Skip to main content
SpringerLink
Log in

OsBC1L4 encodes a COBRA-like protein that affects cellulose synthesis in rice

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Plant morphogenesis is highly dependent on the regulation of cell division and expansion. The organization of the cellulose microfibrils in the cell wall is a key determinant of cell expansion. Previously, a dwarf mutant with fewer tillers, Osbc1l4 (Oryza sativa brittle culm 1 like 4), was identified by screening a rice T-DNA insertion mutant library. It is reported here that OsBC1L4 encodes a COBRA-like protein that exhibits typical structural features of a glycosylphosphatidylinositol-anchor protein. The T-DNA insertion in OsBC1L4 results in abnormal cell expansion. A decrease in cellulose content but the increase in pectin and starch contents was identified in Osbc1l4 mutants by measuring the content of wall components. OsBC1L4 was expressed in all tissues/organs examined, with a low level in leaves. OsBC1L4 protein is mainly located in the cell wall and plasma membrane. Correlation analysis indicated that the expression of OsBC1L4 was highly correlated to that of several primary wall-forming cellulose synthase genes (CESAs). Moreover, the expression level of several cellulose-related genes is increased in Osbc1l4 mutants, which suggests that a feedback mechanism may exist during cellulose synthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

BC1L:

BRITTLE CULM1-like

GPI:

Glycosylphosphatidylinositol

CSLF:

Cellulose synthase-like F gene

CCVS domain:

Cysteine-rich domain

RT–PCR:

Reverse transcription polymerase chain reaction

References

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

    Article  PubMed  CAS  Google Scholar 

  • Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222

    Article  PubMed  CAS  Google Scholar 

  • Bendtsen JD, Nielsen H, Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795

    Article  PubMed  Google Scholar 

  • Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschabacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70

    PubMed  CAS  Google Scholar 

  • Brady SM, Song S, Dhugga KS, Rafalski JA, Benfey PN (2007) Combining expression and comparative evolutionary analysis: the COBRA gene family. Plant Physiol 143:172–187

    Article  PubMed  CAS  Google Scholar 

  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005a) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295

    Article  PubMed  CAS  Google Scholar 

  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005b) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295

    Article  PubMed  CAS  Google Scholar 

  • Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004a) The CesA gene family of barley: quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236

    Article  PubMed  CAS  Google Scholar 

  • Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004b) The CesA gene family of barley: quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236

    Article  PubMed  CAS  Google Scholar 

  • Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB (2006a) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3; 1,4)-beta-D-glucans. Science 311:1940–1942

    Article  PubMed  CAS  Google Scholar 

  • Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB (2006b) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3; 1,4)-beta-D-glucans. Science 311:1940–1942

    Article  PubMed  CAS  Google Scholar 

  • Burton RA, Jobling SA, Harvey AJ, Shirley NJ, Mather DE, Bacic A, Fincher GB (2008) The genetics and transcriptional profiles of the cellulose synthase-like HvCslF gene family in barley. Plant Physiol 146:1821–1833

    Article  PubMed  CAS  Google Scholar 

  • Campbell MM, Sederoff RR (1996) Variation in lignin content and composition: mechanism of control and implications for the genetic improvement of plants. Plant Physiol 110:3–13

    PubMed  CAS  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  PubMed  CAS  Google Scholar 

  • Carpita N, McCann M (2000) The cell wall. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 52–108

    Google Scholar 

  • Ching A, Dhugga KS, Appenzeller L, Meeley B, Bourret TM, Howard RJ, Rafalski A (2006) Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchored protein that affects mechanical strength of maize tissues by altering the composition and structure of secondary cell. Planta 224:1174–1184

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (1997) Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell 9:1031–1041

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2001) Wall structure and wall loosening. A look backwards and forwards. Plant Physiol 125:131–134

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  PubMed  CAS  Google Scholar 

  • Crowell EF, Gonneau M, Vernhettes S, Höfte H (2010) Regulation of anisotropic cell expansion in higher plants. C R Biol 333:320–324

    Article  PubMed  CAS  Google Scholar 

  • Dai X, You C, Wang L, Chen G, Zhang Q, Wu C (2009) Molecular characterization, expression pattern, and function analysis of the OsBC1L family in rice. Plant Mol Biol 71:469–481

