Abstract
This study was initiated to elucidate the taxonomy and host range of Stemphylium species associated with leaf spot of faba bean in Australia. A three-locus phylogenetic analysis of 41 isolates collected from faba bean and other Fabaceae and Brassicaceae crops was constructed employing the internal transcribed spacers and the intervening 5.8S region of the nuclear ribosomal DNA, glyceraldehyde 3-phosphate dehydrogenase, and calmodulin sequences. The results indicated that more than one Stemphylium species occurs on faba bean (Vicia faba), chickpea (Cicer arientinum), lentil (Lens culinaris), and narrow-leafed lupin (Lupinus angustifolius) in Australia. Five Stemphylium species (S. astragali, S. beticola, S. eturmiunum, S. simmonsii, and S. vesicarium) were found associated with legume crops, of which S. astragali is a new report for Australia. Although isolates obtained from faba bean were retrieved within S. eturmiunum and S. vesicarium clades, those pathogenic to faba bean belonged to S. eturmiunum, a species not previously reported on faba bean. Interestingly, some S. eturmiunum isolates obtained from faba bean and other legumes were unable to infect faba bean, which indicated the potential presence of formae speciales within this species. The ability of S. eturmiunum isolates to cause plant death in susceptible faba bean varieties within only a few days emphasises the need for incorporation of Stemphylium blight resistance into faba bean breeding programs. Also, further research into the biology and epidemiology of the disease is warranted.
Similar content being viewed by others
References
Abdel-Hafez SII (1984) Mycoflora of bean, broad bean, lentil, lupine and pea seeds in Saudi Arabia. Mycopathologia 88:45–49
Ahmad A (2014) Stemphylium grey leaf spot disease of lupins in Western Australia (Doctoral dissertation, University of Western Australia), 134
Akagi Y, Akamatsu H, Otani H, Kodama M (2009) Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8:1732–1738
Andersen B, Frisvad JC (2004) Natural occurrence of fungi and fungal metabolites in moldy tomatoes. J Agric Food Chem 52:7507–7513
Barash I, Pupkin G, Netzer D, Kashman Y (1982) A novel enolic β-ketoaldehyde phytotoxin produced by Stemphylium botryosum f. sp. lycopersici: partial chemical and biological characterisation. Plant Physiol 69:23–27
Berbee ML, Pirseyedi M, Hubbard S (1999) Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia 91:964–977
Bobev S (2009) [reference guide for the diseases of cultivated plants] (translated from Russian). Makros Publ 466 pages
Câmara MPS, O’Neill NR, Berkum P (2002) Phylogeny of Stemphylium spp. based on ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycology 94:660–672
Caudillo-Ruiz KB, Bhadauria V, Banniza S (2017) Aetiology of stemphylium blight on lentil in Canada. Can J Plant Pathol 39:422–432
Chalvet F, Grimaldi C, Kaper F, Langin T, Daboussi MJ (2003) Hop, an active Mutator-like element in the genome of the fungus Fusarium oxysporum. Mol Biol Evol 20:1362–1375
Cho WD, Shin HD (2004) List of plant diseases in Korea. 4th edition. Korean Society of Plant Pathology, 779 pages
Cook RP, Dubé AJ (1989) Host-pathogen index of plant diseases in South Australia. South Australian Department of Agriculture, 142 pages
Crous PW, Groenewald JZ (2005) Hosts, species and genotypes: opinions versus data. Australas. Plant Pathol. 34:463–470.
