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Rapidly expanding host range for Puccinia psidii sensu lato in Australia

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Abstract

A rust affecting Myrtaceae was recently detected in New South Wales, Australia. Based on urediniospore morphology and host range, it was identified as Uredo rangelii, a taxon regarded as a member of the eucalyptus/guava rust (Puccinia psidii sensu lato) complex, although confusion currently surrounds its taxonomy. The exotic rust was given the common name of myrtle rust to distinguish it from eucalyptus/guava rust. The more recent discovery of teliospores in NSW that match those of P. psidii sensu stricto indicates the rust in Australia is a strain (with tonsured urediniospores) of P. psidii s.l. Outside Australia, P. psidii has a wide host range within Myrtaceae, being reported from 129 species in 33 genera, and is very damaging in South and Central America–including in eucalypt plantations in Brazil–the Caribbean and in Florida and Hawaii. To ascertain the potential threat to forestry in Australia posed by the introduced rust, we tested key forestry species, as well as key known hosts of eucalyptus/guava rust, in artificial inoculation experiments. We showed that several species of Eucalyptus are susceptible (viz. E. pilularis, E. cloeziana, E. agglomerata and E. grandis), as is Melaleuca quinquenervia. Observations during testing revealed a lengthened latent period (from inoculation until pustule formation and eruption) of four to five weeks during winter. Here we also report on observations on new hosts from surveys in NSW under the emergency response that followed the detection of the exotic rust, and surveys in NSW and Queensland following the cessation of the emergency response. In Australia, P. psidii s.l. has currently been found on 107 host species in 30 genera during surveys, including species in Angophora, Asteromyrtus, Austromyrtus, Backhousia, Callistemon, Chamelaucium, Choricarpia, Decaspermum, Eucalyptus, Eugenia, Gossia, Lenwebbia, Leptospermum, Lophomyrtus, Melaleuca, Metrosideros, Myrtus, Pilidiostigma, Rhodamnia, Rhodomyrtus, Ristantia, Stockwellia, Syncarpia, Syzygium, Tristania, Tristaniopsis, Ugni, Uromyrtus and Xanthostemon. Species under cultivation (in nurseries and gardens) that are severely affected include Gossia inophloia, Agonis flexuosa, Syzygium jambos and S. anisatum while species that are severely damaged in native bushland include Rhodamnia rubescens, Rhodomyrtus psidioides, Choricarpia leptopetala and Melaleuca quinquenervia.

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Acknowledgements

The host testing work was funded by Forest and Wood Products Australia Ltd. (Project No: PRC179-0910) and Forests NSW. We thank the owners of IP1 for the use of their greenhouse and cooperation during the in situ experiments, Michael Priest for diagnostics and Kerrie Sims for assistance with microscope photography. Staff from various agencies in Australia involved in the emergency response, as well as ongoing surveys, especially from NSW DPI and Biosecurity Queensland/DEEDI, are also thanked. We also thank Peter Wilson for advice on nomenclature of species in Myrtaceae, Morag Glen and Acelino Alfenas for sourcing some references, and Fabiano Ximenes for translation of Portuguese literature.

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Correspondence to Angus J. Carnegie.

Appendices

Appendix I. Species of Myrtaceae reported to show some susceptibility to Puccinia psidii outside Australia from field observations and host testing. Plant names according to Govaerts et al. (2011)

Tribea

Species*

Heteropyxideae (2)

Heteropyxis natalensis Harv. (Alfenas et al. 2005)

Callistemon citrinus (Sims) Sweet (Tommerup et al. 2003; Leahy 2004), C. pachyphyllus (Curtis) Skeels (Zauza et al. 2010), C. speciosus (Sims) Sweet (Viégas 1945) (as C. glaucus (DC.) Sweet, OCCPO 2007), C. viminalis (Sol. ex Gaertn.) G.Don ex Loudon (Rayachhetry et al. 2001)

Eremaea asterocarpa Hnatiuk (Old et al. 2004; OCCPO 2007), E. pauciflora (Endl.) Druce (Old et al. 2004; OCCPO 2007)

Melaleuceae (6)

Melaleuca alternifolia (Maiden & Betche) Cheel (Tommerup et al. 2003), M. cajuputi Powell (Tommerup et al. 2003), M. decora (Salisb.) Britten (Rayachhetry et al. 2001), M. hypericifolia Sm. (Old et al. 2004; OCCPO 2007), M. leucadendra (L.) L. (Zauza et al. 2010) (as M. leucodendron (L.) L., Viégas 1961 in Furtado and Marino 2003), M. nesophila F.Muell. (Zauza et al. 2010), M. quinquenervia (Cav.) S.T.Blake (Rayachhetry et al. 1997)

