Teosinte Pollen Drive guides maize domestication and evolution by RNA interference [iPARE-seq]

Meiotic 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. Cryptic drive is thought to be pervasive and can be unleashed following hybridization with a naïve genome, resulting in sterility and hybrid incompatibility. Using single molecule and single pollen genome sequencing, we describe an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Zea mays ssp. mexicana), that depends on RNA interference (RNAi) in the male germline. Multiple hairpin-derived small RNA from mexicana target a novel domestication gene, Teosinte Drive Responder, that is required for pollen fertility and has undergone selection for immunity to RNAi. Introgression of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas. A survey of maize landraces and sympatric populations of teosinte mexicana reveals allelic bias at genes required for RNAi on at least 4 chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive likely played a major role in maize domestication, and offers an explanation for the widespread abundance of hairpin-encoded and other endogenous small RNA in the germlines of plants and animals. iPARE sequencing of Tpd (Tpd1+/-;Tpd2+/) and WT (tpd1;tpd2) bulk pollen