.png){kind=logo}
RESEARCH
Characterizing the Dynamics of Virulence and Fungicide Resistance of Phytophthora capsici in Michigan Vegetable Fields Reveals Loci Associated with Virulence
AffiliationsAuthors and Affiliations
- Yufang Guo
- Charles S. Krasnow
- Mary K. Hausbeck †
- Department of Plant, Soil, and Microbial Sciences, Michigan State University, East Lansing, MI
Published Online:6 Feb 2024https://doi.org/10.1094/PDIS-03-23-0576-RE
Abstract
The oomycete Phytophthora capsici is a destructive pathogen infecting more than 50 plant species and is one of the most serious threats to cucurbit production. Phytophthora blight caused by Phytophthora capsici can affect all plant growth stages, and fungicides and cultural controls are used to limit losses. Dissecting pathogen virulence and fungicide resistance can provide insights into pathogenic mechanisms and inform effective management practices to control P. capsici. In this study, we assessed virulence, mefenoxam sensitivity, and genetic diversity of nine P. capsici populations collected from Cucurbitaceae, Solanaceae, and Fabaceae host families in Michigan from 2002 to 2016. We developed 992 simple sequence repeats (SSRs) in the P. capsici genome and identified 60 SSRs located within or close to RXLR-class (Arginine-any amino acid-Leucine-Arginine) effectors and 29 SSRs within or close to effector CRN (CRinkling and Necrosis) family protein, which represent 62 RXLR and 34 putative CRNs. Population structure analysis shows that mefenoxam resistance was not associated with the year of collection, host type, or location, but there were significant differences in virulence among the populations. Using the general linear model and mixed linear model-based association analyses with all effector-related SSR markers, we identified four SSR markers significantly associated with at least one of the virulence-related parameters. Of these, one (Pce_SC18) was in a predicted CRN effector and had high identity with the putative PhCRN37 effector in the pathogen Plasmopara halstedii, which can be further verified for virulence identification in P. capsici.
Literature Cited
- 2017. Phytophthora megakarya and P. palmivora, closely related causal agents of cacao black pod rot, underwent increases in genome sizes and gene numbers by different mechanisms. Genome Biol. Evol. 9:536‐557. https://doi.org/10.1093/gbe/evx021 CrossrefWeb of ScienceGoogle Scholar
- 2009. Age-related resistance of diverse cucurbit fruit to infection by Phytophthora capsici. J. Am. Soc. Hort. Sci. 134:176‐182. https://doi.org/10.21273/jashs.134.2.176 CrossrefWeb of ScienceGoogle Scholar
- 2005. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl. Acad. Sci. U.S.A. 102:7766‐7771. https://doi.org/10.1073/pnas.0500113102 CrossrefWeb of ScienceGoogle Scholar
- 2000. Outbreak of Phytophthora foliar blight and fruit rot in processing pumpkin fields in Illinois. Plant Dis. 84:1345. https://doi.org/10.1094/PDIS.2000.84.12.1345A LinkWeb of ScienceGoogle Scholar
- 2007. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633‐2635. https://doi.org/10.1093/bioinformatics/btm308 CrossrefWeb of ScienceGoogle Scholar
- 2008. Fitness of isolates of Phytophthora capsici resistant to mefenoxam from squash and pepper fields in North Carolina. Plant Dis. 92:1439‐1443. https://doi.org/10.1094/PDIS-92-10-1439 LinkWeb of ScienceGoogle Scholar
