Zymoseptoria tritici - a global threat for wheat production

Text contributed by: Andrea Sanchez-Vallet, Carolina Sardinha, Javier Palma-Guerrero, Lukas Meile, Julien Alassimone, Petteri Karisto, Anik Dutta, Alexey Mikaberidze, Xin Ma, Simone Fouché, Ziming Zhong and Bruce McDonald

Introduction

Zymoseptoria tritici is the causal agent of septoria tritici blotch (STB), the main leaf disease of wheat in temperate regions (Fones and Gurr 2015) and a major threat for wheat production globally. It causes chlorotic lesions after a latent period of between 9 and 14 dpi that develop into necrotic tissue where the asexual fruiting bodies (pycnidia) develop. STB is especially damaging in humid and temperate areas where yield losses may reach up to 50%. Control of STB relies mainly on fungicide treatments. It is estimated that approximately 70% of fungicides used on wheat in Europe are aimed at controlling Z. tritici (Torriani et al. 2015). Z. tritici (syns. Mycosphaerella graminicola, Septoria tritici) is an Ascomycete fungus (Quaedvlieg et al. 2011) that is thought to have originated from closely related Zymoseptoria species colonizing wild grasses in the Fertile Crescent approximately 10000-12000 years ago during wheat domestication (Stukenbrock et al. 2006, Stukenbrock et al. 2010).

Pathogen Biology

The asexual stage of Z. tritici was first identified on wheat in 1842 by Desmazières (Desmazière, 1842, Shipton et al., 1951). The sexual stage was identified 130 years later by Sanderson in New Zealand (Sanderson, 1972). After sexual or asexual spores land on a leaf, they germinate and grow as filamentous hyphae that enter the host through stomata, other natural openings or wounds. The infection then enters a long asymptomatic phase, typically lasting 8-11 days after stomata penetration. During this phase the fungus colonizes the sub-stomatal cavities and apoplastic spaces without penetrating host cells. This asymptomatic phase is often called a biotrophic phase, although no feeding structures typical of biotrophic pathogens, such as haustoria and arbuscules, have been reported. This is followed by a switch to necrotrophy characterized by a collapse of the host mesophyll cells and the onset of plant cell death between 12-18 days after penetration (Kema, et al., 1996, Duncan & Howard, 1999, Steinberg, 2015). The combination of a prolonged initial asymptomatic phase, followed by a relatively rapid necrotrophic phase led to the suggestion that Z. tritici should be called a latent necrotroph instead of a hemibiotroph (Sanchez-Vallet et al., 2015).

Asexual phase of disease development

The asexual pycnidiospores are slender, elongated, hyaline, and enclosed within a pycnidium. The pycnidia are embedded in the epidermal and mesophyll tissue on both sides of the infected leaf with an opening (ostiole) on the top. The pycnidiospores can be present in two distinct morphologies within the pycnidium: a multicellular form called macropycnidiospores (35-98 x 1-3 µm and including 3-5 septa) and a unicellular form called micropycnidiospores or spermatia (8-10 x 0.8-1 µm). A mass of pycnidiospores is exuded from a pycnidium in a gelatinous matrix called a cirrhus that contains a high concentration of sugars and proteins that wrap the pycnidiospores (Fournet, 1969). The pycnidiospores are dispersed by rain-splash to neighbouring leaves over a short distance (Holmes & Colhoun, 1975) averaging approximately 20 cm (A. Mikaberidze and P. Karristo, unpublished). Many cycles of asexual reproduction can take place during a growing season.

Sexual phase of disease development

Z. tritici has a heterothallic mating system, which requires two compatible partners of opposite mating types (mat1-1 and mat1-2) to come together to produce the sexual spores. Sexual fruiting bodies called pseudothecia form beneath the host epidermis. Each ascus contains eight ascospores, the products of meiotic division followed by mitotic division, that are enclosed within each ascus. The ascospores are hyaline and consist of two cells of unequal size, measuring 2.5-4 x 9-16 µm. When the pseudothecia are mature the ascospores are ejected from the asci and can be transported by wind, enabling long-distance dispersal of the pathogen. 1-2 cycles of sexual reproduction can take place during a growing season, but the majority of sexual reproduction is thought to occur on decayed crop stubble between growing seasons.

