Skip to main content
SpringerLink
Log in

Appressorial interactions with host and their evolution

  • Review
  • Published:
Fungal Diversity Aims and scope Submit manuscript

Abstract

Fungi have evolved diverse strategies to acquire nutrients as endophytes, saprobes, symbionts, or pathogens. Appressoria have been intensively studied due to their importance in attaching and breaching the host surface. These specialized infection structures have evolved into various morpho-types: proto-appressoria, hyaline appressoria, melanized (dark) appressoria, and compound appressoria. In this review, we discuss the differences in the formation, differentiation, and function of appressoria among fungi with diverse life strategies. Using DNA sequence information, LSU, 5.8S, SSU and rpb2 gene fragments, we reconstructed the ancestral states for appressorial types in the main phyla of fungi and fungus-like organisms and found that the hyaline appressoria was the most ancestral form. Our analysis estimated proto-appressoria diversification during the Mesozoic period (92–239 million years ago), however, its origin remains inconclusive. Our data suggest that these hyaline appressoria diversified into melanized or compound appressoria, with evidence of adaptive radiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aist JR, Bushnell WR (1991) Invasion of plants by powdery mildew fungi, and cellular mechanisms of resistance. The fungal spore and disease initiation in plants and animals. Springer, Boston, MA, pp 321–345

    Chapter  Google Scholar 

  • Allen EA (1991) Appressorium formation in response to topographical signals by 27 rust species. Phytopathology 81:323–331

    Article  Google Scholar 

  • Alves JL, Santos-Seixas CD, Rodrigues FA, Barreto RW (2014) Production of viable and infective inoculum of Coccodiella miconiae (Ascomycota: Phyllachoraceae) for the biological control of Miconia calvescens. Biol Control 79:16–23

    Article  Google Scholar 

  • Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer KM, Pradier J-M, Quévillon E, Sharon A, Simon A, ten Have A, Tudzynski B, Tudzynski P, Wincker P, Andrew M, Anthouard V, Beever RE, Beffa R, Benoit I, Bouzid O, Brault B, Chen Z, Choquer M, Collémare J, Cotton P, Danchin EG, da Silva C, Gautier A, Giraud C, Giraud T, Gonzalez C, Grossetete S, Güldener U, Henrissat B, Howlett BJ, Kodira C, Kretschmer M, Lappartient A, Leroch M, Levis C, Mauceli E, Neuvéglise C, Oeser B, Pearson M, Poulain J, Poussereau N, Quesneville H, Rascle C, Schumacher J, Ségurens B, Sexton A, Silva E, Sirven C, Soanes DM, Talbot NJ, Templeton M, Yandava C, Yarden O, Zeng Q, Rollins JA, Lebrun M-H, Dickman M (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7:e1002230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armentrout VN (1987) Factors affecting infection cushion development by Rhizoctonia solani on cotton. Phytopathology 77:623–630

    Article  Google Scholar 

  • Askary H, Yarmand H (2007) Development of the entomopathogenic hyphomycete Lecanicillium muscarium (Hyphomycetes: Moniliales) on various hosts. Eur J Entomol 104:67–72

    Article  Google Scholar 

  • Assante G, Maffi D, Saracchi M, Farina G, Moricca S, Ragazzi A (2004) Histological studies on the mycoparasitism of Cladosporium tenuissimum on urediniospores of Uromyces appendiculatus. Mycol Res 108:170–182

    Article  PubMed  Google Scholar 

  • Au DWT, Jones EBG, Moss ST, Hodgkiss IJ (1996) The role of mucilage in the attachment of conidia, germ tubes, and appressoria in the saprobic aquatic Hyphomycetes Lemonniera aquatica and Mycocentrospora filiformis. Can J Bot 74:1789–1800

    Article  Google Scholar 

  • Babu AM, Philip T, Kariappa BK, Kamble CK (2009) Scanning electron microscopy of the infection process of Cercospora henningsii on cassava leaves. J Phytopathol 157:57–62

    Article  Google Scholar 

  • Backhouse D, Willetts HJ (1987) Development and structure of infection cushions of Botrytis cinerea. Trans Brit Mycol Soc 89:89–95

    Article  Google Scholar 

  • Bailey JA, O’connell RJ, Pring RJ, Nash C (1992) Infection strategies of Colletotrichum species. In: Bailey JA, Jeger MJ (eds) Colletotrichum: Biology, Pathology and Control fection strategies of Colletotrichum species, CABI International, Wallingford, UK, 88–120

  • Balcì Y, Halmschlager E (2003) Phytophthora species in oak ecosystems in Turkey and their association with declining oak trees. Plant Pathol 52:694–702

    Article  Google Scholar 

  • Barkai-Golan R (2001) Postharvest disease initiation. In: Barkai-Golan R (ed) Postharvest diseases of fruits and vegetables. Elsevier, Amsterdam, The Netherlands, pp 3–24

    Chapter  Google Scholar 

  • Bastmeyer M, Deising HB, Bechinger C (2002) Force exertion in fungal infection. Annu Rev Biophys Biomol Struct 31:321–341

    Article  CAS  PubMed  Google Scholar 

  • Bechinger C, Giebel KF, Schnell M, Leiderer P, Deising HB, Bastmeyer M (1999) Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285:1896–1899

    Article  CAS  PubMed  Google Scholar 

  • Becker M, Becker Y, Green K, Scott B (2016) The endophytic symbiont Epichloë festucae establishes an epiphyllous net on the surface of Lolium perenne leaves by development of an expressorium, an appressorium-like leaf exit structure. New Phytol 211:240–254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benito EP, Ten Have A, van't Klooster JW, van Kan JA (1998) Fungal and plant gene expression during synchronized infection of tomato leaves by Botrytis cinerea. Eur J Plant Pathol 104:207–220

    Article  CAS  Google Scholar 

  • Boenisch MJ, Schäfer W (2011) Fusarium graminearum forms mycotoxin producing infection structures on wheat. BMC Plant Biol 11:110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boesewinkel HJ (1980) The morphology of the imperfect states of powdery mildews (Erysiphaceae). Bot Rev 46:167–224

    Article  Google Scholar 

  • Borah N, Albarouki E, Schirawski J (2018) Comparative methods for molecular determination of host-specificity factors in plant-pathogenic fungi. Int J Mol Sci 19:863

    Article  PubMed Central  CAS  Google Scholar 

  • Braun U, Cook RTA, Inman AJ, Shin HD (2002) The taxonomy of the powdery mildew fungi. In: Bélanger RR, Bushnell WR, Dik AJ, Carve TLW (eds) The powdery mildews: a comprehensive treatise. APS Press, St. Paul, US, pp 13–55

    Google Scholar 

  • Brobyn PJ, Wilding N (1977) Invasive and developmental processes of Entomophthora species infecting aphids. Trans Brit Mycol Soc 69:349–366

    Article  Google Scholar 

  • Brun S, Silar P (2010) Convergent evolution of morphogenetic processes in fungi. Evolutionary biology—concepts, molecular and morphological evolution. Springer, Berlin, pp 317–328

    Chapter  Google Scholar 

  • Brun S, Malagnac F, Bidard F, Lalucque H, Silar P (2009) Functions and regulation of the nox family in the filamentous fungus Podospora anserina: A new role in cellulose degradation. Mol Microbiol 74:480–496

    Article  CAS  PubMed  Google Scholar 

  • Brunauer G, Blaha J, Hager A, Turk R, Stocker-Wörgötter E, Grube M (2007) An isolated lichenicolous fungus forms lichenoid structures when co-cultured with various coccoid algae. Symbiosis 44:127–136

    CAS  Google Scholar 

  • Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016) Entomopathogenic fungi: new insights into host-pathogen interactions. Adv Genet 94:307–364

    Article  CAS  PubMed  Google Scholar 

  • Caires NP, Rodrigues FA, Furtado GQ (2015) Infection process of Botrytis cinerea on eucalyp leaves. J Phytopathol 163:604–611

    Article  Google Scholar 

  • Cano-Dominguez N, Alvarez-Delfin K, Hansberg W, Aguirre J (2008) NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot Cell 7:1352–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capella-Gutiérrez S, Silla-Martínez JM, Gabaldon T (2009) TrimAl: ´ a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carnegie AJ, Ades PK (2003) Mycosphaerella leaf disease reduces growth of plantation-grown Eucalyptus globulus. Aust Forestry 66:113–119

    Article  Google Scholar 

  • Chang HX, Miller LA, Hartman GL (2014) Melanin-independent accumulation of turgor pressure in appressoria of Phakopsora pachyrhizi. Phytopathology 104:977–984

    Article  PubMed  Google Scholar 

  • Chen WQ, Gardner DE, Webb DT (1996) Biology and life cycle of Atelocauda koae, an unusual demicyclic rust. Mycoscience 37:91–98

    Article  Google Scholar 

  • Chen C, Wang J, Luo Q, Yuan S, Zhou M (2007) Characterization and fitness of carbendazim-resistant strains of Fusarium graminearum (wheat scab). Pest Manag Sci 63:1201–1207

    Article  CAS  PubMed  Google Scholar 

  • Chethana KWT, Jayawardena RS, Hyde KD (2020) Hurdles in fungal taxonomy: effectiveness of recent methods in discriminating taxa. Megataxa 1:114–122

    Google Scholar 

  • Chethana KWT, Jayawardena RS, Chen YJ, Konta S, Tibpromma S, Abeywickrama PD, Gomdola D, Balasuriya A, Xu J, Lumyong S, Hyde KD (2021) Diversity and function of appressoria. Pathogens 10:746

    Article  PubMed  PubMed Central  Google Scholar 

  • Chetia H, Kabiraj D, Bharali B, Ojha S, Barkataki MP, Saikia D, Singh T, Mosahari PV, Sharma P, Bora U (2019) Exploring the benefits of endophytic fungi via omics. Singh BP, Advances in endophytic fungal research: present status and future challenges. Springer, Cham, Switzerland, pp 51–81

    Chapter  Google Scholar 

  • Cho EM, Kirkland BH, Holder DJ, Keyhani NO (2007) Phage display cDNA cloning and expression analysis of hydrophobins from the entomopathogenic fungus Beauveria (Cordyceps) bassiana. Microbiology 153:3438e3447.

