Evolutionary history of <i>Primula grandis</i>

<p dir="ltr">Despite the evolutionary importance of supergenes, their properties in polyploids remain unexplored. Polyploid genomes are expected to undergo chromosomal rearrangements and gene losses over time, potentially affecting supergene architecture. The iconic distyly supergene (<i>S</i>-locus), controlling a floral heteromorphism with two self-incompatible morphs, has been well-documented in diploids, but remains unknown in polyploids.<i>Primula</i>, the classic model for distyly since Darwin, is ancestrally diploid and distylous, yet polyploid, homostylous species with a single, self-compatible floral morph evolved repeatedly. The intraspecific loss of distyly is associated with small loss-of-function mutations in the <i>S</i>-locus <i>CYP</i><sup><em>T</em></sup> gene controlling style length and female self-incompatibility. Over longer timescales, relaxed selection on <i>CYP</i><sup><em>T</em></sup> should generate greater accumulation of larger mutations, including exon and gene loss. By analyzing the first assembled genome of an allotetraploid, homostylous species (<i>Primula grandis</i>) in a comparative framework, we discovered two, nearly identical<i>S</i>-locus alleles in the same subgenome, suggesting it originated via inter-specific hybridization between a homostylous and a distylous progenitor. Conformant to predictions from theory, the macroevolutionary loss of distyly coincided with considerable degeneration of <i>CYP</i><sup><em>T</em></sup>, while other<i>S</i>-locus genes remained largely unaffected, suggesting the shift to homostyly preceded and facilitated polyploid establishment. At the whole-genome level, we found minimal subgenome dominance — as expected, given the inferred recent origin of<i>P. grandis</i>— and highly reduced genetic diversity, congruently with its narrow distribution and self-compatibility. This study provides the first comparison of a supergene across ploidy levels and reproductive systems, contributing new knowledge on the previously unknown fate of supergenes in polyploids. ######################################## <p dir="ltr">This submission includes: <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.fa #Genome assembly of both subgenomes (11 chromosomes each) <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.gff3 #Gene annotation in GFF format <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.gtf #Gene annotation in GTF format <p dir="ltr">out_JBAT_review3_TEs.FINAL.fa.out.gff #Annotation of transposable and repetitive elements for the P. grandis genome <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.longProt.fasta #Protein sequences of all annotated proteins <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.codingseq.fasta #DNA sequences of all annotated genes in the genome

Publication Details

Journal
Figshare
Published
2025-03-06
DOI
https://doi.org/10.6084/m9.figshare.28540910.v1
Primary Topic
Chromosomal and Genetic Variations
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article
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article

Evolutionary history of Primula grandis

Figshare
Chromosomal and Genetic Variations
article

Evolutionary history of Primula grandis

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Abstract

<p dir="ltr">Despite the evolutionary importance of supergenes, their properties in polyploids remain unexplored. Polyploid genomes are expected to undergo chromosomal rearrangements and gene losses over time, potentially affecting supergene architecture. The iconic distyly supergene (<i>S</i>-locus), controlling a floral heteromorphism with two self-incompatible morphs, has been well-documented in diploids, but remains unknown in polyploids.<i>Primula</i>, the classic model for distyly since Darwin, is ancestrally diploid and distylous, yet polyploid, homostylous species with a single, self-compatible floral morph evolved repeatedly. The intraspecific loss of distyly is associated with small loss-of-function mutations in the <i>S</i>-locus <i>CYP</i><sup><em>T</em></sup> gene controlling style length and female self-incompatibility. Over longer timescales, relaxed selection on <i>CYP</i><sup><em>T</em></sup> should generate greater accumulation of larger mutations, including exon and gene loss. By analyzing the first assembled genome of an allotetraploid, homostylous species (<i>Primula grandis</i>) in a comparative framework, we discovered two, nearly identical<i>S</i>-locus alleles in the same subgenome, suggesting it originated via inter-specific hybridization between a homostylous and a distylous progenitor. Conformant to predictions from theory, the macroevolutionary loss of distyly coincided with considerable degeneration of <i>CYP</i><sup><em>T</em></sup>, while other<i>S</i>-locus genes remained largely unaffected, suggesting the shift to homostyly preceded and facilitated polyploid establishment. At the whole-genome level, we found minimal subgenome dominance — as expected, given the inferred recent origin of<i>P. grandis</i>— and highly reduced genetic diversity, congruently with its narrow distribution and self-compatibility. This study provides the first comparison of a supergene across ploidy levels and reproductive systems, contributing new knowledge on the previously unknown fate of supergenes in polyploids. ######################################## <p dir="ltr">This submission includes: <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.fa #Genome assembly of both subgenomes (11 chromosomes each) <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.gff3 #Gene annotation in GFF format <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.gtf #Gene annotation in GTF format <p dir="ltr">out_JBAT_review3_TEs.FINAL.fa.out.gff #Annotation of transposable and repetitive elements for the P. grandis genome <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.longProt.fasta #Protein sequences of all annotated proteins <p dir="ltr">out_JBAT_review4.FINAL_22scaf_rename.codingseq.fasta #DNA sequences of all annotated genes in the genome

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Chromosomal and Genetic Variations
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