    Article  PubMed  CAS  Google Scholar 

  • Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Höfte 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  PubMed  CAS  Google Scholar 

  • Eisenhaber B, Bork P, Eisenhaber F (1998) Sequence properties of GPI-anchored proteins near the omega-site: constraints for the polypeptide binding site of the putative transamidase. Protein Eng 11:1155–1161

    Article  PubMed  CAS  Google Scholar 

  • Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2423

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Gough J, Karplus K, Hughey R, Chothia C (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313:903–919

    Article  PubMed  CAS  Google Scholar 

  • Hauser MT, Morikami A, Benfey PN (1995) Conditional root expansion mutants of Arabidopsis. Development 121:237–1252

    Google Scholar 

  • Hochholdinger F, Wen TJ, Zimmermann R, Chimot-Marolle P, e Silva O, Bruce W, Lamkey KR, Wienand U, Schnable PS (2008) The maize (Zea mays L.) roothairless 3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield. Plant J 54:888–898

    Article  PubMed  CAS  Google Scholar 

  • Höfte H, Staehelin LA (2000) Plant cells do it differently. Curr Opin Plant Biol 3:447–449

    Article  PubMed  Google Scholar 

  • Jones MA, Raymond MJ, Smirnoff N (2006) Analysis of the roothair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 45:83–100

    Article  PubMed  CAS  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 11:2075–2085

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kotilainen M, Helariutta Y, Mehto M, Pollanen E, Albert VA, Elomaa P, Teeri TH (1999) GEG participates in the regulation of cell and organ shape during corolla and carpel development in Gerbera hybrida. Plant Cell 11:1093–1104

    Article  PubMed  CAS  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  PubMed  CAS  Google Scholar 

  • Lane DR, Wiedemeier A, Peng L, Höfte H, Vernhettes S, Desprez T, Hocart CH, Birch RJ, Baskin TI, Burn JE et al (2001) Temperature sensitive alleles of RSW2 link the KORRIGAN endo-1, 4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol 126:278–288

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X et al (2003) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031

    Article  PubMed  CAS  Google Scholar 

  • Li X, Yang Y, Yao J, Chen G, Li X, Zhang Q, Wu C (2009) FLEXIBLE CULM 1 encoding a cinnamyl-alcohol dehydrogenase controls culm mechanical strength in rice. Plant Mol Biol 69:685–697

    Article  PubMed  CAS  Google Scholar 

  • Martin C, Bhatt K, Baumann K (2001) Shaping in plant cells. Curr Opin Plant Biol 4:540–549

    Article  PubMed  CAS  Google Scholar 

  • Mou Z, He Y, Dai Y, Liu X, Li J (2000) Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12:405–418

    Article  PubMed  CAS  Google Scholar 

  • Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H (1998) A plasma membrane-bound putative endo-1, 4-beta-d-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576

    Article  PubMed  CAS  Google Scholar 

  • Pagant S, Bichet A, Sugimoto K, Lerouxel O, Desprez T, McCann M, Lerouge P, Vernhettes S, Höfte H (2002) KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14:2001–2013

    Article  PubMed  CAS  Google Scholar 

  • Parker JS, Cavell AC, Dolan L, Roberts K, Grierson CS (2000) Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 12:1961–1974

    Article  PubMed  CAS  Google Scholar 

  • Peng L, Hocart CH, Redmond JW, Williamson RE (2000) Fractionation of carbohydrates in Arabidopsis root cell walls shows that three radial swelling loci are specifically involved in cellulose production. Planta 211:406–414

    Article  PubMed  CAS  Google Scholar 

  • Peng L, Kawagoe Y, Hogan P, Delmer D (2002) Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science 295:147–150

    Article  PubMed  CAS  Google Scholar 

  • Persson S, Wei H, Milne J, Page GP, Somerville CR (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102:8633–8638

    Article  PubMed  CAS  Google Scholar 

  • Roudier F, Schindelman G, DeSalle R, Benfey PN (2002) The COBRA family of putative GPI-anchored proteins in Arabidopsis: a new fellowship in expansion. Plant Physiol 130:538–548

    Article  PubMed  CAS  Google Scholar 

  • Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular lycosyl-phosphatidyl inositol anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763

