Pathogen Resistance Signalling in Plants

Abstract

Within natural ecosystems, most plants are resistant to most pathogens. At a fundamental level, this seemingly simply truth may hold the key to our understanding of how plants have evolved to survive under a myriad of environmental conditions and their associated stresses. Indeed, in defining how plants evolve, adapt and maintain broad spectrum resistance to most pathogens – typically referred to as non‐host resistance – we may not only reveal the mechanisms that underpin plant resistance signalling but also the precise manner in which plants regulate these processes under various environmental conditions. Herein lies the greatest challenge and unanswered question in the field of agriculture today: How do we feed 9 billion people by the year 2050? To address this, one of the first hurdles that must be overcome is a full understanding of the processes that regulate stress (i.e. abiotic and biotic) signalling in plants, as well as the processes that define pathogen and host specificity, including the performance of these processes under rapidly changing environmental conditions. In the case of pathogen infection, plants utilise a broad suite of innate and inducible mechanisms to resist invasion. In large part, these processes are governed by the activity of resistance (R) proteins, which are evolutionarily conserved and highly evolved proteins that function not only in pathogen recognition but also in the activation of the cellular processes necessary to defend against proliferation and the elicitation of disease. Furthermore, recent data supports the hypothesis that numerous processes, such as the balance between growth and defence, also contribute to the host resistance and pathogen virulence.

Key Concepts

  • Most plants are resistant to most pathogens.
  • Modern agriculture practices positively impact crop yield and durability. These practices can also have a negative impact on the unintended selection and enrichment of virulent pathogens.
  • Plants defend against pathogen invasion using a suite of highly conserved resistance (R) genes.
  • Pathogens have evolved to recognise and respond to the activity of plant R proteins through the deployment of secreted virulence factors.
  • Immune signalling in plants utilises various pre‐formed and inducible processes to defend against pathogen infection.
  • Many basic physiological processes, including response to light, temperature and water availability, are associated with, and required for, immune signalling.
  • The development of advanced genome sequencing technologies has increased the speed at which the development and selection of elite breeding lines are deployed into cropping systems.
  • Current plant breeding approaches utilise a hybrid of molecular genomics and classical breeding techniques to identify and introduce desirable traits into crops to enhance plant performance (e.g. resistance) and yield.

Keywords: biotic stress; immune signalling; pathogen; disease resistance; disease control; disease management; molecular biology; genomics; plant pathology

