Plants versus pathogens: an evolutionary arms race
Jonathan P. Anderson A , Cynthia A. Gleason A , Rhonda C. Foley A , Peter H. Thrall B , Jeremy B. Burdon B and Karam B. Singh A C DA CSIRO Plant Industry, Centre for Environment and Life Sciences, Private Bag #5, Wembley, WA 6913, Australia.
B CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.
C The Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, Perth, WA 6009, Australia.
D Corresponding author. Email: karam.singh@csiro.au
This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.
Functional Plant Biology 37(6) 499-512 https://doi.org/10.1071/FP09304
Submitted: 21 December 2009 Accepted: 7 April 2010 Published: 20 May 2010
Abstract
The analysis of plant–pathogen interactions is a rapidly moving research field and one that is very important for productive agricultural systems. The focus of this review is on the evolution of plant defence responses and the coevolution of their pathogens, primarily from a molecular-genetic perspective. It explores the evolution of the major types of plant defence responses including pathogen associated molecular patterns and effector triggered immunity as well as the forces driving pathogen evolution, such as the mechanisms by which pathogen lineages and species evolve. Advances in our understanding of plant defence signalling, stomatal regulation, R gene–effector interactions and host specific toxins are used to highlight recent insights into the coevolutionary arms race between pathogens and plants. Finally, the review considers the intriguing question of how plants have evolved the ability to distinguish friends such as rhizobia and mycorrhiza from their many foes.
Additional keywords: bacteria, defence, disease, fungus, insect, symbiosis.
Acknowledgements
We thank members of the Singh laboratory for helpful comments. The work in the authors’ laboratories on biotic stress is supported by CSIRO, The Grains Research and Development Corporation and the National Institute of Health (NIH grant 5RO1 GM074265–01A2). We apologise to those colleagues we could not cite due to the broad scope of this review and space limitations.
Altenbach D, Robatzek S
(2007) Pattern recognition receptors: from the cell surface to intracellular dynamics. Molecular Plant–Microbe Interactions 20, 1031–1039.
| Crossref | GoogleScholarGoogle Scholar |
Araki H,
Tian D,
Goss EM,
Jakob K,
Halldorsdottir SS,
Kreitman M, Bergelson J
(2006) Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 5887–5892.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Asai T,
Tena G,
Plotnikova J,
Willmann MR,
Chiu WL,
Gomez-Gomez L,
Boller T,
Ausubel FM, Sheen J
(2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Axtell MJ, Staskawicz BJ
(2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369–377.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bari R, Jones J
(2009) Role of plant hormones in plant defence responses. Plant Molecular Biology 69, 473–488.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Barrett LG,
Thrall PH, Burdon JJ
(2007) Evolutionary diversification through hybridization in a wild host–pathogen interaction. Evolution 61, 1613–1621.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Barrett LG,
Thrall PH,
Burdon JJ,
Nicotra AB, Linde CC
(2008) Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Molecular Ecology 17, 3401–3415.
| Crossref |
PubMed |
Barrett LG,
Thrall PH,
Dodds PN,
van der Merwe M,
Linde CC,
Lawrence GH, Burdon JJ
(2009) Diversity and evolution of effector loci in natural populations of the plant pathogen Melampsora lini. Molecular Biology and Evolution 26, 2499–2513.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Baudouin E,
Pieuchot L,
Engler G,
Pauly N, Puppo A
(2006) Nitric oxide is formed in Medicago truncatula–Sinorhizobium meliloti functional nodules. Molecular Plant–Microbe Interactions 19, 970–975.
| Crossref | GoogleScholarGoogle Scholar |
Bednarek P, Osbourn A
(2009) Plant–microbe interactions: chemical diversity in plant defense. Science 324, 746–748.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bent AF, Mackey D
(2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annual Review of Phytopathology 45, 399–436.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Birch PRJ,
Boevink PC,
Gilroy EM,
Hein I,
Pritchard L, Whisson SC
(2008) Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Current Opinion in Plant Biology 11, 373–379.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Boland G
(1992) Hypovirulence and double-stranded RNA in Sclerotinia sclerotiorum. Canadian Journal of Plant Pathology 14, 10–17.