  • Choi W, Dean RA (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973–1983

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choquer M, Fournier E, Kunz C, Levis C, Pradier J-M, Simon A, Viaud M (2007) Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol Lett 277:1–10

    Article  CAS  PubMed  Google Scholar 

  • Choquer M, Rascle C, Gonçalves I, de Vallée A, Ribot C, Loisel E, Smilevski P, Ferria J, Savadogo M, Souibgui E, Gagey MJ, Dupuy JW, Rollins JA, Marcato M, Noûs C, Bruel C, Poussereau N (2021) The infection cushion of Botrytis cinerea: a fungal ‘weapon’ of plant-biomass destruction. Environ Microbiol 23:2293–2314

    Article  CAS  PubMed  Google Scholar 

  • Christiansen SK, Smedegaard V (1990) Microscopic studies of the interaction between barley and the saprophytic fungus, Cladosporium macrocarpum. J Phytopathol 128:209–219

    Article  Google Scholar 

  • Clay RP, Enkerli J, Fuller MS (1994) Induction and formation of Cochliobolus sativus appressoria. Protoplasma 178:34–47

    Article  Google Scholar 

  • Cleary MR, Daniel G, Stenlid J (2013) Light and scanning electron microscopy studies of the early infection stages of Hymenoscyphus pseudoalbidus on Fraxinus excelsior. Plant Pathol 6:1294–1301

    Article  Google Scholar 

  • Clement JA, Butt TM, Beckett A (1993a) Characterization of the extracellular matrix produced in vitro by urediniospores and sporelings of Uromyces viciae-fabae. Mycol Res 97:594–602

    Article  Google Scholar 

  • Clement JA, Martin SG, Porter R, Butt TM, Beckett A (1993b) Germination and the role of extracellular matrix in adhesion of urediniospores of Uromyces viciae-fabae to synthetic surfaces. Mycol Res 97:585–593

    Article  Google Scholar 

  • Coertze S, Holz G, Sadie A (2001) Germination and establishment of infection on grape berries by single airborne conidia of Botrytis cinerea. Plant Dis 85:668–677

    Article  CAS  PubMed  Google Scholar 

  • Cook RTA, Braun U (2009) Conidial germination patterns in powdery mildews. Mycol Res 113:616–636

    Article  CAS  PubMed  Google Scholar 

  • Cook RTA, Braun U, Beales PA (2011) Development of appressoria on conidial germ tubes of Erysiphe species. Mycoscience 52:183–197

    Article  Google Scholar 

  • Cousin A, Mehrabi R, Guilleroux M, Dufresne M, van der Lee T, Waalwijk C, Langin T, Kema GHJ (2006) The MAP kinase-encoding gene MgFus3 of the non-appressorium phytopathogen Mycosphaerella graminicola is required for penetration and in vitro pycnidia formation. Mol Plant Pathol 7:269–278

    Article  CAS  PubMed  Google Scholar 

  • Crespo A, Divakar PK, Hawksworth DL (2011) Generic concepts in parmelioid lichens, and the phylogenetic value of characters used in their circumscription. Lichenologist 43:511

    Article  Google Scholar 

  • Custódio FA, Firmino AL, Pereira OL (2018) A new species of Rosenscheldia (Dothideomycetes) from Brazil. Forest Pathol 49:e12472

  • Damm U, Cannon PF, Woudenberg JH, Crous PW (2012) The Colletotrichum acutatum species complex. Stud Mycol 73:37–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Damm U, Sato T, Alizadeh A, Groenewald JZ, Crous PW (2019) The Colletotrichum dracaenophilum, C. ámagnum and C. áorchidearum species complexes. Stud Mycol 92:1–46

    Article  CAS  PubMed  Google Scholar 

  • Daniels A, Lucus JA, Peberdy JF (1991) Morphology and ultrastructure of W and R pathotypes of Pseudocercosporella herpotrichoides on wheal seedlings. Mycol Res 95:385–397

    Article  Google Scholar 

  • de Jong JC, McCormack BJ, Smirnoff N, Talbot NJ (1997) Glycerol generates turgor in rice blast. Nature 389:244–244

    Article  CAS  Google Scholar 

  • de Silva NI, Lumyong S, Hyde KD, Bulgakov T, Phillips AJL, Yan JY (2016) Mycosphere essays 9: defining biotrophs and hemibiotrophs. Mycosphere 7:545–559

    Article  Google Scholar 

  • Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, Nicol R, Purcell S, Nusbaum C, Galagan JE, Birren BW (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–986

    Article  CAS  PubMed  Google Scholar 

  • Deising H, Siegrist J (1995) Chitin deacetylase activity of the rust Uromyces viciae-fabae is controlled by fungal morphogenesis. FEMS Microbiol Lett 127:207–211

    Article  CAS  Google Scholar 

  • Deising H, Rauscher M, Haug M, Heiler S (1995) Differentiation and cell wall degrading enzymes in the obligately biotrophic rust fungus Uromyces viciae-fabae. Can J Bot 73:S624–S631

    Article  CAS  Google Scholar 

  • Deising HB, Werner S, Wernitz M (2000) The role of fungal appressoria in plant infection. Microbes Infect 2:1631–1641

    Article  CAS  PubMed  Google Scholar 

  • Demoor A, Silar P, Brun S (2019) Appressorium: the breakthrough in Dikarya. J Fungi 5:72

    Article  CAS  Google Scholar 

  • DeZwaan TM, Carroll AM, Valent B, Sweigard JA (1999) Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive surface cues. Plant Cell 11:2013–2030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhevan V (1998) The infection of rose and holly by the pathogenic fungus Pestalotiopsis guepinii. Master’s thesis, Stephen F. Austin State University

  • di Pietro A, Roncero MIG (1998) Cloning, expression, and role in pathogenicity of pg1 encoding the major extracellular endopolygalacturonase of the vascular wilt pathogen Fusarium oxysporum. Mol Plant Microbe Interact 11:91–98

    Article  PubMed  Google Scholar 

  • Divakar PK, Kauff F, Crespo A, Leavitt SD, Lumbsch HT (2013) Understanding phenotypical character evolution in parmelioid lichenized fungi (Parmeliaceae, Ascomycota). PLoS ONE 8:e83115

  • Dixon KP, Xu JR, Smirnoff N, Talbot NJ (1999) Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11:2045–2058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doss RP, Potter SW, Soeldner AH, Christian JK, Fukunaga LE (1995) Adhesion of germlings of Botrytis cinerea. Appl Environ Microbiol 61:260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dyakov YT, Dzhavakhiya VG, Korpela T (2007) Molecular basis of plant immunization. In: Dzhavakhiya VG, Korpela T (eds) Dyakov YT. Comprehensive and molecular phytopathology, Elsevier, pp 423–438

    Google Scholar 

  • Emmett RW, Parbery DG (1975) Appressoria. Annu Rev Phytopathol 13:147–165

    Article  Google Scholar 

  • Epstein L, Kaur S, Goins T, Kwon YH, Henson JM (1994) Production of hyphopodia by wild-type and three transformants of Gaeumannomyces graminis var. graminis. Mycologia 86:72

  • Everts KL, Lacy ML (1996) Factors influencing infection of onion leaves by Alternaria porri and subsequent lesion expansion. Plant Dis 80:276–280

    Article  Google Scholar 

  • Fan Y, Fang W, Guo S, Pei X, Zhang Y, Xiao Y, Li D, Jin K, Bidochka MJ, Pei Y (2007) Increased insect virulence in Beauveria bassiana strains overexpressing an engineered chitinase. Appl Environ Microbiol 73:295e302

  • Firmino AL, Inácio CA, Pereira OL, Dianese JC (2016) Additions to the genera Asterolibertia and Cirsosia (Asterinaceae, Asterinales), with particular reference to species from the Brazilian Cerrado. IMA Fungus 7:9–28

    Article  PubMed  PubMed Central  Google Scholar 

  • Fortuna P, Citernesi S, Morini S, Giovannetti M, Loreti F (1992) Infectivity and effectiveness of different species of arbuscular mycorrhizal fungi in micropropagated plants of Mr S 2/5 plum rootstock. Agronomie 12:825–829

    Article  Google Scholar 

  • Fourie JF, Holz G (1995) Initial infection processes by Botrytis cinerea on nectarine and plum fruit and the development of decay. Phytopathology 85:82–87

    Article  Google Scholar 

  • Francis SA, Dewey FM, Gurr SJ (1996) The role of cutinase in germling development and infection by Erysiphe graminis f. sp. hordei. Physiol Mol Plant Pathol 49:201–211

    Article  CAS  Google Scholar 

  • Frank B (1883) Ueber einige neue und weniger bekannte Pflanzenkrankheiten. Ber Deut Bot Ges 1:29–34

    Google Scholar 

  • Frias M, Gonzalez C, Brito N (2011) BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol 192:483–495

    Article  CAS  PubMed  Google Scholar 

  • Fröhlich J, Hyde KD (1999) Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodivers Conserv 8:977–1004

    Article  Google Scholar 

  • Gao S, Choi GH, Shain L, Nuss DL (1996) Cloning and targeted disruption of enpg-1, encoding the major in vitro extracellular endopolygalacturonase of the chestnut blight fungus, Cryphonectria parasitica. Appl Environ Microb 62:1984–1990