Dimorphism

Z. tritici is a dimorphic fungus that displays environmentally regulated morphogenic transitions between filamentous hyphae and blastospores (also called yeast-like form) (Motteram et al., 2006, King et al., 2017, Yemelin et al., 2017). Filamentous growth is required for stomata penetration and host colonization and is essential for pathogenicity. The natural biological role of blastospores remains unclear. The morphological growth transitions are easily induced in vitro. Pycnidiospores placed onto growth media will preferentially replicate as blastospores via budding on nutrient-rich medium incubated at a temperature ranging from 15°C to 18°C. Pycnidiospores incubated at a high temperature (> 22°C) and/or in a nutrient-poor medium will differentiate into filamentous hyphae (Mehrabi et al., 2006, Motteram et al., 2006, King et al., 2017, Yemelin et al., 2017).

Wheat-_Zymoseptoria tritici_ interactions

To cause infection, Z. tritici needs to suppress or evade the wheat immune system. The best understood method of evasion is the tight binding of chitin by the secreted Mg3LysM protein (Marshall et al. 2011) which efficiently blocks chitin perception by the host receptors CEBiP and CERK1 (Lee et al. 2014). Tight transcriptional regulation of pathogen effectors during different phases of infection are also thought to play a major role in evading host surveillance, especially during the early asymptomatic stage (Brunner et al. 2013, Rudd et al. 2015).

The existence of gene-for-gene interactions (Flor 1971) in Z. tritici has been known for many years (Brading et al. 2002, Brown et al. 2015), but the first avirulence gene of Z. tritici, AvrStb6, was cloned only recently. Variation in the coding sequence of AvrStb6 was shown to prevent recognition (Zhong et al. 2017). Until now, major resistance gene-mediated defense was not shown to involve a hypersensitive response and the mechanisms of successful defense remain poorly understood. Another unanswered question is how the necrotrophic phase is triggered. Although several effectors were shown to induce necrosis in wheat or other plants, their role for infection of Z. tritici remains elusive (Motteram et al. 2009, M’Barek et al. 2015).

Genomics of Zymoseptoria tritici

The genome of Z. tritici consists of thirteen core chromosomes and up to eight accessory chromosomes that can be lost without a noticeable effect on pathogen fitness (Goodwin et al., 2011; Wittenberg et al., 2009). Z. tritici has the highest number of accessory chromosomes identified to date. These accessory chromosomes exhibit extensive absence/presence polymorphisms in experimental crosses and in natural field populations and differ from the core chromosomes in both gene and repetitive sequence content (Goodwin et al., 2011). Although their role in the biology of Z. tritici remains unclear, a recent study showed a correlation between the presence of some of the accessory chromosomes and increased virulence (Stewart et al., 2017). Z. tritici has frequent chromosomal rearrangements that may accelerate evolution (Plissonneau et al. 2016).

Compared to other fungal pathogens, the Z. tritici genome encodes very few genes involved in breaking down plant cell walls. This led to the hypothesis that “stealth pathogenesis” (Goodwin et al. 2011) was the strategy that enabled Z. tritici to emerge as a wheat pathogen from its mainly endophytic ancestors ~11000 years ago (Stukenbrock et al., 2007). When compared to its closely related sister species that infect wild grasses, it is evident that positive selection has altered secreted proteins and putative effectors in the Z. tritici genome, (Stukenbrock et al., 2011), suggesting that the co-evolution of the pathogen on its domesticated host greatly affected pathogen evolution.