- 2017. Temporal genetic dynamics of an experimental, biparental field population of Phytophthora capsici. Front. Genet. 8:26. https://doi.org/10.3389/fgene.2017.00026 CrossrefWeb of ScienceGoogle Scholar
- 2017. Genetic diversity of Phytophthora capsici recovered from Massachusetts between 1997 and 2014. Mycol. Prog. 16:999‐1006. https://doi.org/10.1007/s11557-017-1334-9 CrossrefWeb of ScienceGoogle Scholar
- 2019. The RXLR effector PcAvh1 is required for full virulence of Phytophthora capsici. Mol. Plant-Microbe Interact. 32:986‐1000. https://doi.org/10.1094/MPMI-09-18-0251-R LinkWeb of ScienceGoogle Scholar
- 2013. A genome-wide association study identifies genomic regions for virulence in the non-model organism Heterobasidion annosum s.s. PLoS One 8:e53525. https://doi.org/10.1371/journal.pone.0053525 CrossrefWeb of ScienceGoogle Scholar
- 2014. Evolution of an experimental population of Phytophthora capsici in the field. Phytopathology 104:1107‐1117. https://doi.org/10.1094/PHYTO-12-13-0346-R LinkWeb of ScienceGoogle Scholar
- 2012. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4:359‐361. https://doi.org/10.1007/s12686-011-9548-7 CrossrefWeb of ScienceGoogle Scholar
- 1972. The sampling theory of selectively neutral alleles. Theor. Popul. Biol. 3:87‐112. https://doi.org/10.1016/0040-5809(72)90035-4 CrossrefWeb of ScienceGoogle Scholar
- 2018. A Phytophthora capsici RXLR effector targets and inhibits a plant PPIase to suppress endoplasmic reticulum-mediated immunity. Mol. Plant 11:1067‐1083. https://doi.org/10.1016/j.molp.2018.05.009 CrossrefWeb of ScienceGoogle Scholar
- 2011. Identification of 18 genes encoding necrosis-inducing proteins from the plant pathogen Phytophthora capsici (Pythiaceae: Oomycetes). Genet. Mol. Res. 10:910‐922. https://doi.org/10.4238/vol10-2gmr1248 CrossrefWeb of ScienceGoogle Scholar
- 2010. Resistance of pepper to Phytophthora crown, root, and fruit rot is affected by isolate virulence. Plant Dis. 94:24‐30. https://doi.org/10.1094/PDIS-94-1-0024 LinkWeb of ScienceGoogle Scholar
- 2016. Validation of genome-wide association studies as a tool to identify virulence factors in Parastagonospora nodorum. Phytopathology 106:1177‐1185. https://doi.org/10.1094/PHYTO-02-16-0113-FI LinkWeb of ScienceGoogle Scholar
- 2016. RXLR and CRN effectors from the sunflower downy mildew pathogen Plasmopara halstedii induce hypersensitive-like responses in resistant sunflower lines. Front Plant Sci. 7:1887. https://doi.org/10.3389/fpls.2016.01887 CrossrefWeb of ScienceGoogle Scholar
- 2006. A detached cucumber fruit method to screen for resistance to Phytophthora capsici and effect of fruit age on susceptibility to infection. Plant Dis. 90:1276‐1282. https://doi.org/10.1094/PD-90-1276 LinkWeb of ScienceGoogle Scholar
- 2007. Characterization of Phytophthora capsici from Michigan surface irrigation water. Phytopathology 97:421-428. LinkWeb of ScienceGoogle Scholar
- 2008. Characterization of Phytophthora capsici causing foliar and pod blight of snap bean in Michigan. Plant Dis. 92:201-209. LinkWeb of ScienceGoogle Scholar
- 2020. Is the phenomenon of mefenoxam-acquired resistance in Phytophthora infestans universal? Plant Dis. 104:211‐221. https://doi.org/10.1094/PDIS-10-18-1906-RE LinkWeb of ScienceGoogle Scholar
- 1997. The population genetics of Phytophthora. Phytopathology 87:462‐473. https://doi.org/10.1094/PHYTO.1997.87.4.462 LinkWeb of ScienceGoogle Scholar
