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

Abstract

A majority of Turnera species (Passifloraceae) exhibit distyly, a reproductive system involving both self-incompatibility and reciprocal herkogamy. This system differs from self-incompatibility in Passiflora species. The genetic basis of distyly in Turnera is a supergene, restricted to the S-morph, and containing three S-genes. How supergenes and distyly evolved in Turnera, and the other Angiosperm families exhibiting distyly remain largely unknown. Unraveling the evolutionary origins in Turnera requires the generation of genomic resources and extensive phylogenetic analyses. Here, we present the annotated draft genome of the S-morph of distylous Turnera subulata. Our annotation allowed for phylogenetic analyses of the three S-genes’ families across 56 plant species ranging from non-seed plants to eudicots. In addition to the phylogenetic analysis, we identified the three S-genes’ closest paralogs in two species of Passiflora. Our analyses suggest that the S-locus evolved after the divergence of Passiflora and Turnera. Finally, to provide insights into the neofunctionalization of the S-genes, we compared expression patterns of the S-genes with close paralogs in Arabidopsis and Populus trichocarpa. The annotation of the T. subulata genome will provide a useful resource for future comparative work. Additionally, this work has provided insights into the convergent nature of distyly and the origin of supergenes.

Genomic analyses elucidate S‐locus evolution in response to intra‐specific losses of distyly in Primula vulgaris

“…This result corroborates previous studies that found an overall decrease in genetic diversity between the S-locus and its flanking regions in Primula (Potente, Léveillé-Bourret, et al, 2022), Linum (Gutiérrez-Valencia et al, 2022), and Turnera (Henning et al, 2023). Thus, our work confirms predictions that S-locus genomic architecture influences patterns of molecular evolution in S-genes.…”

Haplotype‐resolved genome assembly provides insights into the evolution of S‐locus supergene in distylous Nymphoides indica

“…However, in P. veris (Potente et al ., 2022a), Ty3‐Gypsy retrotransposons are not preferentially accumulated at the S ‐locus, only Ty1‐Copia elements were identified (Table S8). In T. subulata (Henning et al ., 2023) and F. esculentum (Yasui et al ., 2016), both Ty1 ‐ Copia and Ty3‐Gypsy were identified (see Table S8).…”

“…We identified repetitive elements in the assembly using R epeat M asker v.4.1.0 (http://www.repeatmasker.org) with the de novo repeat library built with R epeat M odeler v.2.0.1 (http://www.repeatmasker.org) and the Repbase database (http://www.girinst.org/repbase/). Additionally, we used E dta v.1.9.7 (Ou et al ., 2019), an automated whole‐genome de novo transposable element (TE) annotation software, for the de novo prediction of TEs in the S‐morph genomes of N. indica , P. veris (Potente et al ., 2022a), T. subulata (Henning et al ., 2023), L. tenue (Gutierrez‐Valencia et al ., 2022), and F. esculentum (Yasui et al ., 2016). This analysis focused exclusively on the S‐morph, and the L‐morph was not included.…”

“…org/repbase/). Additionally, we used EDTA v.1.9.7 (Ou et al, 2019), an automated whole-genome de novo transposable element (TE) annotation software, for the de novo prediction of TEs in the S-morph genomes of N. indica, P. veris (Potente et al, 2022a), T. subulata (Henning et al, 2023), L. tenue (Gutierrez-Valencia et al, 2022), and F. esculentum (Yasui et al, 2016). This analysis focused exclusively on the S-morph, and the L-morph was not included.…”

“…These paralogs were scattered throughout the P. veris genome with different relative ages of duplication, supporting the stepwise duplication model. In L. tenue (Gutierrez-Valencia et al, 2022), T. subulata (Henning et al, 2023), and G. elegans (Zhao et al, 2022), the closest paralogs of S-locus genes reside on different scaffolds or the same scaffold but are separated by other genes. The stepwise duplication model therefore appears to be the main mechanism accounting for the origin of the S-locus, although this needs to be confirmed by studies on other distylous lineages and our study investigated this question.…”