Research Article |
Corresponding author: M. Catherine Aime ( maime@purdue.edu ) Academic editor: Marco Thines
© 2018 M. Catherine Aime, Mehrdad Abbasi.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Aime MC, Abbasi M (2018) Puccinia modiolae in North America: distribution and natural host range. MycoKeys 39: 63-73. https://doi.org/10.3897/mycokeys.39.27378
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Puccinia modiolae, a rust fungus pathogen of Carolina bristlemallow, Modiola caroliniana (Malvaceae), is newly reported from North America, appears to be well established along the Gulf coast and is likely to have been introduced from South America. Its taxonomy, distribution and natural host range are discussed and a lectotype designated for this species. Malva sylvestris and Alcea rosea are reported as new hosts for the rust. Additional new records for Malvaceae rusts are made for P. modiolae on Alcea rosea from Brazil, P. heterospora on Herissantia crispa in Florida and P. heterogenea on Malva sp. in Peru. Finally, an identification key for the microcyclic Puccinia species on members of Malvaceae in North America is provided.
Neomycetes, Phytopathogens, Pucciniales , Uredinales
Neomycetes are alien fungi entering a new area (country or continent), typically as a result of non-intentional human activity, that become established in the new region (
Puccinia modiolae P. Syd. & Syd. (Pucciniaceae, Pucciniales) is a microcyclic rust fungus that was originally reported on Modiola prostrata A.St.-Hil. (=M. caroliniana (L.) G. Don; Malvaceae) from South America on the basis of specimens from Argentina and Uruguay (
In this study, we examine numerous fresh collections and herbarium materials and conduct phylogenetic analyses of the 28S rDNA locus to provide the first reports of P. modiolae from North America, discuss its host range and distribution and establish a lectotype for this taxon. A key to the microcyclic Puccinia species on Malvaceae in North America is provided.
Materials studied here were obtained from the Arthur Fungarium (PUR), the U.S. National Fungus Collections (BPI) and from fresh collections (listed in specimens examined below). Voucher specimens for new material are deposited in PUR. Rust spores and cross sections were routinely mounted in lactic acid in glycerol. Light microscopic analyses were performed using a Nikon Eclipse 80i microscope. Photomicrographs were obtained with a DS-Fi1 Nikon camera. In all studied specimens, thirty spores were randomly selected and measured.
DNA was extracted and the 5’ end of the nuclear 28S rDNA, amplified with rust-specific primers and sequenced following previous published protocols (
Study of recently collected materials of malvaceous plants from Texas, Louisiana and Indiana revealed the widespread presence of Puccinia modiolae along the Gulf coast on Modiola caroliniana and occurring as far north as Indiana on new hosts Alcea rosea L. and Malva sylvestris L. Examination of herbarium material also reveals P. modiolae as far south as Brazil on A. rosea (PUR N15322). Additional new records for Malvaceae rusts are made for P. heterospora on Herissantia crispa in Florida and P. heterogenea on Malva sp. in Peru. In total, we generated 28S rDNA sequences for 32 collections of Puccinia species on Malvaceae, including ten collections of P. modiolae for phylogenetic analyses (Fig.
P.
malvacearum
var.
modiolae
Pennington, Anales de la Sociedad Cientifica Argentina 55: 34 (1903). Figures
Lectotype: on Modiola caroliniana (as M. prostrata), Argentina, 1880–1881, C. Spegazzini, Decades Mycologiae Argentinae No. 10, PUR N6057, named as P. malvacearum (designated here). Isolectotype: BPI 086498.
Spermogonia usually epiphyllous, located on the opposite side of the telia in small groups, globose, 140–150 µm in diameter, yellowish-brown, with abundant and outward growing periphyses (Fig.
Teliospores of Puccinia modiolae: A–B on Modiola caroliniana (Lectotype PUR N6057) C on M. caroliniana (PUR N12041) D on M. caroliniana (PUR N12040) E on M. caroliniana (PUR N12550); F on M. caroliniana (PUR N12552) G on Alcea rosea (PUR N12039). Scale bars: 10 µm.
