Zymoseptoria Tritici

Abstract

Zymoseptoria tritici is a filamentous, ascomycete fungus that causes the important foliar disease of wheat, septoria tritici blotch (STB). This disease is of particular concern in Europe and temperate climates worldwide. There are no completely effective methods of control against it. This article summarises the current understanding of Z. tritici biology and its interaction with the wheat host. The fungal pathogen's biology and life cycle are outlined including colonisation, the asymptomatic period, the aggressive necrotrophic period and sporulation. The potential role of Z. tritici effector proteins during infection of the host and the wheat host's resistance genes are also discussed. Finally, recent advances in Z. tritici research and its importance for the development of control methods against STB are explored.

Main points: (1) Zymoseptoria tritici is a serious threat to wheat production worldwide. (2) Currently, there are no durable control methods. (3) This article will summarise the current understanding of the pathogen, specific methods of control and future perspectives. (4) A better understanding of this pathogen will help the development of future control strategies.

Key Concepts

  • Wheat is one of the top three most important cereal crops grown worldwide.
  • Zymoseptoria tritici causes the major disease of wheat, septoria tritici blotch (STB).
  • The lifecycle of Z. tritici comprises an asymptomatic phase, followed by the necrotic phase of infection and spore dispersal.
  • Infection of wheat by Z. tritici is characterised by necrotic lesions on the leaves with dark brown asexual fruiting bodies known as pycnidia.
  • The fungus releases virulence (effector) proteins to aid the successful colonisation and manipulation of the wheat hosts' defence response.
  • The wheat host can defend itself via immune receptors that trigger defence responses.
  • Current methods of control against Z. tritici include the use of fungicides and resistant wheat varieties.
  • Recent tools to study Z. tritici may help the development of novel methods of control against this pathogen.

Keywords: Zymoseptoria tritici; wheat; pathogen; effector; resistance

Figure 1. Zymoseptoria tritici growth on solid media (potato dextrose agar) and in liquid media (potato dextrose broth): (a) Z. tritici colony after a 7‐day incubation period on agar is rosy‐pink in colour and composed of yeast‐like cells; (b) the same colony after 30 days incubation period is hyphal with a black melanised base and white aerial hyphae; (c) Z. tritici cells in liquid media at 3 days incubation period are yeast‐like, short, with some branching; (d) at 10 days incubation period, the fungal cells are long, branched and hyphal.
Figure 2. Infection cycle of Z. tritici. Primary infection occurs via wind‐dispersed ascospores, and secondary infection via rainsplashed pycnidiospores. After contact with the leaf, the fungal spores germinate and enter the host via the stomata. At 0–14 days postinfection, Z. tritici undergoes the asymptomatic period of infection. During this period, the hyphae grow around the plant cells, but no symptoms are visible on the leaf. At 14–21 days postinfection, Z. tritici switches to necrotophic growth. This period is characterised by an increase in fungal biomass and the appearance of chlorotic and necrotic lesions on the leaves. Between 21 and 28 days postinfection, asexual and sexual fruiting bodies develop within the lesions. The fungus releases asexual pycnidia and sexual ascospores from the fruiting bodies, and overwinters in crop debris.
Figure 3. Symptoms of STB caused by Z. tritici IPO323 on susceptible wheat cultivar. Riband at 28 days postinfection: (a) infected wheat leaves are covered with necrotic lesions and pycnidia (black dots); (b) pycnidia within substomatal cavity of wheat leaf oozing cirrhus; (c) pycnidiospores extracted from cirrhus and stained with lactophenol cotton blue.
close

References

Adhikari TB, Balaji B, Breeden J, et al. (2007) Resistance of wheat to Mycosphaerella graminicola involves early and late peaks of gene expression. Physiological and Molecular Plant Pathology 71: 55–68.

Bowler J, Scott E, Tailor R, et al. (2010) New capabilities for Mycosphaerella graminicola research. Molecular Plant Pathology 11 (5): 691–704.

Brading PA, Verstappen ECP, Kema GHJ, et al. (2002) A gene‐for‐gene relationship between wheat and Mycosphaerella graminicola, the septoria tritici blotch pathogen. Phytopathology 92 (4): 439–445.

Braun HJ, Atlin G and Payne T (2010) Multi‐location testing as a tool to identify plant response to global climate change. In: Reynolds MP (ed) Climate Change and Crop Production, pp. 115–138. Wallingford: CABI Publishers.

Brown JKM, Chartrain L, Lasserre‐Zuber P, et al. (2015) Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genetics and Biology 79: 33–41.

Chartrain L, Brading PA, Makepeace JC, et al. (2004) Sources of resistance to septoria tritici blotch and implications for wheat breeding. Plant Pathology 53 (4): 454–460.

