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A missense mutation in the transmembrane domain of CESA4 affects protein abundance in the plasma membrane and results in abnormal cell wall biosynthesis in rice

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Abstract

Cellulose synthase (CESA) is a critical catalytic subunit of the cellulose synthase complex responsible for glucan chain elongation. Our knowledge about how CESA functions is still very limited. Here, we report the functional characterization of a rice mutant, brittle culm11, that shows growth retardation and dramatically reduced plant strength. Map-based cloning revealed that all the mutant phenotypes result from a missense mutation in OsCESA4 (G858R), a highly conserved residue at the end of the fifth transmembrane domain. The aberrant secondary cell wall of the mutant plants is attributed to significantly reduced cellulose content, abnormal secondary wall structure of sclerenchyma cells, and overall altered wall composition, as detected by chemical analyses and immunochemical staining. Importantly, we have found that this point mutation decreases the abundance of OsCESA4 in the plasma membrane, probably due to a defect in the process of CESA complex secretion. The data from our biochemical, genetic, and pharmacological analyses indicate that this residue is critical for maintaining the normal level of CESA proteins in the plasma membrane.

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References

  • Appenzeller L, Doblin M, Barreiro R, Wang HY, Niu XM, Kollipara K, Carrigan L, Tomes D, Chapman M, Dhugga KS (2004) Cellulose synthesis in maize: isolation and expression analysis of the cellulose synthase (CesA) gene family. Cellulose 11:287–299

    Article  CAS  Google Scholar 

  • Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Hofte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720

    Article  CAS  PubMed  Google Scholar 

  • Atanassov II, Pittman JK, Turner SR (2009) Elucidating the mechanisms of assembly and subunit-interaction of the cellulose synthase complex of Arabidopsis secondary cell walls. J Biol Chem 284:3833–3841

    Article  CAS  PubMed  Google Scholar 

  • Bosca S, Barton CJ, Taylor NG, Ryden P, Neumetzler L, Pauly M, Roberts K, Seifert GJ (2006) Interactions between MUR10/CesA7-dependent secondary cellulose biosynthesis and primary cell wall structure. Plant Physiol 142:1353–1363

    Article  CAS  PubMed  Google Scholar 

  • Burn JE, Hocart CH, Birch RJ, Cork AC, Williamson RE (2002) Functional analysis of the cellulose synthase genes CesA1, CesA2, and CesA3 in Arabidopsis. Plant Physiol 129:797–807

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu JK, Gong Z (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 43:273–283

    Article  CAS  PubMed  Google Scholar 

  • Chu Z, Chen H, Zhang Y, Zhang Z, Zheng N, Yin B, Yan H, Zhu L, Zhao X, Yuan M, Zhang X, Xie Q (2007) Knockout of the AtCESA2 gene affects microtubule orientation and causes abnormal cell expansion in Arabidopsis. Plant Physiol 143:213–224

    Article  CAS  PubMed  Google Scholar 

  • Curran AR, Engelman DM (2003) Sequence motifs, polar interactions and conformational changes in helical membrane proteins. Curr Opin Struct Biol 13:412–417

    Article  CAS  PubMed  Google Scholar 

  • Darley CP, Forrester AM, McQueen-Mason SJ (2001) The molecular basis of plant cell wall extension. Plant Mol Biol 47:179–195

    Article  CAS  PubMed  Google Scholar 

  • DeBolt S, Gutierrez R, Ehrhardt DW, Somerville C (2007) Nonmotile cellulose synthase subunits repeatedly accumulate within localized regions at the plasma membrane in Arabidopsis hypocotyl cells following 2, 6-dichlorobenzonitrile treatment. Plant Physiol 145:334–338

    Article  CAS  PubMed  Google Scholar 

  • Delmer DP, Read SM, Cooper G (1987) Identification of a receptor protein in cotton fibers for the herbicide 2, 6-dichlorobenzonitrile. Plant Physiol 84:415–420

    Article  CAS  PubMed  Google Scholar 

  • Desprez T, Vernhettes S, Fagard M, Refregier G, Desnos T, Aletti E, Py N, Pelletier S, Hofte H (2002) Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiol 128:482–490

    Article  CAS  PubMed  Google Scholar 

  • Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Hofte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:15572–15577

    Article  CAS  PubMed  Google Scholar 

  • Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43:1407–1420

    Article  CAS  PubMed  Google Scholar 

  • Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566

    Article  CAS  PubMed  Google Scholar 

  • Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Hofte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2424

    Article  CAS  PubMed  Google Scholar 

  • Farrokhi N, Burton RA, Brownfield L, Hrmova M, Wilson SM, Bacic A, Fincher GB (2006) Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotech J 4:145–167

