Recombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogen
Abstract Background An understanding of plant pathogen evolution is important for sustainable management of crop diseases. Plant pathogen populations must maintain adequate heritable phenotypic variability to survive. Polymorphisms ≥ 50 bp, known as structural variants (SVs), could contribute strong...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2025-04-01
|
| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-025-02179-x |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850284616290664448 |
|---|---|
| author | Mark C. Derbyshire Toby E. Newman Yuphin Khentry Pippa J. Michael Sarita Jane Bennett Ashmita Rijal Lamichhane Carolyn Graham-Taylor Subhash Chander Claudia Camplone Simone Vicini Laura Esquivel-Garcia Cathy Coutu Dwayne Hegedus John Clarkson Kurt Lindbeck Lars G. Kamphuis |
| author_facet | Mark C. Derbyshire Toby E. Newman Yuphin Khentry Pippa J. Michael Sarita Jane Bennett Ashmita Rijal Lamichhane Carolyn Graham-Taylor Subhash Chander Claudia Camplone Simone Vicini Laura Esquivel-Garcia Cathy Coutu Dwayne Hegedus John Clarkson Kurt Lindbeck Lars G. Kamphuis |
| author_sort | Mark C. Derbyshire |
| collection | DOAJ |
| description | Abstract Background An understanding of plant pathogen evolution is important for sustainable management of crop diseases. Plant pathogen populations must maintain adequate heritable phenotypic variability to survive. Polymorphisms ≥ 50 bp, known as structural variants (SVs), could contribute strongly to this variability by disrupting gene activities. SV acquisition is largely driven by mobile genetic elements called transposons, though a less appreciated source of SVs is erroneous meiotic double-strand break repair. The relative impacts of transposons and recombination on SV diversity and the overall contribution of SVs to phenotypic variability is elusive, especially in host generalists. Results We use 25 high-quality genomes to create a graphical pan-genome of the globally distributed host-generalist crop pathogen Sclerotinia sclerotiorum. Outcrossing and recombination rates in this self-fertile species have been debated. Using bisulfite sequencing and short-read data from 190 strains, we show that S. sclerotiorum has many hallmarks of eukaryotic meiosis, including recombination hot and cold spots, centromeric and genic recombination suppression, and rapid linkage disequilibrium decay. Using a new statistic that captures average pairwise structural variation, we show that recombination and transposons make distinct contributions to SV diversity. Furthermore, despite only 5% of genes being dispensable, SVs often had a stronger impact than other variants across 14 life history traits measured in 103 distinct strains. Conclusions Transposons and recombination make distinct contributions to SV diversity in S. sclerotiorum. Despite limited gene content diversity, SVs may strongly impact phenotypic variability. This sheds light on the genomic forces shaping adaptive flexibility in host generalists. |
| format | Article |
| id | doaj-art-163ad2efd8f14553bc6da7b74b002afe |
| institution | OA Journals |
| issn | 1741-7007 |
| language | English |
| publishDate | 2025-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj-art-163ad2efd8f14553bc6da7b74b002afe2025-08-20T01:47:30ZengBMCBMC Biology1741-70072025-04-0123112610.1186/s12915-025-02179-xRecombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogenMark C. Derbyshire0Toby E. Newman1Yuphin Khentry2Pippa J. Michael3Sarita Jane Bennett4Ashmita Rijal Lamichhane5Carolyn Graham-Taylor6Subhash Chander7Claudia Camplone8Simone Vicini9Laura Esquivel-Garcia10Cathy Coutu11Dwayne Hegedus12John Clarkson13Kurt Lindbeck14Lars G. Kamphuis15Centre for Crop and Disease Management, Curtin UniversityCentre for Crop and Disease Management, Curtin UniversityCentre for Crop and Disease Management, Curtin UniversityCentre for Crop and Disease Management, Curtin UniversityCentre for Crop and Disease Management, Curtin UniversityCentre for Crop and Disease Management, Curtin UniversityCentre for Crop and Disease Management, Curtin UniversityDepartment of Genetics and Plant Breeding, Oilseeds Section, CCS Haryana Agricultural UniversityCentre for Crop and Disease Management, Curtin UniversityCentre for Crop and Disease Management, Curtin UniversityPlant Science, Mcgill UniversityAgriculture and Agri-Food CanadaAgriculture and Agri-Food CanadaWarwick Crop Centre, School of Life Sciences, University of WarwickDepartment of Primary IndustriesCentre for