Table 1.
Targets and biochemical functions of type III effector proteins.
| Effectora | Known or predicted biochemical function | Plant targets (organism)b | Effector-triggered modifications and/or functions of plant targetsc | References |
|---|---|---|---|---|
| Pseudomonas syringae | ||||
| AvrB | n.d.d | RAR1 (Arabidopsis) | RAR1 mediates the interaction of AvrB with Hsp90 | Cui et al. (2010) |
| RIN4 (tomato, Arabidopsis) | Phosphorylation of RIN4 in NOI domains and activation of the R protein RPM1; induction of AHA1-mediated stomatal opening; increased interaction between COI1 and JAZ9 | Mackey et al. (2002); Liu et al. (2009); Cui et al. (2010); Zhou et al. (2015) | ||
| MPK4 (Arabidopsis) | Phosphorylation and activation of MPK4; the interaction with AvrB is increased in the presence of RAR1 | Cui et al. (2010) | ||
| RIPK (Arabidopsis) | Disruption of the RIPK-RIN4 complex; phosphorylation of RIN4; phosphorylation of AvrB by RIPK | Liu et al. (2011) | ||
| AvrPphB (HopAR1) | Cysteine protease | PBS1, PBS1-like kinases, RIPK (Arabidopsis) | Cleavage of PBS1 and PBS1-like proteins including RIPK; activation of the R protein RPS5, which guards PBS1 | Shao et al. (2003); Zhang et al. (2010); Russell, Ashfield and Innes (2015) |
| BIK1 (Arabidopsis) | Cleavage of BIK1; interference with PTI | Zhang et al. (2010) | ||
| AvrPto | n.d. | Pto (tomato) | Phosphorylation of Pto; activation of Prf-Pto-mediated ETI responses | Scofield et al. (1996); Tang et al. (1996); Kim, Lin and Martin (2002); Ntoukakis et al. (2013) |
| FLS2 kinase domain (Arabidopsis, tomato) | Inhibition of autophosphorylation of FLS2; suppression of BIK1 phosphorylation | Xiang et al. (2008, 2011) | ||
| EFR kinase domain (Arabidopsis) | Inhibition of autophosphorylation of EFR | Xiang et al. (2008) | ||
| BAK1 kinase domain (Arabidopsis) | Disruption of FLS2-BAK1 complexe | Shan et al. (2008); Xiang et al. (2008); Zhou et al. (2014) | ||
| RIN4 (tomato) | Degradation of RIN4 (dependent on Pto, Prf and the proteasome) | Luo et al. (2009) | ||
| Kinases At2g23200, BSK1, BSK3, CDG1 (Arabidopsis) | n.d. | Xiang et al. (2008, 2011) | ||
| AvrPtoB (HopAB1) | E3 ubiquitin ligase | EFR (Arabidopsis) | Ubiquitination of EFR | Göhre et al. (2008) |
| Kinase Bti9 (tomato) | Suppression of Bti9 kinase activity | Zeng et al. (2012) | ||
| CERK1 (Arabidopsis) | Degradation of CERK1 | Gimenez-Ibanez et al. (2009) | ||
| Pto (tomato) | Phosphorylation of Pto and AvrPtoB; activation of Prf-Pto-mediated ETI responses | Kim, Lin and Martin (2002); Ntoukakis et al. (2009) | ||
| Kinase Fen (tomato) | Degradation of Fen; suppression of Fen-triggered ETI | Rosebrock et al. (2007) | ||
| FLS2 (Arabidopsis) | Dissociation of FLS2-BAK1 complex; degradation of FLS2 | Göhre et al. (2008); Shan et al. (2008) | ||
| BAK1 (Arabidopsis) | Dissociation of FLS2-BAK1 complex; inhibition of BAK1 kinase activity | Göhre et al. (2008); Shan et al. (2008); Cheng et al. (2011) | ||
| RIN4 (tomato) | Degradation of RIN4 (dependent on Pto and Prf) | Luo et al. (2009) | ||
| AvrRpm1 | n.d. | RIN4 (Arabidopsis) | Phosphorylation of RIN4 in NOI domains; activation of RPM1 | Mackey et al. (2002) |
