Published

2017-05-01

Plant responses to pathogen attack: molecular basis of qualitative resistance

Respuestas de las plantas al ataque de patógenos: bases moleculares de la resistencia cualitativa

DOI:

https://doi.org/10.15446/rfna.v70n2.64526

Keywords:

Host resistance, Non-host resistance, Zig-zag model, PTI, ETI, ETS (en)
Resistencia hospedero, Resistencia no hospedero, Modelo zig-zag, PTI, ETI, ETS (es)

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Authors

  • Kelly Ávila Méndez Corporacion Centro de Investigaciones de Palma de Aceite, Cenipalma
  • Hernán Mauricio Romero Universidad Nacional de Colombia
Pathogens attack plants to assimilate nutrients from them. All plant species have succeeded in overcoming pathogenic attack; therefore disease condition is not the rule but the exception. A co-evolutionary battle has equipped plants with sophisticated defense mechanisms and cognate pathogens with a corresponding arsenal of counter strategies to overcome them. Traditionally, plant-pathogen interaction has been associated with molecules involved in recognition processes giving rise to models such as the "Zig-zag Model". However, this model is being re-evaluated because it is not consistent with the complexity of the interaction. Current models propose a holistic view of a process where the response is not always determined by the interaction of two molecules. This review discusses the main aspects related to qualitative responses in the plant-pathogen interaction and the new proposed models.

Los patógenos atacan las plantas en un intento de asimilar los nutrientes de éstas. Todas las especies de plantas han tenido éxito para superar el ataque de patógenos, tanto que la condición de enfermedad no es la norma sino la excepción. Una batalla co-evolutiva ha dotado a las plantas con mecanismos de defensa sofisticados y a los patógenos afines con un arsenal correspondiente para superar dichas respuestas de defensa. Tradicionalmente, la interacción planta-patógeno se ha asociado a las moléculas que están involucradas en los procesos de reconocimiento, permitiendo el desarrollo de modelos que explican esta interacción, como el “Modelo zig-zag”. Sin embargo, éste modelo está siendo revaluado debido a que no es consistente con la complejidad de la interacción. Los modelos actuales proponen una visión holística de un proceso en el que no siempre la respuesta va estar determinada por la interacción de dos moléculas. Esta revisión discute los principales aspectos relacionados con la respuesta cualitativa en la interacción planta-patógeno y los nuevos modelos biológicos propuestos.

References

Albrecht C, Boutrot F, Segonzac C, Schwessinger B, Gimenez-Ibanez S, Chinchilla D, Rathjen JP, de Vries SC and Zipfel C. 2012. Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proceedings of the National Academy of Sciences 109(1): 303–308. doi:10.1073/pnas.1109921108.

Andolfo G, Iovieno, P, Frusciante L and Ercolano M. 2016. Genome-Editing Technologies for Enhancing Plant Disease Resistance. Frontiers in Plant Science 7(December): 1813. doi:org:10.3389/fpls.2016.01813

Baltes N and Voytas D. 2015. Enabling plant synthetic biology through genome engineering. Trends in Biotechnology 33(2): 120–131. doi.org:10.1016/j.tibtech.2014.11.008

Balvanera P, Uriarte M, Leñero L, Altesor A, DeClerck G, Hall J, Lara A, Laterra P, et al. 2012. Ecosystem services research in Latin America: The state of the art. Ecosystem Services 2:56-70. doi:10.1016/j.ecoser.2012.09.006

Bebber D and Gurr S. 2015. Crop-destroying fungal and oomycete pathogens challenge food security. Fungal Genetics and Biology 74:62-64. doi:10.1016/j.fgb.2014.10.012

Beck M, Heard W, Mbengue M and Robatzek S. 2012. The INs and OUTs of pattern recognition receptors at the cell surface. Current Opinion in Plant Biology 15(4): 367–374. doi:10.1016/j.pbi.2012.05.004.

