Cotton fiber: A powerful single-cell model for cell wall and cellulose research

Frontiers in Plant Science

Volumn 3, Issue MAY, 2012, Pages

  Haigler, Candace H ^a   Betancur, Lissete ^a   Stiff, Michael R ^a   Tuttle, John R ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Cellulose; Cotton fiber; Elongation; Gossypium; Pectin; Transition stage; Virus induced gene silencing; Xyloglucan

Indexed keywords

EID: 84871436735     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00104     Document Type: Review

References (77)

1. Abidi, N., Hequet, E., and Cabrales. L. (2010). Changes in sugar composition and cellulose content during the secondary cell wall biogenesis in cotton fibers. Cellulose 17, 153-160.
2. Ahn, J., Verma, R., Kim, M., Lee, J., Kim, Y., Bang, J., Reiter, W., and Pai, H. (2006). Depletion of UDP-d-apiose/UDP-d-xylose synthases results in Rhamnogalacturonan-II deficiency, cell wall thickening, and cell death in higher plants. J. Biol. Chem. 281, 13708-13716.
3. Al-Ghazi, Y., Bourot, S., Arioli, T., Dennis, E. S., and Llewellyn, D. J. (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, 1364-1381.
4. Amor, Y., Haigler, C. H., Johnson, S., Wainscott, M., and Delmer, D. P. (1995). A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc. Natl. Acad. Sci. U.S.A.92, 9353-9357.
5. An, C., Saha, S., Jenkins, J. N., Scheffler, B. E., Wilkins, T. A., and Stelly, D. M. (2007). Transcriptome profiling, sequence characterization, and SNP-based chromosomal assignment of the EXPANSIN genes in cotton. Mol. Genet. Genomics 279, 539-553.
6. Arioli, T., Peng, L., Betzner, A. S., Burn, J., Wittke, W., Herth, W., Camilleri, C., Höfte, H., Plazinski, J., Birch, R., Cork, A., Glover, J., Redmond, J., and Williamson, R. E. (1998). Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279, 717-720.
7. Arpat, A. B., Waugh, M., Sullivan, J. P., Gonzales, M., Frisch, D., Main, D., Wood, T., Leslie, A., Wing, R. A., and Wilkins, T. A. (2004). Functional genomics of cell elongation in developing cotton fibers. Plant Mol. Biol. 54, 911-929.
8. Atalla, R. H., and Vanderhart, D. L. (1984). Native cellulose: a composite of two distinct crystalline forms. Science223, 283-285.
9. Betancur, L., Singh, B., Rapp, R. A., Wendel, J. F., Marks, M. D., Roberts, A. W., and Haigler, C. H. (2010). Phylogenetically distinct cellulose synthase genes support secondary wall thickening in Arabidopsis shoot trichomes and cotton fiber. J. Integr. Plant Biol. 52, 205-220.
10. Bowling, A. J., Vaughn, K. C., and Turley, R. B. (2011). Polysaccharides and glycoprotein distribution in the epidermis of cotton ovules during early fiber initiation and growth. Protoplasma 248, 579-590.
11. Bowman, D. T., van Esbroeck, G. A., Van't Hof, J., and Jividen, G. M. (2001). Ovule fiber cell numbers in modern upland cottons. J. Cotton Sci. 5, 81-83.
12. Boyer, J. S. (2009). Cell wall biosynthesis and the molecular mechanism of plant enlargement. Funct. Plant Biol. 36, 383-394.
13. Brill, E., van Thournout, M., White, R. G., Llewellyn, D., Campbell, P. M., Engelen, S., Ruan, Y.-L., Arioli, T., and Furbank, R. T. (2011). A novel isoform of sucrose synthase is targeted to the cell wall during secondary cell wall synthesis in cotton fibre. Plant Physiol. 157, 40-54.
14. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., and Voinnet, O. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190.
15. Burton, R. A., Gibeaut, D. M., Bacic, A., Findlay, K., Roberts, K., Hamilton, A., Baulcombe, D. C., and Fincher, G. B. (2000). Virus-induced silencing of a plant cellulose synthase gene. Plant Cell 12, 691-706.