Regelia ciliata Schauer (Zauza et al. 2010)

Metrosidereae (9)

Metrosideros collina (J.R.Forst & G.Forst) A.Gray (Loope 2010), M. excelsa Sol. ex Gaertn. (Loope 2010), M. kermadecensis W.R.B.Oliv. (Loope 2010), M. polymorpha Gaudich. (Killgore and Heu 2007)

Syzygieae (11)

Syzygium alatoramulum B.Hyland (Zauza et al. 2010), S. australe (J.C. Wendl. ex Link) B. Hyland (Zauza et al. 2010), S. cumini (L.) Skeels (Junghans et al. 2003) (as Eugenia jambolana L., Hennen et al. 2005), S. fibrosum (F.M.Bailey) T.G.Hartley & L.M.Perry (Zauza et al. 2010), S. grande (Wight) Walp. (as Eugenia grandis Wight, Rangel 1916; Hennen et al. 2005), S. jambos (L.) Alston (as Eugenia jambos L., MacLachlan 1938), S. luehmannii (F.Muell.) L.A.S.Johnson (Zauza et al. 2010), S. malaccense (L.) Merr. & L.M.Perry (as Eugenia malaccensis L. (MacLachlan 1938), S. paniculatum Gaertn. (Leahy 2004), S. samarangense (Blume) Merr. & L.M.Perry (Zambino and Nolan 2011), S. sandwicense (A.Gray) Müll. Stuttg. (Loope 2010), S. smithii (Poir.) Nied. (as Acmena smithii Poir.) (Zauza et al. 2010)

Myrteae (12)

Acca sellowiana (O.Berg.) Burret (as Feijoa sellowiana (O.Berg.) O.Berg., in Blum and Dianese 2001)

Archirhodomyrtus beckleri (F.Muell.) A.J.Scott (Zauza et al. 2010)

Calycorectes pohlianus (O.Berg) Kiaersk. (as Eugenia cambucae b Mattos [Syn. Schizocalyx pohlianus O.Berg], Hennen et al. 2005)

Campomanesia guaviroba (DC.) Kiaersk. (as Abbevillea maschalanthe (DC) O.Berg, Rangel 1916; Hennen et al. 2005)

Decaspermum humile (Sweet ex G.Don.) A.J.Scott (Zauza et al. 2010)

Eugenia brachythrix Urb. (Dale 1955), E. brasiliensis Lam. (Hennen et al. 2005) (as E. dombeyi Skeels, Junghans et al. 2003), E. candolleana DC. (as E. christovana Kiaersk., Rangel 1916; Simpson et al. 2006), E. foetida Pers. (Leahy 2003), E. involucrata DC. (as Phyllocalyx involucratus (DC.) O.Berg, Lindquist 1960 in Hennen et al. 2005), E. kanakana N.Snow (as Monimiastrum globosum J.Gueho & A.J.Scott, Loope 2010), E. koolauensis O.Deg. (Killgore and Heu 2007), E. pyriformis Cambess. (as Eugenia uvalha Cambess., Viégas 1945; Laundon and Waterson 1965), E. pitanga (O.Berg) Nied. (as Stenocalyx pitanga O.Berg, Carvalho et al. 2007), E. reinwardtiana (Blume) A.Cunn. ex DC. (Rayachhetry et al. 2001), E. stipitata McVaugh (as araçá-boi, Junqueira et al. 2001), E. uniflora L. (Rangel 1916; Junghans et al. 2003)

Myrcia splendens (Sw.) DC. (as M. acuminata b (Kunth) DC., Carvalho et al. 2007), M. stenocarpa Krug & Urb. (Baker and Dale 1948), M. xylopioides (Kunth) DC. (Buriticá and Pardo-Cardona 1996 in Simpson et al. 2006)

Myrcianthes fragrans (Sw.) McVaugh (Rayachhetry et al. 2001), M. pungens (O.Berg) D.Legrand (Leahy 2004) (as Eugenia pungens O.Berg, Hennen et al. 2005)

Myrrhinium atropurpureum Schott (Pérez et al. 2010)

Myrtus communis L. (Leahy 2004)

Pilidiostigma glabrum Burret (Zauza et al. 2010), P. tropicum L.S.Sm. (Zauza et al. 2010)

Pimenta dioica (L.) Merr. (as Pimenta officinalis Lindl., MacLachlan 1938), P. racemosa var. racemosa (Mill.) J.W.Moore (as Pimenta acris (SW.) Kostel., MacLachlan 1938)