Figure 1. Illustration of the interactions between plants, pathogens, humans and the environment. As an expansion of the ‘Disease Triangle’ paradigm, human influence on modern agricultural practices has significantly impacted not only the performance of cropping systems as a function of biotic stress performance but also the inadvertent selection of enhanced, often hyper‐virulent pathogen races. As environmental conditions and abiotic stressors become more taxing on both plants and their pathogens, the influence of high temperatures, for example, has opposing effectors. For example, at high temperatures, the growth and selection of microbes with enhanced virulence is often observed. Conversely, at high temperatures, plant performance is often negatively affected, with plant resources and signalling processes shifted to abiotic stress tolerance/response signalling. As a result, plants are ‘forced to choose’ between survival due to abiotic stress and to allocate signalling to support immunity and defence signalling. As a key feature of the interaction of plants with environmental and microbes, human influence on this process is also becoming more evident. As populations increase, there is also an increase in the need to produce crops that generate higher yields, as well as perform under what are typically limiting environmental conditions (i.e. high temperature and drought). As a result, plant breeders must often choose between a balance of phenotypic traits and genotypes to introduce lines with elite performance under one or the other conditions, including the introduction of lines with enhanced nutritional or horticultural qualities. As a function of disease management, chemical treatment of crops with pesticides/fungicides influences not only plant performance under biotic stress conditions but can often times have a negative – unintended – influence on the selection and propagation of hyper‐virulent, pathogenic microbes. As a combination of each of these factors, we present an updated model of the classical ‘Disease Triangle’ to highlight the influence of humans on agricultural systems and plant performance: the ‘Disease Diamond’. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
Figure 2. Plants recognise a myriad of biotic conditions, pathogens and stresses and respond using complex, highly specific immune signalling cascades. The recognition of pathogenic organisms by plants is typically initiated through the perception of evolutionarily conserved features by pattern recognition receptors, and co‐receptors (represented by the blue and red transmembrane proteins, respectively), present on the cell surface of the invading organisms; in short, these molecules are perceived as ‘non‐self’ by the host plant. This form of immune signalling, termed pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI) results in the activation of a broad, non‐specific, defence signalling response that initiates a number of conserved and highly effective pathogen resistance mechanisms, including mitogen‐activated protein kinase (MAPK) signalling, the deposition of callose and the induction of defence‐responsive genes. As a more robust, sustained immune response, following the perception of pathogen‐secreted effector proteins [represented by black circles (bacterial effectors) and orange stars (oomycete effectors)], plants initiate a second, amplified, defence response, termed effector‐triggered immunity (ETI). This form of immune signalling relies on the specific interaction – either direct or indirect – between plant resistance (R) proteins and pathogen‐derived avirulence (Avr) proteins – broadly referred to as effectors. Similar to the activation of PTI, ETI initiates a series of similar, shared, signalling cascades whose outcome results in localised cell death responses, termed the hypersensitive response, which is similar in function to apoptosis. The outcome of this process is the abrogation of pathogen growth, and in most cases, the survival of the host. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
Figure 3. Immune signalling in plants and animals share a number of functionally similar pathogen perception and host signalling processes. The perception of pathogens in both plants and animals uses similar signalling mechanisms to induce changes in gene expression and cellular response to biotic stress. As a first response to pathogen invasion, plants and animals utilise a highly conserved immune signalling process – PTI – to initiate broad, non‐specific defence signalling cascades, including the generation of reactive oxygen species (ROS), activation of MAPK signalling and changes in gene expression associated with host defence. In plants, the induction of a second, amplified response – ETI – is initiated in response to the perception of secreted pathogen avirulence/effector proteins, which are recognised by host‐specific R proteins. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
Figure 4. Classical illustration of the genetic foundation for the ‘Gene‐for‐Gene’ interaction. Proposed by Flor in the 1940s, this foundational hypothesis describing the inheritance of resistance in plants and the maintenance of virulence in pathogens posits that for every gene in a plant that confers resistance, there is a corresponding, host‐recognised, gene in the pathogen that confers avirulence. In the presence of both genes (i.e. R + Avr), plants are resistance. When either gene is lacking (i.e. r + avr), plants are susceptible. This basic process has been used to define a number of R/Avr interactions in plants in the 70+ years since it was first discovered, and moreover, it provided a tractable mechanism to guide a number of plant breeding outcomes aimed at the generation and selection of plants with broad pathogen resistance. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
Figure 5. R protein classes and their cellular location. The predicted domains of R proteins which confer either race‐specific or race‐non‐specific resistance are presented schematically: CC, coiled‐coil domain; TIR, Toll and Interleukin 1 receptor‐like motif; NB, nucleotide binding site; LRD, leucine‐rich domain; LRR, leucine‐rich repeat; NLS, nuclear localisation signal; ECS, endocytosis signal; PEST, Pro‐Glu‐Ser‐Ther‐like sequence; WRKY, motif characteristic of some plant transcription factors; 1, 2, 3, 4 – novel domains that lack significant homology to known proteins; 5, domain with homology to a B‐lectin; 6, structure with a weak similarity to a PAN domain; 7, structure with homology to epidermal growth factor (EGF)‐like domain; Cf‐2, Cf‐4 and Cf‐5 confer resistance to Cladosporium fulvum races expressing, respectively, Avr2, Avr4 and Avr5; L6 flax rust resistance 6; Mla10, resistance to Blumeria graminis f. sp. hordei expressing Avra10; RPM1, resistance to P. syringae pv. maculicola expressing AvrRpm1 or AvrB; RPP5, resistance to Hyaloperonospora parasitica expressing ATR5. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
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References

Amselem J, Cuomo CA, van Kan JA, et al. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genetics 7: e1002230.

Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

Bent A, Kunkel BN, Dahlbeck D, et al. (1994) RPS2 of Arabidopsis thaliana: a leucine‐rich repeat class of plant disease resistance genes. Science 265: 1856–1860.

Bogdanove AJ, Schornack S and Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Current Opinion in Plant Biology 13: 394–401.

Boller T and Felix G (2009) A renaissance of elicitors: perception of microbe‐associated molecular patterns and danger signals by pattern‐recognition receptors. Annual Review of Plant Biology 60: 379–406.

Braam J (2005) In touch: plant responses to mechanical stimuli. New Phytologist 165: 373–389.

Bryant RRM, McGrann GRD, Mitchell AR, et al. (2014) A change in temperature modulates defence to yellow (stripe) rust in wheat line UC1041 independently of resistance gene Yr36. BMC Plant Biology 14: 10.

Burkhardt A, Buchanan A, Cumbie JS, et al. (2015) Alternative splicing in the obligate biotrophic oomycete pathogen Pseudoperonospora cubensis. Molecular Plant‐Microbe Interactions 28: 298–309.

Century KS, Holub EB and Staskawicz BJ (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and fungal pathogen. Proceedings of the National Academy of Sciences of the United States of America 92: 6597–6601.

Chisholm ST, Coaker G, Day B, et al. (2006) Host‐microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803–814.

Choi J, Tanaka K, Cao Y, et al. (2014) Identification of a plant receptor for extracellular ATP. Science 343: 290–294.