Beljah K, Chaparro A, Kamoun S, Patron N, and Nekrasov V. 2015. Editing plant genomes with CRISPR/Cas9. Current Opinion in Biotechnology 32:76-84. doi: 10.1016/j.copbio.2014.11.007

Bellincampi D, Cervone F and Lionetti V. 2014. Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Frontiers in Plant Science 5: 228. doi:10.3389/fpls.2014.00228.

Bent AF and Mackey D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annual Review of Phytopathology 45: 399–436. doi:10.1146/annurev.phyto.45.062806.094427.

Bernoux M, Ellis JG and Dodds PN. 2011. New insights in plant immunity signaling activation. Current Opinion in Plant Biology 14(5): 512–518. doi:10.1016/j.pbi.2011.05.005.

Bever JD, Mangan SA and Alexander HM. 2015. Maintenance of Plant Species Diversity by Pathogens. Annual Review of Ecology, Evolution, and Systematics, 46(1): 305–325. doi:10.1146/annurev-ecolsys-112414-054306

Bigeard J, Colcombet J and Hirt H. 2015. Signaling mechanisms in pattern-triggered immunity (PTI). Molecular Plant 8(4): 521–539. doi:10.1016/j.molp.2014.12.022.

Bonardi V, Cherkis K, Nishimura MT and Dangl JL. 2012. A new eye on NLR proteins: focused on clarity or diffused by complexity. Current Opinion in Immunology 24(1): 41–50. doi:10.1016/j.coi.2011.12.006.

Boyd LA, Ridout C, O’Sullivan DM, Leach JE and Leung H. 2013. Plant-pathogen interactions: disease resistance in modern agriculture. Trends in Genetics 29(4): 233–240. doi:10.1016/j.tig.2012.10.011.

Brauer EK, Singh DK and Popescu SC. 2014. Next-generation plant science: putting big data to work. Genome Biology 15(1): 301. doi:10.1186/gb4149.

Brown JK. 2015. Durable resistance of crops to disease: a Darwinian perspective. Annual Review of Phytopathology 53: 513–539. doi:10.1146/annurev-phyto-102313-045914.

Burdon JJ and Thrall PH. 2014. What have we learned from studies of wild plant-pathogen associations?—the dynamic interplay of time, space and life-history. European Journal of Plant Pathology 138(3): 417–429. doi:10.1007/s10658-013-0265-9.

Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K and Dinesh-Kumar SP. 2008. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132(3): 449–462. doi:10.1016/j.cell.2007.12.031.

Chiang, Y.-H., & Coaker, G. (2015). Effector triggered immunity: NLR immune perception and downstream defense responses. The Arabidopsis Book, 13, e0183. doi:10.1199/tab.0183

Coll NS, Epple P and Dangl JL. 2011. Programmed cell death in the plant immune system. Cell Death and Differentiation 18(8): 1247–1256. doi:10.1038/cdd.2011.37.

Collier SM and Moffett P. 2009. NB-LRRs work a “bait and switch” on pathogens. Trends in Plant Science 14(10): 521–529. doi:10.1016/j.tplants.2009.08.001

Cook DE, Mesarich CH and Thomma BP. 2015. Understanding plant immunity as a surveillance system to detect invasion. Annual Review of Phytopathology 53: 541–563. doi:10.1146/annurev-phyto-080614-120114.

Conrath U, Beckers GJM, Langenbach CJG and Jaskiewicz MR. 2015. Priming for enhanced defense. Annual Review of Phytopathology, 53(JUNE): 97–119. doi:10.1146/annurev-phyto-080614-120132

Couto D and Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nature Reviews Immunology 16: 537–552. doi:10.1038/nri.2016.77

Cui H, Tsuda K and Parke, JE. 2015. Effector-Triggered Immunity: from pathogen perception to robust defense. Annual Review of Plant Biology 66: 487–511. doi:10.1146/annurev-arplant-050213-040012

De Bruyne L, Höfte M and De Vleesschauwer D. 2014. Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Molecular Plant 7(6): 943–959. doi:10.1093/mp/ssu050.

de Jonge R, Bolton MD and Thomma BPHJ. 2011. How filamentous pathogens co-opt plants: the ins and outs of fungal effectors. Current Opinion in Plant Biology 14(4): 400–406. doi:10.1016/j.pbi.2011.03.005.

