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Recent advances in understanding cotton fibre and seed development

Published online by Cambridge University Press:  22 February 2007

Yong-Ling Ruan
Affiliation:
CSIRO Plant Industry, GPO Box 1600, Canberra, ACT, 2601, Australia

Abstract

The unique feature of the seed of tetraploid cotton (Gossypium hirsutum and Gossypium barbadense) is that about 30% of the seed coat epidermal cells develop into cellulose-enriched fibres, while the embryos synthesize oils and proteins. Hence, both the maternal and filial tissues of the cotton seed are of significant economic value. After initiation from the ovule epidermis at or just before anthesis, the single-celled fibres elongate to 2.5–6.0 cm long in the tetraploid species before they switch to intensive secondary cell wall cellulose synthesis. Thus, apart from its agronomic importance, the cotton fibre represents a model single-cell system to study the control of cell differentiation and elongation, carbon partitioning to cellulose synthesis and also the interaction between maternal (fibre) and embryonic tissues in seeds. Over the past decade or so, significant effort has been made to understand the cellular and molecular basis of cotton fibre development and oil biosynthesis in the embryo. Metabolic engineering of the oil biosynthetic pathway in cotton seed has successfully produced healthier and stable oils. A number of candidate genes and cellular processes that potentially regulate various aspects of fibre development have been identified. Further elucidation of the in vivo functions of those candidate genes could significantly deepen our understanding of fibre development and offer potential for improvement of fibre quality through genetic engineering or marker-assisted breeding approaches.

Type
Invited Review
Copyright
Copyright © Cambridge University Press 2005

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References

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. Proceedings of the National Academy of Sciences, USA 92, 93539357.CrossRefGoogle ScholarPubMed
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 Molecular Biology 54, 911929.CrossRefGoogle ScholarPubMed
Basra, A.S. and Malik, C.P. (1984) Development of the cotton fiber. International Review of Cytology 89, 65113.CrossRefGoogle Scholar
Basra, A.S. and Saha, A. (1999) Growth regulation of cotton fibers. pp. 4763. in Basra, A.S. (Ed.) Cotton fibers: Developmental biology, quality improvement, and textile processing. New York, Food Products Press.Google Scholar
Beasley, C.A. (1977) Ovule culture: Fundamental and pragmatic research for the cotton industry. pp. 160178. in Reinert, J.;, Bajaj, Y.P.S. (Eds) Applied and fundamental aspects of plant cell, tissue and organ culture. Berlin, Springer-Verlag.Google Scholar
Beasley, C.A. and Ting, I.P. (1973) Effects of plant growth substances on in vitro fibre development from fertilized cotton ovules. American Journal of Botany 60, 130139.CrossRefGoogle Scholar
Beasley, C.A. and Ting, I.P. (1974) Effects of plant growth substances on in vitro fiber development from unfertilized cotton ovules. American Journal of Botany 61, 188194.CrossRefGoogle Scholar
Brubaker, C.L., Paterson, A.H. and Wendel, J.F. (1999) Comparative genetic mapping of allotetraploid cotton and its diploid progenitors. Genome 42, 184203.CrossRefGoogle Scholar
Cosgrove, D.J. (1997) Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell 9, 10311041.CrossRefGoogle Scholar
Cowan, A.K., Cripps, R.F., Richings, E.W. and Taylor, N.J. (2001) Fruit size: Towards an understanding of the metabolic control of fruit growth using avocado as a model system. Physiologia Plantarum 111, 127136.CrossRefGoogle Scholar