Recent studies provided detailed descriptions of the transcriptomes of Z. tritici during its infection of wheat (Kellner et al., 2014; Palma-Guerrero et al., 2016; Rudd et al., 2015). A recently published project provided a comparative transcriptome analysis that included four strains of Z. tritici during the entire infection cycle on wheat (Palma-Guerrero et al., 2017). This analysis provided the expression profiles of several gene families involved in virulence, including proteases, PCWDEs, lipases, SSPs and secreted peroxidases and showed that differences in gene expression may be major determinants of virulence variation among Z. tritici strains.

Population genetics

Population genetics studies have included Z. tritici populations sampled from approximately 30 wheat fields distributed across five continents. Comparisons of these field populations using neutral genetic markers led to identification of the center of origin and the most likely routes of gene flow among continents (CHEN & McDonald 1996; Linde et al. 2002; Zhan et al. 2003; Jurgens et al. 2006; Kabbage et al. 2009; Abrinbana et al. 2010; Chartouni et al. 2011; Drabesova et al. 2013; Naouari et al. 2016; Stukenbrock et al. 2007; Boukef et al. 2012). Neutral genetic markers have included restriction fragment length polymorphisms (RFLPs), amplified fragment length polymorphisms (AFLPs), microsatellites (SSRs), random amplified polymorphic DNA (RAPDs) and genomic sequences (McDonald 1990; McDonald & MARTINEZ 1990; McDonald & Martinez 1991; McDonald & MARTINEZ 1991; Bahkali et al. 2012; Gautier et al. 2014; Kema et al. 1996).

Z. tritici originated in the Fertile Crescent where the genetic diversity is the highest compared to other populations (Zhan et al. 2003; Stukenbrock et al. 2007). Nearly all field populations exhibit high gene and genotype diversity within populations and low genetic differentiation among populations (Linde et al. 2002; Zhan et al. 2003; Jurgens et al. 2006; Abrinbana et al. 2010; Kabbage et al. 2009; Chartouni et al. 2011; Drabesova et al. 2013; Naouari et al. 2016), consistent with high gene flow among field populations and a high level of sexual recombination within each field population. The few field populations found to have low genetic diversity were usually shown to result from inoculation by one or a few strains.

The population structure of Z. tritici, which includes high genetic diversity distributed over a small spatial scale, large effective population size, long-distance gene flow and regular sexual reproduction, facilitates rapid evolution in these populations at the field scale. This high evolutionary potential explains the rapid development of fungicide resistance and the rapid failure of major STB resistance genes like Stb6 (Torriani et al. 2009; BRUNNER et al. 2008; Estep et al. 2013; Estep et al. 2015). Intragenic recombination was proposed to play an important role in the evolution of new CYP51 alleles that provide high levels of resistance to azole fungicides (Brunner et al. 2008). QTL (quantitative trait locus) mapping led to identification of candidate genes involved in local adaptation, including for thermal adaptation, fungicide resistance and virulence on different wheat cultivars (Lendenmann et al. 2016; Stewart et al. 2016; Lendenmann et al. 2015; Zhong et al. 2017). A recent review summarizes how knowledge of Z. tritici population genetics can be used to improve management of STB (McDonald & Mundt 2016).

Epidemiology and control

STB epidemic development is a result of three processes: infection, spore production and spore dispersal. Epidemics usually start in the autumn on the emerging winter wheat seedlings. The initial source of infection is usually sexual spores (ascospores), which are dispersed by wind (spore dispersal) from infected crop debris leftover in the field from the previous season. Asexual spores are splash-dispersed and cause new infections on emerging leaves. There are usually several (4-6) asexual cycles of infection and at least one sexual cycle of infection during a growing season.

STB epidemics can be controlled by suppressing any of the three processes. Chemical control with fungicides aims to prevent initial infection and remove already established infections. Genetic control with wheat varieties carrying qualitative or quantitative resistance to STB can reduce infection and/or spore production. To date, 20 major genes showing qualitative resistance and 167 genomic regions containing quantitative trait loci (QTLs) conferring quantitative resistance to Z. tritici have been mapped (Brown et al., 2015). Crop rotations and planting crop mixtures can reduce dispersal of spores within fields and between seasons.