    Article  CAS  Google Scholar 

  • Filisetti-Cozzi TM, Carpita NC (1991) Measurement of uronic acids without interference from neutral sugars. Anal Biochem 197:157–162

    Article  CAS  PubMed  Google Scholar 

  • Gillmor CS, Lukowitz W, Brininstool G, Sedbrook JC, Hamann T, Poindexter P, Somerville C (2005) Glycosylphosphatidylinositol-anchored proteins are required for cell wall synthesis and morphogenesis in Arabidopsis. Plant Cell 17:1128–1140

    Article  CAS  PubMed  Google Scholar 

  • Ha HK, Park KB, Kim PN, Lee M, Hong WS, Yang S, Lee SK, Kim MH, Suh DJ, Min YI, Auh YH (1998) Use of methylcellulose in small bowel follow-through examination: comparison with conventional series in normal subjects. Abdom Imaging 23:281–285

    Article  CAS  PubMed  Google Scholar 

  • Herth W (1987) Effects of 2, 6-DCB on plasma membrane rosettes of wheat root cells. Naturwissenschaften 74:556–557

    Article  CAS  Google Scholar 

  • Hoebler C, Barry LD, Delort-Laval J (1989) Rapid hydrolysis of plant cell wall polysaccharides by gas-liquid chromatography. J Agric Food Chem 37:360–367

    Article  CAS  Google Scholar 

  • Javadpour MM, Eilers M, Groesbeek M, Smith SO (1999) Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys J 77:1609–1618

    Article  CAS  PubMed  Google Scholar 

  • Johansen JN, Vernhettes S, Hofte H (2006) The ins and outs of plant cell walls. Curr Opin Plant Biol 9:616–620

    Article  CAS  PubMed  Google Scholar 

  • Joshi CP, Mansfield SD (2007) The cellulose paradox—simple molecule, complex biosynthesis. Curr Opin Plant Biol 10:220–226

    Article  CAS  PubMed  Google Scholar 

  • Kimura S, Laosinchai W, Itoh T, Cui X, Linder CR, Brown RMJ (1999) Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11:2075–2086

    Article  CAS  PubMed  Google Scholar 

  • Kirk TK, Obst JR (1988) Lignin determination. Methods Enzymol 161:87–101

    Article  CAS  Google Scholar 

  • Knox JP, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181:512–521

    Article  CAS  Google Scholar 

  • Kurek I, Kawagoe Y, Jacob-Wilk D, Doblin M, Delmer D (2002) Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. Proc Natl Acad Sci USA 99:11109–11114

    Article  CAS  PubMed  Google Scholar 

  • Landolt-Marticorena C, Williams KA, Deber CM, Reithmeier RA (1993) Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins. J Mol Biol 229:602–608

    Article  CAS  PubMed  Google Scholar 

  • Lazzaro MD, Donohue JM, Soodavar FM (2003) Disruption of cellulose synthesis by isoxaben causes tip swelling and disorganizes cortical microtubules in elongating conifer pollen tubes. Protoplasma 220:201–207

    Article  CAS  PubMed  Google Scholar 

  • Lemmon MA, Treutlein HR, Adams PD, Brunger AT, Engelman DM (1994) A dimerization motif for transmembrane α-helices. Nat Struct Biol 1:157–163

    Article  CAS  PubMed  Google Scholar 

  • Lukowitz W, Nickle TC, Meinke DW, Last RL, Conklin PL, Somerville CR (2001) Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc Natl Acad Sci USA 98:2262–2267

    Article  CAS  PubMed  Google Scholar 

  • Maloof JN, Borevitz JO, Dabi T, Lutes J, Nehring RB, Redfern JL, Trainer GT, Wilson JM, Asami T, Berry CC, Weigel D, Chory J (2001) Natural variation in light sensitivity of Arabidopsis. Nat Genet 29:441–446

    Article  CAS  PubMed  Google Scholar 

  • Mutwil M, Debolt S, Persson S (2008) Cellulose synthesis: a complex complex. Curr Opin Plant Biol 11:252–257

    Article  CAS  PubMed  Google Scholar 

  • Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495

    Article  CAS  PubMed  Google Scholar 

  • Pauly M, Keegstra K (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J 54:559–568

    Article  CAS  PubMed  Google Scholar 

  • Pear JR, Kawagoe Y, Schreckengost WE, Delmer DP, Stalker DM (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci USA 93:12637–12642

    Article  CAS  PubMed  Google Scholar 

  • Persson S, Caffall KH, Freshour G, Hilley MT, Bauer S, Poindexter P, Hahn MG, Mohnen D, Somerville C (2007a) The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell 19:237–255

    Article  CAS  PubMed  Google Scholar 

  • Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville C (2007b) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA 104:15566–15571

