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Population structure of Venturia inaequalis, a hemibiotrophic fungus, under different host resistance specificities in the Kashmir valley

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Abstract

Venturia inaequalis is a notorious fungal pathogen and show classical gene for gene interaction with its apple host. Neutral markers provide clues about history, evolutionary potential, genetic diversity and population structure of V. inaequalis. The genetic diversity and population structure of fungus indicates that the pathogen is highly diverse with the capacity to breach the scab resistance genes. In the present study, we collected 108 V. inaequalis isolates from three apple cultivars differing in Rvi1 resistance gene. Based on the AMOVA, the variation was mostly distributed among the isolates, providing evidence of non-existence of subpopulation in orchards thus founder population is difficult to arise in Kashmir apple orchards. Pair wise genetic differentiation is less due to regular occurrence of gene flow between the populations residing on different orchard as infected material is transported without stringent quarantine measures. Based on principal coordinate analysis and clustering algorithm as implemented in STRUCTURE, we observed admixture between the two subpopulations, which is quite low, suggesting the existence of pre-zygotic and post-zygotic barriers to gene flow and we cannot rule out the existence of other structures shared by accessions belonging to different varieties. Due to the continuous increase in introduction and monoculture of apple varieties, mixed orchard with different host resistance specificities are more suitable for managing the apple scab in Kashmir valley.

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References

  • Agapow PM, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1:101–102

    CAS  Google Scholar 

  • Alaniz S, Leoni C, Bentancur O, Mondino P (2014) Elimination of summer fungicide sprays for apple scab (Venturia inaequalis) management in Uruguay. Sci Hort 165:331–335. https://doi.org/10.1016/j.scienta.2013.11.016

    Article  CAS  Google Scholar 

  • Barbara DJ, Roberts AL, Xu X (2008) Virulence characteristics of apple scab (Venturia inaequalis ) isolates from monoculture and mixed orchards. Plant Pathol 57:552–561

    Google Scholar 

  • Benaouf G, Parisi L (2000) Genetics of host-pathogen relationships between Venturia inaequalis races 6 and 7 Malus Species. Phytopatholgy 90:236–242

    CAS  Google Scholar 

  • Blazek J, Krelinova J, Blazkova J (2003) Results of a trial with 17 chosen apple cultivars bred in the Czech Republic that was evaluated 1996–2002 at Holovousy. Vedecke Prace Ovocnarske 18:7–23

    Google Scholar 

  • Bowen JK, Mesarich CH, Bus VGM, Beresford RM, Plummer KM, Templeton MD (2011) Venturia inaequalis: the causal agent of apple scab. Mol Plant Pathol 12:105–122

    PubMed  Google Scholar 

  • Brown A, Feldman M, Nevo E (1980) Multilocus structure of natural populations of Hordeum spontaneum. Genetics 96:523–536

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bus VG, Rikkerink EH, Caffier V, Durel CE, Plummer KM (2011) Revision of the nomenclature of the differential host-pathogen interactions of Venturia inaequalis and Malus. Annu Rev Phytopathol 49:391–413. https://doi.org/10.1146/annurev-phyto-072910-095339

    Article  CAS  PubMed  Google Scholar 

  • Dar M et al (2015) Distribution of apple scab race flora and identification of resistant sources against Venturia inaequalis in Kashmir. Plant Pathol J 14:196

    CAS  Google Scholar 

  • Decognet V, Bardin M, Trottin-Caudal Y, Nicot P (2009) Rapid change in the genetic diversity of Botrytis cinerea populations after the introduction of strains in a tomato glasshouse. Phytopathology 99:185–193

    CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    PubMed  Google Scholar 

  • Fiaccadori R, Cicognani E, Alberoni G, Collina M, Brunelli A (2011) Sensitivity to strobilurin fungicides of Italian Venturia inaequalis populations with different origin and scab control. Pest Manage Sci 67:535–540

    CAS  Google Scholar 

  • Gavrilets S (2004) Fitness landscapes and the origin of species (MPB-41). Princeton University Press, New jersery

    Google Scholar 

  • Gavrilets S, Losos JB (2009) Adaptive radiation: contrasting theory with data. Science 323:732–737

    CAS  PubMed  Google Scholar 

  • Geiser DM, Pitt JI, Taylor JW (1998) Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus. Proc Natl Acad Sci 95:388–393

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giraud T, Gladieux P, Gavrilets S (2010) Linking the emergence of fungal plant diseases with ecological speciation trends. Ecol Evol 25:387–395

    Google Scholar 

  • Gladieux P, Zhang XG, Afoufa-Bastien D, Valdebenito Sanhueza RM, Sbaghi M, Le Cam B (2008) On the origin and spread of the Scab disease of apple: out of central Asia. PLoS ONE 3:14–55. https://doi.org/10.1371/journal.pone.0001455

    Article  CAS  Google Scholar 

  • Gladieux P et al (2010) Evolution of the population structure of Venturia inaequalis, the apple scab fungus, associated with the domestication of its host. Mol Ecol 19:658–674

    PubMed  Google Scholar 

  • Gladieux P et al (2011) Emergence of novel fungal pathogens by ecological speciation: importance of the reduced viability of immigrants. Mol Ecol 20:4521–4532

    PubMed  Google Scholar 

  • Guerin F, le Cam B (2004) Breakdown of the scab resistance gene Vf in apple leads to a founder effect in populations of the fungal pathogen Venturia inaequalis. Phytopathology 94:364–369

    CAS  PubMed  Google Scholar 

  • Guerin F, Franck P, Loiseau A, Devaux M, Le Cam B (2004) Isolation of 21 new polymorphic microsatellite loci in the phytopathogenic fungus Venturia inaequalis. Mol Ecol Notes 4:268–270. https://doi.org/10.1111/j.1471-8286.2004.00637.x

