Mycosphaerellales » Mycosphaerellaceae » Ramularia

Ramularia endophylla

Ramularia endophylla Verkley & U. Braun, in Verkley et al., Mycol. Res. 108(11): 1276 (2004).

≡ Sphaeria punctiformis Pers., Ann. Bot. (Usteri) 11: 26 (1794).

= Mycosphaerella punctiformis (Pers.) Starbäck, Bih. K. svenska VetenskAkad. Handl., Afd. 3 15(no. 2): 9 (1889).

Index Fungorum number: IF 500737; Facesoffungi number: FoF 11213, Fig. 1–3

Description: see Hyde et al. (2013); Videira et al. (2017).

Material examined: see Hyde et al. (2013); Videira et al. (2017).

Fig. 1 Mycosphaerella punctiformis (= Ramularia endophylla; re-illustrated from Hyde et al. 2013). a Label and herbarium specimens of Mycosphaerella punctiformis. b Appearance of ascomata on host surface. c Section through ascoma. d Section through peridium. e–h Ascus. i–l Ascospores. Scale bars: c = 50 μm, d–h = 10 μm, i–l =5 μm.

Fig. 2 Mycosphaerella punctiformis (epitype, CBS herb. 7949, re-drawn from Verkley et al. 2014). a Ascospores and asci in planta. b Germinating ascospores on MEA. Scale bars = 10 μm.

Fig. 3 Mycosphaerella punctiformis (CBS 113265 – ex-epitype). Conidiogenous cells and conidia in culture. Scale bar =10 μm.

Importance and distribution

Species of Mycosphaerella (= Ramularia) are plant pathogens, saprobes, endophytes (saprobic or plant-pathogenic), and some have mutualistic (in lichen) associations (Crous et al. 2000, 2001; Verkley et al. 2004). Many species of Mycosphaerella (= Ramularia) have been reported to cause severe leaf spot, defoliation and shoot die-back (Crous 1998; Crous et al. 2004b, 2006g; Hunter et al. 2006a, b; Burgess et al. 2007). There are 1588 Mycosphaerella epithets in Index Fungorum (2022), but many have been synonymized or transferred to other genera including Amycosphaerella, Arecophila, Austroafricana, Batcheloromyces, Cercospora, Cladosporium, Davidiella, Delphinella, Didymella, Fusoidiella, Keissleriella, Metasphaeria, Pallidocercospora, Parateratosphaeria, Passalora, Pezicula, Phyllachora, Planistromella, Sphaerellothecium, Stigmidium, Teratosphaeria and Venturia. There are 1,252 species as Mycosphaerella and 410 species as Ramularia known on a wide range of hosts and geographical locations. Mycosphaerella needs a thorough revision and an updated monograph of accepted species is required. No doubt many more species of Mycosphaerella will be discovered in the future but they need to be substantiated with DNA molecular data.

Industrial relevance and applications

Mycosphaerella is useful to the medical and pharmaceutical industry due to the ability to produce wide range of compounds such as (-) mycousnine which exhibits high and selective immunosuppressive activity on T Cells (Wang et al. 2017).

Quarantine significance

Mycosphaerella polygoni-cuspidati is a potential biological control agent for the invasive weed Fallopia japonica (Japanese knotweed), which is bothersome in Europe and North America (Kurose et al. 2016). Other species of Mycosphaerella may have potential to control other pathogens due to their ability to colonize dead tissue of a non-host, perhaps to produce propagules to enable onwards dispersal (“pogo stick hypothesis”) (Verkley et al. 2014).

Biochemical importance of the genus, chemical diversity or applications

Members of Mycosphaerella (= Ramularia) have the ability to produce a wide array of chemicals such as -(2-butyl)-6-ethyl-3-hydroxy-6-methylcyclohex-2-ene-1,5-dione, 3-(2-butyl)-6-ethyl-5-hydroxy-2-methoxy-6-methyl-cyclohex-2-enone (Moreno et al. 2011). Other compounds such as -Mycousunine and (±)-Isomycousunine which are phytotoxic usunic acid derivatives have been reported from M. nawae (Sassa et al. 1989). They may also produce various enzymes, phytotoxins (e.g. fijiensin) and secondary compounds (Upadhyay et al. 1990).

References

Arx JA von. 1983 – Mycosphaerella and its anamorphs. Proceedings van de Koninklijke Nederlandse Akademie van Wetenschappen Series 86, 15–54.

Braun U. 1995 – A monograph of Cercosporella, Ramularia and allied genera (phytopathogenic hyphomycetes). Vol. 1. IHW-Verlag, Eching, Munich, Germany.

Burgess TI, Barber PA, Sufaati S, Xu D, Hardy GE. St J, Dell B. 2007 – Mycosphaerella spp. on Eucalyptus in Asia; new species, new hosts and new records. Fungal Diversity 24, 135–157.

Crous PW, Aptroot A, Kang JC, Braun U, Wingfield MJ. 2000 – The genus Mycosphaerella and its anamorphs. Studies in Mycology 45, 107–121.

Crous PW, Groenewald JZ, Mansilla JP. 2004b – Phylogenetic reassessment of Mycosphaerella spp. and their anamorphs occurring on Eucalyptus. Studies in Mycology 50, 195–214.

