INVITED REVIEW Gene Expression Changes and Early Events in Cotton Fibre Development JINSUK J. LEE1,3,��� , ANDREW W. WOODWARD1,3,��� and Z. JEFFREY CHEN1,2,3,4,* 1Sections of Molecular Cell and Developmental Biology, 2Integrative Biology, 3Center for Computational Biology and Bioinformatics and 4Institute for Cellular and Molecular Biology, The University of Texas at Austin, One University Station A4800, Austin, TX 78712, USA Received: 14 May 2007 Returned for revision: 3 July 2007 Accepted: 1 August 2007 Published electronically: 27 September 2007 ��� Background Cotton is the dominant source of natural textile fibre and a significant oil crop. Cotton fibres, produced by certain species in the genus Gossypium, are seed trichomes derived from individual cells of the epidermal layer of the seed coat. Cotton fibre development is delineated into four distinct and overlapping developmental stages: fibre initiation, elongation, secondary wall biosynthesis and maturation. ��� Scope Recent advances in gene expression studies are beginning to provide new insights into a better understand- ing of early events in cotton fibre development. Fibre cell development is a complex process involving many path- ways, including various signal transduction and transcriptional regulation components. Several analyses using expressed sequence tags and microarray have identified transcripts that preferentially accumulate during fibre devel- opment. These studies, as well as complementation and overexpression experiments using cotton genes in arabidop- sis and tobacco, indicate some similar molecular events between trichome development from the leaf epidermis and fibre development from the ovule epidermis. Specifically, MYB transcription factors regulate leaf trichome devel- opment in arabidopsis and may regulate seed trichome development in cotton. In addition, transcript profiling and ovule culture experiments both indicate that several phytohormones and other signalling pathways mediate cotton fibre development. Auxin and gibberellins promote early stages of fibre initiation ethylene- and brassinosteroid- related genes are up-regulated during the fibre elongation phase and genes associated with calmodulin and calmodulin-binding proteins are up-regulated in fibre initials. Additional genomic data, mutant and functional ana- lyses, and genome mapping studies promise to reveal the critical factors mediating cotton fibre cell development. Key words: Gossypium, cotton, fibre, polyploid, ovule, phytohormone, auxin, gibberellin, trichome, gene expression. INTRODUCTION Cotton is an important crop that is widely grown and is used to produce both natural textile fibre and cottonseed oil. Commercial cotton is grown in .80 countries, including Australia, China, Africa, India, Pakistan, the USA and Uzbekistan. China is the largest user and producer of raw cotton, while the USA is the second largest producer, with the cotton industry contributing about $5 billion per year to the US economy (Agricultural Outlook 2006, http://www.fapri.org/outlook2006/). Cotton fibres can be used for producing innumerable commodities, ranging from textile fabrics and computer screens to automobile brakes. More than 150 countries are involved in import and export of cotton. Economic impact is estimated to be approx. $500 billion year21 worldwide (National Cotton Council 2006, http://www.cotton.org/). The genus Gossypium occurs naturally throughout tropi- cal and subtropical regions, and includes about 45 species split across two ploidy levels, diploid (2n �� 2x �� 26) and tetraploid (2n �� 4x �� 52) (Wendel, 1989 Percival et al., 1999 Wendel and Cronn, 2003). An important event in cotton genome evolution was the spontaneous formation of allopolyploid cotton that has been subsequently selected and domesticated as modern cultivated cotton (Fig. 1). The progenitors of allotetraploid cotton are most closely related to ���AA��� and ���DD��� extant diploid species. This polyploidization event occurred approx. 