Fan J and Doerner P. 2012. Genetic and molecular basis of nonhost disease resistance: complex, yes; silver bullet, no. Current Opinion in Plant Biology 15(4): 400–406. doi:10.1016/j.pbi.2012.03.001.

Fauser F, Schiml S and Puchta H. 2014. Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant Journal 79(2): 348–359. doi:10.1111/tpj.12554

Fei Q, Zhang Y, Xia, R and Meyers B. 2016. Small RNAs add zing to the zig-zag model of plant defenses. MPMI. 29(3):165-169. doi.org/10.1094/MPMI-09-15-0212-FI

Flor HH. 1971. Current status of the gene-for-gene concept. Annual Review of Phytopathology 9(1): 275–296. doi:10.1146/annurev.py.09.090171.001423.

Fu ZQ and Dong X. 2013. Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 64: 839–863. doi:10.1146/annurev-arplant-042811-105606.

Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM and Toulmin C. 2010. Food security: the challenge of feeding 9 billion people. Science 327(5967): 812–818. doi:10.1126/science.1185383.

Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK and Park SW. 2012. Plant disease resistance genes: current status and future directions. Physiological and Molecular Plant Pathology 78: 51–65. doi:10.1016/j.pmpp.2012.01.002.

Hein I, Gilroy EM, Armstrong MR and Birch PR. 2009. The zig-zag-zig in oomycete-plant interactions. Mol Plant Pathology 10(4): 547–562. doi:10.1111/j.1364-3703.2009.00547.x.

Hendel A, Fine EJ, Bao G and Porteus MH. 2015. Quantifying on- and off-target genome editing. Trends in Biotechnology 33(2): 132–140. doi:10.1016/j.tibtech.2014.12.001

Hogenhout SA, Van der Hoorn RAL, Terauchi R and Kamoun S. 2009. Emerging concepts in effector biology of plant-associated organisms. Molecular Plant-Microbe Interactions 22(2): 115–122. doi:10.1094/MPMI-22-2-0115.

Huang S, Weigel D, Beachy RN and Li J. 2016. A proposed regulatory framework for genome-edited crops. Nature Genetics, 48(2): 109–111. doi.org/10.1038/ng.3484

Huang J, Yang M and Zhang X. 2016. The function of small RNA in plant biotic stress response. Journal Of Integrative Plant Biology 58(4): 312-327. doi: 10.1111/jipb.12463

Jia H and Nian W. 2014. Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE 9(4). doi.org/10.1371/journal.pone.0093806

Jones JDG and Dangl JL. 2006. The plant immune system. Nature 444(7117): 323–329. doi:10.1038/nature05286.

Karasov TL, Horton MW and Bergelson J. 2014. Genomic variability as a driver of plant-pathogen coevolution. Current Opinion in Plant Biology 18: 24–30. doi:10.1016/j.pbi.2013.12.003.

Keller H, Boyer L and Abad P. 2016. Disease susceptibility in the zig-zag model of host microbe interactions: only a consequence of inmune suprression?. Molecular Plant Pathology. 17(4):475-479. doi: 10.1111/mpp.12371

Knief C. 2014. Analysis of plant microbe interactions in the era of next generation sequencing technologies. Frontiers in Plant Science 5: 216. doi:10.3389/fpls.2014.00216.

Koeck M, Hardham AR and Dodds PN. 2011. The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell Microbiology 13(12): 1849–1857. doi:10.1111/j.1462-5822.2011.01665.x.

Kole C, Muthamilarasan M, Henry R, Edwards D, Sharma R, Abberton M, … Prasad M. 2015. Application of genomics-assisted breeding for generation of climate resilient crops: progress and prospects. Front Plant Sci, 6(August): 563. doi:10.3389/fpls.2015.00563

Kushalappa AC, Yogendra KN and Karre S. 2016. Plant Innate Immune Response: Qualitative and Quantitative Resistance. Critical Reviews in Plant Sciences 35(1): 38–55. doi:10.1080/07352689.2016.1148980

Lai Z and Mengiste T. 2013. Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens. Current Opinion in Plant Biology 16(4): 505–512. doi:10.1016/j.pbi.2013.06.014.

