The long and short of the S‐locus in Turnera (Passifloraceae)

Abstract

Distyly is an intriguing floral adaptation that increases pollen transfer precision and restricts inbreeding. It has been a model system in evolutionary biology since Darwin. Although the Slocus determines the long-and short-styled morphs, the genes were unknown in Turnera. We have now identified these genes.We used deletion mapping to identify, and then sequence, BAC clones and genome scaffolds to construct S/s haplotypes. We investigated candidate gene expression, hemizygosity, and used mutants, to explore gene function.The s-haplotype possessed 21 genes collinear with a region of chromosome 7 of grape. The S-haplotype possessed three additional genes and two inversions. TsSPH1 was expressed in filaments and anthers, TsYUC6 in anthers and TsBAHD in pistils. Long-homostyle mutants did not possess TsBAHD and a short-homostyle mutant did not express TsSPH1.Three hemizygous genes appear to determine S-morph characteristics in T. subulata. Hemizygosity is common to all distylous species investigated, yet the genes differ. The pistil candidate gene, TsBAHD, differs from that of Primula, but both may inactivate brassinosteroids causing short styles. TsYUC6 is involved in auxin synthesis and likely determines pollen characteristics. TsSPH1 is likely involved in filament elongation. We propose an incompatibility mechanism involving TsYUC6 and TsBAHD.

‘A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions

“…First, the dominant S ‐haplotype of the S‐morph comprises a hemizygous region of several genes absent from the s ‐haplotype of the L‐morph. Significantly, this appears to be a feature of the four genera investigated (Ushijima et al ., ; Yasui et al ., ; Kappel et al ., ; Cocker et al ., ; Shore et al ., ). Second, candidate genes controlling sex organ height have been identified in each genus.…”

“…Studies of Linum have identified a candidate gene ( TSS1 ) controlling style length that is expressed in styles of the S‐morph but not the L‐morph (Ushijima et al ., ). In Turnera , three hemizygous candidate genes, TsBAHD , TsSPH1 and TsYUC6 , appear to determine, respectively, style, filament and anther characteristics in the S‐morph, but are absent from the L‐morph (Shore et al ., ). Significantly, both putative style length genes, TsBAHD and CYP734A50 in Turnera and Primula , respectively, have high homology to genes that inactivate brassinosteroids, known regulators of cell expansion.…”

“…Significantly, both putative style length genes, TsBAHD and CYP734A50 in Turnera and Primula , respectively, have high homology to genes that inactivate brassinosteroids, known regulators of cell expansion. This finding suggests the possibility of biochemical convergence involving the same hormonal pathways controlling style length (Shore et al ., ).…”

“…Second, given the discovery of different candidate causal genes governing style length and anther height, how diverse are these likely to be across a large sample of heterostylous families and how much developmental and physiological convergence is evident in the processes that produce the same functional phenotypes? Third, does the heterostyly linkage group have similar origins in different families, perhaps by segmental duplication, or are other mechanisms that suppress recombination (such as inversions, as occur in several animal supergene systems and also in Turnera (Shore et al ., )) more common?…”

“…Shore et al . () have proposed a novel hypothesis, based on their work on Turnera , which could explain the apparent absence of specific ‘incompatibility genes’, as occur in homomorphic self‐incompatibility systems. They suggest that differences in concentrations of auxin and brassinosteroids during development between the morphs may be the underlying mechanism governing pollen–pistil interactions and intramorph incompatibility.…”