Magnaporthe and Its Relatives

Abstract

One of the main current societal challenges is the production of food supplies to feed a constantly growing human population. In the forthcoming years, we will have to increase the global production of staple cereals such as rice to achieve this goal. Several factors compromise this objective, including the variation of raining patterns due to climate change and pathogen infections that drastically reduce crop yields. Wheat and rice are frequently affected by diseases caused by several root‐infecting species of Magnaporthales such as Gaeumannomyces graminis, Magnaporthiopsis rhizophila and Nakatea oryzae (syn. Magnaporthe salvinii). Other economically significant root pathogen of this fungal family is Magnaporthiopsis poae, which causes severe damages in turfs used for sport courts flooring and home lawns. The blast fungus Magnaporthe oryzae, an extremely damaging airborne fungal pathogen of wheat and rice, also infects underground tissues. This is in accordance with the distinct penetration strategies displayed by M. oryzae during aerial and underground plant colonisation.

Key Concepts

  • A clade is a phylogenetic group, which comprises a single common ancestor and all the descendants of that ancestor.
  • The appressorium in Magnaporthales is a melanised fungal structure required for penetration of aerial plant tissues, and it is formed at the tips of spore germ tubes or hyphae.
  • An hyphopodium in Magnaporthales is a specialised structure produced at the tip of the hyphae to penetrate roots. Gaemannomyces sp. can produce simple or lobed hyphopodia. M. oryzae produces simple hyphopodia.
  • Disease‐suppressive soils are soils in which little or no disease occurs under favorable conditions for disease development. Generally, this is due to the presence of indigenous soil microbes.
  • The immune response in rice roots and leaves against the blast disease differs.

Keywords: root infection; take‐all; rice blast; hyphopodium; fungal pathogenesis

Figure 1. G. graminisandM. oryzaepenetrate plant roots by means of hyphopodia. (a) Light microscope image and (b) scanning electron micrograph of lobed hyphopodia on Mylar films developed by G. graminis strains. Reproduced with permission from Money et al. 1998. © Elsevier. (c) Confocal image of M. oryzae hyphopodia on rice roots. (d) Scanning electron micrograph of M. oryzae hyphopodia on hydrophilic polystyrene. (c,d) Reproduced with permission from Illana et al. 2013. © Springer Nature.
Figure 2. Disease symptoms of take‐all on wheat and summer patch disease on turfgrass. (a) Pigmented runner hyphae of G. tritici on the surface of a wheat root. Reproduced with permission from Cook 2003. © Elsevier. (b) Adult wheat plants with severe take‐all rot symptoms on the roots and the stem base. Courtesy of AHDB (Agriculture and Horticulture Development Board, UK)/BASF. (c) Circular patches of wheat plants in a field showing typical take‐all disease symptoms with visible white heads and stunted growth. Courtesy of Kansas State University. (d) Necrotic root lesions caused by M. poae. (e) Typical circular patches of yellow‐brown colour on turfgrass caused by M. poae. (d,e) Courtesy of Dr. Lane Tredway, North Carolina State University.
Figure 3. Disease symptoms and fungal structures produced by the rice blast fungusM. oryzae. (A) Panicle blast symptoms in a rice field. (B) Noninfected (left) and infected (right) rice panicle with necrotic lesions on neck (a), leaf (b) and collar (c). (A,B) Courtesy of Dr. Yulin Jia, USDA‐ARS, Dale Bumpers National Rice Research Center. (C) Fallen panicle showing necrosis in the neck. (D,E) Typical diamond‐shaped lesions with brown margins on 3‐weeks‐old rice leaves. (F) Necrotic symptoms on rice roots. (G) Scanning electron micrograph of M. oryzae conidia (CO) producing appressoria (AP) on barley leaves. (H) Confocal image of M. oryzae conidia on hydrophilic polystyrene membranes producing simple hyphopodia‐like structures and preinvasive hyphae. The image was taken at 24 h using tetramethylrhodamine isothiocyanate (TRITC)‐labelled wheat germ agglutinin (antichitin lectin), which is shown in red. The pre‐invasive hyphae (pre‐IH) shows reduced levels of chitin compared to the cell wall of the hyphopodium (HY).
Figure 4. Rice blast disease infection cycle. Right panel: M. oryzae leaf cycle. M. oryzae leaf infection cycle starts when a conidium lands on a leaf and attaches to the surface. Shortly after, the conidium produces a small germ tube, which differentiates into a melanised appressorium. A penetration peg formed at the base of the appressorium crosses the plant cell wall initiating fungal invasion. Invasive growth is different compared to the fungal growth on leaf surfaces. The invasive hypha moves beyond the first infected cell during a few days. Finally, conidiophores emerge, and the fungus initiates sporulation between 6 and 15 days, releasing thousands of conidia during weeks to the environment. Reproduced with permission from Ribot et al. 2008. © Elsevier. Left panel: M. oryzae root infection cycle potentially begins from infected plant debris or dormant structures present in the soil. These resting structures can germinate and penetrate into the plant roots. Fungal hypha colonises the vascular system of the root spreading systemically. The fungus moves to the upper parts of the plant producing typical blast lesions from which conidia are formed. These spores are dispersed to other plants by wind or water, propagating the disease. Reproduced with permission from Illana et al. 2013. © Springer Nature.
close

