MPMI Vol. 22, No. 2, 2009, pp. 115–122. doi:10.1094/MPMI-22-2-0115. © 2009 The American Phytopathological Society
CURRENT REVIEW
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Emerging Concepts in Effector Biology
of Plant-Associated Organisms
Saskia A. Hogenhout,1 Renier A. L. Van der Hoorn,2 Ryohei Terauchi,3 and Sophien Kamoun4
1Department of Dia and Stress Biology, The John Innes Centre, Norwich Rearch Park, Norwich, NR4 7UH, U.K.; 2Plant Chemetics lab, Max Planck Institute for Plant Breeding Rearch, 50829 Cologne, Germany; 3Iwate Biotechnology Rearch Center, Kitakami, Iwate, Japan; 4 The Sainsbury Laboratory, John Innes Centre, Norwich NR4 7UH, U.K. Submitted 21 August 2008. Accepted 16 October 2008.
Plant-associated organisms crete proteins and other mole-cules to modulate plant defen circuitry and enable coloni-zation of plant tissue. Understanding the molecular function of the creted molecules, collectively known as effectors, became widely accepted as esntial for a mechanistic un-
derstanding of the process underlying plant colonization. This review summarizes recent findings in the field o f effecto r bio lo gy and highlights the co mmo n co ncepts that have emerged fro m the study o f cellular plant patho gen effectors.
A diversity of plant pathogens, including bacteria, fungi, oo-mycetes, and nematodes, crete proteins and other molecules to different cellular compartments of their hosts to modulate plant defen circuitry and enable parasitic colonization (Abramovitch et al. 2006; Birch et al. 2006; Block et al. 2008; Chisholm et al. 2006; Davis et al. 2008; Kamoun 2006, 2007; Misas-Villamil and van der Hoorn 2008). Understanding the molecular function of the creted molecules, collectively known as effectors, is widely accepted as critical for a mecha-nistic understanding of the process underlying host coloniza-tion and pathogenicity.
Major progress in our understanding of effectors has occurred recently. First, the preci biochemical activities of a number of bacterial effectors have been unraveled. Second, the concept of effectors has extended beyond bacterial plant pathogens with the discovery of effectors in fungi, oomycetes, and nema-todes. Finally, robust computational methods applied to ge-nome quence data of plant pathogenic microbes has resulted in genome-wide catalogs of putative effector genes. All the activities significantly incread our knowledge of effectors from a diversity of plant pathogens, their
host targets, and how and where the molecules interact and affect the outcome of the plant-pathogen interaction. Remarkably, many commonal-ities can be noted among the different pathosystems under study. The objective of this review is to summarize and discuss the common threads that have emerged from the study of cel-lular plant pathogen effectors.
Effectors: Usage and definition.
The usage of the term “effector” became popular in the field of plant-microbe interactions with the discovery that plant pathogenic gram-negative bacteria utilize a specialized ma-chinery, the type III cretion system (T3SS), to deliver pro-teins inside host cells (Abramovitch et al. 2006; Block et al. 2008; McCann and Guttman 2008; Zhou and Chai 2008). The proteins, first discovered becau of their ability to trig-ger the hypernsitive respon in resistant plants (“avirulence” activity), were later found to contribute to virulence in suscep-tible plants (typically host plants that lack effective resistance [R] genes). Hence, the term avirulence became conceptually restrictive, since the same protein with an avirulence activity in incompatible interactions may display a positive virulence ac-tivity in compatible interactions. The term effector address this conceptual limitation of the term avirulence. The increa in the u of effector relative to avirulence in the journal Mo-lecular Plant-Microbe Interactions is striking and reflects a major paradigm shift in the field (Fig. 1).
