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Predominant Clonal Reproduction with Infrequent Genetic Recombination of Phaeoacremonium minimum in Western Cape Vineyards

  • Fungal Microbiology
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Abstract

Phaeoacremonium minimum is an important esca and Petri disease pathogen that causes dieback of grapevines in South Africa. Little is known regarding the reproductive strategy of the pathogen. Sexual reproduction could lead to a better adaptation of the pathogen to disease management strategies by combining alleles through recombination. The study aimed to investigate the genetic diversity and recombination potential of eight populations in the Western Cape, from six commercial vineyards and two nursery rootstock mother blocks. This was achieved by developing and applying nine polymorphic microsatellites and mating-type-specific markers. Thirty-seven genotypes were identified from 295 isolates. Populations were characterised by the same dominant genotype (MLG20 occurring 65.43%), low genotypic diversity (H) and high numbers of clones (81.36% of dataset). However, genotypes from the same sampling sites were not closely related based on a minimum spanning network and had high molecular variation within populations (94%), suggesting that multiple introductions of different genotypes occurred over time. Significant linkage disequilibrium among loci (r̅d) further indicated a dominant asexual cycle, even though perithecia have been observed in these four populations. The two rootstock mother blocks had unique genotypes and genotypes shared with the vineyard populations. Propagation material obtained from infected rootstock mother blocks could lead to the spread of more genotypes to newly established vineyards. Based on our results, it is important to determine the health status of rootstock mother blocks. Management strategies must focus on reducing aerial inoculum to prevent repeated infections and further spread of P. minimum genotypes.

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Data availability

The nucleotide sequence data reported are available in the GenBank databases under the accession number(s) ON238013-ON238019; ON322913-ON322919. The datasets generated during and/or analysed during the current study are available in the supplementary material (Fig. S1-S5 and Tables S1-S7).

Code Availability

All codes used in this study are open source and available via the relevant references. No customs scripts were used.

References

  1. Scheck HJ, Vasquez SJ, Gubler WD (1998) First report of three Phaeoacremonium spp. causing young grapevine decline in California. Plant Dis 82:590. https://doi.org/10.1094/PDIS.1998.82.5.590C

    Article  CAS  PubMed  Google Scholar 

  2. Pascoe I, Cottral E (2000) Developments in grapevine trunk diseases research in Australia. Phytopathol Mediterr 39:e75. https://doi.org/10.14601/Phytopathol_Mediterr-1534

    Article  Google Scholar 

  3. Cloete M, Fischer M, Mostert L, Halleen F (2015) Hymenochaetales associated with esca-related wood rots on grapevine with a special emphasis on the status of esca in South African vineyards. Phytopathol Mediterr 54:299–312. https://doi.org/10.1007/s11557-013-0915-5

    Article  Google Scholar 

  4. Ravaz L (1898) Sur le folletage. Revue de Viticulture 10:184–186

    Google Scholar 

  5. Petri L (1912) Osservazioni sopra le alterazioni del legno della vite in seguito a ferite. Le Stazioni Sperimentali Agrarie Italiane 45:501–547

    Google Scholar 

  6. Gramaje D, Mostert L, Groenewald JZ, Crous PW (2015) Phaeoacremonium: from esca disease to phaeohyphomycosis. Fungal Biol 119:759–783. https://doi.org/10.1016/j.funbio.2015.06.004

    Article  PubMed  Google Scholar 

  7. Mostert L, Groenewald JZ, Summerbell RC, Gams W, Crous PW (2006) Taxonomy and pathology of Togninia (Diaporthales) and its Phaeoacremonium anamorphs. Stud Mycol 54:1–113. https://doi.org/10.3114/sim.54.1.1

    Article  Google Scholar 

  8. Mugnai L, Graniti A, Surico G (1999) Esca (black measles) and brown wood-streaking: two old and elusive diseases of grapevines. Plant Dis 83:404–416. https://doi.org/10.1094/PDIS.1999.83.5.404

    Article  CAS  PubMed  Google Scholar 

  9. Larignon P, Dubos B (1997) Fungi associated with esca disease in grapevine. Eur J Plant Pathol 103:e157. https://doi.org/10.1023/A:1008638409410

    Article  Google Scholar 

  10. Ferreira JHS, van Wyk PS, Venter E (1994) Slow dieback of grapevine: association of Phialophoraparasitica with slow dieback of grapevines. S Afr J Enol Vitic 15:9–11. https://doi.org/10.21548/15-1-2276

    Article  Google Scholar 

  11. White C, Halleen F, Mostert L (2011) Symptoms and fungi associated with esca in South African vineyards. Phytopathol Mediterr 50:236–246. https://doi.org/10.14601/PHYTOPATHOL_MEDITERR-8982