1.5 million years ago (Mya), and the AADD allotetraploids diverged into five species that are distributed throughout the New World and the rest of the globe (Wendel, 1989 Percival et al., 1999 Wendel and Cronn, 2003 Desai et al., 2006). Among the extant diploids resembling the presumed ances- tors of tetraploid cotton, the AA progenitor species produce both lint (long) fibres that are spinnable into yarn and shorter fibres called fuzz. In contrast, the DD genome pro- genitor species produce very few lint fibres that are initiated pre-anthesis, but are much shorter in length than the lint fibres of the AA genome progenitor (Percival et al., 1999 Applequist et al., 2001) (Fig. 1). Among the five allotetraploids, upland or American cotton, Gossypium hirsutum, represents over 95 % of annual cotton crop worldwide. Pima or Egyptian cotton, G. barbadense, and Asian cotton (a diploid), G. arboreum, together represent the remaining 5 % (Smith and Cothren, 1999). Interestingly, compared with the AA and DD genome progenitors, the fibre traits in the allotetraploids are dramatically enhanced. The allotetra- ploids produce more abundant and higher quality fibres than the extant descendant species, suggesting strong selection on polyploid cotton for fibre properties. Cotton is a model system for the study of cell elongation and cell wall and cellulose biosynthesis (Kim and Triplett, 2001). The fibre is composed of nearly pure cellulose, the largest component of plant biomass. Annual world production of cellulose is approx. 100 million metric tons, primarily in the ���These authors contributed equally to the work. * For correspondence. E-mail zjchen@mail.utexas.edu # The Author 2007. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org Annals of Botany 100: 1391���1401, 2007 doi:10.1093/aob/mcm232, available online at www.aob.oxfordjournals.org

cell walls of higher plants. The basic study of cellulose biosynthesis in fibre cells is highly pertinent to the applied objectives of renewable resource and bioenergy research. Cotton fibres are seed trichomes. Cotton fibre develop- ment undergoes several distinctive but overlapping steps including fibre initiation, elongation, secondary cell wall biosynthesis, and maturation, leading to mature fibres (Basra and Malik, 1984 Tiwari and Wilkins, 1995 Wilkins and Jernstedt, 1999 Kim and Triplett, 2001) (Fig. 2). In G. hirsutum, lint fibres develop prior to or on the day of anthesis, and fuzz fibres develop a few days later. The process is quasi-synchronized in each developing ovule and among ovules within each ovary (boll). Initiation of fuzz fibre development occurs after initiation of lint fibre development but the timing varies among genotypes (Basra and Malik, 1984). Fibre cell initials usually emerge on the day of anthesis [0 d post-anthesis (DPA) see Table 1 for a list of abbreviations used]. Therefore, the chronology of fibre cell development is conventionally monitored relative to the number of DPA (a negative number indicates days before fibre cell emergence). Morphologically distinct fibre cell initials continue to grow rapidly without cell div- ision for 16���25 d during the phase of fibre cell elongation and the biosynthesis of secondary wall cellulose (Basra and Malik, 1984 Tiwari and Wilkins, 1995 Wilkins and Jernstedt, 1999 Kim and Triplett, 2001 Haigler et al., 2005). The elongated fibre cells may reach lengths of nearly 6 cm, or one-third the height of an arabidopsis plant (Kim and Triplett, 2001). Finally, fibre cells mature from 50 to 60 DPA when cotton bolls open, and the long and mature (lint) fibres can be detached from the seeds. Both fibre and seed can be used for industrial applications (Basra and Malik, 1984). The molecular basis of the fibre initiation stage remains largely mysterious. About 15���25 % of the epidermal FIG. 1. Evolution of allotetraploid cotton and cotton fibres. Extant diploid progenitors diverge 7���8 millions years ago (Mya), and allotetraploidization occurred naturally 1���2 Mya between a fibre-producing AA-genome extant species and a fibre-poor DD-genome extant species, generating AADD allotetraploid species (Wendel, 1989 Percival et al., 1999 Wendel and Cronn, 2003). Superior fibre yield and quality have been selected in allotetraploid cotton species, as well as the domesticated diploid G. arboreum. There are five allotetraploid species, and two of them, G. hirsutum and G. barbadense, provide .95% of the modern commercial cotton crop. The genome sizes in parentheses are based on published work (Hendrix and Stewart, 2005). Mb, Mega base pairs (106) Gb, gig base pairs (109). Lee et al. ��� Cotton Fibre Cell Initiation and Elongation 1392