Functional analysis of the mating type genes in Verticillium dahliae.
Verticillium dahliae
Asexual reproduction
Mating type
Pheromone
Sexual reproduction
Virulence
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
07 May 2024
07 May 2024
Historique:
received:
06
12
2023
accepted:
22
04
2024
medline:
8
5
2024
pubmed:
8
5
2024
entrez:
7
5
2024
Statut:
epublish
Résumé
Populations of the plant pathogenic fungus Verticillium dahliae display a complex and rich genetic diversity, yet the existence of sexual reproduction in the fungus remains contested. As pivotal genes, MAT genes play a crucial role in regulating cell differentiation, morphological development, and mating of compatible cells. However, the functions of the two mating type genes in V. dahliae, VdMAT1-1-1, and VdMAT1-2-1, remain poorly understood. In this study, we confirmed that the MAT loci in V. dahliae are highly conserved, including both VdMAT1-1-1 and VdMAT1-2-1 which share high collinearity. The conserved core transcription factor encoded by the two MAT loci may facilitate the regulation of pheromone precursor and pheromone receptor genes by directly binding to their promoter regions. Additionally, peptide activity assays demonstrated that the signal peptide of the pheromone VdPpg1 possessed secretory activity, while VdPpg2, lacked a predicted signal peptide. Chemotactic growth assays revealed that V. dahliae senses and grows towards the pheromones FO-a and FO-α of Fusarium oxysporum, as well as towards VdPpg2 of V. dahliae, but not in response to VdPpg1. The findings herein also revealed that VdMAT1-1-1 and VdMAT1-2-1 regulate vegetative growth, carbon source utilization, and resistance to stressors in V. dahliae, while negatively regulating virulence. These findings underscore the potential roles of VdMAT1-1-1 and VdMAT1-2-1 in sexual reproduction and confirm their involvement in various asexual processes of V. dahliae, offering novel insights into the functions of mating type genes in this species.
Sections du résumé
BACKGROUND
BACKGROUND
Populations of the plant pathogenic fungus Verticillium dahliae display a complex and rich genetic diversity, yet the existence of sexual reproduction in the fungus remains contested. As pivotal genes, MAT genes play a crucial role in regulating cell differentiation, morphological development, and mating of compatible cells. However, the functions of the two mating type genes in V. dahliae, VdMAT1-1-1, and VdMAT1-2-1, remain poorly understood.
RESULTS
RESULTS
In this study, we confirmed that the MAT loci in V. dahliae are highly conserved, including both VdMAT1-1-1 and VdMAT1-2-1 which share high collinearity. The conserved core transcription factor encoded by the two MAT loci may facilitate the regulation of pheromone precursor and pheromone receptor genes by directly binding to their promoter regions. Additionally, peptide activity assays demonstrated that the signal peptide of the pheromone VdPpg1 possessed secretory activity, while VdPpg2, lacked a predicted signal peptide. Chemotactic growth assays revealed that V. dahliae senses and grows towards the pheromones FO-a and FO-α of Fusarium oxysporum, as well as towards VdPpg2 of V. dahliae, but not in response to VdPpg1. The findings herein also revealed that VdMAT1-1-1 and VdMAT1-2-1 regulate vegetative growth, carbon source utilization, and resistance to stressors in V. dahliae, while negatively regulating virulence.
CONCLUSIONS
CONCLUSIONS
These findings underscore the potential roles of VdMAT1-1-1 and VdMAT1-2-1 in sexual reproduction and confirm their involvement in various asexual processes of V. dahliae, offering novel insights into the functions of mating type genes in this species.
Identifiants
pubmed: 38714997
doi: 10.1186/s12915-024-01900-6
pii: 10.1186/s12915-024-01900-6
doi:
Substances chimiques
Pheromones
0
Fungal Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
108Subventions
Organisme : National Key Research and Development Program of China
ID : 2022YFE0130800
Organisme : National Key Research and Development Program of China
ID : 2022YFD1400300
Organisme : National Key Research and Development Program of China
ID : 2022YFE0111300
Organisme : Fundamental Research Funds for Central Non‑profit Scientific Institution in CAAS
ID : Y2021XK22
Organisme : National Natural Science Foundation of China
ID : 32370213
Organisme : National Natural Science Foundation of China
ID : 32270212
Informations de copyright
© 2024. The Author(s).