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

Dangl JL, Horvath DM and Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341: 746–751.

Dean R, van Kan JAL, Pretorius ZA, et al. (2012) The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13: 414–430.

Denoeud F, Carretero‐Paulet L, Dereeper A, et al. (2014) The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345: 1181–1184.

Erbs G, Molinaro A, Dow JM, et al. (2010) Lipopolysaccharides and plant innate immunity. Subcellular Biochemistry 53: 387–403.

Flor HH (1955) Host‐parasite interaction in flax rust‐its genetics and other implications. Phytopathology 45: 680–685.

Furutani A, Takaoka M, Sanada H, et al. (2009) Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. Molecular Plant‐Microbe Interactions 22: 96–106.

Gerland P, Raftery AE, Sevcikova H, et al. (2014) World population stabilization unlikely this century. Science 346: 234–237.

Goff SA, Ricke D, Lan T, et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92–100.

Gomez‐Gomez L and Boller T (2000) FLS2: an LRR receptor‐like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Molecular Cell 5: 1003–1011.

Gonsalves D (1998) Control of papaya ringspot virus in papaya: a case study. Annual Review of Phytopathology 36: 415–437.

Hamilton JP and Buell CR (2012) Advances in plant genome sequencing. Plant Journal 70: 177–190.

Hammond‐Kosack KE and Kanyuka K (2007) Resistance genes (R genes) in plants. Encyclopedia of Life Sciences. DOI: 10.1002/9780470015902.a0020119.

Hass BJ, Kamoun S, Zody MC, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393–398.

He SY, Nomura K and Whittam TS (2004) Type III protein secretion mechanism in mammalian and plant pathogens. Biochimica et Biophysica Acta 1694: 181–206.

Holton N, Nekrasov V, Ronald PC, et al. (2014) The phylogenetically‐related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLOS Pathogens 11: e1004602.

Hua J (2013) Modulation of plant immunity by light, circadian rhythm, and temperature. Current Opinion in Plant Biology 16: 406–413.

Huang S, Li R, Zhang Z, et al. (2009) The genome of the cucumber, Cucumis sativus L. Nature Genetics 41: 1275–1283.

Huot B, Yao J, Montgomery BL, et al. (2014) Growth‐defense tradeoffs in plants: a balancing act to optimize fitness. Molecular Plant 7: 1267–1287.

International Rice Genome Sequencing Project (2005) The map‐based sequence of the rice genome. Nature 436: 793–800.

Johnson PTJ and Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Botany 213: 961–970.

Jones JDG (2011) Why genetically modified crops? Philosophical Transactions of the Royal Society A 369: 1807–1816.

Jones JDG and Dangl JL (2006) The plant immune system. Nature 444: 323–329.

Kaku H, Nishizawa Y, Ishii‐Minami N, et al. (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proceedings of the National Academy of Sciences of the United States of America 103: 11086–11091.

Kimes NE, Grim CJ, Johnson WR, et al. (2012) Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME Journal 6: 835–846.

Knepper C, Savory EA and Day B (2011) Arabidopsis NDR1 is an integrin‐like protein with a role in fluid loss and plasma membrane‐cell wall adhesion. Plant Physiology 156: 286–300.

Kumar V and Jain M (2014) The CRISPER‐Cas system for plant genome editing: advances and opportunities. Journal of Experimental Botany 66: 47–57.

Kunze G, Zipfel C, Robatzek S, et al. (2004) The N terminus of bacterial elongation factor tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496–3507.

Lacombe S, Rougon‐Cardoso A, Sherwood E, et al. (2009) Interfamily transfer of a plant pattern‐recognition receptor confers broad‐spectrum bacterial resistance. Nature Biotechnology 28: 365–370.

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.

Liu W, Liu J, Triplett L, et al. (2014) Novel insights into rice innate immunity against bacterial and fungal pathogens. Annual Review Of Phytopathology 52: 213–241.

Lu H, Zhang C, Albrecht U, et al. (2013) Overexpression of a citrus NDR1 ortholog increases disease resistance in Arabidopsis. Frontiers in Plant Science 4: 157.

Macho AP and Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Molecular Cell 54: 263–272.

Malnoy M, Marten S, Norelli JL, et al. (2012) Fire blight: applied genomic insights of the pathogen and host. Annual Review of Phytopathology 50: 475–94.

Mindrinos M, Katagirl F, Yu GL, et al. (1994) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide‐binding site and leucine‐rich repeats. Cell 78: 1089–1099.

Ming R, Hou S, Feng Y, et al. (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452: 991–997.

Nakashima K, Yamaguchi‐Shinozaki K and Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Frontiers in Plant Science 5: 170.

Pagan I, Gonzalez‐Jara P, Moreno‐Letelier A, et al. (2012) Effect of biodiversity changes in disease risk: exploring disease emergence in a plant‐virus system. PLoS Pathogens 8: e1002796.

