Zymoseptoria tritici

Last updated

Zymoseptoria tritici
Septoria-tritici.jpg
Zymoseptoria tritici on leaves of wheat
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Dothideomycetes
Order: Capnodiales
Family: Mycosphaerellaceae
Genus: Zymoseptoria
Species:
Z. tritici
Binomial name
Zymoseptoria tritici
(Roberge ex Desm.) Quaedvl. & Crous (2011)
Synonyms

Septoria curtisiana Sacc., (1884) [1]
Septoria graminumDesm., (1843)
Septoria tritici Desm., 1842 [2] Septoria triticiBerk. & M.A. Curtis, (1874) [3]
Septoria tritici var. lolicolaR. Sprague & Aar. G. Johnson, (1944) [4]
Sphaeria graminicolaFuckel, (1865) [5]
Sphaerella graminicolaFuckel, (1870) [6]
Mycosphaerella graminicola(Fuckel) J. Schröt., (1894) [7]

Contents

Zymoseptoria tritici, synonyms Septoria tritici, Mycosphaerella graminicola, is a species of filamentous fungus, an ascomycete in the family Mycosphaerellaceae . It is a wheat plant pathogen causing septoria leaf blotch that is difficult to control due to resistance to multiple fungicides. The pathogen today causes one of the most important diseases of wheat. [8]

In 2011, Quaedvlieg et al. introduced a new combination for this species: Zymoseptoria tritici, [9] as they found that the type strains of both the genus Mycosphaerella (linked to the anamorph genus Ramularia) and the genus Septoria (linked to the genus Septoria, an extensive clade of very distinct septoria-like species within the Mycosphaerellaceae) clustered separately from the clade containing both Zymoseptoria tritici and Z. passerinii. Since 2011, a total of eight Zymoseptoria species have been described within the genus Zymoseptoria; Z. tritici (the type of the genus Zymoseptoria), Z. pseudotritici, Z. ardabiliae, Z. brevis, Z. passerinii, Z. halophila, Z. crescenta and Z. verkleyi (Named after Gerard J.M. Verkleij, for the contribution that he has made to further the understanding of the genus Septoria). [10]

Description

Ripe pycnidia of Zymoseptoria tritici in a primary leaf of a susceptible wheat seedling. High humidity stimulates the extrusion of cyrrhi, tendril-like mucilages containing asexual pycnidiospores that are rain-splash dispersed over short distances. Mycosphaerella graminicola 8.png
Ripe pycnidia of Zymoseptoria tritici in a primary leaf of a susceptible wheat seedling. High humidity stimulates the extrusion of cyrrhi, tendril-like mucilages containing asexual pycnidiospores that are rain-splash dispersed over short distances.

This fungus causes septoria tritici blotch of wheat, a disease characterized by necrotic blotches on the foliage. [11] These blotches contain asexual (pycnidia) and sexual (pseudothecia) fructifications. [11]

Asexual state (anamorph, asexual stage was previously named as Septoria tritici): Pycnidiospores are hyaline and threadlike and measure 1.7-3.4 x 39-86 μm, with 3 to 7 indistinct septations. Germiniation of pycnidiospores can be lateral or terminal. Cirrhi are milky white to buff. Sometimes in culture nonseptate, hyaline microspores, measuring 1-1.3 × 5-9 μm, occur outside pycnidia by yeastlike budding. [12]

Simultaneous penetration of a wheat leaf stoma by three germ tubes of sexual airborne ascospores (arrows) of Zymoseptoria tritici. Mycosphaerella graminicola 5.png
Simultaneous penetration of a wheat leaf stoma by three germ tubes of sexual airborne ascospores (arrows) of Zymoseptoria tritici.

Sexual state (teleomorph): Pseudothecia are subepidermal, globose, dark brown, and 68-114 μm in diameter. Asci measure 11-14 × 30-40 μm. Ascospores are hyaline, elliptical, and 2.5-4 × 9-16 μm, with two cells of unequal length. [12]

Genetics

Chromosomes 1-13 are the largest and essential. Chromosomes 14-21 are smaller and dispensable. Mycosphaerella graminicola chromosomes.png
Chromosomes 1-13 are the largest and essential. Chromosomes 14-21 are smaller and dispensable.