Plinia cauliflora (Mart.) Kausel (as Myrciaria jaboticaba (Vell.) O.Berg, Laundon and Waterson 1965) (as Myrcia jaboticaba (Vell.) Baill., Hennen et al. 2005) (as Myrciaria cauliflora (Mart.) O.Berg, Rayachhetry et al. 2001), P. edulis (Vell.) Sobral (as Eugenia edulis Vell., Rangel 1916) (as Marlieria edulis Nied., Hennen et al 2005)

Psidium cattleianum Afzel. ex Sabine (as araçazeiro, Junqueira et al. 2001), P. grandifolium Mart. ex DC. (as Psidium incanescens Mart. ex DC., Hennen et al. 2005), P. guajava L. (as Psidium pomiferum L., Winter 1884), P. guineense Sw. (Viégas 1961 in Simpson et al. 2006)

Rhodamnia rubescens Benth. (Zauza et al. 2010)

Rhodomyrtus psidioides (G.Don) Benth. (Zauza et al. 2010), R. tomentosa (Aiton) Hassk. (Loope 2010)

Eucalypteae (13)

Angophora costata (Gaertn.) Hochr. Ex Britten (Tommerup et al. 2003)

Corymbia citriodora (Hook.) K.D.Hill & L.A.S.Johnson (as Eucalyptus citriodora Hook., Joffily 1944; Dianese et al. 1984), C. grandifolia (R.Br. ex Benth.) K.D.Hill & L.A.S.Johnson (as E. grandiflora b, Hennen et al. 2005), C. gummifera (Gaertn.) K.D.Hill & L.A.S.Johnson (Zauza et al. 2010), C. intermedia (F.Muell. ex R.T.Baker) K.D.Hill & L.A.S.Johnson (Zauza et al. 2010), C. maculata (Hook.) K.D.Hill & L.A.S.Johnson (as E. maculata Hook., Dianese et al. 1984), C. torelliana (F.Muell.) K.D.Hill & L.A.S.Johnson (as E. torelliana F.Muell., Ferreira 1983; LaRosa and Hauff 2007)

Eucalyptus acmenoides Schauer (Zauza et al. 2010), E. agglomerata Maiden (Old et al. 2002; OCCPO 2007), E. alba Reinw. ex Blume (Zauza et al. 2010), E. amplifolia Naudin (Kawanishi et al. 2009), E. andrewsii Maiden (as E. montivaga A.R.Bean, Old et al. 2004, incorrectly assigned; OCCPO 2007), E. benthamii Maiden & Cambage (Auer et al. 2010; Vieira et al. 2011), E. botryoides Sm. (Aparecido 2004), E. brassiana S.T.Blake (Tommerup et al. 2003), E. camaldulensis Dehnh. (Dianese et al. 1984), E. cloeziana F.Muell. (Dianese et al. 1984), E. deglupta Blume (Zauza et al. 2010), E. diversicolor F.Muell. (Zauza et al. 2010), E. dunnii Maiden (Zauza et al. 2010), E. elata Dehnh. (Zauza et al. 2010), E. globulus Labill. (Alfenas et al. 2003), E. grandis W.Hill (Dianese et al. 1984), E. guilfoylei Maiden (Zauza et al. 2010), E. melanophloia F.Muell. (Zauza et al. 2010), E. microcorys F.Muell. (Dianese et al. 1984), E. moluccana Wall ex Roxb. (Zauza et al. 2010), E. nigra F.Muell. ex R.T.Baker (as E. phoetricha b [= E. phaeotricha Blakely & McKie], Hennen et al. 2005), E. nitens (H.Deane & Maiden) Maiden (Zauza et al. 2010), E. obliqua ĽHér. (Zauza et al. 2010), E. paniculata Sm. (Dianese et al. 1984), E. pellita F.Muell. (Dianese et al. 1984), E. pilularis Sm. (Ferreira 1983; Zauza et al. 2010), E. propinqua H.Deane & Maiden, E. punctata A.Cunn. ex DC. (Dianese et al. 1984), E. pyrocarpa L.A.S.Johnson & Blaxell (Dianese et al. 1984), E. regnans F.Muell. (Zauza et al. 2010), E. resinifera Sm. (Zauza et al. 2010), E. robusta Sm. (Ferreira 1983; Zauza et al. 2010), E. rubiginosa Brooker (Old et al. 2004; OCCPO 2007), E. rudis Endl. (Kawanishi et al. 2009), E. saligna Sm. (Dianese et al. 1984), E. scias L.A.S.Johnson & K.D.Hill. (Zauza et al. 2010), E. sieberi L.A.S.Johnson (Old et al. 2004; OCCPO 2007), E. smithii F.Muell. ex R.T.Baker (LaRosa and Hauff 2007), E. tereticornis Sm. (Ferreira 1983; Zauza et al. 2010), E. tetrodonta F.Muell. (Old et al. 2004; OCCPO 2007), E. tindaliae Blakely (Old et al. 2004; OCCPO 2007), E. urophylla S.T.Blake (Dianese et al. 1984), E. viminalis Labill. (Alfenas et al. 2003)

