The S-Gene YUC6 Pleiotropically Determines Male Mating Type and Pollen Size in Heterostylous Turnera (Passifloraceae): A Novel Neofunctionalization of the YUCCA Gene Family

Abstract

In heterostylous, self-incompatible Turnera species, a member of the YUCCA gene family, YUC6, resides at the S-locus and has been hypothesized to determine the male mating type. YUCCA gene family members synthesize the auxin, indole-3-acetic acid, via a two-step process involving the TAA gene family. Consequently, it has been speculated that differences in auxin concentration in developing anthers are the biochemical basis underlying the male mating type. Here, we provide empirical evidence that supports this hypothesis. Using a transgenic knockdown approach, we show that YUC6 acts pleiotropically to control both the male physiological mating type and pollen size, but not the filament length dimorphism associated with heterostyly in Turnera. Using qPCR to assess YUC6 expression in different transgenic lines, we demonstrate that the level of YUC6 knockdown correlates with the degree of change observed in the male mating type. Further assessment of YUC6 expression through anther development, in the knockdown lines, suggests that the male mating type is irreversibly determined during a specific developmental window prior to microsporogenesis, which is consistent with the genetically sporophytic nature of this self-incompatibility system. These results represent the first gene controlling male mating type to be characterized in any species with heterostyly.

Annotation of the Turnera subulata (Passifloraceae) Draft Genome Reveals the S-Locus Evolved after the Divergence of Turneroideae from Passifloroideae in a Stepwise Manner

“…Our OrthoVenn2 results coupled with expression patterns suggest that TsYUC6 and Tsubulata_012066-RA may have evolved new functions; however, it is likely that TsYUC6 and Tsubulata_012066-RA, biochemically, are both still involved in the tryptophan-dependent auxin biosynthesis pathway. Knocking down TjYUC6 in distylous Turnera joelii alters the expression of auxin-related genes [ 15 ], as expected for a gene involved in auxin metabolism. In addition, to our knowledge, all YUCCA family members characterized to date are enzymatically involved in the tryptophan-dependent auxin biosynthesis pathway.…”

“…SPH1 , a member of the S - protein homolog family, likely controls filament length [ 3 ]. YUC6 , a member of the YUCCA flavin monooxygenase family, controls male mating-type [ 15 ] likely via alterations of auxin concentration in the S-morph relative to the L-morph [ 16 ]. Currently, it is unknown how the S -locus evolved in Turnera .…”

Comparative transcriptomics reveals commonalities and differences in the genetic underpinnings of a floral dimorphism

“…First, FMOs overlap in function with cytochrome P450 monooxygenases, a superfamily of enzymes that also includes the protein encoded by CYP T , the S-locus gene that controls style length and female incompatibility in P. veris 13,16 . Second, the T. subulata S-locus gene YUC6, which controls male mating type and pollen size 23 , is a FMO, specifically a member of the YUCCA gene family which catalyzes the second step in auxin synthesis from Ltryptophan 20,50 . To better characterize the putative function of these differentially expressed FMOs, we generated a phylogeny that included the sequences of OG0000315 genes as well as those of A. thaliana and barley (Hordeum vulgare) FMOs 51 (Fig.…”

“…above the anthers' attachment point), and width of the corolla tube mouth 8 .Having evolved independently in angiosperms at least 13 times 9 , distyly represents an ideal case to study convergent evolution 10 . Research on distyly has mainly focused on Primula (Primulaceae) [11][12][13][14][15][16][17] , Fagopyrum (Polygonaceae) 18,19 , and Turnera (Passifloraceae) [20][21][22][23] , reviewed below, and, to a lesser extent, Linum (Linaceae) 24 and Lithospermum (Boraginaceae) 25,26 . Phenotypic convergence in floral morphology appears to be mirrored by convergence in the genetic architecture of the locus controlling distyly.…”

ThePrimula edelbergii S-locus is an example of a jumping supergene

“…Recently, research on the S-locus has expanded from Primula to other genera that independently evolved heterostyly, including Turnera (Henning et al, 2022;Matzke et al, 2020Matzke et al, , 2021Shore et al, 2019), Fagopyrum (Fawcett et al, 2023;Yasui et al, 2012Yasui et al, , 2016, Linum (Gutiérrez-Valencia et al, 2022), Gelsemium (Zhao et al, 2023), and Nymphoides (Yang et al, 2023). Surprisingly, in all these cases the S-locus was found to be hemizygous in thrums and absent from pins, pointing to a remarkable consistency in the genomic architecture of the S-locus across heterostylous taxa.…”