Effectors of biotrophic fungal plant pathogens
Pamela H. P. Gan A , Maryam Rafiqi A , Adrienne R. Hardham A and Peter N. Dodds B CA Plant Science Division, Research School of Biology, College of Medicine, Biology and Environment, Australian National University, Canberra, ACT 2601, Australia.
B CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.
C Corresponding author. Email: peter.dodds@csiro.au
Functional Plant Biology 37(10) 913-918 https://doi.org/10.1071/FP10072
Submitted: 31 March 2010 Accepted: 15 June 2010 Published: 23 September 2010
Abstract
Plant pathogenic biotrophic fungi are able to grow within living plant tissue due to the action of secreted pathogen proteins known as effectors that alter the response of plant cells to pathogens. The discovery and identification of these proteins has greatly expanded with the sequencing and annotation of fungal pathogen genomes. Studies to characterise effector function have revealed that a subset of these secreted pathogen proteins interact with plant proteins within the host cytoplasm. This review focuses on the effectors of intracellular biotrophic and hemibiotrophic fungal plant pathogens and summarises advances in understanding the roles of these proteins in disease and in elucidating the mechanism of fungal effector uptake into host cells.
Additional keywords: biotroph, fungi, hemibiotroph, translocation.
Acknowledgements
Research support from the Australian Research Council (ARH, PND) and an Australian Postgraduate Award (PHPG) is acknowledged.
Basse CW,
Stumpferl S, Kahmann R
(2000) Characterization of a Ustilago maydis gene specifically induced during the biotrophic phase: evidence for negative as well as positive regulation. Molecular and Cellular Biology 20, 329–339.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Basse CW,
Kolb S, Kahmann R
(2002) A maize-specifically expressed gene cluster in Ustilago maydis. Molecular Microbiology 43, 75–93.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Catanzariti A-M, Jones DA
(2010) Effector proteins of extracellular fungal plant pathogens that trigger host resistance. Functional Plant Biology 37, 901–906.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Catanzariti A-M,
Dodds PN,
Ve T,
Kobe B,
Ellis JG, Staskawicz BJ
(2010) The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Molecular Plant-Microbe Interactions 23, 49–57.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chugh A, Eudes F
(2008) Study of uptake of cell penetrating peptides and their cargoes in permeabilized wheat immature embryos. The FEBS Journal 275, 2403–2414.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Dean RA,
Talbot NJ,
Ebbole DJ,
Farman ML, Mitchell TK ,
et al
.
(2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434, 980–986.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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 C-IA,
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 |
CAS |
PubMed |
Doehlemann G,
van der Linde K,
Aßmann D,
Schwammbach D,
Hof A,
Mohanty A,
Jackson D, Kahmann R
(2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathogens 5, e1000290.
| Crossref | GoogleScholarGoogle Scholar | 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 |
Hahn M, Mendgen K
(1997) Characterization of in planta-induced rust genes isolated from a haustorium-specific cDNA library. Molecular Plant-Microbe Interactions 10, 427–437.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hardham AR, Cahill DM
(2010) The role of oomycete effectors in plant–pathogen interactions. Functional Plant Biology 37, 919–925.
| Crossref | GoogleScholarGoogle Scholar |
Hogenhout SA,
Van der Hoorn RAL,
Terauchi R, Kamoun S
(2009) Emerging concepts in effector biology of plant-associated organisms. Molecular Plant-Microbe Interactions 22, 115–122.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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 |
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 |
Kamoun S
(2007) Groovy times: filamentous pathogen effectors revealed. Current Opinion in Plant Biology 10, 358–365.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kämper J,
Kahmann R,
Bolker M,
Ma L-J, Brefort T ,
et al
.
(2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444, 97–101.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kang S,
Sweigard J, Valent B
(1995) The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Molecular Plant-Microbe Interactions 8, 939–948.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kankanala P,
Czymmek K, Valent B
(2007) Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. The Plant Cell 19, 706–724.
