation: School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JR, United Kingdom.
authors.forename: Gary J
authors.initials: GJ
authors.lastname: Loake
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China.
authors.forename: Ticao
authors.initials: T
authors.lastname: Zhang
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China Department of Biology, East Carolina University, Greenville, North Carolina 27858.
authors.forename: Jinling
authors.initials: J
authors.lastname: Huang
authors.affiliation: Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100101, China.
authors.forename: Yongping
authors.initials: Y
authors.lastname: Yang
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D002352:Carrier Proteins / Q000378:metabolism; D044842:Cullin Proteins; D035264:Flowers / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D009687:Nuclear Proteins / Q000378:metabolism; D046988:Proteasome Endopeptidase Complex / Q000378:metabolism / Q000502:physiology*; D059748:Proteolysis; D013312:Stress, Physiological / Q000235:genetics; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D054875:Ubiquitination
chemical_list: C500789:AT1G26830 protein, Arabidopsis; D029681:Arabidopsis Proteins; D002352:Carrier Proteins; D044842:Cullin Proteins; C414613:FRI protein, Arabidopsis; C000588971:LRB1 protein, Arabidopsis; C000588972:LRB2 protein, Arabidopsis; D009687:Nuclear Proteins; D014157:Transcription Factors; C552478:WRKY34 protein, Arabidopsis; D046988:Proteasome Endopeptidase Complex