New records of the fungal species associated with insects in Iran

Document Type : Research Paper

Authors

1 Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Iran.

2 Departement of Plant Pathology, Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Iran.Biotechnology and Bioscience Research Center, Shahid Chamran University of Ahvaz, Iran.

Abstract

Summary
Pathogenic and non-pathogenic fungi growing on insect’s body cansignificantly affect their biology and population. To identify insect-associated fungi, the life stages of the insects, including larva, pupa and adults (alive or dead and helthy), were collected from different habitats in Golestan and Khuzestan Provinces during 2017-2018 and their associated fungi were isolated after surface-sterilization. In this study, 13 various isolates were selected (based on primary morphology) and identified according to morphological and molecular analysis. For molecular identification, the sequences of ITS-nrDNA, tef1a, tub2 and gapdh were obtained, where required for identification. Accordingly, eleven species were identified as follow: Auxarthron kuehnii, Biscogniauxia sp., Cladosporium halotolerans, Curvularia mosaddeghii, Fusarium brachygibbosum, Lasiodiplodia mediterranea, Metarhizium brunneum, Nigrospora gorlenkoana, N. oryzae, N. osmanthi, Petriella guttulata and Phascolomyces articulosus. This study firstly reports the genera of Auxarthron (A. kuehnii) and Phascolomyces (P. articulosus) and the species of L. mediterranea, N. gorlenkoana and N. osmanthi for the mycobiota of Iran. 

