Taxonomy of Southeast Asian-Australasian grapevine leaf rust fungus and its close relatives

Mycological Progress volume 19, pages905–919(2020)Cite this article

Abstract

Rust fungi on commercial Vitis cultivars, wild Vitaceae, and Meliosma (Sabiaceae), potential alternate hosts of a grapevine leaf rust (GLR) fungus, were surveyed in Thailand and Vietnam. Molecular phylogenetic analyses using the internal transcribed spacer 2 and the large-subunit rRNA gene (D1/D2 region) and morphological examinations confirmed that the GLR fungus distributed in Southeast Asia and Australasia is distinct from Neophysopella species involved in GLRs in East Asia and the Americas. Therefore, the Southeast Asian-Australasian GLR fungus is recognized as a new Neophysopella species and named as N. tropicalis. Two fungi on Meliosma species in Thailand were aecial anamorph of Neophysopella species. One parasitic on M. simplicifolia and M. simplicifolia subsp. fordii was previously named as Aecidium wareoense, and a new name, N. wareoensis, is proposed for it. Another on M. arnottiana in Thailand was phylogenetically and morphologically distinct from all other Meliosma rust fungi, and, therefore, it is recognized as a new species, N. sriphumensis. A uredinial-telial fungus on Ampelocissus araneosa (Vitaceae) in Thailand was morphologically similar to Phakopsora cronartiiformis on Parthencissus semicordata (Vitaceae) in the Himalayas. However, the former fungus was distinct from the latter in producing characteristic urediniospores with labyrinthiform surface structure and cone-shaped projections. It is, therefore, recognized as a new species, N. doipuiensis.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Aime MC (2006) Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47:112–122. https://doi.org/10.1007/S10267-006-0281-0

    CAS  Article  Google Scholar 

  2. Aime MC, Castlebury LA, Abbasi M, Begerow D, Berndt R, Kirschner R, Marvanová L, Ono Y, Padamsee M, Scholler M, Thines M, Rossman AY (2018) Competing sexual and asexual generic names in Pucciniomycotina and Ustilaginomycotina (Basidiomycota) and recommendations for use. IMA Fungus 9:75–89. https://doi.org/10.5598/imafungus.2018.09.01.06

    Article  PubMed  PubMed Central  Google Scholar 

  3. Aime MC, Rossman AY, Ono Y, Castlebury LA (2019) Proposal to conserve the name Phakopsora (Basidiomycota, Pucciniales) with conserved type. Taxon 68:592. https://doi.org/10.1002/tax.12076

    Article  Google Scholar 

  4. Angelotti F, Regina C, Buffara S, Vieira RA, Vida JB (2014) Protective, curative and eradicative activities of fungicides against grapevine rust. Ciéncia Rural 44:1367–1370. https://doi.org/10.1590/0103-8478cr20121085

    CAS  Article  Google Scholar 

  5. Anonymous (2008) Eradication of grapevine leaf rust (GVLR) from Australia. https://www.ippc.int/en/countries/australia/pestreports/2008/03/eradication-of-grapevine-leaf-rust-gvlr-from-australia. Accessed 1 April 2020

  6. Ashenfelter O, Storchmann K (2016) Climate change and wine: a review of the economic implications. J Wine Econ 11:105–138. https://doi.org/10.1017/jwe.2016.5

    Article  Google Scholar 

  7. Ayawong C, Unartngam J, Chung WS, Ono Y (2020) Ravenelia species (Pucciniales) newly found in Thailand with their additional host and life cycle stage. Mycoscience 61:197–203. https://doi.org/10.1016/j.myc.2020.03.005

    Article  Google Scholar 

  8. Bayer TM, Costa IVFD (2006) Ocorréncia de Phakopsora vitis Ono em Santa Maria, Rio Grande do Sul. Ciéncia Rural 36:1307–1308. https://doi.org/10.1590/S0103-84782006000400042

