Plant Defences against Fungal Attack: Perception and Signal Transduction

Abstract

Plants utilise specialised proteins to perceive fungal invaders as ‘nonself’ by ‘recognising’ specific fungus‐derived molecules. This either results in the onset of massive physical and chemical responses that counter‐invasion by phytopathogenic fungi or enables symbioses with beneficial fungi. Induction of defence occurs when pathogen‐derived molecules such as pathogen‐associated molecular patterns (PAMP) or effectors (AVR) are respectively recognised by specialised plant receptors called pattern recognition receptors (PRR) or resistance proteins (R). Signalling induced downstream of PRR or R activation involves several common events though these may differ in their timing and amplitude.

Key Concepts

  • Plants defend themselves from microbial invasions by recognising the pathogen as ‘nonself’.
  • The perception of ‘nonself’ occurs when plant factors interact with microbial molecules that are either present on the surface of the organism or extruded by them.
  • Pathogen recognition and the subsequent defence response is driven by a two‐tiered innate immune system involving PAMP‐triggered immunity (PTI) and effector‐triggered immunity (ETI).
  • The strength and timing of downstream defence‐related events determine the outcome (resistance or susceptibility) of the host–pathogen interaction.
  • These downstream responses involve reactive oxygen species, ion influxes, MAPK signalling cascades, phytohormones and transcription factors.

Keywords: plant defence; fungal resistance; R gene signalling; plant–fungus interaction; innate immunity

Figure 1. Growth of Hyalopernospora arabidopsidis on resistant (R) and susceptible (S) Arabidopsis thaliana hosts. Upper panel shows prolific growth of fungal mycelia on the susceptible ecotype Nossen (right) as opposed to the resistant ecotype Di‐17 (left). Lower panel shows trypan blue stained leaves exhibiting mycelial growth and sporulation in the susceptible but not in the resistant ecotype. Source: Figure courtesy of Dr. Pradeep Kachroo.
Figure 2. Types of local defence responses induced against fungi. Recognition of pathogen‐/microbe‐associated molecular patterns (PAMP) by plant pattern recognition receptors (PRR) or pathogen effectors (AVR) by plant resistance (R) proteins (directly or indirectly via gaurdee/decoy proteins), induces signalling involving the accumulation of reactive oxygen species (ROS), induction of calcium (Ca2+) signalling and other ion flux, which activates mitogen‐associated protein kinase (MAPK) cascades, resulting in nuclear gene induction via transcription factors. This eventually induces PAMP‐triggered immunity (PTI) upon PAMP recognition or effector‐triggered immunity (ETI) upon AVR recognition in the infected tissue. AVR proteins can interfere with induction of PTI. Induction of ETI is often associated with the onset of the hypersensitive response (HR).
Figure 3. LysM activation by chitin. The LysM domains of Arabidopsis LysM receptor CERK1 bind chitin to activate defence signalling. This involves dimerisation of CERK1 and interactions with the CERK1 orthologue, LYK5. Chitin binding results in phosphorylation of CERK1, which in turn phosphorylates the receptor‐like cytoplasmic kinase PBL27. PBL27, in turn, phosphorylates MAPKKK5. Chitin perception results in dissociation of MAPKKK5 from PBL27 and activates downstream signalling involving the MAPK cascade and induction of transcription factor expression eventually leading to defence activation. The various domains of LysM receptors are depicted in the boxed inset.
Figure 4. Structures of sample R proteins against fungal/oomycete pathogens. (a) Structural depiction of known resistance proteins (R) against fungi (modified and reprinted from Kachroo et al., Signalling mechanisms underlying resistance responses: what have we learned, and how is it being applied? Phytopathology 107:1452–1461). The various structural domains are depicted at the bottom. Subcellular locations are indicated in italics. Although some NLR proteins (containing nucleotide binding and leucine‐rich repeats) are shown to be cytoplasmic, many tend to be attached to the plasma membrane (PM) and can change localisation from the cytoplasm to the nucleus during resistance signalling. (b) Table listing various R proteins shown in a, and the fungal/oomycete pathogen against which they impart resistance.
Figure 5. LOV1 activation in response to the fungal toxin victorin. LOV1 is a CC (coiled coil)‐NB (nucleotide binding)‐LRR (leucine‐rich repeat) type of protein, which imparts disease susceptibility to Cochliobolus victoriae in Arabidopsis thaliana. Binding of the fungal toxin victorin, to the plant thioredoxin TRX‐h5, results in activation of the LOV1 protein. LOV1 activation induces cell death which is proposed to facilitate necrotrophic growth of C. victoriae resulting in disease susceptibility.
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References

AbuQamar S , Chen X , Dhawan R , et al. (2006) Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis cinerea . Plant Journal 48: 28–44.

An C and Mou Z (2013) The function of the Mediator complex in plant immunity. Plant Signaling and Behavior 8: e23182.

Birkenbihl RP , Liu S and Somssich IE (2017) Transcriptional events defining plant immune responses. Current Opinion in Plant Biology 38: 1–9.

