Recent Advances in Cotton Fiber Development

Chapter 10 RECENT ADVANCES IN COTTON FIBER DEVELOPMENT Michael R. Stiff1 and Candace H. Haigler2 Department of Crop Science1 and Department of Plant Biology2 North Carolina State University Raleigh, NC 27695 INTRODUCTION Cotton fiber is the world’s most important natural textile fiber. In the U.S.A. in 2010, cotton fiber had a 61% share of the market for apparel and home textiles (Bearden, 2010), with syn- thetic fibers having most of the remaining market share. A similar demand for renewable cotton fiber occurs worldwide. A highly regulated cellular differentiation process governs the morphogenesis of the fiber. Each long cotton “lint” fiber originates from a single epidermal cell on the ovule surface that transforms into the highly elongated and reinforced dead fiber through dra- matic polar expansion and cell wall thickening. Fiber morphogenesis proceeds through several stages that will be described further in this chapter: initiation, elongation, transitional primary wall remodeling, secondary wall synthesis, and maturation. These differentiation processes, which typically last at least 50 days, directly determine cotton fiber quality characteristics. The number of fibers initiated in the outer integument of the ovule is a major factor in fiber yield. Fiber fineness (weight per unit length) and micronaire are determined by the fiber perimeter and the extent of secondary cell wall thickening. Fiber length and length uniformity are both valued in modern spinning mills, and cell elongation is strongly affected by developing and maintain- ing high turgor pressure within the central vacuole as well as carbon supply in different regions of the seed. Fiber strength is affected by properties of the transitional “winding” cell wall layer as well as secondary wall cellulose (e.g., degree of polymerization and microfibril angle). High fiber tensile properties (including strength and mechanical elongation, or elongation-to-break) help to preserve fiber length during processing, and they are also required to produce strong yarns and fabrics. The potential of cotton fibers to pickup dye molecules and to absorb water are determined by the amount and the degree of crystallinity of the secondary wall cellulose. The final collapse of the fiber into the typical kidney bean shape that facilitates spinning (through improved friction properties) relies on adequate filling, but not over-filling, with secondary wall cellulose (Wakelyn et al., 2007). Since a cotton fiber is a cell wall composite, many of its important developmental processes relate to plant cell wall deposition (Haigler et al., 2012). At first, it was surprising that the single-celled cotton fiber expresses a large percentage of the genes present in a complex allotetraploid genome (Hovav et al., 2008b), but the morphogenetic processes leading to commercial cotton fiber encompass many aspects of whole plant growth. Many years will be required to understand how most of the genes and regulatory networks ex- 164 STIFF AND HAIGLER ert their effects on the fiber differentiation process. Cotton fiber has many advantages for such experiments. It is a single cell that undergoes semi-synchronous differentiation in a series of overlapping developmental stages. Cotton fibers are easily separated from the developing seed. Therefore, researchers can sample a large population of one cell type and have clear knowledge of the predominant cellular activities at that time. Given that cotton fibers are expendable for plant growth, there is unrestricted ability to manipulate fiber development experimentally. The genus Gossypium includes living, non-domesticated, diploid and allotetraploid progenitor spe- cies that provide valuable comparisons and contrasts with commercial fiber (Kim and Triplett, 2001; Hovav et al., 2008b; Rapp et al., 2010). Below we provide a review of emerging experimental evidence on the cellular and physiolog- ical processes underlying the morphogenesis of domesticated G. hirsutum fiber with emphasis on research published since 2005. Useful related information can be found in other reviews dis- cussing: cotton fiber-ovule culture as a unique experimental tool (Kim and Triplett, 2001); the evolutionary and domestication history of cotton (Wendel et al., 2009); genomic scale research on the secondary wall thickening phase (Haigler et al., 2005; Haigler et al., 2009); transcriptional changes during fiber development (Wilkins and Arpat, 2005; Shangguanet al., 2010); and transcriptional and hormonal regulation of fiber development (Leeet al., 2007). COTTON FIBER DEVELOPMENT Cotton Fiber Initiation The first step in cotton fiber morphogenesis is the differentiation of selected ovule epidermal cells into fiber initials, or rounded protrusions above the ovule surface. Fiber