16. Chanzy, H., Imada, K., and Vuong, R. (1978). Electron diffraction from the primary walls of cotton fibers. Protoplasma 94, 299-306.
17. Chen, Z. J., Scheffler, B. E., Dennis, E., Triplett, B., Zhang, T., Chen, X., Stelly, D. M., Rabinowicz, P. D., Town, C., Arioli, T., Brubaker, C., Cantrell, R., Lacape, J.-M., Ulloa, M., Chee, P., Gingle, A. R., Haigler, C. H., Percy, R., Saha, S., Wilkins, T., Wright, R. J., Deynze, A. V., Zhu, Y., Yu, S., Guo, W., Abdurakhmonov, I., Katageri, I., Rahman, M., Zafar, Y., Yu, J. Z., Kohel, R. J., Wendel, J., and Paterson, A. H. (2007). Towards sequencing cotton (Gossypium) genomes. Plant Physiol. 145, 1303-1310.
18. Cosgrove, D. J. (2005). Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 6, 850-861.
19. Divya, K., Jami, S. K., and Kirti, P. B. (2010). Constitutive expression of mustard annexin, AnnBj1, enhances abiotic stress tolerance and fiber quality in cotton under stress. Plant Mol. Biol. 73, 293-308.
20. Eklöf, J. M., and Brumer, H. (2010). The XTH Gene Family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol. 153, 456-466.
21. Fu, D. Q., Zhu, B. Z., Zhu, H. L., Zhang, H. X., Xie, Y. H., Jiang, W. B., Zhao, X. D., and Luo, K. B. (2006). Enhancement of virus-induced gene silencing in tomato by low temperature and low humidity. Mol. Cells 21, 153-160.
22. Gao, X., Wheeler, T., Li, Z., Kenerley, C. M., He, P., and Shan, L. (2011). Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant J. 66, 293-305.
23. Guo, G.-Y., Wang, L.-J., Chen, S.-P., Hu, W.-L., and Chen, X.-Y. (2007). Gene expression and metabolite profiles of cotton fiber during cell elongation and secondary cell wall synthesis. Cell Res. 17, 422-434.
24. Haigler, C. H., Zhang, D., and Wilkerson, C. G. (2005). Biotechnological improvement of cotton fibre. Physiol. Plant.124:285-294.
25. Haigler, C. H., Singh, B., Zhang, D., Hwang, S., Wu, C., Cai, W. X., Hozain, M., Kang, W., Kiedaisch, B., Strauss, R. E., Hequet, E. F., Wyatt, B. G., Jividen, G. M., and Holaday, A. S. (2007). Transgenic cotton over-producing spinach sucrose phosphate synthase showed enhanced leaf sucrose synthesis and improved fiber quality under controlled environmental conditions. Plant Mol. Biol. 63, 815-832.
26. Haigler, C. H., Singh, B., Wang, G., and Zhang, D. (2009). "Genomics of cotton fiber secondary wall deposition and cellulose biogenesis, " in Genetics and Genomics of Cotton, ed. A. H. Paterson (New York: Springer), 385-417.
27. Harmer, S. E., Orford, S. J., and Timmis, J. N. (2002). Characterisation of six alpha-expansin genes in Gossypium hirsutum (upland cotton). Mol. Genet. Genomics 268, 1-9.
28. Hamilton, A. J., and Baulcombe, D. C. (1999). A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950-952.
29. Hinchliffe, D. J., Meredith, W. R., Delhorn, C. D., Thibodeaux, D. P., and Fang, D. D. (2011). Elevated growing degree days influence transition stage timing during cotton fiber development resulting in increased fiber-bundle strength. Crop Sci. 51, 1683-1692.
30. Hinchliffe, D. J., Meredith. W. R., Yeater, K. M., Kim, H. J., Woodward, A. W., Chen, Z. J., and Triplett, B. A. (2010). Near-isogenic cotton germplasm lines that differ in fiber-bundle strength have temporal differences in fiber gene expression patterns as revealed by comparative high-throughput profiling. Theor. Appl. Genet. 120, 1347-1366.
