A generalist-specialist trade-off between switchgrass cytotypes impacts climate adaptation and geographic range.

Polyploidy results from whole-genome duplication and is a unique form of heritable variation with pronounced evolutionary implications. Different ploidy levels, or cytotypes, can exist within a single species, and such systems provide an opportunity to assess how ploidy variation alters phenotypic novelty, adaptability, and fitness, which can, in turn, drive the development of unique ecological niches that promote the coexistence of multiple cytotypes. Switchgrass, Panicum virgatum, is a widespread, perennial C4 grass in North America with multiple naturally occurring cytotypes, primarily tetraploids (4×) and octoploids (8×). Using a combination of genomic, quantitative genetic, landscape, and niche modeling approaches, we detect divergent levels of genetic admixture, evidence of niche differentiation, and differential environmental sensitivity between switchgrass cytotypes. Taken together, these findings support a generalist (8×)­specialist (4×) trade-off. Our results indicate that the 8× represent a unique combination of genetic variation that has allowed the expansion of switchgrass' ecological niche and thus putatively represents a valuable breeding resource.

Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass.

Long-term climate change and periodic environmental extremes threaten food and fuel security1 and global crop productivity2-4. Although molecular and adaptive breeding strategies can buffer the effects of climatic stress and improve crop resilience5, these approaches require sufficient knowledge of the genes that underlie productivity and adaptation6-knowledge that has been limited to a small number of well-studied model systems. Here we present the assembly and annotation of the large and complex genome of the polyploid bioenergy crop switchgrass (Panicum virgatum). Analysis of biomass and survival among 732 resequenced genotypes, which were grown across 10 common gardens that span 1,800 km of latitude, jointly revealed extensive genomic evidence of climate adaptation. Climate-gene-biomass associations were abundant but varied considerably among deeply diverged gene pools. Furthermore, we found that gene flow accelerated climate adaptation during the postglacial colonization of northern habitats through introgression of alleles from a pre-adapted northern gene pool. The polyploid nature of switchgrass also enhanced adaptive potential through the fractionation of gene function, as there was an increased level of heritable genetic diversity on the nondominant subgenome. In addition to investigating patterns of climate adaptation, the genome resources and gene-trait associations developed here provide breeders with the necessary tools to increase switchgrass yield for the sustainable production of bioenergy.

Genome-wide associations with flowering time in switchgrass using exome-capture sequencing data.

Flowering time is a major determinant of biomass yield in switchgrass (Panicum virgatum), a perennial bioenergy crop, because later flowering allows for an extended period of vegetative growth and increased biomass production. A better understanding of the genetic regulation of flowering time in switchgrass will aid the development of switchgrass varieties with increased biomass yields, particularly at northern latitudes, where late-flowering but southern-adapted varieties have high winter mortality. We use genotypes derived from recently published exome-capture sequencing, which mitigates challenges related to the large, highly repetitive and polyploid switchgrass genome, to perform genome-wide association studies (GWAS) using flowering time data from a switchgrass association panel in an effort to characterize the genetic architecture and genes underlying flowering time regulation in switchgrass. We identify associations with flowering time at multiple loci, including in a homolog of FLOWERING LOCUS T and in a locus containing TIMELESS, a homolog of a key circadian regulator in animals. Our results suggest that flowering time variation in switchgrass is due to variation at many positions across the genome. The relationship of flowering time and geographic origin indicates likely roles for genes in the photoperiod and autonomous pathways in generating switchgrass flowering time variation.

Population genomic variation reveals roles of history, adaptation and ploidy in switchgrass.

Geographic patterns of genetic variation are shaped by multiple evolutionary processes, including genetic drift, migration and natural selection. Switchgrass (Panicum virgatum L.) has strong genetic and adaptive differentiation despite life history characteristics that promote high levels of gene flow and can homogenize intraspecific differences, such as wind-pollination and self-incompatibility. To better understand how historical and contemporary factors shape variation in switchgrass, we use genotyping-by-sequencing to characterize switchgrass from across its range at 98 042 SNPs. Population structuring reflects biogeographic and ploidy differences within and between switchgrass ecotypes and indicates that biogeographic history, ploidy incompatibilities and differential adaptation each have important roles in shaping ecotypic differentiation in switchgrass. At one extreme, we determine that two Panicum taxa are not separate species but are actually conspecific, ecologically divergent types of switchgrass adapted to the extreme conditions of coastal sand dune habitats. Conversely, we identify natural hybrids among lowland and upland ecotypes and visualize their genome-wide patterns of admixture. Furthermore, we determine that genetic differentiation between primarily tetraploid and octoploid lineages is not caused solely by ploidy differences. Rather, genetic diversity in primarily octoploid lineages is consistent with a history of admixture. This suggests that polyploidy in switchgrass is promoted by admixture of diverged lineages, which may be important for maintaining genetic differentiation between switchgrass ecotypes where they are sympatric. These results provide new insights into the mechanisms shaping variation in widespread species and provide a foundation for dissecting the genetic basis of adaptation in switchgrass.