More recently, a broader range of plant microbiologists have adopted the term effector and its associated concepts. Indeed, this term is now also routinely ud in the fungal and oomy-cete literature and is becoming increasingly popular in nema-tology to describe creted proteins that exert some effect on plant cells. However, the various scientific communities define
and small molecules that alter host-cell structure and function. The alterations either facilitate infection (virulence factors and toxins) or trigger defen respons (avirulence factors and elicitors) or both (Huitema et al. 2004; Kamoun 2006, 2007). The concept of “extended phenotype” (i.e., “genes who effects reach beyond the cells in which they reside”) put forward by Richard Dawkins in a classic book (Dawkins 1999) sums up perfectly this view of effectors. Effectors can be viewed as “parasite genes having phenotypic expression in host bodies and behavior” (Dawkins 1999). Indeed, effectors are the products of genes that reside in pathogen genomes but that actually function at the interface with the host plant or even inside plant cells, providing a vivid example of Dawkins’ extended phenotype (Kamoun 2006, 2007).
This broader definition of effectors includes many molecules, such as pathogen-associated molecula
r patterns (PAMPs), tox-ins, and degradative enzymes. In the abnce of more informa-tion, it would be suitable to call the molecules effectors until the exact activities of a pathogen molecule are revealed, after which they may be renamed to reflect their specific activities. For lists of specific definitions, we invite readers to consult earlier publications (Kamoun 2006; van der Hoorn and Kamoun 2008).
Corresponding author: S. Kamoun; E-mail: sophien.kamoun@tsl.ac.uk;
website: www.KamounLab
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Emerging concepts in effector biology.
Many effectors are delivered into host cells. Plant pathogenic bacteria, fungi, oomycetes, and nematodes have evolved the capacity to deliver effector proteins inside host cells through a diversity of mechanisms. Gram-negative bacteria u specialized cretion systems, such as T3SS, to deliver proteins inside host cells (Abramovitch et al. 2006; Block et al. 2008; Galan and Wolf-Watz 2006; McCann and Guttman 2008; Zhou and Chai 2008). Biotrophic fungi and oomycetes have evolved ha
ustoria for this purpo. Haustoria are specialized structures that form within plant cells but remain encad in a modified plant cell membrane, known as the extrahaustorial membrane (Hahn and Mendgen 2001; Panstruga 2003). Haustoria were initially thought to primarily function in nutrient uptake, but more re-cently, evidence emerged that haustoria take part in the cretion of particular class of host-translocated fungal and oomycete effectors (Catanzariti et al. 2006; Dodds et al. 2004; Kemen et al. 2005; Whisson et al. 2007). Some fungal proteins, notably the Pyrenophora tritici-repentis host-lective toxin ToxA, do not require the pathogen for translocating inside plant cells (Manning and Ciuffetti 2005; Sarma et al. 2005). ToxA travels inside host cells presumably by coopting a plant surface recep-tor that binds to an Arg-Gly-Asp (RGD) motif (Manning et al. 2008). Plant parasitic nematodes utilize a specialized feeding organ known as the stylet, to inject their effector proteins inside a parasitized plant vascular cell (Davis et al. 2008).
Other effectors act in the apoplast. Some effectors act in the extracellular space at the plant-microbe interface, where they interfere with apoplastic plant defens (Kamoun 2006; Misas-Villamil and van der Hoorn 2008). Examples include the -creted protein effectors of the tomato fungal pathogen Clado-sporium fulvum. This fungus is an extracellular parasite of to-mato that grows exclusively in the apoplast and does not form haustoria or haustoria-like structures (Rivas and Thomas 2005; Tho
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mma et al. 2005). All known C. fulvum effectors, such as Avr2, Avr9, Avr4, and ECP2, are small cysteine-rich proteins that are thought to function exclusively in the apoplast (Thomma et al. 2005). Oomycetes, such as Phytophthora infestans, are also known to crete apoplastic effectors in addition to host translocated (cytoplasmic) effectors (Birch et al. 2006; Damasceno et al. 2008; Kamoun 2006; Ro et al. 2002; Tian et al. 2004, 2005, 2007).