Crous PW, Kang JC, Braun U. 2001 – A phylogenetic redefinition of anamorph genera in Mycosphaerella based on ITS rDNA sequence and morphology. Mycologia 93, 1081–1101.

Crous PW, Summerell BA, Carnegie AJ, Mohammed C et al. 2007 – Foliicolous Mycosphaerella spp. and their anamorphs on Corymbia and Eucalyptus. Fungal Diversity 26, 143–185.

Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ et al. 2009c – Novel species of Mycosphaerellaceae and Teratosphaeriaceae. Persoonia 23, 119– 146.

Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ. 2009e – Unravelling Mycosphaerella: do you believe in genera? Persoonia 23, 99–118.

Crous PW, Verkley GJM, Groenewald JZ, Samson RA. 2009e – Fungal Biodiversity. CBS Laboratory Manual Series 1: 1–269. CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands.

Crous PW. 1998 – Mycosphaerella spp. and their anamorphs associated with leaf spot diseases of Eucalyptus. Mycologia Memoir 21, 1–170.

Hunter GC, Wingfield BD, Crous PW, Wingfield MJ. 2006 – A multi-gene phylogeny for species of Mycosphaerella occurring on Eucalyptus leaves. Studies in Mycology 55, 147–161.

Hyde KD, Jones EBG, Liu JK, Ariyawansa H et al. 2013 – Families of Dothideomycetes. Fungal Diversity 63, 1–313.

Johanson CJ. 1885 – Svampar frăn Island. Bestämda af C.J. Johanson. Öfversigt af Kongl. VetenskapsAkademiens Föhandlingar 41, 157–174.

Kirschner R. 2009 – Cercosporella and Ramularia. Mycologia 101, 110–119.

Klebahn H. 1918 – Borntraeger; Leipzig, Germany: Haupt und Nebenfruchtformen der Askomyzeten.

Kurose D, Furuya N, Saeki T, Tsuchiya K, Tsushima S, Seier MK. 2016 – Species-Specific Detection of Mycosphaerella polygoni-cuspidati as a Biological Control Agent for Fallopia japonica by PCR Assay. Molecular biotechnology 58, 626–633.

Laibach F. 1922 – Untersuchungen über einige Ramularia und Ovularia-Arten und ihre Beziehungen zur Ascomyzetengat tung Mycosphaerella. II. Centralblatt für Bakteriologie und Parasitenkunde, Zweite Abtheilung 55, 284–293.

Moreno E, Varughese T, Spadafora C, Arnold AE et al. 2011 – Chemical constituents of the new endophytic fungus Mycosphaerella sp. nov. and their anti-parasitic activity. Natural product communications 6, 835–840.

Crous PW, Groenewald JZ. 2006 –Mycosphaerella alistairii. Fungal Planet No. 4.

Rossman AY, Crous PW, Hyde KD, Hawksworth DL et al. 2015 – Recommended names for pleomorphic genera in Dothideomycetes. IMA Fungus 6, 507– 523.

Sassa T, Igarashi M, Nukina M. 1989 – Mycousunine and (±)-Isomycousunine, New Phytotoxic Usunic Acid Derivatives from the Phytopathogenic Fungus, Mycosphaerella nawae. Agricultural and Biological Chemistry 53, 1743–1744.

Sutton BC, Hennebert GL. 1994 – Interconnections amongst anamorphs and their possible contribution to Ascomycete systematics. In: Hawksworth DL. (ed.): Ascomycete Systematics. Problems and perspectives in the nineties. pp. 77–98. Plenum Press, New York.

Upadhyay RK, Strobel GA, Coval SJ, Clardy J. 1990 – Fijiensin, the first phytotoxin from Mycosphaerella fijiiensis, the causative agent of Black Sigatoka disease. Experientia 46, 982–984.

Verkley GJM, Crous PW, Groenewald JZ, Braun U, Aptroot A. 2004 – Mycosphaerella punctiformis revisited: morphology, phylogeny, and epitypification of the type species of the genus Mycosphaerella (Dothideales, Ascomycota). Mycological Research 108, 1271–1282.

Videira SIR, Groenewald JZ, Braun U, Shin HD, Crous PW. 2016 – All that glitters is not Ramularia. Studies in Mycology 83, 49–163.

Videira SIR, Groenewald JZ, Kolecka A, Haren LV et al. 2015a – Elucidating the Ramularia eucalypti species complex. Persoonia 34, 50–64.

Videira SIR, Groenewald JZ, Nakashima C, Braun U, Barreto RW, de Wit PJGM, Crous PW. 2017 – Mycosphaerellaceae - Chaos or clarity? Studies in Mycology 87, 257–421.

Videira SIR, Groenewald JZ, Verkley GJM et al. 2015b –The rise of Ramularia from the Mycosphaerella labyrinth. Fungal Biology 119, 823– 843.

Wang X, Li Y, Zhang X, Lai D, Zhou L. 2017 – Structural Diversity and Biological Activities of the Cyclodipeptides from Fungi. Molecules (Basel, Switzerland) 22, 2026.