Crous PW, Wingfield MJ, Richardson DM et al (2016) Fungal planet description sheets: 400–468. Persoonia 36:316–458
De Hoog GS, Gerrits van den Ende AHG (1998) Molecular diagnostics of clinical strains of filamentous Basidiomycetes. Mycoses 41:183–189
Deng JX, Paul NC, Li MJ et al (2014) Stemphylium platycodontis sp. nov. isolated from Platycodon grandifloras in Korea. Mycol Prog 13:477–482
Edel-Hermann V, Lecomte C (2019) Current status of Fusarium oxysporum formae speciales and races. Phytopathology 109:512–530
El-Buni AM, Rattan SS (1981) Check list of Libyan Fungi. Al Faateh Univ., Fac Sci Dept Bot Tripoli, 169 pages
Fernandez J, Rivera-Vargas LI (2008) Leaf blight of onion caused by Pleospora eturmiuna Simm. (teleomorph of Stemphylium eturmiunum) in Puerto Rico. J Agr U Puerto Rico 92:235–239
Foister CE (1961) The economic plant diseases of Scotland. Techn Bull Dept Agric Fish Scotland 1:1–210
French AM (1989) California plant disease host index. Calif. Dept. Food Agric, Sacramento, p 394
Gilardi G, Franco-Ortega S, Gullino ML, Garibaldi A (2018) First report of leaf spot of spinach caused by Stemphylium beticola in Italy. Plant Dis 102:2036
Graf S, Bohlen-Janssen H, Miessner S et al (2016) Differentiation of Stemphylium vesicarium from Stemphylium botryosum as causal agent of the purple spot disease on asparagus in Germany. Eur J Plant Pathol 144:411–418
Hanse B, Raaijmakers EEM, Schoone AHI, van Oorschot PMS (2015) Stemphylium sp., the cause of yellow leaf spot disease in sugar beet (Beta vulgaris L.) in the Netherlands. Eur J Plant Pathol 42:319–330
Hilton S (2000) Canadian plant disease survey. Agric Agri-Food Can 80:151
Hu J, Chen C, Peever T, Dang H, Lawrence C, Mitchell T (2012) Genomic characterization of the conditionally dispensable chromosome in Alternaria arborescens provides evidence for horizontal gene transfer. BMC Genomics 13:171
Inderbitzin P, Mehta YR, Berbee ML (2009) Pleospora species with Stemphylium anamorphs: a four-locus phylogeny resolves new lineages yet does not distinguish among species in the Pleospora herbarum clade. Mycology 101:329–339
Kant P, Materne M, Rodda MS, Slater AT (2017) Screening lentil germplasm for stemphylium blight resistance. Australas Plant Pathol 46:129–136
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Köhl J, Groenenboom-de Haas B, Goossen-van de Geijn H et al (2009) Pathogenicity of Stemphylium vesicarium from different hosts causing brown spot in pear. Euro J Plant Path 124:151
Koike ST, Henderson DM, Butler EE (2001a) Host-specific strain of Stemphylium causes leaf spot disease of California spinach. Calif Agric 55:31–34
Koike ST, Henderson DM, Butler EE (2001b) Leaf spot disease of spinach in California caused by Stemphylium botryosum. Plant Dis 85:126–130
Kurose D, Misawa T, Suzui T et al (2015) Taxonomic re-examination of several Japanese Stemphylium strains based on morphological and molecular phylogenetic analyses. J Gen Plant Pathol 81:358–367
Lawrence DP, Gannibal PB, Peever TL, Pyror BM (2013) The sections of Alternaria: formalizing species-group concepts. Mycologia 105:530–546
Llorente I, Vilardell A, Montesinos E (2006) Infection potential of Pleospora allii and evaluation of methods for reduction of the overwintering inoculum of brown spot of pear. Plant Dis 90:1511–1516
Ma LJ, Geiser DM, Proctor RH, Rooney AP, O'Donnell K, Trail F et al (2013) Fusarium pathogenomics. Annu Rev Microbiol 67:399–416
Marin-Felix Y, Hernández-Restrepo M, Iturrieta-González I, García D, Gené J, Groenewald JZ et al (2019) Genera of phytopathogenic fungi: GOPHY 3. Stud Mycol 94:1–124
Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, Ben M'Barek S et al (2011) Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS microbial Rev 35:542–554