Zymoseptoria tritici represents an intriguing model for fundamental genetic studies of plant-pathogenic fungi. [11] It is haploid plant-pathogenic fungus. [11] Many fungi are haploid, which greatly simplifies genetic studies. [11]

Zymoseptoria tritici was the first species, in 2002, of the family Mycosphaerellaceae to have a linkage map created. [14]

The first report of fully sequenced genome of Zymoseptoria tritici from 2011 was the first genome of a filamentous fungus to be finished according to current standards. [13] The length of the genome is 39.7 Mb, [13] that is similar to other filamentous ascomycetes. [11] The genome contains 21 chromosomes, [13] that is the highest number reported among ascomycetes. [11] Furthermore, these chromosomes have an extraordinary size range, varying from 0.39 to 6.09 Mb. [11]

A striking aspect of Zymoseptoria tritici genetics is the presence of many dispensable chromosomes. [13] Eight of chromosomes could be lost with no visible effect on the fungus and thus are dispensable. [13] Dispensable chromosomes have been found in other fungi but they usually occur at a low frequency and typically represent single or a few chromosomes. [11] Dispensable chromosomes have originated by ancient horizontal transfer from an unknown donor, that was followed by extensive genetic recombination, a possible mechanism of stealth pathogenicity and exciting new aspects of genome structure. [13]

A surprising[ opinion ] feature of the Zymoseptoria tritici genome compared to other sequenced plant pathogens was that it contained very few genes for enzymes that break down plant cell walls, which was more similar to endophytes than to pathogens. [13] Goodwin et al. (2011) [13] suggested, that the stealth pathogenesis of Zymoseptoria tritici probably involves degradation of proteins rather than carbohydrates to evade host defenses during the biotrophic stage of infection and may have evolved from endophytic ancestors. [13]

Evolution

The fungus Zymoseptoria tritici has been a pathogen of wheat since host domestication 10,000–12,000 years ago in the Fertile Crescent. [8] The wheat-infecting lineage emerged from closely related Mycosphaerella pathogens infecting wild grasses. [8] It has coevolved and spread with its host globally. [8] Zymoseptoria tritici shows a significantly higher degree of host specificity and virulence in a detached leaf assay. [8]

The emergence and "co-domestication" of Zymoseptoria tritici was associated with an adaptation to wheat and an agricultural environment. [8] Endemic descendants of the progenitor of Zymoseptoria tritici are still found on wild grasses in the Middle East; however these "wild" pathogens show a broader host range than the "domesticated" wheat pathogen. [8] The closest known relative of Zymoseptoria tritici is named Z. pseudotritici B. [8] Zymoseptoria pseudotritici was isolated in Iran from the two grass species Agropyron repens and Dactylis glomerata growing in close proximity to fields planted to bread wheat ( Triticum aestivum ). [8] Although Z. tritici is a frequent pathogen of wheat in Iran, no evidence of gene flow between Z. pseudotritici and Z. tritici was detected based on sequence analysis of six nuclear loci. [8]

Life cycle

Zymoseptoria tritici overwinters as fruiting bodies on crop debris, mostly as pseudothecia (sexual fruiting bodies) but sometimes also some pycnidia (asexual fruiting bodies). [15] The sexual spores are quantitatively the more significant spores involved in primary inoculum of the disease, while the asexual spores are more significant in the secondary cycle. [16] In early spring, ascospores, the sexual spores of the fungus, are released from the pseudothecia. Ascospores are wind-dispersed and eventually land on the leaves of a host plant (bread wheat or durum wheat). Unlike most other plant pathogens, Zymoseptoria tritici uses a germ tube to enter the host leaf through stomata rather than by direct penetration. [17] There is a long latent period of up to two weeks following infection before symptoms develop. [13] The fungus evades host defenses during the latent phase, followed by a rapid switch to necrotrophy immediately prior to symptom expression 12–20 days after penetration. [13] The period between infection and formation of sporulating structures (latent period) was estimated to be 20.35 ± 4.15 days for Zymoseptoria tritici in Northern Germany and decreased with increasing temperature. [18] Such a switch from biotrophic to necrotrophic growth at the end of a long latent period is an unusual characteristic shared by most fungi in the genus Mycosphaerella. [13] Very little is known about the cause or mechanism of this lifestyle switch even though Mycosphaerella is one of the largest and most economically important genera of plant-pathogenic fungi. [13]

