Molecular basis of interactions between fungal effectors and host plants
amir mirzadi gohari 1 , Farzaneh Lak 2
1 - Plant Protection-univesity of Tehran
2 - Plant protection Department, Tehran university, Iran
Keywords: Biological function, Effector, Interaction, Plant Pathogen,
Abstract :
Molecular interactions between fungal pathogens and host plants is a very complex and dynamic process that manifests itself in two different ways such as adaptive and incompatible responses. In the adaptive state, plants become diseased as a result of pathogen attack. On the other hand, through the incompatibility state, plants show resistance after pathogen attack. One of the key aspects in these interactions is the secretion of small protein molecules by fungal pathogens. These small molecules, commonly known as effectors, are acquired during evolution by fungal pathogens. These effectors play a very vital role in changing the physiology of host plants and suppressing their defense responses. This review article examines the genetic basis of these molecular interactions between the effectors of fungal pathogens and host plants, emphasizing the patho-system consisting of the fungal pathogen Cladosporium fulvum and the tomato plant. This study can help to better understanding how the disease occurs or the resistance of host plants against fungal pathogens and provides a basis for the development of new approaches to control plant diseases.
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References:
Balesdent, M.H., Fudal, I., Ollivier, B., Bally, P., Grandaubert, J., Eber, F., Chèvre, A.M., Leflon, M. and Rouxel, T. 2013. The dispensable chromosome of L eptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytologist 198(3): 887-898.
Ballance, G., Lamari, L. and Bernier, C. 1989. Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiological and Molecular Plant Pathology 35(3): 203-213.
Barlowe, C and Miller, E. 2013. Secretory protein biogenesis and traffic in the early secretory pathway. Genetics 193(2): 383-410.
Bart, P.H.J., Thomma, H., van Esse, P., Crous, P. and de Wit, P. 2005. Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Molecular Plant Pathology 6(4): 379-393.
Basse, C.W., Kolb, S. and Kahmann, R. 2002. A maize‐specifically expressed gene cluster in Ustilago maydis. Molecular Microbiology 43(1): 75-93.
Basse, C.W., Stumpferl, S. and Kahmann, R. 2000. Characterization of a Ustilago maydis gene specifically induced during the biotrophic phase: evidence for negative as well as positive regulation. Molecular and Cellular Biology 20(1): 329-339.
Bolton, M.D., Van Esse, H.P., Vossen, J.H., De Jonge, R., Stergiopoulos, I., Stulemeijer, I.J., Van Den Berg, G.C., Borrás‐Hidalgo, O., Dekker, H.L., De Koster, C.G. and De Wit, P.J. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Molecular microbiology 69(1): 119-136.
Ciuffetti, L.M., Manning, V.A., Pandelova, I., Betts, M.F. and Martinez, J.P. 2010. Host‐selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici‐repentis–wheat interaction. New Phytologist 187(4): 911-919.
Cooke, M. 1883. New american fungi. Grevillea 12: 22-33.
de Jonge, R., Bolton, M.D., Kombrink, A., van den Berg, G.C., Yadeta, K.A. and Thomma, B.P. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Research 23(8): 1271-1282.
de Jonge, R. and Thomma, B.P. 2009. Fungal LysM effectors: extinguishers of host immunity? Trends in Microbiology 17(4): 151-157.
De Jonge, R., Peter van Esse, H., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., Van Der Krol, S., Shibuya, N., Joosten, M.H. and Thomma, B.P. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329(5994): 953-955.
de Wit, P.J. 1992. Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annual Review of Phytopathology 30(1): 391-418.
de Wit, P.J.G.M. 2016. Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato. Annual Review of Phytopathology 54(1):1-23.
de Wit, P.J.G.M., Mehrabi, R., Van Den Burg, H. and Stergiopoulos, I. 2009. Fungal effector proteins: past, present and future. Molecular Plant Pathology 10(6): 735–747.
Dean, R.A., Talbot, N.J., Ebbole, D.J., Farman, M.L., Mitchell, T.K., Orbach, M.J., Thon, M., Kulkarni, R., Xu, J.R., Pan, H. and Read, N.D. 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980–986.
