Distinct ancient structural polymorphisms control heterodichogamy in walnuts and hickories

Abstract

The maintenance of stable mating type polymorphisms is a classic example of balancing selection, underlying the nearly ubiquitous 50/50 sex ratio in species with separate sexes. One lesser known but intriguing example of a balanced mating polymorphism in angiosperms is heterodichogamy - polymorphism for opposing directions of dichogamy (temporal separation of male and female function in hermaphrodites) within a flowering season. This mating system is common throughout Juglandaceae, the family that includes globally important and iconic nut and timber crops - walnuts (Juglans), as well as pecan and other hickories (Carya). We show that two distinct genetic systems control heterodichogamous mating systems in these genera. In each genus, we find ancient (>50Mya) structural variants that segregate as trans-species polymorphisms. TheJuglanslocus maps to a ca. 20kb structural variant adjacent to gene with likely function in the trehalose-6-phosphate signaling pathway, which is known to regulate flowering time in Arabidopsis and inflorescence architecture in maize. Notably, an insertion in the dominant (protogynous) haplotype contains 8-12 complex tandem duplicates of the 3’ UTR of the gene, and transpecies polymorphism within the gene is restricted to the 3’ UTR. In contrast, theCaryaheterodichogamy locus maps to a ca. 200-450 kb cluster of tightly linked polymorphisms across 20 genes, some of which have known roles in flowering and are differentially expressed between morphs in floral primordia. The dominant (protogynous) haplotype in pecan, which is nearly always heterozygous and appears to rarely recombine, shows reduced genetic diversity and is over twice as long as its recessive counterpart due to proliferation of multiple transposable element families. We did not detect either genetic system in another heterodichogamous genus within the Juglandaceae, suggesting that additional genetic systems for heterodichogamy may yet remain undiscovered.