    Article  CAS  Google Scholar 

  • Gardner DE (1991) Atelocauda angustiphylloda n. sp., a Microcyclic rust on Acacia koa in Hawaii. Mycologia 83: 650

  • Gautam AK, Avasthi S (2017) Discovery of Puccinia tiliaefolia (Pucciniales) in Northwestern Himalayas, India. Pol Bot J 62:135–137

    Google Scholar 

  • Genre A, Lanfranco L (2016) Endophytic coming out: the expressorium as a novel fungal structure specialized in outward-directed penetration of the leaf cuticle. New Phytol 211:5–7

    Article  PubMed  Google Scholar 

  • Gilbert G, Reynolds DR (2002) The ecology of foliicolous fungi. In: Ryvarden L (ed), Proceedings of the 7th international mycological congress, Oslo, p. 89

  • Gilbert G, Reynolds DR (2005) Epifoliar fungi from Queensland, Australia. Australian Syst Bot 18:265–289

    Article  Google Scholar 

  • Giovannetti M, Citernesi AS (1993) Time-course of appressorium formation on host plants by arbuscular mycorrhizal fungi. Mycol Res 98:1140–1142

    Article  Google Scholar 

  • Gold RE, Mendgen K (1984) Cytology of basidiospore germination, penetration, and early colonization of Phaseolus vulgaris by Uromyces appendiculatus var. appendiculatus. Can J Bot 62:1989–2002

    Article  Google Scholar 

  • Gold RE, Mendgen K (1991) Rust basidiospore germlings and disease initiation. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 67–99

    Chapter  Google Scholar 

  • Gomes RR, Glienke C, Videira SIR, Lombard L, Groenewald JZ, Crous PW (2013) Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31:1–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodwin SB, M’Barek S ben, Dhillon B, Wittenberg AHJ, Crane CF, Hane JK, Foster AJ, van der Lee TAJ, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canché B, Churchill ACL, Conde-Ferràez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, de Wit P, Donzelli B, van de Geest HC, van Ham RCHJ, Hammond-Kosack KE, Henrissat B, Kilian A, Kobayashi AK, Koopmann E, Kourmpetis Y, Kuzniar A, Lindquist E, Lombard V, Maliepaard C, Martins N, Mehrabi R, Nap JPH, Ponomarenko A, Rudd JJ, Salamov A, Schmutz J, Schouten HJ, Shapiro H, Stergiopoulos I, Torriani SFF, Tu H, de Vries RP, Waalwijk C, Ware SB, Wiebenga A, Zwiers LH, Oliver RP, Grigoriev IV, Kema GHJ (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7:e1002070

  • Goos RD (1974) A scanning electron microscope and in vitro study of Meliola palmicola. Proc Iowa Acad Sci 81:23–27

    Google Scholar 

  • Goos RD, Gessner RV (1975) Hyphal modifications of Sphaerulina pedicellata: appressoria or hyphopodia? Mycologia 67:1035–1038

    Article  Google Scholar 

  • Gordon TR, Martyn RD (1997) The evolutionary biology of Fusarium oxysporum. Annu Rev Phytopathol 35:111–128

    Article  CAS  PubMed  Google Scholar 

  • Gourgues M, Brunet-Simon A, Lebrun MH, Levis C (2004) The tetraspanin BcPIs1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves. Mol Microbiol 51:619–629

    Article  CAS  PubMed  Google Scholar 

  • Green JR, Carver TLW, Gurr SJ (2002) The formation and function of infection feeding structures. In: Bélanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews: a comprehensive treatise. APS Press, St Paul, pp 66–82

    Google Scholar 

  • Green KA, Eaton CJ, Savoian MS, Scott B (2019) A homologue of the fungal tetraspanin Pls1 is required for Epichloë festucae expressorium formation and establishment of a mutualistic interaction with Lolium perenne. Mol Plant Pathol 20:961–975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenfield BPJ, Lord AM, Dudley E, Butt TM (2014) Conidia of the insect pathogenic fungus, Metarhizium anisopliae, fail to adhere to mosquito larval cuticle. R Soc Open Sci 1:140193

  • Gross A, Holdenrieder O, Pautasso M, Queloz V, Sieber TN (2014) Hymenoscyphus pseudoalbidus, the causal agent of European ash dieback. Mol Plant Pathol 15:5–21

    Article  CAS  PubMed  Google Scholar 

  • Güerri-Agulló B, Gómez-Vidal S, Asensio L, Barranco P, Lopez-Llorca LV (2010) Infection of the red palm weevil (Rhynchophorus ferrugineus) by the entomopathogenic fungus Beauveria bassiana: a SEM study. Microsc Res Tech 73:714–725

    PubMed  Google Scholar 

  • Habibi A, Banihashemi Z (2016) Mating system and role of pycnidiospores in biology of Polystigma amygdalinum, the causal agent of almond red leaf blotch. Phytopathol Mediterr 55:98–108

    Google Scholar 

  • Hajek AE, Delalibera I (2010) Fungal pathogens as classical biological control agents against arthropods. Biocontrol 55:147–158

    Article  Google Scholar 

  • Hajek AE, Hodge KT, Liebherr JK, Day WH, Vandenberg JD (1996) Use of RAPD analysis to trace the origin of the weevil pathogen Zoophthora phytonomi in North America. Mycol Res 100:349–355

    Article  Google Scholar 

  • Hajek AE, Davis CI, Eastburn CC, Vermeylen FM (2002) Deposition and germination of conidia of the entomopathogen Entomophaga maimaiga infecting larvae of gypsy moth, Lymantria dispar. J Invertebr Pathol 79:37–43

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hansford CG (1946) The foliicolous ascomycetes, their parasites and associated fungi. Myc Papers 15:1–240

    Google Scholar 

  • Hansford CG (1961) The Meliolineae, a monograph. Sydowia Beih 2:1–806

    Google Scholar 

  • Hasselbring H (1906) The appressoria of the anthracnoses. Bot Gaz 42:135–142

    Article  Google Scholar 

  • Hatzipapas P, Kalosaka K, Dara A, Christias C (2002) Spore germination and appressorium formation in the entomopathogenic Alternaria alternata. Mycol Res 106:1349–1359

    Article  Google Scholar 

  • Hawksworth DL (1981) The lichenicolous coelomycetes. Bull Br Mus Nat Hist Bot 9:1–98

    Google Scholar 

  • Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 2.2 to 3.8 million species. In: Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY, Gow NAR (eds) The fungal kingdom. ASM Press, Washington, pp 79–95

    Chapter  Google Scholar 

  • Hegde Y, Kolattukudy PE (1997) Cuticular waxes relieve self-inhibition of germination and appressorium formation by the conidia of Magnaporthe grisea. Physiol Mol Plant Pathol 51:75–84

    Article  CAS  Google Scholar 

  • Heiler S, Mendgen K, Deising H (1993) Cellulolytic enzymes of the obligated biotrophic rust fungus Uromyces viciae-fabae are regulated differentiation-specifically. Mycol Res 97:77–85

    Article  CAS  Google Scholar 

  • Hoch HC, Staples RC (1987) Structural and chemical changes among the rust fungi during appressorium development. Annu Rev Phytopathol 25:231–247

    Article  Google Scholar 

  • Hofmann TA (2010) Plant parasitic Asterinaceae and Microthyriaceae from the Neotropics (Panama). Doctoral dissertation, PhD thesis, JW Goethe-University Frankfurt, Germany, 10–408

  • Hofmann TA, Piepenbring M (2014) New records of plant parasitic asterinaceae (Dothideomycetes, Ascomycota) with intercalary appressoria from central America and Panama. Trop Plant Pathol 39:419–427

    Article  Google Scholar 

  • Hofmann TA, Kirschner R, Piepenbring M (2010) Phylogenetic relationships and new records of Asterinaceae (Dothideomycetes) from Panama. Fungal Divers 43:39–53

    Article  Google Scholar 

  • Hogekamp C, Küster H (2013) A roadmap of cell-type specific gene expression during sequential stages of the arbuscular mycorrhiza symbiosis. BMC Genomics 14:306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honegger R (1986) Ultrastructural studies in lichens: I. Haustorial types and their frequencies in a range of lichens with trebouxioid photobionts. New Phytol 103:785–795

    Article  Google Scholar 

  • Honegger R (2009) Lichen-forming fungi and their photobionts. In: Plant relationships. Springer, Berlin, 307–333

  • Hongsanan S, Li YM, Liu JK, Hofmann T, Piepenbring M, Bhat JD, Boonmee S, Doilom M, Singtripop C, Tian Q, Mapook A (2014) Revision of genera in Asterinales. Fungal Divers 68:1–68

    Article  Google Scholar 

  • Hongsanan S, Sánchez-Ramírez S, Crous PW, Ariyawansa HA, Zhao RL, Hyde KD (2016) The evolution of fungal epiphytes. Mycosphere 7:1690–1712

    Article  Google Scholar 

  • Hongsanan S, Maharachchikumbura SS, Hyde KD, Samarakoon MC, Jeewon R, Zhao Q, Al-Sadi AM, Bahkali AH (2017) An updated phylogeny of Sordariomycetes based on phylogenetic and molecular clock evidence. Fungal Divers 84:25–41

    Article  Google Scholar 

  • Hosagoudar V (2012) Asterinales of India. Mycosphere 3:617–852

    Article  Google Scholar 

  • Hou PF, Chen CY (2003) Early stages of infection of lily leaves by Botrytis elliptica and B. cinerea. Plant Pathol Bulletin 12:103–108

    Google Scholar 

  • Howard RJ (1997) Breaching the Outer Barriers-Cuticle and Cell Wall Penetration. In: Carroll GC, Tudzynski P (eds) The mucota: plant relationships. Springer, Berlin, vol 5, pp 43–60

  • Howard RJ, Valent B (1996) Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu Rev Microbiol 50:491–513