31. Hoffmann, L., Besseau, S., Geoffroy, P., Ritzenthaler, C., Meyer, D., Lapierre, C., Pollet, B., and Legrand, M. (2004). Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16, 1446-1465.
32. Hovav, R., Udall, J. A., Hovav, E., Rapp, R., Flagel, L., and Wendel, J. F. (2008). A majority of cotton genes are expressed in single-celled fiber. Planta 227, 319-329.
33. Hsieh, Y.-L., Honik, D. D., and Hartzell, M. M. (1995). A developmental study of single fiber strength: greenhouse grown SJ-2 Acala cotton. Text. Res. J. 65, 101-112.
34. Idris, A. M., Tuttle, J. R., Robertson, D., Haigler, C. H., and Brown, J. K. (2010). Differential cotton leaf crumple virus-VIGS-mediated gene silencing and viral genome localization in different Gossypium hirsutum genetic backgrounds. Physiol. Mol. Plant Pathol. 75, 13-22.
35. Kim, H. J., and Triplett, B. A. (2001). Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol. 127, 1361-1366.
36. Kumagai, M. H., Donson, J., della-Cioppa, G., Harvey, D., Hanley, K., and Grill, L. K. (1995). Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc. Natl. Acad. Sci. U.S.A. 92, 1679-1683.
37. Lee, J., Burns, T. H., Light, G., Sun, Y., Fokar, M., Kasukabe, Y., Fujisawa, K., Maekawa, Y., and Allen, R. D. (2010). Xyloglucan endotransglycosylase/hydrolase genes in cotton and their role in fiber elongation. Planta 232, 1191-1205.
38. Maltby, D., Carpita, N. C., Montezinos, D., Kulow, Y., and Delmer, D. P. (1979). Beta-1, 3-glucan in developing cotton fibers-structure, localization, and relationship of synthesis to that of secondary wall cellulose. Plant Physiol. 63, 1158-114.
39. Marks, M. D., Betancur, L, Gilding, E., Chen, F., Bauer, S., Wenger, J., Dixon, R. A., and Haigler, C. H. (2008). A new method for isolating large quantities of Arabidopsis trichomes for transcriptome, cell wall and other types of analyses. Plant J. 56, 483-492.
40. Martin, L. K., and Haigler, C. H. (2004). Cool temperature hinders flux from glucose to sucrose during cellulose synthesis in secondary wall stage cotton fibers. Cellulose 11, 339-349.
41. Meinert, M. C., and Delmer, D. P. (1977). Changes in biochemical composition of the cell wall of the cotton fiber during development. Plant Physiol. 59, 1088-1097.
42. Michailidis, G., Argiriou, A., Darzentas, N., and Tsaftaris, A. (2009). Analysis of xyloglucan endotransglycosylase/hydrolase (XTH) genes from allotetraploid (Gossypium hirsutum) cotton and its diploid progenitors expressed during fiber elongation. J. Plant Physiol. 166, 403-416.
43. Pang, C. Y., Wang, H., Pang, Y., Xu, C., Jiao, Y., Qin, Y. M., Western, T. L., Yu, S. X., and Zhu, Y. X. (2010). Comparative proteomics indicates that biosynthesis of pectic precursors is important for cotton fiber and Arabidopsis root hair elongation. Mol. Cell. Proteomics 9, 2019-2033.
44. Paredez, A. R., Somerville, C. R., and Ehrhardt, D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495.
45. Paterson, A., Rong, J., Gingle, A., Chee, P., Dennis, E., Llewellyn, D., Dure, L., Haigler, C., Myers, G., Peterson, D., Rahman, M., Zafar, Y., Reddy, U., Saranga, Y., Stewart, J., Udall, J., Waghmare, V., Wendel, J., Wilkins, T., Wright, R., Zaki, E., Hafez, E., and Zhu, J. (2010). Sequencing and utilization of the Gossypium genomes. Trop. Plant Biol. 3, 71-74.