    Article  Google Scholar 

  9. Boedijn KB (1960) The Uredinales of Indonesia. Nova Hedwigia 1:463–469+2pl

    Google Scholar 

  10. Chatasiri S, Ono Y (2008) Phylogeny and taxonomy of the Asian grapevine leaf rust fungus, Phakopsora euvitis, and its allies (Uredinales). Mycoscience 49:66–74. https://doi.org/10.1007/s10267-007-0390-4

    CAS  Article  Google Scholar 

  11. Clayton CN, Riding WH (1970) Grape rust, Physopella ampelopsidis, on Vitis rotundifolia in North Carolina. Phytopathology 60:1022–1023. https://doi.org/10.1094/Phyto-60-1022

    Article  Google Scholar 

  12. Commins T, Asavasanti S, Deloire A (2012) What is tropical wine and what defines it? Thailand as a case study. Asian J Food Agro-Ind 5:79–95 http://www.ajofai.info/Abstract/What%20is%20tropical%20wine%20and%20what%20defines%20it%20thailand%20as%20a%20case%20study.pdf

    Google Scholar 

  13. Cummins GB (1937) Studies in the Uredinales of the Philippines. Ann Mycologici 35:98–105

    Google Scholar 

  14. Cummins GB (1941) Uredinales of New Guinea IV. Mycologia 33:380–389. https://doi.org/10.1080/00275514.1941.12020831

    Article  Google Scholar 

  15. Daly AM, Hennessy CR, Schultz GC (2005) New host record for the grapevine leaf rust fungus, Phakopsora euvitis. Australas Plant Pathol 34:415–416. https://doi.org/10.1071/AP05035

    Article  Google Scholar 

  16. de Queiroz K (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 57–75

    Google Scholar 

  17. de Queiroz K (1999) The general lineage concept of species and the defining properties of the species category. In: Wilson RA (ed) Species: new interdisciplinary essays. MIT Press, Cambridge, pp 49–89

    Google Scholar 

  18. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886. https://doi.org/10.1080/10635150701701083

    Article  PubMed  Google Scholar 

  19. Frag H, Malheiro C, Mouninho-Pereira J, Santos JA (2013) An overview of climate change impacts on European viticulture. Food Energy Secur 1:94–110. https://doi.org/10.1002/fes3.14

    Article  Google Scholar 

  20. Freudenstein JV, Broe MB, Folk RA, Sinn BT (2017) Biodiversity and the species concept—lineages are not enough. Syst Biol 66:644–656. https://doi.org/10.1093/sysbio/syw098

    Article  PubMed  Google Scholar 

  21. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  22. Hansen Z, Windham A, Windham M (2018) Grapevine leaf rust. https://extension.tennessee.edu/publications/Documents/W790.pdf. Accessed 1 April 2020

  23. Hayman PT, Leske P, Nidumolu U (2009) Climate change and viticulture. Informing the decision making at a regional level. South Australian Wine Industry Association and South Australian Research and Development Institute. GWRDC Project SAW 06/01 version 1.1, October 2009, 43 pp. https://doi.org/10.13140/2.1.1013.2163

  24. Ji JX, Li Z, Li Y, Kakishima M (2019) Life cycle of Nothoravenelia japonica and its phylogenetic position in Pucciniales, with special reference to the genus Phakopsora. Mycol Prog 18:855–864. https://doi.org/10.1007/sl1557-019-01496-0

    Article  Google Scholar 

  25. Jones GV, White MA, Cooper OR, Storchmann K (2005) Climate change and global wine quality. Clim Chang 73:319–343. https://doi.org/10.1007/s10584-005-4704-2

    Article  Google Scholar 

  26. Katoh K, Standly DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    CAS  Article  Google Scholar 

  28. Leyva-Mir SG, Garcia-Reyes C, Solano-Bacz AR, Camacho-Tapia M, Garcia-Ruiz MT, Tovar-Pedraza JM (2017) Occurrence of Asian grapevine leaf rust disease caused by Phakopsora meliosmae-myrianthae in Mexico. Trop Plant Pathol 42:504–506. https://doi.org/10.1007/s40858-017-0157-1

