Population Dynamics of Phytophthora infestans in Egypt Reveals Clonal Dominance of 23_A1 and Displacement of 13_A2 Clonal Lineage
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Collection and Isolation
2.2. Mating Type and Metalaxyl Sensitivity Assessment
2.3. Aggressiveness Test on Commercial Potato Cultivars
2.4. DNA Extraction and Genotype Identification
2.5. Screening AVR2 and AVR2-like Effector Genes
2.6. Data Analysis
3. Results
3.1. Sample Collection and Isolation
3.2. Mating Type and Metalaxyl Sensitivity Assessment
3.3. Aggressiveness Tests
3.4. Genotyping of Egyptian Isolates
3.5. Analysis of the AV2 and AVR2-like Effector Genes
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Njoroge, A.W.; Andersson, B.; Lees, A.K.; Mutai, C.; Forbes, G.A.; Yuen, J.E.; Pelle, R. Genotyping of Phytophthora infestans in Eastern Africa reveals a dominating invasive European lineage. Phytopathology 2019, 109, 670–680. [Google Scholar] [CrossRef] [Green Version]
- Dong, S.-M.; Zhou, S.-Q. Potato late blight caused by Phytophthora infestans: From molecular interactions to integrated management strategies. J. Integr. Agric. 2022, 21, 3456–3466. [Google Scholar] [CrossRef]
- Fry, W.; Birch, P.; Judelson, H.; Grünwald, N.; Danies, G.; Everts, K.; Gevens, A.; Gugino, B.; Johnson, D.; Johnson, S. Five reasons to consider Phytophthora infestans a reemerging pathogen. Phytopathology 2015, 105, 966–981. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kamoun, S. Molecular genetics of pathogenic oomycetes. Eukaryot. Cell 2003, 2, 191–199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, S.; Boevink, P.C.; Welsh, L.; Zhang, R.; Whisson, S.C.; Birch, P.R. Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways. New Phytol. 2017, 216, 205–215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, J.G.; Hong, S.Y.; Kessel, G.J.; Cooke, D.E.; Vossen, J.H.; Cho, J.H.; Im, J.S.; Park, Y.E.; Cho, K.S. Genotypic and phenotypic characterization of Phytophthora infestans in South Korea during 2009–2016 reveals clonal reproduction and absence of EU_13_A2 genotype. Plant Pathol. 2020, 69, 932–943. [Google Scholar] [CrossRef]
- Elansky, S.; Pobedinskaya, M.; Kokaeva, L.; Statsyuk, N.; Dyakov, Y. Phytophthora infestans populations from the European part of Russia: Genotypic structure and metalaxyl resistance. J. Plant Pathol. 2015, 97, 449–456. [Google Scholar]
- Cardenas, M.; Danies, G.; Tabima, J.; Bernal, A.; Restrepo, S. Phytophthora infestans population structure: A worldwide scale. Acta Biol. Colomb. 2012, 17, 227–240. [Google Scholar]
- Goodwin, S.B.; Cohen, B.A.; Fry, W.E. Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. Proc. Natl. Acad. Sci. USA 1994, 91, 11591–11595. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.; Cooke, D.E.; Jacobsen, E.; van der Lee, T. Efficient multiplex simple sequence repeat genotyping of the oomycete plant pathogen Phytophthora infestans. J. Microbiol. Methods 2013, 92, 316–322. [Google Scholar] [CrossRef]
- Gilroy, E.M.; Breen, S.; Whisson, S.C.; Squires, J.; Hein, I.; Kaczmarek, M.; Turnbull, D.; Boevink, P.C.; Lokossou, A.; Cano, L.M. Presence/absence, differential expression and sequence polymorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants. New Phytol. 2011, 191, 763–776. [Google Scholar] [CrossRef] [PubMed]