Dodds, P. 2023. From Gene-for-Gene to Resistosomes: Flor's Enduring Legacy. MPMI 36(8): 461–467.
D'Silva, I. and Heath, M.C. 1997. Purification and characterization of two novel hypersensitive response-inducing specific elicitors produced by the cowpea rust fungus. Journal of Biological Chemistry 272(7): 3924-3927.
Duplessis, S., Cuomo, C.A., Lin, Y.C., Aerts, A., Tisserant, E., Veneault-Fourrey, C., Joly, D.L., Hacquard, S., Amselem, J., Cantarel, B.L. et al. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. PNAS 108(22): 9166-9171.
Friesen, T.L., Meinhardt, S.W. and Faris, J.D. 2007. The Stagonospora nodorum‐wheat pathosystem involves multiple proteinaceous host‐selective toxins and corresponding host sensitivity genes that interact in an inverse gene‐for‐gene manner. The Plant Journal 51(4): 681-692.
Ghiasi Noei, F., Imami, M., Didaran, F., Ghanbari, M.A., Zamani, E., Ebrahimi, A., Aliniaeifard, S., Farzaneh, M., Javan-Nikkhah, M., Feechan, A. and Mirzadi Gohari, A. 2022. Stb6 mediates stomatal immunity, photosynthetic functionality, and the antioxidant system during the Zymoseptoria tritici-wheat interaction. Frontier in Plant Science 13: 1004691.
Hetmann, A. and Kowalczyk, S. 2019. Suppression of PAMP-triggered immunity (PTI) by effector proteins synthesized by phytopathogens and delivered into cells of infected plant. Postepy Biochemii 22: 65(1): 58-71.
Joosten, M.H. and de Wit, P.J. 1999. The tomato– Cladosporium fulvum interaction: A versatile experimental system to study plant-pathogen interactions. Annual Review of Phytopatholog 37(1): 335-367.
Joosten, M., Vogelsang, R., Cozijnsen, T.J., Verberne, M.C. and de Wit, P.J. 1997. The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. The Plant Cell 9(3): 367-379.
Kämper, J., Kahmann, R., Bölker, M., Ma, L.J., Brefort, T., Saville, B.J., Banuett, F., Kronstad, J.W., Gold, S.E., Müller, O. and Perlin, M.H. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97–101.
Kema, G.H.J., Mirzadi Gohari, A., Aouini, L., Hay, G., Ware, S.B., Van Den Bosch, F., Manning-Smith, R., Alonso-Chavez, V., Helps, J., Ben M'Barek, S., Mehrabi, R., Diaz-Trujillo, C., Zamani, E., et al. 2018. Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance. Nature Genetics 50: 375-380.
Kruger, J., Thomas, C.M., Golstein, C., Dixon, M.S., Smoker, M., Tang, S., Mulder, L. and Jones, J.D. 2002. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296(5568): 744-747.
Lo Presti, L., Lanver, D., Schweizer, G., Tanaka, S., Liang, L., Tollot, M., Zuccaro, A., Reissmann, S. and Kahmann, R. 2015. Fungal effectors and plant susceptibility. Annual Review of Plant Biology 66: 513-545.
Luderer, R., Takken, F.L., de Wit, P.J.d. and Joosten, M.H. 2002. Cladosporium fulvum overcomes Cf‐2‐mediated resistance by producing truncated AVR2 elicitor proteins. Molecular Microbiology 45(3): 875-884.
Ma, L.J., Van Der Does, H.C., Borkovich, K.A., Coleman, J.J., Daboussi, M.J., Di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B. and Houterman, P.M. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464(7287): 367-373.
Mapuranga, J., Zhang, L., Zhang, N. and Yang Wenxiang, Y. 2022. The haustorium: The root of biotrophic fungal pathogens. Plant Pathogen Interactions 13(29): 963705.