One common activity ascribed to many apoplastic effectors of C. fulvum and other fungal and oomycete pathogens is their ability to inhibit and protect against plant hydrolytic enzymes, such as proteas, glucanas, and chitinas (reviewed by (Misas-Villamil and van der Hoorn 2008). C. fulvum Avr2 is a cysteine protea inhibitor targeting the apoplastic cysteine proteas Rcr3 and PIP1 of tomato (Rooney et al. 2005; Shabab et al. 2008; van Es et al. 2008). P. infestans also cretes cysteine protea inhibitors, such as EPIC2B, which inhibits PIP1 as well as other apoplastic cysteine proteas of tomato (Tian et al. 2007), and EPI1 and EPI10, which are mul-tidomain-creted rine protea inhibitors of the Kazal fam-ily that bind and inhibit the pathogenesis-related (PR) protein P69B, a subtilisin-like rine protea of tomato that is thought to function in defen (Tian et al. 2004, 2005). Phytophthora spp. are also known to crete glucana inhibitors that inhibit the host apoplastic enzyme endo-β-1,3 glucana (Damasceno et al. 2008; Ros
e et al. 2002). It ems likely that many other apoplastic effectors act as host enzyme inhibitors. For exam-ple, the creted AvrP123 from the flax rust fungus Melamp-sora lini shows quence similarity to Kazal rine protea inhibitors (Catanzariti et al. 2006).
One effector—many host targets. Plant pathogen effectors frequently have more than one host target (Fig. 2). Pudomo-nas syringae
AvrRpt2 is a T3SS effector with proteolytic activ-Fig. 1. Effectors: The ri of a concept. The graph illustrates the decline in
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the u of the term avirulence compared with the term effector in the journal
Molecular Plant-Microbe Interactions. The numbers were obtained by
keyword arches in the journal website for articles published from 1990
to 2006.
Fig. 2. One effector-many effector targets. The cartoons compare the tradi-
tional one pathogen effector-one host effector target model (left panels)to
the emerging view that effectors frequently have more than one host target
(right panels). The effector targets can be components of the plant defen
respon that are being inactivated by pathogen effectors, and in such cas
have been termed operative effector targets (OT) by V an der Hoorn and
Kamoun (2008). In susceptible plants, the interaction between effectors and
effector targets results in molecular events that facilitate colonization, such as
suppression of defen respons, enhanced dia susceptibility, and elici-
tation of dia symptoms. In resistant plants, plant resistance (R) proteins
recognize the effector-virulence target complex, resulting in the activation of
the hypernsitive respon. Recognition of effectors by R proteins is often
indirect, via perception of a manipulated effector target. The recognized
effector targets may contribute to host defen or susceptibility (guarded
effector targets) or may not function in defen or susceptibility, thus acting
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as decoys that trap the effector (V an der Hoorn and Kamoun 2008). Effectors
are depicted by gray half circles, OT by purple crescents, guarded effector
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targets or decoys by green crescents, and R proteins by red squares.
116 / Molecular Plant-Microbe Interactions
ity against at least five Arabidopsis proteins, including the negative defen regulator RIN4 (Chisholm et al. 2005; Takemoto and Jones 2005). AvrPto, another Pudomonas sy-ringae T3SS effector, is a kina inhibitor that binds and inhib-its the tomato kina Pto (Xing et al. 2007). In addition, AvrPto inhibits the kina domains of FLS2 and EFR, which are two pathogen recognition receptors, as well as the kina domain of their signaling partner BAK1 (Shan et al. 2008; Xiang et al. 2008). The transmembrane receptor-like kina proteins participate in the recognition of conrved pathogen molecules, and their inhibition by AvrPto presumably acts to suppress the innate immune respon mediated by the recep-tors. Other examples of multiple targets include the protea inhibitors Avr2 and EPIC2B, which, as discusd above, in-hibit veral tomato apoplastic proteas (Shabab et al. 2008; Tian et al. 2007; van Es et al. 2008).