Références
Alby K, Schaefer D, Bennett RJ. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature. 2009;460(7257):890–3. https://doi.org/10.1038/nature08252 .
doi: 10.1038/nature08252
pubmed: 19675652
pmcid: 2866515
Almeida P, Barbosa R, Zalar P, Imanishi Y, Shimizu K, Turchetti B, et al. A population genomics insight into the Mediterranean origins of wine yeast domestication. Mol Ecol. 2015;24(21):5412–27. https://doi.org/10.1111/mec.13341 .
doi: 10.1111/mec.13341
pubmed: 26248006
Alvaro CG, Thorner J. Heterotrimeric G protein-coupled receptor signaling in yeast mating pheromone response. J Biol Chem. 2016;291(15):7788–95. https://doi.org/10.1074/jbc.R116.714980 .
doi: 10.1074/jbc.R116.714980
pubmed: 26907689
pmcid: 4824985
Baroudy F, Habib W, Tanos G, Gerges E, Saab C, Choueiri E, et al. Long-distance spread of Verticillium dahliae through rivers and irrigation systems. Plant Dis. 2018;102(8):1559–65. https://doi.org/10.1094/PDIS-08-17-1189-RE .
doi: 10.1094/PDIS-08-17-1189-RE
pubmed: 30673424
Becker K, Beer C, Freitag M, Kück U. Genome-wide identification of target genes of a mating type α-domain transcription factor reveals functions beyond sexual development. Mol Microbiol. 2015;96(5):1002–22. https://doi.org/10.1111/mmi.12987 .
doi: 10.1111/mmi.12987
pubmed: 25728030
Bhat RG, Smith RF, Koike ST, Wu BM, Subbarao KV. Characterization of Verticillium dahliae isolates and wilt epidemics of pepper. Plant Dis. 2003;87(7):789–97. https://doi.org/10.1094/PDIS.2003.87.7.789 .
doi: 10.1094/PDIS.2003.87.7.789
pubmed: 30812888
Bobrowicz P, Pawlak R, Correa A, Bell-Pedersen D, Ebbole DJ. The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock. Mol Microbiol. 2002;45(3):795–804. https://doi.org/10.1046/j.1365-2958.2002.03052.x .
doi: 10.1046/j.1365-2958.2002.03052.x
pubmed: 12139624
Böhm J, Hoff B, O’Gorman CM, Wolfers S, Klix V, Binger D, et al. Sexual reproduction and mating type-mediated strain development in the penicillin-producing fungus Penicillium chrysogenum. Proc Natl Acad Sci U S A. 2013;110(4):1476–81. https://doi.org/10.1073/pnas.1217943110 .
doi: 10.1073/pnas.1217943110
pubmed: 23307807
pmcid: 3557024
Chen H, Zou Y, Shang Y, Lin H, Wang Y, Cai R, et al. Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 2008;146(2):368–76. https://doi.org/10.1104/pp.107.111740 .
doi: 10.1104/pp.107.111740
pubmed: 18065554
pmcid: 2245818
Chen JY, Klosterman SJ, Hu XP, Dai XF, Subbarao KV. Key Insights and research prospects at the dawn of the population genomics era for Verticillium dahliae. Annu Rev Phytopathol. 2021;59:31–51. https://doi.org/10.1146/annurev-phyto-020620-121925 .
doi: 10.1146/annurev-phyto-020620-121925
pubmed: 33891830
Chen JY, Liu C, Gui YJ, Gui YJ, Si KW, Zhang DD, Wang J, et al. Comparative genomics reveals cotton-specific virulence factors in flexible genomic regions in Verticillium dahliae and evidence of horizontal gene transfer from Fusarium. New Phytol. 2018;217(2):756–70. https://doi.org/10.1111/nph.14861 .
doi: 10.1111/nph.14861
pubmed: 29084346
Clark-Cotton MR, Jacobs KC, Lew DJ. Chemotropism and cell-cell fusion in fungi. Microbiol Mol Biol Rev. 2022;86(1):e0016521. https://doi.org/10.1128/mmbr.00165-21 .
doi: 10.1128/mmbr.00165-21
pubmed: 35138122
Collado-Romero M, Mercado-Blanco J, Olivares-García C, Jiménez-Díaz RM. Phylogenetic analysis of Verticillium dahliae vegetative compatibility groups. Phytopathology. 2008;98(9):1019–28. https://doi.org/10.1094/PHYTO-98-9-1019 .
