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Social Impact Statement Although tremendously successful at feeding humanity, row crop agriculture based on annuals contributes to numerous ecosystem dis‐services, ranging from soil degradation and aquatic eutrophication to greenhouse gas production. In contrast, perennial grain crops (which produce harvests for multiple seasons from single plantings) have the potential to provide valuable regulating and supporting ecosystem services in addition to food production. In particular, losses of ecological capital that threaten permanent food insecurity such as ~1% of global soil per year are expected to be mitigated or even reversed by crops that combine the high yield realized by scientific breeding via multiple cropping cycles from single plantings. Summary Perennial herbaceous may provide food and biomass while preserving ecological capital and reducing energy inputs. Sorghum has two perennial relatives and rich morphological diversity being used to breed for perenniality. We elucidate genetic determinants of rhizomatousness and survival, in two BC1F2 populations totaling 246 genotypes derived from backcrossing different annual Sorghum bicolor X perennial S. halepense F1 plants to a tetraploidized S. bicolor. RNA‐seq assisted in identifying candidate genes for rhizomatousness. Correspondence of rhizomatousness quantitative trait loci (QTLs) with those from two populations derived from crosses between S. halepense progenitors S. bicolor X S. propinquum suggests either the preservation of interspecific polymorphism or the formation of novel alleles following polyploid S. halepense formation. Correspondence of tillering and branching QTLs further supports their developmental. Identification of genes from RNA‐seq study within QTL intervals provides insight toward discovery of causal rhizomatous genes. An unexpected finding from both S. halepense‐ and S. propinquum‐derived populations is that alleles contributing to late flowering are related to reduced rhizomatousness. Twelve of 16 QTL regions conferring rhizomatousness fall in paleo‐duplicated regions tracing to single ancestral regions 96 million years ago, indicating that corresponding genes in these regions have retained similar functions since the duplication event.

Despite a “ploidy barrier,” interspecific crosses to wild and/or cultivated sorghum (Sorghum bicolor, 2n = 2x = 20) may have aided the spread across six continents of Sorghum halepense, also exemplifying risks of “transgene escape” from crops that could make weeds more difficult to control. Genetic maps of two BC1F1 populations derived from crosses of S. bicolor (sorghum) and S. halepense with totals of 722 and 795 single nucleotide polymorphism (SNP) markers span 37 and 35 linkage groups, with 2–6 for each of the 10 basic sorghum chromosomes due to fragments covering different chromosomal portions or independent segregation from different S. halepense homologs. Segregation distortion favored S. halepense alleles on chromosomes 2 (1.06–4.68 Mb, near a fertility restoration gene), 7 (1.20–6.16 Mb), 8 (1.81–5.33 Mb, associated with gene conversion), and 9 (47.5–50.1 Mb); and S. bicolor alleles on chromosome 6 (0–40 Mb), which contains both a large heterochromatin block and the Ma1 gene. Regions of the S. halepense genome that are recalcitrant to gene flow from sorghum might be exploited as part a multi-component system to reduce the likelihood of spread of transgenes or other modified genes. Its SNP profile suggests that chromosome segments from its respective progenitors S. bicolor and Sorghum propinquum have extensively recombined in S. halepense. This study reveals genomic regions that might discourage crop-to-weed gene escape, and provides a foundation for marker-trait association analysis to determine the genetic control of traits contributing to weediness, invasiveness, and perenniality of S. halepense.

Johnsongrass (Sorghum halepense) is a striking example of a post-Columbian founder event. This natural experiment within ecological time-scales provides a unique opportunity for understanding patterns of continent-wide genetic diversity following range expansion. Microsatellite markers were used for population genetic analyses including leaf-optimized Neighbor-Joining tree, pairwise FST, mismatch analysis, principle coordinate analysis, Tajima's D, Fu's F and Bayesian clusterings of population structure. Evidence indicates two geographically distant introductions of divergent genotypes, which spread across much of the US in