Marshall, R., Kombrink, A., Motteram, J., Loza-Reyes, E., Lucas, J., Hammond-Kosack, K.E., Thomma, B.P. and Rudd, J.J. 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.
Mendgen, K. and Hahn, M. 2002. Plant infection and the establishment of fungal biotrophy. Trends in plant science 7(8): 352-356.
Mentlak, T.A., Kombrink, A., Shinya, T., Ryder, L.S., Otomo, I., Saitoh, H., Terauchi, R., Nishizawa, Y., Shibuya, N., Thomma, B.P. and Talbot, N.J. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. The Plant Cell 24(1): 322-335.
Gohari, A.M., Ware, S.B., Wittenberg, A.H., Mehrabi, R., M'Barek, S.B., Verstappen, E.C., Van der Lee, T.A., Robert, O., Schouten, H.J., De Wit, P.P. and Kema, G.H. 2015. Effector discovery in the fungal wheat pathogen Zymoseptoria tritici. Molecular Plant Pathology 16(9): 931-945.
Mukhi, N., Gorenkin, D. and Banfield, M.J. 2020. Exploring folds, evolution and host interactions: understanding effector structure/function in disease and immunity. New Phytologist 227 (2): 326–333.
Pedersen, C., ver Loren van Themaat, E., McGuffin, L.J., Abbott, J.C., Burgis, T.A., Barton, G., Bindschedler, L.V., Lu, X., Maekawa, T., Wessling, R., Cramer, R., Thordal-Christensen, H., Panstruga, R. and Spanu, P.D. 2012. Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13: 694.
Oerke, E.C. 2006. Crop losses to pests. The Journal of Agricultural Science 144(1): 31-43.
Rivas, S. and Thomas, C.M. 2005. Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annual Review of Phytopathology 43: 395-436.
Rooney, C.E., Van`t Klooster, J.W., van der Hoom, R.A., Joosten, M.H., Jones, J.D., de Wit, P.J. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance Science 308(5729): 1783-1786.
Raffaele, S., Farrer, R.A., Cano, L.M., Studholme, D.J., MacLean, D., Thines, M., Jiang, R.H., Zody, M.C., Kunjeti, S.G., Donofrio, N.M., Meyers, B.C., Nusbaum, C. and Kamoun, S. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage.SCIENCE 330(6010): 1540-1543.
Sánchez-Vallet, A., Fouché, S., Fudal, I., Hartmann, F.E., Soyer, J.L., Tellier, A. and Croll, D. 2018. The genome biology of effector gene evolution in filamentous plant pathogens. Annual Review of Phytopathology 56: 21-40.
Schottens-Toma I.M. and de Wit, P.J. 1988. Purification and primary structure of a necrosis-inducing peptide from the apoplastic fluids of tomato infected with Cladosporium fulvum (syn. Fulvia fulva). Physiological and Molecular Plant Pathology 33(1): 59-67.
Schirawski, J., Mannhaupt, G., Münch, K., Brefort, T., Schipper, K., Doehlemann, G. Di Stasio, M., Rössel, N., Mendoza-Mendoza, A., Pester, D. and Müller, O. 2010. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330(6010): 1546-1548.
Song, J., Win, J., Tian, M., Schornack, S., Kaschani, F., Ilyas, M., van der Hoorn, R.A. and Kamoun, S. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. PANS 106(5): 1654-1659.
Sperschneider, J., Dodds, P.N., Gardiner, D.M., Singh, K.B. and Taylor, J.M. 2018. Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Molecular Plant Pathology 19(9): 2094-2110.
Strange, R.N. and Scott, P.R. 2005. Plant disease: a threat to global food security. Annual Review of Phytopathology. 43: 83-116.
Stephenson, S.A., Hatfield, J., Rusu, A.G., Maclean, D.J. and Manners, J.M. 2000. CgDN3: an essential pathogenicity gene of Colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Molecular Plant-Microbe Interactions 13(9): 929-941.
Stergiopoulos, I., de Kock, M.J., Lindhout, P. and de Wit, P.J. 2007. Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Molecular Plant-Microbe Interactions 20(10): 1271-1283.