Davidonis, G.H. (1999) Cotton fibers in vitro. pp. 6584. in Basra, A.S. (Ed.) Cotton fibers: Developmental biology, quality improvement, and textile processing. New York, Food Products Press.Google Scholar
Delmer, D.P. (1999) Cellulose biosynthesis in developing cotton fibers. pp. 85112. in Basra, A.S. (Ed.) Cotton fibers: Developmental biology, quality improvement, and textile processing. New York, Food Products Press.Google Scholar
Delmer, D.P., Pear, J.R., Andrawis, A. and Stalker, D.M. (1995) Genes for small GTP-binding proteins analogous to mammalian Rac are preferentially expressed in developing cotton fibers. Molecular and General Genetics 248, 4351.CrossRefGoogle ScholarPubMed
Dhindsa, R.S., Beasley, C.A. and Ting, I.P. (1975) Osmoregulation in cotton fiber. Accumulation of potassium and malate during growth. Plant Physiology 56, 394398.CrossRefGoogle ScholarPubMed
Diekmann, D., Abo, A., Johnston, C., Segal, A.W. and Hall, A. (1994) Interaction of Rac with p67 (phox) and regulation of the phagocytic NADPH oxidase activity. Science 265, 531533.CrossRefGoogle ScholarPubMed
Doblin, M.S., Kurek, I., Jacon-Wilk, D. and Delmer, D.P. (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant and Cell Physiology 43, 14071420.CrossRefGoogle ScholarPubMed
Dougherty, R.M., Allman, M.A. and Iacono, J.M. (1995) Effects of diets containing high or low amounts of stearic acid on plasma lipoprotein fractions and fecal fatty acid excretion of men. American Journal of Clinical Nutrition 61, 11201128.CrossRefGoogle ScholarPubMed
Du, X.M., Pan, J.J., Wang, R.H., Zhang, T.Z. and Shi, Y.Z. (2001) Genetic analysis of presence and absence of lint and fuzz in cotton. Plant Breeding 120, 519522.CrossRefGoogle Scholar
Farley, S.J., Patrick, J.W. and Offler, C.E. (2000) Functional transfer cells differentiate in cultured cotyledons of Vicia faba L. seeds. Protoplasma 214, 102117.CrossRefGoogle Scholar
Ferguson, D.L., Turley, R.B. and Kloth, R.H. (1997) Identification of a δ–TIP cDNA clone and determination of related A and D genome subfamilies in Gossypium species. Plant Molecular Biology 34, 111118.CrossRefGoogle Scholar
Fryxell, P.A. (1963) Morphology of the base of seed hairs of Gossypium. I. Gross morphology. Botanical Gazette 124, 196199.CrossRefGoogle Scholar
Fukuda, H. (1992) Tracheary element formation as a model system of cell differentiation. International Review of Cytology 136, 289332.CrossRefGoogle Scholar
Garcia, D., Saingery, V., Chambrier, P., Mayer, U., Jürgens, G. and Berger, F. (2003) Arabidopsis haiku mutants reveal new controls of seed size by endosperm. Plant Physiology 131, 16611671.CrossRefGoogle ScholarPubMed
Graves, D.A. and Stewart, J.M. (1988) Chronology of the differentiation of cotton (Gossypium hirstum L.) fiber cells. Planta 175, 254258.CrossRefGoogle Scholar
Haigler, C.H., Ivanova-Datcheva, M., Hogan, P.S., Salnikov, V.V., Hwang, S., Martin, K. and Delmer, D.P. (2001) Carbon partitioning to cellulose synthesis. Plant Molecular Biology 47, 2951.CrossRefGoogle ScholarPubMed
Haigler, C.H., Zhang, D.H. and Wilkerson, C.G. (2005) Biotechnological improvement of cotton fibre maturity. Physiologia Plantarum 124, 285294.CrossRefGoogle Scholar
Han, Z.-G., Guo, W.-Z., Song, X.-L., Zhang, T.-Z. (2004) Genetic mapping of EST-derived microsatellites from the diploid Gossypium arboreum in allotetraploid cotton. Molecular Genetics and Genomics 272, 308327.CrossRefGoogle ScholarPubMed
Harmer, S.E., Orford, S.J. and Timmis, J.N. (2002) Characterisation of six α-expansin genes in Gossypium hirsutum (upland cotton). Molecular Genetics and Genomics 268, 19.CrossRefGoogle ScholarPubMed
Ji, S.-J., Lu, Y.-C., Feng, J.-X., Wei, G., Li, J., Shi, Y.-H., Fu, Q., Liu, D., Luo, J.-C., Zhu, Y.-X. (2003) Isolation and analyses of genes preferentially expressed during early cotton fiber development by subtractive PCR and cDNA array. Nucleic Acids Research 31, 25342543.CrossRefGoogle ScholarPubMed