As a result of high levels of sexual reproduction, combined with large population sizes and long-distance dispersal, Z. tritici populations are highly diverse. This makes control of STB using genetic resistance more challenging. Breeding for qualitative resistance is not sustainable because it can be broken down relatively quickly by the rapid evolutionary potential of Z. tritici. A classic example of the breakdown of qualitative resistance to Z. tritici after four years of commercial cultivation in the USA during mid 90’s can be found in the wheat variety “Gene” (Cowger et al., 2000).

The most sustainable control measures are likely to involve an integrative approach that combines quantitative resistance (several genes with small additive effects), multi-target fungicides and agronomical practices that limit the survival of Z. tritici between growing seasons.

Links and selected references

https://www.apsnet.org/edcenter/disandpath/fungalasco/pdlessons/Pages/Septoria.aspx https://en.wikipedia.org/wiki/Mycosphaerella_graminicola https://en.wikipedia.org/wiki/Integrated_pest_management

Abrinbana, M. et al., 2010. Genetic structure of Mycosphaerella graminicola populations in Iran. Plant Pathology, 59(5), pp.829–838.

Bahkali, A.H. et al., 2012. Characterization of Novel Di-, Tri-, and Tetranucleotide Microsatellite Primers Suitable for Genotyping Various Plant Pathogenic Fungi with Special Emphasis on Fusaria and Mycospherella graminicola. International Journal of Molecular Sciences, 13(3), pp.2951–2964.

Boukef, S. et al., 2012. Frequency of mutations associated with fungicide resistance and population structure of Mycosphaerella graminicola in Tunisia. European Journal of Plant Pathology, 132(1), pp.111–122.

Brading, P. A., E. C. Verstappen, G. H. Kema and J. K. Brown (2002). “A gene-for-gene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen.” Phytopathology 92(4): 439-445.

Brown, J. K., Chartrain, L., Lasserre-Zuber, P., & Saintenac, C. (2015). Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genetics and Biology, 79, 33-41.

Brunner, P. C., S. F. Torriani, D. Croll, E. H. Stukenbrock and B. A. McDonald (2013). “Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen.” Molecular biology and evolution 30(6): 1337-1347.

Brunner, P.C., Stefanato, F.L. & McDonald, B.A., 2008. Evolution of the CYP51 gene in Mycosphaerella graminicola: evidence for intragenic recombination and selective replacement. Molecular plant pathology, 9(3), pp.305–316.

Chartouni, El, L. et al., 2011. Genetic diversity and population structure in French populations of Mycosphaerella graminicola. Mycologia, 103(4), pp.764–774.

Chen, R.S. & McDonald, B.A., 1996. Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics, 142(4), pp.1119–1127.

Cook, D. E., C. H. Mesarich and B. P. Thomma (2015). “Understanding plant immunity as a surveillance system to detect invasion.” Annual review of phytopathology 53: 541-563.

Cowger, C., Hoffer, M. E., & Mundt, C. C. (2000). Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathology, 49(4), 445-451.

Desmazières, J.B.H.J. 1842. Neuvième notice sur quelques plantes cryptogames, la plupart inédites, récemment découvertes en France, et que vont paraître en nature dans la collection publiée par l’auteur. Annales des Sciences Naturelles Botanique. 17:91-118.

Drabesova, J. et al., 2013. Population genetic structure of Mycosphaerella graminicola and Quinone Outside Inhibitor (QoI) resistance in the Czech Republic. European Journal of Plant Pathology, 135(1), pp.211–224.

Duncan, K. E., & Howard, R. J. (2000). Cytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola. Mycological research, 104(9), 1074-1082.