Boller T, He SY
(2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324, 742–744.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bonfante P, Genre A
(2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends in Plant Science 13, 492–498.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brasier CM,
Kirk SA,
Delcan J,
Cooke DEL,
Jung T, Man In’t Veld WA
(2004)
Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycological Research 108, 1172–1184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brooks DM,
Bender CL, Kunkel BN
(2005) The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Molecular Plant Pathology 6, 629–639.
| Crossref | GoogleScholarGoogle Scholar |
Brown JKM
(1995) Recombination and selection in populations of plant pathogens. Plant Pathology 44, 279–293.
| Crossref | GoogleScholarGoogle Scholar |
Burdon JJ, Roelfs AP
(1985) Isozyme and virulence variation in asexually reproducing populations of Puccinia graminis and P. recondita on wheat. Phytopathology 75, 907–913.
| Crossref | GoogleScholarGoogle Scholar |
Burdon JJ,
Marshall DR,
Luig NH, Gow DJS
(1982) Isozyme studies on the origin and evolution of Puccinia graminis f. sp. tritici in Australia. Australian Journal of Biological Sciences 35, 231–238.
Cárdenas L,
Martínez A,
Sánchez F, Quinto C
(2008) Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). The Plant Journal 56, 802–813.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chang JH,
Urbach JM,
Law TF,
Arnold LW,
Hu A,
Gombar S,
Grant SR,
Ausubel FM, Dangl JL
(2005) A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proceedings of the National Academy of Sciences of the United States of America 102, 2549–2554.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chen MS
(2008) Inducible direct plant defense against insect herbivores: a review. Insect Science 15, 101–114.
| Crossref | GoogleScholarGoogle Scholar |
Chen Z,
Agnew JL,
Cohen JD,
He P,
Shan L,
Sheen J, Kunkel BN
(2007)
Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proceedings of the National Academy of Sciences of the United States of America 104, 20 131–20 136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chinchilla D,
Bauer Z,
Regenass M,
Boller T, Felix G
(2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. The Plant Cell 18, 465–476.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chisholm ST,
Coaker G,
Day B, Staskawicz BJ
(2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Clarke SF,
McKenzie MJ,
Burritt DJ,
Guy PL, Jameson PE
(1999) Influence of white clover mosaic potexvirus infection on the endogenous cytokinin content of bean. Plant Physiology 120, 547–552.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dangl JL, Jones JDG
(2001) Plant pathogens and integrated defence responses to infection. Nature 411, 826–833.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
de Torres M,
Mansfield JW,
Grabov N,
Brown IR,
Ammouneh H,
Tsiamis G,
Forsyth A,
Robatzek S,
Grant M, Boch J
(2006)
Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. The Plant Journal 47, 368–382.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
de Wit PJGM
(2007) How plants recognize pathogens and defend themselves. Cellular and Molecular Life Sciences 64, 2726–2732.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Deakin WJ, Broughton WJ
(2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nature Reviews Microbiology 7, 312–320.
| PubMed |
Dinan L
(2001) Phytoecdysteroids: biological aspects. Phytochemistry 57, 325–339.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ding Y, Oldroyd GE
(2009) Positioning the nodule, the hormone dictum. Plant Signaling & Behavior 4, 89–93.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dodds PN, Thrall P
(2009) Recognition events and host-pathogen co-evolution in gene-for-gene resistance to flax rust. Functional Plant Biology 36, 395–408.
| Crossref | GoogleScholarGoogle Scholar |
Dodds PN,
Lawrence GJ,
Catanzariti AM,
Teh T,
Wang CIA,
Ayliffe MA,
Kobe B, Ellis JG
(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 of the United States of America 103, 8888–8893.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dou DL,
Kale SD,
Wang X,
Jiang RHY,
Bruce NA,
Arredondo FD,
Zhang XM, Tyler BM
(2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. The Plant Cell 20, 1930–1947.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Edwards O, Singh KB
(2006) Resistance to insect pests: what do legumes have to offer? Euphytica 147, 273–285.
| Crossref | GoogleScholarGoogle Scholar |
Ellis JG,
Dodds PN, Lawrence GJ
(2007) Flax rust resistance gene specificity is based on direct resistance–avirulence protein interactions. Annual Review of Phytopathology 45, 289–306.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Enjalbert J,
Duan M,
Leconte M,
Hovmøller MS, de Vallavieille-Pope C
(2005) Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France. Molecular Ecology 14, 2065–2073.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Felle HH,
Kondorosi E,
Kondorosi A, Schultze M
(2000) How alfalfa root hairs discriminate between Nod factors and oligochitin elicitors. Plant Physiology 124, 1373–1380.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fraser RSS, Whenham RJ
(1982) Plant-growth regulators and virus-infection – a critical review. Plant Growth Regulation 1, 37–59.