能动作用Each interaction of an effector and a host protein can be either beneficial for the pathogen, have negative conquences, or have neutral effects on the interaction between the pathogen and plant. In light of the ideas, Van der Hoorn and Kamoun (2008) defined operative targets as tho host targets that, when manipulated by effectors, result in an altered state of de-fen or susceptibility. It therefore becomes important to dis-tinguish operative targets from other types of host targets. The thoughts led to the concept that some host targets are decoys, proteins that are not operative targets but that, when perturbed by effectors, trigger host recognition by cognate R proteins (van der Hoorn and Kamoun 2008).
Many effectors suppress plant immunity. Suppression of plant innate immunity has emerged as the primary function of effectors, particularly of T3SS effectors of plant pathogenic bacteria (Abramovitch et al. 2006; Block et al. 2008; Chisholm et al. 2006; Jones and Dangl 2006; Zhou and Chai 2008). Sev-eral T3SS effectors contribute to virulence by suppressing basal defens induced by conrved pathogen epitopes named PAMPs (Hauck et al. 2003; M. G. Kim et al. 2005). Other T3SS effectors suppress hypernsitive cell death elicited by various Avr proteins, explaining, in some cas, earlier obr-vations of epistatic interactions among Avr genes (Abramovitch et al. 2003; Jamir et al. 2004; H. S. Kim et al. 2005; Tsiamis et al. 2000). T3SS effectors probably interfere with h
ost immu-nity via a diversity of mechanisms, but the effectors studied so far are known to target three plant process that are key to in-nate immunity, namely protein turnover, RNA homeostasis, and phosphorylation pathways (Block et al. 2008).
The occurrence of effectors that suppress host cell death has been long hypothesized for biotrophic fungal and oomycete pathogens (Panstruga 2003), bad on cytological obrvations of susceptible interactions and the prevalence of cell death suppressors among bacterial T3SS effectors (Jamir et al. 2004; Janjuvic et al. 2006). Emerging findings indicate that veral oomycete RXLR effectors suppress host immunity. P. infestans Avr3a suppress the hypernsitive cell death induced by another P. infestans protein, INF1 elicitin, pointing to a possi-ble virulence function (Bos et al. 2006). Another RXLR effec-tor, P. sojae Avr1b, also suppress programmed cell death induced by the mou protein BAX in yeast and plants (Dou et al. 2008). Sohn and associates (2007) showed that delivery of Hyaloperonospora parasitica ATR1 and ATR13 enhances Pudomonas syringae virulence. ATR13 also suppress cal-lo deposition triggered by Pud omonas syringae, suggest-ing that it targets basic basal defens against pathogens (Sohn et al. 2007). The findings indicate that, similar to bacterial T3SS effectors, oomycete RXLR effectors often function in suppression of plant immunity. However, the mechanisms through which RXLR effectors interfere with plant immunity remain to be elucidated.
A recent study illustrates the concept that plant pathogenic fungi can evade host immunity by evolving effectors that suppress R gene–mediated resistance. Houterman and associ-ates (2008) showed that the effector Avr1 of Fusarium oxy-sporum f. sp. lycopersici suppress the resistance respon conferred by the R genes I-2 and I-3. No apparent virulence function has been detected for Avr1 on plants that do not carry the I
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genes, suggesting that this effector may solely Fig. 3. Effectors mimic plant molecules. In each panel,plant molecules are indicated in green at left and the corresponding mimicking plant pathogen effectors in red at right. A, The Pudomonas syringae phytotoxin coro-natine mimics jasmonoyl-isol
eucine (JA-Ile), which is a crucial plant sig-naling molecule for regulating plant defen respons (Weiler et al. 1994; Bender et al. 1999). B, The P. syringae AvrPtoB effector has anti–pro-grammed cell death activity and mimics E3 ubiquitin ligas (Janjuvic et al. 2006), such as Arabid opsis thaliana Pub14 (AtPub14), that regulate protein degradation in plants (Andern et al. 2004). Structures were de-rived from Protein Data Bank identities 1T1H (AtPub14) and 2FD4 (AvrPtoB) and were visualized in iMol v. 0.4. The three residues shown by asterisks bind the E2 ubiquitin-conjugating enzyme and locate in the con-rved α-helix (red ribbon) and two-loop structures (gray ribbon) that form the E2-binding groove (Janjuvic et al. 2006). The locations of the β-sheets (blue ribbon) flanking the lower part of the groove are also con-rved. C, The Xanthomonas campestris pv. vesicatoria effector AvrBs3 binds a conrved element (upa-box) of promoter regions. In compatible interactions, AvrBs3 induces hyperthrophy through induction of the ex-pression of upa20 and other upa genes (upaxx) with unknown functions (Kay et al. 2007). In incompatible interactions, AvrBs3 also binds the pro-moter of the resistance gene Bs3, resulting in a hypernsitive respon (Romer et al. 2007). AvrBs3 is thought to mimic an unknown plant tran-scription factor (TFx) that also presumably binds the upa-box, and induce Bs3transcription only in specific plant developmental stages when specific localized cell death is required.