    Article  CAS  PubMed  Google Scholar 

  • Howard RJ, Ferrari MA, Roach DH, Money NP (1991) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci 88:11281–11284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh TF, Huang JW, Hsiang T (2001) Light and scanning electron microscopy studies on the infection of oriental lily leaves by Botrytis elliptica. Eur J Plant Pathol 107:571–581

    Article  Google Scholar 

  • Hückelhoven R (2005) Powdery mildew susceptibility and biotrophic infection strategies. FEMS Microbiol Lett 245:9–17

    Article  PubMed  CAS  Google Scholar 

  • Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173

    Google Scholar 

  • Hyde KD, Bussaban B, Paulus B, Crous PW, Lee S, Mckenzie EHCC, Photita W, Lumyong S (2007) Diversity of saprobic microfungi. Biodivers Conserv 16:7–35

    Article  Google Scholar 

  • Hyde KD, Jeewon R, Chen YJ, Bhunjun CS, Calabon MS, Jiang HB, Lin CG, Norphanphoun C, Sysouphanthong P, Pem D, Tibpromma S (2020) The numbers of fungi: is the descriptive curve flattening? Fungal Divers 103:219–271

    Article  Google Scholar 

  • Inácio CA, Cannon PF (2003) Viegasella and Mintera, two new genera of Parmulariaceae (Ascomycota), with notes on the species referred to Schneepia. Mycol Res 107:82–92

    Article  PubMed  Google Scholar 

  • Inácio CA, Araúz K, Piepenbring M (2012) A new genus of Parmulariaceae from Panama. Mycol Prog 11:1–6

    Article  Google Scholar 

  • Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, pp 23–69

    Chapter  Google Scholar 

  • Inoue S, Kato T, Jordan VWL, Brent KJ (1987) Inhibition of appressorial adhesion of Pyricularia oryzae to barley leaves by fungicides. Pestic Sci 19:145–152

    Article  CAS  Google Scholar 

  • Jacobi WR (1982) Microscopy of cultured loblolly pine seedlings and callus inoculated with Cronartium fusiforme. Phytopathology 72:138

    Article  Google Scholar 

  • Jacobson ES (2000) Pathogenic roles for fungal melanins. Clin Microbiol Rev 13:708–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakupović M, Heintz M, Reichmann P, Mendgen K, Hahn M (2006) Microarray analysis of expressed sequence tags from haustoria of the rust fungus Uromyces fabae. Fungal Genet Biol 43:8–19

    Article  PubMed  CAS  Google Scholar 

  • Jayawardena RS, Hyde KD, Damm U, Cai L, Liu M, Li XH, Zhang W, Zhao WS, Yan JY (2016) Notes on currently accepted species of Colletotrichum. Mycosphere 7:1192–1260

    Article  Google Scholar 

  • Jayawardena RS, Bhunjun CS, Hyde KD, Gentekaki E, Itthayakorn P (2021) Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species. Mycosphere 12:519–669

    Article  Google Scholar 

  • Jones H, Whipps JM, Gurr SJ (2001) The Tomato powdery mildew fungus Oidium neolycopersici. Mol Plant Pathol 2:303–309

    Article  CAS  PubMed  Google Scholar 

  • Joseph ME, Hering TF (1997) Effects of environment on spore germination and infection by broad bean rust (Uromyces viciae-fabae). J Agric Sci 128:73–78

    Article  Google Scholar 

  • Kamakura T, Yamaguchi S, Saitoh KI, Teraoka T, Yamaguchi I (2002) A novel gene, CBP1, encoding a putative extracellular chitin-binding protein, may play an important role in the hydrophobic surface sensing of Magnaporthe grisea during appressorium differentiation. Mol Plant Microbe Interact 15:437–444

    Article  CAS  PubMed  Google Scholar 

  • Kapooria RG (1971) A cytological study of promycelia and basidiospores and the chromosome number in Uromyces fabae. Neth J Plant Pathol 77:91–96

    Article  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawamura C, Moriwaki J, Kimura N, Fujita Y, Fuji SI, Hirano T, Koizumi S, Tsuge T (1997) The melanin biosynthesis genes of Alternaria alternata can restore pathogenicity of the melanin-deficient mutants of Magnaporthe grisea. Mol Plant Microbe Interact 10:446–453

    Article  CAS  PubMed  Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th ed, Wallingford, UK

  • Kleemann J, Rincon-Rivera LJ, Takahara H, Neumann U, van Themaat EVL, van der Does HC, Hacquard S, Stüber K, Will I, Schmalenbach W, Schmelzer E, O’Connell RJ (2012) Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathog 8:e1002643

  • Kolattukudy PE, Rogers LM, Li D, Hwang CS, Flaishman MA (1995) Surface signaling in pathogenesis. Proc Natl Acad Sci 92:4080–4087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong LA, Li GT, Liu Y, Liu MG, Zhang SJ, Yang J, Zhou XY, Peng YL, Xu JR (2013) Differences between appressoria formed by germ tubes and appressorium-like structures developed by hyphal tips in Magnaporthe oryzae. Fungal Genet Biol 56:33–41

    Article  CAS  PubMed  Google Scholar 

  • Konta S, Hongsanan S, Tibpromma S, Thongbai B, Maharachchikumbura SSN, Bahkali AH, Hyde KD, Boonmee S (2016) An advance in the endophyte story: Oxydothidaceae fam. nov. with six new species of Oxydothis. Mycosphere 7:1425–1446

    Article  Google Scholar 

  • Konta S, Hyde KD, Phookamsak R, Xu JC, Maharachchikumbura SS, Daranagama DA, McKenzie EH, Boonmee S, Tibpromma S, Eungwanichayapant PD, Samarakoon MC (2020) Polyphyletic genera in Xylariaceae (Xylariales): Neoxylaria gen. nov. and Stilbohypoxylon. Mycosphere 11:2629–2651

    Article  Google Scholar 

  • Krombach S, Reissmann S, Kreibich S, Bochen F, Kahmann R (2018) Virulence function of the Ustilago maydis sterol carrier protein 2. New Phytol 220:553–566

    Article  CAS  PubMed  Google Scholar 

  • Kubicek CP, Starr TL, Glass NL (2014) Plant cell wall–degrading enzymes and their secretion in plant-pathogenic fungi. Annu Rev Phytopathol 52:427–451

    Article  PubMed  CAS  Google Scholar 

  • Kumar V, Singh GP, Babu AM, Ahsan MM, Datta RK (1999) Germination, penetration, and invasion of Beauveria bassiana on silkworm, bombyx mori, causing white muscardine. Ital J Zool 66:39–43

    Article  Google Scholar 

  • Kuo KC (1998) The early stages of infection behavior in plant pathogenic fungi. Plant Prot Bull (taipei) 40:1–24

    Google Scholar 

  • Kwon YH, Hoch HC, Aist JR (1991) Initiation of appressorium formation in Uromyces appendiculatus: organization of the apex, and the responses involving microtubules and apical vesicles. Can J Bot 69:2560–2573

    Article  Google Scholar 

  • Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41

    Article  CAS  PubMed  Google Scholar 

  • Lambou K, Malagnac F, Barbisan C, Tharreau D, Lebrun MH, Silar P (2008) The crucial role of the Pls1 Tetraspanin during ascospore germination in Podospora anserina provides an example of the convergent evolution of morphogenetic processes in fungal plant pathogens and saprobes. Eukaryot Cell 7:1809–1818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanver D, Tollot M, Schweizer G, Presti L, lo, Reissmann S, Ma LS, Schuster M, Tanaka S, Liang L, Ludwig N, (2017) Ustilago maydis effectors and their impact on virulence. Nat Rev Microbiol 15:409–421

    Article  CAS  PubMed  Google Scholar 

  • Latunde-Dada AO (2001) Colletotrichum: tales of forcible entry, stealth, transient confinement and breakout. Mol Plant Pathol 2:187–198

    Article  CAS  PubMed  Google Scholar 

  • Lecuona R, Riba G, Cassier P, Clement JL (1991) Alterations of insect epicuticular hydrocarbons during infection with Beauveria bassiana or B. brongniartii. J Invertebr Pathol 58:10–18

    Article  CAS  Google Scholar 

  • Lee MH, Bostock RM (2006) Induction, regulation, and role in pathogenesis of appressoria in Monilinia fructicola. Phytopathology 96:1072–1080

    Article  CAS  PubMed  Google Scholar 

  • Lee YH, Dean RA (1994) Hydrophobicity of contact surface induces appressorium formation in Magnaporthe grisea. FEMS Microbiol Lett 115:71–76

    Article  Google Scholar 

  • Leger RJS, Durrands PK, Cooper RM, Charnley AK (1988) Regulation of production of proteolytic enzymes by the entomopathogenic fungus Metarhizium anisopliae. Arch Microbiol 150:413–416

    Article  Google Scholar 

  • Lévesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, Huitema E, Raffaele S, Robideau GP, Thines M, Win J, Zerillo MM, Beakes GW, Boore JL, Busam D, Dumas B, Ferriera S, Fuerstenberg SI, Gachon CMM, Gaulin E, Govers F, Grenville-Briggs L, Horner N, Hostetler J, Jiang RHY, Johnson J, Krajaejun T, Lin H, Meijer HJG, Moore B, Morris P, Phuntmart V, Puiu D, Shetty J, Stajich JE, Tripathy S, Wawra S, van West P, Whitty BR, Coutinho PM, Henrissat B, Martin F, Thomas PD, Tyler BM, de Vries RP, Kamoun S, Yandell M, Tisserat N, Buell CR (2010) Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11:R73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li R, Rimmer R, Buchwaldt L, Sharpe AG, Séguin-Swartz G, Hegedus DD (2004) Interaction of Sclerotinia sclerotiorum with Brassica napus: cloning and characterization of endo- and exo-polygalacturonases expressed during saprophytic and parasitic modes. Fungal Genet Biol 41:754–765