Bowman SM and Free SJ (2006) The structure and synthesis of the fungal cell wall. Bioessays 28: 799–808.

Brasier CM and Buck KW (2001) Rapid evolutionary changes in a globally invading fungal pathogen (Dutch elm disease). Biological Invasions 3: 223–233.

Chanda B , Venugopal SC , Kulshrestha S , et al. (2008) Glycerol‐3‐phosphate levels are associated with basal resistance to the hemibiotrophic fungus Colletotrichum higginsianum in Arabidopsis . Plant Physiology 147: 2017–2029.

Chen J , Gutjahr C , Bleckmann A and Dresselhaus T (2015) Calcium signaling during reproduction and biotrophic fungal interactions in plants. Molecular Plant 8: 595–611.

Cheng HQ , Han LB , Yang CL , et al. (2016) The cotton MYB108 forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection. Journal of Experimental Botany 67: 1935–1950.

Dangl JL and Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826–833.

Desaki Y , Miyata K , Suzuki M , Shibuya N and Kaku H (2018) Plant immunity and symbiosis signaling mediated by lysm receptors. Innate Immunity 24: 92–100.

Djamei A , Schipper K , Rabe F , et al. (2011) Metabolic priming by a secreted fungal effector. Nature 478: 395.

Dodds PN , Lawrence GJ , Catanzariti AM , et al. (2006) Direct protein interaction underlies gene‐for‐gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proceedings of the National Academy of Sciences USA 103: 8888–8893.

Flor HH (1971) Current status of the gene‐for‐gene concept. Annual Review of Phytopathology 9: 275–296.

French KE (2017) Engineering mycorrhizal symbioses to alter plant metabolism and improve crop health. Frontiers in Microbiology 8: 1403.

Grant MR and Jones JD (2009) Hormone (dis)harmony moulds plant health and disease. Science 324: 750–752.

van der Hoorn RA and Kamoun S (2008) From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell 20: 2009–2017.

Houterman PM , Cornelissen BJ and Rep M (2008) Suppression of plant resistance gene‐based immunity by a fungal effector. PLoS Pathogens 4: e1000061.

Jia Y , McAdams SA , Bryan GT , Hershey HP and Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. European Molecular Biology Organisation Journal 19: 4004–4014.

de Jonge R , van Esse HP , Maruthachalam K , et al. (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proceedings of the National Academy of Sciences USA 109: 5110–5115.

Kachroo A and Kachroo P (2006) Salicylic acid‐, jasmonic acid– and ethylene–mediated regulation of plant defense signaling. Genetic Engineering (NY) 28: 55–83.

Kachroo P and Kachroo A (2018) Plants pack a quiver full of arrows. Cell Host and Microbe 23: 573–575.

Kachroo A and Robin GP (2013) Systemic signaling during plant defense. Current Opinion in Plant Biology 16: 527–533.

Kachroo A , Venugopal SC , Lapchyk L , et al. (2004) Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis . Proceedings of the National Academy of Sciences USA 101: 5152–5157.

Kachroo A , Vincelli P and Kachroo P (2017) Signaling mechanisms underlying resistance responses: What have we learned, and how is it being applied?. Phytopathology 107: 1452–1461.

Kubicek CP , Starr TL and Glass NL (2014) Plant cell wall‐degrading enzymes and their secretion in plant‐pathogenic fungi. Annual Reviews in Phytopathology 52: 427–451.

Laluk K , Luo H , Chai M , et al. (2011) Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS‐INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP‐triggered immunity in Arabidopsis . Plant Cell 23: 2831–2849.

Lamb C and Dixon RA (1997) The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48: 251–275.

Liu XQ , Bai XQ , Qian Q , et al. (2005) OsWRKY03, a rice transcriptional activator that functions in defense signaling pathway upstream of OsNPR1. Cell Research 15: 593–603.

Liu S , Ziegler J , Zeier J , Birkenbihl RP and Somssich IE (2017) Botrytis cinerea B05.10 promotes disease development in Arabidopsis by suppressing WRKY33‐mediated host immunity. Plant, Cell and Environment 40: 2189–2206.

Lorang JM , Sweat TA and Wolpert TJ (2007) Plant disease susceptibility conferred by a resistance gene. Proceedings of the National Academy of Sciences 37: 14861–14866.

Lorang J , Kidarsa T , Bradford CS , et al. (2012) Science 338: 659–662.

Mandal MK , Chandra‐Shekara AC , Jeong RD , et al. (2012) Oleic acid‐dependent modulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxide‐mediated defense signaling in Arabidopsis . Plant Cell 24: 1654–1674.

Manning VA and Ciuffetti LM (2005) Localization of Ptr ToxA produced by Pyrenophora tritici‐repentis reveals protein import into wheat mesophyll cells. Plant Cell 17: 3203–3212.

Mathur S , Tomar RS and Jajoo A (2018) Arbuscular mycorrhizal fungi (AMF) protects photosynthetic apparatus of wheat under drought stress. Photosynthesis Research. DOI: 10.1007/s11120-018-0538-4.