    Article  CAS  Google Scholar 

  • Guerin F, Gladieux P, Le Cam B (2007) Origin and colonization history of newly virulent strains of the phytopathogenic fungus Venturia inaequalis Fungal. Genet Biol 44:284–292. https://doi.org/10.1016/j.fgb.2006.10.005

    Article  CAS  Google Scholar 

  • Gupta G (1990) Apple scab-a review Indian. J Plant Prot 18:157–165

    Google Scholar 

  • Joshi NC, Malik AG, Kaul MH, Anand SK (1973) Some observations on the epidemic of scab disease of apple in Jammu and Kashmir during 1973. Indian Phytopath 28:288–289

    Google Scholar 

  • Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:281

    Google Scholar 

  • Koller W, Wilcox WF (2001) Evidence for the predisposition of fungicide-resistant isolates of Venturia inaequalis to a preferential selection for resistance to other fungicides. Phytopathology 91:776–781

    CAS  PubMed  Google Scholar 

  • Leroy T, Lemaire C, Dunemann F, Le Cam B (2013) The genetic structure of a Venturia inaequalis population in a heterogeneous host population composed of different Malus species. BMC Evol Biol 13:64

    PubMed  PubMed Central  Google Scholar 

  • Matsuoka Y, Mitchell S, Kresovich S, Goodman M, Doebley J (2002) Microsatellites in Zea–variability, patterns of mutations, and use for evolutionary studies. Theor Appl Genet 104:436–450

    CAS  PubMed  Google Scholar 

  • Matute DR et al (2006) Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Mol Biol Evol 23:65–73

    CAS  PubMed  Google Scholar 

  • Maynard-Smith J, Smith NH, O’Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci 90:4384–4388

    Google Scholar 

  • Montarry J, Cartolaro P, Delmotte F, Jolivet J, Willocquet L (2008) Genetic structure and aggressiveness of Erysiphe necator populations during grapevine powdery mildew epidemics. Appl Environ Microbiol 74:6327–6332

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nath P (1935) Studies in the diseases of apples in Northern India II. A short note on apple scab due to Fusicladium dendritium. J Indian Botanical Soc 14:121–124

    Google Scholar 

  • Nosil P, Vines TH, Funk DJ (2005) Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719

    PubMed  Google Scholar 

  • Padder BA, Shah MD, Ahmad M, Sofi TA, Ahanger FA, Hamid A (2011) Genetic differentiation amoung populations of Venturia inaequalis in Kashmir: a North-Western state of India Asian. J Plant Pathol 5:75–83

    Google Scholar 

  • Padder BA, Sofi TA, Mushtaq A, Shah MD, Aflaq H, Sehar S, Ahanger FA (2013) Virulence and molecular diversity of Venturia inaequalis in commercial apple growing regions in Kashmir. J Phytopathol 161:271–279

    CAS  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perseguini JMKC et al (2011) Genetic diversity in cultivated carioca common beans based on molecular marker analysis. Genet Mol Biol 34:88–102

    CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual. Springer, Londen

    Google Scholar 

  • Shulaev V et al (2008) Multiple models for rosaceae genomics. Plant Physiol Biochem 147:985–1003

    CAS  Google Scholar 

  • Taylor J, Jacobson D, Fisher M (1999) The evolution of asexual fungi: reproduction, speciation and classification. Annu Rev Phytopathol 37:197–246

    CAS  PubMed  Google Scholar 

  • Tenzer I, Gessler C (1997) Subdivision and genetic structure of four populations of Venturia inaequalis in Switzerland. Eur J Plant Pathol 103:565–571

    Google Scholar 

  • Tenzer I, Gessler C (1999) Genetic diversity of Venturia inaequalis across Europe. Eur J Plant Pathol 105:515–522

    Google Scholar 

  • Tenzer I, Ivanissevich SD, Morgante M, Gessler C (1999) Identification of microsatellite markers and their application to population genetics of Venturia inaequalis. Phytopatholgy 89:748–753

    CAS  Google Scholar 

  • Thakur VS, Gupta CK, Garg ID (1992) Effect of post-infection application of fungicides on the apple scab pathogen, Venturia inaequalis (Cke). Wint J Phytopathol 135:160–166

    CAS  Google Scholar 

  • Xu X, Yang J, Thakur V, Roberts A, Barbara DJ (2008) Population variation of apple scab (Venturia inaequalis) isolates from Asia and Europe. Plant Dis 92:247–252. https://doi.org/10.1094/pdis-92-2-0247

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Harvey N, Roberts A, Barbara D (2012) Population variation of apple scab (Venturia inaequalis) within mixed orchards in the UK. Eur J Plant Pathol 135:97–104. https://doi.org/10.1007/s10658-012-0068-4

    Article  Google Scholar 

  • Zhan J, Mundt CC, Hoffer M, McDonald BA (2002) Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem. J Evol Biol 15:634–647

    Google Scholar 

Download references

Acknowledgements

The research was partially funded by Department of Biotechnology, Government of India, New Delhi (Grant No: BT/PR17344/AGII/106/1005/2016) to the corresponding author.

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Correspondence to Bilal A. Padder.

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Communicated by Erko Stackebrandt.

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Dar, M.S., Padder, B.A., Ahmad, M. et al. Population structure of Venturia inaequalis, a hemibiotrophic fungus, under different host resistance specificities in the Kashmir valley. Arch Microbiol 202, 2245–2253 (2020). https://doi.org/10.1007/s00203-020-01950-8

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