- 2012a. Advances in research on Phytophthora capsici on vegetable crops in the United States. Plant Dis. 96:1588‐1600. https://doi.org/10.1094/PDIS-02-12-0211-FE LinkWeb of ScienceGoogle Scholar
- 2012b. Differences in virulence of Phytophthora capsici isolates from a worldwide collection on host fruits. Eur. J. Plant Pathol. 132:281‐296. https://doi.org/10.1007/s10658-011-9873-4 CrossrefWeb of ScienceGoogle Scholar
- 2011. Evolution and population genetics of exotic and re-emerging pathogens: Novel tools and approaches. Annu. Rev. Phytopathol. 49:249‐267. https://doi.org/10.1146/annurev-phyto-072910-095246 CrossrefWeb of ScienceGoogle Scholar
- 2004. Phytophthora capsici on vegetable crops: Research progress and management challenges. Plant Dis. 88:1292‐1303. https://doi.org/10.1094/PDIS.2004.88.12.1292 LinkWeb of ScienceGoogle Scholar
- 2007. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801‐1806. https://doi.org/10.1093/bioinformatics/btm233 CrossrefWeb of ScienceGoogle Scholar
- 2011. adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070‐3071. https://doi.org/10.1093/bioinformatics/btr521 CrossrefWeb of ScienceGoogle Scholar
- 2010. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11:94. https://doi.org/10.1186/1471-2156-11-94 CrossrefWeb of ScienceGoogle Scholar
- 2013. Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biol. 14:R63. https://doi.org/10.1186/gb-2013-14-6-r63 CrossrefWeb of ScienceGoogle Scholar
- 2014. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281. https://doi.org/10.7717/peerj.281 CrossrefWeb of ScienceGoogle Scholar
- 2008. Efficient control of population structure in model organism association mapping. Genetics 178:1709‐1723. https://doi.org/10.1534/genetics.107.080101 CrossrefWeb of ScienceGoogle Scholar
- 1992. Virulence to Korean pepper cultivars of isolates of Phytophthora capsici from different geographic regions. Plant Dis. 76:486‐489. https://doi.org/10.1094/PD-76-0486 CrossrefWeb of ScienceGoogle Scholar
- 2016. Evaluation of winter squash and pumpkin cultivars for age-related resistance to Phytophthora capsici fruit rot. HortScience 51:1251‐1255. https://doi.org/10.21273/hortsci11173-16 CrossrefWeb of ScienceGoogle Scholar
- 2017. Evaluation of pepper root rot resistance in an integrated Phytophthora blight management program. HortTechnology 27:408‐415. https://doi.org/10.21273/horttech03697-17 CrossrefWeb of ScienceGoogle Scholar
- 2000. Mefenoxam insensitivity and the sexual stage of Phytophthora capsici in Michigan cucurbit fields. Phytopathology 90:396‐400. https://doi.org/10.1094/PHYTO.2000.90.4.396 LinkWeb of ScienceGoogle Scholar
- 2001. Investigating the spatiotemporal genetic structure of Phytophthora capsici in Michigan. Phytopathology 91:973‐980. https://doi.org/10.1094/PHYTO.2001.91.10.973 LinkWeb of ScienceGoogle Scholar
- 2012. Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol. Plant-Microbe Interact. 25:1350‐1360. https://doi.org/10.1094/MPMI-02-12-0028-R LinkWeb of ScienceGoogle Scholar
- 2003. PyPop: A software framework for population genomics: Analyzing large-scale multi-locus genotype data. Pac. Symp. Biocomput. 8:514‐525. https://doi.org/10.1142/9789812776303_0048 Google Scholar
- 2012. Variation and selection of quantitative traits in plant pathogens. Annu. Rev. Phytopathol. 50:319‐338. https://doi.org/10.1146/annurev-phyto-081211-173031 CrossrefWeb of ScienceGoogle Scholar
