Sugar inhibits brassinosteroid signaling by enhancing BIN2 phosphorylation of BZR1
Sugar, light, and hormones are major signals regulating plant growth and development, however, the interactions among these signals are not fully understood at the molecular level. Recent studies showed that sugar promotes hypocotyl elongation by activating the brassinosteroid (BR) signaling pathway...
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| Published in | PLoS genetics Vol. 17; no. 5; p. e1009540 |
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| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
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United States
Public Library of Science
14.05.2021
Public Library of Science (PLoS) |
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| Abstract | Sugar, light, and hormones are major signals regulating plant growth and development, however, the interactions among these signals are not fully understood at the molecular level. Recent studies showed that sugar promotes hypocotyl elongation by activating the brassinosteroid (BR) signaling pathway after shifting Arabidopsis seedlings from light to extended darkness. Here, we show that sugar inhibits BR signaling in Arabidopsis seedlings grown under light. BR induction of hypocotyl elongation in seedlings grown under light is inhibited by increasing concentration of sucrose. The sugar inhibition of BR response is correlated with decreased effect of BR on the dephosphorylation of BZR1, the master transcription factor of the BR signaling pathway. This sugar effect is independent of the sugar sensors Hexokinase 1 (HXK1) and Target of Rapamycin (TOR), but requires the GSK3-like kinase Brassinosteroid-Insensitive 2 (BIN2), which is stabilized by sugar. Our study uncovers an inhibitory effect of sugar on BR signaling in plants grown under light, in contrast to its promotive effect in the dark. Such light-dependent sugar-BR crosstalk apparently contributes to optimal growth responses to photosynthate availability according to light-dark conditions. |
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| AbstractList | Sugar, light, and hormones are major signals regulating plant growth and development, however, the interactions among these signals are not fully understood at the molecular level. Recent studies showed that sugar promotes hypocotyl elongation by activating the brassinosteroid (BR) signaling pathway after shifting Arabidopsis seedlings from light to extended darkness. Here, we show that sugar inhibits BR signaling in Arabidopsis seedlings grown under light. BR induction of hypocotyl elongation in seedlings grown under light is inhibited by increasing concentration of sucrose. The sugar inhibition of BR response is correlated with decreased effect of BR on the dephosphorylation of BZR1, the master transcription factor of the BR signaling pathway. This sugar effect is independent of the sugar sensors Hexokinase 1 (HXK1) and Target of Rapamycin (TOR), but requires the GSK3-like kinase Brassinosteroid-Insensitive 2 (BIN2), which is stabilized by sugar. Our study uncovers an inhibitory effect of sugar on BR signaling in plants grown under light, in contrast to its promotive effect in the dark. Such light-dependent sugar-BR crosstalk apparently contributes to optimal growth responses to photosynthate availability according to light-dark conditions. Sugar, light, and hormones are major signals regulating plant growth and development, however, the interactions among these signals are not fully understood at the molecular level. Recent studies showed that sugar promotes hypocotyl elongation by activating the brassinosteroid (BR) signaling pathway after shifting Arabidopsis seedlings from light to extended darkness. Here, we show that sugar inhibits BR signaling in Arabidopsis seedlings grown under light. BR induction of hypocotyl elongation in seedlings grown under light is inhibited by increasing concentration of sucrose. The sugar inhibition of BR response is correlated with decreased effect of BR on the dephosphorylation of BZR1, the master transcription factor of the BR signaling pathway. This sugar effect is independent of the sugar sensors Hexokinase 1 (HXK1) and Target of Rapamycin (TOR), but requires the GSK3-like kinase Brassinosteroid-Insensitive 2 (BIN2), which is stabilized by sugar. Our study uncovers an inhibitory effect of sugar on BR signaling in plants grown under light, in contrast to its promotive effect in the dark. Such light-dependent sugar-BR crosstalk apparently contributes to optimal growth responses to photosynthate availability according to light-dark conditions. Genetic studies of the brassinosteroid (BR) deficient mutants revealed its essential role in seedling development in the dark, but subsequent studies showed no significant difference in BR level between seedlings grown under light and darkness. We recently observed that light does affect BR levels in Arabidopsis, but in a sugar dependent manner. In the dark, sugar increases BR level as well as BR sensitivity by stabilizing the steroid response factor BZR1 through the Target of Rapamycin (TOR) signaling pathway. However, the BR level is decreased by sugar under light and by darkness on sugar-free medium. These observations raised the question of how the combinations of light and sugar modulate BR signaling. We addressed this question using genetic physiological analyses and found interestingly that sugar inhibits brassinosteroid response in light-grown plants by stabilizing the glycogen synthase kinase 3 homolog BIN2 and attenuating the dephosphorylation of BZR1, but independently of TOR. Our results indicate that sugar acts through distinct pathways to promote and inhibit BR signaling in dark and light conditions. Our work illustrates an intricate three-way crosstalk whereby the combination of light and sugar signals modulate the brassinosteroid signaling pathway to