| AvrRps4 | n.d. | Lipase/esterase-like protein EDS1 (Arabidopsis) | Disruption of the complex between EDS1 and the R protein RPS4f | Bhattacharjee et al. (2011) |
| WRKY domains of RRS1-R and RRS1-S, WRKY41, WRKY70, WRKY33, WRKY60 | Activation of RPS4-dependent ETI | Sarris et al. (2015) | ||
| AvrRpt2 | Cysteine protease | RIN4 (Arabidopsis) | Cleavage of RIN4 and activation of RPS2 | Axtell et al. (2003b); Mackey et al. (2003); Kim et al. (2005a) |
| ROC1 (Arabidopsis) | Activation of AvrRpt2 protease activity | Coaker, Falick and Staskawicz (2005); Coaker et al. (2006) | ||
| Unknown | Degradation of the Aux/IAA repressor protein AXR2 (depends on protease activity of AvrRpt2 and proteasome; no direct cleavage) | Cui et al. (2013) | ||
| HopA1 (HopPsyA) | n.d. | EDS1 (Arabidopsis) | Disruption of the complex between EDS1 and RPS4f | Bhattacharjee et al. (2011) |
| HopAF1 | n.d. | Methylthioadenosine nucleosidase proteins MTN1 and MTN2 (Arabidopsis) | MTN1 and MTN2 are involved in the methionine recycling pathway and required for PAMP-induced ethylene production; HopAF1 inhibits MTN1 activity in vitro and displays structural homology to deamidases | Washington et al. (2016) |
| HopAI1 (HolPtoAI) | Phosphothreonine lyase | MPK3 (Arabidopsis) | Dephosphorylation and inactivation of MPK3 | Zhang et al. (2007) |
| MPK4 (Arabidopsis) | Reduced kinase activity of MPK4 | Zhang et al. (2012) | ||
| MPK6 (Arabidopsis, tomato) | Dephosphorylation and inactivation of MPK6 | Singh et al. (2014); Zhang et al. (2007) | ||
| Kinase BSK7 (tomato) | n.d. | Singh et al. (2014) | ||
| HopAO1 (HopPtoD2) | Tyrosine phosphatase | FLS2 kinase domain (Arabidopsis) | Suppression of FLS2-mediated PTI responses | Macho et al. (2014) |
| EFR kinase domain (Arabidopsis) | Reduced phosphorylation of EFR | Macho et al. (2014) | ||
| HopD1 (AvrPphD) | n.d. | Transcription factor NTL9 (Arabidopsis) | Suppression of NTL9-regulated gene expression during ETI | Block et al. (2014) |
| HopE1 | n.d. | Calmodulin (Arabidopsis) | Dissociation of MAP65 from microtubules in the presence of calmodulin | Guo et al. (2016) |
| MAP65 (Arabidopsis) | ||||
| HopF2 | ADP-RT | MKK5, MAP2Ks (Arabidopsis) | ADP-ribosylation of MKK5 at R313, which presumably leads to the inactivation of MKK5 | Wang et al. (2010); Singh et al. (2014) |
| MPK6 (tomato) | n.d. | Singh et al. (2014) | ||
| RIN4 (Arabidopsis) | ADP-ribosylation of RIN4; inhibition of RIN4 degradation by AvrRpt2 | Wilton et al. (2010); Hurley et al. (2014) | ||
| BAK1 (Arabidopsis) | Interference with BIK1 phosphorylation and MAPK signaling | Wang et al. (2010); Wu et al. (2011); Zhou et al. (2014) | ||
| Kinase BSK7 (tomato) | n.d. | Singh et al. (2014) | ||
| HopG1 | n.d. | Mitochondrial-localized kinesin motor protein (Arabidopsis) | HopG1 associates with actin presumably via its interaction with kinesin and induces actin filament bundling | Shimono et al. (2016) |
| HopI1 (HopPmaI) | n.d. | Hsp70 (Arabidopsis) | Increased ATPase activity of Hsp70 in vitro; recruitment of cytosolic Hsp70 to chloroplasts | Jelenska, van Hal and Greenberg (2010) |
| HopM1 | n.d. | ARF-GEF MIN7 (Arabidopsis) | Degradation of MIN7; inhibition of vesicle trafficking | Nomura et al. (2006, 2011) |
