Domestication and Spread of Broomcorn Millet (Panicum miliaceum L.) Revealed by Phylogeography of Cultivated and Weedy Populations

Abstract

Cultivated broomcorn millet (Panicum miliaceum L.), one of the most ancient crops, has long been an important staple food in the semiarid regions of Eurasia. Weedy broomcorn millet (Panicum ruderale (Kitag.) Chang comb. Nov.), the companion weed of cultivated broomcorn millet, is also widely distributed throughout Eurasia and can produce fertile offspring by crossing with cultivated broomcorn millet. The evolutionary and genetic relationships between weedy and cultivated broomcorn millets, and the explicit domestication areas and detailed spread routes of this cereal are still unclear. The genetic diversity and population structure of 200 accessions of weedy and cultivated broomcorn millets were explored to elucidate the genetic relationship between weedy and cultivated broomcorn millets, and to trace the explicit domestication areas and detailed spread routes of broomcorn millets by using 23 simple sequence repeats (SSR) markers. Our results show that the weedy populations in China may harbor the ancestral variations that gave rise to the domesticated broomcorn millet. The population structure pattern observed in the wild and domesticated broomcorn millets is consistent with the hypothesis that there may be at least two independent domestication areas in China for the cultivated broomcorn millet, the Loess Plateau and the Northeast China, with both following the westward spread routes. These two westward spread routes of cultivated broomcorn millet coincide exactly with the prehistoric Oasis Route and Steppe Route, respectively.

Genetic Divergence and Population Structure in Weedy and Cultivated Broomcorn Millets (Panicum miliaceum L.) Revealed by Specific-Locus Amplified Fragment Sequencing (SLAF-Seq)

“…The genetic diversity indices ( H O , H E , and π) of the cultivated broomcorn millets were significantly lower than those of the weedy broomcorn millets across the entire genome ( p < 0.05) ( Table 1 ). Similarly, higher genetic diversity in weedy broomcorn millet was also observed in our previous comparative studies of weedy and cultivated broomcorn millet based on microsatellite markers ( Xu et al, 2019 ). The decreased genetic diversity in cultivated broomcorn millet compared with that of weedy broomcorn millet is consistent with the hypothesis that domestication process causes a genetic bottleneck, which decreases genetic diversity in crops in comparison to their progenitors ( Doebley et al, 2006 ).…”

“…The endoferal types are formed from a single domesticated lineage and the exoferal types are derived via admixture, either among domesticated lineages or between domesticated taxa and their wild relatives ( Barazani et al, 2016 ; Wang et al, 2017 ; Gering et al, 2019 ; Page et al, 2019 ). Although both the wild and the feral types were found in weedy broomcorn millet in our previous investigation ( Xu et al, 2019 ), the genetic difference between wild and feral types has not been clarified. In the present study, the genetic polymorphism of weedy broomcorn millet was further explored at genomic level.…”

“…On the other hand, it was suggested that the Western Liao River Basin in Northeast China might be the domestication area due to the discovery of abundant seed remains of broomcorn millet in Xinglonggou site (8,000–7,500 years ago) in this area ( Zhao, 2004 ). Recently, results of our study based on microsatellite markers suggested that two different genetic clusters were probably derived from Loess Plateau and Northeast China, respectively ( Xu et al, 2019 ). However, the existence of alternative domestication areas for some other genetic clusters was not completely ruled out.…”

“…As the only weedy species in the genus Panicum exhibiting a widespread distribution across a region spanning from northern China to western Eurasia, weedy broomcorn millet was thought to be either the descendant of the wild ancestor of cultivated broomcorn millet which had never been domesticated ( De Wet, 1992 ; Wang, 2006 ) or a feral type formed by either reverse mutations of cultivars ( Scholz, 1983 ) or introgression between cultivars and their wild relatives ( You, 1984 ). It has been suggested that the weedy broomcorn millet in China may be composed of both wild and feral types based on microsatellite markers, while the wild type may harbor the ancestral variations that gave rise to the cultivated broomcorn millet ( Xu et al, 2019 ). However, the feral individuals could not be distinguished from the wild individuals.…”

“…Furthermore, two spread routes from the domestication areas in northern China to the western end of Eurasia have been proposed based on archeological and genetic evidence. One is the “Oasis Route” starting from northern China to southern Central Asia, West Asia, and Europe through the “Inner Asia mountain corridor zone” and the other is the “Steppe Route” starting from the Northeast China, passing through the Mongolian Plateau and South Siberia, to Europe ( Spengler et al, 2014 , 2016 ; Miller et al, 2016 ; Xu et al, 2019 ). However, the detailed pathways of these two routes and possibly other routes are not clear.…”