optimize growth according to both environmental and metabolic conditions. Unphosphorylated BZR1 accumulates in the nucleus, where it recruits the TOPLESS family repressors to inhibit gene expression [20,21] and interacts with transcription factors of other hormonal and light signaling pathways to promote shoot cell elongation [8,22–24]. [...]after shifting light-grown Arabidopsis seedlings into darkness, the BR levels increased in seedlings grown on media containing sugar but decreased in those grown on sugar-free media, suggesting light-dependent effects of sugar on the BR pathway [2]. [...]we further tested how sugar affects BR responses under light conditions. S, sucrose; M, mannitol. https://doi.org/10.1371/journal.pgen.1009540.g001 Sucrose attenuates BR-induced dephosphorylation of BZR1 in light As BR promotes hypocotyl elongation through dephosphorylation of the BZR1 family transcription factors, we further examined whether sugar affects the phosphorylation status of BZR1. [...]sugar may inhibit dephosphorylation or degradation of phospho-BZR1 Unphosphorylated BZR1 accumulates in the nucleus, where it recruits the TOPLESS family repressors to inhibit gene expression [20,21] and interacts with transcription factors of other hormonal and light signaling pathways to promote shoot cell elongation [8,22–24]. [...]after shifting light-grown Arabidopsis seedlings into darkness, the BR levels increased in seedlings grown on media containing sugar but decreased in those grown on sugar-free media, suggesting light-dependent effects of sugar on the BR pathway [2]. [...]we further tested how sugar affects BR responses under light conditions. S, sucrose; M, mannitol. https://doi.org/10.1371/journal.pgen.1009540.g001 Sucrose attenuates BR-induced dephosphorylation of BZR1 in light As BR promotes hypocotyl elongation through dephosphorylation of the BZR1 family transcription factors, we further examined whether sugar affects the phosphorylation status of BZR1. [...]sugar may inhibit dephosphorylation or degradation of phospho-BZR1 |
| Audience | Academic |
| Author | Sun, Ying Wang, Wenfei Jiang, Xue Zhang, Zhenzhen Wang, Zhi-Yong |
| AuthorAffiliation | Peking University, CHINA 3 Hebei Key Laboratory of Molecular and Cellular Biology, Key Laboratory of Molecular and Cellular Biology of Ministry of Education, College of Life Science, Hebei Normal University, Hebei Collaboration Innovation Center for Cell Signaling, Shijiazhuang, China 1 College of Life Sciences, Fujian Agriculture and Forestry University (FAFU), Fuzhou, China 2 Department of Plant Biology, Carnegie Institution for Science, Stanford, California, United States of America |
| AuthorAffiliation_xml | – name: 3 Hebei Key Laboratory of Molecular and Cellular Biology, Key Laboratory of Molecular and Cellular Biology of Ministry of Education, College of Life Science, Hebei Normal University, Hebei Collaboration Innovation Center for Cell Signaling, Shijiazhuang, China – name: Peking University, CHINA – name: 1 College of Life Sciences, Fujian Agriculture and Forestry University (FAFU), Fuzhou, China – name: 2 Department of Plant Biology, Carnegie Institution for Science, Stanford, California, United States of America |
| Author_xml | – sequence: 1 givenname: Zhenzhen orcidid: 0000-0003-1617-8543 surname: Zhang fullname: Zhang, Zhenzhen organization: Department of Plant Biology, Carnegie Institution for Science, Stanford, California, United States of America – sequence: 2 givenname: Ying orcidid: 0000-0002-1444-5057 surname: Sun fullname: Sun, Ying organization: Hebei Key Laboratory of Molecular and Cellular Biology, Key Laboratory of Molecular and Cellular Biology of Ministry of Education, College of Life Science, Hebei Normal University, Hebei Collaboration Innovation Center for Cell Signaling, Shijiazhuang, China – sequence: 3 givenname: Xue surname: Jiang fullname: Jiang, Xue organization: College of Life Sciences, Fujian Agriculture and Forestry University (FAFU), Fuzhou, China – sequence: 4 givenname: Wenfei orcidid: 0000-0001-7053-6677 surname: Wang fullname: Wang, Wenfei organization: College of Life Sciences, Fujian Agriculture and Forestry University (FAFU), Fuzhou, China – sequence: 5 givenname: Zhi-Yong orcidid: 0000-0003-4602-3390 surname: Wang fullname: Wang, Zhi-Yong organization: Department of Plant Biology, Carnegie Institution for Science, Stanford, California, United States of America |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33989283$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2021 Public Library of Science 2021 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2021 Zhang et al 2021 Zhang et al |
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| Snippet | Sugar, light, and hormones are major signals regulating plant growth and development, however, the interactions among these signals are not fully understood at... Unphosphorylated BZR1 accumulates in the nucleus, where it recruits the TOPLESS family repressors to inhibit gene expression [20,21] and interacts with... |
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| SubjectTerms | Arabidopsis thaliana Biology and Life Sciences Carbohydrate metabolism Dephosphorylation Elongation Gene expression Hormones Kinases Light Mannitol Observations Phosphorylation Physical Sciences Physiological aspects Proteins Repressors Seedlings Signal transduction Steroid hormones Sucrose Sugar Transcription factors |
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| Title | Sugar inhibits brassinosteroid signaling by enhancing BIN2 phosphorylation of BZR1 |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/33989283 https://www.proquest.com/docview/2541857386/abstract/ https://search.proquest.com/docview/2528175637 https://pubmed.ncbi.nlm.nih.gov/PMC8153450 https://doaj.org/article/f11a874e9da6400c9dd9ae8cf4dbaf21 http://dx.doi.org/10.1371/journal.pgen.1009540 |
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