    Article  Google Scholar 

  12. Spies CFJ, Moyo P, Halleen F, Mostert L (2018) Phaeoacremonium species diversity on woody hosts in the Western Cape Province of South Africa. Persoonia 40:26–62. https://doi.org/10.3767/persoonia.2018.40.02

    Article  CAS  PubMed  Google Scholar 

  13. Eskalen A, Feliciano AJ, Gubler WD (2007) Susceptibility of grapevine pruning wounds and symptom development in response to infection by Phaeoacremonium aleophilum and Phaeomoniella chlamydospora. Plant Dis 91:1100–1104. https://doi.org/10.1094/PDIS-91-9-1100

    Article  CAS  PubMed  Google Scholar 

  14. Baloyi MA, Halleen F, Mostert L, Eskalen A (2013) First report of Togninia minima perithecia on Esca and Petri-diseased grapevines in South Africa. Disease Notes 97:1247. https://doi.org/10.1094/PDIS-10-12-0963-PDN

    Article  CAS  Google Scholar 

  15. Rooney-Latham S, Eskalen A, Gubler WD (2005) Occurence of Togninia minima perithecia in esca affected vineyards in California. Plant Dis 89:867–871. https://doi.org/10.1094/PD-89-0867

    Article  CAS  PubMed  Google Scholar 

  16. Mostert L, Crous PW, Groenewald JZ, Gams W, Summerbell RC (2003) Togninia (Calosphaeriales) is confirmed as teleomorph of Phaeoacremonium by means of morphology, sexual compatibility and DNA phylogeny. Mycologia 95:646–649. https://doi.org/10.1080/15572536.2004.11833069

    Article  PubMed  Google Scholar 

  17. Rooney-Latham S, Eskalen A, Gubler WD (2005) Teleomorph formation of Phaeoacremonium aleophilum, cause of esca and grapevine decline in California. Plant Dis 87:177–184. https://doi.org/10.1094/PD-89-0177

    Article  Google Scholar 

  18. Pascoe IG, Edwards J, Cunnington JH, Cottral E (2004) Detection of the Togninia teleomorph of Phaeoacremonium aleophilum in Australia. Phytopathol Mediterr 43:51–58. https://doi.org/10.1400/14571

    Article  Google Scholar 

  19. Baloyi MA (2016) Occurence of fruiting bodies of Petri disease pathogens in South African vineyards and in vitro induction of Phaeoacremonium sexual morphs. Chapter 3Inoculum ecology of Petri disease fungi in grapevines of South Africa, PhD thesis. Stellenbosch University, Stellenbosch, South Africa

  20. Halleen F, Baloyi MA, Bester MC, Mostert L (2020) Aerial inoculum patterns of Petri disease pathogens in South African vineyards and rootstock mother blocks. Phytopathol Mediterr 59:515–536. https://doi.org/10.14601/Phyto-11370

    Article  Google Scholar 

  21. Eskalen A, Gubler WD (2001) Association of spores of Phaeomoniellachlamydospora, Phaeoacremoniuminflatipes and Phaeoacremoniumaleophilum with grapevine cordons in California. Phytopathol Mediterr 40:S429–S432. https://doi.org/10.14601/Phytopathol_Mediterr-1613

    Article  Google Scholar 

  22. Ni M, Feretzaki M, Sun S, Wang X, Heitman J (2011) Sex in fungi. Annu Rev Genet 45:405. https://doi.org/10.1146/annurev-enet-110410-132536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Damm U, Mostert L, Crous PW, Fourie PH (2008) Novel Phaeoacremonium species associated with necrotic wood of Prunus trees. Persoonia 20:87–102. https://doi.org/10.3767/003158508X324227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Blanco-Ulate B, Rolshaussen P, Cantu D (2013) Draft genome sequence of the Ascomycete Phaeoacremonium aleophilum strain UCR-PA7, a causal agent of the esca disease complex in grapevines. Genome Announc 1:e00390-e313. https://doi.org/10.1128/genomeA.00390-13

    Article  PubMed  PubMed Central  Google Scholar 

  25. Du L, Li Y, Zhang X, Yue B (2013) MSDB: a user-friendly program for reporting distribution and building databases of microsatellites from genome sequences. J Hered 104:154–157. https://doi.org/10.1093/jhered/ess082

    Article  PubMed  Google Scholar 

  26. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols in the series methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  27. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590. https://doi.org/10.1093/genetics/89.3.583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Pielou EC (1975) Ecological diversity. Wiley, New York, p 165