- Vleeshouwers, V.G.; Raffaele, S.; Vossen, J.H.; Champouret, N.; Oliva, R.; Segretin, M.E.; Rietman, H.; Cano, L.M.; Lokossou, A.; Kessel, G.; et al. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 2011, 49, 507–531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El-Ganainy, S.M.; Iqbal, Z.; Awad, H.M.; Sattar, M.N.; Tohamy, A.M.; Abbas, A.O.; Squires, J.; Cooke, D.E. Genotypic and phenotypic structure of the population of Phytophthora infestans in Egypt revealed the presence of European genotypes. J. Fungi 2022, 8, 468. [Google Scholar] [CrossRef] [PubMed]
- Dyer, A.; Matusralt, M.; Drenth, A.; Cohen, A.; Splelman, L. Historical and recent migrations of Phytophthora infestans: Chronology, pathways, and implications. Plant Dis. 1993, 77, 653–661. [Google Scholar]
- Goodwin, S.B.; Spielman, L.J.; Matuszak, J.; Bergeron, S.; Fry, W. Clonal diversity and genetic differentiation of Phytophthora infestans populations in northern and central Mexico. Phytopathology 1992, 82, 955–961. [Google Scholar] [CrossRef]
- Goodwin, S.B.; Drenth, A. Origin of the A2 mating type of Phytophthora infestans outside Mexico. Phytopathology 1997, 87, 992–999. [Google Scholar] [CrossRef] [Green Version]
- Daggett, S.; Götz, E.; Therrien, C. Phenotypic changes in populations of Phytophthora infestans from eastern Germany. Phytopathology 1993, 83, 319–323. [Google Scholar] [CrossRef]
- Cooke, D.E.; Cano, L.M.; Raffaele, S.; Bain, R.A.; Cooke, L.R.; Etherington, G.J.; Deahl, K.L.; Farrer, R.A.; Gilroy, E.M.; Goss, E.M. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathog. 2012, 8, e1002940. [Google Scholar] [CrossRef]
- Rekad, F.Z.; Cooke, D.E.L.; Puglisi, I.; Randall, E.; Guenaoui, Y.; Bouznad, Z.; Evoli, M.; Pane, A.; Schena, L.; di San Lio, G.M. Characterization of Phytophthora infestans populations in northwestern Algeria during 2008–2014. Fungal Biol. 2017, 121, 467–477. [Google Scholar] [CrossRef]
- Saville, A.C.; Ristaino, J.B. Global historic pandemics caused by the FAM-1 genotype of Phytophthora infestans on six continents. Sci. Rep. 2021, 11, 12335. [Google Scholar] [CrossRef]
- Njoroge, A.; Tusiime, G.; Forbes, G.; Yuen, J. Displacement of US-1 clonal lineage by a new lineage of Phytophthora infestans on potato in Kenya and Uganda. Plant Pathol. 2016, 65, 587–592. [Google Scholar] [CrossRef] [Green Version]
- Puidet, B.; Mabon, R.; Guibert, M.; Kiiker, R.; Loit, K.; Le, V.H.; Eikemo, H.; Dewaegeneire, P.; Saubeau, G.; Chatot, C.; et al. Investigating phenotypic traits as potential drivers of the emergence of EU_37_A2, an invasive new lineage of Phytophthora infestans in Western Europe. Plant Pathol. 2023. [Google Scholar] [CrossRef]
- Saad, N. Epiphytology of Potato Blight in Arab Republic of Egypt. Ph.D. Thesis, Cairo University, Giza, Egypt, 1978. [Google Scholar]
- El-Korany, A.E. Occurrence of oospores of Phytophthora infestans in the field and under controlled conditions. Alex. J. Agric. Sci. 2008, 7, 31–52. [Google Scholar]
- El-Sheikh, M.A.; El-Farnawany, M.; EI-Korany, A. Characterization of the Egyptian population of tomato isolates of Phytophthora infestans. J. Agric. Env. Sci. 2005, 37–55, 37–55. [Google Scholar]
- Harbaoui, K.; Hamada, W.; Li, Y.; Vleeshouwers, V.G.; van der Lee, T. Increased difficulties to control late blight in Tunisia are caused by a genetically diverse Phytophthora infestans population next to the clonal lineage NA-01. Plant Dis. 2014, 98, 898–908. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sedegui, M.; Carroll, R.; Morehart, A.; Evans, T.; Kim, S.; Lakhdar, R.; Arifi, A. Genetic structure of the Phytophthora infestans population in Morocco. Plant Dis. 2000, 84, 173–176. [Google Scholar] [CrossRef] [Green Version]