Primary inoculum requires wet conditions and cool temperatures of 50-68 °F. [19] Under appropriate environmental conditions, lesions are able to develop on infected leaves, and soon pycnidia begin to develop on the lesions. [19] The pycnidia appear as small dark dots on the lesions. From the pycnidia, conidiospores, the asexual spores of the fungus, are released. These asexual spores are dispersed via rain splash and are response for the secondary inoculum of this polycyclic disease cycle. [17] When the conidiospores are splashed onto leaves, they act similarly to ascospores and cause the development of foliar lesions. In addition to pycnidia, pseudothecia also develop within these lesions. Pycnidia and pseudothecia are the structures in which the fungus overwinters, and the cycle begins again.[ citation needed ]

Disease Management

Zymoseptoria tritici is a difficult fungus to control because populations contain extremely high levels of genetic variability and it has very unusual biology for a pathogen. [13] Z. tritici has an active sexual cycle under natural conditions, which is an important driver of septoria tritici blotch epidemics and results in high genetic diversity of populations in the field. [11]

The most effective, economical, and simple method of Z. tritici management is planting resistant cultivars. Twenty-one resistant genes have been named, mapped, and published. [20] Mikaberidze and McDonald 2020 found a fitness tradeoff between genes for Septoria tolerance and Septoria resistance in wheat. [21] Some cultivars are resistant in one region but susceptible in another; it depends on the local pathogen population. All varieties of bread wheat and durum wheat are susceptible to the disease to some extent, but planting varieties that have at least partial resistance to the local population of Zymoseptoria tritici can greatly improve yield.

There are also cultural management strategies that may be effective, including regular rotation of crops, deep plowing, and late planting. [15] More specifically, rotating a recently infected field to any non-host crop can be useful in minimizing the amount of fungus present in the field. Planting winter wheat after the first ascospore flights in September is a way to reduce primary inoculum of winter wheat. [22]

Fungicide use often simply is not economical for Septoria Leaf Blotch. The rapid evolution of pathogen resistance to fungicides is a major barrier. Zymoseptoria tritici has resistance to multiple fungicides, because it has number of substitutions of CYP51. CYP51 substitutions include Y137F which confers resistance to triadimenol, I381V which confers resistance to tebuconazole and V136A that confers resistance to prochloraz. [23] Chemical control of the pathogen (using fungicides) now relies on the application of SDHIs, [24] azole fungicides which are demethylase inhibitors that inhibit lanosterol 14 alpha-demethylase (CYP51) activity. [23]

The last method of control for Zymoseptoria tritici is biological control using bacteria. Bacillus megaterium has been shown to cause about an 80% decrease in disease development in the trials done so far. [17] Pseudomonads are also a promising bacterial control option. A benefit to using pseudomonads or bacillus is that they are not harmed by most fungicides, so they can be used in combination with chemical controls. [17] However, a lack of commercial availability limits the use of biological controls.[ citation needed ]

Disease Importance

The ascomycete fungus Zymoseptoria tritici causes septoria tritici blotch, a foliar disease of wheat that poses a significant threat to global food production. [13] It is the primary foliar disease of winter wheat in most western European countries. [23] Zymoseptoria tritici infects wheat crops throughout the world and is also currently a big problem in Iran, Tunisia, and Morocco. [17] Severe epidemics of the disease have decreased wheat yields by 35-50%. [17] In the United States, Septoria leaf blotch is a very important disease in wheat, second only to wheat rust. An estimated $275 million is lost per year in the US due to this disease. In Europe the annual losses are equivalent to over 400 million USD. [17]