| Crossref | GoogleScholarGoogle Scholar |
Friesen T,
Stukenbrock EH,
Lui Z,
Meinhardt S,
Ling H,
Faris JD,
Rasmussen JB,
Solomon PS,
McDonald BA, Oliver RP
(2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics 38, 953–956.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Friesen TL,
Faris JD,
Solomon PS, Oliver RP
(2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cellular Microbiology 10, 1421–1428.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Friesen TL,
Chu CG,
Liu ZH,
Xu SS,
Halley S, Faris JD
(2009) Host-selective toxins produced by Stagonospora nodorum confer disease susceptibility in adult wheat plants under field conditions. Theoretical and Applied Genetics 118, 1489–1497.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Frugier F,
Kosuta S,
Murray JD,
Crespi M, Szczyglowski K
(2008) Cytokinin: secret agent of symbiosis. Trends in Plant Science 13, 115–120.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Genre A,
Chabaud M,
Timmers T,
Bonfante P, Barker DG
(2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. The Plant Cell 17, 3489–3499.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Genre A,
Ortu G,
Bertoldo C,
Martino E, Bonfante P
(2009) Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi. Plant Physiology 149, 1424–1434.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gimenez-Ibanez S,
Hann DR,
Ntoukakls V,
Petutschnig E,
Lipka V, Rathjen JP
(2009) AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Current Biology 19, 423–429.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Glazebrook J
(2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205–227.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gomez-Gomez L, 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Govrin EM, Levine A
(2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10, 751–757.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grunewald W,
van Noorden G,
Van Isterdael G,
Beeckman T,
Gheysen G, Mathesius U
(2009) Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. The Plant Cell 21, 2553–2562.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gudesblat GE,
Torres PS, Vojnov AA
(2009)
Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiology 149, 1017–1027.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Haque S,
Park RF,
Keiper FJ,
Bariana HS, Wellings CR
(2008) Pathogenic and molecular variation support the presence of genetically distinct clonal lineages in Australian populations of Puccinia graminis f. sp. avenae. Mycological Research 112, 663–673.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hardham AR,
Jones DA, Takemoto D
(2007) Cytoskeleton and cell wall function in penetration resistance. Current Opinion in Plant Biology 10, 342–348.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
He P,
Shan L,
Lin NC,
Martin GB,
Kemmerling B,
Nurnberger T, Sheen J
(2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125, 563–575.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heese A,
Hann DR,
Gimenez-Ibanez S,
Jones AME,
He K,
Li J,
Schroeder JI,
Peck SC, Rathjen JP
(2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proceedings of the National Academy of Sciences of the United States of America 104, 12 217–12 222.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heil M
(2008) Indirect defence via tritrophic interactions. New Phytologist 178, 41–61.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hovmøller MS,
Justesen AF, Brown JKM
(2002) Clonality and long-distance migration of Puccinia striiformis f. sp. tritici in north-west Europe. Plant Pathology 51, 24–32.
| Crossref | GoogleScholarGoogle Scholar |
Howe GA, Jander G
(2008) Plant immunity to insect herbivores. Annual Review of Plant Biology 59, 41–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jameson PE
(2000) Cytokinins and auxins in plant–pathogen interactions – an overview. Plant Growth Regulation 32, 369–380.
| Crossref | GoogleScholarGoogle Scholar |
Janjusevic R,
Abramovitch RB,
Martin GB, Stebbins CE
(2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311, 222–226.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jones JDG, Dangl JL
(2006) The plant immune system. Nature 444, 323–329.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kambara K,
Ardissone S,
Kobayashi H,
Saad MM,
Schumpp O,
Broughton WJ, Deakin WJ
(2009) Rhizobia utilize pathogen-like effector proteins during symbiosis. Molecular Microbiology 71, 92–106.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim MG,
da Cunha L,
McFall AJ,
Belkhadir Y,
DebRoy S,
Dangl JL, Mackey D
(2005) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121, 749–759.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kobayashi Y,
Kobayashi I,
Funaki Y,
Fujimoto S,
Takemoto T, Kunoh H
(1997) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. The Plant Journal 11, 525–537.
