Teosinte Pollen Drive guides maize domestication and evolution by RNA interference [small RNA-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. Overall design: Small RNA sequencing of Tpd1/tpd1;Tpd2/tpd2 and tpd1;tpd2 pollen and leaf, and dcl2T-/- and dcl2-mu1-/- pollen减数分裂驱动因子通过调控生殖发育以偏向自身传递，从而打破孟德尔遗传定律的预期。染色体驱动通常在不对称的雌性减数分裂中发挥作用，而基因驱动则多发生于减数分裂后阶段，且常见于雄性个体。隐性驱动被认为广泛存在，当其与未接触过该驱动的基因组杂交后可被激活，进而引发不育与杂交不亲和现象。本研究借助单分子测序与单花粉基因组测序技术，报道了玉米（Zea mays ssp. mays）与墨西哥类玉米（Zea mays ssp. mexicana）杂交后代中存在的一例基因驱动现象，该过程依赖于雄性生殖系中的RNA干扰（RNA interference, RNAi）通路。多个源自墨西哥类玉米的发夹结构衍生小RNA可靶向作用于一个新的驯化基因——类玉米驱动响应因子（Teosinte Drive Responder），该基因是花粉育性所必需的，且已进化出抵御RNA干扰的免疫能力。墨西哥类玉米向早期栽培玉米的渐渗事件，被认为对玉米在整个美洲的地理扩散起到了关键作用。对玉米地方品种与墨西哥类玉米同域种群的调查显示，至少有4条染色体上的RNAi相关基因存在等位基因偏倚，这些基因在人工合成杂交种的花粉中同样受到基因驱动的作用。类玉米花粉驱动很可能在玉米驯化过程中发挥了重要作用，同时也解释了为何动植物生殖系中广泛存在大量由发夹结构编码的内源小RNA及其他内源小RNA。实验设计概述：对Tpd1/tpd1;Tpd2/tpd2与tpd1;tpd2植株的花粉及叶片，以及dcl2T-/-和dcl2-mu1-/-植株的花粉进行小RNA测序。