Planta

, Volume 237, Issue 6, pp 1585–1597 | Cite as

An integrative analysis of four CESA isoforms specific for fiber cellulose production between Gossypium hirsutum and Gossypium barbadense

  • Ao Li
  • Tao Xia
  • Wen Xu
  • Tingting Chen
  • Xianliang Li
  • Jian Fan
  • Ruyi Wang
  • Shengqiu Feng
  • Yanting Wang
  • Bingrui Wang
  • Liangcai Peng
Original Article

Abstract

Cotton fiber is an excellent model system of cellulose biosynthesis; however, it has not been widely studied due to the lack of information about the cellulose synthase (CESA) family of genes in cotton. In this study, we initially identified six full-length CESA genes designated as GhCESA5–GhCESA10. Phylogenetic analysis and gene co-expression profiling revealed that CESA1, CESA2, CESA7, and CESA8 were the major isoforms for secondary cell wall biosynthesis, whereas CESA3, CESA5, CESA6, CESA9, and CESA10 should involve in primary cell wall formation for cotton fiber initiation and elongation. Using integrative analysis of gene expression patterns, CESA protein levels, and cellulose biosynthesis in vivo, we detected that CESA8 could play an enhancing role for rapid and massive cellulose accumulation in Gossypium hirsutum and Gossypium barbadense. We found that CESA2 displayed a major expression in non-fiber tissues and that CESA1, a housekeeping gene like, was predominantly expressed in all tissues. Further, a dynamic alteration was observed in cell wall composition and a significant discrepancy was observed between the cotton species during fiber elongation, suggesting that pectin accumulation and xyloglucan reduction might contribute to cell wall transition. In addition, we discussed that callose synthesis might be regulated in vivo for massive cellulose production during active secondary cell wall biosynthesis in cotton fibers.

Keywords

Cellulose CESA Cotton fiber Secondary cell wall biosynthesis 

Abbreviations

CalS

Callose synthase

CESA

Cellulose synthase

CrI

Crystalline index

CSC

Cellulose synthase complex

DP

Degree of polymerization

EST

Expression sequence tag

Gb

Gossypium barbadense

Gh

Gossypium hirsutum

Kor

Korrigan

RACE

Rapid-amplification of cDNA ends

SGT

Sterol glycosyltransferase

UBQ

Ubiquitin

Supplementary material

425_2013_1868_MOESM1_ESM.pdf (1.2 mb)
Supplementary material 1 (PDF 1193 kb)

