A large accessory genome and high recombination rates may influence global distribution and broad host range of the fungal plant pathogen Claviceps purpurea

Wyka, Stephen; Mondo, Stephen; Liu, Miao; Nalam, Vamsi; Broders, Kirk

doi:10.1371/journal.pone.0263496

Title: A large accessory genome and high recombination rates may influence global distribution and broad host range of the fungal plant pathogen Claviceps purpurea

Journal Article · 09 February 2022 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0263496 · OSTI ID:1892179

Wyka, Stephen ^[1]; Mondo, Stephen ^[2];

^[3];

^[1];

^[4]

Colorado State Univ., Fort Collins, CO (United States)
Colorado State Univ., Fort Collins, CO (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Agriculture and Agri-Food Canada, Ottawa, ON (Canada). Ottawa Research and Development Centre
US Dept. of Agriculture (USDA), Peoria, IL (United States). Agricultural Research Service; Smithsonian Tropical Research Institute, Panama City (Panama)

Pangenome analyses are increasingly being utilized to study the evolution of eukaryotic organisms. While pangenomes can provide insight into polymorphic gene content, inferences about the ecological and adaptive potential of such organisms also need to be accompanied by additional supportive genomic analyses. In this study we constructed a pangenome of Claviceps purpurea from 24 genomes and examined the positive selection and recombination landscape of an economically important fungal organism for pharmacology and agricultural research. Together, these analyses revealed that C. purpurea has a relatively large accessory genome (~ 38%), high recombination rates (ρ = 0.044), and transposon mediated gene duplication. However, due to observations of relatively low transposable element (TE) content (8.8%) and a lack of variability in genome sizes, prolific TE expansion may be controlled by frequent recombination. We additionally identified that within the ergoline biosynthetic cluster the lpsA1 and lpsA2 were the result of a recombination event. However, the high recombination rates observed in C. purpurea may be influencing an overall trend of purifying selection across the genome. These results showcase the use of selection and recombination landscapes to identify mechanisms contributing to pangenome structure and primary factors influencing the evolution of an organism.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1892179

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 2 Vol. 17; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