Keywords


Rferences
 
Ahmadpour SA, Mehrabi-Koushki M, Farokhinejad R, 2017. Neodidymelliopsis farokhinejadii, a new fungal species from dead branches of trees in Iran. Sydowia 69: 171–182.
Alexopoulos, CJ, Beneke ES, 1962. Laboratory Manual for Introductory Mycology. Burgess Pub. Co, Minneapolis. 199 pp.
Alidadi A, Javan-Nikkhah MJ, Kowsari M, Karami S, 2018. Some species of fungi associated with declined Persian oak trees in Ilam province with emphasis on new records to mycobiota of Iran. Rostaniha 19 (2): 75–91. (In Persian with English abstract).
Araujo JPM, Hughes DP, 2016. Diversity of Entomopathogenic Fungi: Which Groups Conquered the Insect Body. Genetics and Molecular Biology of Entomopathogenic Fungi. Elsevier, Cambridge. 94 pp.
Asadalapour M, Zafari D, Zare R, 2011. Hyphomycetous fungi isolated from insects and their pathogenic effect on colorado beetle in Hamedan province. Iranian Journal of Plant Protection 24 (4): 447–465.
Babaahmadi G, Mehrabi-Koushki M, Hayati J, 2018. Allophoma hayatii sp. nov., an undescribed pathogenic fungus causing dieback of Lantana camara in Iran. Mycological Progress 17 (3): 365–379.
Barron GL, Cain RF, Gilman JC, 1961. A revision of the genus Petriella. Canadian Journal of Botany 39(4): 837–845.
Balasubramanian R, Manocha MS, 1992. Cytosolic and membrane-bound chitinases of two mucoraceous fungi: a comparative study. Canadian Journal of Microbiology 38 (4): 331–338.
Berbee M, 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.
Benny GL, Benjamin RK, 1976. Observations on Thamnidiaceae (Mucorales). Chaetocladium, Cokeromyces, Mycotypha and Phascolomyces. Aliso 8: 391–424.
Beneke ES, Rogers AL, 1996. Medical Mycology and Human Mycoses. Star Publishing Company, Belmont. 239 pp.
Blackwell M, Jones K, 1997. Taxonomic diversity and interactions of insect-associated ascomycetes. Biodiversity and Conservation 6: 689–699.
Boedijn KB, 1958. Notes on the Mucorales of Indonesia. Sydowia 12: 321–362.
Carbone I, Kohn LM, 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556.
Charnley AK, 2003. Fungal pathogens of insects: Cuticle degrading enzymes and toxin. Advances in Botanical Research 40: 241–321.
Currah RS, 1985. Taxonomy of the Onygenales: Arthrodermataceae, Gymnoascaceae, Myxotrichaceae and Onygenaceae. Mycotaxon 24: 1–216.
de Hoog GS, Guarro J, Gene J, Figueras MJ, 2000. Atlas of Clinical Fungi. 2nd edition, Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands. 1126 pp.
Doroodgar A, Khorshidi A, Shajari GR, Tashakkor Z, 2005. Bacterial infection of cockroaches in Kashan hospitals. Feyz 8(4): 30–38.
Ershad D, 2009. Fungi of Iran. 3rd edition, Iranian Research Institute of Plant Protection, Tehran. 531 pp.
Farokhy N, Jokar M, Parsaeiyan M, Derakhshan-Shadmehri A, Masoudi A, 2018. Identification of 30 isolates of the Metarhizium spp. via ITS1-5 / 8S-ITS2 sequence. Applied Biology 31 (1): 228–256.
Ferial P, Elford L, Subramanian G, Abdullah A, 2017. Investigation of entomopathogenic fungi from insects at University of Guyana Turkeyen Campus. Current Trends in Biomedical Engineering & Biosciences 5 (2): 30–34.
Gautam AK, Kant M, Thakur Y, 2013. Isolation of endophytic fungi from Cannabis sativa and study their antifungal potential. Archive of Phytopathology and Plant Protection 46: 627–635.
Gouli V, Gouli S, Marcelino JAP, Skinner M, Parker BL, 2013. Entomopathogenic fungi associated with exotic invasive insect pests in northeastern forests of the USA. Insects 4: 631–645.
Greif MD, Currah RS, 2003. A functional interpretation of the role of the reticuloperidium in whole-ascoma dispersal by arthropods. Mycology Reserches 107: 77–81.
Guarro J, Summerbell RC, Samson RA, 2002. Onygenales: the dermatophytes, dimorphics and keratin degraders in their evolutionary context. Studies in Mycology 47: 1–220.
Gul HT, Saeed S, Khan FZA, 2014. Entomopathogenic fungi as effective insect pest management tactic: A review. Applied Sciences and Business Economics 1: 1018.
Habibi A, Mansouri SM, Sadeghi B. 2018. Fusarium species associated with medicinal plants of Lamiaceae and Asteraceae. Mycologia Iranica 5: 91–101.
Hajizadeh A, Jahanshir A, Abdollahzadeh J, 2015. New records of endophytic fungi isolated from oak trees in Kurdistan province (Iran). Rostaniha 16 (1): 109–122.
Hall TA, 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
Hao Y, Aluthmuhandiram JVS, Chethana KWT, Manawasinghe IS, Li X, et al., 2020. Nigrospora species associated with various hosts from Shandong Peninsula, China. Mycobiology 48(3): 169–183.
