New Phytophthora species in clade 2a from the Asia-Pacific region including a re-examination of P. colocasiae and P. meadii

Abstract

Five new taxa from Phytophthora ITS clade 2a are described from Cinnamomum cassia plantations and adjacent waterways in Van Yen, Vietnam, disturbed rainforest in the Hela Province of Papua New Guinea and from disturbed forest on Christmas Island. Phylogenetic analyses were performed using data from nuclear regions (ITS, β-tubulin; heat shock protein 90) and mitochondrial regions (cytochrome c oxidase subunit 1; cytochrome c oxidase subunit 2; NADH dehydrogenase subunit 1; ribosomal protein L10). The molecular data supported recognition of three species: Phytophthora insulinativitatica, P. multibullata and P. x vanyenensis, and two informal taxa: P. sp. germisporangia and P. sp. awatangi. P. x vanyenensis appears to be a hybrid between P. mekongensis and an unknown species. P. multibullata and P. sp. germisporangia are phylogenetically close to P. citrophthora, but morphologically distinct. P. insulinativitatica is most closely related to P. botryosa, but has distinct morphology. P. sp. germisporangia and P. sp. awatangi were morphologically distinct and separated in the phylogeny based on mitochondrial sequences, but their nuclear sequences were identical. When comparing the sequences of these new species to that available on GenBank, it became evident that some of these species shared similarity with isolates submitted to GenBank under other species names. A re-evaluation of all P. meadii and P. colocasiae ITS sequence data identified an additional 7 putatively new species all isolated from Asia. The results support the view that many more Phytophthora species remain to be discovered in the Asia-Pacific region.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Data availability

All new sequences have been uploaded to GenBank. All sequence alignments are available from Dryad (https://doi.org/10.5061/dryad.02v6wwq22). Type cultures have been submitted to CBS (WesterDijk Fungal Biodiversity Institute, Utrecht, The Netherlands). Species names have been submitted to MycoBank.

References

  1. Abad ZG, Burgess TI, Bienapfl JC, Redford AJ, Coffey M, & Knight L (2019) IDphy: molecular and morphological identification of Phytophthora based on the types. USDA APHIS PPQ S&T Beltsville Lab, USDA APHIS PPQ S&T ITP, Centre for Phytophthora Science and Management, and World Phytophthora Collection. Retrieved from https://idtools.org/id/phytophthora/index.php

  2. Brasier CM, Kirk SA, Delcan J, Cooke DEL, Jung T, Man in’t Veld WA (2004) Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycol Res 108:1172–1184

    CAS  Article  Google Scholar 

  3. Burgess TI (2015) Molecular characterization of natural hybrids formed between five related indigenous clade 6 Phytophthora species. PLoS One 10:e0134225

    Article  Google Scholar 

  4. Cacciola SO, La Spada F, Hoa NV, Jung MH, Scanu B (2017) Phytophthora mekongensis Cacciola & N.V. Hoa, sp. nov. Fungal Planet description sheet: 615. Persoonia 38:363

  5. Chee KH (1969) Leaf fall due to Phytophthora botryosa. Planters’ Bulletin Rubber Research Institute of Malaya 104:190–198

    Google Scholar 

  6. Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related Oomycetes. Fungal Genet Biol 30:17–32

    CAS  Article  Google Scholar 

  7. Dick MW (1990) Keys to Pythium. University of Reading Press, Reading

    Google Scholar 

  8. Érsek T, English JT, Schoelz JE (1995) Creation of species hybrids of Phytophthora with modified host ranges by zoospore fusion. Phytopathology 85:1343–1347

    Article  Google Scholar 

  9. Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. APS Press, St. Paul

    Google Scholar 

  10. Goodwin SB, Fry WE (1994) Genetic analyses of interspecific hybrids between Phytophthora infestans and Phytophthora mirabilis. Experimental Mycol 18:20–32

    Article  Google Scholar 

  11. Hansen EM, Reeser PW, Sutton W (2012) Phytophthora beyond agriculture. Annu Rev Phytopathol 50:359–378

    CAS  Article  Google Scholar 

  12. Hüberli D, Tommerup IC, Hardy GES (2000) False-negative isolations or absence of lesions may cause mis-diagnosis of diseased plants infected with Phytophthora cinnamomi. Aust Plant Pathol 29:164–169

