A farnesyl pyrophosphate synthase gene expressed in pollen functions in S ‐ RN ase‐independent unilateral incompatibility

Summary Multiple independent and overlapping pollen rejection pathways contribute to unilateral interspecific incompatibility ( UI ). In crosses between tomato species, pollen rejection usually occurs when the female parent is self‐incompatible ( SI ) and the male parent self‐compatible ( SC ) (the ‘ SI × SC rule’). Additional, as yet unknown, UI mechanisms are independent of self‐incompatibility and contribute to UI between SC species or populations. We identified a major quantitative trait locus on chromosome 10 ( ui10.1 ) which affects pollen‐side UI responses in crosses between cultivated tomato, Solanum lycopersicum , and Solanum pennellii LA 0716, both of which are SC and lack S ‐ RN ase, the pistil determinant of S ‐specificity in Solanaceae. Here we show that ui10.1 is a farnesyl pyrophosphate synthase gene ( FPS 2 ) expressed in pollen. Expression is about 18‐fold higher in pollen of S. pennellii than in S. lycopersicum . Pollen with the hypomorphic S. lycopersicum allele is selectively eliminated on pistils of the F 1 hybrid, leading to transmission ratio distortion in the F 2 progeny. CRISPR /Cas9‐generated knockout mutants ( fps2 ) in S. pennellii LA 0716 are self‐sterile due to pollen rejection, but mutant pollen is fully functional on pistils of S. lycopersicum . F 2 progeny of S. lycopersicum × S. pennellii ( fps2 ) show reversed transmission ratio distortion due to selective elimination of pollen bearing the knockout allele. Overexpression of FPS 2 in S. lycopersicum pollen rescues the pollen elimination phenotype. FPS 2 ‐based pollen selectivity does not involve S‐ RN ase and has not been previously linked to UI . Our results point to an entirely new mechanism of interspecific pollen rejection in plants.