Puccinia modiolae – ARGENTINA: on Modiola caroliniana (as M. prostrata), C. Spegazzini, Decades Mycologiae Argentinae No. 10, 1880–1881 (Lectotype, PUR N6057, as P. malvacearum; Isolectotype, BPI 086498, as P. malvacearum). USA: Indiana, Tippecanoe Co., Lafayette, Alcea rosea L., M.C. Aime, MCA5059, 2012 Nov 05 (PUR N12038; GenBank accession #MH742985); A. rosea, M.C. Aime, MCA5042, 2012 Oct 01 (PUR N12039; GenBank accession #MH742978); West Lafayette, Purdue University Campus, Malva sylvestris L., Amnat Eamvijarn, MCA6961, 2016 Sept 16 (PUR N15171; GenBank accession #MH742977); Louisiana, East Baton Rouge Parish, Baton Rouge, Louisiana State University campus, M. caroliniana (L.) G. Don, Amnat Eamvijarn, U1374, July 2008 (PUR N12550; GenBank accession #MH742981); M. caroliniana, M.C. Aime, MCA3680, 2009 Mar 26 (PUR N12040; GenBank accession #MH742980); M. caroliniana, Don Ferrin, MCA3565, 2008 Mar 14 (PUR N12547, GenBank accession #MH742975); LSU Campus parking lot, M. caroliniana, Don Ferrin, MCA3589, 2008 May 14 (PUR N12552; GenBank accession #MH742979); Baton Rouge, private house, Malvaceae sp., Chris Clark, MCA4228, 2011 May 09 (PUR N22678; GenBank accession #MH742984); Bossier Parish, Red River Research Station, M. caroliniana, M.C. Aime, MCA4719, 2012 Apr 19 (PUR N12551); Evangeline Parish, Mamou, Main Street, Malvaceae sp., M.C. Aime, MCA3523, 2008 Feb 05 (PUR N22676); Tangipahoa Parish, 10 mi East of Independence, M. caroliniana, Charles Rush, MCA3854, 2009 Oct 22 (PUR N12549; GenBank accession #MH742982); St. James Parish, Convent, on the River Road in lawn next to Manresa House of Retreats, M. caroliniana, M.C. Aime & Tom Bruns, MCA3671, 2009 Jan 22 (PUR N12546); Orleans Parish, New Orleans, private residence, Malvaceae sp., Beth Kennedy, U1663, 2017 Mar 03 (PUR N22654; GenBank accession #MH742983); Modiola sp., M.C. Aime, MCA3568, 2008 Mar 23 (PUR N16658); Texas, Harris Co., Shell Station on Rt. 146, Seabrook Waterfront District, M. caroliniana, M.C. Aime, MCA3717, 2009 May 04 (PUR N12041; GenBank accession #MH742976). BRAZIL: Sao Paulo, Alcea rosea, M. Figueiredo, J. Hennen s.n., 1999 Jan 12 (PUR N15322).
Puccinia heterogenea – PERU: Cajamarca Provence, Shudall, Malva sp., Jorge Diaz Valderrama, U1568, 2014 Dec 30 (PUR N12885; GenBank accession #MH743006).
Puccinia heterospora – USA: Florida, Monroe Co., Marathon, Herissantia crispa (L.) Briz., M.C. Aime, MCA2876, 2004 Dec 31 (PUR N22677; GenBank accession #MH742974).
