Abstract
During 2016 and 2017, surveys for leaf diseases were conducted across several corn fields in Algiers (north) and Ghardaïa (south) regions, Algeria. Leaves samples exhibiting leaf spots were collected for recovering the potential fungal pathogens associated with the symptoms. Seventy isolates were recovered from the samples and characterized using phylogenetic, morphological, and pathogenic features. The isolates were morphologically grouped into two genera: Exserohilum and Bipolaris. Based on ITS, GAPDH, and RPB2 sequence data, Exserohilum isolates were identified as E. rostratum and E. monoceras, while Bipolaris isolates were identified as B. sorokiniana, B. microlaenae, and B. omanensis. Pathogenicity test was carried out under greenhouse conditions using the susceptible corn cultivars “Giza 352” and “Qing Qing 300.” B. sorokiniana caused light green to grayish leaf spots with rounded or irregular margins (0.2–0.5 × 0.2–0.4 mm); some lesions were circular to oval, white–gray with brown margins, surrounded by yellow-green halo (0.3–2.5 × 0.3–1.3 mm). B. microlaenae induced grayish-white or light brown leaf spots, encircled by a reddish border (0.25–0.94 × 0.1–0.52 mm). B. omanensis caused irregular, circular or oval necrotic spots, whitish gray in color and surrounded by a dark brown border (0.4–1.2 × 0.2–0.7 mm). E. rostratum caused grayish brown lesions (0.2–5.0 × 0.2–1.5 mm), which may develop to form tan to dark brown necrotic streaks. Finally, E. monoceras induced grayish or tan lesions (0.2–0.5 × 0.1–0.4 mm), surrounded by yellow or orange halo. The lesions elongated parallel to the veins and may coalesce to form long gray streaks. To our knowledge, this is the first report of these five fungal species associated with corn leaf spots in Algeria. Furthermore, B. microlaenae and B. omanensis are recorded for the first time in the world as causal agents of leaf spot diseases in corn.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Not applicable.
Code availability
Not applicable.
References
Ahmadpour A, Karami S, Heidarian Z, Javan-Nikkhah M (2013) Exserohilum rostratum causing sugarcane leaf spot in Iran. Aust Plant Dis Notes 8:97–99. https://doi.org/10.1007/s13314-013-0105-y
Alcorn JL (1983) Generic concepts in Drechslera, Bipolaris and Exserohilum. Mycotaxon 17:1–86
Alcorn JL (1988) The taxonomy of “Helminthosporium” species. Annu Rev Phytopathol 26:37–56. https://doi.org/10.1146/annurev.py.26.090188.000345
Alcorn JL (1990) Additions to Cochliobolus, Bipolaris and Curvularia. Mycotaxon 39:361–392
Amaradasa BS, Madrid H, Crous PW, Amundsen K (2014) Porocercospora seminalis gen. et comb. nov., the causal organism of buffalograss false smut. Mycologia 106:77–85. https://doi.org/10.3852/13-147
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. https://doi.org/10.1080/00275514.1999.12061106
Bhunjun CH, Dong Y, Jayawardena RS, Jeewon R, Phukhamsakda C, Bundhun D, Hyde D, Sheng J (2020) A polyphasic approach to delineate species in Bipolaris. Fungal Divers 102:225–256. https://doi.org/10.1007/s13225-020-00446-6
Burges GE, Walls CT, Maize JC (1987) Subcutaneous phaeohyphomycosis caused by Exserohilum rostratum in an immunocompetent host. Arch Dermatol 123:1346–1350. https://doi.org/10.1001/archderm.1987.01660340108030
Contidíaz IA, Vargas R, Apolo A, Moraña JA, Pedrana G, Cardozo E, Almeida E (2003) Mycotic bovine nasal granuloma. Rev Inst Med Trop Sao Paulo 45(3):163–166. https://doi.org/10.1590/S0036-46652003000300009
Chung YR, Kim BS, Kim HT, Cho KY (1990) Identification of Exserohilum species, a fungal pathogen causing leaf blight of barnyardgrass (Echinochloa crus-galli). Plant Pathol J 6:429–433
Dettman JR, Jacobson DJ, Taylor JW (2003) A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57:2703–2720. https://doi.org/10.1111/j.0014-3820.2003.tb01514.x
Dughaishi S, Maharachchikumbura SSN, Al-Sadi AM (2018) Bipolaris omanensis, a novel saprobic species of Bipolaris from Oman based on morphology and sequence data. Phytotaxa 385(1): 023–030. https://doi.org/10.11646/phytotaxa.385.1.3
Duveiller E, Gilchrist LI (1994) Production constraints due to Bipolaris sorokiniana in wheat: current situation and future prospects. Proceedings of the CIMMYT/UNDP workshop, Nashipur (Dinajpur), Bangladesh, February 1994, 343–345