| Crossref | GoogleScholarGoogle Scholar |
Krings M,
Taylor TN,
Hass H,
Kerp H,
Dotzler N, Hermsen EJ
(2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytologist 174, 648–657.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kumar M,
Busch W,
Birke H,
Kemmerling B,
Nurnberger T, Schoffl F
(2009) Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Molecular Plant 2, 152–165.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kunkeaw S,
Tan S, Coaker G
(2010) Molecular and evolutionary analyses of Pseudomonas syringae pv. tomato race 1. Molecular Plant–Microbe Interactions 23, 415–424.
| Crossref | GoogleScholarGoogle Scholar |
Kunze G,
Zipfel C,
Robatzek S,
Niehaus K,
Boller T, Felix G
(2004) The N-terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. The Plant Cell 16, 3496–3507.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lawrence GJ,
Boelen MG, Pryor A
(1988) Transmission of double-stranded RNAs in flax rust, Melampsora lini. Canadian Journal of Botany 66, 61–66.
Lee J,
Klessig DF, Nurnberger T
(2001) A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity. The Plant Cell 13, 1079–1093.
| Crossref |
PubMed |
Liu ZH,
Friesen TL,
Ling H,
Meinhardt SW,
Oliver RP,
Rasmussen JB, Faris JD
(2006) The Tsn1-ToxA interaction in the wheat–Stagonospora nodorum pathosystem parallels that of the wheat–tan spot system. Genome 49, 1265–1273.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu J,
Elmore JM,
Fuglsang AT,
Palmgren MG,
Staskawicz BJ, Coaker G
(2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. Plos Biology 7, e1000139.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
López MA,
Bannenberg G, Castresana C
(2008) Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Current Opinion in Plant Biology 11, 420–427.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lorang JM,
Sweat TA, Wolpert TJ
(2007) Plant disease susceptibility conferred by a “resistance” gene. Proceedings of the National Academy of Sciences of the United States of America 104, 14 861–14 866.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lovell HC,
Mansfield JW,
Godfrey SAC,
Jackson RW,
Hancock JT, Arnold DL
(2009) Bacterial evolution by genomic island transfer occurs via DNA transformation in planta. Current Biology 19, 1586–1590.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ma WB,
Dong FFT,
Stavrinides J, Guttman DS
(2006) Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLOS Genetics 2, 2131–2142.
| Crossref | GoogleScholarGoogle Scholar |
Ma L-J,
van der Does HC,
Borkovich KA,
Coleman JJ, Daboussi M-J ,
et al
.
(2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium oxysporum. Nature 464, 367–373.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mackey D,
Holt BF,
Wiig A, Dangl JL
(2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mackey D,
Belkhadir Y,
Alonso JM,
Ecker JR, Dangl JL
(2003)
Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Madsen EB,
Madsen LH,
Madsen EB,
Madsen LH, Radutoiu S ,
et al
.
(2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637–640.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Markmann K, Parniske M
(2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends in Plant Science 14, 77–86.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Martin GB,
Bogdanove AJ, Sessa G
(2003) Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology 54, 23–61.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McDonald BA, Linde C
(2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology 40, 349–379.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Melotto M,
Underwood W,
Koczan J,
Nomura K, He SY
(2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126, 969–980.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Melotto M,
Underwood W, He SY
(2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annual Review of Phytopathology 46, 101–122.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Morrissey JP, Osbourn AE
(1999) Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiology and Molecular Biology Reviews 63, 708–724.
| PubMed |
Naum M,
Brown EW, Mason-Gamer RJ
(2009) Phylogenetic evidence for extensive horizontal gene transfer of type III secretion system genes among enterobacterial plant pathogens. Microbiology 155, 3187–3199.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nurnberger T,
Brunner F,
Kemmerling B, Piater L
(2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunological Reviews 198, 249–266.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ochman H, Moran NA
(2001) Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292, 1096–1099.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Oldroyd GE,
Harrison MJ, Paszkowski U
(2009) Reprogramming plant cells for endosymbiosis. Science 324, 753–754.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Oliver RP, Solomon PS
(2008) Recent fungal diseases of crop plants: is lateral gene transfer a common theme? Molecular Plant–Microbe Interactions 21, 287–293.
| Crossref | GoogleScholarGoogle Scholar |
Oliver RP,
Rybak K,
Shankar M,
Loughman R,
Harry N, Solomon PS
(2008) Quantitative disease resistance assessment by real-time PCR using the Stagonospora nodorum–wheat pathosystem as a model. Plant Pathology 57, 527–532.
| Crossref | GoogleScholarGoogle Scholar |
Papadopoulou K,
Melton RE,
Leggett M,
Daniels MJ, Osbourn AE
(1999) Compromised disease resistance in saponin-deficient plants. Proceedings of the National Academy of Sciences of the United States of America 96, 12 923–12 928.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Parniske M
(2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6, 763–775.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peleg-Grossman S,
Volpin H, Levine A
(2007) Root hair curling and rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. Journal of Experimental Botany 58, 1637–1649.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Penmetsa RV,
Uribe P,
Anderson JP,
Gish JC, Nam YW ,
et al
.
