Comparative Evolutionary Genomics of Cotton

Evolutionary history of the genus Gossypium. As Gossypium diversified and colonized arid regions of the globe it underwent extensive chromosomal evolution. Presently, eight diploid genome groups (A through G, plus K) are recognized among the 50 species. Relationships within and among the various genome groups have been addressed in detail. Genome groups largely correspond to monophyletic lineages. This i nformation has been embodied in our synthesis of relationships and of genome evolution (Fig. 1), which reveals four major lineages of diploid species corresponding to three continents.

 

Polyploidy and genome evolution in Gossypium . Polyploidization is a prominent process in plant evolution, and is important in crop plants as well. Both G. hirsutum and G. barbadense are classic allopolyploids, tracing to a seemingly improbable hybridization of an African/Asian A-genome and an American D-genome species ~1-2 mya. Each has a large indigenous range and encompasses myriad morphological forms that span the wild-to-domesticated continuum. Polyploidization is widely perceived to provide raw material for evolutionary novelty; in this respect genome doubling in cotton may have offered novel opportunities for agronomic improvement through human selection. Because modern tetraploid cotton has lint characteristics that are non-additive relative to their diploid progenitors (Fig. 2), polyploidy per se has been critical to the productivity and quality of modern cotton. We recently developed a novel microarray platform for studying the contributions of two co-resident genomes to cotton development, which promises to provide insight into the evolutionary and agronomic significance of genome doubling.

Fig. 1. Phylogenetic framework and genome size variation. Gossypium contains 45 diploid (n = 13) and five allopolyploid (n = 26) species, the latter with two genomes, A and D, from species in different hemispheres. A- and D- genome groups diverged ~ 5-10 MYA. Allopolyploid cottons originated following trans-oceanic dispersal of an A-genome progenitor to the New World. Arrows indicate taxa representing the best living models of the species involved in allopolyploid formation. Allopolyploids diversified during the Pleistocene into three lineages, of which two include the commercially important species, G. hirsutum (upland cotton) and G. barbadense (Pima cotton), each domesticated within the last 4000-7000 years.

Cotton fiber diversity and evolution. As Gossypium diversified so did seed and trichome morphology. Extant species exhibit extraordinary variation in seed size and in the length, color, and density of the layer of single-celled trichomes on the seed surface (Fig. 2). Seed coverings range from nearly glabrous (e.g., G. klotzschianum and G. davidsonii), to short (several mm) stiff, brown hairs that aid in wind-dispersal (G. australe, G. nelsonii), to the long, fine white fibers that characterize improved forms of the four cultivated species. In all but the modern forms of the domesticated species, seed fibers are adherent to the seed coat. As noted above, a parallel domestication involved two species from the Americas, G. hirsutum and G. barbadense, and two from Africa-Asia, G. arboreum and G. herbaceum. In each case, aboriginal peoples discovered thousands of years ago that the unique properties of cotton fibers made them useful for ropes, textiles and other applications. A notable aspect of this history is that similar domestication processes resulted in apparently similar morphological transformations, including decreased plant stature, loss of photoperiod sensitivity, loss of seed dormancy, and most notably, a dramatic increase in the abundance, length, and quality of seed epidermal fiber (Fig. 2). Gossypium hirsutum presently accounts for >90% of the global cotton crop, having spread from its ancestral home in Mesoamerica to over 50 countries in both hemispheres. To understand developmental differences that account for fiber length variation and to place these differences in a phylogenetic context, Applequist et al. conducted SEM of ovules at and near the time of flowering, and generated growth curves. They showed that variation in mature morphologies reflects diversity during expansion, secondary wall synthesis, and maturation. Developmental profiles of the fibers of most wild species are similar, with fiber elongation terminating at ~14 days post-anthesis. In contrast, growth is extended to ~21 days in the A-genome and F-genome diploids. Prolonged elongation is thus phylogenetically (Fig. 1) revealed as a key evolutionary step in the origin of spinnable fiber, prior to domestication and in Africa. Our recent comparative expression profiling work suggests that the evolutionary transition leading to spinnable A-genome fiber involved a prolongation of an ancestral developmental program, as well as a novel metabolism involving enhanced regulation of reactive oxygen species.

Fig. 2. Variation in seed trichome (fiber) morphology in wild and domesticated cottons. Gossypium seeds exhibits remarkable variation among the ~50 wild and domesticated species. Illustrated are examples from wild species at both the diploid and allopolyploid levels. Early stages in fiber initiation are similar in all species, but developmental variation during primary and secondary wall deposition lead to radically different mature morphologies (Taxa studied here include domesticated and wild G. hirsutum (Cult. and Wild AD1, respectively) and G. barbadense (not shown)).

Domestication itself has been associated with further elongation at both the diploid and allopolyploid levels. This provokes speculation that the effects of parallel selection for long fiber in the cultivated species resulted in a genetically convergent or parallel transformation in the developmental program. Ongoing work using a microarray platform capable of distinguishing homoeologous transcripts, is testing this notion. Analyses also indicate a high level of novel expression of D-genome genes during fiber development in allopolyploid cotton. It may be that allopolyploidization provided the raw material necessary for the evolution of novel gene expression patterns, which subsequently were exploited by the aboriginal domesticators (and perhaps modern plant breeders) of G. hirsutum and G. barbadense. Superimposing the morphological/developmental variation and the multiple, parallel domestications on the organismal framework (Fig. 1) identifies the key transformations in cotton fiber evolution and improvement. This perspective provides the foundation for the proposed expression profiling experiments on phenotypically selected introgression lines.

 

Experimental Design – One of the exciting opportunities stimulated by the convergence of modern genomic approaches with other areas of biology is that of resolving the enigmatic processes by which new phenotypes arise. Here we propose a multifaceted program designed to further our understanding of the complex genetic architecture that underlies form, and to elucidate biological processes involved in developmental, agronomic, and evolutionary change. Using a well-developed model system from the cotton genus (Gossypium) and new genomic resources, we will reveal steps and complexities involved in transforming primitive trichomes to the economically important fibers of modern cotton cultivars. This experiment promises insight into fundamental biological processes underlying fiber development and evolution, while providing vital resources for cotton improvement. The research involves four interrelated components:

 

Component 1: Develop and characterize immortal introgression populations, to reduce complex morphology into defined constituents amenable to functional genomic analyses

 

  

Component 2: Developing an enriched EST resource for expression profiling, gene discovery, and SNP discovery

 

 

 

Component 3: Study perturbations in genetic networks and gene expression associated with naturally-occurring variation in fiber phenotypes using the introgression lines

 

 

 

Component 4: Provide the foundation for understanding the effects of selection on genetic diversity in cotton.