Plant Disease Resistance Proteins: R-gene Products as Immune Defense Molecules

Year 2021, Volume: 4 Issue: 3, 523 - 545, 15.12.2021

Berna Baş

https://doi.org/10.38001/ijlsb.938954

Abstract

Disease resistance-related R genes encoding NBS-LRR proteins are functional in systemic acquired immunity, briefly referred as ETI, in plant pathology. Upon infection of pathogens at first stage of plant immune responses, if plant pathogens subvert PTI immunity that activated by cell membrane surface receptor, then ETI immunity is initiated the relay to second step of defense. Also when pathogen effectors are directly translocated into cell cytoplasm across host membranes where can be faced with plant R proteins, ETI immunity develops faster and stronger than PTI efficacy. A great number of pathogen effectors are directly or indirectly reacted with R-gene proteins in similar to epitope-paratope structural interaction. With what kind of mechanisms do the plants that show similar immune responses to all known biotic agents recognize the effectors of a wide variety of pathogenic organisms? However many approaches are available involved in molecular mechanisms of intracellular pattern-recognition receptors in plants, findings for each mechanism have been obtained from specific workings of personally researchers. It is not known how many different strategy models prevailing in molecular interaction of a wide variety of effector-receptor recognition are functional. So in the presented review article is focused just to molecular mechanism kinds of physical connection between many different effectors and intracellular receptors.

Keywords

Proteins related with plant disease resistance, R-gene proteins, Effector-receptor interactions, NB-LRR proteins

Bitki Hastalık Dayanıklılık Proteinleri; İmmün Savunma Molekülleri Olarak R-gen Ürünleri

Abstract

Çoğu bitkinin NBS-LRR proteinlerini kodlayan hastalık dayanıklılığı ile ilgili R genleri, sistemik olarak kazanılmış immünitede işlevseldir, kısaca ETI olarakta bilinir. Patojen organizmalar hücre yüzey reseptörleri ile harekete geçirilen PTI immüniteyi bertaraf ettikten sonra, daha sonraki aşamada ETI immünite aktif hale geçmektedir. Aynı zamanda patojen organizmaların efektörleri direkt sitoplazmaya ulaşınca, efektörleri tanıyan R proteinleri aracılığı ile PTI’nin etkisinden daha hızlı ve güçlü bir ETI immün tepki gelişmektedir. Patojen efektörlerinin çoğu, epitop-paratop ilişkisindeki yapısal interaksiyona benzer şekilde direkt veya indirekt olarak R-gen proteinleri ile reaksiyona girerler. Bilinen bütün biyotik ajentlere benzer immün tepki veren bitkiler ne tür mekanizmalarla çok çeşitli patojenik organizmaların efektörlerini tanımaktadır? Ancak bitkilerdeki hücre içi örnek-tanıma reseptörlerinin moleküler mekanizmalarıyla ilgili birçok yaklaşım mevcut olmakla beraber, her mekanizmaya ait sonuçlar, kişisel olarak araştırmacıların kendi özel çalışmalarından elde edilmiştir. Çok çeşitli efektör-reseptör tanımanın moleküler interaksiyonunda geçerli olan toplam kaç farklı strateji modelinin işlevsel olduğu bilinmemektedir. Bu nedenle sunulan derlemede, birçok farklı efektörler ile intraselüler reseptörleri arasındaki fiziki bağlantının moleküler mekanizma çeşitlerine odaklanılmıştır.

Keywords

Bitki hastalık dayanıklılığıyla ilgili proteinler, R-gen proteinleri, Efektör-reseptör interaksiyonları, NB-LRR proteinleri