| 14-3-3 protein GRF8/MIN10 (Arabidopsis) | GRF8/MIN10 retains TF BZR1 in the cytoplasm; HopM1 presumably alters the activity of GRF8/MIN10 and leads to increased accumulation of TF BZR1 in the nucleus and downregulation of BZR1 target genes (the ortholog of MIN10 is TFT1 which is targeted by XopN) | Nomura et al. (2006); Lozano-Duran et al. (2014) | ||
| HopN1 | Cysteine protease | Photosystem II component PsbQ (tomato) | Destabilization of PsbQ; reduced activity of PSII; suppression of ROS production | Rodriguez-Herva et al. (2012) |
| HopQ1 | n.d. | 14-3-3 proteins (N. benthamiana, tomato) | n.d. | Giska et al. (2013); Li et al. (2013b); Hann et al. (2014) |
| HopU1 (HopPtoS2) | ADP-RT | RNA-binding proteins including GRP7 and GRP8 (Arabidopsis) | ADP-ribosylation of GRP7; reduced binding of GRP7 to PRR transcripts; reduced FLS2 protein levels; no influence on FLS2 transcript levels | Fu et al. (2007); Jeong et al. (2011); Nicaise et al. (2013) |
| HopW1 | n.d. | Actin (Arabidopsis) | Disruption of actin cytoskeleton; inhibition of protein trafficking and interference with endocytosis | Kang et al. (2014) |
| Acetylornithine transaminase WIN1, protein phosphatase WIN2, firefly luciferase superfamily protein WIN3 (Arabidopsis) | Overexpression of WIN1 in Arabidopsis increases growth of P. syringae pv. tomato DC3000 delivering HopW1 | Lee, Jelenska and Greenberg (2008) | ||
| HopX1 (AvrPphE) | Cysteine protease | JAZ proteins (Arabidopsis) | Proteaseome-dependent degradation of JAZ proteins | Gimenez-Ibanez et al. (2014) |
| HopZ1a | Acetyltransferase | JAZ proteins (Soybean, Arabidopsis) | Acetylation and degradation of JAZ proteins; induction of JA-responsive genes; Hopz1a activity depends on phytate | Jiang et al. (2013) |
| Tubulin (Arabidopsis) | Acetylation of tubulin and destruction of MT; interference with vesicle trafficking | Lee et al. (2012) | ||
| GmHID1 (Soybean) | Degradation of GmHID1 | Zhou et al. (2011) | ||
| Pseudokinase ZED1 (Arabidopsis) | Acetylation of ZED1 and activation of the R protein ZAR1 | Lewis et al. (2013) | ||
| HopZ4 | Protease/ acetyltransferase | ATPase of proteasome RPT6 (Arabidopsis) | Inhibition of proteasome activity | Üstün et al. (2014) |
| Xanthomonas spp. | ||||
| AvrAC (XopACXcc) | Uridylyltransferase | BIK1 (Arabidopsis) | Uridylylation of BIK1; inhibition of BIK1 phosphorylation | Feng et al. (2012) |
| RIPK (Arabidopsis) | Uridylylation of RIPK | Feng et al. (2012); Guy et al. (2013) | ||
| RLCKs of family VII including PBL2 (Arabidopsis) | Uridylylation of RLCKs; activation of R protein ZAR1, which guards PBL2 interaction partner RKS1 | Guy et al. (2013); Wang et al. (2015) | ||
| AvrBsTXcv | Acetyltransferase | Tubulin-binding protein ACIP1 (Arabidopsis) | Acetylation of ACIP1; formation of ACIP1 aggregates | Cheong et al. (2014) |
| Arginine decarboxylase CaADC1 (pepper) | n.d. | Kim, Kim and Hwang (2013) | ||
| SGT1 (pepper) | Inhibition of SGT1 phosphorylation | Kim et al. (2014) | ||
| Hsp70 (pepper) | n.d. | Kim and Hwang (2015b) | ||
| SNF1-related kinase SnRK1 (pepper) | n.d. | Szczesny et al. (2010) | ||
| 19S subunit of proteasome RPN8 (pepper) | n.d. | Szczesny et al. (2010) | ||