    Article  CAS  PubMed  Google Scholar 

  • Li YH, Windham MT, Trigiano RN, Fare DC, Spiers JM, Copes WE (2005) Spore germination, infection structure formation, and colony development of Erysiphe pulchra on dogwood leaves and glass slides. Plant Dis 89:1301–1304

    Article  CAS  PubMed  Google Scholar 

  • Li J, Ying SH, Shan LT, Feng MG (2010) A new non-hydrophobic cell wall protein (CWP10) of Metarhizium anisopliae enhances conidial hydrophobicity when expressed in Beauveria bassiana. Appl Microbiol Biotechnol 85:975e984

  • Li M, Liang X, Rollins JA (2012) Sclerotinia sclerotiorum γ-glutamyl transpeptidase (Ss-Ggt1) is required for regulating glutathione accumulation and development of sclerotia and compound appressoria. Mol Plant Microbe Interact 25:412–420

    Article  PubMed  CAS  Google Scholar 

  • Li J, Zhang X, Li L, Liu J, Zhang Y, Pan H (2018) Proteomics analysis of SsNsd1-mediated compound appressoria formation in Sclerotinia sclerotiorum. Int J Mol Sci 19:2946

    Article  PubMed Central  CAS  Google Scholar 

  • Li WJ, McKenzie EH, Liu JK, Bhat DJ, Dai DQ, Camporesi E, Tian Q, Maharachchikumbura SS, Luo ZL, Shang QJ, Zhang JF, Tangthirasunun N, Karunarathna SC, Xu JC, Hyde KD (2020) Taxonomy and phylogeny of hyaline-spored coelomycetes. Fungal Divers 100:279–801

    Article  CAS  Google Scholar 

  • Liu ZM, Kolattukudy PE (1998) Identification of a gene product induced by hard-surface contact of Colletotrichum gloeosporioides conidia as an ubiquitin-conjugating enzyme by yeast complementation. J Bacteriol 180:3592–3597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu ZM, Kolattukudy PE (1999) Early expression of the calmodulin gene, which precedes appressorium formation in Magnaporthe grisea, is inhibited by self-inhibitors and requires surface attachment. J Bacteriol 181:3571–3577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu JK, Hyde KD, Jeewon R, Phillips AJL, Maharachchikumbura SSN, Ryberg M, Liu ZY, Zhao Q (2017) Ranking higher taxa using divergence times: a case study in Dothideomycetes. Fungal Divers 84:75–99

    Article  Google Scholar 

  • Liu JK, Chang HW, Liu Y, Qin YH, Ding YH, Wang L, Zhao Y, Zhang MZ, Cao SN, Li LT, Liu W (2018) The key gluconeogenic gene PCK1 is crucial for virulence of Botrytis cinerea via initiating its conidial germination and host penetration. Environ Microbiol 20:1794–1814

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Liu JK, Li GH, Zhang MZ, Zhang YY, Wang YY, Hou J, Yang S, Sun J, Qin QM (2019) A novel Botrytis cinerea-specific gene BcHBF1 enhances virulence of the grey mould fungus via promoting host penetration and invasive hyphal development. Mol Plant Pathol 20:731–747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lovett B, Leger RJS (2017) The insect pathogens. The Fungal Kingdom, pp 923–943

  • Lubbe CM, Denman S, Cannon PF, Groenewald JZ, Lamprecht SC, Crous PW (2004) Characterization of Colletotrichum species associated with diseases of Proteaceae. Mycologia 96:1268–1279

    Article  PubMed  Google Scholar 

  • Luo X, Keyhani NO, Yu X, He Z, Luo Z, Pei Y, Zhang Y (2012) The MAP kinase Bbslt2 controls growth, conidiation, cell wall integrity, and virulence in the insect pathogenic fungus Beauveria bassiana. Fungal Genet Biol 49:544–555

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Nontachaiyapoom S, Jayawardena RS, Hyde KD, Gentekaki E, Zhou S, Qian Y, Wen T, Kang J (2018) Endophytic Colletotrichum species from Dendrobium spp. in China and northern Thailand. MycoKeys 43:23–57

    Article  Google Scholar 

  • Magalhães BP, Humber RA, Shields EJ, Roberts DW (1991) Effects of environment and nutrition on conidium germination and appressorium formation by Zoophthora radicans (Zygomycetes: Entomophthorales): a pathogen of the potato leafhopper (Homoptera: Cicadellidae). Environ Entomol 20:1460–1468

    Article  Google Scholar 

  • Malagnac F, Lalucque H, Lepere G, Silar P (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet Biol 41:982–997

    Article  CAS  PubMed  Google Scholar 

  • Malagnac F, Bidard F, Lalucque H, Brun S, Lambou K, Lebrun MH, Silar P (2008) Convergent evolution of morphogenetic processes in fungi: Role of tetraspanins and NADPH oxidases 2 in plant pathogens and saprobes. Commun Integr Biol 1:180–181

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Manawasinghe IS, Dissanayake AJ, Li X, Liu M, Wanasinghe DN, Xu J, Zhao W, Zhang W, Zhou Y, Hyde KD, Brooks S, Yan J (2019) High genetic diversity and species complexity of Diaporthe associated with Grapevine Dieback in China. Front Microbiol 10:1936

    Article  PubMed  PubMed Central  Google Scholar 

  • Mannino MC, Huarte-Bonnet C, Davyt-Colo B, Pedrini N (2019) Is the insect cuticle the only entry gate for fungal infection? Insights into alternative modes of action of entomopathogenic fungi. J Fungi 5:33

    Article  CAS  Google Scholar 

  • Marin-Felix Y, Groenewald JZ, Cai L, Chen Q, Marincowitz S, Barnes I, Bensch K, Braun U, Camporesi E, Damm U, de Beer ZW, Dissanayake A, Edwards J, Giraldo A, Hernández-Restrepo M, Hyde KD, Jayawardena RS, Lombard L, Luangsaard J, McTaggart AR, Rossman AY, Sandoval-Denis M, Shen M, Shivas RG, Tan YP, van der Linde EJ, Wingfield MJ, Wood AR, Zhang JQ, Zhang Y, Crous PW (2017) Genera of phytopathogenic fungi: GOPHY 1. Stud Mycol 86:99–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marschall R, Siegmund U, Burbank J (2016) Tudzynski P (2016) Update on Nox function, site of action and regulation in Botrytis cinerea. Fungal Biol Biotechnol 3:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall DS (1980) Infection cushion formation on rice sheaths by Rhizoctonia solani. Phytopathology 70:947

    Article  Google Scholar 

  • McNicol RJ, Williamson B, Young K (1989) Ethylene production by black currant flowers infected by Botrytis cinerea. Int Symp Rubus Ribes 262:209–216

    Google Scholar 

  • Mehrotra MD (1990) Rhizoctonia solani, a potentially dangerous pathogen of khasi pine and hardwoods in forest nurseries in India. Eur J for Pathol 20:329–338

    Article  Google Scholar 

  • Mendgen K (1997) The Uredinales. In: Esser K, Lemke PA (eds) The mycota plant relationships part B, vol V. Springer, Berlin, pp 79–94

    Chapter  Google Scholar 

  • Mendgen K, Hahn M, Deising H (1996) Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34:367–386

    Article  CAS  PubMed  Google Scholar 

  • Miller M, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Gateway computing environments workshop (GCE), pp 1–8

  • Minelli A, Contrafatto G (2009) Biological science fundamentals and systematics. EOLSS Publications, pp 472

  • Money NP, Caesar-TonThat TC, Frederick B, Henson JM (1998) Melanin synthesis is associated with changes in hyphopodial turgor, permeability, and wall rigidity in Gaeumannomyces graminis var. graminis. Fungal Genet Biol 24:240–251

    Article  CAS  PubMed  Google Scholar 

  • Monkhung S, Takamatsu S, To-anun C (2013) Molecular and morphological characterization of Phyllactinia cassia-fistulae (Erysiphaceae; Ascomycota) from Thailand. Afr J Biotechnol 12:109–114

    Article  CAS  Google Scholar 

  • Morley CD, Mosse B (1976) Abnormal vesicular-arbuscular mycorrhizal infections in white clover induced by lupin. Trans Brit Mycol Soc 67:510–513

    Article  Google Scholar 

  • Muggia L, Grube M (2018) Fungal diversity in lichens: from extremotolerance to interactions with algae. Life 8:15

    Article  PubMed Central  CAS  Google Scholar 

  • Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456

    Article  PubMed  CAS  Google Scholar 

  • Müller E, von Arx JA (1962) Die Gattungen der didymosporen Pyrenomyceten. Beitr Kryptogamenfl Schweiz 11:1–922

    Google Scholar 

  • Murrin F, Nolan RA (1987) Ultrastructure of the infection of spruce budworm larvae by the fungus Entomophaga aulicae. Can J Bot 65:1694–1706

    Article  Google Scholar 

  • Nadeau MP, Dunphy GB, Boisvert JL (1996) Development of Erynia conica (Zygomycetes: Entomophthorales) on the cuticle of the adult black flies Simulium rostratum and Simulium decorum (Diptera: Simuliidae). J Invertebr Pathol 68:50–58

    Article  CAS  PubMed  Google Scholar 

  • Neergaard P (2017) Seed pathology. London, Macmillan Education, Limited, pp 226

  • Nishimura M, Park G, Xu JR (2003) The G-beta subunit MGB1 is involved in regulating multiple steps of infection-related morphogenesis in Magnaporthe grisea. Mol Plant Pathol 4:347–359

    Google Scholar 

  • Nonomura T, Nishitomi A, Matsuda Y, Soma C, Xu L, Kakutani K, Takikawa Y, Toyoda H (2010) Polymorphic change of appressoria by the tomato powdery mildew Oidium neolycopersici on host tomato leaves reflects multiple unsuccessful penetration attempts. Fungal Biol 114:917–928

    Article  PubMed  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • Oh Y, Donofrio N, Pan H, Coughlan S, Brown DE, Meng S, Mitchell T, Dean RA (2008) Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae. Genome Biol 9:R85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ortiz-Urquiza A, Keyhani NO (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4:357–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Urquiza A, Keyhani NO (2016) Molecular genetics of Beauveria bassiana infection of insects. Adv Genet 94: 165e250

  • Osorio M, Stephan BR (1989) Ascospore germination and appressorium formation in vitro of some species of the Rhytismataceae. Mycol Res 93:439–451

    Article  Google Scholar 

  • Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Curr Opin Plant Biol 6:320–326

    Article  CAS  PubMed  Google Scholar 

  • Parbery DG, Emmett RW (1977) Hypothesis regarding appressoria, spores, survival and phylogeny in parasitic fungi. Rev Mycol 41:429–447

    Google Scholar 

  • Pastirčáková K (2004) Guignardia aesculi (Peck) Stewart-fungal pathogen on Aesculus leaves in Slovakia. Acta Fytotech Zootech 7 č. Mimoriadne číslo.