References

• 1. Dong, O.X. and P.C. Ronald, Genetic engineering for disease resistance in plants: Recent Progress and Future Perspectives. Plant Physiology, 2019. 180(1): p. 26-38.
• 2. Yin, K. and J.L. Qiu, Genome editing for plant disease resistance: applications and perspectives. Philosophical Transactions of the Royal Society of Londan. Series B, Biological Sciences, 2019. 374(1767): p. 20180322.
• 3. Engelhardt, S., R. Stam, and R. Hückelhoven, 2018. Good Riddance? Breaking Disease Susceptibility in the Era of New Breeding Technologies. Agronomy, 2018. 8(7): p. 114.
• 4. Franceschetti, M., et al., Effectors of filamentous plant pathogens: Commonalities amid diversity. Microbiology and Molecular Biology Reviews, 2017. 81(2): p. e00066-16.
• 5. Kubicek, C.P., T.L. Starr, and N.L. Glass, Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. Annual Review of Phytopathology, 2014. 52: p. 427-451.
• 6. Wang, M.B., et al., RNA silencing and plant viral diseases. Molecular Plant Microbe-Interactions: MPMI, 2012. 25(10): p. 1275-1285.
• 7. Giese, W., et al., Spatial modeling of the membrane-cytosolic interface in protein kinase signal transduction. PLoS Computational Biology, 2018. 14(4): p. e1006075.
• 8. Silva, M.S., et al., Review: Potential biotechnological assets related to plant immunity modulation applicable in engineering disease-resistant crops. Plant Science: an International Journal of Experimental Plant Biology, 2018. 270: p. 72-84.
• 9. Césari, S., et al.,A novel conserved mechanism for plant NLR protein pairs: the ''integrated decay'' hypothesis. Frontiers in Plant Science, 2014. 5: p. 606.
• 10. Jatwa, T.K., M. Sharma, and A.K. Malav, R gene and its role in disease managements in plants. International Journal of Current Research in Biosciences and Plant Biology, 2017. 4(5): p. 61-64.
• 11. Nepal, M.P., et al., Comparative Genomics of Non-TNL Disease Resistance Genes from Six Plant Species. Genes, 2017. 8(10): p. 249.
• 12. Zhang, Y., T. Lubberstedt, and M. Xu, 2013. The genetic and molecular basis of plant resistance to pathogens. Journal of Genetics and Genomics ꞊ Yi chuan xue bao, 2013. 40(1): p. 23-35.
• 13. Heath, M.C., Nonhost resistance and nonspecific plant defenses. Current Opinion in Plant Biology, 2000. 3(4): p. 315-319.
• 14. Staskawicz, B.J., et al., Molecular genetics of plant disease resistance. Science(New York, N.Y.), 1995. 268(5211): p. 661-667.
• 15. Heath, M.C., Evolution of plant resistance and susceptibility to fungal invaders. Canadian Journal of Plant Pathology, 1987. 9(4): p. 389-397.
• 16. Heath, M. C., 2003. Nonhost resistance in plants to microbial pathogens, in Innate immunity. Infectious disease, R.A.B. Ezekowitz and J.A. Hoffmann, Editors. 2003, Humana Press Totowa, NJ. p. 47-57.
• 17. Nie, J., et al., A small cysteine-rich protein from two kingdoms of microbes is recognized as a novel pathogen-associated molecular pattern. The New Phytologist, 2019. 222(2): p. 995-1011.
• 18. Schwessinger, B. and C. Zipfel, News from the frontline: recent insights into PAMP-triggered immunity in plants. Current Opinion in Plant Biology, 2008. 11(4): p. 389-395.
• 19. Zipfel, C., Pattern-recognition receptors in plant innate immunity. Current Opinion in Immunology, 2008. 20(1): p. 10-16.
• 20. Gururani, M.A., et al., Plant disease resistance genes: Current status and future directions. Physiological and Molecular Plant Pathology, 2012. 78: p. 51-65.
• 21. Freeman, B.C. and G.A. Beattie, An overview of plant defenses against pathogens and herbivores. Plant Health Instructor, 2008. http://dx.doi.org/10.1094/PHI-I-2008-0226-01%20 [Erişim Tarihi: 17. 05. 2021].
• 22. Monaghan J. and C. Zipfel, Plant pattern recognition receptor complexes at the plasma membrane. Current Opinion in Plant Biology, 2012. 15(4): p. 349-357.
• 23. Kazan, K. and R. Lyons, Intervention of Phytohormone Pathways by Pathogen Effectors. The Plant Cell, 2014. 26(6): p. 2285-2309.
• 24. Macho, A.P. and C. Zipfel, Plant PRRs and the activation of innate immune signaling. Molecular Cell, 2014. 54(2): p. 263-272.
• 25. Jones, J. D. and J.L. Dangl, 2006. The plant immune system. Nature, 2006. 444(7117): p. 323-329.
• 26. Chang, J.H., D. Desveaux, and A.L. Creason, ABCs and 123s Bacterial Secretion Systems in Plant Pathogenesis. Annual Review of Phytopathology, 2014. 52: p. 317-345.
• 27. MacQueen, A. and J. Bergelson, Modulation of R-gene expression across environments. Journal of Experimental Botany, 2016. 67(7): p. 2093-2105.
