From noble beginnings as a prospective forage, polyploid Sorghum halepense ('Johnsongrass') is both an invasive species and one of the world's worst agricultural weeds. Formed by S. bicolor x S. propinquum hybridization, we show S. halepense to have S. bicolor-enriched allele composition and striking mutations in 5,957 genes that differentiate it from representatives of its progenitor species and an outgroup. The spread of S. halepense may have been facilitated by introgression from closelyrelated cultivated sorghum near genetic loci affecting rhizome development, seed size, and levels of lutein, a photochemical protectant and abscisic acid precursor. Rhizomes, subterranean stems that store carbohydrates and spawn clonal propagules, have growth correlated with reproductive rather than other vegetative tissues, and increase survival of both temperate cold seasons and tropical dry seasons. Rhizomes of S. halepense are more extensive than those of its rhizomatous progenitor S. propinquum, with gene expression including many alleles from its non-rhizomatous S. bicolor progenitor. The first surviving polyploid in its lineage in ∼96 million years, its post-Columbian spread across six continents carried rich genetic diversity that in the United States has facilitated transition from agricultural to non-agricultural niches. Projected to spread another 200-600 km northward in the coming century, despite its drawbacks S. halepense may offer novel alleles and traits of value to improvement of sorghum.

Perennial germplasm derived from crosses between Sorghum bicolor and either S. halepense or S. propinquum is being developed with the goal of preventing and reversing soil degradation in the world's grain sorghum-growing regions. Perennial grain sorghum plants produce subterranean stems known as rhizomes that sprout to form the next season's crop. In Kansas, breeding perennial sorghum involves crossing S. bicolor cultivars or breeding lines to S. halepense or perennial S. bicolor n × S. halepense breeding lines, selecting perennial plants from F 2 or subsequent populations, crossing those plants with S. bicolor, and repeating the cycle. A retrospective field trial in Kansas showed that selection and backcrossing during 2002-2009 had improved grain yields and seed weights of breeding lines. Second-season grain yields of sorghum lines regrowing from rhizomes were similar to yields in the first season. Further selection cycles have been completed since 2009. Many rhizomatous lines that cannot survive winters in Kansas are perennial at subtropical or tropical locations in North America and Africa. Grain yield in Kansas was not correlated with rhizomatousness in either Kansas or Uganda. Genomic regions affecting rhizome growth and development have been mapped, providing new breeding tools. The S. halepense gene pool may harbor many alleles useful for improving sorghum for a broad range of traits in addition to perenniality.

When developed, perennial grain sorghum could provide an opportunity for more ecologically sound food production. In 2002, we initiated a perennial sorghum breeding program, using Sorghum bicolor (L.) Moench 9 S. halepense (L.) Pers. populations. In 2011-2013, we evaluated 27 breeding lines from three stages of the program in field experiments to estimate response to selection during the program's first 7 years for perenniality and more domesticated phenotype. Regression analysis of mean grain yield and single-grain weight on breeding cycle (0, 1, 2) indicated a significant increase in each of the seeded experiments and for means over all years. For winter survival index, the regression coefficient was small but significant and negative in 2011, while non-significant in 2012. Grain yield was not significantly correlated with survival index, while single grain weight was significant and negatively correlated with survival index, with r = -0.4923. We conclude that combined selection for perenniality, a more domesticated phenotype, adaptation, greater grain size, and higher grain yield can result in progress in breeding perennial sorghum.

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 BC 1 F 1 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.

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