  • Paulitz TC, Adams K (2003) Composition and distribution of Pythium communities in wheat fields in eastern Washington State. Phytopathology 93:867–873

    Article  CAS  PubMed  Google Scholar 

  • Pawlowski ML, Hartman GL (2016) Infection mechanisms and colonization patterns of fungi associated with Soybean. In: Cumagan CJ (ed) Plant Pathology. InTech, Rijeka, Croatia, 25

  • Pedrini N, Crespo R, Juárez MP (2007) Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comp Biochem Physiol - C Toxicol Pharmacol 146:124–137

    Article  PubMed  CAS  Google Scholar 

  • Pedrini N, Ortiz-Urquiza A, Huarte-Bonnet C, Zhang S, Keyhani NO (2013) Targeting of insect epicuticular lipids by the entomopathogenic fungus Beauveria bassiana: Hydrocarbon oxidation within the context of a host-pathogen interaction. Front Microbiol 4:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Pekrul S, Grula EA (1979) Mode of infection of the corn earworm (Heliothus zea) by Beauveria bassiana as revealed by scanning electron microscopy. J Invertebr Pathol 34:238–247

    Article  CAS  Google Scholar 

  • Pepe A, Giovannetti M, Sbrana C (2020) Appressoria and phosphorus fluxes in mycorrhizal plants: connections between soil- and plant-based hyphae. Mycorrhiza 30:589–600

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Garcia A, Olalla L, Rivera E, del Pino D, Cánovas I, de Vicente A, Torés JA (2001) Development of Sphaerotheca fusca on susceptible, resistant, and temperature-sensitive resistant melon cultivars. Mycol Res 105:1216–1222

    Article  Google Scholar 

  • Perfect SE, Green JR (2001) Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2:101–108

    Article  CAS  PubMed  Google Scholar 

  • Perfect SE, Hughes HB, O’Connell RJ, Green JR (1999) Colletotrichum: a model genus for studies on pathology and fungal–plant interactions. Fungal Genet Biol 27:186–198

    Article  CAS  PubMed  Google Scholar 

  • Phillips AJ, Hyde KD, Alves A, Liu JK (2019) Families in Botryosphaeriales: a phylogenetic, morphological and evolutionary perspective. Fungal Divers 94:1–22

    Article  Google Scholar 

  • Phookamsak R, Hyde KD, Jeewon R, Bhat DJ, Jones EBG, Maharachchikumbura SSN, Raspé O, Karunarathna SC, Wanasinghe DN, Hongsanan S, Doilom M, Tennakoon DS, Machado AR, Firmino AL, Ghosh A, Karunarathna A, Mešić A, Dutta AK, Thongbai B, Devadatha B, Norphanphoun C, Senwanna C, Wei D, Pem D, Ackah FK, Wang GN, Jiang HB, Madrid H, Lee HB, Goonasekara ID, Manawasinghe IS, Kušan Cano J, Gené J, Li J, Das K, Acharya K, Raj KNA, Latha KPD, Chethana KWT, He MQ, Dueñas M, Jadan M, Martín MP, Samarakoon MC, Dayarathne MC, Raza M, Park MS, Telleria MT, Chaiwan N, Matočec N, de Silva NI, Pereira OL, Singh PN, Manimohan P, Uniyal P, Shang QJ, Bhatt RP, Perera RH, Alvarenga RLM, Nogal-Prata S, Singh SK, Vadthanarat S, Oh SY, Huang SK, Rana S, Konta S, Paloi S, Jayasiri SC, Jeon SJ, Mehmood T, Gibertoni TB, Nguyen TTT, Singh U, Thiyagaraja V, Sarma VV, Dong W, Yu XD, Lu YZ, Lim YW, Chen Y, Tkalčec Z, Zhang ZF, Luo ZL, Daranagama DA, Thambugala KM, Tibpromma S, Camporesi E, Bulgakov T, Dissanayake AJ, Senanayake IC, Dai DQ, Tang LZ, Khan S, Zhang H, Promputtha I, Cai L, Chomnunti P, Zhao RL, Lumyong S, Boonmee S, Wen TC, Mortimer PE, Xu J (2019) Fungal diversity notes 929–1036: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Divers 95:1–273

    Article  Google Scholar 

  • Photita W, Lumyong S, Lumyong P, McKenzie EHC, Hyde KD (2004) Are some endophytes of Musa acuminata latent pathogens? Fungal Divers 16:131–140

    Google Scholar 

  • Phukhamsakda C, Ariyawansa HA, Phillips AJL, Wanasinghe DN, Bhat DJ, McKenzie EHC, Singtripop C, Camporesi E, Hyde KD (2016) Additions to sporormiaceae: introducing two novel genera, Sparticola and Forliomyces, from Spartium. Cryptogamie Mycol 37:75–97

    Article  Google Scholar 

  • Podila GK, Rogers LM, Kolattukudy PE (1993) Chemical signals from avocado surface wax trigger germination and appressorium formation in Colletotrichum gloeosporioides. Plant Physiol 103:267–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poulter R, Harvey L, Burritt DJ (2003) Qualitative resistance to powdery mildew in hybrid sweet peas. Euphytica 133:349

    Article  Google Scholar 

  • Powers H Jr (1977) Evaluation of pathogenic variability of Cronartium fusiforme on loblolly pine in the Southern USA. Phytopathology 77:1403

    Article  Google Scholar 

  • Promputtha I, Lumyong S, Dhanasekaran V, McKenzie EHC, Hyde KD, Jeewon R (2007) A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb Ecol 53:579–590

    Article  PubMed  Google Scholar 

  • Promputtha I, Hyde KD, McKenzie EH, Peberdy JF, Lumyong S (2010) Can leaf degrading enzymes provide evidence that endophytic fungi becoming saprobes? Fungal Divers 41:89–99

    Article  Google Scholar 

  • Pryce-Jones E, Carver T, Gurr SJ (1999) The roles of cellulase enzymes and mechanical force in host penetration by Erysiphe graminis f. sp. hordei. Physiol Mol Plant Pathol 55:175–182

    Article  CAS  Google Scholar 

  • Purahong W, Hyde KD (2011) Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Divers 47:1–7

    Article  Google Scholar 

  • Qi Z, Wang Q, Dou X, Wang W, Zhao Q, Lv R, Zhang H, Zheng X, Wang P, Zhang Z (2012) MoSwi6, an APSES family transcription factor, interacts with MoMps1 and is required for hyphal and conidial morphogenesis, appressorial function and pathogenicity of Magnaporthe oryzae. Mol Plant Pathol 13:677–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer, version 1.5. MCMC Trace File Analyser. Computer program and documentation distributed by the authors, website: http://beast.bio.ed.ac.uk/Tracer

  • Rathnayaka AR, Chethana KWT, Phillips AJL, Liu JK, Samarakoon MC, Hyde KD (2021) Ancestral character Analysis of selected characters in order Botryosphaeriales and evolution of nutritional modes. In prep

  • Rauscher M, Mendgen K, Deising H (1995) Extracellular proteases of the rust fungus Uromyces viciae-fabae. Exp Myco 19:26–34

    Article  CAS  Google Scholar 

  • Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716

    Article  PubMed  Google Scholar 

  • Ren W, Zhang Z, Shao W, Yang Y, Zhou M, Chen C (2017) The autophagy-related gene BcATG1 is involved in fungal development and pathogenesis in Botrytis cinerea. Mol Plant Pathol 18:238–248

    Article  CAS  PubMed  Google Scholar 

  • Riedel M, Werres S, Elliott M, McKeever K, Shamoun S (2012) Histopathological investigations of the infection process and propagule development of Phytophthora ramorum on rhododendron leaves. Forest Phytophthoras. https://doi.org/10.5399/osu/fp.2.1.3036.2012

    Article  Google Scholar 

  • Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles: Tansley review. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Gálvez E, Mendgen K (1995) The infection process of Fusarium oxysporum in cotton root tips. Protoplasma 189:61–72

    Article  Google Scholar 

  • Rojas EI, Rehner SA, Samuels GJ, van Bael SA, Herre EA, Cannon P, Chen R, Pang J, Wang R, Zhang Y, Peng YQ, Sha T (2010) Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panamá: Multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102:1318–1338

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes Bayesian phylogenetic Inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rustiani US, Sinaga MS, Hidayat SH, Wiyono S (2015) Penyebab penyakit bulai jagung di indonesia (Three species of Peronosclerospora as a cause Downy Mildew on Maize in Indonesia). Berita Biologi 14:29–37