Lapin D and Van den Ackerveken G. 2013. Susceptibility to plant disease: more than a failure of host immunity. Trends in Plant Science 18(10): 546–554. doi:10.1016/j.tplants.2013.05.005.

Lee S-J and Rose JKC. 2010. Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins. Plant Signaling & Behavior 5(6): 769–772. doi:10.4161/psb.5.6.11778.

Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS and Ronald PC. 2009. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326(5954): 850–853. doi:10.1126/science.1173438.

Lee D, Edmeades S, Nys E, McDonald A and Janssen Y. 2014. Developing local adaptation strategies for climate change in agriculture: A priority-setting approach with application to Latin America. Global Enviromental Change 29: 78-91. doi:10.1016/j.gloenvcha.2014.08.002

Li Y, Huang F, Lu Y, Shi Y, Zhang M, Fan J and Wang W. 2013. Mechanism of plant--microbe interaction and its utilization in disease-resistance breeding for modern agriculture. Physiological and Molecular Plant Pathology 83: 51–58. doi:10.1016/j.pmpp.2013.05.001.

Liu J, Elmore JM, Lin Z-JD and Coaker G. 2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host & Microbe 9(2): 137–146. doi:10.1016/j.chom.2011.01.010.

Lopez C. 2011. Descifrando las bases moleculares de la resistencia cuantitativa. Acta Biologica Colombiana 16(2): 3.

Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X, Zheng X, … et al. 2015. A CRISPR/Cas9 Toolbox for Multiplexed Plant Genome Editing and Transcriptional Regulation. Plant Physiology 169(2): 971–85. doi:10.1104/pp.15.00636

Lu D, Wu S, Gao X, Zhang Y, Shan L and He P. 2010. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proceedings of the National Academy of Sciences 107(1): 496–501. doi:10.1073/pnas.0909705107.

Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B et al. 2015. A Robust CRISPR/Cas9 System for Convenient, High-Efficiency Multiplex Genome Editing in

Monocot and Dicot Plants. Molecular Plant. 8. 1274-1284. doi:10.1016/j.molp.2015.04.007

Mahesh S. 2016. The State of Art of New Transgenic Techniques in Plant Breeding: A Review. Journal of Advances in Biology & Biotechnology 9(4): 1–11. doi:10.9734/JABB/2016/27846

Macho AP and Zipfel C. 2014. Plant PRRs and the activation of innate immune signaling. Molecular Cell 54(2): 263–272. doi:10.1016/j.molcel.2014.03.028.

Maekawa T, Kufer TA and Schulze-Lefert P. 2011. NLR functions in plant and animal immune systems: so far and yet so close. Nature Immunology 12(9): 817–826. doi:10.1038/ni.2083.

Marone D, Russo MA, Laidò G, De Leonardis AM and Mastrangelo AM. 2013. Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. International Journal of Molecular Science 14(4): 7302–7326. doi:10.3390/ijms14047302.

Mba C, Guimaraes E and Ghosh K. 2012. Re-orienting crop improvement for the changing climatic conditions of the 21st century. Agriculture & Food Security. 1:7. doi: 10.1186/2048-7010-1-7

Mattews, R., Rivington, M., Muhammed, S., Newton, A., Hallet, P., 2013. Adapting crops and cropping systems to future climates to ensure food security: The role of crop modelling. Global Food Security. 2 24-28

Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H and Shibuya N. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proceedings of the National Academy of Sciences 104(49): 19613–19618. doi:10.1073/pnas.0705147104.

Monaghan J and Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Current Opinion in Plant Biology 15(4): 349–357. doi:10.1016/j.pbi.2012.05.006.