    Article  PubMed  CAS  Google Scholar 

  • Sato S, Kato T, Kakegawa K, Ishii T, Liu YG, Awano T, Takabe K, Nishiyama Y, Kuga S, Sato S, Nakamura Y, Tabata S, Shibata D (2001) Role of the putative membrane-bound endo-1, 4-beta-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 42:251–263

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Suzuki R, Nishikubo N, Takenouchi S, Ito S, Nakano Y, Nakaba S, Sano Y, Funada R, Kajita S, Kitano H, Katayama Y (2010) Isolation of a novel cell wall architecture mutant of rice with defective Arabidopsis COBL4 ortholog BC1 required for regulated deposition of secondary cell wall components. Planta 232:257–270

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127

    Article  PubMed  CAS  Google Scholar 

  • Seifert GJ, Blaukopf C (2010) Irritable walls: the plant extracellular matrix and signaling. Plant Physiol 153:467–478

    Article  PubMed  CAS  Google Scholar 

  • Sindhu A, Langewisch T, Olek A, Multani DS, McCann MC, Vermerris W, Carpita NC, Johal G (2007) Maize Brittle stalk2 encodes a COBRA-like protein expressed in early organ development but required for tissue flexibility at maturity. Plant Physiol 145:1444–1459

    Article  PubMed  CAS  Google Scholar 

  • Smith LG (2003) Cytoskeletal control of plant cell shape: getting the fine points. Curr Opin Plant Biol 6:63–73

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Szyjanowicz PMJ, McKinnon I, Taylor NG, Gardiner J, Jarvis MC, Turner SR (2004) The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J 37:730–740

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Taylor NG, Scheible WR, Cutler S, Somerville CR, Turner SR (1999) The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11:769–779

    Article  PubMed  CAS  Google Scholar 

  • Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2539

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424

    Article  PubMed  CAS  Google Scholar 

  • Urbanowicz BR, Catalá C, Irwin D, Wilson DB, Ripoll DR, Rose JK (2007) A tomato endo-beta-1,4-glucanase, SlCel9C1, represents a distinct subclass with a new family of carbohydrate binding modules (CBM49). J Biol Chem 282:12066–12074

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, Zhang Q (2010) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61:752–766

    Article  PubMed  CAS  Google Scholar 

  • Wu C, Li X, Yuan W, Chen G, Kilian A, Li J, Xu C, Li X, Zhou D, Wang S, Zhang Q (2003) Development of enhancer trap lines for functional analysis of the rice genome. Plant J 35:418–427

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Guo D, Chang Y, You C, Li X, Dai X, Weng Q, Zhang J, Chen G, Li X et al (2007) Non-random distribution of T-DNA insertions at various levels of the genome hierarchy as revealed by analyzing 13804 T-DNA flanking sequences from an enhancer-trap mutant library. Plant J 49:947–959

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, He S, Cao Y, Chen T, Du B, Chu C, Zhang J, Chen S (2006) OsGLU1, a putative membrane-bound endo-1,4-beta-D-glucanase from rice, affects plant internode elongation. Plant Mol Biol 60:137–151

    Article  PubMed  CAS  Google Scholar 

  • Zuo J, Niu QW, Nishizawa N, Wu Y, Kost B, Chua NH (2000) KORRIGAN, an Arabidopsis endo-1,4-β-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12:1137–1152

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Drs. Liangcai Peng and J. Peter Etchells for critical comments on the manuscript. This research was supported by grants from the National Natural Science Foundation of China and the National Special Key Project of China on Functional Genomics of Major Plants and Animals.

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, 430070, Wuhan, China

    Xiaoxia Dai, Changjun You, Guoxing Chen, Xianghua Li, Qifa Zhang & Changyin Wu

Authors
  1. Xiaoxia Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Changjun You
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guoxing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianghua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qifa Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Changyin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Changyin Wu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 45 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dai, X., You, C., Chen, G. et al. OsBC1L4 encodes a COBRA-like protein that affects cellulose synthesis in rice. Plant Mol Biol 75, 333–345 (2011). https://doi.org/10.1007/s11103-011-9730-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-011-9730-z

Keywords

Search

Navigation