Sympatric divergence of the ergot fungus, Claviceps purpurea , populations infecting agricultural and nonagricultural grasses in North America Liu, Miao; Shoukouhi, Parivash; Bisson, Kassandra R. Ecology and Evolution, Vol. 11, Issue 1 https://doi.org/10.1002/ece3.7028	journal	December 2020
The genomic determinants of adaptive evolution in a fungal pathogen Grandaubert, Jonathan; Dutheil, Julien Y.; Stukenbrock, Eva H. Evolution Letters, Vol. 3, Issue 3 https://doi.org/10.1002/evl3.117	journal	May 2019
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
Biological roles of fungal carotenoids Avalos, Javier; Carmen Limón, M. Current Genetics, Vol. 61, Issue 3 https://doi.org/10.1007/s00294-014-0454-x	journal	October 2014
Manipulation of cytokinin level in the ergot fungus Claviceps purpurea emphasizes its contribution to virulence Kind, Sabine; Hinsch, Janine; Vrabka, Josef Current Genetics, Vol. 64, Issue 6 https://doi.org/10.1007/s00294-018-0847-3	journal	May 2018
Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit Xia, Chao; Christensen, Michael J.; Zhang, Xingxu Plant and Soil, Vol. 424, Issue 1-2 https://doi.org/10.1007/s11104-018-3561-5	journal	January 2018
Overview of genomic and bioinformatic resources for Zymoseptoria tritici Testa, Alison; Oliver, Richard; Hane, James Fungal Genetics and Biology, Vol. 79 https://doi.org/10.1016/j.fgb.2015.04.011	journal	June 2015
RIP: the evolutionary cost of genome defense Galagan, James E.; Selker, Eric U. Trends in Genetics, Vol. 20, Issue 9 https://doi.org/10.1016/j.tig.2004.07.007	journal	September 2004
Evolutionary history of ergot with a new infrageneric classification (Hypocreales: Clavicipitaceae: Claviceps) Píchová, Kamila; Pažoutová, Sylvie; Kostovčík, Martin Molecular Phylogenetics and Evolution, Vol. 123 https://doi.org/10.1016/j.ympev.2018.02.013	journal	June 2018
A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements Hartmann, Fanny E.; Sánchez-Vallet, Andrea; McDonald, Bruce A. The ISME Journal, Vol. 11, Issue 5 https://doi.org/10.1038/ismej.2016.196	journal	January 2017
The genome sequence of the filamentous fungus Neurospora crassa Galagan, James E.; Calvo, Sarah E.; Borkovich, Katherine A. Nature, Vol. 422, Issue 6934 https://doi.org/10.1038/nature01554	journal	April 2003
Why prokaryotes have pangenomes McInerney, James O.; McNally, Alan; O'Connell, Mary J. Nature Microbiology, Vol. 2, Issue 4 https://doi.org/10.1038/nmicrobiol.2017.40	journal	March 2017
The long-term epidemic of Claviceps purpurea on Spartina anglica in Poole Harbour: pattern of infection, effects on seed production and the role of Fusarium heterosporum Raybould, A. F.; Gray, A. J.; Clarke, R. T. New Phytologist, Vol. 138, Issue 3 https://doi.org/10.1046/j.1469-8137.1998.00123.x	journal	March 1998
Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava , a pathogen of Arabidopsis Araki, Hitoshi; Tian, Dacheng; Goss, Erica M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 15 https://doi.org/10.1073/pnas.0601431103	journal	April 2006
An overview of the ergot (Claviceps purpurea) issue in western Canada: challenges and solutions Menzies, J. G.; Turkington, T. K. Canadian Journal of Plant Pathology, Vol. 37, Issue 1 https://doi.org/10.1080/07060661.2014.986527	journal	December 2014
Evaluation of Claviceps purpurea isolates on wheat reveals complex virulence and host susceptibility relationships Menzies, James G.; Klein-Gebbinck, Henry W.; Gordon, Anna Canadian Journal of Plant Pathology, Vol. 39, Issue 3 https://doi.org/10.1080/07060661.2017.1355334	journal	July 2017
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
A high-performance computing toolset for relatedness and principal component analysis of SNP data Zheng, X.; Levine, D.; Shen, J. Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts606	journal	October 2012
nhmmer: DNA homology search with profile HMMs Wheeler, T. J.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 19 https://doi.org/10.1093/bioinformatics/btt403	journal	July 2013
InterProScan 5: genome-scale protein function classification Jones, P.; Binns, D.; Chang, H. -Y. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu031	journal	January 2014
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Whole-Genome Comparisons of Ergot Fungi Reveals the Divergence and Evolution of Species within the Genus Claviceps Are the Result of Varying Mechanisms Driving Genome Evolution and Host Range Expansion Wyka, Stephen A.; Mondo, Stephen J.; Liu, Miao Genome Biology and Evolution, Vol. 13, Issue 2 https://doi.org/10.1093/gbe/evaa267	journal	January 2021