    Article  Google Scholar 

  29. Liu XQ, Ickert-Bond SM, Nie ZL, Zou Z, Chen LQ, Wen J (2016) Phylogeny of the Ampelocissus–Vitis clade in Vitaceae supports the New World origin of the grape genus. Mol Phylogenet Evol 95:217–228. https://doi.org/10.1016/j.ympev.2015.10.013

    Article  PubMed  Google Scholar 

  30. Lorsuwan C, Tontyaporn S, Visarathanonth N, Manoch L, Kakishima M (1984) Materials for the rust flora in Thailand I. Trans Mycol Soc Jpn 25:57–65

    Google Scholar 

  31. McTaggart AR, Aime MC (2018) The species of Coleosporium (Pucciniales) on Solidago in North America. Fungal Biol 122:800–809. https://doi.org/10.1016/j.funbio.2018.04.007

    Article  PubMed  Google Scholar 

  32. Mozell MR, Thach L (2014) The impact of climate change on the global wine industry: challenges & solutions. Wine Econ Policy 3:81–89. https://doi.org/10.1016/j.wep.2014.08.001

    Article  Google Scholar 

  33. Nylander JAA (2004) MrModeltest v.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala

    Google Scholar 

  34. O'Donnell K (1993). Fusarium and its near relatives. Pp. 225e233 IN: Reynolds DR, Taylor JW (eds.) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CABI, Wallingford

  35. Okane I, Ono Y (2018) Phylogenetic study of indigenous grapevine leaf rust fungi in North America and biological identity of an invasive grapevine leaf rust fungus in Brazil. Mycoscience 59:99–104. https://doi.org/10.1016/j.myc.2017.07.005

    Article  Google Scholar 

  36. Ono Y (2000) Taxonomy of the Phakopsora ampelopsidis species complex on vitaceous hosts in Asia including a new species. P euvitis Mycologia 92:154–173. https://doi.org/10.2307/3761460

    Article  Google Scholar 

  37. Ono Y (2008) Why life-cycle studies? Implications in the taxonomy of rust fungi (Uredinales). (in Japanese with English abstract, tables and figures). Nippon Kingakkai Kaiho 49:1–28

    Google Scholar 

  38. Ono Y (2013) Ampelocissus plants harbor Phakopsora rust pathogens of grapevines and Boston Ivy. Bull Fac Educ Ibaraki Univ (Natural Sciences) 62:1–7 https://rose-ibadai.repo.nii.ac.jp/?action=pages_view_main&active_action=repository_view_main_item_detail&item_id=11626&item_no=1&page_id=13&block_id=21

    Google Scholar 

  39. Ono Y (2015) Geographic distribution of two American grapevine leaf rust fungi (Phakopsoraceae, Pucciniales). Bull Fac Educ Ibaraki Univ (Natural Sciences) 64:11–19 https://rose-ibadai.repo.nii.ac.jp/?action=pages_view_main&active_action=repository_view_main_item_detail&item_id=17390&item_no=1&page_id=13&block_id=21

    Google Scholar 

  40. Ono Y (2016a) Mixed infections of grapevine leaf rusts Phakopsora meliosmae-myrianthae and P. montana in Japan. J Gen Plant Pathol 82:149–153. https://doi.org/10.1007/s10327-016-0655-x

    Article  Google Scholar 

  41. Ono Y (2016b) Phakopsora hornotina, an additional autoecious rust species on Meliosma in the Philippines and the Ryukyu Islands, Japan. Mycoscience 57:71–78. https://doi.org/10.1016/j.myc.2015.09.003

    Article  Google Scholar 

  42. Ono Y (2017) Phakopsora muscadiniae on Vitis rotundifolia parasitizes grape cultivars derived from V. labrusca and V. vinifera. Bull Fac Educ Ibaraki Univ (Natural Sciences) 66:5–17 https://rose-ibadai.repo.nii.ac.jp/?action=pages_view_main&active_action=repository_view_main_item_detail&item_id=17740&item_no=1&page_id=13&block_id=21