References

Besi MI, Tucker SL and Sesma A (2009) Magnaporthe and its relatives. In: Encyclopedia of Life Sciences (eLS). Chichester: John Wiley & Sons, Ltd.

Bowyer P, Clarke BR, Lunness P, Daniels MJ and Osbourn AE (1995) Host‐range of a plant‐pathogenic fungus determined by a saponin detoxifying enzyme. Science 267 (5196): 371–374.

Bryan GT, Wu K‐S, Farrall L, et al. (2000) A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi‐ta. Plant Cell 12 (11): 2033–2046.

Campo S, Peris‐Peris C, Sire C, et al. (2013) Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance‐associated macrophage protein 6) gene involved in pathogen resistance. New Phytologist 199 (1): 212–227.

Campos‐Soriano L and San Segundo B (2009) Assessment of blast disease resistance in transgenic PRms rice using a gfp‐expressing Magnaporthe oryzae strain. Plant Pathology 58: 677–689.

Cannon PF (1994) The newly recognized family Magnaporthaceae and its interrelationships. Systema Ascomycetum 13: 25–42.

Castroagudín VL, Moreira SI, Pereira DAS, et al. (2016) Pyricularia graminis‐tritici, a new Pyricularia species causing wheat blast. Persoonia 37 (1): 199–216.

Chanclud E and Morel JB (2016) Plant hormones: a fungal point of view. Molecular Plant Pathology 17 (8): 1289–1297.

Chanclud E, Kisiala A, Emery NR, et al. (2016) Cytokinin production by the rice blast fungus is a pivotal requirement for full virulence. PLoS Pathogens 12 (2): e1005457.

Cook RJ (2003) Take‐all of wheat. Physiological and Molecular Plant Pathology 62: 73–86.

Couch BC and Kohn LM (2002) A multilocus gene genealogy concordant with host preference indicates segregation of a new species, Magnaporthe oryzae, from M. grisea. Mycologia 94 (4): 683–693.

Cruz CD and Valent B (2017) Wheat blast disease: danger on the move. Tropical Plant Pathology 42 (3): 210–222.

Daval S, Lebreton L, Gracianne C, et al. (2013) Strain‐specific variation in a soilborne phytopathogenic fungus for the expression of genes involved in pH signal transduction pathway, pathogenesis and saprophytic survival in response to environmental pH changes. Fungal Genetics and Biology 61: 80–89.

Fukuoka S, Saka N, Koga H, et al. (2009) Loss of function of a proline‐containing protein confers durable disease resistance in rice. Science 325 (5943): 998–1001.