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function in interfering with perception of the pathogen by the R proteins.
Some effectors alter plant behavior and d evelopment. As the previous ction illustrates, it is now well established that many effectors interfere with host innate immunity. Nonethe-
less, there are instances of effectors that have activities other than suppression of innate immunity. Some effectors alter host plant behavior and morphology. One elegant example is coronatine, which was shown by Melotto and coauthors (2006) to trigger stomatal reopening in Arabidopsis and thereby facilitate bacterial entry inside the plant apoplast. Xanthomonas effectors of the AvrBs3 family of transcrip-tional activators are known to induce cellular division and enlargement in susceptible host plants (Duan et al. 1999; Kay et al. 2007) (Fig. 3C). Expression of Xanthomonas citri pthA in citrus cells is sufficient to cau macroscopic hyperplastic lesions analogous to the canker symptoms caud by the pathogen (Duan et al. 1999) (Fig. 3B). The canker lesions are thought to facilitate bacterial relea from infected tissue and to enhance bacterial dismination. X. vesicatoria AvrBs3 is also known to cau cell hypertrophy, although the impact of such a symptom on bacterial fitness is less clear (Kay et al. 2007).
Many other plant-associated organisms are known to alter the morphology of their host plant, resulting in malformations that either create a protective niche or enhance dispersal. Classic examples include rhizobial nodules (Oldroyd and Downie 2008), galls induced by Agrobacterium spp. and other bacteria (Chalupowicz et al. 2006), and Witches’ broom and other de-velopmental alterations caud by veral pathogens such as phytoplasmas (Hogenhout et al. 2008).
In summary, some phytopathogen effectors appear to have activities other than suppression of immunity. It is reasonable to expect that natural lection would favor effectors with any type of phenotypic expression that improves pathogen fitness, and rearchers in the field should keep an open mind to effec-tor activities that do not involve the host immune respon. Molecular mimicry by effectors. Although effectors are en-coded by pathogen genes, they function in a plant cellular en-vironment and, therefore, could have been lected to mimic plant molecules. Strikingly, many effectors produce analogs and mimics of plant hormones. One example is coronatine, a toxin creted by veral pathovars of Pudomonas syringae that is a structural and functional mimic of the plant hormone jasmonoyl-isoleucine (Fig. 4A) (Bender et al. 1999; Weiler et al. 1994). Coronatine has many effects that enhance bacterial colonization of plants. The include impacting phytohormone pathways, such as jamming the induction of the salicylic acid–mediated resistance re
spon and increasing the opening of plant stomates (Fig. 3A). Other classic examples of phytohor-mone mimicry in plant pathogens include auxins and cytoki-nins produced by various bacteria, including agrobacterium (Costacurta and Vanderleyden 1995), modified cytokinins produced by the fas operons of Rhod ococcus fascians and Streptomyces turgidiscabies (Hogenhout and Loria 2008), and gibberrellins produced by veral fungi (Kawaide 2006) such as Gibberrella fujikuroi , which caus the foolish edling dia of rice (Tudzynski 1999) (Fig. 3C).