initiation typically begins on the day of anthesis and continues to at least 5 days post anthesis (DPA) when each ovule has about 16,000 fiber initials (inclusive of young elongating fibers) in modern cultivars (Fig. 1; Stewart, 1975; Seagull and Giavalis, 2004). As initials expand, the central vacuole forms and the nucleus migrates from the base toward the middle of the developing fiber. The density of fiber initials at 0 and 1 DPA was positively correlated with lint percentage and lint index in five G. hirsutum cultivars (Li et al., 2009). Humans selected for higher density and more synchronous fiber initiation during cotton domestication (Butterworthet al., 2009). Generation of turgor pressure within the central vacuole drives the expansion of fiber initials. Ruan and coworkers (Ruan et al., 2003) showed that both fiber initiation and fiber elongation were inhibited by sup- pressed expression of the SS3 isoform of sucrose synthase (Sus) in transgenic cotton (Ruan et al., 2003). Plants with lower Sus protein in the seed coat compared to wild-type cotton produced fewer fibers that appeared shrunken and collapsed when viewed by scanning electron microscopy. The transgenic fibers had lower Sus activity, which correlated with decreased levels of hexoses and starch, but not sucrose. Possibly decreased hexoses caused lower osmotic potential and reduced turgor, but the fiber defects might also have been at least partly explained by factors such as less Sus-generated UDP-glucose to provide the substrate for cell wall synthesis (see further discussion below) and/or disruption of signaling pathways that might depend on hexose. RECENT ADVANCES IN COTTON FIBER DEVELOPMENT 165 Figure 1. Representation of a mature cotton plant containing bolls and fibers at all stages of development. The stem indicates the fastest timeline for cultivated fiber development when plants are grown in an optimal (30°C) environment. Branches indicate days post-anthesis (DPA) and the images show many of the key features of fiber development. Cryo-field-emis- sion scanning electron microscopy of (A) fiber initials on the ovule surface (bar = 10µ m); (B) twisting and elongating 3 DPA fibers (bar = 100µ m); (C) cotton fiber middle lamella (CFML) stretched between two 3 DPA fibers (bar = 4µ m); (D) ordered bundles of fibers inside the boll (bar = 100 µm). Differential interference contrast micrographs indicating microfibril angle of (E) 16 DPA and (F) 20 DPA fiber, with a steeper angle at 20 DPA (bars = 10 µm). TEM fiber cross-section showing (G) an early stage of secondary wall thickening (bar = 300 nm); and (H) a more advanced stage of secondary wall (bar = 1 µm). (I) Mature cotton boll and (J) cross-section of mature fiber viewed in the light microscope. SCW, secondary cell wall. 166 STIFF AND HAIGLER Transcriptional Regulation of Initiation Transcription is regulated by various small RNAs, such as small interfering RNAs (siRNAs), as well as the activity of transcription factors. Small RNAs occur in size classes that regulate gene expression differently. siRNAs are predominantly 24 nucleotides long and direct DNA methylation and chromatin remodeling. The typically 18-21 nucleotide microRNAs (miRNAs) are derived from an endogenous hairpin structure and participate in the RNA-induced silencing complex (RISC) to target homologous mRNA for degradation or inhibit translation (Voinnet 2009). Some of the miRNAs expressed in cotton fiber have been identified by bioinformatics (Zhang et al., 2007) and, along with siRNAs, through sequencing approaches (Pang et al., 2009; Kwak et al., 2009). Ovules engaged in early fiber development (0 and 3 DPA) showed a marked increase in the expression of 24 nucleotide siRNAs compared to -3 DPA ovules and leaves, which led to the proposal that siRNA-mediated chromatin remodeling may contribute to fiber initiation. In general, miRNAs were expressed more highly in -3 DPA ovules compared to 3 DPA fiber-bearing ovules and 10 DPA fibers, suggesting that miRNAs may maintain low expression of target genes prior to initiation (Pang et al., 2009). Consistent with a decline in miRNAs by 3 DPA, a large percentage of the cotton genome is expressed in 2 to 25 DPA fiber (Hovav et al., 2008b). In the fuzzless-lintless (fl) mutant that does not initiate fiber, more miRNA families were expressed compared to wild-type, leading to the hypothesis that targeted down-regulation of genes controlling fiber initiation could underpin the mutant phenotype (Kwaket al., 2009). Transcription factors, often working together in complexes, bind with specific genomic sequences to promote, enhance, or block transcription. Given the importance of fiber initiation for fiber yield, several studies have focused on identifying transcription factors

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