(2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. The Plant Journal 55, 580–595.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pii Y,
Crimi M,
Cremonese G,
Spena A, Pandolfini T
(2007) Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biology 7, 21.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Plummer KM, Howlett BJ
(1995) Inheritance of chromosomal length polymorphisms in the ascomycete Leptosphaeria maculans. Molecular & General Genetics 247, 416–422.
| Crossref | GoogleScholarGoogle Scholar |
Radutoiu S,
Madsen LH,
Madsen EB,
Felle HH, Umehara Y ,
et al
.
(2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ramu SK,
Peng H-M, Cook DR
(2002) Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Molecular Plant–Microbe Interactions 15, 522–528.
| Crossref | GoogleScholarGoogle Scholar |
Rehmany AP,
Gordon A,
Allen RL,
Armstrong MR,
Whisson SC,
Kamoun S,
Tyler BM,
Birch PRJ, Beynon JL
(2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. The Plant Cell 17, 1839–1850.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Remy W,
Taylor TN,
Hass H, Kerp H
(1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proceedings of the National Academy of Sciences of the United States of America 91, 11 841–11 843.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Robert-Seilaniantz A,
Navarro L,
Bari R, Jones JD
(2007) Pathological hormone imbalances. Current Opinion in Plant Biology 10, 372–379.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rosenblueth M, Martinez-Romero E
(2006) Bacterial endophytes and their interactions with hosts. Molecular Plant–Microbe Interactions 19, 827–837.
| Crossref | GoogleScholarGoogle Scholar |
Sato M,
Mitra RM,
Coller J,
Wang D,
Spivey NW,
Dewdney J,
Denoux C,
Glazebrook J, Katagiri F
(2007) A high-performance, small-scale microarray for expression profiling of many samples in Arabidopsis–pathogen studies. The Plant Journal 49, 565–577.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schardl CL,
Leuchtmann A, Spiering MJ
(2004) Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55, 315–340.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schulz B, Boyle C
(2005) The endophytic continuum. Mycological Research 109, 661–686.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schwessinger B, Zipfel C
(2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Current Opinion in Plant Biology 11, 389–395.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shan LB,
He P, Sheen J
(2007) Endless hide-and-seek: dynamic co-evolution in plant–bacterium warfare. Journal of Integrative Plant Biology 49, 105–111.
| Crossref | GoogleScholarGoogle Scholar |
Shan L,
He P,
Li J,
Heese A,
Peck SC,
Nurnberger T,
Martin GB, Sheen J
(2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host & Microbe 4, 17–27.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Soltis DE,
Soltis PS,
Morgan DR,
Swensen SM,
Mullin BC,
Dowd JM, Martin PG
(1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences of the United States of America 92, 2647–2651.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Soriano IR,
Riley IT,
Potter MJ, Bowers WS
(2004) Phytoecdysteroids: a novel defense against plant-parasitic nematodes. Journal of Chemical Ecology 30, 1885–1899.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Soto MJ,
Sanjuan J, Olivares J
(2006) Rhizobia and plant–pathogenic bacteria: common infection weapons. Microbiology 152, 3167–3174.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Soto MJ,
Dominguez-Ferreras A,
Perez-Mendoza D,
Sanjuan J, Olivares J
(2009) Mutualism versus pathogenesis: the give-and-take in plant–bacteria interactions. Cellular Microbiology 11, 381–388.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Spaepen S,
Vanderleyden J, Remans R
(2007) Indole-3-acetic acid in microbial and microorganism–plant signaling. FEMS Microbiology Reviews 31, 425–448.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Spiers AG, Hopcroft DH
(1994) Comparative studies of the poplar rusts Melampsora medusae, M. larici-populina and their interspecific hybrid M. medusae-populina. Mycological Research 98, 889–903.
| Crossref | GoogleScholarGoogle Scholar |
Sprent JI
(2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174, 11–25.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sprent JI, James EK
(2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiology 144, 575–581.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Staskawicz BJ,
Mudgett MB,
Dangl JL, Galan JE
(2001) Common and contrasting themes of plant and animal diseases. Science 292, 2285–2289.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stukenbrock EH, McDonald BA
(2009) Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Molecular Plant–Microbe Interactions 22, 371–380.