doi: 10.1094/PHYTO-98-9-1019
pubmed: 18943740
Collado-Romero M, Mercado-Blanco J, Olivares-García C, Valverde-Corredor A, Jiménez-Díaz RM. Molecular variability within and among Verticillium dahliae vegetative compatibility groups determined by fluorescent amplified fragment length polymorphism and polymerase chain reaction markers. Phytopathology. 2006;96(5):485–95. https://doi.org/10.1094/PHYTO-96-0485 .
doi: 10.1094/PHYTO-96-0485
pubmed: 18944308
de Jonge R, Bolton MD, Kombrink A, van den Berg GC, Yadeta KA, Thomma BP. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 2013;23(8):1271–82. https://doi.org/10.1101/gr.152660.112 .
doi: 10.1101/gr.152660.112
pubmed: 23685541
pmcid: 3730101
Dohlman HG. G proteins and pheromone signaling. Annu Rev Physiol. 2002;64:129–52. https://doi.org/10.1146/annurev.physiol.64.081701.133448 .
doi: 10.1146/annurev.physiol.64.081701.133448
pubmed: 11826266
Doughan B, Rollins JA. Characterization of MAT gene functions in the life cycle of Sclerotinia sclerotiorum reveals a lineage-specific MAT gene functioning in apothecium morphogenesis. Fungal Biol. 2016;120(9):1105–17. https://doi.org/10.1016/j.funbio.2016.06.007 .
doi: 10.1016/j.funbio.2016.06.007
pubmed: 27567717
Dung JK, Peever TL, Johnson DA. Verticillium dahliae populations from mint and potato are genetically divergent with predominant haplotypes. Phytopathology. 2013;103(5):445–59. https://doi.org/10.1094/PHYTO-06-12-0133-R .
doi: 10.1094/PHYTO-06-12-0133-R
pubmed: 23113547
Dyer PS, Kück U. Sex and the imperfect fungi. Microbiol Spectr. 2017;5(3). https://doi.org/10.1128/microbiolspec.FUNK-0043-2017 .
Fradin EF, Thomma BP. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol. 2006;7(2):71–86. https://doi.org/10.1111/j.1364-3703.2006.00323.x .
doi: 10.1111/j.1364-3703.2006.00323.x
pubmed: 20507429
Goddard MR, Godfray HC, Burt A. Sex increases the efficacy of natural selection in experimental yeast populations. Nature. 2005;434(7033):636–40. https://doi.org/10.1038/nature03405 .
doi: 10.1038/nature03405
pubmed: 15800622
Gorelick R, Carpinone J. Origin and maintenance of sex: the evolutionary joys of self sex. Biol J Linn Soc. 2009;98:707–28. https://doi.org/10.1111/j.1095-8312.2009.01334.x .
doi: 10.1111/j.1095-8312.2009.01334.x
Gui YJ, Chen JY, Zhang DD, Li NY, Li TG, Zhang WQ, et al. Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate-binding module 1. Environ Microbiol. 2017;19(5):1914–32. https://doi.org/10.1111/1462-2920.13695 .
doi: 10.1111/1462-2920.13695
pubmed: 28205292
Heitman J. Sexual reproduction and the evolution of microbial pathogens. Curr Biol. 2006;16(17):R711–25. https://doi.org/10.1016/j.cub.2006.07.064 .
doi: 10.1016/j.cub.2006.07.064
pubmed: 16950098
Heitman J. Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe. 2010;8(1):86–99. https://doi.org/10.1016/j.chom.2010.06.011 .
doi: 10.1016/j.chom.2010.06.011
pubmed: 20638645
pmcid: 2916653
Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods. 2005;1:13. https://doi.org/10.1186/1746-4811-1-13 .
doi: 10.1186/1746-4811-1-13
pubmed: 16359558
pmcid: 1334188
Inderbitzin P, Davis RM, Bostock RM, Subbarao KV. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLoS One. 2011;6(3):e18260. https://doi.org/10.1371/journal.pone.0018260 .
doi: 10.1371/journal.pone.0018260
pubmed: 21455321
pmcid: 3063834
Jacobs KA, Collins-Racie LA, Colbert M, Duckett M, Golden-Fleet M, Kelleher K, et al. A genetic selection for isolating cDNAs encoding secreted proteins. Gene. 1997;198(1–2):289–96. https://doi.org/10.1016/s0378-1119(97)00330-2 .