| 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 |
PubMed |
Khang CH,
Berruyer R,
Giraldo MC,
Kankanala P,
Park S-Y,
Czymmek K,
Kang S, Valent B
(2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22, 1388–1403.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lawrence GJ,
Dodds PN, Ellis JG
(2010) Transformation of the flax rust fungus, Melampsora lini: selection via silencing of an avirulence gene. The Plant Journal 61, 364–369.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Leborgne-Castel N,
Lherminier J,
Der C,
Fromentin J,
Houot V, Simon-Plas F
(2008) The plant defense elicitor cryptogein stimulates clathrin-mediated endocytosis correlated with reactive oxygen species production in Bright Yellow-2 tobacco cells. Plant Physiology 146, 1255–1266.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Mäe M,
Myrberg H,
Jiang Y,
Paves H,
Valkna A, Langel U
(2005) Internalisation of cell-penetrating peptides into tobacco protoplasts. Biochimica et Biophysica Acta 1669, 101–107.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mendgen K, Hahn M
(2002) Plant infection and the establishment of fungal biotrophy. Trends in Plant Science 7, 352–356.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Mosquera G,
Giraldo MC,
Khang CH,
Coughlan S, Valent B
(2009) Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1–4 as biotrophy-associated secreted proteins in rice blast disease. The Plant Cell 21, 1273–1290.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Mueller O,
Kahmann R,
Aguilar G,
Trejo-Aguilar B,
Wu A, de Vries RP
(2008) The secretome of the maize pathogen Ustilago maydis. Fungal Genetics and Biology 45, S63–S70.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Müller O,
Schreier P, Uhrig J
(2008) Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Molecular Genetics and Genomics 279, 27–39.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Oliver RP, Ipcho SVS
(2004) Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Molecular Plant Pathology 5, 347–352.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Orbach MJ,
Farrall L,
Sweigard JA,
Chumley FG, Valent B
(2000) A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. The Plant Cell 12, 2019–2032.
|
CAS |
Crossref |
PubMed |
Panstruga R, Dodds PN
(2009) Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324, 748–750.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Rafiqi M,
Gan P,
Ravensdale M,
Lawrence GJ,
Ellis JG,
Jones DA,
Hardham AR, Dodds PN
(2010) Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. The Plant Cell 22, 2017–2032.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ridout CJ,
Skamnioti P,
Porritt O,
Sacristan S,
Jones JDG, Brown JKM
(2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. The Plant Cell 18, 2402–2414.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Rooney HCE,
Van’t Klooster JW,
Van Der Hoorn RAL,
Joosten MHAJ,
Jones JDG, De Wit PJGM
(2005) Plant science: Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308, 1783–1786.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Schornack S,
Huitema E,
Cano LM,
Bozkurt TO, Oliva R ,
et al
.
(2009) Ten things to know about oomycete effectors. Molecular Plant Pathology 10, 795–803.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Shen Q-H,
Saijo Y,
Mauch S,
Biskup C, Bieri S ,
et al
.
(2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315, 1098–1103.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Stergiopoulos I, De Wit PJGM
(2009) Fungal effector proteins. Annual Review of Phytopathology 47, 233–263.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sweigard JA,
Carroll AM,
Kang S,
Farrall L,
Chumley FG, Valent B
(1995) Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. The Plant Cell 7, 1221–1233.
|
CAS |
Crossref |
PubMed |
Tan K-C,
Oliver RP,
Solomon PS, Moffat CS
(2010) Proteinaceous necrotrophic effectors in fungal virulence. Functional Plant Biology 37, 907–912.
| Crossref | GoogleScholarGoogle Scholar |
Teertstra WR,
Deelstra HJ,
Vranes M,
Bohlmann R,
Kahmann R,
Kämper J, Wösten HAB
(2006) Repellents have functionally replaced hydrophobins in mediating attachment to a hydrophobic surface and in formation of hydrophobic aerial hyphae in Ustilago maydis. Microbiology 152, 3607–3612.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Tian M,
Win J,
Song J,
van der Hoorn R,
van der Knaap E, Kamoun S
(2007) A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiology 143, 364–377.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Valent B,
Crawford MS,
Weaver CG, Chumley FG
(1986) Genetic studies of fertility and pathogenicity in Magnaporthe grisea (Pyricularia oryzae). Iowa State Journal of Research 60, 569–594.
van den Burg HA,
Harrison SJ,
Joosten MHAJ,
Vervoort J, de Wit PJGM
(2006)
Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Molecular Plant-Microbe Interactions 19, 1420–1430.
| 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 |
Xu JR,
Zhao X, Dean RA
(2007) From genes to genomes; a new paradigm for studying fungal pathogenesis in Magnaporthe oryzae. Advances in Genetics 57, 175–218.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yoshida K,
Saitoh H,
Fujisawa S,
Kanzaki H, Matsumura H ,
et al
.
(2009) Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. The Plant Cell 21, 1573–1591.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