Different areas of the world are currently trying different management strategies. For example, in the Nordic-Baltic region, one of the largest wheat-producing regions of the world, the use of fungicides has substantially increased wheat yields. [25] The fungicides that have been shown to be effective include quinone outside inhibitors (QoIs), which, like most fungicides, are expensive to apply in large quantities. As climate change begins to increase temperatures around the globe, Zymoseptoria tritici, along with many other fungal pathogens, is likely to show increased overwintering survival and therefore more substantial primary inocula. [26] The need for effective management techniques will become even more important as the prevalence of Septoria leaf blotch increases with climate change. [27]

Related Research Articles

<span class="mw-page-title-main">Powdery mildew</span> Fungal plant disease

Powdery mildew is a fungal disease that affects a wide range of plants. Powdery mildew diseases are caused by many different species of ascomycete fungi in the order Erysiphales. Powdery mildew is one of the easier plant diseases to identify, as the signs of the causal pathogen are quite distinctive. Infected plants display white powdery spots on the leaves and stems. This mycelial layer may quickly spread to cover all of the leaves. The lower leaves are the most affected, but the mildew can appear on any above-ground part of the plant. As the disease progresses, the spots get larger and denser as large numbers of asexual spores are formed, and the mildew may spread up and down the length of the plant.

<span class="mw-page-title-main">Black sigatoka</span> Pathogenic fungus

Black sigatoka is a leaf-spot disease of banana plants caused by the ascomycete fungus Mycosphaerella fijiensis (Morelet), also known as black leaf streak. It was discovered in 1963 and named for its similarities with yellow Sigatoka, which is caused by Mycosphaerella musicola (Mulder), which was itself named after the Sigatoka Valley in Fiji. In the same valley an outbreak of this disease reached epidemic proportions from 1912 to 1923.

Pyrenophora teres is a necrotrophic fungal pathogen of some plant species, the most significant of which are economically important agricultural crops such as barley. Toxins include aspergillomarasmine A and related compounds.

The cereal grain wheat is subject to numerous wheat diseases, including bacterial, viral and fungal diseases, as well as parasitic infestations.

<i>Venturia inaequalis</i> Species of fungus

Venturia inaequalis is an ascomycete fungus that causes the apple scab disease.

<i>Blumeria graminis</i> Fungal pathogen of grasses

Blumeria graminis is a fungus that causes powdery mildew on grasses, including cereals. It is the only species in the genus Blumeria. It has also been called Erysiphe graminis and Oidium monilioides or Oidium tritici.

Leptosphaeria maculans is a fungal pathogen of the phylum Ascomycota that is the causal agent of blackleg disease on Brassica crops. Its genome has been sequenced, and L. maculans is a well-studied model phytopathogenic fungus. Symptoms of blackleg generally include basal stem cankers, small grey lesions on leaves, and root rot. The major yield loss is due to stem canker. The fungus is dispersed by the wind as ascospores or rain splash in the case of the conidia. L. maculans grows best in wet conditions and a temperature range of 5–20 degrees Celsius. Rotation of crops, removal of stubble, application of fungicide, and crop resistance are all used to manage blackleg. The fungus is an important pathogen of Brassica napus (canola) crops.

Spot blotch is a leaf disease of wheat caused by Cochliobolus sativus. Cochliobolus sativus also infects other plant parts and in conjunction with other pathogens causes common root rot and black point.

Leptosphaeria coniothyrium is a plant pathogen. It can be found around the world.

<i>Pyrenophora tritici-repentis</i> Species of fungus

Pyrenophora tritici-repentis (teleomorph) and Drechslera tritici-repentis (anamorph) is a necrotrophic plant pathogen of fungal origin, phylum Ascomycota. The pathogen causes a disease originally named yellow spot but now commonly called tan spot, yellow leaf spot, yellow leaf blotch or helminthosporiosis. At least eight races of the pathogen are known to occur based on their virulence on a wheat differential set.