Jiang, C.X., Wright, R.J., El-Zik, K.M. and Paterson, A.H. (1998) Polyploid formation created unique avenues for response to selection in Gossypium (cotton). Proceedings of National Academy of Sciences, USA 95, 44194424.CrossRefGoogle ScholarPubMed
John, M.E. (1997) Cotton crop improvement through genetic engineering. Critical Reviews in Biotechnology 17, 185208.CrossRefGoogle Scholar
John, M.E. (1999) Genetic engineering strategies for cotton fiber modification. pp. 271292. in Basra, A.S.Cotton fibers: Developmental biology, quality improvement, and textile processing. New York, Food Products Press.Google Scholar
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 Physiology 127, 13611366.CrossRefGoogle ScholarPubMed
King, S.P., Lunn, J.E. and Furbank, R.T. (1997) Carbohydrate content and enzyme metabolism in developing canola siliques. Plant Physiology 114, 153160.CrossRefGoogle ScholarPubMed
Kirik, V., Simon, M., Hüelskamp, M. and Schiefelbein, J. (2004) The ENHANCER of TRY and CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Developmental Biology 268, 506513.CrossRefGoogle ScholarPubMed
Koroleva, O.A., Farrar, J.F., Thomas, A.D. and Pollock, C.J. (1998) Carbohydrates in individual cells of epidermis, mesophyll and bundle sheath in barley leaves with changed export or photosynthetic rate. Plant Physiology 118, 15251532.CrossRefGoogle ScholarPubMed
Loguercio, L.L., Zhang, J.-Q. and Wilkins, T.A. (1999) Differential regulation of six novel MYB -domain genes defines two distinct expression patterns in allotetraploid cotton (Gossypium hirsutum L). Molecular and General Genetics 261, 660671.CrossRefGoogle Scholar
Li, X.B., Fan, X.P., Wang, X.L., Cai, L. and Yang, W.C. (2005) The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant Cell 17, 859875.CrossRefGoogle ScholarPubMed
Li, Y.-L., Sun, J. Xia G.-X. (2005) Cloning and characterization of an LRR receptor-like protein kinase gene associated with cotton fibre development. Molecular Genetics and Genomics 273, 217224.CrossRefGoogle Scholar
Liu, Q., Singh, S. and Green, A. (2002a) High-oleic and high-stearic cottonseed oils: Nutritionally improved cooking oils developed using gene silencing. Journal of the American College of Nutrition 21 205S – 211SCrossRefGoogle ScholarPubMed
Liu, Q., Singh, S.P. and Green, A.G. (2002b) High-stearic and high-oleic cottonseed oils produced by hairpin RNA-mediated post-transcriptional gene silencing. Plant Physiology 129, 17321743.CrossRefGoogle ScholarPubMed
Ma, D.P., Tan, H., Si, Y., Creech, R.G. and Jenkins, J.N. (1995b) Differential expression of a lipid transfer protein gene in cotton fiber. Biochimica et Biophysica Acta 1257, 8184.CrossRefGoogle ScholarPubMed
Martin, C., Bhatt, K. and Baumann, K. (2001) Shaping in plant cells. Current Opinion in Plant Biology 4, 540549.CrossRefGoogle ScholarPubMed
Mathur, J., Spielhofer, P., Kost, B., Chua, N.-H. (1999) The actin cytoskeleton is required to elaborate and maintain spatial patterning during cell morphogenesis in Arabidopsis thaliana. Development 126, 55595568.CrossRefGoogle ScholarPubMed
Murray, F., Llewellyn, D., McFadden, H., Last, D., Dennis, E.S. and Peacock, W.J. (1999) Expression of the Talaromyces flavus glucose oxidase gene in cotton and tobacco reduces fungal infection, but is also phytotoxic. Molecular Breeding 5, 219232.CrossRefGoogle Scholar
Mutsaers, H.J.W. (1976) Growth and assimilate conversion of cotton bolls (Gossypium hirsutum L.). I. Growth of fruits and substrate demand. Annals of Botany 40, 301315.CrossRefGoogle Scholar
Nolte, K.D., Hendrix, D.L., Radin, J.W. and Koch, K.E. (1995) Sucrose synthase localization during initiation of seed development and trichome differentiation in cotton ovules. Plant Physiology 109, 12851293.CrossRefGoogle ScholarPubMed