doi: 10.1016/s0378-1119(97)00330-2
pubmed: 9370294
Jiménez-GascoMdel M, Malcolm GM, Berbegal M, Armengol J, Jiménez-Díaz RM. Complex molecular relationship between vegetative compatibility groups (VCGs) in Verticillium dahliae: VCGs do not always align with clonal lineages. Phytopathology. 2014;104(6):650–9. https://doi.org/10.1094/PHYTO-07-13-0180-R .
doi: 10.1094/PHYTO-07-13-0180-R
Kim H, Borkovich KA. A pheromone receptor gene, pre-1, is essential for mating type-specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Mol Microbiol. 2004;52(6):1781–98. https://doi.org/10.1111/j.1365-2958.2004.04096.x .
doi: 10.1111/j.1365-2958.2004.04096.x
pubmed: 15186425
Kim H, Borkovich KA. Pheromones are essential for male fertility and sufficient to direct chemotropic polarized growth of trichogynes during mating in Neurospora crassa. Eukaryot Cell. 2006;5(3):544–54. https://doi.org/10.1128/EC.5.3.544-554.2006 .
doi: 10.1128/EC.5.3.544-554.2006
pubmed: 16524909
pmcid: 1398069
Kim HK, Jo SM, Kim GY, Kim DW, Kim YK, Yun SH. A Large-Scale Functional analysis of putative target genes of mating type loci provides insight into the regulation of sexual development of the cereal pathogen Fusarium graminearum. PLoS Genet. 2015;11(9):e1005486. https://doi.org/10.1371/journal.pgen.1005486 . Published 2015 Sep 3.
doi: 10.1371/journal.pgen.1005486
pubmed: 26334536
pmcid: 4559316
Klix V, Nowrousian M, Ringelberg C, Loros JJ, Dunlap JC, Pöggeler S. Functional characterization of MAT1-1-specific mating type genes in the homothallic ascomycete Sordaria macrospora provides new insights into essential and nonessential sexual regulators. Eukaryot Cell. 2010;9(6):894–905. https://doi.org/10.1128/EC.00019-10 .
doi: 10.1128/EC.00019-10
pubmed: 20435701
pmcid: 2901639
Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV. Diversity, pathogenicity, and management of verticillium species. Annu Rev Phytopathol. 2009;47:39–62. https://doi.org/10.1146/annurev-phyto-080508-081748 .
doi: 10.1146/annurev-phyto-080508-081748
pubmed: 19385730
Kück U, Pöggeler S. Cryptic sex in fungi. Fungal Biol Rev. 2009;23:86–90. https://doi.org/10.1016/j.fbr.2009.10.004 .
doi: 10.1016/j.fbr.2009.10.004
Kück U, Böhm J. mating type genes and cryptic sexuality as tools for genetically manipulating industrial molds. Appl Microbiol Biotechnol. 2013;97(22):9609–20. https://doi.org/10.1007/s00253-013-5268-0 .
doi: 10.1007/s00253-013-5268-0
pubmed: 24085397
Lee J, Leslie JF, Bowden RL. Expression and function of sex pheromones and receptors in the homothallic ascomycete Gibberella zeae. Eukaryot Cell. 2008;7(7):1211–21. https://doi.org/10.1128/EC.00272-07 .
doi: 10.1128/EC.00272-07
pubmed: 18503004
pmcid: 2446672
Lee SC, Ni M, Li W, Shertz C, Heitman J. The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev. 2010;74(2):298–340. https://doi.org/10.1128/MMBR.00005-10 .
doi: 10.1128/MMBR.00005-10
pubmed: 20508251
pmcid: 2884414
Lin X, Hull CM, Heitman J. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature. 2005;434(7036):1017–21. https://doi.org/10.1038/nature03448 .
doi: 10.1038/nature03448
pubmed: 15846346
Liu SY, Chen JY, Wang JL, et al. Molecular characterization and functional analysis of a specific secreted protein from highly virulent defoliating Verticillium dahliae. Gene. 2013;529(2):307–16. https://doi.org/10.1016/j.gene.2013.06.089 .
doi: 10.1016/j.gene.2013.06.089
pubmed: 23891822
Lobuglio KF, Taylor JW. Recombination and genetic differentiation in the mycorrhizal fungus Cenococcum geophilum Fr. Mycologia. 2002;94(5):772–80. https://doi.org/10.1080/15572536.2003.11833171 .