    Google Scholar 

  29. Arzanlou M, Narmani A (2014) Multiplex PCR for specific identification and determination of mating type in Togninia minima (anamorph Phaeoacremoniumaleophilum), a causal agent of esca disease of grapevine. Phytopathol Mediterr 53:240–249. https://doi.org/10.14601/Phytopathol_Mediterr-12899

    Article  CAS  Google Scholar 

  30. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  31. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinform 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129

    Article  CAS  Google Scholar 

  32. 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:e281. https://doi.org/10.7717/peerj.281

    Article  PubMed  PubMed Central  Google Scholar 

  33. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: URL http://www.R-project.org/

  34. Grünwald NJ, Goodwin SB, Milgroom MG, Fry WE (2003) Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 93:738–746. https://doi.org/10.1094/PHYTO.2003.93.6.738

    Article  PubMed  Google Scholar 

  35. Simpson EH (1949) Measurement of diversity. Nature 163:688. https://doi.org/10.1038/163688a0

    Article  Google Scholar 

  36. Shannon CE (2001) A mathematical theory of communication. Mob Comput Commun Rev 5:3–55

    Article  Google Scholar 

  37. Brown AHD, Feldman MW, Nevo E (1980) Multilocus structure of natural populations of Hordeum spontaneum. Genetics 96:523–536. https://doi.org/10.1093/genetics/96.2.523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Agapow PM, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1:101–102. https://doi.org/10.1046/j.1471-8278.2000.00014.x

    Article  CAS  Google Scholar 

  39. Stenberg P, Lundmark M, Saura A (2003) MLGsim: a program for detecting clones using a simulation approach. Mol Ecol Resour 3:329–331. https://doi.org/10.1046/j.1471-8286.2003.00408.x

    Article  CAS  Google Scholar 

  40. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B 57:289–300. https://doi.org/10.2307/2346101

    Article  Google Scholar 

  41. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491. https://doi.org/10.1093/genetics/131.2.479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Hendrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638. https://doi.org/10.1111/j.0014-3820.2005.tb01814.x

    Article  Google Scholar 

  43. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587. https://doi.org/10.1093/genetics/164.4.1567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 5:1179–1191. https://doi.org/10.1111/1755-0998.12387

    Article  CAS  Google Scholar 

  45. Bruvo R, Michiels NK, D’Souza TG, Schulenburg H (2004) A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol Ecol 13:2101–2106. https://doi.org/10.1111/j.1365-294X.2004.02209.x

    Article  CAS  PubMed  Google Scholar 

  46. Moyo P, Allsopp E, Roets F, Mostert L, Halleen F (2014) Arthropods vector grapevine trunk disease pathogens. Phytopathol 104:1063–1069. https://doi.org/10.1094/PHYTO-11-13-0303-R

    Article  CAS  Google Scholar 

  47. Drenth A, McTaggart AR, Wingfield BD (2019) Fungal clones win the battle, but recombination wins the war. IMA Fungus 10:18. https://doi.org/10.1186/s43008-019-0020-8

    Article  PubMed  PubMed Central  Google Scholar 

  48. Borie B, Jacquiot L, Jamaux-Despréaux I, Larignon P, Péros J-P (2002) Genetic diversity in populations of the fungi Phaeomoniella chlamydospora and Phaeoacremonium aleophilum on grapevine in France. Plant Pathol 51:85–96. https://doi.org/10.1046/j.0032-0862.2001.658.x

    Article  Google Scholar 

  49. Péros JP, Jamaux-Despréaux I, Berger G (2000) Population genetics of fungi associated with esca disease in French vineyards. Phytopathol Mediterr 39:150–155. https://doi.org/10.14601/Phytopathol_Mediterr-1553

    Article  Google Scholar 

  50. Tegli S, Santilli E, Bertelli E, Surico G (2000) Genetic variation within Phaeoacremonium aleophilum and P chlamydosporum in Italy. Phytopathol Mediterr 39:125–133. https://doi.org/10.14601/Phytopathol_Mediterr-1540

    Article  CAS  Google Scholar 

  51. Gramaje D, Armengol J, Ridgway H (2013) Genetic and virulence diversity, and mating type distribution of Togninia minima causing grapevine trunk diseases in Spain. Eur J Plant Pathol 135:727–743. https://doi.org/10.1007/s10658-012-0110-6

    Article  Google Scholar 

  52. Martín L, de Miera LES, Martín MT (2014) Characterization of Phaeoacremonium aleophilum associated with Vitis vinifera decline in Spain. J Phytopathol 162:245–257. https://doi.org/10.1111/jph.12180