Miya A , Albert P , Shinya T , et al. (2007) CERK1, a lysm receptor kinase, is essential for chitin elicitor signaling in Arabidopsis . Proceedings of the National Academy of Sciences of the United States of America 104: 19613–19618.

Money NP (2007) The Triumph of the Fungi: A Rotten History. New York: Oxford University Press.

Nambeesan S , AbuQamar S , Laluk K , et al. (2012) Polyamines attenuate ethylene‐mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiology 158: 1034–1045.

Oliveira‐Garcia E and Valent B (2015) How eukaryotic filamentous pathogens evade plant recognition. Current Opinions in Microbiology 26: 92–101.

Patkar RN , Benke PI , Qu Z , et al. (2015) A fungal monooxygenase‐derived jasmonate attenuates host innate immunity. Nature Chemical Biology 11: 733–740.

Petersen M , Brodersen P , Naested H , et al. (2000) Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103: 1111–1120.

Petit‐Houdenot Y and Fudal I (2017) Complex interactions between fungal avirulence genes and their corresponding plant resistance genes and consequences for disease resistance management. Frontiers in Plant Science 8: 1072.

Pieterse CM , Leon‐Reyes A , Van der Ent S and Van wees SC (2009) Networking by small‐molecule hormones in plant immunity. Nature Chemical Biology 5: 308–316.

Plett JM , Daguerre Y , Wittulsky S , et al. (2014) Effector missp7 of the mutualistic fungus. Proceedings of the National Academy of Sciences USA 111: 8299–8304.

Reyna NS and Yang Y (2006) Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Molecular Plant Microbe Interaction 19: 530–540.

Rivas S and Thomas CM (2005) Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum . Annual Review of Phytopathology 43: 395–436.

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: 1604–1615.

Shabab M , Shindo T , Gu C , et al. (2008) Fungal effector protein AVR2 targets diversifying defense‐related cys proteases of tomato. Plant Cell 20: 1169–1183.

Shen Q , Liu Y and Naqvi NI (2018) Fungal effectors at the crossroads of phytohormone signaling. Current Opinion in Microbiology 46: 1–6.

Shimizu T , Nakano T , Takamizawa D , et al. (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant Journal 64: 204–214.

Shine MB , Yang JW , El‐Habbak M , et al. (2016) Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. New Phytologist 212: 627–636.

Shinya T , Nakagawa T , Kaku H and Shibuya N (2015) Chitin‐mediated plant‐fungal interactions: catching, hiding and handshaking. Current Opinions in Plant Biology 26: 64–71.

Tena G , Boudsocq M and Sheen J (2011) Protein kinase signaling networks in plant innate immunity. Current Opinion in Plant Biology 14: 519–529.

Thomma BP , Nürnberger T and Joosten MH (2011) Of PAMPs and effectors: the blurred PTI‐ETI dichotomy. Plant Cell 23: 4–15.

Torres MA , Jones JD and Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiology 141: 373–378.

Tsuda K and Katagiri F (2010) Comparing signaling mechanisms engaged in pattern‐triggered and effector‐triggered immunity. Current Opinion in Plant Biology 13: 459–465.

Tyler BM (2002) Molecular basis of recognition between Phytophthora pathogens and their hosts. Annual Review of Phytopathology 40: 137–167.

Wang C , El‐Shetehy M , Shine MB , et al. (2014) Free radicals mediate systemic acquired resistance. Cell Reports 7: 348–355.

Wang J , Tao F , Tian W , et al. (2017) The wheat WRKY transcription factors tawrky49 and tawrky62 confer differential high‐temperature seedling‐plant resistance to Puccinia striiformis f. sp. tritici . Plos One 12: e0181963.

Wendehenne D , Gao QM , Kachroo A and Kachroo P (2014) Free radical ‐mediated systemic immunity in plants. Current Opinion in Plant Biology 20: 127–134.

Yu X , Feng B , He P and Shan L (2017) From chaos to harmony: responses and signaling upon microbial pattern recognition. Annual Reviews in Phytopathology 55: 109–137.

Yuan P , Jauregui E , Du L , Tanaka K and Poovaiah BW (2017) Calcium signatures and signaling events orchestrate plant‐microbe interactions. Current Opinion in Plant Biology 38: 173–183.

Zhang L , Kars I , Essenstam B , et al. (2014) Fungal endopolygalacturonases are recognized as microbe associated molecular patterns by the Arabidopsis receptor‐like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiology 164: 352–364.

Zhou XT , Jia LJ , Wang HY , et al. (2018) The potato transcription factor stbzip61 regulates dynamic biosynthesis of salicylic acid in defense against Phytophthora infestans infection. Plant Journal 95 (6): 1055–1068.

Zipfel C (2008) Pattern‐recognition receptors in plant innate immunity. Current Opinions in Immunology 20: 10–16.

Further Reading

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

Lo Presti L and Kahmann R (2017) How filamentous plant pathogen effectors are translocated to host cells. Current Opinion in Plant Biology 38: 19–24.

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Xiao, Xueqiong, and Kachroo, Aardra(Jan 2019) Plant Defences against Fungal Attack: Perception and Signal Transduction. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0003438.pub3]