Stergiopoulos, I. and de Wit, P.J. 2009. Fungal effector proteins. Annual Review of Phytopathology 47: 233-263.
Takken, F.L., Luderer, R., Gabriëls, S.H., Westerink, N., Lu, R., De Wit, P.J. and Joosten, M.H. 2000. A functional cloning strategy, based on a binary PVX‐expression vector, to isolate HR‐inducing cDNAs of plant pathogens. The Plant Journal 24(2): 275-283.
Thomas, C.M., Dixon, M.S., Parniske, M., Golstein, C. and Jones, J.D. 1998. Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 353(1374): 1413-1424.
Thomma, B.P., van Esse, H.P., Crous, P.W. and de Wit, P.J. 2005. Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Molecular Plant Pathology 6(4): 379-393.
Tuori, R., Wolpert, T. and Ciuffetti, L. 1995. Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions 9(43): 10.3.
Van Kan, J.A. 2006. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends in plant science 11(5): 247-253.
Van den Burg, H.A., Harrison, S.J., Joosten, M.H., Vervoort, J. and de Wit, CP.J. 2006. ladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Molecular Plant-Microbe Interactions 19(12): 1420-1430.
Van der Does, H.C., Duyvesteijn, R., Goltstein, P., Schie, C., Manders, E., Cornelissen, B and Rep, M. 2008. Expression of effector gene SIX1 of Fusarium oxysporum requires living plant cells. Fungal Genetics Biology 45(9): 1257-1264.
van Esse, H.P., Bolton, M.D., Stergiopoulos, I., de Wit, P.J. and Thomma, B.P. 2007. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Molecular Plant-Microbe Interactions 20(9): 1092-1101.
Vleeshouwers, V.G. and Oliver, R.P. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Molecular pLant-Microbe Interactions 27(3): 196-206.
Wollenberg, T. and Schirawski, J. 2014. Comparative genomics of plant fungal pathogens: The Ustilago sporisorium paradigm. PLoS Pathogy 10(7): e1004218.
Yoshida, M., Takayanagi, Y., Inoue, K., Kimura, T., Young, L.J., Onaka, T. and Nishimori, K. 2009. Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. Journal of Neuroscience 29(7): 2259-2271.
Yu, I., Parker. J. and Bent A.F. 1998. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. PNAS 95(13): 7819-7824.
Zhao, T., Pei, T., Jiang, J., Yang, H., Zhang, H., Li, J. and Xu, X. 2022. Understanding the mechanisms of resistance to tomato leaf mold: A review. Horticultural Plant Journal 8(6): 667-675.
Balesdent, M.H., Fudal, I., Ollivier, B., Bally, P., Grandaubert, J., Eber, F., Chèvre, A.M., Leflon, M. and Rouxel, T. 2013. The dispensable chromosome of L eptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytologist 198(3): 887-898.
Ballance, G., Lamari, L. and Bernier, C. 1989. Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiological and Molecular Plant Pathology 35(3): 203-213.
Barlowe, C and Miller, E. 2013. Secretory protein biogenesis and traffic in the early secretory pathway. Genetics 193(2): 383-410.
Bart, P.H.J., Thomma, H., van Esse, P., Crous, P. and de Wit, P. 2005. Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Molecular Plant Pathology 6(4): 379-393.
Basse, C.W., Kolb, S. and Kahmann, R. 2002. A maize‐specifically expressed gene cluster in Ustilago maydis. Molecular Microbiology 43(1): 75-93.
Basse, C.W., Stumpferl, S. and Kahmann, R. 2000. Characterization of a Ustilago maydis gene specifically induced during the biotrophic phase: evidence for negative as well as positive regulation. Molecular and Cellular Biology 20(1): 329-339.
Bolton, M.D., Van Esse, H.P., Vossen, J.H., De Jonge, R., Stergiopoulos, I., Stulemeijer, I.J., Van Den Berg, G.C., Borrás‐Hidalgo, O., Dekker, H.L., De Koster, C.G. and De Wit, P.J. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Molecular microbiology 69(1): 119-136.
