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      BRASSINOSTEROID INSENSITIVE2 negatively regulates cellulose synthesis in Arabidopsis by phosphorylating cellulose synthase 1

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          Significance

          Cellulose is the most abundant biopolymer on Earth and is a critical component for plants to grow and develop. Cellulose is synthesized by large cellulose synthase complexes containing multiple cellulose synthase A (CESA) subunits; however, how cellulose synthesis is regulated remains unclear. In this study, we identify BRASSINOSTEROID INSENSITIVE2 (BIN2) as a protein kinase that directly phosphorylates Arabidopsis CESA1 and further demonstrate that this phosphorylation event negatively regulates CESA activity, and thus cellulose biosynthesis, in Arabidopsis. Therefore, this study provides a clear link between cell wall biosynthesis and hormonal signal transduction pathways that regulate plant growth and development.

          Abstract

          The deposition of cellulose is a defining aspect of plant growth and development, but regulation of this process is poorly understood. Here, we demonstrate that the protein kinase BRASSINOSTEROID INSENSITIVE2 (BIN2), a key negative regulator of brassinosteroid (BR) signaling, can phosphorylate Arabidopsis cellulose synthase A1 (CESA1), a subunit of the primary cell wall cellulose synthase complex, and thereby negatively regulate cellulose biosynthesis. Accordingly, point mutations of the BIN2-mediated CESA1 phosphorylation site abolished BIN2-dependent regulation of cellulose synthase activity. Hence, we have uncovered a mechanism for how BR signaling can modulate cellulose synthesis in plants.

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          Most cited references 47

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          Modular cloning in plant cells.

          New plant genes are being discovered at a rapid pace. Yet, in most cases, their precise function remains elusive. The recent advent of recombinational cloning techniques has significantly improved our ability to investigate gene functions systematically. For example, proteins fused with diverse fluorescent tags can be expressed at will using versatile cloning cassettes. In addition, novel binary T-DNA vectors are now available to assemble multiple DNA fragments simultaneously, which greatly facilitate plant cell and protein engineering.
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            Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets.

            Coexpression patterns of gene expression across many microarray data sets may reveal networks of genes involved in linked processes. To identify factors involved in cellulose biosynthesis, we used a regression method to analyze 408 publicly available Affymetrix Arabidopsis microarrays. Expression of genes previously implicated in cellulose synthesis, as well as several uncharacterized genes, was highly coregulated with expression of cellulose synthase (CESA) genes. Four candidate genes, which were coexpressed with CESA genes implicated in secondary cell wall synthesis, were investigated by mutant analysis. Two mutants exhibited irregular xylem phenotypes similar to those observed in mutants with defects in secondary cellulose synthesis and were designated irx8 and irx13. Thus, the general approach developed here is useful for identification of elements of multicomponent processes.
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              A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development.

              Brassinosteroids are widely distributed plant compounds that modulate cell elongation and division, but little is known about the mechanism of action of these plant growth regulators. To investigate brassinosteroids as signals influencing plant growth and development, we identified a brassinosteroid-insensitive mutant in Arabidopsis thaliana (L.) Henyh. ecotype Columbia. The mutant, termed bri1, did not respond to brassinosteroids in hypocotyl elongation and primary root inhibition assays, but it did retain sensitivity to auxins, cytokinins, ethylene, abscisic acid, and gibberellins. The bri1 mutant showed multiple deficiencies in developmental pathways that could not be rescued by brassinosteroid treatment including a severely dwarfed stature; dark green, thickened leaves; males sterility; reduced apical dominance; and de-etiolation of dark-grown seedlings. Genetic analysis suggests that the Bri1 phenotype is caused by a recessive mutation in a single gene with pleiotropic effects that maps 1.6 centimorgans from the cleaved, amplified, polymorphic sequence marker DHS1 on the bottom of chromosome IV. The multiple and dramatic effects of mutation of the BRI1 locus on development suggests that the BRI1 gene may play a critical role in brassinosteroid perception or signal transduction.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                28 March 2017
                13 March 2017
                : 114
                : 13
                : 3533-3538
                Affiliations
                aDepartment of Biology, Eidgenössiche Technische Hochschule Zurich , 8092 Zurich, Switzerland;
                bDepartment of Biochemistry and Molecular Biology, University of Nevada , Reno, NV 89557;
                cSchool of Biosciences, University of Melbourne , Parkville 3010, VIC, Australia;
                dEnergy Biosciences Institute, University of California, Berkeley , CA 94720
                Author notes
                2To whom correspondence may be addressed. Email: crs@ 123456berkeley.edu , staffan.persson@ 123456unimelb.edu.au , or iwallace@ 123456unr.edu .

                Contributed by Chris R. Somerville, February 12, 2017 (sent for review September 7, 2016; reviewed by Steve C. Huber and Simon R. Turner)

                Author contributions: C.S.-R., R.S., C.R.S., S.P., and I.S.W. designed research; C.S.-R., K.K., R.S., J.A.V., and I.S.W. performed research; I.S.W. contributed new reagents/analytic tools; C.S.-R., K.K., R.S., J.A.V., C.R.S., S.P., and I.S.W. analyzed data; and C.S.-R., K.K., R.S., C.R.S., S.P., and I.S.W. wrote the paper.

                Reviewers: S.C.H., University of Illinois; and S.R.T., University of Manchester.

                1C.S.-R. and K.K. contributed equally to this work.

                3S.P. and I.S.W. contributed equally to this work.

                Article
                PMC5380027 PMC5380027 5380027 201615005
                10.1073/pnas.1615005114
                5380027
                28289192
                Page count
                Pages: 6
                Funding
                Funded by: Max-Planck-Gesellschaft (Max Planck Society) 501100004189
                Award ID: n/a
                Funded by: Energy Biosciences Institute
                Award ID: n/a
                Funded by: Philomathia Foundation
                Award ID: n/a
                Funded by: University of Melbourne 501100001782
                Award ID: n/a
                Funded by: University of Nevada Reno
                Award ID: n/a
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: IOS 1449068
                Funded by: Nevada Agricultural Experiment Station
                Award ID: NEV00382
                Categories
                Biological Sciences
                Plant Biology

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