Besides hormone mimicry, protein effectors reprent veral additional striking examples of molecular mimicry as well. The C-terminal region of the Pud omonas syringae type-III effector AvrPtoB, for example, was found to be a structural and functional mimic of eukaryotic E3 ubiquitin ligas (Fig. 4B) (Janjuvic et al. 2006). AvrPtoB-mediated degradation of the target host kina Fen is dependent on the E3 ubiquitin liga activity of AvrPto (Robrock et al. 2007). Another ex-ample of molecular mimicry is the Xanthomonas vesicatoria type-III effector AvrBs3, which travels to the host nucleus, where it acts as a transcriptional activator by binding to a con-rved promoter quence called the upa box (Kay et al. 2007; Romer et al. 2007) (Fig. 4C). Becau the upa box is conrved
in veral pepper genes, AvrBs3 is thought to mimic a yet-to-
Fig. 4. Effectors can alter plant behavior and development. Each panel illus-trates an example of an effector function with the unaffected plant on the left and the outcome of the effector activity on the right. A,Plant stomata clo upon detection of pathogen-associated molecular patterns from the bacterium Pudomonas syringae (left panel) (Melotto et al. 2006). How-ever, the phytotoxin coronatine (COR) inhibits stomatal closure,resulting in bacterial entry into plant leaves through the open stomata (right panel)(Melotto et al. 2006). B, During plant infection, Xanthomonas citri grows in the intracellular spaces of the leaf spongy mesophyll (left). The effector PthA induces hyperthrophy, hyperplasia, and necrosis, which result in the formation of cankers on the leaf surface (right) (Duan et al. 1999). Xantho-monas citri bacteria ooze from the canker-ruptured epidermis and then spread to other plants by rain splash (Duan et al. 1999). C,The fungus Gibberella fujikuroi (also known as Fusarium moniliforme ) (yellow spots) infects a single rice edling (left). The fungus produces the growth hor-mone gibberellin, which induces plant elongation, resulting in an elon-gated (foolish) edling veral inches taller than noninfected edlings (right). The height of the plant facilitates the spread of airborne fungus spores by the wind.
be-discovered host transcription factor that also targets the upa box. Emerging work by veral groups revealed that plant parasitic nematodes crete a battery of proteins that mimic plant molecul
es (Davis et al. 2008). Fascinating examples of plant mimics include creted nematode proteins with similar-ity to expansins, components of the plant proteasome, and CLA V ATA3 signaling peptides. Remarkably, the CLA V ATA3-like 4G12 gene of the soybean cyst nematode Heterodera gly-cines complements the Arabidopsis clv3-1 mutant and, simi-larly to CLA V ATA3, negatively regulates the expression of the Arabidopsis WUSCHEL gene (Wang et al. 2005). How the CLA V ATA3-mimicking peptides contribute to parasitism is un-known but could involve interfering with plant-cell growth and development (Mitchum et al. 2008).
Effector genes evolve at highly accelerated rates relative to the core genome. Genes that encode effector proteins are ex-pected to be direct targets of the evolutionary forces that drive coevolution between host and pathogen (Ma and Guttman 2008; McCann and Guttman 2008). Effector alleles that increa the reproductive success of the pathogen will be immediately favored by natural lection and positively lected. Indeed, many effector genes have evolved at accelerated rates compared with the pathogen core genome and often display extreme levels of positive lection with significantly higher rates of nonsyn-onymous to synonymous nucleotide substitutions (Ka/Ks or d N/d S ratios greater than 1) (Allen et al. 2004; Dodds et al. 2006; Liu et al. 2005; Ma et al. 2006; Win et al. 2007). In modular effector proteins, such as bacterial T3SS effectors and oomycete RXLR effecto
rs, the different domains are under dif-ferent lective pressures, depending on whether they function in cretion or carry the effector activity per . Thus, N-termi-nal domains, such as the signal peptide, RXLR domain, and T3SS targeting quence, typically exhibit reduced levels of polymorphisms compared with the C-terminal effector region (Stavrinides et al. 2006; Ma and Guttman 2008; Win et al. 2007).