Mehta YR (1998) Severe outbreak of Stemphylium leaf blight, a new disease of cotton in Brazil. Plant Dis 82:333–336
Melnik VA, Pystina KA (1995) Novitates de micromycetibus reservati Svirensis inferioris. Novosti Sist Nizsh Rast 30:29–36
Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S, Matsumae H et al (2016) Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat Genet 48:201
Mendes MAS, da Silva VL, Dianese JC et al (1998) Fungos em Plants no Brasil. Embrapa-SPI/Embrapa-Cenargen, Brasilia, p 555
Mulenko W, Majewski T, Ruszkiewicz-Michalska M (2008) A preliminary checklist of micromycetes in Poland. W. Szafer Institute of Botany. Polish Acad Sci 9:752
Nylander JAA (2009) MrModeltest 2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
Olsen KJK, Rossman A, Andersen B (2018) Metabolite production by species of Stemphylium. Fung Biol 122:172–181
Orieux L, Felix S (1968) List of plant diseases in Mauritius. Phytopathol Pap 7:1–48
Padhi B, Snyder WC (1954) Stemphylium leaf spot of lettuce. Phytopathology 44:175–180
Pande A, Rao VG (1998) A compendium fungi on legumes from India. Scientific Publishers (India), Jodhpur, p 188
Pantidou ME (1973) Fungus-host index for Greece. Benaki Phytopathol Inst, Kiphissia, p 382
Pasquali M, Dematheis F, Gullino ML, Garibaldi A (2007) Identification of race 1 of Fusarium oxysporum f. sp. lactucae on lettuce by inter-retrotransposon sequence-characterized amplified region technique. Phytopathology 97:987–996
Pei Y, Wang Y, Geng Y et al (2011) Three novel species of Stemphylium from Sinkiang, China: their morphological and molecular characterization. Mycol Prog 10:163–173
Poursafar A, Ghosta Y, Javan-Nikkhah M (2016) A taxonomic study on Stemphylium species associated with black (sooty) head mold of wheat and barley in Iran. Mycol Iran 3:99–109
Rahman T, Ahmed AU, Islam MR, Hosen MI (2010) Physical study and both in vitro and in vivo antifungal activities against Stemphylium botryosum causing stemphylium blight disease in lentil (Lens culinaris). Plant Pathol J 9:179–187
Raid RN, Davis RM, Subbarao KV, Raid RN, Kurtz EA (1997) Stemphylium leaf spot. Compendium of lettuce diseases. American Phytopathological Society Press, St. Paul, pp 25–26
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Rotem J, Cohen Y, Wahl I (1966) A new tomato foliage disease in Israel caused by Stemphylium botryosum. Can J Plant Sci 46:265–270
Sampson PJ, Walker J (1982) An annotated list of plant diseases in Tasmania. Department of Agriculture Tasmania, 121 pages
Shaner G, Stromberg EL, Lacy GH et al (1992) Nomenclature and concepts of pathogenicity and virulence. Annu Rev Phytopathol 30:47–66
Shaw CG (1973) Host fungus index for the Pacific northwest - I. Hosts Washington State Univ Agric Exp Sta Bull 765:1–121
Sheikh F, Dehghani H, Aghajani MA (2015) Screening faba bean (Vicia faba L.) genotypes for resistance to Stemphylium blight in Iran. Eur J Pl Pathol 143:677–689
Shishkoff N, Lorbeer JW (1989) Etiology of Stemphylium leaf blight of onion. Phytopathology 79:301–304
Shivas RG (1989) Fungal and bacterial diseases of plants in Western Australia. J Roy Soc W Australia 72:1–62
Simmonds JH (1966) Host index of plant diseases in Queensland. Queensland Department of Primary Industries, Brisbane, p 111
Simmons EG (1985) Perfect states of Stemphylium II. Sydowia 38:284–293
Simmons EG (2001) Perfect states of Stemphylium—IV. Harvard papers in botany 199–208
Singh P, Bugiani R, Cavanni P et al (1999) Purification and biological characterization of host-specific SV-toxins from Stemphylium vesicarium causing brown spot of European pear. Phytopathology 89:947–953