    Article  Google Scholar 

  13. Jafari F, Mostowfizadeh-Ghalamfarsa R, Safaiefarahani B, Burgess TI (2020) Potential host range of four Phytophthora interspecific hybrids from Clade 8a. Plant Pathol 69:1281–1290. https://doi.org/10.1111/ppa.13205

    Article  Google Scholar 

  14. Jung T, Chang TT, Bakonyi J, Seress D, Pérez-Sierra A, Yang X, Hong C, Scanu B et al (2016) Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathol 66:194–211

    Article  Google Scholar 

  15. Jung T, Horta-Jung M, Cacciola SO, Cech T, Bakonyi J, Seress D, Mosca S, Schena L et al (2017a) Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA Fungus 8:219–244

    Article  Google Scholar 

  16. Jung T, Horta-Jung M, Scanu B, Seress D, Kovács GM, Maia C, Pérez-Sierra A, Chang T et al (2017b) Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia 38:100–135

    CAS  Article  Google Scholar 

  17. Jung T, Durán A, Sanfuentes von Stowasser E, Schena L, Mosca S, Fajardo S, González M, Navarro Ortega AD et al (2018) Diversity of Phytophthora species in Valdivian rainforests and association with severe dieback symptoms. Forest Pathol 48:e12443

    Article  Google Scholar 

  18. Jung T, Scanu B, Brasier CM, Webber J, Milenković I, Corcobado T, Tomšovský M, Pánek M et al (2020) A survey in natural forest ecosystems of Vietnam reveals high diversity of both new and described Phytophthora taxa including P. ramorum. Forests 11:93

    Article  Google Scholar 

  19. Leonian LH (1925) Physiological studies on the genus Phytophthora. Am J Bot 12:444–498

    Article  Google Scholar 

  20. Lin MJ, Ko WH (2008) Occurrence of isolates of Phytophthora colocasiae in Taiwan with homothallic behavior and its significance. Mycol 100:727–734

    CAS  Article  Google Scholar 

  21. Man in’t Veld WA, de Cock AWAM, Summerbell RC (2007) Natural hybrids of resident and introduced Phytophthora species proliferating on multiple new hosts. Eur J Plant Pathol 117:25–33

    Article  Google Scholar 

  22. Man in’t Veld WA, Rosendahl KCHM, Hong C (2012) Phytophthora x serendipita sp. nov. and P. x pelgrandis, two destructive pathogens generated by natural hybridization. Mycol 104:1390–1396

    Article  Google Scholar 

  23. Man in’t Veld WA, Rosendahl KCHM, van Rijswick PCJ, Meffert JP, Westenberg M, van de Vossenberg BTLH, Denton G, van Kuik FAJ (2015) Phytophthora terminalis sp. nov. and Phytophthora occultans sp. nov., two invasive pathogens of ornamental plants in Europe. Mycol 107:54–65

    Article  Google Scholar 

  24. McRae W (1918) Phytophthora meadii n. sp, on Hevea brasiliensis. Memoirs of the Department of Agriculture in India. Botanical Series 9:219–273

    Google Scholar 

  25. Oh E, Gryzenhout M, Wingfield BD, Wingfield MJ, Burgess TI (2013) Surveys of soil and water reveal a goldmine of Phytophthora diversity in South African natural ecosystems. IMA Fungus 4:123–131

    Article  Google Scholar 

  26. Park B, Martin F, Geiser DM, Kim H-S, Mansfield MA, Nikolaeva E, Park S-Y, Coffey MD et al (2013) Phytophthora database 2.0: update and future direction. Phytopathol 103:1204–1208

    Article  Google Scholar 

  27. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    CAS  Article  Google Scholar 

  28. Puglisi I, De Patrizio A, Schena L, Jung T, Evoli M, Pane A, Van Hoa N, Van Tri M et al (2017) Two previously unknown Phytophthora species associated with brown rot of Pomelo (Citrus grandis) fruits in Vietnam. PloS One 12:e0172085

    Article  Google Scholar 

  29. Raciborski M (1900) Parasitic algae and fungi, Java. Batavia Bulletin of the New York State Museum 19:189

    Google Scholar 

  30. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L et al (2011) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  Google Scholar 

