Ackerman, G. | bioRxiv Science

bioRxiv2025

Balanced polymorphism in a floral transcription factor underlies an ancient rhythm of daily sex alternation in avocado

In avocado and certain wild relatives in Lauraceae, pollination occurs via a synchronized rhythm of floral sex timing between two hermaphroditic flowering types. A-type plants present female-phase flowers in the morning and male-phase flowers in the afternoon, while B-types show the complementary pattern, a form of heterodichogamy. We map this dimorphism in avocado to a genomic region overlapping a single strong candidate gene, SDMYB, where a dominant haplotype confers A-type flowering. SDMYB belongs to a subgroup of R2R3 MYB transcription factors established as key regulators of floral maturation in diverse species with links to circadian jasmonate signaling. Haplotypes at this locus form an ancient trans-species polymorphism maintained by negative frequency-dependent balancing selection over 44 million years, and they segregate in at least 26 non-avocado species, including in a genus where this mating system has not been reported. Across several species examined, rhythmic diel SDMYB expression is associated with biphasic floral anthesis, and the dominant allele, which contains nonsynonymous changes in conserved functional domains, exhibits a cis-regulated phase delay, corresponding to the delayed 2nd anthesis of A-types. The coupling of dichogamy with diel flower movements, widespread among magnoliids, is a likely precursor to daily forms of heterodichogamy. Absence of the SDMYB polymorphism in true cinnamon, which exhibits a highly similar mating system, suggests the possibility that heterodichogamy has convergently evolved within Lauraceae.

evolutionary biology↗

bioRxiv2025

Allelic turnover and dominance reversal at a single-gene balanced polymorphism controlling heterodichogamous flowering in wingnuts (Juglandaceae)

Angiosperms have evolved a wide variety of spatial and temporal developmental mechanisms to limit sexual interference and inbreeding. In heterodichogamy, two hermaphroditic morphs exploit distinct temporal reproductive niches by alternating phases of male and female flowering, promoting disassortative mating. This system is widespread within Juglandaceae, and known to be controlled by ancient balanced polymorphisms in walnuts (Juglans) and hickories (Carya). Here we identify distinct inheritance mechanisms controlling heterodichogamy in two separate Juglandaceae genera, the wingnuts (Pterocarya and Cyclocarya). We first document the occurrence of heterodichogamy in Pterocarya and map its genomic basis to haplotypes overlapping a single candidate gene in the FANTASTIC FOUR superfamily (GFAFL). These haplotypes segregate throughout the entire genus and the dominant haplotype controls female-first flowering. We show heterodichogamy in the sister genus Cyclocarya is associated with a distinct pair of ancient haplotypes at the same locus in both diploids and tetraploids, but with a dominant allele controlling male-first flowering. We infer a well-resolved fossil-calibrated phylogeny of Juglandaceae and date the divergence of the Pterocarya and Cyclocarya haplotypes to 51 and 44 million years ago, more recent than the divergence of these genera. In Pterocarya female-first heterozygotes, the dominant haplotype is associated with allele-specific suppression of the recessive copy of GFAFL during early male flower development. In Cyclocarya male-first heterozygotes, the dominant haplotype is associated with allele-specific activation of the recessive copy of GFAFL during male flower development, while the dominant copy itself shows higher expression in female flowers. We propose a model for the evolution of reciprocal sex matching in heterodichogamy through the combination of cis-regulatory divergence and allelic interactions involving fast and slow alleles at a single gene regulating flowering time. The non-independent expression of alleles in both systems is reminiscent of trans-sensing phenomena in other systems and suggests a mechanism mediated by DNA homology or an RNA intermediary. Notably, the dominant haplotypes in both genera show parallel architecture with a hemizygous region containing tandem duplicates of the same 1 kb motif downstream of the transcribed region of GFAFL which may be linked with such a mechanism. Our findings shed light on the molecular basis of heterodichogamy and contribute to an emerging view that diverse genetic pathways can be co-opted during its evolution and facilitate turnover in its genetic control.

evolutionary biology↗