<i>Phaeosphaeria nodorum</i> Species of fungus

Phaeosphaeria nodorum is a major fungal pathogen of wheat, causing the disease Septoria nodorum blotch. It is a member of the Dothideomycetes, a large fungal taxon that includes many important plant pathogens affecting all major crop plant families.

<i>Ascochyta</i> Genus of fungi

Ascochyta is a genus of ascomycete fungi, containing several species that are pathogenic to plants, particularly cereal crops. The taxonomy of this genus is still incomplete. The genus was first described in 1830 by Marie-Anne Libert, who regarded the spores as minute asci and the cell contents as spherical spores. Numerous revisions to the members of the genus and its description were made for the next several years. Species that are plant pathogenic on cereals include, A. hordei, A. graminea, A. sorghi, A. tritici. Symptoms are usually elliptical spots that are initially chlorotic and later become a necrotic brown. Management includes fungicide applications and sanitation of diseased plant tissue debris.

Mycosphaerella angulata is a fungal plant pathogen infecting muscadine grapes. This pathogen causes the common disease angular leaf spot. Mycosphaerella angulate is an ascomycete in the fungi kingdom.

<i>Didymella pinodes</i> Species of fungus

Didymella pinodes is a hemibiotrophic fungal plant pathogen and the causal agent of ascochyta blight on pea plants. It is infective on several species such as Lathyrus sativus, Lupinus albus, Medicago spp., Trifolium spp., Vicia sativa, and Vicia articulata, and is thus defined as broadrange pathogen.

Septoria cannabis is a species of plant pathogen from the genus Septoria that causes the disease commonly known as Septoria leaf spot. Early symptoms of infection are concentric white lesions on the vegetative leaves of cannabis plants, followed by chlorosis and necrosis of the leaf until it is ultimately overcome by disease and all living cells are then killed. Septoria, which is an ascomycete and pycnidia producing fungus, has been well known to attack Solanaceae and Cucurbitaceae species as well as many tree species. This genus is known to comprise over 1,000 species of pathogens, each infecting a specific and unique host.

<i>Didymella bryoniae</i> Species of fungus

Didymella bryoniae, syn. Mycosphaerella melonis, is an ascomycete fungal plant pathogen that causes gummy stem blight on the family Cucurbitaceae, which includes cantaloupe, cucumber, muskmelon and watermelon plants. The anamorph/asexual stage for this fungus is called Phoma cucurbitacearum. When this pathogen infects the fruit of cucurbits it is called black rot.

<i>Septoria malagutii</i> Species of fungus

Septoria malagutii is a fungal plant pathogen infecting potatoes. The casual fungal pathogen is a deuteromycete and therefore has no true sexual stage. As a result, Septoria produces pycnidia, an asexual flask shaped fruiting body, on the leaves of potato and other tuber-bearing spp. causing small black to brown necrotic lesions ranging in size from 1-5mm. The necrotic lesions can fuse together forming large necrotic areas susceptible to leaf drop, early senescence, dieback, and dwarfing. Septoria malagutii has been found only in the Andean countries of Bolivia, Ecuador, Peru, and Venezuela at altitudes of near 3000 meters. Consequently, the fungi grows and disperses best under relatively low temperatures with high humidities, with optimal growth occurring at 20 °C (68 °F). The disease has caused devastation on potato yields in South America and in areas where this disease is common, potato yields have been seen to drop by 60%.

<span class="mw-page-title-main">Ascochyta diseases of pea</span> Group of diseases affecting pea plants

Ascochyta blights occur throughout the world and can be of significant economic importance. Three fungi contribute to the ascochyta blight disease complex of pea. Ascochyta pinodes causes Mycosphaerella blight. Ascochyta pinodella causes Ascochyta foot rot, and Ascochyta pisi causes Ascochyta blight and pod spot. Of the three fungi, Ascochyta pinodes is of the most importance. These diseases are conducive under wet and humid conditions and can cause a yield loss of up to fifty percent if left uncontrolled. The best method to control ascochyta blights of pea is to reduce the amount of primary inoculum through sanitation, crop-rotation, and altering the sowing date. Other methods—chemical control, biological control, and development of resistant varieties—may also be used to effectively control ascochyta diseases.