Ciuffetti, L.M., Manning, V.A., Pandelova, I., Betts, M.F. and Martinez, J.P. 2010. Host‐selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici‐repentis–wheat interaction. New Phytologist 187(4): 911-919.
Cooke, M. 1883. New american fungi. Grevillea 12: 22-33.
de Jonge, R., Bolton, M.D., Kombrink, A., van den Berg, G.C., Yadeta, K.A. and Thomma, B.P. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Research 23(8): 1271-1282.
de Jonge, R. and Thomma, B.P. 2009. Fungal LysM effectors: extinguishers of host immunity? Trends in Microbiology 17(4): 151-157.
De Jonge, R., Peter van Esse, H., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., Van Der Krol, S., Shibuya, N., Joosten, M.H. and Thomma, B.P. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329(5994): 953-955.
de Wit, P.J. 1992. Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annual Review of Phytopathology 30(1): 391-418.
de Wit, P.J.G.M. 2016. Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato. Annual Review of Phytopathology 54(1):1-23.
de Wit, P.J.G.M., Mehrabi, R., Van Den Burg, H. and Stergiopoulos, I. 2009. Fungal effector proteins: past, present and future. Molecular Plant Pathology 10(6): 735–747.
Dean, R.A., Talbot, N.J., Ebbole, D.J., Farman, M.L., Mitchell, T.K., Orbach, M.J., Thon, M., Kulkarni, R., Xu, J.R., Pan, H. and Read, N.D. 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980–986.
Dodds, P. 2023. From Gene-for-Gene to Resistosomes: Flor's Enduring Legacy. MPMI 36(8): 461–467.
D'Silva, I. and Heath, M.C. 1997. Purification and characterization of two novel hypersensitive response-inducing specific elicitors produced by the cowpea rust fungus. Journal of Biological Chemistry 272(7): 3924-3927.
Duplessis, S., Cuomo, C.A., Lin, Y.C., Aerts, A., Tisserant, E., Veneault-Fourrey, C., Joly, D.L., Hacquard, S., Amselem, J., Cantarel, B.L. et al. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. PNAS 108(22): 9166-9171.
Friesen, T.L., Meinhardt, S.W. and Faris, J.D. 2007. The Stagonospora nodorum‐wheat pathosystem involves multiple proteinaceous host‐selective toxins and corresponding host sensitivity genes that interact in an inverse gene‐for‐gene manner. The Plant Journal 51(4): 681-692.
Ghiasi Noei, F., Imami, M., Didaran, F., Ghanbari, M.A., Zamani, E., Ebrahimi, A., Aliniaeifard, S., Farzaneh, M., Javan-Nikkhah, M., Feechan, A. and Mirzadi Gohari, A. 2022. Stb6 mediates stomatal immunity, photosynthetic functionality, and the antioxidant system during the Zymoseptoria tritici-wheat interaction. Frontier in Plant Science 13: 1004691.
Hetmann, A. and Kowalczyk, S. 2019. Suppression of PAMP-triggered immunity (PTI) by effector proteins synthesized by phytopathogens and delivered into cells of infected plant. Postepy Biochemii 22: 65(1): 58-71.
Joosten, M.H. and de Wit, P.J. 1999. The tomato– Cladosporium fulvum interaction: A versatile experimental system to study plant-pathogen interactions. Annual Review of Phytopatholog 37(1): 335-367.
Joosten, M., Vogelsang, R., Cozijnsen, T.J., Verberne, M.C. and de Wit, P.J. 1997. The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. The Plant Cell 9(3): 367-379.
Kämper, J., Kahmann, R., Bölker, M., Ma, L.J., Brefort, T., Saville, B.J., Banuett, F., Kronstad, J.W., Gold, S.E., Müller, O. and Perlin, M.H. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97–101.
