Genome-wide transcriptional changes associated with allopolyploidy and fiber domestication in cotton (Gossypium spp. L.)

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2009-01-01
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Rapp, Ryan
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Jonathan F. Wendel
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Ecology, Evolution, and Organismal Biology
Abstract

Interspecific hybridization and subsequent genome doubling (allopolyploidy) is a common phenomenon in flowering plant lineages. Within the cotton genus, Gossypium L., two diploid species merged 1-2 mya to form an allopolyploid species that would eventually give rise to 5 distinct species; two of which would be domesticated and dominate world cotton commerce. This series of experiments examines two facets of the human-entwined evolution of the Gossypium genus: one, genome-wide expression alterations associated with the formation of nascent allopolyploids and two, the transcriptome-wide changes in fiber, concomitant with domestication.

To better understand the genome-wide transcriptional changes that occur during the formation of nascent polyploids, these experiments examined the transcriptional state of two sets of diploid parents and their synthetic, colchicine doubled, allopolyploid derivatives. Specifically, RNA from leaf tissue for each trio (maternal, paternal and colchicine-doubled synthetic) was hybridized to a custom Nimblegen microarray platform capable of interrogating over 40,000 unique loci with an average of 7 probes. For each trio, we grew 5 individuals in a random block design in each of 3 growth chambers. We pooled RNA from these individuals to create 3 samples per chamber, per taxon, per trio, for a total of 54 slides. To understand the context of genome wide expression levels in the nascent allotetraploid plants, we compared the expression levels of the allotetraploid to that of its two progenitors and a midparent in silico value derived from a combination of the mean expression value and the combined deviation. The analysis revealed a strong bias of per-gene expression values in the allotetraploids toward one parent in each trio. In one trio the allotetraploid is heavily biased to the paternal genome donor and in the other trio biased to the maternal donor, indicating the direction of the cross does not control dominance. Additionally, the dominance effect is bi-directional, where the allotetraploid may be up- or down-regulated to match the dominant parent. These data offer intriguing insight into the potential evolutionary relevance of polyploids in plant diversification.

To understand the genome-wide expression changes associated with domestication, we examined the global transcriptional state of developing fiber in three separate domesticated cotton species and their wild progenitors. Cotton plants from the allotetraploid species G. hirsutum, G. barbadense and the diploid G. herbaceum were grown alongside their wild progenitors. Beginning 2 days post anthesis (dpa) we isolated fiber from wild-domesticate contrasts at 5 time points corresponding to just after initiation, primary expansion, primary cell wall growth, the transition to secondary cell wall growth and secondary cell wall deposition. When compared to their wild counterparts, we diagnose >5,000 unique genes differentially expressed in each contrast yet only a small group (611) shared among all; potentially illustrating that parallel morphological domestication may have convergent origins at the molecular level. Many genes whose products are directly relevant to cell wall and fiber biogenesis were diagnosed as differentially expressed, including the cell wall biosynthetic machinery, cytoskeletal structural and modifying proteins, members of apoptotic pathways, primary hormone receptors and transcriptional factors known to be key regulators of trichome and fiber development.

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Thu Jan 01 00:00:00 UTC 2009