doi: 10.1080/15572536.2003.11833171
pubmed: 21156551
Mayrhofer S, Weber JM, Pöggeler S. Pheromones and pheromone receptors are required for proper sexual development in the homothallic ascomycete Sordaria macrospora. Genetics. 2006;172(3):1521–33. https://doi.org/10.1534/genetics.105.047381 .
doi: 10.1534/genetics.105.047381
pubmed: 16387884
pmcid: 1456310
McDonald MJ, Rice DP, Desai MM. Sex speeds adaptation by altering the dynamics of molecular evolution. Nature. 2016;531(7593):233–6. https://doi.org/10.1038/nature17143 .
doi: 10.1038/nature17143
pubmed: 26909573
pmcid: 4855304
Milgroom MG, Jiménez-GascoMdel M, Olivares García C, Drott MT, Jiménez-Díaz RM. Recombination between clonal lineages of the asexual fungus Verticillium dahliae detected by genotyping by sequencing. PLoS One. 2014;9(9):e106740. https://doi.org/10.1371/journal.pone.0106740 .
doi: 10.1371/journal.pone.0106740
pubmed: 25181515
pmcid: 4152335
Ni M, Feretzaki M, Sun S, Wang X, Heitman J. Sex in fungi. Annu Rev Genet. 2011;45:405–30. https://doi.org/10.1146/annurev-genet-110410-132536 .
doi: 10.1146/annurev-genet-110410-132536
pubmed: 21942368
pmcid: 3310392
Noor MA, Grams KL, Bertucci LA, Reiland J. Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci U S A. 2001;98(21):12084–8. https://doi.org/10.1073/pnas.221274498 .
doi: 10.1073/pnas.221274498
pubmed: 11593019
pmcid: 59771
Ojeda-López M, Chen W, Eagle CE, et al. Evolution of asexual and sexual reproduction in the aspergilli. Stud Mycol. 2018;91:37–59. https://doi.org/10.1016/j.simyco.2018.10.002 .
doi: 10.1016/j.simyco.2018.10.002
pubmed: 30425416
pmcid: 6231087
Otto SP. The evolutionary enigma of sex. Am Nat. 2009;174(Suppl 1):S1–14. https://doi.org/10.1086/599084 .
doi: 10.1086/599084
pubmed: 19441962
Santhanam P, van Esse HP, Albert I, Faino L, Nürnberger T, Thomma BP. Evidence for functional diversification within a fungal NEP1-like protein family. Mol Plant Microbe Interact. 2013;26(3):278–86. https://doi.org/10.1094/MPMI-09-12-0222-R .
doi: 10.1094/MPMI-09-12-0222-R
pubmed: 23051172
Saupe SJ. Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev. 2000;64(3):489–502. https://doi.org/10.1128/MMBR.64.3.489-502.2000 .
doi: 10.1128/MMBR.64.3.489-502.2000
pubmed: 10974123
pmcid: 99001
Schmoll M, Seibel C, Tisch D, Dorrer M, Kubicek CP. A novel class of peptide pheromone precursors in ascomycetous fungi. Mol Microbiol. 2010;77(6):1483–501. https://doi.org/10.1111/j.1365-2958.2010.07295.x .
doi: 10.1111/j.1365-2958.2010.07295.x
pubmed: 20735770
pmcid: 3068285
Seidl MF, Thomma BP. Sex or no sex: evolutionary adaptation occurs regardless. BioEssays. 2014;36(4):335–45. https://doi.org/10.1002/bies.201300155 .
doi: 10.1002/bies.201300155
pubmed: 24531982
pmcid: 4158867
Short DP, Gurung S, Gladieux P, et al. Globally invading populations of the fungal plant pathogen Verticillium dahliae are dominated by multiple divergent lineages. Environ Microbiol. 2015;17(8):2824–40. https://doi.org/10.1111/1462-2920.12789 .
doi: 10.1111/1462-2920.12789
pubmed: 25630463
Short DP, Gurung S, Hu X, Inderbitzin P, Subbarao KV. Maintenance of sex-related genes and the co-occurrence of both mating types in Verticillium dahliae. PLoS One. 2014;9(11):e112145. https://doi.org/10.1371/journal.pone.0112145 .
doi: 10.1371/journal.pone.0112145
pubmed: 25383550
pmcid: 4226480
Sieber B, Coronas-Serna JM, Martin SG. A focus on yeast mating: from pheromone signaling to cell-cell fusion. Semin Cell Dev Biol. 2023;133:83–95. https://doi.org/10.1016/j.semcdb.2022.02.003 .