Funnell Deanna L, Schardl Christopher L and Bednarek Pawel (2010) Plant Defences against Fungal Attack: Biochemistry. In: Encyclopedia of Life Sciences (eLS). Chichester: John Wiley & Sons, Ltd. DOI: 10.1002/9780470015902.a0001323.pub2

Gladieux P, Condon B, Ravel S, et al. (2018) Gene flow between divergent cereal‐ and grass‐specific lineages of the rice blast fungus Magnaporthe oryzae. mBio 9 (1): e01219–17.

Godfrey Dale and Rathjen JP (2012) Recognition and Response in Plant PAMP Triggered Immunity. In: Encyclopedia of Life Sciences (eLS). Chichester: John Wiley & Sons, Ltd. DOI: 10.1002/9780470015902.a0023725

Guimil S, Chang HS, Zhu T, et al. (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proceedings of the National Academy of Sciences of the United States of America 102 (22): 8066–8070.

Hashimoto M, Kisseleva L, Sawa S, et al. (2004) A novel rice PR10 protein, RSOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signaling pathway. Plant & Cell Physiology 45 (5): 550–559.

Hernandez‐Restrepo M, Groenewald JZ, Elliott ML, et al. (2016) Take‐all or nothing. Studies in Mycology 83: 19–48.

Hibbett DS, Binder M, Bischoff JF, et al. (2007) A higher‐level phylogenetic classification of the Fungi. Mycological Research 111: 509–547.

Illana A, Rodriguez‐Romero J and Sesma A (2013) Major plant pathogens of the Magnaporthaceae family. In: Horwitz BA (ed) Genomics of Soil‐ and Plant‐associated Fungi, pp. 45–88. Berlin/Heidelberg: Springer‐Verlag Ltd.

Islam MT, Croll D, Gladieux P, et al. (2016) Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biology 14 (1): 84.

Klaubauf S, Tharreau D and Fournier E (2014) Resolving the polyphyletic nature of Pyricularia (Pyriculariaceae). Studies in Mycology 79: 85–120.

Li Y, Lu YG, Shi Y, et al. (2014) Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiology 164 (2): 1077–1092.

Liu W and Wang G‐L (2016) Plant innate immunity in rice: a defense against pathogen infection. National Science Review 3 (3): 295–308.

Luo J and Zhang N (2013) Magnaporthiopsis, a new genus in Magnaporthaceae (Ascomycota). Mycologia 105 (4): 1019–1029.

Luo J, Qiu H, Cai GH, et al. (2015) Phylogenomic analysis uncovers the evolutionary history of nutrition and infection mode in rice blast fungus and other Magnaporthales. Scientific Reports 5 (1): 9448.

Luo J, Vines PL, Grimshaw A, et al. (2017) Magnaporthiopsis meyeri‐festucae, sp. nov., associated with a summer patch‐like disease of fine fescue turfgrasses. Mycologia 109 (5): 780–789.

Marcel S, Sawers R, Oakeley E, Angliker H and Paszkowski U (2010) Tissue‐adapted invasion strategies of the rice blast fungus Magnaporthe oryzae. Plant Cell 22 (9): 3177–3187.

Mitsuhara I, Iwai T, Seo S, et al. (2008) Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense‐related signal compounds (121/180). Molecular Genetics and Genomics 279 (4): 415–427.

Money NP, Caesar‐TonThat TC, Frederick B and Henson JM (1998) Melanin synthesis is associated with changes in hyphopodial turgor, permeability, and wall rigidity in Gaeumannomyces graminis var. graminis. Fungal Genetics and Biology 24 (1–2): 240–251.

Muthukrishnan S, Liang GH, Trick HN and Gill BS (2001) Pathogenesis‐related proteins and their genes in cereals. Plant Cell Tissue and Organ Culture 64: 93–114.