Kema, G.H.J., Mirzadi Gohari, A., Aouini, L., Hay, G., Ware, S.B., Van Den Bosch, F., Manning-Smith, R., Alonso-Chavez, V., Helps, J., Ben M'Barek, S., Mehrabi, R., Diaz-Trujillo, C., Zamani, E., et al. 2018. Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance. Nature Genetics 50: 375-380.
Kruger, J., Thomas, C.M., Golstein, C., Dixon, M.S., Smoker, M., Tang, S., Mulder, L. and Jones, J.D. 2002. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296(5568): 744-747.
Lo Presti, L., Lanver, D., Schweizer, G., Tanaka, S., Liang, L., Tollot, M., Zuccaro, A., Reissmann, S. and Kahmann, R. 2015. Fungal effectors and plant susceptibility. Annual Review of Plant Biology 66: 513-545.
Luderer, R., Takken, F.L., de Wit, P.J.d. and Joosten, M.H. 2002. Cladosporium fulvum overcomes Cf‐2‐mediated resistance by producing truncated AVR2 elicitor proteins. Molecular Microbiology 45(3): 875-884.
Ma, L.J., Van Der Does, H.C., Borkovich, K.A., Coleman, J.J., Daboussi, M.J., Di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B. and Houterman, P.M. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464(7287): 367-373.
Mapuranga, J., Zhang, L., Zhang, N. and Yang Wenxiang, Y. 2022. The haustorium: The root of biotrophic fungal pathogens. Plant Pathogen Interactions 13(29): 963705.
Marshall, R., Kombrink, A., Motteram, J., Loza-Reyes, E., Lucas, J., Hammond-Kosack, K.E., Thomma, B.P. and Rudd, J.J. 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.
Mendgen, K. and Hahn, M. 2002. Plant infection and the establishment of fungal biotrophy. Trends in plant science 7(8): 352-356.
Mentlak, T.A., Kombrink, A., Shinya, T., Ryder, L.S., Otomo, I., Saitoh, H., Terauchi, R., Nishizawa, Y., Shibuya, N., Thomma, B.P. and Talbot, N.J. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. The Plant Cell 24(1): 322-335.
Gohari, A.M., Ware, S.B., Wittenberg, A.H., Mehrabi, R., M'Barek, S.B., Verstappen, E.C., Van der Lee, T.A., Robert, O., Schouten, H.J., De Wit, P.P. and Kema, G.H. 2015. Effector discovery in the fungal wheat pathogen Zymoseptoria tritici. Molecular Plant Pathology 16(9): 931-945.
Mukhi, N., Gorenkin, D. and Banfield, M.J. 2020. Exploring folds, evolution and host interactions: understanding effector structure/function in disease and immunity. New Phytologist 227 (2): 326–333.
Pedersen, C., ver Loren van Themaat, E., McGuffin, L.J., Abbott, J.C., Burgis, T.A., Barton, G., Bindschedler, L.V., Lu, X., Maekawa, T., Wessling, R., Cramer, R., Thordal-Christensen, H., Panstruga, R. and Spanu, P.D. 2012. Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13: 694.
Oerke, E.C. 2006. Crop losses to pests. The Journal of Agricultural Science 144(1): 31-43.
Rivas, S. and Thomas, C.M. 2005. Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annual Review of Phytopathology 43: 395-436.
Rooney, C.E., Van`t Klooster, J.W., van der Hoom, R.A., Joosten, M.H., Jones, J.D., de Wit, P.J. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance Science 308(5729): 1783-1786.
Raffaele, S., Farrer, R.A., Cano, L.M., Studholme, D.J., MacLean, D., Thines, M., Jiang, R.H., Zody, M.C., Kunjeti, S.G., Donofrio, N.M., Meyers, B.C., Nusbaum, C. and Kamoun, S. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage.SCIENCE 330(6010): 1540-1543.
Sánchez-Vallet, A., Fouché, S., Fudal, I., Hartmann, F.E., Soyer, J.L., Tellier, A. and Croll, D. 2018. The genome biology of effector gene evolution in filamentous plant pathogens. Annual Review of Phytopathology 56: 21-40.