Leaf blotch may refer to:

Sarrah Ben M'barek-Ben Romdhane is a Tunisian-Dutch crop researcher. She works on developing fungus-resistant wheat strains to reduce the toll of Mycosphaerella graminicola on yields.

References

This article incorporates CC-BY-2.5 text from references [8] [11] [13] [23]

  1. ↑ Saccardo P. A. (1884). Syll. fung. (Abellini) 3: 561.
  2. ↑ 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, Bot., sér. 2, 17: 91-118. page 107.
  3. ↑ Berk. & Curtis M. A. (1874). N. Amer. Fung.: no. 441 bis.
  4. ↑ Sprague R. & Johnson A. G. (1944). In: Sprague, Ore. St. Monog., Bot.6: 32.
  5. ↑ Fuckel (1865). Fungi rhenani exsic.: no. 1578.
  6. ↑ Fuckel (1870). Jb. nassau. Ver. Naturk.23-24: 101.
  7. ↑ Schröter J. (1894). In: Cohn, "Kryptogamen-Flora von Schlesien" (Breslau) 3-2(9): 257-384. page 340.
  8. 1 2 3 4 5 6 7 8 9 10 11 Stukenbrock E.H., Jørgensen F.G., Zala M., Hansen T.T., McDonald B.A. & Schierup M.H. (2010). "Whole-Genome and Chromosome Evolution Associated with Host Adaptation and Speciation of the Wheat Pathogen Mycosphaerella graminicola". PLoS Genetics6(12): e1001189. doi : 10.1371/journal.pgen.1001189
  9. ↑ Quaedvlieg, W.; Kema, G. H. J.; Groenewald, J. Z.; Verkley, G. J. M.; Seifbarghi, S.; Razavi, M.; Gohari, A. M.; Mehrabi, R.; Crous, P. W. (2011). "Zymoseptoria gen. Nov.: A new genus to accommodate Septoria-like species occurring on graminicolous hosts". Persoonia. 26: 57–69. doi:10.3767/003158511X571841. PMC   3160802 . PMID   22025804.
  10. ↑ "Zymoseptoria". Global Biodiversity Information Facility . Retrieved 24 March 2024.
  11. 1 2 3 4 5 6 7 8 9 10 11 Wittenberg A.H.J., van der Lee T.A.J., Ben M'Barek S., Ware S.B., Goodwin S.B., et al. (2009). "Meiosis Drives Extraordinary Genome Plasticity in the Haploid Fungal Plant Pathogen Mycosphaerella graminicola". PLoS ONE4(6): e5863. doi : 10.1371/journal.pone.0005863.
  12. 1 2 Wiese, M.V. (1987). Compendium of wheat diseases. American Phytopathological Society. p. 124.
  13. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Goodwin S.B., Ben M'Barek S., Dhillon B., Wittenberg A.H.J., Crane C.F., et al. (2011). "Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis". PLoS Genetics7(6): e1002070. doi : 10.1371/journal.pgen.1002070
  14. ↑ Kema, G. H.; Goodwin, S. B.; Hamza, S.; Verstappen, E. C.; Cavaletto, J. R.; Van Der Lee, T. A.; De Weerdt, M.; Bonants, P. J.; Waalwijk, C. (2002). "A combined amplified fragment length polymorphism and randomly amplified polymorphism DNA genetic kinkage map of Mycosphaerella graminicola, the septoria tritici leaf blotch pathogen of wheat". Genetics. 161 (4): 1497–1505. doi:10.1093/genetics/161.4.1497. PMC   1462205 . PMID   12196395.
  15. 1 2 "Fungal Leaf Spot Diseases of Wheat: Tan spot, Septoria/Stagonospora nodorum blotch and Septoria tritici blotch — Publications". www.ag.ndsu.edu. Retrieved 2020-12-06.
  16. ↑ Suffert, F.; Sache, I.; Lannou, C. (April 2011). "Early stages of septoria tritici blotch epidemics of winter wheat: build-up, overseasoning, and release of primary inoculum: Primary inoculum of Mycosphaerella graminicola". Plant Pathology. 60 (2): 166–177. doi: 10.1111/j.1365-3059.2010.02369.x .