    Article  CAS  Google Scholar 

  53. Fourie PH, Halleen F (2004) Proactive control of Petri disease of grapevine through treatment of propagation material. Plant Dis 88:1241–1245. https://doi.org/10.1094/PDIS.2004.88.11.1241

    Article  PubMed  Google Scholar 

  54. Retief E, Damm U, van Niekerk JM, McLeod A, Fourie PH (2005) A protocol for molecular detection of Phaeomoniella chlamydospora in grapevine wood. S Afr J Sci 101:139–142

    CAS  Google Scholar 

  55. Halleen F, Crous PW, Petrini O (2003) Fungi associated with healthy grapevine cuttings in nurseries, with special reference to pathogens involved in the decline of young vines. Australas Plant Pathol 32:47–52. https://doi.org/10.1071/AP02062

    Article  Google Scholar 

  56. Nieuwenhuis BP, James TY (2016) The frequency of sex in fungi. Philos Trans Royal Soc 371:1–12. https://doi.org/10.1098/rstb.2015.0540

    Article  CAS  Google Scholar 

  57. Bertelli E, Mugnai L, Surico G (1998) Presence of Phaeoacremonium chlamydosporum in apparently healthy rooted grapevine cuttings. Phytopathol Mediterr 37:79–82

    Google Scholar 

  58. Billiard S, Lopez-Villavicencio M, Hood ME, Giraud T (2012) Sex, outcrossing and mating types: unsolved questions in fungi and beyond. J Evol Biol 25:1020–1038. https://doi.org/10.1111/j.1420-9101.2012.02495.x

    Article  CAS  PubMed  Google Scholar 

  59. Cottral E, Ridgway H, Pascoe I, Edwards J, Taylor P (2001) UP-PCR analysis of Australian isolates of Phaeomoniella chlamydospora and Phaeoacremonium aleophilum. Phytopathol Mediterr 40:S479–S486

    Google Scholar 

  60. Narmani A, Arzanlou M, Babai-Ahari A (2016) Uneven distribution of mating-type alleles among Togninia minima isolates, one of the causal agents of leaf stripe disease on grapevines in Northwest Iran. J Phytopathol 164:441–447

    Article  CAS  Google Scholar 

  61. Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9. https://doi.org/10.1016/0027-5107(64)90047-8

    Article  Google Scholar 

  62. Gramaje D, Úrbez-Torres JR, Sosnowski MR (2018) Managing grapevine trunk diseases with respect to etiology and epidemiology: current strategies and future prospects. Plant Dis 102:12–39. https://doi.org/10.1094/PDIS-04-17-0512-FE

    Article  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Carine Vermeulen, Julia Marais, Danie Marais, Abraham Vermeulen, Palesa Lebenya, Bongiwe Sokwaliwa, Levocia Williams, Lydia Maart and Muriel Knipe at Plant Protection Division, ARC Infruitec- Nietvoorbij for their technical assistance. ARC for infrastructure and resources.

Funding

This work benefitted from the financial support of The National Research Foundation, Winetech (Project WW 06/41), THRIP (Project ID: TP2009072900007) and Agricultural Research Council (ARC) Infruitec-Nietvoorbij.

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Authors and Affiliations

  1. Plant Protection Division, ARC Infruitec-Nietvoorbji, The Fruit, Vine and Wine Institute of the Agricultural Research Council, Private Bag X5026, Stellenbosch, 7599, South Africa

    Minette Havenga, Francois Halleen, Annabella Baloyi & Michael Bester

  2. Department of Plant Pathology, University of Stellenbosch, Private Bag X1 Matieland, Stellenbosch, 7602, South Africa

    Francois Halleen, Annabella Baloyi, Michael Bester & Lizel Mostert

  3. Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT, 2601, Australia

    Celeste C. Linde

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  1. Minette Havenga
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  2. Francois Halleen
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  3. Annabella Baloyi
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  4. Michael Bester
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  5. Celeste C. Linde
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  6. Lizel Mostert
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Contributions

All authors contributed to the study conception and design. Material preparation was performed by Annabella Baloyi and Francois Halleen, data collection and analysis were performed by Minette Havenga, Michael Bester and Celeste Linde. Funding acquisition, resources and supervision were performed by Lizel Mostert and Francois Halleen. The first draft of the manuscript was written by Minette Havenga and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Lizel Mostert.

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Havenga, M., Halleen, F., Baloyi, A. et al. Predominant Clonal Reproduction with Infrequent Genetic Recombination of Phaeoacremonium minimum in Western Cape Vineyards. Microb Ecol 86, 887–899 (2023). https://doi.org/10.1007/s00248-022-02142-1

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