Edler D, Klein J, Antonelli A, Silvestro D (2019) raxmlGUI 2.0 beta: a graphical interface and toolkit for phylogenetic analyses using RAxML. bioRxiv. https://doi.org/10.1101/800912
Ellis MB (1971) Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew, England
FAOSTAT Statisical Database (2020) http://www.fao.org/faostat/en/#data/QC. Accessed 15 Jun 2020
Farr DF, Rossman AY (2017) Fungal databases, U.S. National Fungus Collections, ARS, USDA. https://nt.ars-grin.gov/fungaldatabases/. Accessed 12 May 2020
Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323
Heidarian Z, Arzanlou M, Babaei-ahari A, Ahmadpour A (2016) Phenotypic and molecular characterization of Exserohilum species from Iran. Nova Hedwigia 103(3–4):327–338. https://doi.org/10.1127/nova_hedwigia/2016/0353
Hernández-Restrepo M, Madrid H, Tan YP, da Cunha KC, Gené J, Guarro J, Crous PW (2018) Multi-locus phylogeny and taxonomy of Exserohilum. Persoonia 41:71–108. https://doi.org/10.3767/persoonia.2018.41.05
Ho WC (1944) Soil-lnhabiting Fungi Attacking the Roots of Maize. Agricultural Experiment Station, Iowa State College of Agriculture and Mechanic Arts., Research Bulletin 332
Ito S (1930) On some new ascigerous stages of the species of Helminthosporium parasitic on cereals. Proc Imperial Acad 6:352–355. https://doi.org/10.2183/pjab1912.6.352
Jeewon R, Hyde KD (2016) Establishing species boundaries and new taxa among fungi: recommendations to resolve taxonomic ambiguities. Mycosphere 7:1669–1677. https://doi.org/10.5943/mycosphere/7/11/4
Katoh K, Standley 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
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
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
Leonard KJ, Suggs EG (1974) Setosphaeria prolata, the ascigerous state of Exserohilum prolatum. Mycologia 66:281–297. https://doi.org/10.1080/00275514.1974.12019603
Leonard KJ, Thakur RP, Leath S (1988) Incidence of Bipolaris and Exserohilum species in corn leaves in North Carolina. Plant Dis 72:1034–1038. https://doi.org/10.1094/PD-72-1034
Lin SH, Huang SL, Li QQ, Hu CJ, Fu G, Qin LP, Ma YF, Xie L, Cen ZL, Yan WH (2011) Characterization of Exserohilum rostratum, a new causal agent of banana leaf spot disease in China. Australas Plant Pathol 40:246–259. https://doi.org/10.1007/s13313-011-0037-y
Luttrell ES (1963) Taxonomic criteria in Helminthosporium. Mycologia 55:643–674. https://doi.org/10.2307/3756441
Luttrell ES (1964) Morphology of Trichometasphaeria turcica. Am J Bot 51:213–219. https://doi.org/10.2307/2440108
Madrid H, da Cunha KC, Gené J, Dijksterhuis J, Cano J, Sutton DA, Guarro J, Crous PW (2014) Novel Curvularia species from clinical specimens. Persoonia 33:48–60. https://doi.org/10.3767/003158514X683538
Majeed RA, Shahid AA, Liaqat GA, Saleem K, Asif M, Shafiq M, Haider MS, Noreen M (2016) First report of Setosphaeria rostrata causing brown leaf spot of rice in Pakistan. Plant Disease Notes Vol. 100, No 10. https://doi.org/10.1094/PDIS-02-16-0220-PDN
Manamgoda DS, Cai L, McKenzie EHC, Crous PW, Madrid H, Chukeatirote E, Shivas RG, Tan YP, Hyde KD (2012) A phylogenetic and taxonomic re-evaluation of the Bipolaris-Cochliobolus-Curvularia Complex. Fungal Divers 56:131–144. https://doi.org/10.1007/s13225-012-0189-2
Manamgoda DS, Rossman AY, Castlebury LA, Crous PW, Madrid H, Chukeatirote E, Hyde KD (2014) The genus Bipolaris. Stud Mycol 79:221–288. https://doi.org/10.1016/j.simyco.2014.10.002
Manamgoda DS, Rossman AY, Castlebury LA, Chukeatirote E, Hyde KD (2015) A taxonomic and phylogenetic re-appraisal of the genus Curvularia (Pleosporaceae): human and plant pathogens. Phytotaxa 212: 175–198. https://doi.org/10.11646/phytotaxa.212.3.1
Marin-Felix Y, Senwanna C, Cheewangkoon R, Crous PW (2017) New species and records of Bipolaris and Curvularia from Thailand. Mycosphere 8(9):1556–1574. https://doi.org/10.5943/mycosphere/8/9/11
Ning G, Xuan N, Jie S, Jing-yu M, Chun-sheng X, Jie S (2017) The occurrence and pathogen identification of leaf spot on maize. Acta Phytopathologica Sinica 47(1):1–8
Nylander JAA (2004) MrModeltest v. 2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
