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 (Juglans) and hickories (Carya), 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 Juglans contains tandem repeats of the 3' untranslated region of a gene putatively involved in trehalose-6-phosphate metabolism and is associated with increased cis gene expression in developing male flowers, possibly mediated by small RNAs. The Carya 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.