Abstract
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 closely-related 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.
Highlights
Cytological, morphological (Celarier, 1958; Doggett, 1976), and molecular data (Paterson et al, 1995) suggest that tetraploid Sorghum halepense (2n = 40) arose as a naturally occurring hybrid between S. bicolor (2n = 20), an annual, polytypic African species which includes cultivated sorghum; and S. propinquum (2n = 20), a perennial southeast Asian native of moist habitats
Assuming that tetraploid S. halepense has twice the 41,800,275 bp coding DNA sequence (CDS) length of the S. bicolor reference genome (Paterson et al, 2009) (Table 1 and Supplementary Table 1), 99.4% of S. halepense CDS nucleotides match those of representatives of ‘eusorghum (Kellogg, 2013; Hawkins et al, 2015)’ progenitor species S. bicolor (Paterson et al, 2009) and S. propinquum (SRX030701-03), and an outgroup Sorghum [Sarga (Hawkins et al, 2015)] timorense (SRX124552)
This is consistent with largely normal pairing and recombination between S. bicolor and S. propinquum diploids that is wellknown from genetic studies (Chittenden et al, 1994; Paterson et al, 1995; Kong et al, 2015), and with segregation patterns in two interspecific (S. bicolor x S. halepense) BC1F1 populations that suggest a mixture of disomic and polysomic inheritance (Kong, 2017)
Summary
Cytological, morphological (Celarier, 1958; Doggett, 1976), and molecular data (Paterson et al, 1995) suggest that tetraploid Sorghum halepense (2n = 40) arose as a naturally occurring hybrid between S. bicolor (2n = 20), an annual, polytypic African species which includes cultivated sorghum; and S. propinquum (2n = 20), a perennial southeast Asian native of moist habitats. Used as forage and even food (seed/flour), S. halepense has spread in postColumbian times from its hypothesized west Asian center of origin across much of Asia, Africa, Europe, North and South America, and Australia. While sorghum largely remained confined to cultivation, S. halepense readily naturalized and has spread across much of North America, both to agricultural and non-agricultural habitats (Sezen et al, 2016) – suggesting capabilities for adaptation well beyond those of sorghum. Its ability to cross with sorghum despite a ploidy barrier (reviewed in Warwick and Black, 1983; Tang and Liang, 1988) makes Johnsongrass a paradigm for the dangers of crop ‘gene escape,’ and restricts deployment of many transgenes that could reduce the cost and increase the stability of sorghum production
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