Paine JA, Shipton CA, Chaggar S, et al. (2005) Improving the nutritional value of Golden Rice through increased pro‐vitamin A content. Nature Biotechnology 23: 482–487.

Paterson AH, Bowers JE, Bruggmann R, et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551–556.

Roscher C, Schumacher J, Foitzik O, et al. (2007) Resistance to rust fungi in Lolium perenne depends on within‐species variation and performance of the host species in grassland of different plant diversity. Oecologia 153: 173–183.

Sano S, Aoyama M, Nakai K, et al. (2014) Light‐dependent expression of flg22‐induced defense genes in Arabidopsis. Frontiers in Plant Science 5: 531.

Schmutz J, Cannon SB, Schlueter J, et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature 463: 178–183.

Scholthof KBG (2007) The disease triangle: pathogens, the environment and society. Nature Reviews Microbiology 5: 152–156.

Sherd LB, Tan X, Mao H, et al. (2010) Jasmonate perception by inositol‐phosphate‐potentiated COI1‐JAZ co‐receptor. Nature 468: 400–407.

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

Staskawicz BJ, Dahlbeck D and Keen NT (1984) Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race‐specific incompatibility on Glycine max (L.) Merr. Proceedings of the National Academy of Sciences of the United States of America 81: 6024–6028.

Steen BR, Lian T, Zuyderduyn S, et al. (2002) Temperature‐regulated transcription in the pathogenic fungus Cryptococcus neoformans. Genome Research 12: 1386–1400.

Tester M and Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327: 818–822.

Tintor N, Ross A, Kanehara K, et al. (2013) Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proceedings of the National Academy of Sciences of the United States of America 110: 6211–6216.

Triplett LR, Wedemeyer WJ and Sundin GW (2010) Homology‐based modelling of the Erwinia amylovora type III secretion chaperone DspF used to identify amino acids required for virulence and interaction with the effector DspE. Research in Microbiology 161: 613–618.

Tuskan GA, DiFazio S, Jansson S, et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596–1604.

Valent B and Khang CH (2010) Recent advances in rice blast effector research. Current Opinion in Plant Biology 13: 434–441.

Van Der Biezen E and Jones JDG (1998) Plant disease‐resistance proteins and the gene‐for‐gene concept. Trends in Biochemical Sciences 23: 454–456.

Velasco R, Zharkikh A, Affourtit J, et al. (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics 42: 833–841.

Venter JC, Adams MD, Myers EW, et al. (2001) The sequence of the human genome. Science 291: 1304–1351.

Wang Y, Cheng X, Shan Q, et al. (2014a) Simultaneous editing of three homoealleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Biotechnology 32: 947–952.

Wang Y, Kwon SJ, Wu J, et al. (2014b) Transcriptome analysis of early responsive genes in rice during Magnaporthe oryzae infection. Plant Pathology Journal 4: 343–354.

Woycicki R, Witkowicz J, Gawronski P, et al. (2011) The genome sequence of the North‐European cucumber (Cucumis sativus L.) unravels evolutionary adaptation mechanisms in plants. PLoS One 6: e22728.

Wu F (2006) Mycotoxin reduction in Bt corn: potential economic, health, and regulatory impacts. Transgenic Research 15: 277–289.

Xin XF and He SY (2013) Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annual Review of Phytopathology 51: 473–498.

Yu J, Hu S, Wang J, et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. Indica). Science 296: 79–92.

Zimin A, Stevens KA, Crepeau MW, et al. (2014) Sequencing and assembly of the 22‐Gb Loblolly pine genome. Genetics 196: 875–890.

Zipfel C (2014) Plant pattern‐recognition receptors. Trends in Immunology 35: 345–351.

Zipfel C, Kunze G, Chinchilla D, et al. (2006) Perception of the bacterial PAMP EF‐Tu by the receptor EFR restricts Agrobacterium‐mediation transformation. Cell 125: 749–760.

Zipfel C, Robatzek S, Navarro L, et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764–767.

Further Reading

Belhaj K, Chaparro‐Garcia A, Kamoun S, et al. (2014) Editiong plant genomes with CRISPR/Cas9. Current Opinion in Biotechnology 29: 76–84.

Boyle PC and Martin GB (2015) Greasy tactics in the plant‐pathogen molecular arms race. Journal of Experimental Botany. DOI: 10.1093/jxb/erv059[Epub ahead of print].

Weilberg A, Wang M, Lin FM, et al. (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342: 118–123.

Zhao H, Sun R, Albrecht U, et al. (2013) Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus huanglongbing disease. Molecular Plant 6: 301–310.

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Corrion, Alex, and Day, Brad(Jun 2015) Pathogen Resistance Signalling in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020119.pub2]