• 28. Zhang, H. and S. Wang, Rice versus Xanthomonas oryzae pv oryzae: a unique pathosystem. Current Opinion in Plant Biology, 2013. 16(2): p. 188-195.
• 29. Petre, B., D.L. Joly, and S. Duplessis, Effector proteins of rust fungi. Frontiers in Plant Science, 2014. 5: p. 416.
• 30. Kemen, E., et al., A novel structural effector from rust fungi is capable of fibril formation. The Plant Journal, 2013. 75(5): p. 767-780.
• 31. Rafiqi, M., et al., Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. The Plant Cell, 2010. 22(6): p. 2017-2032.
• 32. Kemen, E., et al., Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Molecular Plant-Microbe Interactions: MPMI, 2005. 18(11): p. 1130-1139.
• 33. Kourelis, J. and R. van der Hoorn, Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms of R protein function. The Plant Cell, 2018. 30(2): p. 285-299.
• 34. Neupane, S., et al., Genome-Wide Identification of NBS-Encoding Resistance Genes in Sunflower (Helianthus annuus L). Genes, 2018. 9(8): p. 384.
• 35. Shao, Z.Q., et al., Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiology, 2016. 170(4): p. 2095-2109.
• 36. Meyers, B.C., et al., Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. The Plant Cell, 2003. 15(4): p. 809-834.
• 37. McHale, L., et al., Plant NBS-LRR proteins: adaptable guards. Genome Biology, 2006. 7(4): p. 212.
• 38. Baggs, E., G. Dagdas, and K.V. Krasileva, NLR diversity, helpers and integrated domains: making sense of the NLR identity. Current Opinion in Plant Biology, 2017. 38: p. 59-67.
• 39. Bonardi, V. and J.L. Dangl, How complex are intracellular immune receptor signaling complexes?. Frontiers in Plant Science, 2012. 3: p. 237.
• 40. Kapos, P., K.T. Devendrakumar, and X. Li, Plant NLRs: From discovery to application. Plant Science: an international journal of experimental plant biology, 2019. 279: p. 3-18.
• 41. Belkhadir, Y., R. Subramaniam, and J.L. Dangl, Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Current Opinion in Plant Biology, 2004. 7(4): p. 391-399.
• 42. Williams, S.J., et al., An autoactive mutant of the M flax rust resistance protein has a preference for binding ATP, whereas wild-type M protein binds ADP. Molecular Plant-Microbe Interactions: MPMI, 2011. 24(8): p. 897-906.
• 43. Tameling, W.I., et al., Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiology, 2006. 140(4): p. 1233-1245.
• 44. Riedl, S.J., et al., Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature, 2005. 434(7035): p. 926-933.
• 45. Tameling, W.I., et al., The tomato R gene product I-2 and MI-1 are functional ATP binding proteins with ATPase activity. The Plant Cell, 2002. 14(11): p. 2929-2939.
• 46. Hu, Z., et al., Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science(New York, N.Y.), 2013. 341(6142): p. 172-175.
• 47. Tameling, W.I., et al., RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the solanaceae, thereby dictating Rx function. The Plant Cell, 2010. 22(12): p. 4176-4194.
• 48. Ade, J., et al., Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proceedings of the National Academy of Sciences of the United States of America, 2007. 104(7): p. 2531-2536.
• 49. Ravensdale, M., et al., Intramolecular interaction influences binding of the Flax L5 and L6 resistance proteins to their AvrL567 ligands. PLoS Pathogens, 2012. 8(11): p. e1003004.
• 50. Burch-Smith, T.M., et al., A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biology, 2007. 5(3): p. e68.
• 51. Lewis, J.D., et al., Allele-specific virulence attenuation of the Pseudomonas syringae HopZ1a type III effector via the Arabidopsis ZAR1 resistance protein. PLoS Genetics, 2010. 6(4): p. e1000894.
• 52. Jayaraman, J., et al., A bacterial acetyltransferase triggers immunity in Arabidopsis thaliana independent of hypersensitive response. Scientific Reports, 2017. 7(1): p. 3557.
• 53. Lewis, J.D., et al., The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. Proceedings of the National Academy of Sciences of the United States of America, 2013. 110(46): p. 18722-18727.
• 54. MAPK Group., Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends in Plant Science, 2002. 7(7): p. 301-308.
• 55. Zhang, Z., et al., Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host & Microbe, 2012. 11(3): p. 253–263.
• 56. Zhang, Z., et al., The NLR protein SUMM2 senses the disruption of an immune signaling MAP kinase cascade via CRCK3. EMBO Reports, 2017. 18(2): p. 292–302.