46. Pattathil, S. K., Avci, U., Baldwin, D., Alton, G. S., McGill, J. A., Popper, Z., Bootten, T., Albert, A., Davis, R. H., Chennareddy, C., Dong, R., O'Shea, B., Rossi, R., Leoff, C., Freshour, G., Narra, R., O'Neil, M., York, W. S., and Hahn, M. G. (2010). A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol. 153, 514-525.
47. Pear, J. R., Kawagoe, Y., Schreckengost, W. E., Delmer, D. P., and Stalker, D. M. (1996). Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc. Natl. Acad. Sci. U.S.A. 93, 12637-12642.
48. Qin, Y. M., Hu, C. Y., Pang, Y., Kastaniotis, A. J., Hiltunen, J. K., and Zhu, Y. X. (2007). Saturated very-long-chain fatty acids promote cotton fiber and Arabidopsis cell elongation by activating ethylene biosynthesis. Plant Cell 19, 3692-3704.
49. Quadrana, L., Rodriguez, M. C., Lopez, M., Bermudez, L., Nunes-Nesi, A., Fernie, A. R., Descalzo, A., Asis, R., Rossi, M., Asurmendi, S., and Carrari, F. (2011). Coupling virus-induced gene silencing to exogenous green fluorescence protein expression provides a highly efficient system for functional genomics in Arabidopsis and across all stages of tomato fruit development. Plant Physiol. 156, 1278-1291.
50. Rapp, R. A., Haigler, C. H., Flagel, L., Hovav, R. H., Udall, J. A., and Wendel, J. F. (2010). Gene expression in developing fibers of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication. BMC Biol. 8, 139. doi: 10.1186/1741-7007-8-139
51. Roberts, E. M., Nunna, R. R., Huang, J. Y., Trolinder, N. L., and Haigler, C. H. (1992). Effects of cycling temperatures on fiber metabolism in cultured cotton ovules. Plant Physiol. 100, 979-986
52. Robertson, D. (2004). VIGS vectors for gene silencing: many targets, many tools. Annu. Rev. Plant. Biol. 55, 495-519.
53. Ruan, Y. L., Llewellyn, D. J., and Furbank, R. T. (2001). The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13, 47-60.
54. Ruiz, M., and Baulcombe, D. (1998). Initiation and maintenance of virus-induced gene silencing. Plant Cell 10, 937-946.
55. Salnikov, V., Grimson, M. J., Seagull, R. W., and Haigler, C. H. (2003). Localization of sucrose synthase and callose in freeze substituted, secondary wall stage, cotton fibers. Protoplasma 221, 175-184.
56. Seagull, R. W. (1993). Cytoskeletal involvement in cotton fiber growth and development. Micron 24, 643-660.
57. Shao, M. Y., Wang, X. D., Ni, M., Bibi, N., Yuan, S. N., Malik, W., Zhang, H. P., Liu, Y. X., and Hua, S. J. (2011). Regulation of cotton fiber elongation by xyloglucan endotransglycosylase/hydrolase genes. Genet. Mol. Res. 10, 3771-3782.
58. Singh, B., Avci, U., Eichler Inwood, C. H., Grimson, M. J., Landgraf, J., Mohnen, D., Sorenson, I., Wilkerson, C. G., Willats, W. G. T., and Haigler, C. H. (2009a). A specialized outer layer of the primary cell wall joins elongating cotton fibers into tissue-like bundles. Plant Physiol. 150, 684-699.
59. Singh, B., Cheek, H. D., and Haigler, C. H. (2009b). A synthetic auxin (NAA) suppresses secondary wall cellulose synthesis and enhances elongation in cultured cotton fiber. Plant Cell Rep. 28, 1023-1032.
60. Stiff, M. R., and Haigler, C. H. (in press). "Recent advances in cotton fiber development, " in Cotton Flowering and Fruiting, Cotton Physiology Book Series, eds, D. Oosterhuis and T. Cothren (Cordova TN: The Cotton Foundation).