Puccinia malvacearum –USA: California, Alameda Co., Berkeley, Alcea rosea, M.C. Aime, MCA6367, 2016 Aug 05 (PUR N15060; GenBank accession #MH743003); Idaho, Gem Co., Alcea rosea, Krishna Mohan, U888, 2006 May 26 (BPI 878033; GenBank accession #MH742996); Canyon Co., Parma, Alcea sp., Ram Sampangi, U1384, April 2009 (PUR N16292; GenBank accession #MH742995); Malva neglecta, Krishna Mohan, U1277, 2007 (PUR N16174; GenBank accession #MH743002); TURKEY: Bingöl Province, Lavatera trimestris, Lütfi Behçet, U1562, Jun 21 2014 (PUR N11582; GenBank accession #MH743004); SPAIN: Córdoba Province, near Montilla, Malva sylvestris, Walter J. Kaiser, U928, 2006 May 19 (BPI 878041; GenBank accession #MH742988); M. sylvestris, Walter J. Kaiser, U981, 2006 May 19 (BPI 878046; GenBank accession #MH742997); edge of wheat field, M. sylvestris, Walter J. Kaiser, U929, 2006 May 21 (BPI 878042; GenBank accession #MH743000); Cabra, edge of olive grove at Centro de Investigacion y Foirmacion Agraria, M. sylvestris, Walter J. Kaiser, U970, 2006 May 15 (BPI 878044; GenBank accession #MH742991); M. sylvestris, Walter J. Kaiser, U956, 2006 May 15 (BPI 878043; GenBank accession #MH742994); near Carcabury, Alcea sp., Walter J. Kaiser, U1258, April 2007 (PUR N16156; GenBank accession #MH743005); Córdoba, Colegio Mayor Universitario, Nuestra Senora de la Asuncion, Avenida Menendez Pidal, Lavatera cretica, Walter J. Kaiser, U958, 2006 May 09 (BPI 878038; GenBank accession #MH742998); L. cretica, Walter J. Kaiser, U916, 2006 May 09 (BPI 878035; GenBank accession #MH742999); Malaga Province, outskirts of El Burgo, Alcea rosea, U937, 2006 May 27 (BPI 875152; GenBank accession #MH742989); A. rosea, Walter J. Kaiser, U989, 2006 May 27 (BPI 878034; GenBank accession #MH742990); Jaén Province, Baéza, L. cretica, Walter J. Kaiser, U974, 2006 May 19 (BPI 878040; GenBank accession #MH742993); L. cretica, Walter J. Kaiser, U922, 2006 May 19 (BPI 878036; GenBank accession #MH743001); GERMANY, Thuringia, Weimar, A. rosea, G.R.W. Arnold, U474, 2004 Jun 22 (BPI 878032; GenBank accession #MH742992).
Puccinia malvastri –Arizona, Cochise, Cottonwood Canyon, Peloncillo Mountains, Sphaeralcea sp., George Cummins 61265, 1961 Sep 27 (topotype, PUR 59015).
Puccinia sherardiana sensu
Puccinia sphaeralceae –New Mexico, Mesilla Park, Sphaeralcea angustifolia, T. Cockerell 3478, 1896 Aug 01 (isotype, PUR 39636).
Phytoparasitic Neomycetes have the potential to cause great losses across the world via infestation of crops, ornamental plants and native flora (
Puccinia modiolae is a native rust fungus of South America and was most likely introduced in the USA by accompanying its host plant Modiola. The rust species is quite common on Modiola caroliniana in Louisiana and was also found in Texas, making the Gulf coast a likely site for the original introduction of the rust species in North America. We are unable to pinpoint when P. modiolae was introduced into the USA. However, we were unable to locate any historical North American herbarium material of P. modiolae in BPI or PUR, nor were we able to find records of any rust species on Modiola in the USA, Canada or Mexico in all available literature, making it likely that P. modiolae became established in the southern USA probably no earlier than the second half of the 20th century. Before the present study, P. modiolae was only known from Argentina and Uruguay. In Argentina, Althaea officinalis L., Lavatera arborea L. and Malva parviflora L., in addition to M. caroliniana, have been reported as the natural host range of the rust species; only M. caroliniana is a reported host in Uruguay (
The presence or absence of spermogonia is one of the morphological features for distinguishing microcyclic rust fungi on Malvaceae members (
1 | spermogonia absent | 2 |
– | spermogonia present | 6 |
2 | one-celled teliospores predominating | P. heterospora |
– | one-celled teliospores rare or absent | 3 |
3 | telia usually dark brown | P. lobata |
– | telia usually light brown | 4 |
4 | teliospore length mostly > 40 µm | P. malvacearum |
– | teliospore length mostly < 40 µm | 5 |
5 | teliospore wall 2–3 µm thick at sides, much thicker above | P. anodae |
– | teliospore wall 1–2 µm thick at sides, scarcely thicker above | P. exilis |
6 | teliospores with many anomalies because of the concretion of spores, making them appear notched at apex | P. modiolae |
– | teliospores without spore anomalies | (P. sherardiana s. lat.) 7 |
7 | teliospore length mostly > 50 µm, oblong-ellipsoid |
P.
sphaeralceae
|
– | teliospore length mostly < 50 µm, broadly ellipsoid |
P.
malvastri
|
MCA gratefully acknowledges funding from the National Science Foundation (CSBR program: DEB-1458290; TCN program: DEB-1502887) for the Purdue University herbaria, without which this work would not have been possible. This work was also supported by the USDA National Institute of Food and Agriculture Hatch project 1010662.