• 57. Kroj, T., et al., Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. The New Phytologist, 2016. 210(2): p. 618-626.
• 58. Sarris, P.F., et al., Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biology, 2016. 14: p. 8.
• 59. Sarris, P.F., et al., A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell, 2015. 161(5): p. 1089-1100.
• 60. Yoshida, K., et al., Association genetics reveals three avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. The Plant Cell, 2009. 21(5): p. 1573-1591.
• 61. Orbach, M.J., et al., A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. The Plant Cell, 2000. 12(11): p. 2019-2032.
• 62. Li, W., et al., The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Molecular Plant-Microbe Interactions: MPMI, 2009. 22(4): p. 411-420.
• 63. Ribot, C., et al., The Magnaporthe oryzae effector AVR1-CO39 is translocated into rice cells independently of a fungal-derived machinery. The Plant Journal: for cell and molecular biology, 2013. 74(1): p. 1-12.
• 64. Césari, S., et al., The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by directing binding. The Plant Cell, 2013. 25(4): p. 1463-1481.
• 65. Okuyama, Y., et al., A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. The Plant Journal: for cell and molecular biology, 2011. 66(3): p. 467-479.
• 66. Ashikawa, I., et al., Two adjacent nucleotide-binding site-leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics, 2008. 180(4): p. 2267-2276.
• 67. Wu, W., et al., Stepwise arms race between AvrPik and Pik alleles in the rice blast pathosystem. Molecular Plant-Microbe Interactions: MPMI, 2014. 27(8): p. 759-769.
• 68. Zhai, C., et al., Function and interaction of the coupled genes responsible for Pik-h encoded rice blast resistance. PloS One, 2014. 9(6): p. e98067.
• 69. Kanzaki, H., et al., Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. The Plant Journal, 2012. 72(6): p. 894-907.
• 70. Fujisaki, K., et al., An unconventional NOI/RIN4 domain of a rice NLR protein binds host EXO70 protein to confer fungal immunity. bioRxiv, 2017. 239400. https://doi.org/10.1101/239400 [Erişim Tarihi: 17. 05. 2021]
• 71. Afzal, A.J., J.H. Kim, and D. Mackey, The role of NOI-domain containing proteins in plant immune signaling. BMC Genomics, 2013. 14: p. 327.
• 72. Chisholm, S.T., et al., Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proceedings of the National Academy of Sciences of the United States of America, 2005. 102(6): p. 2087-2092.
• 73. Bialas, A., et al., Lessons in Effector and NLR Biology of Plant-Microbe Systems. Molecular Plant-Microbe Interactions: MPMI, 2018. 31(1): p. 34-45.
• 74. Heuer, H., et al., Repeat domain diversity of avrBs3-like genes in Ralstonia solanacearum strains and association with host preferences in the field. Applied and Environmental Microbiology, 2007. 73(13): p. 4379-4384.
• 75. Salanoubat, M., et al., Genome sequence of the plant pathogen Ralstonia solanacearum. Nature, 2002. 415(6871): p. 497-502.
• 76. De Feyter, R., Y. Yang, and D.W. Gabriel, 1993. Gene-for-genes interactions between cotton R genes and Xanthomonas campestris pv malvacearum avr genes. Molecular Plant-Microbe Interactions: MPMI, 1993. 6(2): p. 225-237.
• 77. Hopkins, C.M., et al., Identification of a family of avirulence genes from Xanthomonas oryzae pv oryzae. Molecular Plant-Microbe Interactions: MPMI, 1992. 5(6): p. 451-459.
• 78. Juillerat, A., et al., BurrH: a new modular DNA binding protein for genome engneering. Scientific Reports, 2014. 4: p. 3831.
• 79. de Lange, O., et al., Programmable DNA-binding proteins from Burkholderia provide a fresh perspective on the TALE-like repeat domain. Nucleic Acids Research, 2014. 42(11): p. 7436-7449.
• 80. Bonas, U., R.E. Stall, and B. Staskawicz, Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv vesicatoria. Molecular and General Genetics, 1989. 218(1): p. 127-136.
• 81. Bogdanove, A.J., S. Schornack, and T. Lahaye, TAL effectors: finding plant genes for disease and defense. Current Opinion in Plant Biology, 2010. 13(4): p. 394-401.
• 82. Zhang, J., Z. Yin, and F. White, TAL effectors and the executor R genes. Frontiers in Plant Science, 2015. 6: p. 641.
• 83. Gu, K., et al., R gene expression induced by a type-III effector triggers disease resistance in rice. Nature, 2005. 435(7045): p. 1122-1125.
• 84. Tian, D., et al., The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. The Plant Cell, 2014. 26(1): p. 497-515.
• 85. Wang, C., et al., XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. Molecular Plant, 2015. 8(2): p. 290-302.