Offler, C.E., McCurdy, D.W., Patrick, J.W. and Talbot, M.J. (2003) Transfer cells: Cells specialized for a special purpose. Annual Review of Plant Biology 54, 431454.CrossRefGoogle ScholarPubMed
Paterson, A.H., Saranga, Y., Menz, M., Jiang, C.X. and Wright, R.J. (2003) QTL analysis of genotype × environment interactions affecting cotton fiber quality. Theoretical and Applied Genetics 106, 384396.CrossRefGoogle ScholarPubMed
Patrick, J.W. and Offler, C.E. (1995) Post-sieve element transport of sucrose in developing seeds. Australian Journal of Plant Physiology 22, 681702.Google Scholar
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. Proceedings of National Academy of Sciences, USA 93, 1263712642.CrossRefGoogle ScholarPubMed
Percival, A.E., Wendel, J.F. and Stewart J., McD (1999) Taxonomy and germplasm resources. 3363. in Smith, C.W.;, Cothren, J.T.;Cotton: Origin, history, technology and production. New York, John Wiley & Sons.Google Scholar
Pesch, M. and Hulskamp, M. (2004) Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. Current Opinion in Genetics and Development 14, 422427.CrossRefGoogle ScholarPubMed
Pfluger, J. and Zambryski, P.C. (2001) Cell growth: The power of symplastic isolation. Current Biology 11, R436R439CrossRefGoogle ScholarPubMed
Potikha, T.S., Collins, C.C., Johnson, D.I., Delmer, D.P. and Levine, A. (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiology 119, 849858.CrossRefGoogle ScholarPubMed
Ruan, Y.-L. and Chourey, P.S. (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 Physiology 118, 399406.CrossRefGoogle ScholarPubMed
Ruan, Y.-L. and Chourey, P.S. (2006) Carbon partitioning in developing seed. in Basra, A.S. (Ed.) Seed science and technology: Trends and advances. New York, Haworth Press (in press).Google Scholar
Ruan, Y.-L., Chourey, P.S., Delmer, D.P., Perez-Grau, L. (1997) The differential expression of sucrose synthase in relation to diverse patterns of carbon partitioning in developing cotton seed. Plant Physiology 115, 375385.CrossRefGoogle ScholarPubMed
Ruan, Y.-L., Llewellyn, D.J. and Furbank, R.T. (2000) Pathway and control of sucrose import into initiating cotton fibre cells. Australian Journal of Plant Physiology 27, 795800.Google Scholar
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, 4760.Google Scholar
Ruan, Y.-L., Llewellyn, D.J. and Furbank, R.T. (2003) Suppression of sucrose synthase expression represses cotton fiber cell initiation, elongation and seed development. Plant Cell 15, 952964.CrossRefGoogle ScholarPubMed
Ruan, Y.-L., Xu, S.-M., White, R. and Furbank, R.T. (2004) Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiology 136, 41044113.CrossRefGoogle ScholarPubMed
Ruan, Y.-L., Llewellyn, D.J., Furbank, R.T. and Chourey, P.S. (2005) The delayed initiation and slow elongation of fuzz-like short fibre cells in relation to altered patterns of sucrose synthase expression and plasmodesmata gating in a lintless mutant of cotton. Journal of Experimental Botany 56, 977984.CrossRefGoogle Scholar
Ryser, U. (1999) Cotton fiber initiation and histodifferentiation. pp. 144. in Basra, A.S. (Ed.) Cotton fibers: Developmental biology, quality improvement, and textile processing. New York, Food Products Press.Google Scholar
Ryser, U., Schorderet, M., Jauch, U. and Meier, H. (1988) Ultrastructure of the ‘fringe-layer’, the innermost epidermis of cotton seed coats. Protoplasma 147, 8190.CrossRefGoogle Scholar
Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., Thumfahrt, J., Jürgens, G., Hülskamp, M. (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO Journal 21, 50365046.CrossRefGoogle ScholarPubMed
Schubert, A.M., Benedict, C.R. and Kohel, R.J. (1986) Carbohydrate distribution in bolls. pp. in 311323. Mauney, J.R., Stewart, J.M. (Eds) Cotton physiology. Memphis, Tennessee, Cotton Foundation.Google Scholar