| Crossref | GoogleScholarGoogle Scholar |
Takai R,
Isogai A,
Takayama S, Che FS
(2008) Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Molecular Plant–Microbe Interactions 21, 1635–1642.
| Crossref | GoogleScholarGoogle Scholar |
Thatcher LF,
Anderson JP, Singh KB
(2005) Plant defence responses: what have we learnt from Arabidopsis? Functional Plant Biology 32, 1–19.
| Crossref | GoogleScholarGoogle Scholar |
Thomma B,
Penninckx I,
Broekaert WF, Cammue BPA
(2001) The complexity of disease signaling in Arabidopsis. Current Opinion in Immunology 13, 63–68.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thomma B,
Cammue BPA, Thevissen K
(2002) Plant defensins. Planta 216, 193–202.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thordal-Christensen H
(2003) Fresh insights into processes of nonhost resistance. Current Opinion in Plant Biology 6, 351–357.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thrall PH,
Bever JD,
Mihail J, Alexander HM
(1997) The population dynamics of annual plants and soil-borne pathogens. Journal of Ecology 85, 313–328.
| Crossref | GoogleScholarGoogle Scholar |
Tsuda K,
Sato M,
Glazebrook J,
Cohen JD, Katagiri F
(2008) Interplay between MAMP-triggered and SA-mediated defense responses. The Plant Journal 53, 763–775.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Van Alfen NK,
Janes RA,
Anagnostakis SL, Day PR
(1975) Chestnut blight: biological control by transmissible hypovirulence in Endothia parasitica. Science 189, 890–891.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
van den Burg HA,
Westerink N,
Francoijs KJ,
Roth R,
Woestenenk E,
Boeren S,
de Wit PJGM,
Joosten MHAJ, Vervoort J
(2003) Natural disulfide bond-disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability. The Journal of Biological Chemistry 278, 27 340–27 346.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
van Esse HP,
Bolton MD,
Stergiopoulos L,
de Wit P, Thomma B
(2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Molecular Plant–Microbe Interactions 20, 1092–1101.
| Crossref | GoogleScholarGoogle Scholar |
VanEtten H,
Funnell-Baerg D,
Wasmann C, McCluskey K
(1994) Location of pathogenicity genes on dispensible chromosomes in Nectria haematococca MPVI. Antonie Van Leeuwenhoek 65, 263–267.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vasse J,
Billy F, Truchet G
(1993) Abortion of infection during the Rhizobium meliloti–alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. The Plant Journal 4, 555–566.
| Crossref | GoogleScholarGoogle Scholar |
Wan J,
Zhang XC,
Neece D,
Ramonell KM,
Clough S,
Kim SY,
Stacey MG, Stacey G
(2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. The Plant Cell 20, 471–481.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wellings CR, McIntosh RA
(1990)
Puccinia striiformis f. sp. tritici in Australia – pathogenic changes during the first ten years. Plant Pathology 39, 316–325.
| Crossref | GoogleScholarGoogle Scholar |
Wilson DJ,
Gabriel E,
Leatherbarrow AJ,
Cheesbrough J,
Gee S,
Bolton E,
Fox A,
Hart CA,
Diggle PJ, Fearnhead P
(2009) Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Molecular Biology and Evolution 26, 385–397.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zambryski PC
(1992) chronicles from the agrobacterium-plant cell-DNA transfer story. Annual Review of Plant Physiology and Plant Molecular Biology 43, 465–490.
| Crossref | GoogleScholarGoogle Scholar |
Zarate SI,
Kempema LA, Walling LL
(2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiology 143, 866–875.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhang X,
Dai Y,
Xiong Y,
DeFraia C,
Li J,
Dong X, Mou Z
(2007) Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. The Plant Journal 52, 1066–1079.
| Crossref |
PubMed |
Zhang W,
He SY, Assmann SM
(2008) The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation. The Plant Journal 56, 984–996.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhao YF,
Thilmony R,
Bender CL,
Schaller A,
He SY, Howe GA
(2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. The Plant Journal 36, 485–499.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zipfel C,
Kunze G,
Chinchilla D,
Caniard A,
Jones JDG,
Boller T, Felix G
(2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749–760.
| Crossref | GoogleScholarGoogle Scholar | PubMed |