Mujica N and Kroschel J. 2013. Pest intensity-crop loss relationships for the leafminer fly Liriomyza huidobrensis (Blanchard) in different potato (Solanum tuberosum L.)

varieties. Crop Protection 6-16. doi:10.1016/j.cropro.2012.12.019

Nagamangala Kanchiswamy C, Sargent DJ, Velasco R, Maffei ME and Malnoy M. 2015. Looking forward to genetically edited fruit crops. Trends in Biotechnology 33(2): 62–64. doi:10.1016/j.tibtech.2014.07.003

Niks RE, Qi X and Marcel TC. 2015. Quantitative resistance to biotrophic filamentous plant pathogens: concepts, misconceptions, and mechanisms. Annual Review of Phytopathology 53: 445–470. doi:10.1146/annurev-phyto-080614-115928.

Okmen B and Doehlemann G. 2014. Inside plant: biotrophic strategies to modulate host immunity and metabolism. Current Opinion in Plant Biology 20: 19–25. doi:10.1016/j.pbi.2014.03.011.

Pais M, Win J, Yoshida K, Etherington GJ, Cano LM, Raffaele S, Banfield MJ, Jones A, Kamoun S and Saunders DG. 2013. From pathogen genomes to host plant processes: the power of plant parasitic oomycetes. Genome Biology 14(6): 211. doi:10.1186/gb-2013-14-6-211.

Poppy G, Jepson P, Pickett A and Birkett A. 2014. Achieving food and environmental

security: new approaches to close the gap. Phylosophical transactions of the Royal Society. 369:20120272

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. doi:10.1146/annurev-arplant-043014-114623.

Pritchard L and Birch P. 2011. A systems biology perspective on plant-microbe interactions: biochemical and structural targets of pathogen effectors. Plant Science 180(4): 584–603. doi:10.1016/j.plantsci.2010.12.008.

Pritchard L and Birch PR. 2014. The zigzag model of plant-microbe interactions: is it time to move on. Molecular Plant Pathology 15(9): 865–870. doi:10.1111/mpp.12210.

Quetier, F. 2016. The CRISPR-Cas9 technology: Closer to the ultimate toolkit fortargeted genome editing. Plant Science. 242:65-76. http://dx.doi.org/10.1016/j.plantsci.2015.09.003

Robert-Seilaniantz A, Navarro L, Bari R and Jones J. 2007. Pathological hormone imbalances. Current Opinion in Plant Biology 10(4): 372 – 379. doi:http://dx.doi.org/10.1016/j.pbi.2007.06.003.

Ron M and Avni A. 2004. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16(6): 1604–1615. doi:10.1105/tpc.022475.

Ronald P. 2011. Plant genetics, sustainable agriculture and global food security. Genetics 188(1): 11–20. doi:10.1534/genetics.111.128553.

Saintenac C, Zhang W, Salcedo A, Rouse MN, Trick HN, Akhunov E and Dubcovsky J. 2013. Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science 341(6147): 783–786. doi:10.1126/science.1239022.

Savary A, Ficke A and Aubertot J. 2012. Crop losses due to diseases and their implications for global food production losses and food security. Food Security. doi:10.1007/s12571-012-0200-5

Schmidt SM and Panstruga R. 2011. Pathogenomics of fungal plant parasites: what have we learnt about pathogenesis. Current Opinion in Plant Biology 14(4): 392–399. doi:10.1016/j.pbi.2011.03.006.

Schulze-Lefert P and Panstruga R. 2011. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends in Plant Science 16(3): 117–125. doi:10.1016/j.tplants.2011.01.001.

Shan Q, Wang Y, Li J and Gao C. 2014. Genome editing in rice and wheat using the CRISPR/Cas system. Nature Protocols 9(10): 2395–410. doi:10.1038/nprot.2014.157

Smale ST. 2012. Transcriptional regulation in the innate immune system. Current Opinion in Immunology 24(1): 51–57. doi:10.1016/j.coi.2011.12.008.

Song J, Win J, Tian M, Schornack S, Kaschani F, Ilyas M, van der Hoorn RAL and Kamoun S. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proceedings of the National Academy of Sciences 106(5): 1654–1659. doi:10.1073/pnas.0809201106.

Spoel SH and Dong X. 2012. How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews Immunology 12(2): 89–100. doi:10.1038/nri3141.