References

  1. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 92:9353–9357PubMedCrossRefGoogle Scholar
  2. 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 11:287–299CrossRefGoogle Scholar
  3. 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 RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720PubMedCrossRefGoogle Scholar
  4. Basra A, Malik CP (1984) Development of the cotton fiber. Int Rev Cytol 89:65–113CrossRefGoogle Scholar
  5. Blakeney AB, Harris PJ, Henry RJ, Stone BA (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr Res 113:291CrossRefGoogle Scholar
  6. Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484PubMedCrossRefGoogle Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  8. Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236PubMedCrossRefGoogle Scholar
  9. Carroll A, Somerville C (2009) Cellulosic biofuels. Annu Rev Plant Biol 60:165–182PubMedCrossRefGoogle Scholar
  10. Chaudhary B, Hovav R, Rapp R, Verma N, Udall JA, Wendela JF (2008) Global analysis of gene expression in cotton fibers from wild and domesticated Gossypium barbadense. Evol Dev 10:567–582PubMedCrossRefGoogle Scholar
  11. Chen F, Duran AL, Blount JW, Sumner LW, Dixon RA (2003) Profiling phenolic metabolites in transgenic alfalfa modified in lignin biosynthesis. Phytochemistry 64:1013PubMedCrossRefGoogle Scholar
  12. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedCrossRefGoogle Scholar
  13. Cui X, Shin H, Song C, Laosinchai W, Amano Y, Brown RM Jr (2001) A putative plant homolog of the yeast (1 → 3)-β-glucan synthase subunit FKS1 from cotton (Gossypium hirsutum L.) fibers. Planta 213:223–230PubMedCrossRefGoogle Scholar
  14. Dische Z (1962) Color reactions of carbohydrates. In: Whistler RL, Wolfrom ML (eds) Methods in carbohydrate chemistry, vol 1. Academic Press, New York, pp 477–512Google Scholar
  15. Djerbi S, Aspeborg H, Nilsson P, Mellerowicz E, Sundberg B, Blomqvist K, Teeri TT (2004) Identification and expression analysis of genes encoding putative cellulose synthases (CesA) in the hybrid aspen, Populus tremula (L.) × P tremuloides (Michx.). Cellulose 11:301–312CrossRefGoogle Scholar
  16. Djerbi S, Lindskog M, Arvestad L, Sterky F, Teeri TT (2005) The genome sequence of black cotton wood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes. Planta 221:739–746PubMedCrossRefGoogle Scholar
  17. Doblin MS, De Melis L, Newbigin E, Bacic A, Read SM (2001) Pollen tubes of Nicotiana alata express two genes from different β-glucan synthase families. Plant Physiol 125:2040–2052PubMedCrossRefGoogle Scholar
  18. Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43:1407–1420 PubMedCrossRefGoogle Scholar
  19. 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 12:2409–2423PubMedGoogle Scholar
  20. Frohman MA, Dushand MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligo nucleotide primer. Proc Natl Acad Sci USA 85:8998–9002PubMedCrossRefGoogle Scholar
  21. Fry SC (1988) The growing plant cell wall: chemical and metabolic analysis. Longman, LondonGoogle Scholar
  22. Ghazi YA, Bourot S, Arioli T, Dennis ES, Llewellyn DJ (2009) Transcript profiling during fiber development identifies pathways in secondary metabolism and cell wall structure that may contribute to cotton fiber quality. Plant Cell Physiol 50:1364–1381CrossRefGoogle Scholar
  23. Goldberg R, Morvan C, Jauneau A, Jarvis MC (1996) Methyl-esterification, de-esterification and gelation of pectins in the primary cell wall. In: Visser J, Voragen AFG (eds) Pectins and pectinases. Elsevier, Amsterdam, pp 151–172CrossRefGoogle Scholar
  24. Grover CE, Kim HR, Wing RA, Paterson AH, Wendel JF (2004) Incongruent patterns of local and global genome size evolution in cotton. Genome Res 14:1474–1482PubMedCrossRefGoogle Scholar
  25. Haigler CH, Zhang DS, Wilkerson CG (2005) Biotechnological improvement of cotton fibre maturity. Physiol Plant 124:285–294CrossRefGoogle Scholar
  26. Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168CrossRefGoogle Scholar
  27. Hayashi T, Delmer DP (1988) Xyloglucan in the cell walls of cotton fiber. Carbohydr Res 181:273–277CrossRefGoogle Scholar
  28. Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1323PubMedCrossRefGoogle Scholar
  29. Hong Z, Delauney AJ, Verma DPS (2001) A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell 13:755–768PubMedGoogle Scholar
  30. Hu XP, Hsieh YL (1997) Crystalline structure of developing cotton fibers. J Polym Sci Pol Phys 34:1451–1459CrossRefGoogle Scholar
  31. Ji SJ, Lu YC, Feng JX, Wei G, Li J, Shi YH, Fu Q, Liu D, Luo JC, Zhu YX (2003) Isolation and analyses of genes preferentially expressed during early cotton fiber development by subtractive PCR and cDNA array. Nucleic Acids Res 31:2534–2543PubMedCrossRefGoogle Scholar
  32. Kim HJ, Triplett BA (2001) Cotton fiber growth in planta and in vitro: models for plant cell elongation and cell wall biogenesis. Plant Physiol 127:1361–1366PubMedCrossRefGoogle Scholar
  33. Kim HJ, Triplett BA, Zhang HB, Lee MK, Hinchliffe DJ, Li P, Fang DD (2012) Cloning and characterization of homeologous cellulose synthase catalytic subunit 2 genes from allotetraploid cotton (Gossypium hirsutum L.). Gene 494:181–189PubMedCrossRefGoogle Scholar
  34. Kudlicka K, Brown RM Jr (1997) Cellulose and callose biosynthesis in higher plants. Solubilization and separation of (1 → 3)- and (1 → 4)-beta-glucan synthase activities from mung bean. Plant Physiol 115:643–656PubMedCrossRefGoogle Scholar
  35. Lane DR, Wiedemeier A, Peng LC, Höfte H, Vernhettes S, Desprez T, Hocart CH, Birch RJ, Baskin TI, Burn JE, Arioli T, Betzner AS, Williamson RE (2001) Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol 126:278–288PubMedCrossRefGoogle Scholar
  36. Laosinchai W, Cui X, Brown RM Jr (2000) A full length cDNA of cotton cellulose synthase has high homology with the Arabidopsis rsw1 gene and the cotton Cel1 gene. Plant Physiol 122:291CrossRefGoogle Scholar