    Google Scholar 

  • Ryder LS, Talbot NJ (2015) Regulation of appressorium development in pathogenic fungi. Curr Opin Plant Biol 26:8–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salinas J, Verhoeff K (1995) Microscopical studies of the infection of gerbera flowers by Botrytis cinerea. Eur J Plant Pathol 101:377–386

    Article  Google Scholar 

  • Samarakoon MC, Peršoh D, Hyde KD, Bulgakov TS, Manawasinghe IS, Jayawardena RS, Promputtha I (2018) Colletotrichum acidae sp. nov. from northern Thailand and a new record of C. dematium on Iris sp. Mycosphere 9:583–597

    Article  Google Scholar 

  • Samarakoon MC, Hyde KD, Hongsanan S, McKenzie EHC, Ariyawansa HA, Promputtha I, Zeng XY, Tian Q, Liu JK (2020) Divergence time calibrations for ancient lineages of Ascomycota classification based on a modern review of estimations. Fungal Divers 100:279–801

    Google Scholar 

  • Sánchez-Torres P, Hinarejos R, Tuset JJ (2009) Characterization and pathogenicity of Fusicladium eriobotryae, the fungal pathogen responsible for loquat scab. Plant Dis 93:1151–1157

    Article  PubMed  CAS  Google Scholar 

  • Sbrana C, Turrini A, Giovannetti M (2017) The crosstalk between plants and their arbuscular mycorrhizal symbionts: a mycocentric view. In: Gordon R, Seckbach J (eds) Biocommunication: sign-mediated interactions between cells and organisms. World Scientific, pp 285–308

  • Schaper T, Ott S (2003) Photobiont selectivity and interspecific interactions in lichen communities. I. Culture experiments with the mycobiont Fulgensia bracteata. Plant Biol 5:441–450

    Article  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Schumacher J, Simon A, Cohrs KC, Viaud M, Tudzynski P (2014) The transcription factor BcLTF1 regulates virulence and light responses in the necrotrophic plant pathogen Botrytis cinerea. PLoS Genet 10: e1004040

  • Scott-Craig JS, Panaccione DG, Cervone F, Walton JD (1990) Endopolygalacturonase is not required for pathogenicity of Cochliobolus carbonum on maize. Plant Cell 2:1191–1200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Senanayake IC, Rathnayaka AR, Marasinghe DS, Calabon MS, Gentekaki E, Lee HB, Hurdeal VG, Pem D, Dissanayake LS, Wijesinghe SN, Bundhun D (2020) Morphological approaches in studying fungi: collection, examination, isolation, sporulation and preservation. Mycosphere 11:2678–2754

  • Senwanna C, Hongsanan S, Phookamsak R, Tibpromma S, Cheewangkoon R, Hyde KD (2019) Muyocopron heveae sp. nov. and M. dipterocarpi appears to have host-jumped to rubber. Mycol Prog 18:741–752

    Article  Google Scholar 

  • Sharma KK (2016) Fungal genome sequencing: basic biology to biotechnology. Crit Rev Biotechnol 36:743–759

    Article  CAS  PubMed  Google Scholar 

  • Sharman S, Heale JB (1977) Penetration of carrot roots by the grey mould fungus Botrytis cinerea Pers. Physiol Plant Pathol 10:63–71

    Article  Google Scholar 

  • Shivas RG, Ryley MJ, Telle S, Liberato JR, Thines M (2012) Peronosclerospora australiensis sp. nov. and Peronosclerospora sargae sp. nov., two newly recognized downy mildews in northern Australia, and their biosecurity implications. Austral Plant Pathol 41:125–130

    Article  Google Scholar 

  • Siegmund U, Heller J, van Kann JAL, Tudzynski P (2013) The NADPH oxidase complexes in Botrytis cinerea: evidence for a close association with the ER and the Tetraspanin Pls1. PLoS ONE 8:e55879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skinner M, Parker BL, Kim JS (2014) Role of entomopathogenic fungi. In: Abrol DP (ed) Integrated pest management. Academic Press, Cambridge, pp 169–191

    Chapter  Google Scholar 

  • Smith PH, Foster EM, Boyd LA, Brown JKM (1996) The early development of Erysiphe pisi on Pisum sativum L. Plant Pathol 45:302–309

    Article  Google Scholar 

  • Staehelin C, Charon C, Boller T, Crespi M, Kondorosi Á (2001) Medicago truncatula plants overexpressing the early nodulin gene enod40 exhibit accelerated mycorrhizal colonization and enhanced formation of arbuscules. Proc Natl Acad Sci 98:15366–15371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steiner U, Oerke EC (2007) Localized melanization of appressoria is required for pathogenicity of Venturia inaequalis. Phytopathology 97:1222–1230

    Article  PubMed  Google Scholar 

  • Stone JK, Capitano BR, Kerrigan JL (2008) The histopathology of Phaeocryptopus gaeumannii on Douglas-fir needles. Mycologia 100:431–444

    Article  PubMed  Google Scholar 

  • Suto Y (2009) Three ascomycetes on leaves of evergreen Ilex trees from Japan: Rhytisma ilicis-integrae sp. nov., R. ilicis-latifoliae, and R. ilicis-pedunculosae sp. nov. Mycoscience 50:357–368

    Article  Google Scholar 

  • Sutton BC (1980) The coelomycetes. Fungi imperfecti with pycnidia, acervuli and stromata. Commonwealth Mycological Institute

  • Sutton JC, Sopher CR, Owen-Going TN, Liu W, Grodzinski B, Hall JC, Benchimol RL (2006) Etiology and epidemiology of Pythium root rot in hydroponic crops: current knowledge and perspectives. Summa Phytopathol 32:307–321

    Article  Google Scholar 

  • Suzuki T, Maeda A, Hirose M, Ichinose Y, Shiraishi T, Toyoda K (2017) Ultrastructural and cytological studies on Mycosphaerella pinodes infection of the model legume Medicago truncatula. Front Plant Sci 8:1132

    Article  PubMed  PubMed Central  Google Scholar 

  • Szabo LJ, Bushnell WR (2001) Hidden robbers: the role of fungal haustoria in parasitism of plants. Proc Natl Acad Sci 98:7654–7665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takamatsu S (1999) Phylogenetic relationships of Microsphaera and Erysiphe section Erysiphe (powdery mildews) inferred from the rDNA ITS sequences. Mycoscience 40:259–268

    Article  CAS  Google Scholar 

  • Talbot NJ (2003) On the trail of a serial killer: exploring the biology of Magnaporthe grisea. Annu Rev Microbiol 57:177–202

    Article  CAS  PubMed  Google Scholar 

  • Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575–1590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanada N, Sakurai T, Mitsuno H, Bakkum DJ, Kanzaki R, Takahashi H (2012) Dissociated neuronal culture expressing ionotropic odorant receptors as a hybrid odorant biosensor - Proof-of-concept study. Analyst 137:3452–3458

    Article  CAS  PubMed  Google Scholar 

  • Telle S, Shivas RG, Ryley MJ, Thines M (2011) Molecular phylogenetic analysis of Peronosclerospora (Oomycetes) reveals cryptic species and genetically distinct species parasitic to maize. Eur J Plant Pathol 130:521–528

    Article  Google Scholar 

  • Thines E, Weber RWS, Talbot NJ (2000) MAP kinase and protein kinase A–dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell 12:1703–1718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thiyagaraja V, Lücking R, Ertz D, Wanasinghe DN, Karunarathna SC, Camporesi E, Hyde KD (2020) Evolution of non-lichenized, saprotrophic species of Arthonia (Ascomycota, Arthoniales) and resurrection of Naevia, with notes on Mycoporum. Fungal Divers 102:205–224

    Article  Google Scholar 

  • Tibpromma S, Hyde KD, McKenzie EHC, Bhat DJ, Phillips AJL, Wanasinghe DN, Samarakoon MC, Jayawardena RS, Dissanayake AJ, Tennakoon DS, Doilom M, Phookamsak R, Tang AMC, Xu J, Mortimer PE, Promputtha I, Maharachchikumbura SSN, Khan S, Karunarathna SC (2018) Fungal diversity notes 840–928: micro-fungi associated with Pandanaceae. Fungal Divers 93:1–160

    Article  Google Scholar 

  • Tucker SL, Talbot N (2001) Surface attachment and peg development by plant pathogenic fungi. Annu Rev Phytopathol 39:385–417

    Article  CAS  PubMed  Google Scholar 

  • Uzma F, Mohan CD, Siddaiah CN, Chowdappa S (2019) Endophytic fungi: promising source of novel bioactive compounds. Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 243–265

    Chapter  Google Scholar 

  • Valero-Jiménez CA, Wiegers H, Zwaan BJ, Koenraadt CJM, van Kan JAL (2016) Genes involved in virulence of the entomopathogenic fungus Beauveria bassiana. J Invertebr Pathol 133:41–49

    Article  PubMed  CAS  Google Scholar 

  • Van Den Heuvel J (1981) Effect of inoculum composition on infection of French bean leaves by conidia of Botrytis cinerea. Neth J Plant Pathol 87:55–64

    Article  Google Scholar 

  • Van den Heuvel J, Waterreus LP (1983) Conidial concentration as an important factor determining the type of prepenetration structures formed by Botrytis cinerea on leaves of French bean (Phaseolus vulgaris). Plant Pathol 32:263–272

    Article  Google Scholar 

  • Van der Does HC, Rep M (2007) Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Mol Plant Microbe Interact 20:1175–1182

    Article  PubMed  CAS  Google Scholar 

  • Vaneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ (2006) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312:580–583

    Article  CAS  Google Scholar 

  • Vega FE, Meyling NV, Luangsaard JJ, Blackwell M (2012) Fungal Entomopathogens. In: Vega FE, Kaya HK (eds) Insect pathology, 2nd edn. Academic Press, Amsterdam, pp 171–220