doi: 10.1016/j.semcdb.2022.02.003
pubmed: 35148940
Taylor J, Jacobson D, Fisher M. The evolution of asexual fungi: reproduction, speciation and classification. Annu Rev Phytopathol. 1999;37:197–246. https://doi.org/10.1146/annurev.phyto.37.1.197 .
doi: 10.1146/annurev.phyto.37.1.197
pubmed: 11701822
Turgeon BG, Yoder OC. Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet Biol. 2000;31(1):1–5. https://doi.org/10.1006/fgbi.2000.1227 .
doi: 10.1006/fgbi.2000.1227
pubmed: 11118130
Usami T, Itoh M, Amemiya Y. Asexual fungus Verticillium dahliae is potentially heterothallic. J Gen Plant Pathol. 2009;75:422–7. https://doi.org/10.1007/s10327-009-0197-6 .
doi: 10.1007/s10327-009-0197-6
Usami T, Itoh M, Amemiya Y. Mating type gene mat1-2-1 is common among japanese isolates of Verticillium dahliae. Physiol Mol Plant P. 2008;73(6):133–7. https://doi.org/10.1016/j.pmpp.2009.04.002 .
doi: 10.1016/j.pmpp.2009.04.002
Vitale S, Di Pietro A, Turrà D. Autocrine pheromone signalling regulates community behaviour in the fungal pathogen Fusarium oxysporum. Nat Microbiol. 2019;4(9):1443–9. https://doi.org/10.1038/s41564-019-0456-z .
doi: 10.1038/s41564-019-0456-z
pubmed: 31133754
Wang JY, Wang SZ, Zhang Z, Hao ZN, Shi XX, Li L, et al. MAT loci play crucial roles in sexual development but are dispensable for asexual reproduction and pathogenicity in rice blast fungus Magnaporthe oryzae. J Fungi (Basel). 2021;7(10):858. https://doi.org/10.3390/jof7100858 .
doi: 10.3390/jof7100858
pubmed: 34682279
Wang Q, Wang S, Xiong CL, James TY, Zhang XG. mating type genes of the anamorphic fungus Ulocladium botrytis affect both asexual sporulation and sexual reproduction. Sci Rep. 2017;7(1):7932. https://doi.org/10.1038/s41598-017-08471-3 .
doi: 10.1038/s41598-017-08471-3
pubmed: 28801599
pmcid: 5554195
Wang Y, Dohlman HG. Pheromone signaling mechanisms in yeast: a prototypical sex machine. Science. 2004;306(5701):1508–9. https://doi.org/10.1126/science.1104568 .
doi: 10.1126/science.1104568
pubmed: 15567849
Xu W, Liang G, Peng J, Long Z, Li D, Fu M, et al. The influence of the mating type on virulence of Mucor irregularis. Sci Rep. 2017;7(1):10629. https://doi.org/10.1038/s41598-017-10954-2 .
doi: 10.1038/s41598-017-10954-2
pubmed: 28878325
pmcid: 5587739
Yong M, Yu J, Pan X, et al. Two mating type genes MAT1-1-1 and MAT1-1-2 with significant functions in conidiation, stress response, sexual development, and pathogenicity of rice false smut fungus Villosiclava virens. Curr Genet. 2020;66(5):989–1002. https://doi.org/10.1007/s00294-020-01085-9 .
doi: 10.1007/s00294-020-01085-9
pubmed: 32572596
Zhang DD, Wang J, Wang D, et al. Population genomics demystifies the defoliation phenotype in the plant pathogen Verticillium dahliae. New Phytol. 2019;222(2):1012–29. https://doi.org/10.1111/nph.15672 .
doi: 10.1111/nph.15672
pubmed: 30609067
pmcid: 6594092
Zheng Q, Hou R, Juanyu, et al. The MAT locus genes play different roles in sexual reproduction and pathogenesis in Fusarium graminearum. PLoS One. 2015;10(7):e0131623. https://doi.org/10.1371/journal.pone.0066980 .
Zhou L, Zhao J, Guo W, Zhang T. Functional analysis of autophagy genes via Agrobacterium-mediated transformation in the vascular Wilt fungus Verticillium dahliae. J Genet Genomics. 2013;40(8):421–31. https://doi.org/10.1016/j.jgg.2013.04.006 .
doi: 10.1016/j.jgg.2013.04.006
pubmed: 23969251