Artificial selection during crop domestication has dramatically shaped many wild plant species into high yielding food, fiber, medicinal, and biofuel crops. The trajectory from wild to domesticated is a long and complex process that leaves strong signatures of selection on the genome. Here we use a population genetics approach and transcriptome survey to scan for signatures of selection and domestication in sugarcane (Saccharum), the leading source of global sugar production. The sugarcane genome is highly complex, with ploidy levels ranging from 8n-14n. This complexity has hindered advances in marker assisted breeding and subjects sugarcane to a unique set of evolutionary forces not experienced during the domestication of most diploid crop species. Modern sugarcane is an interspecific hybrid mainly between the cultivated S. officinarum (2n=80) and the wild species S. spontaneum (2n=40-128), with some marginal contribution from S. robustum (2n=60-200) in a few breeding stations. We screened 48 representative accessions of the domesticated S. officinarum and the wild species S. spontaneum and S. robustum to identify genes selected during domestication. 2.8 million single nucleotide polymorphisms (SNPs) were found from 2.2 billion RNA-seq reads generated from leaf and stalk tissue. S. officinarum has twice as much inter-population allelic diversity compared to S. spontaneum and to S. robustum. The stalk transcriptome has more allele diversity than the leaf, reflective of gene expression changes during domestication. The allele diversity in Saccharum is characterized by the prevalence of intermediate-allele frequency typical of a balancing selection and reflective of the high degree of heterozygosity in this species. The population structure of sugarcane does not render to conventional population genetics tests for signals of selection due to the dynamics imposed by fixed heterozygosity. Site frequency spectrum (SFS) pattern describes higher per-site heterozygosity in genes that might be targets of domestication. Around 200 candidate domestication genes were detected in S. officinarum based on the prevalence of balancing selection among ~3000 SNPs.To gain insight into the nature of gene expression divergence in Saccharum, we conducted a comparative transcriptome profiling of leaf and stalk developmental stages in S. officinarum, S. spontaneum and S. robustum. A summary of all the pairwise differential expression tests shows 3,346 genes were differentially expressed between the cultivated and the wild species, most of which were observed in immature stalk and mature leaf tissues. Maturation of stalks and leaves seems to be associated with significant transcript abundance in gene networks related to post-embryonic morphogenesis, lipid localization and perturbation of the phenylpropanoid pathway. This suggests that expression between the cultivated and wild Saccharum are related to differences related to maturation and response to external stimuli, in general, and the biomass accumulation, in particular.In addition, genes associated with sugar metabolism and transport have dynamic expression in the surveyed tissues, reflective of the known source-sink feedback signaling for sucrose accumulation in the sugar-bearing Saccharum species. While these studies might highlight the unique challenges imposed by a complicated genome of Saccharum, the results presented also elucidate the population genetics and expression pattern dynamics of this highly complex, heterozygous, autopolyploid crop.
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Evolution and domestication of Saccharum using transcriptomic analyses
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