Ning YS, Liu WD and Wang GL (2017) Balancing immunity and yield in crop plants. Trends in Plant Science 22 (12): 1069–1079.

Okagaki LH, Sailsbery JK, Eyre AW and Dean RA (2016) Comparative genome analysis and genome evolution of members of the magnaporthaceae family of fungi. BMC Genomics 17: 135.

Patkar RN, Benke PI, Qu Z, et al. (2015) A fungal monooxygenase‐derived jasmonate attenuates host innate immunity. Nature Chemical Biology 11 (9): 733–740.

Redecker D, Kodner R and Graham LE (2000) Glomalean fungi from the Ordovician. Science 289 (5486): 1920–1921.

Ribot C, Hirsch J, Batzergue S, et al. (2008) Susceptibility of rice to the blast fungus, Magnaporthe grisea. Journal of Plant Physiology 165 (1): 114–124.

Rosas JE, Martínez S, Bonnecarrère V, et al. (2016) Comparison of phenotyping methods for resistance to stem rot and aggregated sheath spot in rice. Crop Science 56: 1619–1627.

Schreiber C, Slusarenko AJ and Schaffrath U (2011) Organ identity and environmental conditions determine the effectiveness of nonhost resistance in the interaction between Arabidopsis thaliana and Magnaporthe oryzae. Molecular Plant Pathology 12 (4): 397–402.

Sesma A and Osbourn AE (2004) The rice leaf blast pathogen undergoes developmental processes typical of root‐infecting fungi. Nature 431: 582–586.

Sun Z, He Y, Li J, Wang X and Chen J (2015) Genome‐wide characterization of rice black streaked dwarf virus‐responsive microRNAs in rice leaves and roots by small RNA and degradome sequencing. Plant Cell Physiology 56 (4): 688–699.

Tamasloukht M, Sejalon‐Delmas N, Kluever A, et al. (2003) Root factors induce mitochondrial‐related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiology 131 (3): 1468–1478.

Thongkantha S, Jeewon R, Vijaykrishna D, et al. (2009) Molecular phylogeny of Magnaporthaceae (Sordariomycetes) with a new species Ophioceras chiangdaoense from Dracaena loureiroi in Thailand. Fungal Diversity 34: 157–173.

Tian L, Shi S, Nasir F, et al. (2018) Comparative analysis of the root transcriptomes of cultivated and wild rice varieties in response to Magnaporthe oryzae infection revealed both common and species‐specific pathogen responses. Rice (NY) 11 (1): 26.

Tredway LP (2006) Genetic relationships among Magnaporthe poae isolates from turfgrass hosts and relative susceptibility of ‘Penncross’ and ‘Penn A‐4’ creeping bentgrass. Plant Disease 90: 1531–1538.

Tucker SL, Besi MI, Galhano R, et al. (2010) Common genetic pathways regulate organ‐specific infection‐related development in the rice blast fungus. Plant Cell 22 (3): 953–972.

Vasudevan K, Vera Cruz CM, Gruissem W and Bhullar NK (2016) Geographically distinct and domain‐specific sequence variations in the alleles of rice blast resistance gene Pib. Frontiers in Plant Science 7: 915.

Wennman A and Oliw EH (2013) Secretion of two novel enzymes, manganese 9S‐lipoxygenase and epoxy alcohol synthase, by the rice pathogen Magnaporthe salvinii. Journal of Lipid Research 54 (3): 762–775.

Yamaguchi T, Yamada A, Hong N, et al. (2000) Differences in the recognition of glucan elicitor signals between rice and soybean: beta‐glucan fragments from the rice blast disease fungus Pyricularia oryzae that elicit phytoalexin biosynthesis in suspension‐cultured rice cells. Plant Cell 12 (5): 817–826.

Zhai C, Lin F, Dong ZQ, et al. (2011) The isolation and characterization of Pik, a rice blast resistance gene which emerged after rice domestication. New Phytologist 189 (1): 321–334.