Besides acting on nucleotide polymorphisms, natural lec-tion is known to act on copy number polymorphisms of effec-tor genes (prence or abnce polymorphisms and variation in gene copy number). Effector genes of filamentous pathogens often localize in loci with high genome plasticity including transposon-rich and telomeric regions (Gout et al. 2006; Orbach et al. 2000). K. Yoshida and R. Terauchi (unpublished data) recently showed that two effector loci of Magnaporthe oryzae display low nucleotide diversity but a high degree of prence or abnce polymorphisms. The P. infestans Avr3b-Avr10-Avr11 locus exhibits remarkable copy number variation resulting in amplification of up to 25 truncated copies of the candidate Avr gene pi3.4 (Jiang et al. 2006). The association of effector genes with plastic genomic loci could confer a mecha-nism of adaptation to host resistance, perhaps by increasing genetic and epigenetic variation and enabling accelerated evo-lution.
Some effector targets evolved to evade manipulation by ef-fectors. Since it is becoming evident that effectors enhance dia susceptibility, it can be expected that host target alleles would evolve to elude tho effectors. The recessive rice muta-tions in xa13 render the promoter of this gene innsitive to transcription-activating effectors of Xanthomonas oryzae pv. oryzae, thus resulting in resistance to bacterial blight dia (Iyer-Pascuzzi and McCouch 2007; Sugio et al. 2007; Yang et al. 2006) (Fig. 5B). Another recessive rice blast resistance gene, xa5, is caud by mutations in transcription factor IIA, which presumably prevents actions by the cognate effector (Iyer-Pascuzzi and McCouch 2007). Furthermore, mutations in elongation factor elF4E are known to evade interactions with potyvirus effector VPg (Charron et al. 2008). More recently, an allele of the tomato cysteine protea Rcr3 was identified to carry a mutation that renders the protein innsitive to inhibi-tion by C. fulvum Avr2 (Shabab et al. 2008) (Fig. 5A). We ex-pect many additional examples to emerge in the future as rearchers exploit next-generation quencing technologies to systematically probe variation in effector target quences for evidence of lection. One fascinating question is to fully under-stand how the three-party interplay between effectors, effector targets, and R proteins evolve, given the conflicting lective forces that are likely to occur in natural populations of plants and pathogens (van der Hoorn and Kamoun 2008). Identification of effector target alleles that are innsitive to effector manipulation but yet retain their intrinsic function pro-vides an alternati
ve strategy to the usage of classic R genes for engineering dia-resistant plants. Mechanistic understand-ing of the mode of action of effectors is powerful information that can guide the relea and deployment of dia resistance in agriculture and is an improvement compared with the hit or miss approach that has been characteristic of plant-resistance breeding so far. One impressive example is the effective man-agement of bacterial blight of rice through the relea of resis-tant cultivars that combine complementary types of resistance, i.e., loss of susceptibility and classic resistance genes (Leung
2008). Resistance encoded by the cultivars proved to be par-Fig. 5. Effector targets can evolve to evade manipulation by effectors. A, The N194D mutation in tomato cysteine protea RCR3 prevents inhibi-tion by the A VR2 effector. In the model of RCR3, the substrate-binding groove with the catalytic cysteine residue (yellow) is flanked by Asn194 in RCR3 of Solanum lycopersicum (lyc) but is replaced by Asp in RCR3 of Solanum chilen (chi). This variance reduces the interaction with protea inhibitor A VR2 from the tomato pathogen Cladosporium fulvum (Shabab et al. 2008). B, M
utations in the promotor of the Xa13gene prevents induction by a Xanthomonas transcription activator-like (TAL) effector. Xa13 is a pollen-expresd gene that is induced in leaves during infection by various Xanthomonas oryzae pv. oryzae strains, presumably mediated by a type III–creted TAL effector similar to AvrBs3. Mutations in the promoter of Xa13 prevent induction during infection and cau resistance that is inherited as a recessive trait (Chu et al. 2006).
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