  37. Lee JJ, Woodward AW, Jeffery CZ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot-Lond 100:1391–1401CrossRefGoogle Scholar
  38. Lee J, Burns TH, Light G, Sun Y, Fokar M, Kasukabe Y, Fujisawa K, Maekawa Y, Allen RD (2010) Xyloglucan endotransglycosylase/hydrolase genes in cotton and their role in fiber elongation. Planta 232:1191–1205PubMedCrossRefGoogle Scholar
  39. Lin ZX, Wang Y, Zhang XL, Zhang JF (2012) Functional markers for cellulose synthase and their comparison to SSRs in cotton. Plant Mol Biol Rep 30:1270–1275CrossRefGoogle Scholar
  40. Maltby D, Carpita NC, Montezinos D, Kulow C, Delmer DP (1979) β-1, 3-Glucan in developing cotton fibers. Plant Physiol 63:1158–1164PubMedCrossRefGoogle Scholar
  41. Meinert MC, Delmer DP (1977) Changes in biochemical composition of the cell wall in cotton fiber during development. Plant Physiol 59:1088–1097PubMedCrossRefGoogle Scholar
  42. Mutwil M, Obro J, Willats WG, Persson S (2008) Gene CAT—novel web tools that combine BLAST and co-expression analyses. Nucleic Acids Res 36(Web server Issue):W320–W326PubMedCrossRefGoogle Scholar
  43. 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 14:2001–2013PubMedCrossRefGoogle Scholar
  44. Pang CY, Wang H, Pang Y, Xu C, Jiao Y, Qin YM, Western TL, Yu SX, Zhu YX (2010) Comparative proteomics indicates that biosynthesis of pectic precursors is important for cotton fiber and Arabidopsis root hair elongation. Mol Cell Proteomics 9:2019–2033PubMedCrossRefGoogle Scholar
  45. 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 93:12637–12642PubMedCrossRefGoogle Scholar
  46. Peng LC, 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 211:406–414PubMedCrossRefGoogle Scholar
  47. Peng LC, Kawagoe Y, Hogan P, Delmer DP (2002) Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science 295:147–150PubMedCrossRefGoogle Scholar
  48. Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA 104:15566–15571PubMedCrossRefGoogle Scholar
  49. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GHH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfeya PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763PubMedCrossRefGoogle Scholar
  50. Ruan YL, Chourey PS (1998) A fiberless seed mutation in cotton is associated with lack of fiber cell initiation in ovule epidermis and alterations in sucrose synthase expression and carbon partitioning in developing seeds. Plant Physiol 118:399–406PubMedCrossRefGoogle Scholar
  51. Ryser U (1985) Cell wall biosynthesis in differentiating cotton fibres. Eur J Cell Biol 39:236–256Google Scholar
  52. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedCrossRefGoogle Scholar
  53. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78PubMedCrossRefGoogle Scholar
  54. Song DL, Shen JH, Li LG (2010) Characterization of cellulose synthase complexes in Populus xylem differentiation. New Phytol 187:777–790PubMedCrossRefGoogle Scholar
  55. 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 133:73–83PubMedCrossRefGoogle Scholar
  56. 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 11:769–780PubMedGoogle Scholar
  57. Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2540PubMedGoogle Scholar
  58. 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 100:1450–1455PubMedCrossRefGoogle Scholar
  59. Timpa JD, Triplett BA (1993) Analysis of cell-wall polymers during cotton fiber development. Planta 189:101–108CrossRefGoogle Scholar
  60. Triplett BA, Kim HJ (2006) Using cotton fiber development to discover how plant cells grow. In: Hayashi T (ed) The science and lore of the plant cell wall. Florida, Boca Raton, p 367Google Scholar
  61. Vaughn KC, Turley RB (1999) The primary walls of cotton fibers contain an ensheathing pectin layer. Protoplasma 209:226–237CrossRefGoogle Scholar
  62. Wang LQ, Guo K, Li Y, Tu YY, Hu HZ, Wang BR, Cui XC, Peng LC (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10:282–297PubMedCrossRefGoogle Scholar
  63. Wu YT, Liu JY (2004) A modified hot borate method for efficient isolation of total RNA from different cotton tissues. Cotton Sci 16:67–71Google Scholar
  64. Xie GS, Yang B, Xu ZD, Li FC, Guo K, Zhang ML, Wang LQ, Zou WH, Wang YT, Peng LC (2013) Global identification of multiple OsGH9 family members and their involvement in cellulose crystallinity modification in rice. PLoS One 8:e50171PubMedCrossRefGoogle Scholar
  65. Xu N, Zhang W, Ren SF, Liu F, Zhao CQ, Liao HF, Xu ZD, Huang JF, Li Q, Tu YY, Yu B, Wang YT, Jiang JX, Qin JP, Peng LC (2012) Hemicelluloses negatively affect lignocellulose crystallinity for high biomass digestibility under NaOH and H2SO4 pretreatments in Miscanthus. Biotechnol Biofuels 5:58PubMedCrossRefGoogle Scholar
  66. Zhu HY, Han XY, Lv JH, Zhao L, Xu XY, Zhang TZ, Guo WZ (2011) Structure, expression differentiation and evolution of duplicated fiber developmental genes in Gossypium barbadense and G. hirsutum. BMC Plant Biol 11:40–54PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Ao Li
    • 1
    • 2
    • 3
  • Tao Xia
    • 1
    • 2
    • 4
  • Wen Xu
    • 1
    • 2
    • 4
  • Tingting Chen
    • 1
    • 2
    • 4
  • Xianliang Li
    • 1
    • 2
    • 3
  • Jian Fan
    • 1
    • 2
    • 3
  • Ruyi Wang
    • 1
    • 2
    • 3
  • Shengqiu Feng
    • 1
    • 2
    • 3
  • Yanting Wang
    • 1
    • 2
    • 3
  • Bingrui Wang
    • 3
  • Liangcai Peng
    • 1
    • 2
    • 3
    • 4
  1. 1.National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research (Wuhan)Huazhong Agricultural UniversityWuhanChina
  2. 2.Biomass and Bioenergy Research CentreHuazhong Agricultural UniversityWuhanChina
  3. 3.College of Plant Science and TechnologyHuazhong Agricultural UniversityWuhanChina
  4. 4.College of Life Science and TechnologyHuazhong Agricultural UniversityWuhanChina

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