Australia: A Continent Without Native Powdery Mildews? The First Comprehensive Catalog Indicates Recent Introductions and Multiple Host Range Expansion Events, and Leads to the Re-discovery of Salmonomyces as a New Lineage of the Erysiphales

Levente Kiss; Niloofar Vaghefi; Kaylene Bransgrove; John D W Dearnaley; Susumu Takamatsu; Yu Pei Tan; Craig Marston; Shu-Yan Liu; Dan-Ni Jin; Dante L Adorada; Jordan Bailey; Maria Graciela Cabrera de Álvarez; Andrew Daly; Pamela Maia Dirchwolf; Lynne Jones; Thuan Dat Nguyen; Jacqueline Edwards; Wellcome Ho; Lisa Kelly; Sharl J L Mintoff; Jennifer Morrison; Márk Z Németh; Sandy Perkins; Roger G Shivas; Reannon Smith; Kara Stuart; Ronald Southwell; Unaisi Turaganivalu; Kálmán Zoltán Váczy; Annie Van Blommestein; Dominie Wright; Anthony Young; Uwe Braun

doi:10.3389/fmicb.2020.01571

Australia: A Continent Without Native Powdery Mildews? The First Comprehensive Catalog Indicates Recent Introductions and Multiple Host Range Expansion Events, and Leads to the Re-discovery of Salmonomyces as a New Lineage of the Erysiphales

Front Microbiol. 2020 Jul 16:11:1571. doi: 10.3389/fmicb.2020.01571. eCollection 2020.

Authors

Levente Kiss¹, Niloofar Vaghefi¹, Kaylene Bransgrove², John D W Dearnaley¹, Susumu Takamatsu^{1

3}, Yu Pei Tan², Craig Marston⁴, Shu-Yan Liu⁵, Dan-Ni Jin⁵, Dante L Adorada¹, Jordan Bailey⁶, Maria Graciela Cabrera de Álvarez⁷, Andrew Daly⁸, Pamela Maia Dirchwolf⁷, Lynne Jones⁴, Thuan Dat Nguyen⁹, Jacqueline Edwards^{10

11}, Wellcome Ho¹², Lisa Kelly¹³, Sharl J L Mintoff¹⁴, Jennifer Morrison⁴, Márk Z Németh¹⁵, Sandy Perkins⁴, Roger G Shivas^{1

2}, Reannon Smith^{10

11}, Kara Stuart¹⁶, Ronald Southwell¹⁷, Unaisi Turaganivalu¹⁸, Kálmán Zoltán Váczy¹⁹, Annie Van Blommestein²⁰, Dominie Wright²⁰, Anthony Young²¹, Uwe Braun²²

Affiliations

¹ Centre for Crop Health, Institute for Life Sciences and the Environment, University of Southern Queensland, Toowoomba, QLD, Australia.
² Queensland Plant Pathology Herbarium, Department of Agriculture and Fisheries, Dutton Park, QLD, Australia.
³ Laboratory of Plant Pathology, Faculty of Bioresources, Mie University, Tsu, Japan.
⁴ Science and Surveillance Group, Department of Agriculture, Water and the Environment, Brisbane, QLD, Australia.
⁵ College of Plant Protection, Jilin Agricultural University, Changchun, China.
⁶ Plant Pathology & Mycology Herbarium, New South Wales Department of Primary Industries, Orange, NSW, Australia.
⁷ Department of Plant Protection, Faculty of Agricultural Science, National University of the Northeast, Corrientes, Argentina.
⁸ Plant Health Diagnostic Service, New South Wales Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Menangle, NSW, Australia.
⁹ Field Crops Research Institute, Hanoi, Vietnam.
¹⁰ Agriculture Victoria Research, Agriculture Victoria, Department of Jobs, Precincts and Regions, Bundoora, VIC, Australia.
¹¹ School of Applied Systems Biology, La Trobe University, Bundoora, VIC, Australia.
¹² New Zealand Ministry for Primary Industries, Auckland, New Zealand.
¹³ Department of Agriculture and Fisheries, Queensland Government, Toowoomba, QLD, Australia.
¹⁴ Department of Primary Industry and Resources, Northern Territory Government, Darwin, NT, Australia.
¹⁵ Plant Protection Institute, Centre for Agricultural Research, Budapest, Hungary.
¹⁶ Ecosciences Precinct, Department of Agriculture and Fisheries, Dutton Park, QLD, Australia.
¹⁷ Science and Surveillance Group, Department of Agriculture, Water and the Environment, Sydney, NSW, Australia.
¹⁸ Secretariat for the Pacific Community, Suva, Fiji.
¹⁹ Food and Wine Research Institute, Eszterházy Károly University, Eger, Hungary.
²⁰ Department of Primary Industries and Regional Development, South Perth, WA, Australia.
²¹ School of Agriculture and Food Sciences, The University of Queensland, Brisbane, QLD, Australia.
²² Herbarium, Department of Geobotany and Botanical Garden, Institute for Biology, Martin Luther University, Halle (Saale), Germany.

Abstract

In contrast to Eurasia and North America, powdery mildews (Ascomycota, Erysiphales) are understudied in Australia. There are over 900 species known globally, with fewer than currently 60 recorded from Australia. Some of the Australian records are doubtful as the identifications were presumptive, being based on host plant-pathogen lists from overseas. The goal of this study was to provide the first comprehensive catalog of all powdery mildew species present in Australia. The project resulted in (i) an up-to-date list of all the taxa that have been identified in Australia based on published DNA barcode sequences prior to this study; (ii) the precise identification of 117 specimens freshly collected from across the country; and (iii) the precise identification of 30 herbarium specimens collected between 1975 and 2013. This study confirmed 42 species representing 10 genera, including two genera and 13 species recorded for the first time in Australia. In Eurasia and North America, the number of powdery mildew species is much higher. Phylogenetic analyses of powdery mildews collected from Acalypha spp. resulted in the transfer of Erysiphe acalyphae to Salmonomyces, a resurrected genus. Salmonomyces acalyphae comb. nov. represents a newly discovered lineage of the Erysiphales. Another taxonomic change is the transfer of Oidium ixodiae to Golovinomyces. Powdery mildew infections have been confirmed on 13 native Australian plant species in the genera Acacia, Acalypha, Cephalotus, Convolvulus, Eucalyptus, Hardenbergia, Ixodia, Jagera, Senecio, and Trema. Most of the causal agents were polyphagous species that infect many other host plants both overseas and in Australia. All powdery mildews infecting native plants in Australia were phylogenetically closely related to species known overseas. The data indicate that Australia is a continent without native powdery mildews, and most, if not all, species have been introduced since the European colonization of the continent.

Keywords: host jumps; host-pathogen interactions; invasive species; obligate biotrophs; plant-microbe interactions; rapid evolution.

Copyright © 2020 Kiss, Vaghefi, Bransgrove, Dearnaley, Takamatsu, Tan, Marston, Liu, Jin, Adorada, Bailey, Cabrera de Álvarez, Daly, Dirchwolf, Jones, Nguyen, Edwards, Ho, Kelly, Mintoff, Morrison, Németh, Perkins, Shivas, Smith, Stuart, Southwell, Turaganivalu, Váczy, Blommestein, Wright, Young and Braun.