- El-Korany, A.E. Occurrence of the self-fertile phenotype of Phytophthora infestans in El-Behera governorate. Egypt. J. Agri. Sci 2002, 27, 7855–7863. [Google Scholar]
- El-Ganainy, S.; Ahmed, Y.; Soliman, M.; Ismail, A.; Tohamy, A.; Randall, E.; Cooke, D. A shift in the population of Phytophthora infestans on Egyptian potato crops. In Proceedings of the APS annual meeting, Tampa, FL, USA, 30 July–3 August 2016; p. 140. [Google Scholar]
- Deahl, K.; DeMuth, S.; Sinden, S.; Rivera-Pena, A. Identification of mating types and metalaxyl resistance in North American populations of Phytophthora infestans. Am. Potato J. 1995, 72, 35–49. [Google Scholar] [CrossRef]
- Therrien, C.; Tooley, P.; Spielman, L.; Fry, W.; Ritch, D.; Shelly, S. Nuclear DNA content, allozyme phenotypes and metalaxyl sensitivity of Phytophthora infestans from Japan. Mycol. Res. 1993, 97, 945–950. [Google Scholar] [CrossRef]
- Flier, W.; Turkensteen, L. Foliar aggressiveness of Phytophthora infestans in three potato growing regions in the Netherlands. Eur. J. Plant Pathol. 1999, 105, 381–388. [Google Scholar] [CrossRef]
- Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef] [PubMed]
- Snedecor, G.; Cochran, W. Statistical Methods, 7th ed.; Iowa State University Press: Ames, IA, USA, 1980; p. 507. [Google Scholar]
- Kamvar, Z.N.; Tabima, J.F.; Grünwald, N.J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2014, 2, e281. [Google Scholar] [CrossRef] [Green Version]
- Stoddart, J.A.; Taylor, J.F. Genotypic diversity: Estimation and prediction in samples. Genetics 1988, 118, 705–711. [Google Scholar] [CrossRef]
- Nei, M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 1978, 89, 583–590. [Google Scholar] [CrossRef] [PubMed]
- Grünwald, N.J.; Goodwin, S.B.; Milgroom, M.G.; Fry, W.E. Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 2003, 93, 738–746. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nei, M.; Li, W.-H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA 1979, 76, 5269–5273. [Google Scholar] [CrossRef] [Green Version]
- Pritchard, J.K.; Stephens, M.; Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 2000, 155, 945–959. [Google Scholar] [CrossRef]
- Evanno, G.; Regnaut, S.; Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 2005, 14, 2611–2620. [Google Scholar] [CrossRef] [Green Version]
- Essa, T.A.; Kamel, S.M.; Ismail, A.M.; Omara, R.I. Partial resistance stability of some common potato cultivars to natural late blight infection caused by Phytophthora infestans under Egyptian conditions. Egypt. J. Phytopathol. 2018, 46, 227–242. [Google Scholar] [CrossRef]
- Arafa, R.A.; Soliman, N.E.K.; Moussa, O.M.; Kamel, S.M.; Shirasawa, K. Characterization of Egyptian Phytophthora infestans population using simple sequence repeat markers. J. Gen. Plant Pathol. 2018, 84, 104–107. [Google Scholar] [CrossRef]
- Sharma, S.; Lal, M. Advances in Management of Late Blight of Potato. In Sustainable Management of Potato Pests and Diseases; Chakrabarti, S.K., Sharma, S., Shah, M.A., Eds.; Springer: Singapore, 2022; pp. 163–184. [Google Scholar]
- Matson, M.E.H.; Small, I.M.; Fry, W.E.; Judelson, H.S. Metalaxyl Resistance in Phytophthora infestans: Assessing Role of RPA190 Gene and Diversity within Clonal Lineages. Phytopathology 2015, 105, 1594–1600. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matson, M.E.H.; Liang, Q.; Lonardi, S.; Judelson, H.S. Karyotype variation, spontaneous genome rearrangements affecting chemical insensitivity, and expression level polymorphisms in the plant pathogen Phytophthora infestans revealed using its first chromosome-scale assembly. PLoS Pathog. 2022, 18, e1010869. [Google Scholar] [CrossRef] [PubMed]