Singh P, Park P, Bugiani R et al (2000) Effects of host-selective SV-toxin from Stemphylium vesicarium, the cause of brown spot of European pear plants, on ultrastructure of leaf cells. J Phytopathol 148:87–93
Šišić A, Baćanović-Šišić J, Al-Hatmi AM, Karlovsky P, Ahmed SA et al (2018) The ‘forma specialis’ issue in Fusarium: a case study in Fusarium solani f. sp. pisi. Sci Rep 8:1252
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313
Swofford DL (2003) PAUP phylogenetic analysis using parsimony (and other methods). Version 4. Sinauer associates, Sunderland
Thompson SM, Tan YP, Shivas RG, Neate SM, Morin L et al (2015) Green and brown bridges between weeds and crops reveal novel Diaporthe species in Australia. Persoonia 35:39
Tianyu Z (2009) Flora Fungorum Sincorum Vol. 31: 26 genera of dematiaceous dictyosporous hyphomycetes excluding Alternaria. Science Press, Beijing 31:231
Tomioka K, Sato T (2011) Fruit rot of sweet pepper caused by Stemphylium lycopersici in Japan. J Gen Plant Pathol 77:342–344
Trigos Á, Mendoza G, Espinoza C et al (2011) The role of macrosporin in necrotic spots. Phytochem Lett 4:122–125
Turland NJ, Wiersema JH, Barrie FR, Greuter W, Hawksworth DL, Herendeen PS, Knapp S et al. (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Glashütten: Koeltz Botanical Books
Vaghefi N, Kikkert JR, Hay FS, Carver GD, Koenick LB, Bolton MD et al (2018) Cryptic diversity, pathogenicity, and evolutionary species boundaries in Cercospora populations associated with Cercospora leaf spot of Beta vulgaris. Fung Biol 122:264–282
Wallroth CFW (1833) Flora cryptogamica Germaniae section 2. J.L. Schrag, Nürnberg
Wang Y, Geng Y, Pei Y, Zhang X (2010) Molecular and morphological description of two new species of Stemphylium from China and France. Mycology 102:708–717
Wells HD, Forbes I, Webb TE, Edwardson JR (1956) Two Stemphylium diseases of blue lupine. Pl Dis Report 40:803–806
White TJ, Bruns T, Lee S, Taylor JL (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ et al (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Whiteside JO (1966) A revised list of plant diseases in Rhodesia. Kirkia 5:87–196
Wilson VE, Brandsberg J (1965) Fungi isolated from diseased lentil seedlings in 1963-1964. Pl Dis Report 49:660–662
Wong DH, Barbetti MJ, Sivasithamparam K (1985) Fungi associated with root rot of subterranean clover in Western Australia. Austral J Exp Agric Anim Husb 25:574–579
Woudenberg JHC, Seidl MF, Groenewald JZ et al (2015) Alternaria section Alternaria: species, formae speciales or pathotypes? Stud Mycol 82:1–21
Woudenberg JHC, Hanse B, Van Leeuwen GCM et al (2017) Stemphylium revisited. Stud Mycol 87:77–103
Yu SH (2001) Korean species of Alternaria and Stemphylium. National Institute of Agricultural Science and Technology. Suwon, Korea, 212 pages
Acknowledgements
We would like to thank Dr. Raechelle Grams, Ms. Encarnacion Adorada, and Ms. Christina Harris, University of Southern Queensland, for excellent technical support. We are very grateful to Professor Roger Shivas and Dr. Yu Pei Tan, Department of Agriculture and Fisheries, Queensland, for constructive discussions.
Funding
This research was funded by the Grains Research and Development Corporation (project DAN00213, DAQ00194 and DAQ00186), the University of Southern Queensland, and the New South Wales Department of Primary Industries.
Author information
Authors and Affiliations
Corresponding author
Additional information
Section Editor: Gerhard Rambold
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vaghefi, N., Thompson, S.M., Kimber, R.B.E. et al. Multi-locus phylogeny and pathogenicity of Stemphylium species associated with legumes in Australia. Mycol Progress 19, 381–396 (2020). https://doi.org/10.1007/s11557-020-01566-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11557-020-01566-8