Zhang N, Luo J, Rossman AY, et al. (2016a) Generic names in Magnaporthales. IMA Fungus 7 (1): 155–159.

Further Reading

Arx JA and Olivier DL (1952) The taxonomy of Ophiobolus graminis Sacc. Transactions of the British Mycological Society 35 (1): 29–33.

Azizi P, Rafii MY, Abdullah SN, et al. (2016) Toward understanding of rice innate immunity against Magnaporthe oryzae. Crit Rev Biotechnol 36 (1): 165–174.

Fernandez J, Marroquin‐Guzman M and Wilson RA (2014) Mechanisms of nutrient acquisition and utilization during fungal infections of leaves. Annual Review of Phytopathology 52: 155–174.

Foster AJ, Ryder LS, Kershaw MJ and Talbot NJ (2017) The role of glycerol in the pathogenic lifestyle of the rice blast fungus Magnaporthe oryzae. Environmental Microbiology 19 (3): 1008–1016.

Freeman J and Ward E (2004) Gaeumannomyces graminis, the take‐all fungus and its relatives. Molecular Plant Pathology 5 (4): 235–252.

McNeill J, Barrie FR, Buck WR, et al. (2012) International Code of Nomenclature for Algae, Fungi, and Plants (Melbourne Code). Regnum Vegetabile 154. Königstein: Koeltz Scientific Books.

Sprague SJ, Watt M, Kirkegaard JA and Howlett BJ (2007) Pathways of infection of Brassica napus roots by Leptosphaeria maculans. New Phytologist 176 (1): 211–222.

Sukno SA, Garcia VM, Shaw BD and Thon MR (2008) Root infection and systemic colonization of maize by Colletotrichum graminicola. Applied and Environmental Microbiology 74 (3): 823–832.

Vereijssen J, Schneider HJM and Termorshuizen AJ (2004) Possible root infection of Cercospora beticola in sugar beet. European Journal of Plant Pathology 110: 103–106.

Yan X and Talbot NJ (2016) Investigating the cell biology of plant infection by the rice blast fungus Magnaporthe oryzae. Current Opinion in Microbiology 34: 147–153.

Web Links

FungiDB – an integrated genomic and functional genomic database for the fungal kingdom, http://fungidb.org/fungidb

Magnaporthe grisea genome database (Ensembl Fungi), https://fungi.ensembl.org/Magnaporthe_oryzae/Info/Index

Magnaporthe oryzae Poly(A) Sites Database provides all polyadenylation sites mapped in M. oryzae genome. Rodríguez‐Romero J, Marconi M, Ortega‐Campayo V, et al. (2018) Virulence‐ and signaling‐associated genes display a preference for long 3′UTRs during rice infection and metabolic stress in the rice blast fungus. New Phytologist. DOI: 10.1111/nph.15405.

Oryzabase: Integrated Rice Science Database, http://www.shigen.nig.ac.jp/rice/oryzabase/top/top.jsp

OrygenesDB: an interactive tool for rice reverse genetics, http://orygenesdb.cirad.fr

PHI base (Pathogen‐Host Interaction database) offers molecular and biological information on genes involved in host‐pathogen interactions, http://www.phi‐base.org

Phytopathogenic Fungi and Oomycete EST Database provides Expressed Sequence Tags obtained from eighteen species of plant pathogenic fungi, two species of phytopathogenic oomycetes and three species of saprophytic fungi. Soanes DM and Talbot NJ (2005) A bioinformatic tool for analysis of EST transcript abundance during infection‐related development by Magnaporthe grisea. Molecular Plant Pathology 6: 503–512. https://ore.exeter.ac.uk/repository/handle/10871/581.

RAP‐DB: The Rice Annotation Project Database, http://rapdb.dna.affrc.go.jp

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Ortega‐Campayo, Víctor, Pérez‐Martín, Marta, and Sesma, Ane(Nov 2018) Magnaporthe and Its Relatives. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021311.pub2]