Crop and Disease Management, Curtin UniversityAbstract Background An understanding of plant pathogen evolution is important for sustainable management of crop diseases. Plant pathogen populations must maintain adequate heritable phenotypic variability to survive. Polymorphisms ≥ 50 bp, known as structural variants (SVs), could contribute strongly to this variability by disrupting gene activities. SV acquisition is largely driven by mobile genetic elements called transposons, though a less appreciated source of SVs is erroneous meiotic double-strand break repair. The relative impacts of transposons and recombination on SV diversity and the overall contribution of SVs to phenotypic variability is elusive, especially in host generalists. Results We use 25 high-quality genomes to create a graphical pan-genome of the globally distributed host-generalist crop pathogen Sclerotinia sclerotiorum. Outcrossing and recombination rates in this self-fertile species have been debated. Using bisulfite sequencing and short-read data from 190 strains, we show that S. sclerotiorum has many hallmarks of eukaryotic meiosis, including recombination hot and cold spots, centromeric and genic recombination suppression, and rapid linkage disequilibrium decay. Using a new statistic that captures average pairwise structural variation, we show that recombination and transposons make distinct contributions to SV diversity. Furthermore, despite only 5% of genes being dispensable, SVs often had a stronger impact than other variants across 14 life history traits measured in 103 distinct strains. Conclusions Transposons and recombination make distinct contributions to SV diversity in S. sclerotiorum. Despite limited gene content diversity, SVs may strongly impact phenotypic variability. This sheds light on the genomic forces shaping adaptive flexibility in host generalists.https://doi.org/10.1186/s12915-025-02179-xRecombinationStructural variantGenome graphPlant pathogenFungusSclerotinia sclerotiorum |
| spellingShingle | Mark C. Derbyshire Toby E. Newman Yuphin Khentry Pippa J. Michael Sarita Jane Bennett Ashmita Rijal Lamichhane Carolyn Graham-Taylor Subhash Chander Claudia Camplone Simone Vicini Laura Esquivel-Garcia Cathy Coutu Dwayne Hegedus John Clarkson Kurt Lindbeck Lars G. Kamphuis Recombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogen BMC Biology Recombination Structural variant Genome graph Plant pathogen Fungus Sclerotinia sclerotiorum |
| title | Recombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogen |
| title_full | Recombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogen |
| title_fullStr | Recombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogen |
| title_full_unstemmed | Recombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogen |
| title_short | Recombination and transposition drive genomic structural variation potentially impacting life history traits in a host-generalist fungal plant pathogen |
| title_sort | recombination and transposition drive genomic structural variation potentially impacting life history traits in a host generalist fungal plant pathogen |
| topic | Recombination Structural variant Genome graph Plant pathogen Fungus Sclerotinia sclerotiorum |
| url | https://doi.org/10.1186/s12915-025-02179-x |
| work_keys_str_mv | AT markcderbyshire recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT tobyenewman recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT yuphinkhentry recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT pippajmichael recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT saritajanebennett recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT ashmitarijallamichhane recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT carolyngrahamtaylor recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT subhashchander recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT claudiacamplone recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT simonevicini recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT lauraesquivelgarcia recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT cathycoutu recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT dwaynehegedus recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT johnclarkson recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT kurtlindbeck recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen AT larsgkamphuis recombinationandtranspositiondrivegenomicstructuralvariationpotentiallyimpactinglifehistorytraitsinahostgeneralistfungalplantpathogen |