Goldacre paper: Recognition events and host–pathogen co-evolution in gene-for-gene resistance to flax rust

Peter Dodds; Peter Thrall

doi:10.1071/FP08320

EVOLUTIONARY REVIEW

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Goldacre paper: Recognition events and host–pathogen co-evolution in gene-for-gene resistance to flax rust

Peter Dodds ^A ^B and Peter Thrall ^A

+ Author Affiliations

- Author Affiliations

^A CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.

^B Corresponding author. Email: peter.dodds@csiro.au

^C This paper originates from the Peter Goldacre Award 2006 of the Australian Society of Plant Scientists, received by the author.

Functional Plant Biology 36(5) 395-408 https://doi.org/10.1071/FP08320
Submitted: 16 December 2008 Accepted: 12 March 2009 Published: 6 May 2009

Abstract

The outcome of infection of individual plants by pathogenic organisms is governed by complex interactions between the host and pathogen. These interactions are the result of long-term co-evolutionary processes involving selection and counterselection between plants and their pathogens. These processes are ongoing, and occur at many spatio-temporal scales, including genes and gene products, cellular interactions within host individuals, and the dynamics of host and pathogen populations. However, there are few systems in which host–pathogen interactions have been studied across these broad scales. In this review, we focus on research to elucidate the structure and function of plant resistance and pathogen virulence genes in the flax-flax rust interaction, and also highlight complementary co-evolutionary studies of a related wild plant–pathogen interaction. The confluence of these approaches is beginning to shed new light on host–pathogen molecular co-evolution in natural environments.

Additional keywords: avirulence, innate immunity, NB-LRR.

References

Akira S (2003) Mammalian Toll-like receptors. Current Opinion in Immunology 15, 5–11.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, Rose LE, Beynon JL (2004) Host-parasite co-evolutionary conflict between Arabidopsis and downy mildew. Science 306, 1957–1960.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ, Ellis JG (1997) Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. The Plant Cell 9, 641–651.
| CAS | Crossref | PubMed |

Armstrong MR, Whisson SC, Pritchard L, Bos JI, Venter E , et al. (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proceedings of the National Academy of Sciences of the United States of America 102, 7766–7771.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified resistance in Arabidopsis is coupled to AvrRpt2-directed elimination of RIN4. Cell 112, 369–377.
| Crossref | GoogleScholarGoogle Scholar | CAS | 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 | CAS | PubMed |

Barrett LG, Thrall PH, Burdon JJ, Linde C (2008a) Pathogen life-history and the evolutionary potential of populations. Trends in Ecology & Evolution 23, 678–685.
| Crossref | GoogleScholarGoogle Scholar |

Barrett LG, Thrall PH, Burdon JJ, Nicotra AB, Linde CC (2008b) Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Molecular Ecology 17, 3401–3415.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292, 2281–2285.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Bhattacharjee S, Hiller NL, Liolio K, Win J, Kanneganti T-D, Young C, Kamoun S, Haldar K (2006) The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathogens 2, e50.
| 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 | CAS | PubMed |

Burdon JJ (1994) The distribution and origin of genes for race specific resistance to Melampsora lini in Linum marginale. Evolution 48, 1564–1575.
| Crossref |

Burdon JJ (1997) The evolution of gene-for-gene interactions in natural pathosystems. In ‘The gene-for-gene relationship in plant–parasite interactions’. (Eds IR Crute, EB Holub, JJ Burdon) pp. 245–262. (CAB International: Wallingford, UK)

Burdon JJ, Jarosz AM (1991) Host–pathogen interactions in natural populations of Linum marginale and Melampsora lini: I. Patterns of resistance and racial variation in a large host population. Evolution 45, 205–217.
| Crossref | GoogleScholarGoogle Scholar |

Burdon JJ, Roberts JK (1995) The population genetic structure of the rust fungus Melampsora lini as revealed by pathogenicity, isozyme and RFLP markers. Plant Pathology 44, 270–278.
| Crossref | GoogleScholarGoogle Scholar |

Burdon JJ, Thompson JN (1995) Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini. Journal of Ecology 83, 199–206.
| Crossref | GoogleScholarGoogle Scholar |

Burdon JJ, Thrall PH (2000) Co-evolution at multiple spatial scales: Linum marginale-Melampsora lini from the individual to the species. Evolutionary Ecology 14, 261–281.
| Crossref | GoogleScholarGoogle Scholar |

Burdon JJ, Thrall PH, Brown AHD (1999) Resistance and virulence structure in two Linum marginale – Melampsora lini host–pathogen metapopulations with different mating systems. Evolution 53, 704–716.
| Crossref | GoogleScholarGoogle Scholar |

Burdon JJ, Thrall PH, Lawrence GJ (2002) Co-evolutionary patterns in the Linum marginale–Melampsora lini association at a continental scale. Canadian Journal of Botany 80, 288–296.
| Crossref | GoogleScholarGoogle Scholar |