| Aldehyde dehydrogenase ALDH1 (pepper) | n.d. | Kim and Hwang (2015a) | ||
| AvrGf2Xfa (XopAG family) | n.d. | Cyclophilin (grapefruit) | The interaction depends on the predicted cyclophilin binding domain of AvrGf2 | Gochez et al. (2016) |
| AvrXccBXccB186 | Cysteine protease/ acetyltransferase (YopJ family) | S-Adenosyl-L-methionine-dependent methyltransferases (SAM-MT1 and SAM-MT2) (Arabidopsis) | The interaction with SAM-MT2 was only observed in vivo but not detectable by in vitro approaches. | Liu et al. (2016) |
| XopDXcv | SUMO protease | Transcription factor MYB30 (Arabidopsis) | Reduced MYB30 activity; relocalization of MYB30 to subnuclear foci | Canonne et al. (2011) |
| Transcription factor ERF4 (tomato) | DeSUMOylation of ERF4; destabilization of ERF4 and reduced ethylene levels | Kim, Stork and Mudgett (2013) | ||
| XopDXccB100 | SUMO protease | Transcription factor MYB30 (Arabidopsis) | Reduced MYB30 activity; relocalization of MYB30 from nucleus to subnuclear foci; reduced expression of MYB30 target genes | Canonne et al. (2011) |
| XopDXcc8004 | SUMO protease | DELLA proteins (Arabidopsis) | Delay of the GA-induced degradation of the DELLA protein RGA; no effect on transcription of GA-responsive genes | Tan et al. (2014) |
| Transcription factor HFR1 (Arabidopsis) | DeSUMOylation of HFR1 | Tan et al. (2015) | ||
| XopJXcv | Cysteine protease/ acetyltransferase | ATPase RPT6 of the proteasome (Arabidopsis, tobacco) | Degradation of RPT6; inhibition of proteasome activity | Üstün, Bartetzko and Börnke (2013); Üstün and Börnke (2015) |
| XopLXcv | E3 ubiquitin ligase | n.d. | Ubiquitination of N. benthamiana proteins | Singer et al. (2013) |
| XopNXcv | n.d. | Tomato atypical receptor-like kinase (TARK) 1 (tomato) | Stabilization of a TARK1/TFT1 complex; suppression of PTI responses | Kim et al. (2009a); Taylor et al. (2012) |
| 14-3-3 proteins TFT1, TFT3, TFT5, TFT6 (tomato) | Interaction was observed in yeast | Kim et al. (2009a) | ||
| XopNXoo | n.d. | Putative zinc finger protein OsVOZ2 (rice) | n.d. | Cheong et al. (2013) |
| Putative thiamine synthase OsXNP (rice) | n.d. | Cheong et al. (2013) | ||
| XopPXoo | n.d. | U box domain of E3 ubiquitin ligase OsPUB44 (rice) | Inhibition of the E3 ubiquitin ligase activity of OsPUB44 | Ishikawa et al. (2014). |
| XopQXcv | n.d. | 14-3-3 protein TFT4 (tomato, pepper, N. benthamiana) | n.d. | Teper et al. (2014) |
| 14-3-3 proteins (tomato) | n.d. | Teper et al. (2014) | ||
| XopQXoo | n.d. | n.d. | XopQXoo is present in complex with adenosine diphosphate ribose | Yu, Hwang and Rhee (2014) |
| Xoo2875 | n.d. | BAK1 (rice) | n.d. | Yamaguchi et al. (2013a) |
| Xoo1488 (XopY) | n.d. | Kinase RLCK55 (rice) | n.d. | Yamaguchi et al. (2013b) |
| Kinase RLCK185 (rice) | Suppression of CERK1-mediated phosphorylation of RLCK185 | Yamaguchi et al. (2013b) | ||
| TAL effectors g | ||||
| AvrBs3Xcv | Importin alpha (pepper) | Szurek et al. (2001) | ||
| PthA4X.citri | DNA- and RNA-binding proteins (Citrus sinensis) | de Souza et al. (2012) | ||
| Putative chromatin-associated protein HMG (Citrus sinensis) | PthA4 binds to poly(U) RNA and forms higher molecular weight complexes with poly(U) RNA in the presence of CsHMG | de Souza et al. (2012) | ||
