Ancient structural variants control sex-specific flowering time morphs in walnuts and hickories.

Abstract

Balanced mating type polymorphisms offer a distinct window into the forces shaping sexual reproduction strategies. Multiple hermaphroditic genera in Juglandaceae, including walnuts (<i>Juglans</i>) and hickories (<i>Carya</i>), show a 1:1 genetic dimorphism for male versus female flowering order (heterodichogamy). We map two distinct Mendelian inheritance mechanisms to ancient (>37 million years old) genus-wide structural DNA polymorphisms. The dominant haplotype for female-first flowering in <i>Juglans</i> contains tandem repeats of the 3' untranslated region of a gene putatively involved in trehalose-6-phosphate metabolism and is associated with increased <i>cis</i> gene expression in developing male flowers, possibly mediated by small RNAs. The <i>Carya</i> locus contains ~20 syntenic genes and shows molecular signatures of sex chromosome-like evolution. Inheritance mechanisms for heterodichogamy are deeply conserved, yet may occasionally turn over, as in sex determination.