Schottens-Toma I.M. and de Wit, P.J. 1988. Purification and primary structure of a necrosis-inducing peptide from the apoplastic fluids of tomato infected with Cladosporium fulvum (syn. Fulvia fulva). Physiological and Molecular Plant Pathology 33(1): 59-67.
Schirawski, J., Mannhaupt, G., Münch, K., Brefort, T., Schipper, K., Doehlemann, G. Di Stasio, M., Rössel, N., Mendoza-Mendoza, A., Pester, D. and Müller, O. 2010. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330(6010): 1546-1548.
Song, J., Win, J., Tian, M., Schornack, S., Kaschani, F., Ilyas, M., van der Hoorn, R.A. and Kamoun, S. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. PANS 106(5): 1654-1659.
Sperschneider, J., Dodds, P.N., Gardiner, D.M., Singh, K.B. and Taylor, J.M. 2018. Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Molecular Plant Pathology 19(9): 2094-2110.
Strange, R.N. and Scott, P.R. 2005. Plant disease: a threat to global food security. Annual Review of Phytopathology. 43: 83-116.
Stephenson, S.A., Hatfield, J., Rusu, A.G., Maclean, D.J. and Manners, J.M. 2000. CgDN3: an essential pathogenicity gene of Colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Molecular Plant-Microbe Interactions 13(9): 929-941.
Stergiopoulos, I., de Kock, M.J., Lindhout, P. and de Wit, P.J. 2007. Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Molecular Plant-Microbe Interactions 20(10): 1271-1283.
Stergiopoulos, I. and de Wit, P.J. 2009. Fungal effector proteins. Annual Review of Phytopathology 47: 233-263.
Takken, F.L., Luderer, R., Gabriëls, S.H., Westerink, N., Lu, R., De Wit, P.J. and Joosten, M.H. 2000. A functional cloning strategy, based on a binary PVX‐expression vector, to isolate HR‐inducing cDNAs of plant pathogens. The Plant Journal 24(2): 275-283.
Thomas, C.M., Dixon, M.S., Parniske, M., Golstein, C. and Jones, J.D. 1998. Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 353(1374): 1413-1424.
Thomma, B.P., van Esse, H.P., Crous, P.W. and de Wit, P.J. 2005. Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Molecular Plant Pathology 6(4): 379-393.
Tuori, R., Wolpert, T. and Ciuffetti, L. 1995. Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions 9(43): 10.3.
Van Kan, J.A. 2006. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends in plant science 11(5): 247-253.
Van den Burg, H.A., Harrison, S.J., Joosten, M.H., Vervoort, J. and de Wit, CP.J. 2006. ladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Molecular Plant-Microbe Interactions 19(12): 1420-1430.
Van der Does, H.C., Duyvesteijn, R., Goltstein, P., Schie, C., Manders, E., Cornelissen, B and Rep, M. 2008. Expression of effector gene SIX1 of Fusarium oxysporum requires living plant cells. Fungal Genetics Biology 45(9): 1257-1264.
van Esse, H.P., Bolton, M.D., Stergiopoulos, I., de Wit, P.J. and Thomma, B.P. 2007. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Molecular Plant-Microbe Interactions 20(9): 1092-1101.
Vleeshouwers, V.G. and Oliver, R.P. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Molecular pLant-Microbe Interactions 27(3): 196-206.
Wollenberg, T. and Schirawski, J. 2014. Comparative genomics of plant fungal pathogens: The Ustilago sporisorium paradigm. PLoS Pathogy 10(7): e1004218.
Yoshida, M., Takayanagi, Y., Inoue, K., Kimura, T., Young, L.J., Onaka, T. and Nishimori, K. 2009. Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. Journal of Neuroscience 29(7): 2259-2271.
Yu, I., Parker. J. and Bent A.F. 1998. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. PNAS 95(13): 7819-7824.
Zhao, T., Pei, T., Jiang, J., Yang, H., Zhang, H., Li, J. and Xu, X. 2022. Understanding the mechanisms of resistance to tomato leaf mold: A review. Horticultural Plant Journal 8(6): 667-675.