    Google Scholar 

  43. Ono Y, Chatasiri S, Pota S, Yamaoka Y (2012) Phakopsora montana, another grapevine leaf rust pathogen in Japan. J Gen Plant Pathol 78:338–347. https://doi.org/10.1007/s10327-012-0401-y

    CAS  Article  Google Scholar 

  44. Ono Y, Unartngam J, Ayawong C, Abe J, Okane I (2015) Rust fungi (Pucciniales) forming the Aecidium state on Meliosma (Meliosmaceae) in Asia. Bull Fac Educ Ibaraki Univ (Natural Sciences) 64:1–9 https://rose-ibadai.repo.nii.ac.jp/?action=pages_view_main&active_action=repository_view_main_item_detail&item_id=17391&item_no=1&page_id=13&block_id=21

    Google Scholar 

  45. Ozoe S, Kadowaki Y (1971) Ecology and control of the grapevine rust disease (in Japanese). Shokubutsuboeki 25:401–404

    CAS  Google Scholar 

  46. Possingham JV (2008) Developments in the production of table grapes, wine and raisins in tropical regions of the world. Acta Hortic 785:45–50. https://doi.org/10.17660/ActaHortic.2008.785.1

    Article  Google Scholar 

  47. Pota S, Chatasiri S, Ono Y, Yamaoka Y (2013) Taxonomy of two host specialized Phakopsora populations on Meliosma in Japan. Mycoscience 54:19–28. https://doi.org/10.1016/j.myc.2012.07.004

    Article  Google Scholar 

  48. Pota S, Chatasiri S, Unartngam J, Yamaoka Y, Hosaka K, Ono Y (2015) Taxonomic identity of a Phakopsora fungus causing the grapevine leaf rust disease in Southeast Asia and Australasia. Mycoscience 56:198–204. https://doi.org/10.1016/j.myc.2014.06.003

    Article  Google Scholar 

  49. Primiano IV, Loehrer M, Amorim L, Schaffrath U (2017) Asian grapevine leaf rust caused by Phakopsora euvitis: an important disease in Brazil. Plant Pathol 66:691–701. https://doi.org/10.1111/ppa.12662

    Article  Google Scholar 

  50. Ribeiro LFC, Lima MG (2007) Primeiro relato da ocorrência da ferrugem da videira na região de Alta Floresta - MT. Revista de Ciências Agroambientais, Alta Floresta 5:105–109

    Google Scholar 

  51. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S et al (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and modelchoice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  52. Scapin-Buffara CR, Angelotti F, Dufault NS, Pereira CB, Tessmann DJ (2018) Seasonal progression of leaf rust in ‘Niagara Rosada’ grapevine in a biannual crop system in Brazil. Eur J Plant Pathol 152:589–597. https://doi.org/10.1007/s10658-018-1501-0

    Article  Google Scholar 

  53. Schaefer WW (2016) New developments in tropical viticulture under monsoon climate. Acta Hortic 1115:195–201. https://doi.org/10.17660/ActaHortic.2016.1115.29

    Article  Google Scholar 

  54. Shear CL (1924) Grape rust in Florida. Phytopathology 14:170–171

    Google Scholar 

  55. Sonego OR, Garrido LR, Gava R (2005) Ferrugem da videira no Brasil. Communicado Tecnico 62:1–4

    Google Scholar 

  56. Souza NS (2004) Ocorrência de ferrugem em videira em Mato Grosso. Fitopatol Bras 29:226. https://doi.org/10.1590/S0100-41582004000200021

    Article  Google Scholar 

  57. Stevens FL (1932) Additional Philippine Uredineae. Nat Appl Sci Bull, University of the Philippines 2:441–447

    Google Scholar 

  58. Tessmann DJ, Dianese JC, Genta W, Vida JB, May-de Mio LL (2004) Grape rust caused by Phakopsora euvitis, a new disease for Brazil. Fitopatol Bras 29:338. https://doi.org/10.1590/S0100-41582004000300022

    Article  Google Scholar 

  59. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4239–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990

    Article  Google Scholar 

  60. Weinet MP, Shivas RG, Pitkethley RN, Daly AM (2003) First record of grapevine leaf rust in the Northern Territory, Australia. Australas Plant Pathol 32:117–118. https://doi.org/10.1071/AP02060