• 86. Römer, P., et al., Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science (New York, N.Y.), 2007. 318(5850): p. 645-648.
• 87. Strauss, T., et al., RNA-seq pinpoints a Xanthomonas TAL-effector activated resistance gene in a large-crop genome. Proceedings of the National Academy of Sciences of the United States of America, 2012. 109(47): p. 19480-19485.
• 88. Römer, P., S. Recht, and T. Lahaye, A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proceedings of the National Academy of Sciences of the United States of America, 2009. 106(48): p. 20526-20531.
• 89. Zeng, X., et al., Genetic engineering of the Xa10 promoter for broad-spectrum and durable resistance to Xanthomonas oryzae pv oryzae. Plant Biotechnology Journal, 2015. 13(7): p. 993-1001.
• 90. Hummel, A.W., E.L. Doyle, and A.J. Bogdanove, Additional of transcription activator-like effector binding sites to a pathogen strain-specific rice bacterial blight resistance gene makes it effective against additional strains and against bacterial leaf streak. New Phytologist, 2012. 195(4): 883-893.
• 91. Puri, M., et al., Ribosome-inactivating proteins: current status and biomedical applications. Drug Discovery Today, 2012. 17(13-14): p. 774-783.
• 92. Stirpe, F. and M.G. Battelli, Ribosome-inactivating proteins: progress and problems. Cellular and Molecular Life Sciences: CMLS, 2006. 63(16): p. 1850-1866.
• 93. Girbés, T., et al., Description, distribution, activity and phylogenetic relationship of ribosome-inactivating proteins in plants, fungi and bacteria. Mini-Reviews in Medicinal Chemistry, 2004. 4(5): p. 461-476.
• 94. van Damme, E.J., et al., Ribosome-inactivating proteins: a family of plant proteins that do more than inactivate ribosomes. Critical Reviews in Plant Sciences, 2001. 20: p. 395-465.
• 95. Jiang, S.Y., et al., Over-expression of OSRIP18 increases drought and salt tolerance in transgenic rice plants. Transgenic Research, 2012. 21(4): p. 785-795.
• 96. Stirpe, F., Ribosome-inactivating proteins: from toxins to useful proteins. Toxicon: official journal of the International Society on Toxinology, 2013. 67: p. 12-16.
• 97. Musidlak, O., R. Nawrot, and A. Goździcka-Józefiak, 2017. Which Plant Proteins Are Involved in Antiviral Defense? Review on In Vivo and In Vitro Activities of Selected Plant Proteins against Viruses. International Journal of Molecular Sciences, 2017. 18(11): p. 2300.
• 98. Domashevskiy, A.V., et al., Plant Translation Initiation Complex eIFiso4F Directs Pokeweed Antiviral Protein to Selectively Depurinate Uncapped Tobacco Etch Virus RNA. Biochemistry, 2017. 56(45): p. 5980-5990.
• 99. Lellis, A.D., et al., Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Current Biology: CB, 2002. 12(12): p. 1046-1051.
• 100. Ishibashi, K. and M. Ishikawa, Mechanisms of tomato mosaic virus RNA replication and its inhibition by the host resistance factor Tm-1. Current Opinion in Virology, 2014. 9: p. 8-13.
• 101. Ishibashi, K., et al., Structural basis for the recognition-evasion arms race between Tomato mosaic virus and the resistance gene Tm-1. Proceedings of the National Academy of Sciences of the United States of America, 2014. 111(33): p. E3486-E3495.
• 102. Boch, J., et al., Breaking the code the DNA binding specificity of TAL-type III effectors. Science, 2009. 326(5959): p. 1509-1512.
• 103. Yuan, M., et al., A host basal transcription factor is a key component for infection of rice by TALE-carrying bacteria. eLife, 2016. 5: p. e19605.
• 104. Ellis, J.G., et al., The past, present and future of breeding rust resistance wheat. Frontiers in Plant Science, 2014. 5: p. 641.
• 105. Lyngkjær, M.F. and T.L.W. Carver, Conditioning of cellular defence responses to powdery mildew in cereal leaves by prior attack. Molecular Plant Pathology, 2000. 1: p. 41-49.
• 106. Jørgensen, I. H., Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica, 1992. 63: p. 141-152.
• 107. Hückelhoven, R. and R. Panstruga, Cell biology of the plant-powdery mildew interaction. Current Opinion in Plant Biology, 2011. 14(6): p. 738-746.
• 108. Andolfo, G., et al., Evolutionary conservation of MLO gene promoter signatures. BMC Plant Biology, 2019. 19: p. 150.
• 109. Gkarmiri, K., Interactions of fungal pathogens and antagonistic bacteria in the rhizosphere of Brassica napus. Faculty of Forest Sciences Department of Forest Mycology and Plant Pathology, Doctoral thesis, 2018. Swedish University of Agricultural Sciences, Uppsala, Sweden 125 pp.