Estep, L.K. et al., 2015. Emergence and early evolution of fungicide resistance in North American populations of Zymoseptoria tritici. Plant Pathology, 64(4), pp.961–971.

Estep, L.K. et al., 2013. First Report of Resistance to QoI Fungicides in North American Populations of Zymoseptoria tritici, Causal Agent of Septoria Tritici Blotch of Wheat. Plant Disease, 97(11), pp.1511–1511.

Flor, H. H. (1971). Current status of the gene-for-gene concept. Annual review of phytopathology 9(1): 275-296.

Fones, H. and S. Gurr (2015). “The impact of Septoria tritici Blotch disease on wheat: an EU perspective.” Fungal Genetics and Biology 79: 3-7.

Fournet, J. 1969. Properties et role du cirrhe du Septoria nodorum Berk. Ann. Phytopathol. 87-94.

Gautier, A. et al., 2014. Development of a rapid multiplex SSR genotyping method to study populations of the fungal plant pathogen Zymoseptoria tritici. BMC research notes, 7(1), p.373.

Goodwin, S.B., M’Barek, S.B., Dhillon, B., Wittenberg, A.H.J., Crane, C.F., Hane, J.K., Foster, A.J., Lee, T.A.J.V. der, Grimwood, J., Aerts, A., Antoniw, J., Bailey, A., Bluhm, B., Bowler, J., Bristow, J., Burgt, A. van der, Canto-Canché, B., Churchill, A.C.L., Conde-Ferràez, L., Cools, H.J., Coutinho, P.M., Csukai, M., Dehal, P., Wit, P.D., Donzelli, B., Geest, H.C. van de, Ham, R.C.H.J. van, Hammond-Kosack, K.E., Henrissat, B., Kilian, A., Kobayashi, A.K., Koopmann, E., Kourmpetis, Y., Kuzniar, A., Lindquist, E., Lombard, V., Maliepaard, C., Martins, N., Mehrabi, R., Nap, J.P.H., Ponomarenko, A., Rudd, J.J., Salamov, A., Schmutz, J., Schouten, H.J., Shapiro, H., Stergiopoulos, I., Torriani, S.F.F., Tu, H., Vries, R.P. de, Waalwijk, C., Ware, S.B., Wiebenga, A., Zwiers, L.-H., Oliver, R.P., Grigoriev, I.V., Kema, G.H.J., 2011. Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis. PLOS Genet 7, e1002070. doi:10.1371/journal.pgen.1002070

Holmes, S. J. I., & Colhoun, J. (1975). Straw‐borne Inoculum of Septoria nodorum and S. tritici in relation to Incidence of Disease on Wheat Plants. Plant Pathology, 24(2), 63-66.

Kellner, R., Bhattacharyya, A., Poppe, S., Hsu, T.Y., Brem, R.B., Stukenbrock, E.H., 2014. Expression Profiling of the Wheat Pathogen Zymoseptoria tritici Reveals Genomic Patterns of Transcription and Host-Specific Regulatory Programs. Genome Biol. Evol. 6, 1353–1365. doi:10.1093/gbe/evu101.

Jurgens, T., Linde, C.C. and McDonald, B.A., 2006. Genetic structure of Mycosphaerella graminicola populations from Iran, Argentina and Australia. European Journal of Plant Pathology, 115(2), pp.223–233.

Kabbage, M. et al., 2009. Comparison of natural populations of Mycosphaerella graminicola from single fields in Kansas and California. Physiological and Molecular Plant Pathology, 74(1), pp.55–59.

Kema, G. H., Yu, D., Rijkenberg, F. H., Shaw, M. W., & Baayen, R. P. (1996). Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology, 86(7), 777-786.

King, R., Urban, M., Lauder, R. P., Hawkins, N., Evans, M., Plummer, A., … & Rudd, J. J. (2017). A conserved fungal glycosyltransferase facilitates pathogenesis of plants by enabling hyphal growth on solid surfaces. PLoS pathogens, 13(10), e1006672.