- Cooke, L.; Schepers, H.; Hermansen, A.; Bain, R.; Bradshaw, N.; Ritchie, F.; Shaw, D.; Evenhuis, A.; Kessel, G.; Wander, J. Epidemiology and integrated control of potato late blight in Europe. Potato Res. 2011, 54, 183–222. [Google Scholar] [CrossRef] [Green Version]
- Saville, A.C.; La Spada, F.; Faedda, R.; Migheli, Q.; Scanu, B.; Ermacora, P.; Gilardi, G.; Fedele, G.; Rossi, V.; Lenzi, N. Population structure of Phytophthora infestans collected on potato and tomato in Italy. Plant Pathol. 2021, 70, 2165–2178. [Google Scholar] [CrossRef]
- Lees, A.; Stewart, J.; Lynott, J.; Carnegie, S.; Campbell, H.; Roberts, A. The effect of a dominant Phytophthora infestans genotype (13_A2) in Great Britain on host resistance to foliar late blight in commercial potato cultivars. Potato Res. 2012, 55, 125–134. [Google Scholar] [CrossRef]
- Harbaoui, K.; van der Lee, T.; Vleeshouwers, V.G.; Khammassy, N.; Harrabi, M.; Hamada, W. Characterisation of Phytophthora infestans isolates collected from potato and tomato crops in Tunisia during 2006–2008. Potato Res. 2013, 56, 11–29. [Google Scholar] [CrossRef]
- Brylińska, M.; Sobkowiak, S.; Stefańczyk, E.; Śliwka, J. Potato cultivation system affects population structure of Phytophthora infestans. Fungal Ecol. 2016, 20, 132–143. [Google Scholar] [CrossRef]
- Yuen, J.; Andersson, B. What is the evidence for sexual reproduction of P hytophthora infestans in Europe? Plant Pathol. 2013, 62, 485–491. [Google Scholar] [CrossRef]
- Shaw, D.S.; Fyfe, A.; Hibberd, P.; Abdel-Sattar, M. Occurrence of the rare A2 mating type of Phytophthora infestans on imported Egyptian potatoes and the production of sexual progeny with A1 mating types from the UK. Plant Pathol. 1985, 34, 552–556. [Google Scholar] [CrossRef]
- Cooke, D.; Lees, A.; Shaw, D.; Taylor, M.; Prentice, M.; Bradshaw, N.; Bain, R. Survey of GB blight populations. PPO-Spec. Rep. 2007, 12, 145–151. [Google Scholar]
- Lees, A.; Cooke, D.; Stewart, J.; Sullivan, L.; Williams, N.; Carnegie, S. Phytophthora infestans population changes: Implications. PPO Spec. Rep. 2009, 13, 55. [Google Scholar]
- Cooke, D.E.L.; Lees, A.K.; Lassen, P.; Gronbech-Hansen, J.; Schepers, H.T.A.M. Making sense of Phytophthora infestans diversity at national and international scales. Environ. Sci. 2012, 15, 37–44. [Google Scholar]
- Chowdappa, P.; Kumar, N.B.; Madhura, S.; Kumar, M.S.; Myers, K.L.; Fry, W.E.; Squires, J.N.; Cooke, D.E. Emergence of 13_ A 2 blue lineage of Phytophthora infestans was Responsible for Severe Outbreaks of Late Blight on Tomato in South-West India. J. Phytopathol. 2013, 161, 49–58. [Google Scholar] [CrossRef]
- Li, Y.; Van der Lee, T.; Zhu, J.; Jin, G.; Lan, C.; Zhu, S.; Zhang, R.; Liu, B.; Zhao, Z.; Kessel, G. Population structure of P hytophthora infestans in China–geographic clusters and presence of the EU genotype Blue_13. Plant Pathol. 2013, 62, 932–942. [Google Scholar] [CrossRef]
- White, S.; Shaw, D. Resistance of Sarpo clones to the new strain of Phytophthora infestans, Blue-13. PPO-Spec. Rep. 2009, 13, 61–69. [Google Scholar]
- Haas, B.J.; Kamoun, S.; Zody, M.C.; Jiang, R.H.; Handsaker, R.E.; Cano, L.M.; Grabherr, M.; Kodira, C.D.; Raffaele, S.; Torto-Alalibo, T. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 2009, 461, 393–398. [Google Scholar] [CrossRef] [Green Version]