- 2011. Isolation of nine Phytophthora capsici pectin methylesterase genes which are differentially expressed in various plant species. J. Basic Microbiol. 51:61‐70. https://doi.org/10.1002/jobm.201000317 CrossrefWeb of ScienceGoogle Scholar
- 2020. A Phytophthora capsici effector suppresses plant immunity via interaction with EDS1. Mol. Plant Pathol. 21:502‐511. https://doi.org/10.1111/mpp.12912 CrossrefWeb of ScienceGoogle Scholar
- 2021. A Phytophthora capsici RXLR effector targets and inhibits the central immune kinases to suppress plant immunity. New Phytol. 232:264‐278. https://doi.org/10.1111/nph.17573 CrossrefWeb of ScienceGoogle Scholar
- 2016. Genomes and virulence difference between two physiological races of Phytophthora nicotianae. Gigascience 5:3. https://doi.org/10.1186/s13742-016-0108-7 CrossrefWeb of ScienceGoogle Scholar
- 2011. Two host cytoplasmic effectors are required for pathogenesis of Phytophthora sojae by suppression of host defenses. Plant Physiol. 155:490‐501. https://doi.org/10.1104/pp.110.166470 CrossrefWeb of ScienceGoogle Scholar
- 2015. A virulence essential CRN effector of Phytophthora capsici suppresses host defense and induces cell death in plant nucleus. PLoS One 10:e0127965. https://doi.org/10.1371/journal.pone.0127965 CrossrefWeb of ScienceGoogle Scholar
- 2013. Using soil-applied fungicides to manage Phytophthora crown and root rot on summer squash. Plant Dis. 97:107‐112. https://doi.org/10.1094/PDIS-12-11-1071-RE LinkWeb of ScienceGoogle Scholar
- 2016. Activity of the novel fungicide oxathiapiprolin against plant‐pathogenic oomycetes. Pest Manag. Sci. 72:1572‐1577. https://doi.org/10.1002/ps.4189 CrossrefWeb of ScienceGoogle Scholar
- 2003. Differentiation of race specific resistance to Phytophthora root rot and foliar blight in Capsicum annuum. J. Am. Soc. Hortic. Sci. 128:213‐218. https://doi.org/10.21273/jashs.128.2.0213 CrossrefWeb of ScienceGoogle Scholar
- 2008. Evaluation of Cucurbita pepo accessions for crown rot resistance to isolates of Phytophthora capsici. HortScience 43:1996‐1999. https://doi.org/10.21273/hortsci.43.7.1996 CrossrefWeb of ScienceGoogle Scholar
- 1988. Phytophthora root rot of pepper influence of host genotype and pathogen strain on the inoculum density-disease severity relationships. J. Phytopathol. 123:25‐33. https://doi.org/10.1111/j.1439-0434.1988.tb01033.x CrossrefWeb of ScienceGoogle Scholar
- 2001. Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing Phytophthora blight of bell pepper. Plant Dis. 85:1069‐1075. https://doi.org/10.1094/PDIS.2001.85.10.1069 LinkWeb of ScienceGoogle Scholar
- 2012. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537‐2539. https://doi.org/10.1093/bioinformatics/bts460 CrossrefWeb of ScienceGoogle Scholar
- 2010. Factors of the Fusarium verticillioides-maize environment modulating fumonisin production. Crit. Rev. Microbiol. 36:221‐231. https://doi.org/10.3109/10408411003720209 CrossrefWeb of ScienceGoogle Scholar
- 1972. Identification of strains and inheritance of pathogenicity in Phytophthora capsici. Phytopathology 62:20‐26. https://doi.org/10.1094/Phyto-62-20 CrossrefWeb of ScienceGoogle Scholar
- 2000. Inference of population structure using multilocus genotype data. Genetics 155:945‐959. https://doi.org/10.1093/genetics/155.2.945 CrossrefWeb of ScienceGoogle Scholar
- 2009. Susceptibility of Fraser fir to Phytophthora capsici. Plant Dis. 93:135‐141. https://doi.org/10.1094/PDIS-93-2-0135 LinkWeb of ScienceGoogle Scholar