Chartrain L, Brading PA and Brown JKM (2005) Presence of the Stb6 gene for resistance to septoria tritici blotch (Mycosphaerella graminicola) in cultivars used in wheat‐breeding programmes worldwide. Plant Pathology 54 (2): 134–143.

Cools HJ and Fraaije BA (2013) Update on mechanisms of azole resistance in Mycosphaerella graminicola and implications for future control. Pest Management Science 69 (2): 150–155.

Cowger C, Hoffer ME and Mundt CC (2000) Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathology 49 (4): 445–451.

Duncan KE and Howard RJ (2000) Cytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola. Mycological Research 104 (9): 1074–1082.

Eyal Z, Scharen AL, Prescott JM, et al. (1987) The Septoria Diseases of Wheat: Concepts and Methods of Disease Management, 1st edn. Mexico: CIMMYT.

Eyal Z (1999) The septoria tritici and stagonospora nodorum blotch diseases of wheat. European Journal of Plant Pathology 105: 629–641.

Fones HN and Gurr S (2015) The impact of septoria tritici blotch disease on wheat: an EU perspective. Fungal Genetics and Biology 79: 3–7.

Fones HN, Eyles CJ, Kay W, et al. (2017) A role for random humidity‐dependent epiphytic growth prior to invasion of wheat by Zymoseptoria tritici. Fungal Genetics and Biology 106: 51–60.

Franco‐Orozco B, Berepiki A, Ruiz O, et al. (2017) A new proteinaceous pathogen‐associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae. New Phytologist 214: 1657–1672.

Ghaffary SMT, Faris JD, Friesen TL, et al. (2012) New broad‐spectrum resistance to septoria tritici blotch derived from synthetic hexaploid wheat. Theoretical and Applied Genetics 124 (1): 125–142.

Goodwin SB, M'Barek SB, Dhillon B, et al. (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genetics 7 (6): e1002070.

Jones JD and Dangl JL (2006) The plant immune system. Nature 444: 323–329.

Kema GHJ, Verstappen ECP, Todorova M, et al. (1996a) Successful crosses and molecular tetrad and progeny analyses demonstrate heterothallism in Mycosphaerella graminicola. Current Genetics 30 (3): 251–258.

Kema GH, Yu D and Rijkenberg F (1996b) Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86 (7): 777–786.

Kema GHJ and van Silfhout CH (1997) Genetic variation for virulence and resistance in the wheat‐Mycosphaerella graminicola pathosystem III. Comparative seedling and adult plant experiments. Phytopathology 87: 266–272.

Kettles GJ, Bayon C, Canning G, et al. (2017) Apoplastic recognition of multiple candidate effectors from the wheat pathogen Zymoseptoria tritici in the nonhost plant Nicotiana benthamiana. New Phytologist 213: 338–350.

Kettles GJ, Bayon C, Sparks C, et al. (2018) Characterisation of an antimicrobial and phytotoxic ribonuclease secreted by the fungal wheat pathogen Zymoseptoria tritici. New Phytologist 217: 320–331.

Kilaru S, Schuster M, Studholme D, et al. (2015) A codon‐optimised green fluorescent protein for live cell imaging in Zymoseptoria tritici. Fungal Genetics and Biology 79: 125–131.

Lee WS, Rudd JJ, Hammond‐Kosack K, et al. (2014) Mycosphaerella graminicola LysM effector‐mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Molecular Plant‐Microbe Interactions 27: 236–243.

Lee J, Orosa B, Millyard L, et al. (2015) Functional analysis of a Wheat Homeodomain protein, TaR1, reveals that host chromatin remodelling influences the dynamics of the switch to necrotrophic growth in the phytopathogenic fungus Zymoseptoria tritici. New Phytologist 206: 598–605.

M'Barek SB, Cordewener JH, Ghaffary SM, et al. (2015) FPLC and liquid‐chromatography mass spectrometry identify candidate necrosis‐inducing proteins from culture filtrates of the fungal wheat pathogen Zymoseptoria tritici. Fungal Genetics and Biology 79: 54–62.

Marshall R, Kombrink A, Motteram J, et al. (2011) Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiology 156: 756–769.

Millyard L, Lee J, Zhang C, et al. (2016) The ubiquitin conjugating enzyme, TaU4 regulates wheat defence against the phytopathogen Zymoseptoria tritici. Scientific Reports 6: 35683.

Motteram J, Küfner I, Deller S, et al. (2009) Molecular characterization and functional analysis of MgNLP, the sole NPP1 domain–containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola. Molecular Plant‐Microbe Interactions 22: 790–799.

Nødvig CS, Nielsen JB, Kogle ME, et al. (2015) A CRISPR‐Cas9 system for genetic engineering of filamentous fungi. PLoS One 10 (7): 1–18.

Oerke EC (2006) Crop losses to pests. Journal of Agricultural Science 144: 31–43.