Stael S, Kmiecik P, Willems P, Van Der Kelen K, Coll NS, Teige M and Van Breusegem F. 2015. Plant innate immunity--sunny side up. Trends in Plant Science 20(1): 3–11. doi:10.1016/j.tplants.2014.10.002.

Stuart, 2015. Insect effectors and gene-for-gene interactions with host plants. Current Opinion in Insect Science. Vol 9: 56-61. http://dx.doi.org/10.1016/j.cois.2015.02.010

Thynne E, McDonald MC and Solomon PS. 2015. Phytopathogen emergence in the genomics era. Trends in Plant Science 20(4): 246–255. doi:10.1016/j.tplants.2015.01.009.

Trapet P, Kulik A, Lamotte O, Jeandroz S, Bourque S, Nicolas-Francès V, Rosnoblet C, Besson-Bard A and Wendehenne D. 2015. NO signaling in plant immunity: a tale of messengers. Phytochemistry 112: 72–79. doi:10.1016/j.phytochem.2014.03.015.

Uma B, Rani TS and Podile AR. 2011. Warriors at the gate that never sleep: non-host resistance in plants. Journal of Plant Physiology 168(18): 2141–2152. doi:10.1016/j.jplph.2011.09.005.

Van der Hoorn RAL and Kamoun S. 2008. From guard to decoy: a new model for perception of plant pathogen effectors. The Plant Cell 20(8): 2009–2017. doi:10.1105/tpc.108.060194.

Vayssier-Taussat M, Albina E, Citti C, Cosson JF, Jacques MA, Lebrun MH, Le Loir Y, Ogliastro M, Petit MA, Roumagnac P and Candresse T. 2014. Shifting the paradigm from pathogens to pathobiome: new concepts in the light of meta-omics. Frontiers in Cellular and Infection Microbiology 4: 29. doi:10.3389/fcimb.2014.00029.

Vleeshouwers VG and Oliver RP. 2014. Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Molecular Plant and Microbe Interactions 27(3): 196–206. doi:10.1094/MPMI-10-13-0313-IA.

Vlesshouwers VG, Xu J., and Hofte. 2014. Making sense of hormone-mediated defense networking: from rice to Arabidopsis. Frontiers in Plant Science. Vol 5. Article 611. doi: 10.3389/fpls.2014.00611.

Wang ZY. 2012. Brassinosteroids modulate plant immunity at multiple levels. Proceedings of the National Academy of Sciences 109(1): 7–8. doi:10.1073/pnas.1118600109.

Weeks DP, Spalding MH and Yang B. 2016. Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnology Journal 14(2): 483–495. doi:10.1111/pbi.12448

Wu CH, Krasileva KV, Banfield MJ, Terauchi R and Kamoun S. 2015. The “sensor domains” of plant NLR proteins: more than decoys. Frontiers in Plant Science 6: 134. doi:10.3389/fpls.2015.00134.

Wu S, Shan L and He P. 2014a. Microbial signature-triggered plant defense responses and early signaling mechanisms. Plant Science 228: 118–126. doi:10.1016/j.plantsci.2014.03.001.

Wu L, Chen H, Curtis C and Fu, Z. Q. 2014b. Go in for the kill. Virulence 5(7): 710–21. doi:10.4161/viru.29755

Yoshioka H, Mase K, Yoshioka M, Kobayashi M and Asai S. 2011. Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity. Nitric Oxide 25(2): 216–221. doi:10.1016/j.niox.2010.12.008.

Zipfel C. 2014. Plant pattern-recognition receptors. Trends in Immunology 35(7). doi:10.1016/j.it.2014.05.004

Zvereva A and Poggin M. 2012. Silencing and Innate Immunity in Plant defense against viral and non-viral pathogens. Viruses. 4: 2578-2597. doi: 10.3390/v4112578

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Plant responses to pathogen attack: molecular basis of qualitative resistance. (2017). Revista Facultad Nacional De Agronomía Medellín, 70(2), 8225-8235. https://doi.org/10.15446/rfna.v70n2.64526