    Article  Google Scholar 

  61. Xavier AA, Dariva JM, Ribeiro RCF, Mizobutsi EH (2012) Ocorrência daf errugem da videira em Minas Gerais. Rev Bras Frutic 34:317–319. https://doi.org/10.1590/S0100-29452012000100041

    Article  Google Scholar 

  62. Zhang N, Wen J, Zimmer EA (2015) Congruent deep relationships in the grape family (Vitaceae) based on sequences of chloroplast genomes and mitochondrial genes via genome skimming. PLoS One 10(12):e0144701. https://doi.org/10.1371/journal.pone.0144701

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This study was carried out under the permission from the National Research Council of Thailand (NRCT) for the international project entitled “Taxonomy and life cycle of rust fungi with special reference to grapevine and fern leaf rusts” (Project ID: 2018/043). We thank the Department of National Parks, Wildlife and Plant Conservation, Ministry of Natural Resources and Environment, Thailand, for permitting to survey plant rusts and to sample rusted plants at Doi Suthep-Pui National Park. The Forest Herbarium (the Department of National Parks, Wildlife and Plant Conservation) provided us with the opportunity to examine Meliosma specimens for search of possible rust infection. Small portion of rust-infected shoot was detached from Meliosma simplicifolia specimens for microscopic observations under their permission. The holotype and additional two specimens of Aecidium wareoense were loaned from the Arthur Fungarium, Purdue University, U. S. A. (PUR), for which we are grateful. Field survey and sample collection in Vietnam was supported by the Biotechnology Center of Ho Chi Minh City (CTML & IO).

Funding

This study was supported, in part, by a Grant-in-Aid (G-2018-1-019) from the Institute of Fermentation, Osaka (IFO) and a Grant-in-Aid for Scientific Research Nos.18570081 and 25450056 from the Japan Society for the Promotion of Sciences (YO).

Author information

Affiliations

  1. Faculty of Education, Ibaraki University, Mito, Ibaraki, 310-8512, Japan

    Yoshitaka Ono

  2. Department of Plant Pathology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom, 73140, Thailand

    Yoshitaka Ono, Jintana Unartngam & Chanjira Ayawong

  3. Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Izumi Okane

  4. Novartis Crop Protection (Thailand) Ltd., Takfah, Nakhon Sawan, 6019, Thailand

    Sinchai Chatasiri

  5. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Siriporn Pota & Cham Thi Mai Le

  6. Department of National Parks, Wildlife and Plant Conservation, Ministry of Natural Resources and Environment, Bangkok, 110900, Thailand

    Chanjira Ayawong

  7. Department of Plant Pathology, Faculty of Agronomy, Vietnam National University of Agriculture, Gia Lam, 12450, Hanoi, Vietnam

    Huy Duc Nguyen

  8. Division of Microbial Technology, Biotechnology Center of Ho Chi Minh City, Trung My Tay Ward, District 12, 71507, Ho Chi Minh, Vietnam

    Cham Thi Mai Le

Authors
  1. Yoshitaka Ono
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Izumi Okane
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sinchai Chatasiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Siriporn Pota
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jintana Unartngam
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chanjira Ayawong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Huy Duc Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Cham Thi Mai Le
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoshitaka Ono.

Ethics declarations

Conflict of interests

The authors declare that they have no conflict of interests.

Additional information

Publisher’s note

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

Section Editor: Meike Piepenbring

Electronic supplementary material

ESM 1

(PDF 181 kb)

ESM 2

(PDF 165 kb)

ESM 3

(PDF 217 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ono, Y., Okane, I., Chatasiri, S. et al. Taxonomy of Southeast Asian-Australasian grapevine leaf rust fungus and its close relatives. Mycol Progress 19, 905–919 (2020). https://doi.org/10.1007/s11557-020-01607-2

Download citation

Keywords

  • Meliosma
  • New taxa
  • Phylogeny
  • Pucciniales
  • Taxonomy
  • Vitaceae