Palma-Guerrero, J., Ma, X., Torriani, S.F.F., Zala, M., Francisco, C.S., Hartmann, F.E., Croll, D., McDonald, B.A., 2017. Comparative Transcriptome Analyses in Zymoseptoria tritici Reveal Significant Differences in Gene Expression Among Strains During Plant Infection. Mol. Plant. Microbe Interact. 30, 231–244. doi:10.1094/MPMI-07-16-0146-R

Palma-Guerrero, J., Stefano F. F. Torriani, Zala, M., Carter, D., Courbot, M., Rudd, J.J., McDonald, B.A., Croll, D., 2016. Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles. Mol. Plant Pathol. 17, 845–859. doi:10.1111/mpp.12333

Plissonneau, C., A. Stürchler and D. Croll (2016). “The evolution of orphan regions in genomes of a fungal pathogen of wheat.” mBio 7(5): e01231-01216.

Quaedvlieg, W., G. Kema, J. Groenewald, G. Verkley, S. Seifbarghi, M. Razavi, A. M. Gohari, R. Mehrabi and P. Crous (2011). “Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts.” Persoonia: Molecular Phylogeny and Evolution of Fungi 26: 57.

Lee, W.-S., J. J. Rudd, K. E. Hammond-Kosack and K. Kanyuka (2014). “Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat.” Molecular Plant-Microbe Interactions 27(3): 236-243.

Lendenmann, M.H. et al., 2016. QTL mapping of temperature sensitivity reveals candidate genes for thermal adaptation and growth morphology in the plant pathogenic fungus Zymoseptoria tritici. Heredity, 116(4), pp.384–394.

Lendenmann, M.H., Croll, D. & McDonald, B.A., 2015. QTL mapping of fungicide sensitivity reveals novel genes and pleiotropy with melanization in the pathogen Zymoseptoria tritici. Fungal genetics and biology : FG & B, 80, pp.53–67.

Linde, C.C., Zhan, J. & McDonald, B.A., 2002. Population structure of Mycosphaerella graminicola: From lesions to continents. Phytopathology, 92(9), pp.946–955.

M’Barek, S. B., J. H. Cordewener, S. M. T. Ghaffary, T. A. van der Lee, Z. Liu, A. M. Gohari, R. Mehrabi, A. H. America, O. Robert and T. L. Friesen (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.

McDonald, B.A., 1990. DNA Restriction Fragment Length Polymorphisms Among Mycosphaerella graminicola(Anamorph Septoria tritici) Isolates Collected from a Single Wheat Field. Phytopathology, 80(12), p.1368.

McDonald, B.A. and Martinez, J.P., 1991. Chromosome Length Polymorphisms in a Septoria-Tritici Population. Current Genetics, 19(4), pp.265–271.

McDonald, B.A. and Martinez, J.P., 1990. Restriction Fragment Length Polymorphisms in Septoria-Tritici Occur at a High-Frequency. Current Genetics, 17(2), pp.133–138.

McDonald, B.A. and Martinez, J.P., 1991. DNA fingerprinting of the plant pathogenic fungusMycosphaerella graminicola (anamorphSeptoria tritici). Experimental Mycology, 15(2), pp.146–158.

McDonald, B.A. & Mundt, C.C., 2016. How Knowledge of Pathogen Population Biology Informs Management of Septoria Tritici Blotch. Phytopathology, 106(9), pp.948–955.

Marshall, R., A. Kombrink, J. Motteram, E. Loza-Reyes, J. Lucas, K. E. Hammond-Kosack, B. P. Thomma and J. J. Rudd (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(2): 756-769.

Mehrabi, R., Zwiers, L. H., de Waard, M. A., & Kema, G. H. (2006). MgHog1 regulates dimorphism and pathogenicity in the fungal wheat pathogen Mycosphaerella graminicola. Molecular Plant-Microbe Interactions, 19(11), 1262-1269.