- 2010. Differences in virulence of Phytophthora capsici isolates from a worldwide collection on zucchini fruits. Pages 248-251 in: Proc. of Cucurbitaceae 2010. J. A. Thies, C. S. Kousik, and A. Levi, eds. American Society of Horticultural Science, Alexandria, VA. Google Scholar
- 2011. Investigating the genetic structure of Phytophthora capsici populations. Phytopathology 101:1061‐1073. https://doi.org/10.1094/PHYTO-11-10-0325 LinkWeb of ScienceGoogle Scholar
- 1990. Intraspecific variation among isolates of Phytophthora capsici from pepper and cucurbit fields in North Carolina. Phytopathology 80:1253‐1259. https://doi.org/10.1094/Phyto-80-1253 CrossrefWeb of ScienceGoogle Scholar
- 1999. Ecologically based approaches to management of Phytophthora blight on bell pepper. Plant Dis. 83:1080‐1089. https://doi.org/10.1094/PDIS.1999.83.12.1080 LinkWeb of ScienceGoogle Scholar
- 2004. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes 4:137‐138. https://doi.org/10.1046/j.1471-8286.2003.00566.x CrossrefWeb of ScienceGoogle Scholar
- 2019. Identification of Phytophthora capsici causing collar rot in hot peppers in Trinidad. Can. J. Plant Pathol. 41:129‐134. https://doi.org/10.1080/07060661.2018.1564940 CrossrefWeb of ScienceGoogle Scholar
- 2013. Characterization of cell death inducing Phytophthora capsici CRN effectors suggests diverse activities in the host nucleus. Front. Plant Sci. 4:387. https://doi.org/10.3389/fpls.2013.00387 CrossrefWeb of ScienceGoogle Scholar
- 2003. Genetic variation among isolates of Phytophthora capsici from Illinois. (Abstr.) Phytopathology 93:S84. https://doi.org/10.1094/PHYTO.2003.93.6.S1 Google Scholar
- 2020. First report of Phytophthora capsici causing wilting and root and crown rot on Capsicum annuum (bell pepper) in Ecuador. Plant Dis. 104:2032. https://doi.org/10.1094/PDIS-11-19-2432-PDN LinkWeb of ScienceGoogle Scholar
- 2021. Genome-wide association study in New York Phytophthora capsici isolates reveals loci involved in mating type and mefenoxam sensitivity. Phytopathology 111:204‐216. https://doi.org/10.1094/PHYTO-04-20-0112-FI LinkWeb of ScienceGoogle Scholar
- 2021. Fitness and competitive ability of field isolates of Phytophthora capsici resistant or sensitive to fluopicolide. Plant Dis. 105:873‐878. https://doi.org/10.1094/PDIS-08-20-1729-RE LinkWeb of ScienceGoogle Scholar
- 1978. The homozygosity test of neutrality. Genetics 88:405‐417. https://doi.org/10.1093/genetics/88.2.405 CrossrefWeb of ScienceGoogle Scholar
- 2012. Avirulence protein 3a (AVR3a) from the potato pathogen Phytophthora infestans forms homodimers through its predicted translocation region and does not specifically bind phospholipids. J. Biol. Chem. 287:38101‐38109. https://doi.org/10.1074/jbc.M112.395129 CrossrefWeb of ScienceGoogle Scholar
- 2020. Sensitivity of different developmental stages and resistance risk assessment of Phytophthora capsici to fluopicolide in China. Front. Microbiol. 11:185. https://doi.org/10.3389/fmicb.2020.00185 CrossrefWeb of ScienceGoogle Scholar
- 2006. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38:203‐208. https://doi.org/10.1038/ng1702 CrossrefWeb of ScienceGoogle Scholar
- 2015. Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases. Plant Physiol. 167:164‐175. https://doi.org/10.1104/pp.114.252437 CrossrefWeb of ScienceGoogle Scholar