Heidari K, Mehrabi-Koushki M, Farokhinejad R, 2018. Curvularia mosaddeghii sp. nov., a novel species from the family Pleosporaceae. Mycosphere 9: 635–646.
Henriques J, Barrento MJ, Bonifácio L, Gomes AA, Lima A, et al., 2014. Factors affecting the dispersion of Biscogniauxia mediterranea in Portuguese cork oak stands. Silva Lusitana 22 (1): 83–97.
Hoog GS, 2005. Hortaeaacidophila a new acid-to lerant black yeast fromlignite. Antonie Van Leeuwenhoek 86: 287–294.
Jena SK, Tayung K, 2013. Endophytic fungal communities associated with two ethno-medicinal plants of Similipal Biosphere Reserve, India and their antimicrobial prospective. Journal of Applied Pharmaceutical Science 3: 7.
Joop G, Vilcinskas A, 2016. Coevolution of parasitic fungi and insect hosts. Zoology 119: 350–358.
Karimpour E, Niknam G, Khodaei S, Arzanlou M, 2021. Morphology and DNA phylogeny differentiate several anamorphic ascomycetes associated with a cereal cyst
nematode, Heterodera filipjevi, and new records for the mycobiota of Iran. Nova Hedwigia 113: 429–451.
Kaczmarek A, Boguś MI, 2021. Fungi of entomopathogenic potential in Chytridiomycota and Blastocladiomycota, and in fungal allies of the Oomycota and Microsporidia. IMA Fungus 12: 29.
Khodadadi-pourarpanei S, Mehrabi-Koushki M, Farokhinejad R, 2019. Contribution to identification of some fungal endophytes associated with the harsh ecosystems of Abadan and Ahvaz. Journal of Applied Research in Plant Protection 8: 49–64.
Kirk PM, Cannon PF, David JC, Stalpers JA, 2001. Ainsworth & Bisby’s Dictionary of the Fungi. 9th edition, CABI Publishing, Wallingford. 655 pp.
Kouvelise VN, Zare R, Bridge PD, Typas MA, 1999. Differentiation of mitochondrial subgroup in the Verticillium lecanii species complex. Letters in Applied Microbiology 28: 263–268.
Lacey LA, Frutos R, Kaya HK, Vail P, 2001. Insect pathogens as biological control agents: do they have a future. Biological Control 21 (3): 230–248.
Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, et al., 2015. Insect pathogens as biological control agents: back to the future. Journal of Invertebrate Pathology 132: 1–41.
Laraba I, McCormick SP, Vaughan MM, Geiser DM, O’Donnell K, 2021. Phylogenetic diversity, trichothecene potential, and pathogenicity within Fusarium sambucinum species complex. PLoS ONE 16: e0245037.
Linaldeddu BT, Deidda A, Scanu B, Franceschini A, Serra S, et al., 2014. Diversity of Botryosphaeriaceae species associated with grapevine and other woody hosts in Italy, Algeria and Tunisia, with descriptions of Lasiodiplodia exigua and Lasiodiplodia mediterranea sp. nov. Fungal Diversity 71: 201–214.
Majchrowicz I, 2004. Species of fungi of the genus Auxarthron on insects. Journal of Invertebrate Pathology 8: 431–432.
Manamgoda DS, Rossman AY, Castlebury LA, Chukeatirote E, Hyde KD, 2015. Taxonomic and phylogenetic re-appraisal of the genus Curvularia (Pleosporaceae): human and plant pathogens. Phytotaxa 212: 175–198.
Mason EW, 1927. On species of the genus Nigrospora Zimmermann recorded on monocotyledons. Transactions of the British Mycological Society 12: 152–165.
Meepagala KM, Becnel JJ, Estep AS, 2015. Phomalactone as the active constituent against mosquitoes from Nigrospora spherica. Agricultural Sciences 6: 1195.
Mehrabi-Koushki M, Bavarsad M, Farokhinejad R, Jamshidi M, Alimohamadi A, 2017. The comparison of ITS-rDNA and tef1α genomic regions for phylogenetic study of some Trichoderma species. Iranian Journal of Plant Protection Science 47: 67–77. (In Persian with English abstract).
Mehrabi-Koushki M, Pooladi P, Eisvand P, Babaahmadi G, 2018. Curvularia ahvazensis and C. rouhanii spp. nov. from Iran. Mycosphere 9: 1173–1186.
Mirabolphathi M, 2013. Outbreak of charcoal disease on Quercus spp. and Zelkova carpinifolia trees in forest of Zagros and Alborz Mountains in Iran. Iranian Journal Plant Pathology 49: 257–263.
Mirhosseini HA, Babaeizad V, Hashemi L, 2014. First report of Fusarium brachygibbosum causing leaf spot on oleander in Iran. Journal of Plant Patholology 96 (2): 431.
Mohammadi H, Sharifi S, 2016. Association of Botryosphaeriaceae and Phaeoacremonium species with insect-damaged quince shoots. Journal of Plant Patholology 98: 35–42.
Nago H, Matsumoto M, Johnson GI, Highley E, Jouce DC, 1997. Lasiodiplodia theobromae and the roles of insects in dispersal of the fungi. An International Workshop, May 18-21, Chiang Mai, Thailand. P. 208–216.