O’Donnell K, Sarver BAJ, Brandt M, Chang DC, Noble-Wang J, Park BJ, Sutton DA, Benjamin L, Lindsley M, Padhye A, Geiser DM, Ward TJ (2007) Phylogenetic diversity and microsphere array-based genotyping of humanpathogenic fusaria including isolates from the 2005–06 multistate contactlens-associated U.S. keratitis outbreaks. J Clin Microbiol 45:2235–2248. https://doi.org/10.1128/JCM.00533-07
Rambaut A, Drummond A (2008) FigTree: tree figure drawing tool, version 1.2.2. Institute of Evolutionary Biology, University of Edinburgh, UK
Ranum P, Pena-Rosas JP, Garcia-Casal MN (2014) Global maize production, utilization, and consumption. Ann N Y Acad Sci 1312:105–112. https://doi.org/10.1111/nyas.12396
Raza M, Zhang ZF, Hyde KD, Diao YZ, Cai L (2019) Culturable plant pathogenic fungi associated with sugarcane in southern China. Fungal Divers 99:1–104. https://doi.org/10.1007/s13225-019-00434-5
Robert AL (1953) Some of the leaf blights of corn. Year Book of Agriculture, United States Department of Agriculture, North Carolina, pp 380–385. https://naldc.nal.usda.gov/download/IND43894350/PDF
Ronquist F, Teslenko M, Van der Mark P, Ayres D, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Saint-Jean M, St-Germain G, Laferrière C, Tapiero B (2007) Hospital acquired phaeohyphomycosis due to Exserohilum rostratum in a child with leukemia. Can J Infect Dis Med Microbiol 18(3):200–202. https://doi.org/10.1155/2007/384743
Shoemaker RA (1959) Nomenclature of Drechslera and Bipolaris, grass parasites segregated from “Helminthosporium”. Can J Bot 37:879–887. https://doi.org/10.1139/b59-073
Sivanesan A (1987) Graminicolous species of Bipolaris, Curvularia, Drechslera, Exserohilum and their teleomorphs. Myc Papers 158:1–261. https://doi.org/10.2307/3759472
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Tan YP, Crous PW, Shivas RG (2016) Eight novel Bipolaris species identified from John L. Alcorn’s collections at the Queensland Plant Pathology Herbarium (BRIP). Mycol Prog 15:1203–1214. https://doi.org/10.1007/s11557-016-1240-6
Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21–32. https://doi.org/10.1006/fgbi.2000.1228
Tsai JN, Tsai WH, Chen JL (2001) Pathogenicity of Exserohilum rostratum on corn and weeds in the corn fields. Plant Pathol Bulletin 10:181–186
Ullstrup AJ (1972) The impacts of the southern corn leaf blight epidemics of 1970–1971. Annu Rev Phytopathol 10:37–50. https://doi.org/10.1146/annurev.py.10.090172.000345
Zhang W, Watson AK (1997) Host range of Exserohilum monoceras, a potential bioherbicde for the control of Echinochloa species. Can J Bot 75:685–692. https://doi.org/10.1139/b97-077
Acknowledgements
We express our gratitude to Prof. Pedro W. Crous and Dr. Ewald Gronewald from the Fungal Biodiversity Institute, Netherlands, for their precious contribution, by conducting sequencing of ITS, GAPDH, and RPB2 regions provided in this study. We thank Mr. Messaoud Bellaragueb and Mr. Kaddour Chenina from the Directorate of Agricultural Services (DSA) of Ghardaïa, Mr. Hakim Hassnaoui from the DSA of Boumerdès, and the National Institute of the Agronomic Research (INRAA), experimental station of Adrar, Algeria, for their logistical support during the surveys.
Author information
Authors and Affiliations
Contributions
Mr. Abdenour Zibani carried out the experiment and phylogenetic analyses, and he wrote the manuscript under the supervision of Dr. Hamida Benslimane. Dr. Shaukat Ali reviewed and conducted a critical revision of the manuscript. Dr. Hamida Benslimane has supervised the project; she conceived the study and was in charge of overall direction and planning.
Corresponding author
Ethics declarations
Conflicts of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Ethics approval
Not applicable.
Additional information
Communicated by Á. Mesterházy.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zibani, A., Ali, S. & Benslimane, H. Corn diseases in Algeria: first report of three Bipolaris and two Exserohilum species causing leaf spot and leaf blight diseases. CEREAL RESEARCH COMMUNICATIONS 50, 449–461 (2022). https://doi.org/10.1007/s42976-021-00192-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42976-021-00192-8