Feature: The remarkable cotton genome

Read part I, Genetics and the origins of modern cotton.

Professor Jonathan Wendel, of the Department of Ecology, Evolutionary and Organismal Biology at Iowa State University in Ames, Iowa, describes Gossypium as “a fantastic genus”, and says upland cotton still blows him away. “For a long time, people have been trying to find the genes that have made today’s crops what they are. Cotton is an ideal model for studying the integration and regulation of gene expression in polyploid crops.

“To put the creation of cotton in context, every gene in the genome was doubled, and the two genomes now carried two families of transposable elements. They were very different organisms, with different morphologies, yet somehow, everything still worked when they fused.

“That led me into the mystery of how evolution worked to reconcile the conflicts between two genomes in the cells of one plant. There was an immediate doubling of genome content, and two entirely different regulatory systems had to merge and resolve all their differences.

“That’s why understanding what went on in cotton is so important to understanding how genomes are regulated and interact in all polyploid plants. Wheat is perhaps is another famous example of a polyploid crop, and a very active polyploidy research community has developed around wheat and cotton, whose origins are lost in the mists of prehistory.

“We’re now looking at cotton in the context of genomic control of expression levels, and finding all sorts of weird and wonderful mechanisms for reciprocal silencing of equivalent genes, involving tiny RNA regulatory molecules. We’re trying to understand what that means functionally, and how it influences crop productivity. The research keeps exploding into new areas.”

It is increasingly clear that selection pressure from different human cultures resulted in massive changes in genome function in the wild progenitors of the four modern domesticated Gossypium species – the two diploids from Africa and Asia, and the two tetraploids the Americas.

Studying the changes in genome function between the domesticated species and their wild progenitors is like “rewinding the genetic tape of domestication.

“They took the tropical, photoperiod-sensitive progenitors of today’s cotton varieties, with their crappy, coarse fibres and, knowing nothing about genetics, developed annualised plants with long, strong fibres that a superior to those of both diploid parents.”

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Changes

“The American D genome progenitors have crummy-looking, short, tightly appressed, non-spinnable epidermal trichomes [fibres], yet it contributed a lot of the genes that make cotton what it is today. We’re trying to work out which genes were involved.

“Domestication upregulated entire families of genes. Some of the improvements involved upregulated transcription factors that influenced whole networks of genes. There has been massive over-writing of one family of ribosomal RNA genes by another. The changes don’t just involve upregulation; we’re also starting to look at the pattern of expression of duplicated genes over time.

“We can recreate the allotetraploids from their diploid progenitors, to see how their transcriptomes have changed under domestication and we are using the same experimental framework to studying changes in the expression of small regulatory RNAs.

“I’ve taken single cells from wild versus domesticated forms of G. hirsutum and studied their transcriptomes during the formation of the primary and secondary cell walls. Three days after cell-wall synthesis begins, we see 10,000 differences in gene expression, even though we suspect that that only 10 to 20 major mutations separate them.

“What does that tell us about the complexity of the genetics, and the intricacies of development, and how humans, selecting only on the basis of phenotypes resulting from a relatively small number of mutations, have caused changes that have propagated through cellular gene networks to affect the expression of 10,000 genes?

“We have a 10,000-dimensional network of gene expression, acting through the proteome, which alters cell metabolism and physiology to create new phenotypes for human selection. It has been a huge lesson, and it has fundamentally changed the way I think about evolutionary biology.

“It raises new questions: what controls the microRNAs and short interfering RNAs, and how they regulate the activity of two completely different sets of transposable elements?

“One of my great interests is in why polyploidy has been so important in plant evolution, and in the generation of biodiversity. All plants and animals are polyploids, so it must be important.

“But until now efforts to explain polyploidy have usually relied on ‘just-so stories’ about polyploid organisms having greater flexibility to adapt to hostile environments, or new environmental niches. There really hasn’t been much direct experimental evidence for these ideas.

“Evolution always occurs within an ecological context, and cotton provides one of the first good ecological models. Polyploidy is good because it gives organisms extra genes to experiment with. They are the fodder for natural selection, but they are an extra cost to the cell, so the process must involve many trade-offs.

“Inevitably, polyploids will defy any effort to rope all the explanations into one corner. Evolution has as many ways to skin a cat as there are potential interactions between all the genes in a genome – or two genomes.”