  31. Safaiefarahani B, Mostowfizadeh-Ghalamfarsa R, Hardy GES, Burgess TI (2016) Species from within the Phytophthora cryptogea complex and related species, P. erythroseptica and P. sansomeana, readily hybridize. Fungal Biol 120:975–987

    CAS  Article  Google Scholar 

  32. Sakalidis ML, Ray JD, Lanoiselet V, Hardy GES, Burgess TI (2011) Pathogenic Botryosphaeriaceae associated with Mangifera indica in the Kimberley Region of Western Australia. Eur J Plant Pathol 130:379–391. https://doi.org/10.1007/s10658-011-9760-z

    Article  Google Scholar 

  33. Sarker SR, McComb JA, Burgess TI, Hardy GES (2020) Antimicrobials in Phytophthora isolation media and the growth of Phytophthora species. Plant Pathol 69:1426–1436. https://doi.org/10.1111/ppa.13224

    CAS  Article  Google Scholar 

  34. Scott P, Bader M, Burgess TI, Hardy GESJ, Williams N (2019) Global biogeography and invasion risk of the plant destroyer genus Phytophthora. Environ Sci Pol 101:175–182. https://doi.org/10.1016/j.envsci.2019.08.020

    Article  Google Scholar 

  35. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    CAS  Article  Google Scholar 

  36. Vettraino A-M, Brasier CM, Brown AV, Vannini A (2011) Phytophthora himalsilva sp. nov. an unusually phenotypically variable species from a remote forest in Nepal. Fungal Biol 115:275–287

    Article  Google Scholar 

  37. Waterhouse GM (1963) Key to the species of Phytophthora de Bary. Mycology Paper no. 92. vol 92. Mycology Paper. CMI Kew, UK

  38. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innes MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

Download references

Acknowledgements

The senior author received a joint PhD scholarship between the Vietnam Government and Murdoch University. The authors would like to thank Prof. Alex George for helping with Latin names and Emeritus Prof. Jen McComb for editing and giving valuable suggestions. Prof. Chuanexue Hong kindly provided additional information on isolate 46C3. The staff from the Forest Protection Research Centre of Vietnam Academy of Forest Sciences helped with the collection of data. Diane White provided much appreciated molecular technical support.

Funding

Provided by Murdoch University as part of PhD student operational funds and by the Forest Protection Research Centre of Vietnam Academy of Forest Sciences.

Author information

Affiliations

Authors

Contributions

Conceptualization: T.B., G.H., T.P. F. A., and Q.D.; methodology: Q.D. and T.B; validation: T.B. and Q.D.; formal analysis: T.B. and Q.D.; investigation: Q.D. and F.A.; resources: G.H., T.B., and T.P.; data curation: T.B. and Q.D.; writing—original draft preparation: Q.D.; writing—review and editing: T.B., F.A., and G.H.; supervision: T.B., T.P., and G.H.; funding acquisition: F.A., G.H., T.P., and T.B.; all authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Treena I Burgess.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Code availability

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Section Editor: Marco Thines

Electronic Supplementary Material

ESM 1

(DOCX 1103 kb)

ESM 2

(DOCX 39 kb)

ESM 3

(DOCX 3108 kb)

Appendix

S1 ITS sequence data for all isolates submitted to Genbank as P. meadii or P. colocasiae or isolates matching the sequence of the type isolate of these species. Columns are species name on Genbank, organism (identity based on phylogenetic analysis), country, host, isolate code, sequence length and sequence. Duplicates accessions for the same isolate have been removed. (XLSX 80 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dang, Q.N., Pham, T.Q., Arentz, F. et al. New Phytophthora species in clade 2a from the Asia-Pacific region including a re-examination of P. colocasiae and P. meadii. Mycol Progress 20, 111–129 (2021). https://doi.org/10.1007/s11557-020-01656-7

Download citation

Keywords

  • Phytophthora insulinativitatica
  • P. multibullata
  • P. x vanyenensis
  • P. sp. germisporangia and P. sp. awatangi
  • Hybrid species
  • Cryptic species
  • Molecular phylogenetics
  • Vietnam