Teosinte Pollen Drive guides maize diversification and domestication by RNAi

Benjamin Berube, Evan Ernst, Jonathan Cahn, Benjamin Roche, Cristiane Santis Alves, Jason Lynn, Armin Scheben, Daniel Grimanelli, Adam Siepel, Jeffrey Ross-Ibarra, Jerry Kermicle and Robert A. Martienssen ()
Additional contact information
Benjamin Berube: Cold Spring Harbor Laboratory
Evan Ernst: Cold Spring Harbor Laboratory
Jonathan Cahn: Cold Spring Harbor Laboratory
Benjamin Roche: Cold Spring Harbor Laboratory
Cristiane Santis Alves: Cold Spring Harbor Laboratory
Jason Lynn: Cold Spring Harbor Laboratory
Armin Scheben: Cold Spring Harbor Laboratory
Daniel Grimanelli: Université de Montpellier
Adam Siepel: Cold Spring Harbor Laboratory
Jeffrey Ross-Ibarra: University of California at Davis
Jerry Kermicle: University of Wisconsin
Robert A. Martienssen: Cold Spring Harbor Laboratory

Nature, 2024, vol. 633, issue 8029, 380-388

Abstract: Abstract Selfish genetic elements contribute to hybrid incompatibility and bias or ‘drive’ their own transmission1,2. Chromosomal drive typically functions in asymmetric female meiosis, whereas gene drive is normally post-meiotic and typically found in males. Here, using single-molecule and single-pollen genome sequencing, we describe Teosinte Pollen Drive, an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Z. mays ssp. mexicana) that depends on RNA interference (RNAi). 22-nucleotide small RNAs from a non-coding RNA hairpin in mexicana depend on Dicer-like 2 (Dcl2) and target Teosinte 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 of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas3, and a tightly linked inversion in mexicana spans a major domestication sweep in modern maize4. A survey of maize traditional varieties and sympatric populations of teosinte mexicana reveals correlated patterns of admixture among unlinked genes required for RNAi on at least four chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive probably had a major role in maize domestication and diversification, and offers an explanation for the widespread abundance of ‘self’ small RNAs in the germ lines of plants and animals.

Date: 2024
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DOI: 10.1038/s41586-024-07788-0

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