Teosinte Pollen Driveguides maize diversification and domestication by RNAi

Abstract

AbstractMeiotic drivers subvert Mendelian expectations by manipulating reproductive development to bias their own transmission. Chromosomal drive typically functions in asymmetric female meiosis, while gene drive is normally postmeiotic and typically found in males. Using single molecule and single-pollen genome sequencing, we describeTeosinte Pollen Drive, an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosintemexicana(Zea mays ssp. mexicana), that depends on RNA interference (RNAi). 22nt small RNAs from a non-coding RNA hairpin inmexicanadepend onDicer-Like 2 (Dcl2)and targetTeosinte Drive Responder 1 (Tdr1),which encodes a lipase required for pollen viability.Dcl2,Tdr1, and the hairpin are in tight pseudolinkage on chromosome 5, but only when transmitted through the male. Introgression ofmexicanainto early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas, and a tightly linked inversion inmexicanaspans a major domestication sweep in modern maize. A survey of maize landraces and sympatric populations of teosintemexicanareveals correlated patterns of admixture among unlinked genes required for RNAi on at least 4 chromosomes that are also subject to gene drive in pollen from synthetic hybrids.Teosinte Pollen Drivelikely played a major role in maize domestication and diversification, and offers an explanation for the widespread abundance of “self” small RNAs in the germlines of plants and animals.