    Chapter  Google Scholar 

  • Vey A, Fargues J (1977) Histological and ultrastructural studies of Beauveria bassiana infection in Leptinotarsa decemlineata larvae during ecdysis. J Invertebr Pathol 30:207–215

    Article  Google Scholar 

  • Viret O, Petrini O (1994) Colonization of beech leaves (Fagus sylvatica) by the endophyte Discula umbrinella (teleomorph: Apiognomonia errabunda). Mycol Res 98:423–432

    Article  Google Scholar 

  • Vittal R, Paul C, Hill CB, Hartman GL (2014) Characterization and quantification of fungal colonization of Phakopsora pachyrhizi in soybean genotypes. Phytopathology 104:86–94

    Article  CAS  PubMed  Google Scholar 

  • Voegele RT (2006) Uromyces fabae: development, metabolism, and interactions with its host Vicia faba. FEMS Microbiol Lett 259:165–173

    Article  CAS  PubMed  Google Scholar 

  • Wade GC, Cruickshank RH (1992) The establishment and structure of latent infections with Monilinia fructicola on apricots. J Phytopathol 136:95–106

    Article  Google Scholar 

  • Wagner BL, Lewis LC (2000) Colonization of Corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 66:3468–3473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, St. Leger RJ (2006) A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc Natl Acad Sci 103:6647–6652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, St. Leger RJ, (2005) Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum. Eukaryot Cell 4:937–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson RA, Talbot NJ (2009) Under pressure: Investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7:185–195

    Article  CAS  PubMed  Google Scholar 

  • Woods AM, Beckett A (1987) Wall structure and ornamentation of the urediniospores of Uromyces viciae-fabae. Can J Bot 65:2007–2016

    Article  Google Scholar 

  • Wraight SP, Butt TM, Galaini-Wraight S, Allee LL, Soper RS, Roberts DW (1990) Germination and infection processes of the entomophthoralean fungus Erynia radicans on the potato leafhopper, Empoasca fabae. J Invertebr Pathol 56:157–174

    Article  Google Scholar 

  • Xu J (2020) Fungal species concepts in the genomics era. Genome 63:459–468

    Article  PubMed  Google Scholar 

  • Xu JR, Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10:2696–2706

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Harris AJ, Blair C, He X (2015) RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Mol Phylogenet Evol 87:46–49

    Article  PubMed  Google Scholar 

  • Yu L, Xiong D, Han Z, Liang Y, Tian C (2019a) The mitogen-activated protein kinase gene CcPmk1 is required for fungal growth, cell wall integrity and pathogenicity in Cytospora chrysosperma. Fungal Genet Biol 128:1–13

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Blair C, He X (2019b) RASP 4: ancestral state reconstruction tool for multiple genes and characters. Mol Phylogenet Evol 37:604–606

    Article  CAS  Google Scholar 

  • Zeilinger S, Gupta VK, Dahms TES, Silva RN, Singh HB, Upadhyay RS, Gomes EV, Tsui CKM, Nayak SC (2016) Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiol Rev 40:182–207

    Article  CAS  PubMed  Google Scholar 

  • Zeng XY, Wu HX, Hongsanan S, Jeewon R, Wen TC, Maharachchikumbura SS, Chomnunti P, Hyde KD (2019) Taxonomy and the evolutionary history of Micropeltidaceae. Fungal Divers 97:393–436

    Article  Google Scholar 

  • Zhang YJ, Feng MG, Fan YH, Luo ZB, Yang XY, Wu D, Pei Y (2008) A cuticle-degrading protease (CDEP-1) of Beauveria bassiana enhances virulence. Biocontrol Sci Technol 18:551–563

    Article  Google Scholar 

  • Zhang Y, Zhao J, Fang W, Zhang J, Luo Z, Zhang M, Fan Y, Pei Y (2009) Mitogen activated protein kinase hog1 in the entomopathogenic fungus Beauveria bassiana regulates environmental stress responses and virulence to insects. Appl Environ Microbiol 75:3787–3795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Zhang J, Jiang X, Wang G, Luo Z, Fan Y, Wu Z, Pei Y (2010) Requirement of a mitogen-activated protein kinase for appressorium formation and penetration of insect cuticle by the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 76:2262–2270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Xia YX, Kim B, Keyhani NO (2011) Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana. Mol Microbiol 80:811–826

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Widemann E, Bernard G, Lesot A, Pinot F, Pedrini N, Keyhani NO (2012) CYP52X1, representing new cytochrome P450 subfamily, displays fatty acid hydroxylase activity and contributes to virulence and growth on insect cuticular substrates in entomopathogenic fungus Beauveria bassiana. J Biol Chem 287:13477–13486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Chen Y, Li B, Chen T, Tian S (2020) Reactive oxygen species: a generalist in regulating development and pathogenicity of phytopathogenic fungi. Comput Struct Biotechnol J 18:3344–3349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou D, Hyde KD (2001) Host-specificity, host-exclusivity, and host-recurrence in saprobic fungi. Mycol Res 105:1449–1457

    Article  Google Scholar 

  • Zúñiga E, Romero J, Ollero-Lara A, Lovera M, Arquero O, Miarnau X, Torguet L, Trapero A, Luque J (2020) Inoculum and infection dynamics of Polystigma amygdalinum in almond orchards in spain. Plant Dis 104:1239–1246

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Thailand Research Fund entitled “Impact of climate change on fungal diversity and biogeography in the Greater Mekong Sub region” (Grant Number RDG6130001). Kevin D Hyde thanks Chiang Mai University for the award of Visiting Professor. Ruvishika S. Jayawardena thanks National Research Council of Thailand, grant for new researcher NRCT5-TRG630010-01, entitled “Biodiversity, taxonomy, phylogeny and evolution of Colletotrichum in northern Thailand”. Saowaluck Tibpromma would like to thank the International Postdoctoral Exchange Fellowship Program (Grant Number Y9180822S1), CAS President’s International Fellowship Initiative (Grant Number 2020PC0009), China Postdoctoral Science Foundation and the Yunnan Human Resources, and Social Security Department Foundation for funding her postdoctoral research. Pranami D. Abeywickrama would like to thank Associate Professor Dr. Mathias Choquer (Univ Lyon, Université Lyon 1, CNRS, INSA-Lyon, Microbiologie, Adaptation et Pathogénie, Villeurbanne, France) and Associate Professor Dr. Gleiber Quintão Furtado (Departamento de Fitopatologia,Universidade Federal de Vicßosa, Minas Gerais, Brasil) for their kind permission to reprint the figures from Choquer et al. (2021) and Caires et al. (2015).

Author information

Authors and Affiliations

  1. Innovative Institute of Plant Health, Zhongkai University of Agriculture and Engineering, Guangzhou, 510225, People’s Republic of China

    K. W. Thilini Chethana & Kevin D. Hyde

  2. Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    K. W. Thilini Chethana, Ruvishika S. Jayawardena, Yi-Jyun Chen, Sirinapa Konta, Pranami D. Abeywickrama, Milan C. Samarakoon, Chanokned Senwanna, Ausana Mapook, Xia Tang, Deecksha Gomdola, Diana S. Marasinghe, Oundhyalah D. Padaruth & Kevin D. Hyde

  3. School of Science, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    K. W. Thilini Chethana, Ruvishika S. Jayawardena, Yi-Jyun Chen, Sirinapa Konta, Pranami D. Abeywickrama, Xia Tang, Deecksha Gomdola, Diana S. Marasinghe, Oundhyalah D. Padaruth & Kevin D. Hyde

  4. Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming, 650201, Yunnan, People’s Republic of China

    Kevin D. Hyde

  5. Beijing Key Laboratory of Environment-Friendly Management on Fruit Diseases and Pests in North China, Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, People’s Republic of China

    Pranami D. Abeywickrama

  6. Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand

    Milan C. Samarakoon & Saisamorn Lumyong

  7. Engineering and Research Center for Southwest Biopharmaceutical Resource of National Education Ministry of China, Gui Zhou University, Gui Yang, 550025, Gui Zhou, People’s Republic of China

    Xia Tang

  8. Department of Plant Sciences, Faculty of Agriculture, Rajarata University of Sri Lanka, Anuradhapura, Sri Lanka

    Abhaya Balasuriya

  9. Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1, Canada

    Jianping Xu

  10. Center of Excellence in Microbial Diversity and Sustainable Utilization, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand

    Saisamorn Lumyong & Kevin D. Hyde

  11. Academy of Science, The Royal Society of Thailand, Bangkok, 10300, Thailand

    Saisamorn Lumyong

  12. Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun City, 130118, Jilin Province, People’s Republic of China

    Chayanard Phukhamsakda

  13. Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai, 50200, Thailand

    Chanokned Senwanna

  14. Center for Mountain Futures, Kunming Institute of Botany, Kunming, 650201, Yunnan, People’s Republic of China

    Saowaluck Tibpromma

Authors
  1. K. W. Thilini Chethana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruvishika S. Jayawardena
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yi-Jyun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sirinapa Konta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Saowaluck Tibpromma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chayanard Phukhamsakda
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pranami D. Abeywickrama
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Milan C. Samarakoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chanokned Senwanna
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ausana Mapook
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Xia Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Deecksha Gomdola
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Diana S. Marasinghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Oundhyalah D. Padaruth
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Abhaya Balasuriya
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Jianping Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Saisamorn Lumyong
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Kevin D. Hyde
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kevin D. Hyde.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Handling editor: Hiran Ariyawansa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chethana, K.W.T., Jayawardena, R.S., Chen, YJ. et al. Appressorial interactions with host and their evolution. Fungal Diversity 110, 75–107 (2021). https://doi.org/10.1007/s13225-021-00487-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13225-021-00487-5

Keywords

Search

Navigation