Seagull, R.W. (1990) The effect of microtuble and microfilament disrupting agents on cytoskeletal arrays and wall deposition in developing cotton fibers. Protoplasma 159, 4459.CrossRefGoogle Scholar
Seagull, R.W. (1992) A quantitative electron microscopic study of changes in microtuble arrays and wall microfibril orientation during in vitro cotton fiber development. Journal of Cell Science 101, 561577.CrossRefGoogle Scholar
Shimizu, Y., Aotsuka, S., Hasegawa, O., Kawada, T., Sakuno, T., Sakai, F. and Hayashi, T. (1997) Changes in levels of mRNAs for cell wall-related enzymes in growing cotton fiber cells. Plant and Cell Physiology 38, 375378.CrossRefGoogle ScholarPubMed
Smart, L.B., Vojdani, F., Maeshima, M. and Wilkins, T.A. (1998) Genes involved in osmoregulation during turgor-driven cell expansion of developing cotton fibers are differentially regulated. Plant Physiology 116, 15391549.CrossRefGoogle ScholarPubMed
Stewart, J.M. (1975) Fiber initiation on the cotton ovule (Gossypium hirsutum). American Journal of Botany 62, 723730.CrossRefGoogle Scholar
Suo, J.-F., Liang, X.-O., Pu, L., Zhang, Y.-S., Xue, Y.-B. (2003) Identification of GhMYB109 encoding a R2R3 MYB transcription factor that expressed specifically in fiber initials and elongating fibers of cotton (Gossypium hirsutum L.). Biochimica et Biophysica Acta 1630, 2534.CrossRefGoogle ScholarPubMed
Szymanski, D.B., Marks, M.D. and Wick, S.M. (1999) Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11, 23312347.CrossRefGoogle ScholarPubMed
Thompson, R.D., Hueros, G., Becker, H.A. and Maitz, M. (2001) Development and functions of seed transfer cells. Plant Science 160, 775783.CrossRefGoogle ScholarPubMed
Tiwari, S.C. and Wilkins, T.A. (1995) Cotton (Gossypium hirsutum) seed trichomes expand via diffuse growing mechanism. Canadian Journal of Botany 73, 746757.CrossRefGoogle Scholar
Trelease, R.N., Miernyk, J.A., Choinski, J.S. and Bortman, S.J. (1986) Synthesis and compartmentation of enzymes during seed maturation. pp. 441460. in Mauney, J.R.;, Stewart, J.M.Cotton physiology. Memphis, Tennessee Cotton Foundation.Google Scholar
Trotochaud, A.E., Hao, T., Wu, G., Yang, Z.B. and Clark, S.E. (1999) The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11, 393405.CrossRefGoogle Scholar
Wada, T., Kurata, T., Tominaga, R., Koshino-Kimura, Y., Tachibana, T., Goto, K., Marks, M.D., Shimura, Y. and Okada, K. (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129, 54095419.CrossRefGoogle ScholarPubMed
Walker, A.R., Davison, P.A., Bolognesi-Winfield, A.C., James, C.-M., Srinivasan, N., Blundell, T.L., Esch, J.J., Marks, M.D. and Gray, J.C. (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11, 13371350.CrossRefGoogle ScholarPubMed
Wang, S., Wang, J.-W., Yu, N., Li, C.-H., Luo, B., Gou, J.-Y., Wang, L.-J., Chen, X.-Y. (2004) Control of plant trichome development by a cotton fiber MYB gene. Plant Cell 16, 23232334.CrossRefGoogle ScholarPubMed
Weber, H., Borisjuk, L. and Wobus, U. (1997) Sugar import and metabolism during seed development. Trends in Plant Science 2, 169174.CrossRefGoogle Scholar
Wilkins, T.A. and Jernstedt, J.A. (1999) Molecular genetics of developing cotton fibers. pp. 231267. in Basra, A.S. (Ed.) Cotton fibers: Developmental biology, quality improvement, and textile processing. New York, Food Products Press.Google Scholar
Yang, Y.-M., Xu, C.-N., Wang, B.-M., Jia, J.-Z. (2001) Effect of plant growth regulators on secondary wall thickening of cotton fibres. Plant Growth Regulation 35, 233237.Google Scholar
Zhang, T.Z., Yuan, Y.L., Yu, J., Guo, W.Z. and Kohel, R.J. (2003) Molecular tagging of a major QTL for fiber strength in Upland cotton and its marker-assisted selection. Theoretical and Applied Genetics 106, 262268.CrossRefGoogle Scholar