    Article  CAS  PubMed  Google Scholar 

  • Scheible WR, Pauly M (2004) Glycosyltransferases and cell wall biosynthesis: novel players and insights. Curr Opin Plant Biol 7:285–295

    Article  CAS  PubMed  Google Scholar 

  • Scheible WR, Eshed R, Richmond T, Delmer D, Somerville C (2001) Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proc Natl Acad Sci USA 98:10079–10084

    Article  CAS  PubMed  Google Scholar 

  • Smallwood M, Yates EA, Willats WGT, Martin H, Knox JP (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459

    Article  CAS  Google Scholar 

  • Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78

    Article  CAS  PubMed  Google Scholar 

  • Somerville C (2007) Biofuels. Curr Biol 17:R115–R119

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Murata K, Yamazaki M, Onosato K, Miyao A, Hirochika H (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol 133:73–83

    Article  CAS  PubMed  Google Scholar 

  • Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2540

    Article  CAS  PubMed  Google Scholar 

  • Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci USA 100:1450–1455

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Howles PA, Cork AH, Birch RJ, Williamson RE (2006) Chimeric proteins suggest that the catalytic and/or C-terminal domains give CesA1 and CesA3 access to their specific sites in the cellulose synthase of primary walls. Plant Physiol 142:685–695

    Article  CAS  PubMed  Google Scholar 

  • Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D (2005) FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170:1197–1207

    Article  CAS  PubMed  Google Scholar 

  • Willats WG, Marcus SE, Knox JP (1998) Generation of monoclonal antibody specific to (1–5)-α-L-arabinan. Carbohydr Res 308:149–152

    Article  CAS  PubMed  Google Scholar 

  • Williamson R, Burn J, Birch R, Baskin T, Arioli T, Betzner A, Cork A (2001) Morphology of rsw1, a cellulose-deficient mutant of Arabidopsis thaliana. Protoplasma 215:116–127

    Article  CAS  PubMed  Google Scholar 

  • Yan C, Yan S, Zeng X, Zhang Z, Gu M (2007) Fine mapping and isolation of Bc7(t), allelic to OsCesA4. J Genet Genomics 34:1019–1027

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Morrison WHIII, Freshour GD, Hahn MG, Ye ZH (2003) Expression of a mutant form of cellulose synthase AtCesA7 causes dominant negative effect on cellulose biosynthesis. Plant Physiol 132:786–795

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Pena MJ, Zhou GK, Nairn CJ, Wood-Jones A, Richardson EA, Morrison WHIII, Darvill AG, York WS, Ye ZH (2005) Arabidopsis fragile fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell 17:3390–3408

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Li S, Qian Q, Zeng D, Zhang M, Guo L, Liu X, Zhang B, Deng L, Liu X, Luo G, Wang X, Li J (2009) BC10, a DUF266-containing and golgi-located type II membrane protein, is required for cell-wall biosynthesis in rice (Oryza sativa L.). Plant J 57:446–462

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Laigeng Li (Institute of Plant Physiology and Ecology, Chinese Academy of Sciences) and Chunming Liu (Institute of Botany, Chinese Academy of Sciences) for critical comments on the manuscript, Taihua Zhang (Institute of Mechanics, Chinese Academy of Sciences) for measurement of breaking force of rice plants, Hongjing Hao (Institute of Atomic Energy, Chinese Academy of Agricultural Sciences) for transmission electron microscopy examination, Xiangning Jiang (Beijing Forestry University) for sugar analysis by GC–MS, and Xiangyu Wen (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) for confocal microscope examination. Development and distribution of the antibodies (JIM5 and JIM7) were supported in part by NSF grants DBI-0421683 and RCN-0090281. This work was supported by the grant from the Ministry of Science and Technology of China (2006AA10A101) and by the knowledge innovation program of the Chinese Academy of Sciences (KSCX2-YW-G-033).

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Authors and Affiliations

  1. National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, 100101, Beijing, China

    Baocai Zhang, Lingwei Deng, Guangyan Xiong, Rui Li, Jiayang Li & Yihua Zhou

  2. State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, 310006, Hangzhou, China

    Qian Qian, Dali Zeng & Longbiao Guo

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  1. Baocai Zhang
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  2. Lingwei Deng
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  3. Qian Qian
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Correspondence to Yihua Zhou.

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Baocai Zhang, Lingwei Deng, and Qian Qian have contributed equally to this work.

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Zhang, B., Deng, L., Qian, Q. et al. A missense mutation in the transmembrane domain of CESA4 affects protein abundance in the plasma membrane and results in abnormal cell wall biosynthesis in rice. Plant Mol Biol 71, 509 (2009). https://doi.org/10.1007/s11103-009-9536-4

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