Syncarpieae (14)

Syncarpia glomulifera (Sm.) Nied. (Tommerup et al. 2003), S. hillii F.M.Bailey (Zauza et al. 2010)

Leptospermeae (16)

Kunzea baxteri (Klotzsch) Schauer (Tommerup et al. 2003), K. ericoides (A.Rich.) Joy Thomps. (Old et al. 2004; OCCPO 2007), K. recurva Schauer (Old et al. 2004)

Pericalymma ellipticum (Endl.) Schauer (Zauza et al. 2010)

Chamelaucieae (17)

Astartea fascicularis (Labill.) A.Cunn. ex DC. (Old et al. 2004; OCCPO 2007), A. heteranthera C.A.Gardner (Zauza et al. 2010)

Chamelaucium uncinatum Schauer (Loope 2010)

Hypocalymma robustum (Endl.) Lindl. (Zauza et al. 2010)

Thryptomene australis Endl. (Old et al. 2004; OCCPO 2007)

a Tribes according to Wilson et al. 2005

b Citing authors uncertain of host identification

* Synonym table:

Names used by cited author, or commonly used synonyms

Currently accepted name

Abbevillea maschalantha (DC) O.Berg

Campomanesia guaviroba (DC.) Kiaersk.

Acmena smithii Poir.

Syzygium smithii (Poir.) Nied.

Callistemon glaucus (DC.) Sweet

Callistemon speciosus (Sims) Sweet

Eucalyptus citriodora Hook.

Corymbia citriodora (Hook.) K.D.Hill & L.A.S.Johnson

Eucalyptus grandiflora

Corymbia grandifolia (R.Br. ex Benth.) K.D.Hill & L.A.S.Johnson

Eucalyptus maculata Hook.

Corymbia maculata (Hook.) K.D.Hill & L.A.S.Johnson

Eucalyptus phaeotricha Blakely & McKie

Eucalyptus nigra F.Muell. ex R.T.Baker

Eucalyptus torelliana F.Muell.

Corymbia torelliana (F.Muell.) K.D.Hill & L.A.S.Johnson

Eugenia brasiliensis Lam.

Eugenia dombeyi Skeels

Eugenia cambucae Mattos

Calycorectes pohlianus (O.Berg) Kiaersk.

Eugenia christovana Kiaersk.

Eugenia candolleana DC.

Eugenia dombeyi Skeels

Eugenia brasiliensis Lam.

Eugenia edulis Vell.

Plinia edulis (Vell.) Sobral

Eugenia grandis Wight

Syzygium grande (Wight)

Eugenia jambolana L.

Syzygium cumini (L.) Skeels

Eugenia jambos L.

Syzygium jambos (L.) Alston

Eugenia malaccensis L.

Syzygium malaccense (L.) Merr. & L.M.Perry

Eugenia pungens O.Berg

Myrcianthes pungens (O.Berg)

Eugenia uvalha Cambess.

Eugenia pyriformis Cambess.

Feijoa sellowiana (O.Berg) O.Berg

Acca sellowiana (O.Berg) Burret

Melaleuca leucodendron (L.) L.

Melaleuca leucadendra (L.) L.

Monimiastrum globosum J.Gueho & A.J.Scott

Eugenia kanakana N.Snow

Stenocalyx pitanga O.Berg

Eugenia pitanga (O.Berg) Nied.

Pimenta acris (SW.) Kostel.

Pimenta dioica (L.) Merr.

Pimenta officinalis Lindl.

Pimenta dioica (L.) Merr.

Marlieria edulis Nied.

Plinia edulis (Vell.) Sobral

Myrcia jaboticaba (Vell.) Baill.

Plinia cauliflora (Mart.) Kausel

Myrciaria cauliflora (Mart.) O.Berg

Plinia cauliflora (Mart.) Kausel

Myrciaria jaboticaba (Vell.) O.Berg

Plinia cauliflora (Mart.) Kausel

Phyllocalyx involucratus (DC.) O.Berg

Eugenia involucrata DC.

Psidium pomiferum L.

P. guajava L.

Psidium incanescens Mart. ex DC.

P. grandifolium Mart. ex DC.

Appendix II. Distribution of key hosts of Puccinia psidii sensu lato in Australia (Australian Virtual Herbarium, http://avh.rbg.vic.gov.au/avh/)

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Carnegie, A.J., Lidbetter, J.R. Rapidly expanding host range for Puccinia psidii sensu lato in Australia. Australasian Plant Pathol. 41, 13–29 (2012). https://doi.org/10.1007/s13313-011-0082-6

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