Nemati Mandanipour O, Farokhinejad R, Mehrabi-Koushki M, 2021. Identification of Fusarium species associated with root rot symptoms of the rapeseed in Khuzestan Province. Journal of Applied Research in Plant Protection 10: 31–47.
Nicoletti R, Becchimanzi A, 2022. Ecological and molecular interactions between Insects and Fungi. Microorganisms 10: 96.
O’Donnell K, 1993. Fusarium and ITS near relatives. In: Reynolds DR, Taylor JW (eds). The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics. CABI Publishing, Wallingford. Pp. 225–233.
Padwick GW, 1945. Notes on Indian fungi III. Mycological Papers 12: 1–15.
Pai HH, Chen WC, Peng CF, 2004. Cockroaches as potential vectors of nosocomial infections. Infection Control Hospital Epidemiology 25: 979–984.
Petch T, 1935. Notes on entomogenous fungi. Transactions of the British Mycological Society 19 (3): 161–194.
Raeder U, Broda P, 1985. Rapid preparation of DNA from filamentous fungi. Letters in Applied Microbiology 1: 17–20.
Raimondo ML, Lops F, Carlucci A, 2016. Charcoal canker of pear, pulm, and quince trees caused by Biscogniauxia rosacearum sp. nov. in southern Italy. Plant Diseases 100: 1813–1822.
Saichua P, Pinmai K, Somrithipol S, Torudom S, 2008. Isolation of medically important fungi from cockroaches trapped at Thammasat Chalermprakiat Hospital. Thammasat Medical Journal 8 (3): 345–351.
Samson RA, Brady BL, 1983. Paraisaria, a new genus for Isaria dubia, the anamorph of Cordyceps gracilis. Transactions of the British Mycological Society 81 (2): 285–290.
Samson RA, Evans HC, Latgé J.P, 1988. Taxonomy of entomopathogenic fungi. In: Atlas of entomopathogenic fungi. Springer, Berlin, Heidelberg, Pp. 5–16.
Santos MNS, 2003. Contribution towards the knowledge of the relationship Quercus suber Biscogniauxia mediterranea (syn. Hypoxilon mediterraneum). Silva Lusitana 11 (1): 21–29.
Sharma L, Marques G, 2018. Fusarium, an Entomopathogen-A Myth or Reality? Pathogens 7 (4): 93.
Shoukouhi E, Bissett J, 2008. Preferred primers for sequencing the end of the translation elongation factor 1-alpha gene (EF1-a1) and subunit 2 of the RNA polymerase B gene (RPB2). ISTH, from: http://www.isth.info/methods.
Solé M, Cano J, Guarro J, 2002a. Molecular phylogeny of Amauroascus, Auxarthron, and morphologically similar onygenalean fungi. Mycological Research 106: 388–396.
Sole M, Cano J, Stchigel AM, Guarro J, 2002b. Two new species of Auxarthron morphologically and genetically close to A. kuehnii. Studies in Mycology 47: 103–110.
Thalavaipandian A, Ramesh V, Bagyalakshmi V, 2011. Diversity of fungal endophytes in medicinal plants of Courtallam hills, Western Ghats, India. Mycosphere 2: 575–582.
Tadych M, Bergen M, Johnson JC, Polashock J, Vorsa N, 2012. Endophytic and pathogenic fungi of developing cranberry ovaries from flower to mature fruit: diversity and succession. Fungal Diversity 54: 101–116.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.
Wang C, Wang S, 2017. Insect pathogenic fungi: genomics, molecular interactions and genetic improvements. Annual Review of Entomology 62: 73–90.
Wang M, Liu F, Crous PW, Cai L, 2017. Phylogenetic reassessment of Nigrospora: Ubiquitous endophytes, plant and human pathogens. Persoonia 39: 118–142.
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, White TJ (eds). PCR Protocols: A Guide to Methods and Applications. Academic Press, New York. Pp. 315–322.
Woudenberg JHC, Aveskamp MM, de Gruyter J, Spiers AG, Crous PW, 2009. Multiple Didymella teleomorphs are linked to the Phoma clematidina morphotype. Persoonia 22: 56–62.
Wu SH, Che, YW, Sha, SC, 2009. Two new solanapyrone analogues from the endophytic fungus Nigrospora sp. YB‐141 of Azadirachta indica. Chemistry & Biodiversity 6: 79–85.
Yuanyuan H, Aluthmuhandiram JVS, Chethana KWT, Manawasinghe IS, Li X, Liu M, et al., 2020. Nigrospora species associated with various hosts from shandong peninsula, China. Mycobiology 48: 169–183.
Zalar P, de Hoog GS, Schroers HJ, Crous PW, Groenewald JZ, et al., 2007. Phylogeny and ecology of the ubiquitous saprobe Cladosporium sphaerospermum, with descriptions of seven new species from hypersaline environments. Studies in Mycology 58: 157–183.
Zebold SL, Whisler HC, Shemanchuk J, Travland LB, 1979. Host specificty and penetration in the mosquito pathogen Coelomomyces psorophorae. Canadian Journal of Botany 57(24): 2766–2770.
Zibarova L, Kout J, 2017. Xylariaceous pyrenomycetes from Bohemia: species of Biscogniauxia and Hypoxylon new to the Czech Republic, and notes on other rare species. Czech Mycology 69 (1): 77–108.