|ARRO, JIE - University Of Illinois|
|PARK, JONG-WON - Texas A&M Agrilife|
|MAN WAI, CHING - University Of Illinois|
|VAN BUREN, ROBERT - University Of Illinois|
|NAGAI, CHIFUMI - Hawaii Agricultural Research Center|
|DA SILVA, JORGE - Texas A&M Agrilife|
|MING, RAY - University Of Illinois|
Submitted to: Euphytica
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/2/2016
Publication Date: 3/7/2016
Publication URL: https://handle.nal.usda.gov/10113/63058
Citation: Arro, J., Park, J.-W., Wai, C. M., Van Buren, R., Pan, Y.-B., Nagai, C., Da Silva, J., Ming, R. 2016. Balancing selection contributed to domestication of autopolyploid sugarcane (Saccharum officinarum L.). Euphytica. 209:477-493. DOI: 10.1007/s10681-016-1672-8
Interpretive Summary: Sugarcane is a source of plant sugar and a promising biofuel feedstock. Because of multiple sets of chromosomes in the nucleus of sugarcane, the genetic basis of sugar yield and its components remains unresolved despite numerous genetic linkage and association mapping studies. In this study, vegetative clones of three ancestral species of sugarcane (Saccharum), including 15 clones of domesticated species S. officinarum, 15 clones of wild species S. robustum, and 18 clones of wild species S. spontaneum, were subject to genome-wide scans based on second generation nucleotide sequencing data called RNA-seq using two plant tissues, namely, leaf and stem. A total of 2.3 billion RNA-seq reads were obtained, from which 2.8 million single nucleotide polymorphism (SNP) markers were detected. Major findings: 1) there was a high level of genetic differentiation among the three species, especially among genes expressed in the stem tissues; 2) variability among SNP markers was not higher than the average genetic differentiation, suggesting that frequencies of various SNP markers were maintained in equilibrium in each species perhaps as a result of balancing selection; 3) a large number of genes in S. officinarum showed relatively high per-site heterozygosity, including genes related to sucrose accumulation; and 4) genes detected at intermediate-frequencies were prevalent in Saccharum, due probably to its vegetative reproduction background. About 180 candidate genes for domestication were identified in S. officinarum. Although rare forms of genes associated with sucrose accumulation tended to show higher frequencies among the clones of the wild species S. spontaneum and S. robustum, higher nucleotide diversity was detected among domesticated S. officinarum clones. These results will help explore the molecular mechanism of selection and domestication in Saccharum evolution.
Technical Abstract: Sugarcane is a source of plant sugar and a promising biofuel feedstock. The genetic basis of sugar yield and its components remain unresolved despite numerous genetic linkage and association mapping studies because of its complex polyploid genome. Genome-wide scans to identify genes or regions in the genome involved in the transition from wild to cultivated species may provide additional resolution on the genetic control of traits such as sucrose accumulation in a complex polyploid like sugarcane. A total of 2.8 million SNPs were found from 2.3 billion RNA-seq reads generated from leaf and stalk tissues of 15 S. officinarum, 15 S. robustum, and 18 S. spontaneum accessions. There is a high allelic diversity in Saccharum, especially among genes expressed in the stalk tissues where S. officinarum (Fst = 0.69) has 67% higher allele diversity than its wild relative S. spontaneum (Fst = 0.41). While there is a considerable level of genetic differentiation among the three species, there were no SNP loci statistically higher than the average genetic differentiation, suggesting that allele frequencies are maintained in polymorphic equilibrium in each species perhaps as a result of balancing selection. This is corroborated by both nucleotide diversity and site frequency spectrum (SFS) patterns showing a large number of genes in the domesticated S. officinarum having relatively high per-site heterozygosity, including genes related to sucrose accumulation. Around 180 candidate domestication genes were chosen in S. officinarum based on the prevalence of balancing selection and excess singleton SNPs. Saccharum is characterized by the prevalence of intermediate-frequency alleles in the context of a heterozygous and predominantly asexual reproduction. Genes associated with sucrose accumulation tend to show higher frequencies of rare alleles among the wild species S. spontaneum and S. robustum but a higher nucleotide diversity (per-site heterozygosity) in domesticated S. officinarum. Thus, it could be that the emergence of the sugar-bearing species S. officinarum is due to the spread of a few new alleles related to sucrose accumulation maintained at a heterozygous state at each single locus.