Motteram, J., I. Küfner, S. Deller, F. Brunner, K. E. Hammond-Kosack, T. Nürnberger and J. J. Rudd (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(7): 790-799.

Naouari, M. et al., 2016. Mitochondrial DNA-based genetic diversity and population structure of Zymoseptoria tritici in Tunisia. European Journal of Plant Pathology, 146(2), pp.305–314.

Rudd, J.J., Kanyuka, K., Hassani-Pak, K., Derbyshire, M., Andongabo, A., Devonshire, J., Lysenko, A., Saqi, M., Desai, N.M., Powers, S.J., Hooper, J., Ambroso, L., Bharti, A., Farmer, A., Hammond-Kosack, K.E., Dietrich, R.A., Courbot, M., 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 Physiol. 167, 1158–1185.

Sánchez-Vallet, A., McDonald, M. C., Solomon, P. S., & McDonald, B. A. (2015). Is Zymoseptoria tritici a hemibiotroph?. Fungal Genetics and Biology, 79, 29-32.

Sanderson, F. R. (1972). A Mycosphaerella species as the Ascogenous state of Septoria tritici Rob. and Desm. New Zealand Journal of Botany, 10(4), 707-709.

Shipton, W. A.; Boyd, W. R. J.; Rosielle, A. A.; Shearer, B. I. 1971: The common Septoria diseases of wheat. Botanical Review 37: 231-62.

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

Stewart, E. l., Croll, D., Lendenmann, M.H., Sanchez-Vallet, A., Hartmann, F.E., Palma-Guerrero, J., Ma, X., McDonald, B.A., 2017. Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. Mol. Plant Pathol. n/a-n/a. doi:10.1111/mpp.12515

Stukenbrock, E. H., S. Banke, M. Javan-Nikkhah and B. A. McDonald (2006). “Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation.” Molecular Biology and Evolution 24(2): 398-411.

Stukenbrock, E. H., F. G. Jørgensen, M. Zala, T. T. Hansen, B. A. McDonald and M. H. Schierup (2010). “Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola.” PLos genetics 6(12): e1001189.

Stukenbrock, E.H., Bataillon, T., Dutheil, J.Y., Hansen, T.T., Li, R., Zala, M., McDonald, B.A., Wang, J., Schierup, M.H., 2011. The making of a new pathogen: Insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res. doi:10.1101/gr.118851.110

Torriani, S. F., J. P. Melichar, C. Mills, N. Pain, H. Sierotzki and M. Courbot (2015). “Zymoseptoria tritici: a major threat to wheat production, integrated approaches to control.” Fungal Genetics and Biology 79: 8-12.

Torriani, S.F.F. et al., 2009. QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Management Science, 65(2), pp.155–162.

Wittenberg, A.H.J., Lee, T.A.J. van der, M’Barek, S.B., Ware, S.B., Goodwin, S.B., Kilian, A., Visser, R.G.F., Kema, G.H.J., Schouten, H.J., 2009. Meiosis Drives Extraordinary Genome Plasticity in the Haploid Fungal Plant Pathogen Mycosphaerella graminicola. PLOS ONE 4, e5863. doi:10.1371/journal.pone.0005863.

Yemelin, A., Brauchler, A., Jacob, S., Laufer, J., Heck, L., Foster, A. J., … & Thines, E. (2017). Identification of factors involved in dimorphism and pathogenicity of Zymoseptoria tritici. PloS one, 12(8), e0183065.

Zhan, J., Pettway, R.E. & McDonald, B.A., 2003. The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal genetics and biology : FG & B, 38(3), pp.286–297.

Zhong, Z., T. C. Marcel, F. E. Hartmann, X. Ma, C. Plissonneau, M. Zala, A. Ducasse, J. Confais, J. Compain and N. Lapalu (2017). “A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene.” New Phytologist 214(2): 619-631.