Diverse origins of waxy foxtail millet crops in East and Southeast Asia mediated by multiple transposable element insertions

Abstract

The naturally occurring waxy and low-amylose variants of foxtail millet and other cereals, like rice and barley, originated in East and Southeast Asia under human selection for sticky foods. Mutations in the GBSS1 gene for granule-bound starch synthase 1 are known to be associated with these traits. We have analyzed the gene in foxtail millet, and found that, in this species, these traits were originated by multiple independent insertions of transposable elements and by subsequent secondary insertions into these elements or deletion of parts of the elements. The structural analysis of transposable elements inserted in the GBSS1 gene revealed that the non-waxy was converted to the low-amylose phenotype once, while shifts from non-waxy to waxy occurred three times, from low amylose to waxy once and from waxy to low amylose once. The present results, and the geographical distribution of different waxy molecular types, strongly suggest that these types originated independently and were dispersed into their current distribution areas. The patterns of GBSS1 variation revealed here suggest that foxtail millet may serve as a key to solving the mystery of the origin of waxy-type cereals in Asia. The GBSS1 gene in foxtail millet provides a new example of the evolution of a gene involved in the processes of domestication and its post-domestication fate under the influence of human selection.

Foxtail Millet: A Sequence-Driven Grass Model System

“…This has been interpreted as supporting multiple domestications of foxtail millet Sakamoto, 1984, 1987;Jusuf and Pernes, 1985;Fukunaga et al, 1997Fukunaga et al, , 2002Fukunaga et al, , 2005Fukunaga et al, , 2006Li et al, 1998;Nakayama et al, 1998;Le Thierry d'Ennequin et al, 2000;Benabdelmouna et al, 2001;Kawase et al, 2005), followed by episodes of genetic introgression from green millet (Darmency et al, 1987;Wang et al, 1995;Jarvis and Hodgkin, 1999). Green millet is a serious weed, not only of foxtail millet, but of wheat and other temperate cropping systems worldwide (Defelice, 2002;Dekker, 2003).…”

Dramatic amplification of a rice transposable element during recent domestication

“…Many plant genes, in contrast, contain members of TE families that have recently proliferated and, as such, provide opportunities to observe the impact of TEs on gene expression and allelic diversification (5)(6)(7). Miniature inverted-repeat TEs (MITEs) are the predominant TE associated with plant genes.…”

Genetic structure of landraces in foxtail millet (Setaria italica(L.) P. Beauv.) revealed with transposon display and interpretation to crop evolution of foxtail millet

“…This fact indicated that people in early Asia favored and repeatedly selected for the sticky endosperm trait of waxy phenotype generated by TE insertions (Kawase et al 2005). …”

“…In foxtail millet, several TEs including LTR-retrotransposons and MITEs have been identified in the mutant alleles of Waxy (GBSS1) gene, which controls amylose content in the endosperm starch (Fukunaga et al 2002a;Kawase et al 2005). This fact indicated that people in early Asia favored and repeatedly selected for the sticky endosperm trait of waxy phenotype generated by TE insertions (Kawase et al 2005).…”