61. Taliercio, E. W., and Boykin, D. (2007). Analysis of gene expression in cotton fiber initials. BMC Plant Biol. 7, 22. doi: 10.1186/1471-2229-7-22
62. Timpa, J. D., and Triplett, B. A. (1993). Analysis of cell-wall polymers during cotton fiber development. Planta 189, 101-108.
63. Tokumoto, H., Wakabayashi, K., Kamisaka, S., and Hoson, T. (2002). Changes in the sugar composition and molecular mass distribution of matrix polysaccharides during cotton fiber development. Plant Cell Physiol. 43, 411-418.
64. Tokumoto, H., Wakabayashi, K., Kamisaka, S., and Hoson, T. (2003). Xyloglucan breakdown during cotton fiber development. J. Plant Physiol. 160, 1411-1414.
65. Tuttle, J. R. (2011). Development of a Virus-induced Gene Silencing System for Cotton and its Application for Functional Genomics in Fiber. Doctoral Dissertation, 201 p. Available at: http://www.lib.ncsu.edu/resolver/1840.16/7024
66. Tuttle, J. R., Idris, A. M., Brown, J. K., Haigler, C. H., and Robertson, D. (2008). Geminivirus-mediated gene silencing from cotton leaf crumple virus is enhanced by low temperature in cotton. Plant Physiol. 148, 41-50.
67. Vaughn, K. C., and Turley, R. B. (1999). The primary walls of cotton fibers contain an ensheathing pectin layer. Protoplasma 209, 226-237.
68. Voinnet, O., Vain, P., Angell, S., and Baulcombe, D. C. (1998). Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95, 177-187.
69. Wakelyn, P. J., Bertoniere, N. R., French, A. D., Thibodeaux, D. P., Triplett, B. A., Rousselle, M. A., Goynes, W. R. Jr., Edwards, J. V., Hunter, L., McAlister, D. D., and Gamble, G. R. (2007). Cotton Fiber Chemistry and Technology. Boca Raton, FL: CRC Press, 162 p.
70. Wang, H., Guo, Y., Lv, F., Zhu, H., Wu, S., Jiang, Y., Li, F., Zhou, B., Guo, W., and Zhang, T. (2010a). The essential role of GhPEL gene, encoding a pectate lyase, in cell wall loosening by depolymerization of the de-esterified pectin during fiber elongation in cotton. Plant Mol. Biol. 72, 397-406.
71. Wang, J., Wang, H., Zhao, P., Han, L., Jiao, G., Zheng, Y., Huang, S., and Xia, G. (2010b). Overexpression of a profilin (GhPFN2) promotes the progression of developmental phases in cotton fibers. Plant Cell Physiol. 51, 1276-1290.
72. Wang, H., Wang, J., Gao, P., Jiao, G., Zhao, P., Li, Y., Wang, G., and Xia, G. (2009). Down-regulation of GhADF1 gene expression affects cotton fibre properties. Plant Biotechnol. J. 7, 13-23.
73. Wendel, J. F., Brubaker, C., Alvarez, I., Cronn, R., and Stewart, J. M. D. (2009). "Evolution and natural history of the cotton genus, " in Genetics and Genomics of Cotton, ed. A. H. Paterson (New York: Springer).
74. Wilkins, T. A., Mishra, R., and Tro-linder, N. L. (2004). Agrobacterium-mediated transformation and regeneration of cotton. J. Food Agric. Envt. 2, 179-187.
75. Ye, J., Chua, N. H., Qu, J., Gene, Y. F., and Bu, Y. P. (2010). Virus Induced Gene Silencing (VIGS) for Functional Analysis of Genes in Cotton. Patent: WO/2010/144058, Publication Date: 16.12.2010, 1-92.
76. Zhong, R., Lee, C., and Ye, Z.-H. (2010). Evolutionary conservation of the transcriptional network regulating secondary wall biosynthesis. Trends Plant Sci. 15, 625-632.
77. Zhu, X., Pattathil, S., Mazumder, K., Brehm, A., Hahn, M. G., Dinesh-Kumar, S. P., and Joshi, C. P. (2010). Virus-induced gene silencing offers a functional genomics platform for studying plant cell wall formation. Mol. Plant 3, 818-833.