Omrane S, Audeon C, Ignace A, et al. (2017) Plasticity of the MFS1 promoter leads to multi drug resistance in the wheat pathogen Zymoseptoria tritici. mSphere 2 (5): e00393‐17.

Orton ES, Deller S and Brown JK (2011) Mycosphaerella graminicola: from genomics to disease control. Molecular Plant Pathology 12: 413–424.

Owen WJ, Yao C, Myung K, et al. (2017) Biological characterization of fenpicoxamid, a new fungicide with utility in cereals and other crops. Pest Management Science 73 (10): 2005–2016.

Palma‐Guerrero J, Torriani SF, Zala M, et al. (2016) Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles. Molecular Plant Pathology 17 (6): 845–859.

Palmer CL and Skinner W (2002) Pathogen profile Mycosphaerella graminicola: latent infection, crop devastation and genomics. Molecular Plant Pathology 3 (2): 63–70.

Ponomarenko A, Goodwin SB and Kema GHJ (2011) Septoria tritici blotch (STB) of wheat. Plant Health Instructor 10.

Ray S, Anderson JM, Urmeev FI, et al. (2003) Rapid induction of a protein disulfide isomerase and defense‐related genes in wheat in response to the hemibiotrophic fungal pathogen Mycosphaerella graminicola. Plant Molecular Biology 53: 741–754.

Rudd JJ, Kanyuka K, Hassani‐Pak K, et al. (2015) Transcriptome and metabolite profiling of the infection cycle of Zymoseptoria tritici on wheat reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions and a variation on the hemibiotrophic lifestyle definition. Plant Physiology 167 (3): 1158–1185.

Sánchez‐Vallet A, McDonald MC, Solomon PS, et al. (2015) Is Zymoseptoria tritici a hemibiotroph? Fungal Genetics and Biology 79: 29–32.

Shetty NP, Mehrabi R, Lütken H, et al. (2007) Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytologist 174: 637–647.

Shetty NP, Jensen JD, Knudsen A, et al. (2009) Effects of β‐1, 3‐glucan from Septoria tritici on structural defence responses in wheat. Journal of Experimental Botany 60: 4287–4300.

Sidhu YS, Cairns TC, Chaudhari YK, et al. (2015) Exploitation of sulfonylurea resistance marker and non‐homologous end joining mutants for functional analysis in Zymoseptoria tritici. Fungal Genetics and Biology 79: 102–109.

Sierotzki H and Scalliet G (2013) A review of current knowledge of resistance aspects for the next‐generation succinate dehydrogenase inhibitor fungicides. Phytopathology 103 (9): 880–887.

Stukenbrock EH, Banke S, Javan‐Nikkhah M, et al. (2007) Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Molecular Biology and Evolution 24 (2): 398–411.

Torriani SFF, Melichar JPE, Mills C, et al. (2015) Zymoseptoria tritici: a major threat to wheat production, integrated approaches to control. Fungal Genetics and Biology 79: 8–12.

Quaedvlieg W, Kema GHJ, Groenewald JZ, et al. (2011) Zymoseptoria gen. nov.: a new genus to accommodate septoria‐like species occurring on graminicolous hosts. Persoonia 26: 57–69.

Zhong Z, Marcel TC, Hartmann FE, et al. (2017) A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytologist 214: 619–631.

Welch T, Feechan A and Kildea S (2018) Effect of host resistance on genetic structure of core and accessory chromosomes in Irish Zymoseptoria tritici populations. European Journal of Plant Pathology 150 (1): 139–148.

Zwiers LH and De Waard MA (2001) Efficient Agrobacterium tumefaciens‐mediated gene disruption in the phytopathogen Mycosphaerella graminicola. Current Genetics 39 (5–6): 388–393.

Further Reading

Dean R and Van Kan J (2012) The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant 13: 414–430.

Friesen T (2017) Nicotiana benthamiana as a nonhost of Zymoseptoria tritici. New Phytologist 213 (1): 7–9.

Kettles GJ and Kanyuka K (2016) Dissecting the molecular interactions between wheat and the fungal pathogen Zymoseptoria Tritici. Frontiers in Plant Science 7: 508.

O'Driscoll A, Kildea S, Doohan F, Spink J and Mullins E (2014) The wheat–septoria conflict: a new front opening up? Trends in Plant Science 19 (9): 602–610.

Solomon PS (2017) Have we finally opened the door to understanding septoria tritici blotch disease in wheat? New Phytologist 214 (2): 493–495.

Steinberg G (2015) Cell biology of Zymoseptoria tritici: pathogen cell organization and wheat infection. Fungal Genetics and Biology 79: 17–23.

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

* Required Field

How to Cite close
Tiley, Anna MM, Karki, Sujit J, and Feechan, Angela(May 2018) Zymoseptoria Tritici. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027948]