| RNA polymerase III repressor MAF1 (Citrus sinensis) | PthA4 presumably counteracts MAF1 activity to increase transcription of host genes | Soprano et al. (2013) | ||
| PthA1, PthA2, PthA3, PthA4Xac306 | Importin alpha, cyclophilin CsCyp, thioredoxin, ubiquitin-conjugating enzyme complex (Citrus sinensis) | Inhibition of the peptidyl-prolyl cis–trans isomerase activity of cyclophilin | Domingues et al. (2010, 2012) | |
| C-terminal domain of RNA polymerase II (Citrus sinensis) | Domingues et al. (2012) | |||
| Ralstonia solanacearum | ||||
| GALA proteins (RipG family) | F box proteins | SKP1-like proteins (Arabidopsis) | n.d. | Remigi et al. (2011) |
| PopP2 (RipP2) | Acetyltransferase | WRKY domains of RRS1-R and RRS1-S (Arabidopsis) | Stabilization of RRS1-R and RRS1-S; acetylation of WRKY domains and reduced DNA binding of RRS1-R and RRS1-S; elicitation of RRS1-R-dependent ETI responses | Deslandes et al. (2003); Tasset et al. (2010); Le Roux et al. (2015); Sarris et al. (2015) |
| WRKY41, WRKY70, WRKY60, WRKY33 | Acetylation of WRKY41, WRKY70 and WRKY33 | Sarris et al. (2015) | ||
| Protease RD19 (Arabidopsis) | Relocalization of RD19 from vacuole-associated cellular compartments to the nucleus; RD19 is not acetylated by PopP2 but contributes to the RRS1-R-triggered ETI | Bernoux et al. (2008); Tasset et al. (2010) | ||
| RipTps | Trehalose phosphate synthase | n.d. | Synthesis of trehalose-6-phosphate | Poueymiro et al. (2014) |
| RipAY | γ-Glutamyl cyclo-transferase | Thioredoxins (Arabidopsis) | RipAY presumably reduces glutathione levels in eggplant; activity of RipAY is stimulated by thioredoxin AtTrx-h5 from Arabidopsis | Fujiwara et al. (2016)h |
| Degradation of glutathione; RipAY is activated by the cytosolic thioredoxins AtTrx-h1, -h2, -h4 and -h5, and the mitochondrial thioredoxin AtTrx-o1 from Arabidopsis | Mukaihara et al. (2016)i | |||
a
Alternative names of effectors are given in brackets. Xac, Xanthomonas axonopodis pv. citri; Xcc, X. campestris pv. campestris; Xcv, X. campestris pv. vesicatoria; Xfa, Xanthomonas fuscans subsp. aurantifolii; Xoo, X. oryzae pv. oryzae.
b
The plants, in which the effector targets were identified and/or studied, are given in brackets.
c
For details, see also the text.
d
n.d., not determined.
e
This result could not be reproduced in an independent study (Xiang et al.2011) (see the text for details).
f
EDS1 (enhanced disease susceptibility 1) contributes to both ETI and PTI responses and was shown to interact with the NLRs RPS4 and RPS6 (Bhattacharjee et al. 2011; Heidrich et al.2011). The interaction of EDS1 with RPS4 and RPS6 was reduced in the presence of the effector proteins AvrRps4 and HopA1 from P. syringae, which were detected in a complex with EDS1 (Bhattacharjee et al. 2011; Heidrich et al.2011). EDS1 was therefore proposed to be a guarded effector target. Notably, however, the in planta interaction of EDS1 with AvrRps4 could not be reproduced in an independent study (Sohn et al.2012).
g
TAL effectors induce the expression of plant target genes, which are summarized in Table S2.
h
First published on 1 February 2016.
i
Published on 12 April 2016.