  17. 1 2 3 4 5 6 7 "Septoria tritici blotch (STB) of wheat". Septoria tritici blotch (STB) of wheat. Retrieved 2020-12-06.
  18. ↑ Henze M., Beyer M., Klink H. & Verreet J.-A. (2007). "Characterizing meteorological scenarios favorable for Septoria tritici infections in wheat and estimation of latent periods". Plant Disease91: 1445-1449.
  19. 1 2 Markell, Sam (26 October 2006). "Fungal Leaf-Spotting Diseases of Wheat: Septoria Blotch, Stagonospora Blotch and Tan Spot". University of Arkansas Division of Agriculture. Retrieved 6 December 2020.
  20. ↑ Brown, James K.M.; Chartrain, Laëtitia; Lasserre-Zuber, Pauline; Saintenac, Cyrille (June 2015). "Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding". Fungal Genetics and Biology. 79: 33–41. doi:10.1016/j.fgb.2015.04.017. PMC   4510316 . PMID   26092788.
  21. ↑ Pagán, Israel; García-Arenal, Fernando (2020-08-25). "Tolerance of Plants to Pathogens: A Unifying View". Annual Review of Phytopathology . 58 (1). Annual Reviews: 77–96. doi:10.1146/annurev-phyto-010820-012749. hdl: 10261/339066 . ISSN   0066-4286. PMID   32403981. S2CID   218632778.
  22. ↑ "Leaf Blotch Diseases of Wheat—Septoria tritici Blotch, Stagonospora nodorum Blotch and Tan Spot". ohioline.osu.edu. Retrieved 2020-12-06.
  23. 1 2 3 4 Mullins J. G. L., Parker J. E., Cools H. J., Togawa R. C., Lucas J. A., et al. (2011). "Molecular Modelling of the Emergence of Azole Resistance in Mycosphaerella graminicola". PLoS ONE 6(6): e20973. doi : 10.1371/journal.pone.0020973.
  24. ↑ Downie, Rowena C.; Lin, Min; Corsi, Beatrice; Ficke, Andrea; Lillemo, Morten; Oliver, Richard P.; Phan, Huyen T. T.; Tan, Kar-Chun; Cockram, James (2021-07-27). "Septoria Nodorum Blotch of Wheat: Disease Management and Resistance Breeding in the Face of Shifting Disease Dynamics and a Changing Environment". Phytopathology . 111 (6). American Phytopathological Society: PHYTO–07–20–028. doi:10.1094/phyto-07-20-0280-rvw. hdl: 20.500.11937/83208 . ISSN   0031-949X. PMID   33245254. S2CID   227181536.
  25. ↑ Jalli, Marja; Kaseva, Janne; Andersson, Björn; Ficke, Andrea; Nistrup-Jørgensen, Lise; Ronis, Antanas; Kaukoranta, Timo; Ørum, Jens-Erik; Djurle, Annika (October 2020). "Yield increases due to fungicide control of leaf blotch diseases in wheat and barley as a basis for IPM decision-making in the Nordic-Baltic region". European Journal of Plant Pathology. 158 (2): 315–333. Bibcode:2020EJPP..158..315J. doi: 10.1007/s10658-020-02075-w . hdl: 11250/2732701 . ISSN   0929-1873. S2CID   220611931.
  26. ↑ Cotuna, Otilia (2018). "Influence of Crop Management on the Impact of Zymoseptoria tritici in Winter Wheat in the Context of Climate Change: An Overview". Research Journal of Agricultural Science. 50: 69–76.
  27. ↑ Fones, Helen; Gurr, Sarah (2015). "The impact of Septoria tritici Blotch disease on wheat: An EU perspective". Fungal Genetics and Biology. 79: 3–7. doi:10.1016/j.fgb.2015.04.004. PMC   4502551 . PMID   26092782.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.