Büttner D, Bonas U (2003) Common strategies of plant and animal pathogenic bacteria. Current Opinion in Plant Biology 6, 312–319.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Catanzariti A-M, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. The Plant Cell 18, 243–256.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Catanzariti A-M, Dodds PN, Ellis JG (2007) Avirulence proteins from haustoria-forming pathogens. FEMS Microbiology Letters 269, 181–188.
| Crossref | GoogleScholarGoogle Scholar | CAS | 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 | CAS | PubMed |

Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411, 826–833.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y (2003) Physical interaction between RRS1-R-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proceedings of the National Academy of Sciences of the United States of America 100, 8024–8029.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Dodds PN , Lawrence GJ , Pryor AJ , Ellis JG (2000) Genetic analysis and evolution of plant disease resistance genes. In ‘Molecular plant pathology’. (Eds M Dickinson, J Beynon) pp. 88–107. (Sheffield Academic Press: Sheffield, UK)

Dodds PN, Lawrence GJ, Ellis JG (2001a) Contrasting modes of evolution acting on the complex N locus for rust resistance in flax. The Plant Journal 27, 439–453.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Dodds PN, Lawrence GJ, Pryor AJ, Ellis JG (2001b) Six amino acid changes confined to the leucine-rich repeat β-strand/β-turn motif determine the difference between the P and P2 rust resistance specificities in flax. The Plant Cell 13, 163–178.
| CAS | Crossref | PubMed |

Dodds PN, Lawrence GJ, Catanzariti A-M, Ayliffe MA, Ellis JG (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. The Plant Cell 16, 755–768.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Wang CA, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and co-evolution 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 | CAS | PubMed |

Panstruga R, Dodds PN (2009) Terrific protein traffic: the mystery of how filamentous pathogens deliver effectors into host plant cells. Science in press. ,
| PubMed |

Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, Arredondo FD, Zhang X, 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 | CAS | PubMed |

Ellis JG, Dodds PN (2003) Plant disease resistance: monitoring a pathogen targeted host protein. Current Biology 13, R400–R402.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. The Plant Cell 11, 495–506.
| CAS | Crossref | PubMed |

Ellis JG, Dodds PN, Lawrence GJ (2007) The role of secreted proteins in diseases of plants caused by rusts, powdery mildew and smut fungi. Current Opinion in Microbiology 10, 326–331.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Endo T, Ikeo K, Gojobori T (1996) Large scale search for genes on which positive selection may operate. Molecular Biology and Evolution 13, 685–690.
| CAS | PubMed |

Flor HH (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology 9, 275–296.
| Crossref | GoogleScholarGoogle Scholar |

Girardin SE, Travassos LH, Nerve M, Blanot D, Boneca IG, Philpott DJ, Sansonetti PJ, Mengin-Lecreulx D (2003) Peptidoglycan molecular requirements allowing detection by Nod 1 and Nod 2. Journal of Biological Chemistry 278, 41702–41708.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Hahn M, Mendgen K (1992) Isolation by ConA binding of haustoria from different rust fungi and comparison of their surface qualities. Protoplasma 170, 95–103.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Hahn M, Mendgen K (2001) Signal and nutrient exchange at biotrophic plant–fungus interfaces. Current Opinion in Plant Biology 4, 322–327.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Heath MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Annals of Botany 80, 713–720.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estraño C, Haldar K (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306, 1934–1937.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167–170.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Hwang C-F, Williamson VM (2003) Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signalling by the tomato resistance protein Mi. The Plant Journal 34, 585–593.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Jarosz AM, Burdon JJ (1991) Host–pathogen interactions in natural populations of Linum marginale and Melampsora lini: II Local and regional variation in patterns of resistance and racial structure. Evolution 45, 1618–1627.
| Crossref | GoogleScholarGoogle Scholar |

Jarosz AM, Burdon JJ (1992) Host–pathogen interactions in natural populations of Linum marginale and Melampsora lini: III Influence of pathogen epidemics on host survivorship and flower production. Oecologia 89, 53–61.
| Crossref | GoogleScholarGoogle Scholar |

Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO Journal 19, 4004–4014.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Jones JDG, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology 44, 41–60.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Kemen E, Kemen AC, Rafiqi M, Hempel U, Mendgen K, Hahn M, Voegele RT (2005) Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Molecular Plant–Microbe Interactions 18, 1130–1139.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Kobayashi I, Kobayashi Y, Hardham AR (1994) Dynamic reorganisation of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195, 237–247.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Kobayashi I, Murdoch LJ, Kunoh H, Hardham AR (1995) Cell biology of early events in the resistance response to infection by pathogenic fungi. Canadian Journal of Botany 73, 418–425.
| Crossref | GoogleScholarGoogle Scholar |

Kobayashi I, Kobayashi Y, Hardham AR (1997) Inhibition of rust-induced hypersensitive response in flax cells by the microtubule inhibitor oryzalin. Australian Journal of Plant Physiology 24, 733–740.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Lawrence GJ, Burdon JJ (1989) Flax rust from L. marginale: variation in a natural host–pathogen interaction. Canadian Journal of Botany 66, 3192–3198.