Gene Presence–Absence Polymorphism in Castrating Anther-Smut Fungi: Recent Gene Gains and Phylogeographic Structure Hartmann, Fanny E.; Rodríguez de la Vega, Ricardo C.; Brandenburg, Jean-Tristan Genome Biology and Evolution, Vol. 10, Issue 5 https://doi.org/10.1093/gbe/evy089	journal	May 2018
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server Kall, L.; Krogh, A.; Sonnhammer, E. L. L. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm256	journal	May 2007
LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons Xu, Z.; Wang, H. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm286	journal	May 2007
Fine-grained annotation and classification of de novo predicted LTR retrotransposons Steinbiss, Sascha; Willhoeft, Ute; Gremme, Gordon Nucleic Acids Research, Vol. 37, Issue 21 https://doi.org/10.1093/nar/gkp759	journal	September 2009
Meiotic recombination protein Rec12: functional conservation, crossover homeostasis and early crossover/non-crossover decision Kan, Fengling; Davidson, Mari K.; Wahls, Wayne P. Nucleic Acids Research, Vol. 39, Issue 4 https://doi.org/10.1093/nar/gkq993	journal	October 2010
The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database Rawlings, Neil D.; Barrett, Alan J.; Thomas, Paul D. Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1134	journal	November 2017
antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline Blin, Kai; Shaw, Simon; Steinke, Katharina Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz310	journal	April 2019
Estimating Synonymous and Nonsynonymous Substitution Rates Under Realistic Evolutionary Models Yang, Ziheng; Nielsen, Rasmus Molecular Biology and Evolution, Vol. 17, Issue 1 https://doi.org/10.1093/oxfordjournals.molbev.a026236	journal	January 2000
Repeat-Induced Point Mutation (RIP) as an Alternative Mechanism of Evolution Toward Virulence in Leptosphaeria maculans Fudal, Isabelle; Ross, Simon; Brun, Hortense Molecular Plant-Microbe Interactions®, Vol. 22, Issue 8 https://doi.org/10.1094/MPMI-22-8-0932	journal	August 2009
Salt Marsh Claviceps purpurea in Native and Invaded Spartina Marshes in Northern California Fisher, A. J.; DiTomaso, J. M.; Gordon, T. R. Plant Disease, Vol. 91, Issue 4 https://doi.org/10.1094/PDIS-91-4-0380	journal	April 2007
Identifying copy number variation of the dominant virulence factors msa and p22 within genomes of the fish pathogen Renibacterium salmoninarum Brynildsrud, Ola; Gulla, Snorre; Feil, Edward J. Microbial Genomics, Vol. 2, Issue 4 https://doi.org/10.1099/mgen.0.000055	journal	April 2016
Aligning Multiple Genomic Sequences With the Threaded Blockset Aligner Blanchette, M. Genome Research, Vol. 14, Issue 4 https://doi.org/10.1101/gr.1933104	journal	April 2004
Recombination rate estimation in the presence of hotspots Auton, A.; McVean, G. Genome Research, Vol. 17, Issue 8 https://doi.org/10.1101/gr.6386707	journal	July 2007
GenomeTools: A Comprehensive Software Library for Efficient Processing of Structured Genome Annotations Gremme, Gordon; Steinbiss, Sascha; Kurtz, Stefan IEEE/ACM Transactions on Computational Biology and Bioinformatics, Vol. 10, Issue 3 https://doi.org/10.1109/TCBB.2013.68	journal	May 2013
De novo biosynthesis of cytokinins in the biotrophic fungus C laviceps purpurea: De novo cytokinin synthesis by a fungal pathogen Hinsch, Janine; Vrabka, Josef; Oeser, Birgitt Environmental Microbiology, Vol. 17, Issue 8 https://doi.org/10.1111/1462-2920.12838	journal	April 2015
Brachypodium distachyon as alternative model host system for the ergot fungus Claviceps purpurea Kind, Sabine; Schurack, Selma; Hinsch, Janine Molecular Plant Pathology, Vol. 19, Issue 4 https://doi.org/10.1111/mpp.12563	journal	June 2017
Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0: Prediction of fungal effectors with EffectorP 2.0 Sperschneider, Jana; Dodds, Peter N.; Gardiner, Donald M. Molecular Plant Pathology, Vol. 19, Issue 9 https://doi.org/10.1111/mpp.12682	journal	May 2018
Functional characterization of the first filamentous fungal tRNA ‐isopentenyltransferase and its role in the virulence of Claviceps purpurea Hinsch, Janine; Galuszka, Petr; Tudzynski, Paul New Phytologist, Vol. 211, Issue 3 https://doi.org/10.1111/nph.13960	journal	April 2016
Running with the Red Queen: Host-Parasite Coevolution Selects for Biparental Sex Morran, L. T.; Schmidt, O. G.; Gelarden, I. A. Science, Vol. 333, Issue 6039 https://doi.org/10.1126/science.1206360	journal	July 2011
Ergotamine Production in Submerged Culture and Physiology of Claviceps purpurea Amici, Alba M.; Minghetti, A.; Scotti, T. Applied Microbiology, Vol. 15, Issue 3 https://doi.org/10.1128/am.15.3.597-602.1967	journal	May 1967
The Genome Biology of Effector Gene Evolution in Filamentous Plant Pathogens Sánchez-Vallet, Andrea; Fouché, Simone; Fudal, Isabelle Annual Review of Phytopathology, Vol. 56, Issue 1 https://doi.org/10.1146/annurev-phyto-080516-035303	journal	August 2018
LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons Ellinghaus, David; Kurtz, Stefan; Willhoeft, Ute BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-18	journal	January 2008
The relationship of recombination rate, genome structure, and patterns of molecular evolution across angiosperms Tiley, George P.; Burleigh, J. Gordon BMC Evolutionary Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12862-015-0473-3	journal	September 2015
Cross-talk of the biotrophic pathogen Claviceps purpurea and its host Secale cereale Oeser, Birgitt; Kind, Sabine; Schurack, Selma BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3619-4	journal	April 2017
A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici Badet, Thomas; Oggenfuss, Ursula; Abraham, Leen BMC Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12915-020-0744-3	journal	February 2020
OrthoFinder: phylogenetic orthology inference for comparative genomics Emms, David M.; Kelly, Steven Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1832-y	journal	November 2019
Repbase Update, a database of repetitive elements in eukaryotic genomes Bao, Weidong; Kojima, Kenji K.; Kohany, Oleksiy Mobile DNA, Vol. 6, Issue 1 https://doi.org/10.1186/s13100-015-0041-9	journal	June 2015
Identification and characterization of the ergochrome gene cluster in the plant pathogenic fungus Claviceps purpurea Neubauer, Lisa; Dopstadt, Julian; Humpf, Hans-Ulrich Fungal Biology and Biotechnology, Vol. 3, Issue 1 https://doi.org/10.1186/s40694-016-0020-z	journal	March 2016
Plant-Symbiotic Fungi as Chemical Engineers: Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci Schardl, Christopher L.; Young, Carolyn A.; Hesse, Uljana PLoS Genetics, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pgen.1003323	journal	February 2013
Effector gene reshuffling involves dispensable mini-chromosomes in the wheat blast fungus Peng, Zhao; Oliveira-Garcia, Ely; Lin, Guifang PLOS Genetics, Vol. 15, Issue 9 https://doi.org/10.1371/journal.pgen.1008272	journal	September 2019
Is the Pathogenic Ergot Fungus a Conditional Defensive Mutualist for Its Host Grass? Wäli, Pauliina P.; Wäli, Piippa R.; Saikkonen, Kari PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069249	journal	July 2013
Evolution of Linked Avirulence Effectors in Leptosphaeria maculans Is Affected by Genomic Environment and Exposure to Resistance Genes in Host Plants Van de Wouw, Angela P.; Cozijnsen, Anton J.; Hane, James K. PLoS Pathogens, Vol. 6, Issue 11 https://doi.org/10.1371/journal.ppat.1001180	journal	November 2010
The Impact of Recombination Hotspots on Genome Evolution of a Fungal Plant Pathogen Croll, Daniel; Lendenmann, Mark H.; Stewart, Ethan Genetics, Vol. 201, Issue 3 https://doi.org/10.1534/genetics.115.180968	journal	September 2015
Fine-Scale Recombination Maps of Fungal Plant Pathogens Reveal Dynamic Recombination Landscapes and Intragenic Hotspots Stukenbrock, Eva H.; Dutheil, Julien Y. Genetics, Vol. 208, Issue 3 https://doi.org/10.1534/genetics.117.300502	journal	March 2018
Fungal Endophytes of Grasses: A Defensive Mutualism between Plants and Fungi Clay, Keith Ecology, Vol. 69, Issue 1 https://doi.org/10.2307/1943155	journal	February 1988
Advances in Research on Epichloë endophytes in Chinese Native Grasses Song, Hui; Nan, Zhibiao; Song, Qiuyan Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01399	journal	September 2016
Genomic and Genetic Insights Into a Cosmopolitan Fungus, Paecilomyces variotii (Eurotiales) Urquhart, Andrew S.; Mondo, Stephen J.; Mäkelä, Miia R. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03058	journal	December 2018
Secondary metabolites in fungus-plant interactions Pusztahelyi, TÃ¼nde; Holb, Imre J.; PÃ³csi, IstvÃ¡n Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00573	journal	August 2015
Ergochromes: Heretofore Neglected Side of Ergot Toxicity Flieger, Miroslav; Stodůlková, Eva; Wyka, Stephen A. Toxins, Vol. 11, Issue 8 https://doi.org/10.3390/toxins11080439	journal	July 2019
Identification and characterization of the ergochrome gene cluster in the plant pathogenic fungus Claviceps purpurea Neubauer, Lisa; Dopstadt, Julian; Humpf, Hans-Ulrich Figshare https://doi.org/10.6084/m9.figshare.c.3611099	collection	January 2016
Cross-talk of the biotrophic pathogen Claviceps purpurea and its host Secale cereale Oeser, Birgitt; Kind, Sabine; Schurack, Selma Figshare https://doi.org/10.6084/m9.figshare.c.3733138	collection	January 2017
A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici Badet, Thomas; Oggenfuss, Ursula; Abraham, Leen figshare https://doi.org/10.6084/m9.figshare.c.4852938.v1	collection	January 2020