- Arafa, R.A.; Kamel, S.M.; Rakha, M.T.; Soliman, N.E.K.; Moussa, O.M.; Shirasawa, K. Analysis of the lineage of Phytophthora infestans isolates using mating type assay, traditional markers, and next generation sequencing technologies. PLoS ONE 2020, 15, e0221604. [Google Scholar] [CrossRef]
- Lacaze, A.; Sormany, F.; Judelson, H.; Joly, D.L. The expression of cytoplasmic effectors by Phytophthora infestans in potato leaves and tubers is organ-biased. In PhytoFrontiers™; APS Publications: Northwood Circle, MN, USA, 2022. [Google Scholar] [CrossRef]
- Gu, B.; Gao, W.; Liu, Z.; Shao, G.; Peng, Q.; Mu, Y.; Wang, Q.; Zhao, H.; Miao, J.; Liu, X. A single region of the Phytophthora infestans avirulence effector Avr3b functions in both cell death induction and plant immunity suppression. Mol. Plant Pathol. 2023. online ahead of print. [Google Scholar] [CrossRef]
- Vleeshouwers, V.G.; Rietman, H.; Krenek, P.; Champouret, N.; Young, C.; Oh, S.-K.; Wang, M.; Bouwmeester, K.; Vosman, B.; Visser, R.G. Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS ONE 2008, 3, e2875. [Google Scholar] [CrossRef]
SSR Locus | Allele Fragments | 1-D b | Hexp c | Evenness d |
---|---|---|---|---|
PiG11 | 6 | 0.7403 | 0.7419 | 0.8803 |
Pi02 | 4 | 0.6681 | 0.6696 | 0.9868 |
PinfSSR11 | 2 | 0.4998 | 0.5015 | 0.9996 |
D13 | 7 | 0.5467 | 0.5485 | 0.8023 |
PinfSSR8 | 2 | 0.5 | 0.5016 | 1 |
PinfSSR4 | 5 | 0.5501 | 0.5518 | 0.8347 |
Pi04 | 2 | 0.0131 | 0.0131 | 0.3278 |
Pi70 | 1 | . | . | |
PinfSSR6 | 2 | 0.0066 | 0.0066 | 0.2955 |
Pi63 | 2 | 0.5 | 0.5016 | 1 |
PinfSSR2 | 2 | 0.4998 | 0.5015 | 0.9996 |
Pi4B | 3 | 0.5096 | 0.5113 | 0.9459 |
Isolate Name | Host | Location | MLG | Genotype | GenBank Accession Numbers | |
---|---|---|---|---|---|---|
AVR2 | AVR2-like | |||||
EG_ 237 | Solanummelongena | Beheira | MLG_21 | 23_A1_19 | OQ107577 | OQ107598 |
EG_ 271 | S. tuberosum | Menofia | MLG_33 | 23_A1_12 | OQ107578 | OQ107592 |
EG_ 272 | S. tuberosum | Menofia | MLG_21 | 23_A1_19 | OQ107579 | OQ107594 |
EG_ 273 | S. tuberosum | Menofia | MLG_21 | 23_A1_19 | OQ107580 | OQ107591 |
EG_ 274 | S. tuberosum | Menofia | MLG_21 | 23_A1_19 | OQ107581 | OQ107593 |
EG_ 275 | S. tuberosum | Beheira | MLG_14 | 23_A1_21 | OQ107583 | OQ107595 |
EG_ 276 | S. tuberosum | Beheira | MLG_25 | 23_A1_43 | OQ107584 | OQ107596 |
EG_ 277 | S. tuberosum | Beheira | MLG_21 | 23_A1_19 | OQ107585 | OQ107588 |
EG_ 278 | S. tuberosum | Beheira | MLG_21 | 23_A1_19 | OQ107586 | OQ107589 |
EG_ 279 | S. lycopersicum | Kafr El Sheikh | MLG_21 | 23_A1_19 | OQ107582 | OQ107597 |
EG_ 280 | S. tuberosum | Beheira | MLG_25 | 23_A1_43 | OQ107587 | OQ107590 |
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El-Ganainy, S.M.; Ismail, A.M.; Soliman, M.S.; Ahmed, Y.; Sattar, M.N.; Chellappan, B.V.; Cooke, D.E.L. Population Dynamics of Phytophthora infestans in Egypt Reveals Clonal Dominance of 23_A1 and Displacement of 13_A2 Clonal Lineage. J. Fungi 2023, 9, 349. https://doi.org/10.3390/jof9030349
El-Ganainy SM, Ismail AM, Soliman MS, Ahmed Y, Sattar MN, Chellappan BV, Cooke DEL. Population Dynamics of Phytophthora infestans in Egypt Reveals Clonal Dominance of 23_A1 and Displacement of 13_A2 Clonal Lineage. Journal of Fungi. 2023; 9(3):349. https://doi.org/10.3390/jof9030349
Chicago/Turabian StyleEl-Ganainy, Sherif Mohamed, Ahmed Mahmoud Ismail, Maali Shaker Soliman, Yosra Ahmed, Muhammad Naeem Sattar, Biju Vadakkemukadiyil Chellappan, and David E. L. Cooke. 2023. "Population Dynamics of Phytophthora infestans in Egypt Reveals Clonal Dominance of 23_A1 and Displacement of 13_A2 Clonal Lineage" Journal of Fungi 9, no. 3: 349. https://doi.org/10.3390/jof9030349