Lawrence GJ, Shepherd KW, Mayo GME (1981) Fine structure of genes controlling pathogenicity in flax rust, Melampsora lini. Heredity 46, 297–313.
| Crossref | GoogleScholarGoogle Scholar |

Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. The Plant Cell 7, 1195–1206.
| CAS | Crossref | PubMed |

Lawrence GJ, Dodds PN, Ellis JG (2007) Rust of flax and linseed caused by Melampsora lini. Molecular Plant Pathology 8, 349–364.
| Crossref | GoogleScholarGoogle Scholar |

Lawrence GJ, Anderson PA, Dodds PN, Ellis JG (2009) Relationships between rust resistance genes at the M locus in flax. Molecular Plant Pathology , in press.

Luck JE, Lawrence GJ, Dodds PN, Shepherd KW, Ellis JG (2000) Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. The Plant Cell 12, 1367–1378.
| CAS | Crossref | PubMed |

Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III efector molecules and is required for RPM1-mediated resistance in Arabidopisis. Cell 108, 743–754.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Marti M, Good RT, Rug M, Knuepfer E, Cowman AF (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306, 1930–1933.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Mauricio R, Stahl EA, Korves T, Tian D, Kreitman M, Bergelson J (2003) Natural selection for polymorphism in the disease resistance gene RPS2 of Arabidopsis thaliana. Genetics 163, 735–746.
| CAS | PubMed |

Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Research 8, 1113–1130.
| CAS | PubMed |

Moffett P, Farnham G, Peart J, Baulcombe DC (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO Journal 21, 4511–4519.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Mondragon-Palomino M, Meyers B, Michelmore RW, Gaut BS (2002) Patterns of positive selection in the coplete NBS-LRR family of Arabidopsis thaliana. Genome Research 12, 1305–1315.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Murdoch LJ, Hardham AR (1998) Components in the haustorial wall of the flax rust fungus, Melampsora lini, are labelled by three anti-calmodulin monoclonal antibodies. Protoplasma 201, 180–193.
| Crossref | GoogleScholarGoogle Scholar |

Murdoch LJ, Kobayashi I, Hardham AR (1998) Production and characterisation of monoclonal antibodies to cell wall components of the flax rust fungus. European Journal of Plant Pathology 104, 331–346.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proceedings of the National Academy of Sciences of the United States of America 94, 7799–7806.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Nurnberger T, Brunner F, Kemmerking B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunological Reviews 198, 249–266.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz BJ, Dixon JE (2000) Disruption of signalling by Yersinia effector YopJ, A ubiquitin-like protein protease. Science 290, 1594–1597.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Current Opinion in Plant Biology 6, 320–326.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BBH, Jones JDG (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated gene at the Cf-4/9 locus of tomato. Cell 91, 821–832.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Perfect SE, Green JR (2001) Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Molecular Plant Pathology 2, 101–108.
| Crossref | GoogleScholarGoogle Scholar |

Rehmany AP, Gordon A, Rose LE, 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 | CAS | PubMed |

Shan W, Cao M, Leung D, Tyler BM (2004) The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Molecular Plant-Microbe Interactions 17, 394–403.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301, 1230–1233.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400, 667–671.
| Crossref | GoogleScholarGoogle Scholar | CAS | 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 | CAS | PubMed |

Thompson JN (1994) ‘The co-evolutionary process.’ (University of Chicago Press: Chicago, IL)

Thompson JN (1999) Specific hypotheses on the geographic mosaic of co-evolution. American Naturalist 153, S1–S14.
| Crossref | GoogleScholarGoogle Scholar |

Thrall PH, Burdon JJ (2000) Effects of resistance variation in a natural plant host–pathogen metapopulation on disease dynamics. Plant Pathology 49, 767–773.
| Crossref | GoogleScholarGoogle Scholar |

Thrall PH, Burdon JJ (2003) Evolution of virulence in a plant host–pathogen metapopulation. Science 299, 1735–1737.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Thrall PH, Burdon JJ, Young AG (2001) Variation in resistance and virulence among demes of a plant host–pathogen metapopulation. Journal of Ecology 89, 736–748.

Thrall PH, Burdon JJ, Bever JD (2002) Local adaptation in the Linum marginale–Melampsora lini host–pathogen interaction. Evolution 56, 1340–1351.
| PubMed |

Tyler BM (2009) Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cellular Microbiology 11, 13–20.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Ueda H, Yamaguchi Y, Sano H (2006) Direct Interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Molecular Biology 61, 31–45.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

van der Hoorn RAL, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. The Plant Cell 20, 2009–2017.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

van der Hoorn RAL, de Wit PJGM, Joosten MHAJ (2002) Balancing selection favors guarding resistance proteins. Trends in Plant Science 7, 67–71.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytologist 159, 93–100.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Wang C-IA, Gunčar G, Forwood JK, Teh T, Catanzariti A-M , et al. (2007) Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. The Plant Cell 19, 2898–2912.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG , et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450, 115–118.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

White SN, Taylor KH, Abbey CA, Gill CA, Womack JE (2003) Haplotype variation in bovine Toll-line receptor 4 and computational prediction of a positively selected ligand-binding domain. Proceedings of the National Academy of Sciences of the United States of America 100, 10364–10369.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |