| No . | Secreted Nops . | Rhizobial strains—host species . | Putative function . | Homologs in pathogens . | Localization compartment . | Putative Associated- Host genes/Host target . | Effect on nodulation . | References . |
|---|---|---|---|---|---|---|---|---|
| (a) Rhizobial TE3s that conserved in both rhizobia and pathogenic bacteria | ||||||||
| 1 | Bel2-5 | Bradyrhizobium elkanii USDA61–nfr1 mutant, Rj4 soybeans | Cysteine protease (C48) | XopD (Xanthomonas campestris) | Nucleus | Triggers NF-independent nodulation on nfr1 mutant, but restricts nodule formation on Rj4 soybeans | Faruque et al.2015; Ratu et al.2021a, 2021b | |
| 2 | NopD | Bradyrhizobium sp. XS1105–Tephrosia vogelii | Cysteine protease (C48) | XopD (Xanthomonas campestris) | Nucleus | Suppresses nodules formation on T. vogelii | Xiang et al.2020 | |
| Sinorhizobium fredii HH103–Glycine max | Soybean F-Box/LRR-repeat (FBD/LRR) (Glyma.19g068600) and protein phosphatase 2C (PP2C) (Glyma.19g069200)* | Regulates nodulation either positively or negatively on 10 soybean germplasms tested in QTL analysis | Wang et al.2020 | |||||
| 3 | NopF | Bradyrhizobium elkanii USDA61–Lotus spp. | Acyl-CoA N-acyltransferase | HopBG1 (Pseudomonas syringae pv. maculicola ES4326) | Triggers the inhibition of USDA61 infection in Lotus spp. | Kusakabe et al.2020 | ||
| 4 | NopJ | Rhizobium sp. NGR234–Crotalaria juncea | Cysteine protease (C55) | YopJ (Yersinia pestis) AvrRxv (Xanthomonas pv. vesicatoria) | Minor negative effect on the nodulation of C. juncea | Kambara et al.2009 | ||
| 5 | NopM | Rhizobium sp. NGR234–Lablab purpureus or Lotus japonicus | E3 ubiquitin ligase | IpaH9.8, IpaH1.4 (Shigella flexneri), SspH1, SspH2, SlrP (Salomonella enterica), HpX29 (Ralstonia solanacearum) | Plasma membrane | MAPK signaling pathway | Promotes nodulation on L. purpureus, whereas reduce nodule formation of Lotus japonicus | Xin et al.2012; Xu et al.2018 |
| Bradyrhizobium sp. ORS3257–Aeschynomene indica | Positively promotes nodulation on A. indica | Teulet et al.2019 | ||||||
| Bradyrhizobium elkanii USDA61–Lotus spp. | Induces ETI-like response, thereby nodule early senescence in Lotus spp. | Kusakabe et al.2020 | ||||||
| 6 | NopT | Rhizobium sp. NGR234 –Phaseolus vulgaris, Tephrosia vogelii, Crotalaria juncea, and C. pallida | Cysteine protease (C58) | AvrPphB (Pseudomonas syringae pv. phaseolicola) YopT (Yersinia pestis) | Affects nodulation positively on P. vulgaris, T. vogelii, and suppresses nodulation of C. juncea and C. pallida | Dai et al.2008; Kambara et al.2009 | ||
| Sinorhizobium fredii USDA257 (expressing NopT of NGR234)—Glycine max | Plasma membrane | Associated with soybean protein kinases, GmPBS1-1 (Glycine max AvrPphB Susceptible 1) | Impairs nodulation in G. max cv. Nenfeng 15 | Khan et al. 2022 | ||||
| Sinorhizobium (Ensifer) fredii HH103–Glycine max | Associated with peroxidase superfamily protein (Glyma.02G135100) and aspartyl protease family protein 2 (Glyma.02G100800)* | Regulates nodulation either positively, negatively or with no effects on 30 soybean germplasms tested in QTL analysis | Liu Y et al.2021 | |||||
| Mesorhizobium amphore CCNWGS0123–Robinia pseudoacacia | Plasma membrane and nucleus | ATP-citrate synthase alpha chain protein 2 (ATP-CSACP2) and hypersensitive-induced response protein (HIRP) | Minor positive effect on the nodulation of R. pseudoacacia | Luo et al.2020 | ||||
| Bradyrhizobium sp. ORS3257–Aeschynomene indica or Vigna spp. | Promotes nodule formation V. mungo and V. unguiculata and plays lesser role on A. indica | Teulet et al.2019; Songwattana et al.2021 | ||||||
| (b) Rhizobial-specific T3Es | ||||||||
| 7 | ErnA | Bradyrhizobium sp. ORS3257–Aeschynomene indica | Rhizobium-specific | Nucleus | Triggers NF-independent nodulation and cell-division on A. indica | Teulet et al.2019 | ||
| Bradyrhizobium elkanii USDA61–nfr1 mutant soybean | Positively affects nodulation on nfr1 mutant soybean | Ratu et al.2021a | ||||||
| 8 | InnB | Bradyrhizobium elkanii USDA61–Vigna spp. | Unknown | Rhizobium-specific | Restricts nodulation on KPS1, but promotes nodulation on V. mungo | Nguyen et al.2018 | ||
| 9 | NopAA | Sinorhizobium fredii HH103–Glycine max, Vigna unguiculata | Glycoside hydrolase 12 (GH12) | Rhizobium-specific | GmARP (Glyma.19g074200)*; | Promotes rhizobial infection on soybean, but has a detrimental effect on V. unguiculata cv. Red Caloona | Jiménez-Guerrero et al.2019; Dorival et al.2020; Wang et al.2022 | |
| 10 | NopAB | Bradyrhizobium sp. ORS3257–Aeschynomene indica or Vigna spp. | Unknown | Rhizobium-specific | Promotes nodules formation on V. mungo and V. unguiculata and plays lesser role on A. indica | Teulet et al.2019; Songwattana et al.2021 | ||
| 11 | NopC | Sinorhizobium fredii HH103–Glycine max, Vigna unguiculata, Lotus japonicus GIFU | Unknown | Rhizobium-specific | Positively affects nodulation on G. max cv. William 82 and Vigna unguiculata, but blocks nodulation on Lotus japonicus GIFU | Jiménez-Guerrero et al.2015, 2020 | ||
| 12 | NopE | Bradyrhizobium diazoefficiens USDA110–Vigna spp. Glycine max. Macroptilium atropurpureum | Calcium binding protein | Rhizobium-specific | Promotes nodulation on G. max, M. atropurpureum, and V. radiata cv. KPS1, but has negative effect on V. radiata cv. KPS2 via SA-mediated ETI-responses | Wenzel et al.2010; Piromyou et al.2021 | ||
| 13 | NopL | Sinorhizobium fredii NGR234–Phaseolus vulgaris, Flemingia congesta | Protein phosphorylation | Rhizobium-specific | Nucleus | MAP Kinase | Suppresses the expression of pathogenesis-related (PR) proteins on L. japonicus, inhibits P. vulgaris nodule-senescence, promotes nodulation of F. congesta | Marie et al.2003; Bartsev et al.2004; Zhang et al.2011; |
| Bradyrhizobium elkanii USDA61–nfr1 mutant soybean | Positively affects nodulation on nfr1 mutant soybean | Ratu et al.2021a | ||||||
| 14 | NopP | Rhizobium sp. NGR234–Vigna unguiculata, Flemingia congesta, Tephrosia vogelii | Protein phosphorylation | Rhizobium-specific | Promotes nodulation on F. congesta and T. vogelii but inhibits nodulation on V. unguiculata | Ausmees et al.2004; Skorpil et al.2005 | ||
| Bradyrhizobium USDA110–Glycine max | Endoplasmic reticulum (ER) | GmNNL1 | Inhibits root hair infection on soybean carrying GmNNL1 | Zhang et al.2021 | ||||
| Bradyrhizobium diazoefficiens USDA122–Glycine max | Severely restricts nodulation with Rj2-soybean via ETI-like responses | Sugawara et al.2018 | ||||||
| Sinorhizobium fredii HH103–Glycine max | Associated with pathogenesis-related 5 (PR5) family (Glyma.12g031200) and mitogen-activated protein kinase 3 (MAPK3) (Glyma.12g073000)* | Regulates nodulation either positively or negatively on 10 soybean germplasms tested in QTL analysis | Wang et al.2018 | |||||
| Mesorhizobium amorphae—Robinia pseudoacacia | Plasma membrane | Trafficking protein particle complex subunit 13–like protein (TRAPPC13) | Plays roles at the early stage of M. amorphae infection. Minor positive effect on nodule biomass, but significantly promotes N-fixing activity of M. amorphae on R. pseudoacacia | Liu D et al.2021 | ||||
| No . | Secreted Nops . | Rhizobial strains—host species . | Putative function . | Homologs in pathogens . | Localization compartment . | Putative Associated- Host genes/Host target . | Effect on nodulation . | References . |
|---|---|---|---|---|---|---|---|---|
| (a) Rhizobial TE3s that conserved in both rhizobia and pathogenic bacteria | ||||||||
| 1 | Bel2-5 | Bradyrhizobium elkanii USDA61–nfr1 mutant, Rj4 soybeans | Cysteine protease (C48) | XopD (Xanthomonas campestris) | Nucleus | Triggers NF-independent nodulation on nfr1 mutant, but restricts nodule formation on Rj4 soybeans | Faruque et al.2015; Ratu et al.2021a, 2021b | |
| 2 | NopD | Bradyrhizobium sp. XS1105–Tephrosia vogelii | Cysteine protease (C48) | XopD (Xanthomonas campestris) | Nucleus | Suppresses nodules formation on T. vogelii | Xiang et al.2020 | |
| Sinorhizobium fredii HH103–Glycine max | Soybean F-Box/LRR-repeat (FBD/LRR) (Glyma.19g068600) and protein phosphatase 2C (PP2C) (Glyma.19g069200)* | Regulates nodulation either positively or negatively on 10 soybean germplasms tested in QTL analysis | Wang et al.2020 | |||||
| 3 | NopF | Bradyrhizobium elkanii USDA61–Lotus spp. | Acyl-CoA N-acyltransferase | HopBG1 (Pseudomonas syringae pv. maculicola ES4326) | Triggers the inhibition of USDA61 infection in Lotus spp. | Kusakabe et al.2020 | ||
| 4 | NopJ | Rhizobium sp. NGR234–Crotalaria juncea | Cysteine protease (C55) | YopJ (Yersinia pestis) AvrRxv (Xanthomonas pv. vesicatoria) | Minor negative effect on the nodulation of C. juncea | Kambara et al.2009 | ||
| 5 | NopM | Rhizobium sp. NGR234–Lablab purpureus or Lotus japonicus | E3 ubiquitin ligase | IpaH9.8, IpaH1.4 (Shigella flexneri), SspH1, SspH2, SlrP (Salomonella enterica), HpX29 (Ralstonia solanacearum) | Plasma membrane | MAPK signaling pathway | Promotes nodulation on L. purpureus, whereas reduce nodule formation of Lotus japonicus | Xin et al.2012; Xu et al.2018 |
| Bradyrhizobium sp. ORS3257–Aeschynomene indica | Positively promotes nodulation on A. indica | Teulet et al.2019 | ||||||
| Bradyrhizobium elkanii USDA61–Lotus spp. | Induces ETI-like response, thereby nodule early senescence in Lotus spp. | Kusakabe et al.2020 | ||||||
| 6 | NopT | Rhizobium sp. NGR234 –Phaseolus vulgaris, Tephrosia vogelii, Crotalaria juncea, and C. pallida | Cysteine protease (C58) | AvrPphB (Pseudomonas syringae pv. phaseolicola) YopT (Yersinia pestis) | Affects nodulation positively on P. vulgaris, T. vogelii, and suppresses nodulation of C. juncea and C. pallida | Dai et al.2008; Kambara et al.2009 | ||
| Sinorhizobium fredii USDA257 (expressing NopT of NGR234)—Glycine max | Plasma membrane | Associated with soybean protein kinases, GmPBS1-1 (Glycine max AvrPphB Susceptible 1) | Impairs nodulation in G. max cv. Nenfeng 15 | Khan et al. 2022 | ||||
| Sinorhizobium (Ensifer) fredii HH103–Glycine max | Associated with peroxidase superfamily protein (Glyma.02G135100) and aspartyl protease family protein 2 (Glyma.02G100800)* | Regulates nodulation either positively, negatively or with no effects on 30 soybean germplasms tested in QTL analysis | Liu Y et al.2021 | |||||
| Mesorhizobium amphore CCNWGS0123–Robinia pseudoacacia | Plasma membrane and nucleus | ATP-citrate synthase alpha chain protein 2 (ATP-CSACP2) and hypersensitive-induced response protein (HIRP) | Minor positive effect on the nodulation of R. pseudoacacia | Luo et al.2020 | ||||
| Bradyrhizobium sp. ORS3257–Aeschynomene indica or Vigna spp. | Promotes nodule formation V. mungo and V. unguiculata and plays lesser role on A. indica | Teulet et al.2019; Songwattana et al.2021 | ||||||
| (b) Rhizobial-specific T3Es | ||||||||
| 7 | ErnA | Bradyrhizobium sp. ORS3257–Aeschynomene indica | Rhizobium-specific | Nucleus | Triggers NF-independent nodulation and cell-division on A. indica | Teulet et al.2019 | ||
| Bradyrhizobium elkanii USDA61–nfr1 mutant soybean | Positively affects nodulation on nfr1 mutant soybean | Ratu et al.2021a | ||||||
| 8 | InnB | Bradyrhizobium elkanii USDA61–Vigna spp. | Unknown | Rhizobium-specific | Restricts nodulation on KPS1, but promotes nodulation on V. mungo | Nguyen et al.2018 | ||
| 9 | NopAA | Sinorhizobium fredii HH103–Glycine max, Vigna unguiculata | Glycoside hydrolase 12 (GH12) | Rhizobium-specific | GmARP (Glyma.19g074200)*; | Promotes rhizobial infection on soybean, but has a detrimental effect on V. unguiculata cv. Red Caloona | Jiménez-Guerrero et al.2019; Dorival et al.2020; Wang et al.2022 | |
| 10 | NopAB | Bradyrhizobium sp. ORS3257–Aeschynomene indica or Vigna spp. | Unknown | Rhizobium-specific | Promotes nodules formation on V. mungo and V. unguiculata and plays lesser role on A. indica | Teulet et al.2019; Songwattana et al.2021 | ||
| 11 | NopC | Sinorhizobium fredii HH103–Glycine max, Vigna unguiculata, Lotus japonicus GIFU | Unknown | Rhizobium-specific | Positively affects nodulation on G. max cv. William 82 and Vigna unguiculata, but blocks nodulation on Lotus japonicus GIFU | Jiménez-Guerrero et al.2015, 2020 | ||
| 12 | NopE | Bradyrhizobium diazoefficiens USDA110–Vigna spp. Glycine max. Macroptilium atropurpureum | Calcium binding protein | Rhizobium-specific | Promotes nodulation on G. max, M. atropurpureum, and V. radiata cv. KPS1, but has negative effect on V. radiata cv. KPS2 via SA-mediated ETI-responses | Wenzel et al.2010; Piromyou et al.2021 | ||
| 13 | NopL | Sinorhizobium fredii NGR234–Phaseolus vulgaris, Flemingia congesta | Protein phosphorylation | Rhizobium-specific | Nucleus | MAP Kinase | Suppresses the expression of pathogenesis-related (PR) proteins on L. japonicus, inhibits P. vulgaris nodule-senescence, promotes nodulation of F. congesta | Marie et al.2003; Bartsev et al.2004; Zhang et al.2011; |
| Bradyrhizobium elkanii USDA61–nfr1 mutant soybean | Positively affects nodulation on nfr1 mutant soybean | Ratu et al.2021a | ||||||
| 14 | NopP | Rhizobium sp. NGR234–Vigna unguiculata, Flemingia congesta, Tephrosia vogelii | Protein phosphorylation | Rhizobium-specific | Promotes nodulation on F. congesta and T. vogelii but inhibits nodulation on V. unguiculata | Ausmees et al.2004; Skorpil et al.2005 | ||
| Bradyrhizobium USDA110–Glycine max | Endoplasmic reticulum (ER) | GmNNL1 | Inhibits root hair infection on soybean carrying GmNNL1 | Zhang et al.2021 | ||||
| Bradyrhizobium diazoefficiens USDA122–Glycine max | Severely restricts nodulation with Rj2-soybean via ETI-like responses | Sugawara et al.2018 | ||||||
| Sinorhizobium fredii HH103–Glycine max | Associated with pathogenesis-related 5 (PR5) family (Glyma.12g031200) and mitogen-activated protein kinase 3 (MAPK3) (Glyma.12g073000)* | Regulates nodulation either positively or negatively on 10 soybean germplasms tested in QTL analysis | Wang et al.2018 | |||||
| Mesorhizobium amorphae—Robinia pseudoacacia | Plasma membrane | Trafficking protein particle complex subunit 13–like protein (TRAPPC13) | Plays roles at the early stage of M. amorphae infection. Minor positive effect on nodule biomass, but significantly promotes N-fixing activity of M. amorphae on R. pseudoacacia | Liu D et al.2021 | ||||
* means putative associated-host gene/host target of effector was identified by the Quantitative trait locus (QTL) analysis on the respective host
| No . | Secreted Nops . | Rhizobial strains—host species . | Putative function . | Homologs in pathogens . | Localization compartment . | Putative Associated- Host genes/Host target . | Effect on nodulation . | References . |
|---|---|---|---|---|---|---|---|---|
| (a) Rhizobial TE3s that conserved in both rhizobia and pathogenic bacteria | ||||||||
| 1 | Bel2-5 | Bradyrhizobium elkanii USDA61–nfr1 mutant, Rj4 soybeans | Cysteine protease (C48) | XopD (Xanthomonas campestris) | Nucleus | Triggers NF-independent nodulation on nfr1 mutant, but restricts nodule formation on Rj4 soybeans | Faruque et al.2015; Ratu et al.2021a, 2021b | |
| 2 | NopD | Bradyrhizobium sp. XS1105–Tephrosia vogelii | Cysteine protease (C48) | XopD (Xanthomonas campestris) | Nucleus | Suppresses nodules formation on T. vogelii | Xiang et al.2020 | |
| Sinorhizobium fredii HH103–Glycine max | Soybean F-Box/LRR-repeat (FBD/LRR) (Glyma.19g068600) and protein phosphatase 2C (PP2C) (Glyma.19g069200)* | Regulates nodulation either positively or negatively on 10 soybean germplasms tested in QTL analysis | Wang et al.2020 | |||||
| 3 | NopF | Bradyrhizobium elkanii USDA61–Lotus spp. | Acyl-CoA N-acyltransferase | HopBG1 (Pseudomonas syringae pv. maculicola ES4326) | Triggers the inhibition of USDA61 infection in Lotus spp. | Kusakabe et al.2020 | ||
| 4 | NopJ | Rhizobium sp. NGR234–Crotalaria juncea | Cysteine protease (C55) | YopJ (Yersinia pestis) AvrRxv (Xanthomonas pv. vesicatoria) | Minor negative effect on the nodulation of C. juncea | Kambara et al.2009 | ||
| 5 | NopM | Rhizobium sp. NGR234–Lablab purpureus or Lotus japonicus | E3 ubiquitin ligase | IpaH9.8, IpaH1.4 (Shigella flexneri), SspH1, SspH2, SlrP (Salomonella enterica), HpX29 (Ralstonia solanacearum) | Plasma membrane | MAPK signaling pathway | Promotes nodulation on L. purpureus, whereas reduce nodule formation of Lotus japonicus | Xin et al.2012; Xu et al.2018 |
| Bradyrhizobium sp. ORS3257–Aeschynomene indica | Positively promotes nodulation on A. indica | Teulet et al.2019 | ||||||
| Bradyrhizobium elkanii USDA61–Lotus spp. | Induces ETI-like response, thereby nodule early senescence in Lotus spp. | Kusakabe et al.2020 | ||||||
| 6 | NopT | Rhizobium sp. NGR234 –Phaseolus vulgaris, Tephrosia vogelii, Crotalaria juncea, and C. pallida | Cysteine protease (C58) | AvrPphB (Pseudomonas syringae pv. phaseolicola) YopT (Yersinia pestis) | Affects nodulation positively on P. vulgaris, T. vogelii, and suppresses nodulation of C. juncea and C. pallida | Dai et al.2008; Kambara et al.2009 | ||
| Sinorhizobium fredii USDA257 (expressing NopT of NGR234)—Glycine max | Plasma membrane | Associated with soybean protein kinases, GmPBS1-1 (Glycine max AvrPphB Susceptible 1) | Impairs nodulation in G. max cv. Nenfeng 15 | Khan et al. 2022 | ||||
| Sinorhizobium (Ensifer) fredii HH103–Glycine max | Associated with peroxidase superfamily protein (Glyma.02G135100) and aspartyl protease family protein 2 (Glyma.02G100800)* | Regulates nodulation either positively, negatively or with no effects on 30 soybean germplasms tested in QTL analysis | Liu Y et al.2021 | |||||
| Mesorhizobium amphore CCNWGS0123–Robinia pseudoacacia | Plasma membrane and nucleus | ATP-citrate synthase alpha chain protein 2 (ATP-CSACP2) and hypersensitive-induced response protein (HIRP) | Minor positive effect on the nodulation of R. pseudoacacia | Luo et al.2020 | ||||
| Bradyrhizobium sp. ORS3257–Aeschynomene indica or Vigna spp. | Promotes nodule formation V. mungo and V. unguiculata and plays lesser role on A. indica | Teulet et al.2019; Songwattana et al.2021 | ||||||
| (b) Rhizobial-specific T3Es | ||||||||
| 7 | ErnA | Bradyrhizobium sp. ORS3257–Aeschynomene indica | Rhizobium-specific | Nucleus | Triggers NF-independent nodulation and cell-division on A. indica | Teulet et al.2019 | ||
| Bradyrhizobium elkanii USDA61–nfr1 mutant soybean | Positively affects nodulation on nfr1 mutant soybean | Ratu et al.2021a | ||||||
| 8 | InnB | Bradyrhizobium elkanii USDA61–Vigna spp. | Unknown | Rhizobium-specific | Restricts nodulation on KPS1, but promotes nodulation on V. mungo | Nguyen et al.2018 | ||
| 9 | NopAA | Sinorhizobium fredii HH103–Glycine max, Vigna unguiculata | Glycoside hydrolase 12 (GH12) | Rhizobium-specific | GmARP (Glyma.19g074200)*; | Promotes rhizobial infection on soybean, but has a detrimental effect on V. unguiculata cv. Red Caloona | Jiménez-Guerrero et al.2019; Dorival et al.2020; Wang et al.2022 | |
| 10 | NopAB | Bradyrhizobium sp. ORS3257–Aeschynomene indica or Vigna spp. | Unknown | Rhizobium-specific | Promotes nodules formation on V. mungo and V. unguiculata and plays lesser role on A. indica | Teulet et al.2019; Songwattana et al.2021 | ||
| 11 | NopC | Sinorhizobium fredii HH103–Glycine max, Vigna unguiculata, Lotus japonicus GIFU | Unknown | Rhizobium-specific | Positively affects nodulation on G. max cv. William 82 and Vigna unguiculata, but blocks nodulation on Lotus japonicus GIFU | Jiménez-Guerrero et al.2015, 2020 | ||
| 12 | NopE | Bradyrhizobium diazoefficiens USDA110–Vigna spp. Glycine max. Macroptilium atropurpureum | Calcium binding protein | Rhizobium-specific | Promotes nodulation on G. max, M. atropurpureum, and V. radiata cv. KPS1, but has negative effect on V. radiata cv. KPS2 via SA-mediated ETI-responses | Wenzel et al.2010; Piromyou et al.2021 | ||
| 13 | NopL | Sinorhizobium fredii NGR234–Phaseolus vulgaris, Flemingia congesta | Protein phosphorylation | Rhizobium-specific | Nucleus | MAP Kinase | Suppresses the expression of pathogenesis-related (PR) proteins on L. japonicus, inhibits P. vulgaris nodule-senescence, promotes nodulation of F. congesta | Marie et al.2003; Bartsev et al.2004; Zhang et al.2011; |
| Bradyrhizobium elkanii USDA61–nfr1 mutant soybean | Positively affects nodulation on nfr1 mutant soybean | Ratu et al.2021a | ||||||
| 14 | NopP | Rhizobium sp. NGR234–Vigna unguiculata, Flemingia congesta, Tephrosia vogelii | Protein phosphorylation | Rhizobium-specific | Promotes nodulation on F. congesta and T. vogelii but inhibits nodulation on V. unguiculata | Ausmees et al.2004; Skorpil et al.2005 | ||
| Bradyrhizobium USDA110–Glycine max | Endoplasmic reticulum (ER) | GmNNL1 | Inhibits root hair infection on soybean carrying GmNNL1 | Zhang et al.2021 | ||||
| Bradyrhizobium diazoefficiens USDA122–Glycine max | Severely restricts nodulation with Rj2-soybean via ETI-like responses | Sugawara et al.2018 | ||||||
| Sinorhizobium fredii HH103–Glycine max | Associated with pathogenesis-related 5 (PR5) family (Glyma.12g031200) and mitogen-activated protein kinase 3 (MAPK3) (Glyma.12g073000)* | Regulates nodulation either positively or negatively on 10 soybean germplasms tested in QTL analysis | Wang et al.2018 | |||||
| Mesorhizobium amorphae—Robinia pseudoacacia | Plasma membrane | Trafficking protein particle complex subunit 13–like protein (TRAPPC13) | Plays roles at the early stage of M. amorphae infection. Minor positive effect on nodule biomass, but significantly promotes N-fixing activity of M. amorphae on R. pseudoacacia | Liu D et al.2021 | ||||
| No . | Secreted Nops . | Rhizobial strains—host species . | Putative function . | Homologs in pathogens . | Localization compartment . | Putative Associated- Host genes/Host target . | Effect on nodulation . | References . |
|---|---|---|---|---|---|---|---|---|
| (a) Rhizobial TE3s that conserved in both rhizobia and pathogenic bacteria | ||||||||
| 1 | Bel2-5 | Bradyrhizobium elkanii USDA61–nfr1 mutant, Rj4 soybeans | Cysteine protease (C48) | XopD (Xanthomonas campestris) | Nucleus | Triggers NF-independent nodulation on nfr1 mutant, but restricts nodule formation on Rj4 soybeans | Faruque et al.2015; Ratu et al.2021a, 2021b | |
| 2 | NopD | Bradyrhizobium sp. XS1105–Tephrosia vogelii | Cysteine protease (C48) | XopD (Xanthomonas campestris) | Nucleus | Suppresses nodules formation on T. vogelii | Xiang et al.2020 | |
| Sinorhizobium fredii HH103–Glycine max | Soybean F-Box/LRR-repeat (FBD/LRR) (Glyma.19g068600) and protein phosphatase 2C (PP2C) (Glyma.19g069200)* | Regulates nodulation either positively or negatively on 10 soybean germplasms tested in QTL analysis | Wang et al.2020 | |||||
| 3 | NopF | Bradyrhizobium elkanii USDA61–Lotus spp. | Acyl-CoA N-acyltransferase | HopBG1 (Pseudomonas syringae pv. maculicola ES4326) | Triggers the inhibition of USDA61 infection in Lotus spp. | Kusakabe et al.2020 | ||
| 4 | NopJ | Rhizobium sp. NGR234–Crotalaria juncea | Cysteine protease (C55) | YopJ (Yersinia pestis) AvrRxv (Xanthomonas pv. vesicatoria) | Minor negative effect on the nodulation of C. juncea | Kambara et al.2009 | ||
| 5 | NopM | Rhizobium sp. NGR234–Lablab purpureus or Lotus japonicus | E3 ubiquitin ligase | IpaH9.8, IpaH1.4 (Shigella flexneri), SspH1, SspH2, SlrP (Salomonella enterica), HpX29 (Ralstonia solanacearum) | Plasma membrane | MAPK signaling pathway | Promotes nodulation on L. purpureus, whereas reduce nodule formation of Lotus japonicus | Xin et al.2012; Xu et al.2018 |
| Bradyrhizobium sp. ORS3257–Aeschynomene indica | Positively promotes nodulation on A. indica | Teulet et al.2019 | ||||||
| Bradyrhizobium elkanii USDA61–Lotus spp. | Induces ETI-like response, thereby nodule early senescence in Lotus spp. | Kusakabe et al.2020 | ||||||
| 6 | NopT | Rhizobium sp. NGR234 –Phaseolus vulgaris, Tephrosia vogelii, Crotalaria juncea, and C. pallida | Cysteine protease (C58) | AvrPphB (Pseudomonas syringae pv. phaseolicola) YopT (Yersinia pestis) | Affects nodulation positively on P. vulgaris, T. vogelii, and suppresses nodulation of C. juncea and C. pallida | Dai et al.2008; Kambara et al.2009 | ||
| Sinorhizobium fredii USDA257 (expressing NopT of NGR234)—Glycine max | Plasma membrane | Associated with soybean protein kinases, GmPBS1-1 (Glycine max AvrPphB Susceptible 1) | Impairs nodulation in G. max cv. Nenfeng 15 | Khan et al. 2022 | ||||
| Sinorhizobium (Ensifer) fredii HH103–Glycine max | Associated with peroxidase superfamily protein (Glyma.02G135100) and aspartyl protease family protein 2 (Glyma.02G100800)* | Regulates nodulation either positively, negatively or with no effects on 30 soybean germplasms tested in QTL analysis | Liu Y et al.2021 | |||||
| Mesorhizobium amphore CCNWGS0123–Robinia pseudoacacia | Plasma membrane and nucleus | ATP-citrate synthase alpha chain protein 2 (ATP-CSACP2) and hypersensitive-induced response protein (HIRP) | Minor positive effect on the nodulation of R. pseudoacacia | Luo et al.2020 | ||||
| Bradyrhizobium sp. ORS3257–Aeschynomene indica or Vigna spp. | Promotes nodule formation V. mungo and V. unguiculata and plays lesser role on A. indica | Teulet et al.2019; Songwattana et al.2021 | ||||||
| (b) Rhizobial-specific T3Es | ||||||||
| 7 | ErnA | Bradyrhizobium sp. ORS3257–Aeschynomene indica | Rhizobium-specific | Nucleus | Triggers NF-independent nodulation and cell-division on A. indica | Teulet et al.2019 | ||
| Bradyrhizobium elkanii USDA61–nfr1 mutant soybean | Positively affects nodulation on nfr1 mutant soybean | Ratu et al.2021a | ||||||
| 8 | InnB | Bradyrhizobium elkanii USDA61–Vigna spp. | Unknown | Rhizobium-specific | Restricts nodulation on KPS1, but promotes nodulation on V. mungo | Nguyen et al.2018 | ||
| 9 | NopAA | Sinorhizobium fredii HH103–Glycine max, Vigna unguiculata | Glycoside hydrolase 12 (GH12) | Rhizobium-specific | GmARP (Glyma.19g074200)*; | Promotes rhizobial infection on soybean, but has a detrimental effect on V. unguiculata cv. Red Caloona | Jiménez-Guerrero et al.2019; Dorival et al.2020; Wang et al.2022 | |
| 10 | NopAB | Bradyrhizobium sp. ORS3257–Aeschynomene indica or Vigna spp. | Unknown | Rhizobium-specific | Promotes nodules formation on V. mungo and V. unguiculata and plays lesser role on A. indica | Teulet et al.2019; Songwattana et al.2021 | ||
| 11 | NopC | Sinorhizobium fredii HH103–Glycine max, Vigna unguiculata, Lotus japonicus GIFU | Unknown | Rhizobium-specific | Positively affects nodulation on G. max cv. William 82 and Vigna unguiculata, but blocks nodulation on Lotus japonicus GIFU | Jiménez-Guerrero et al.2015, 2020 | ||
| 12 | NopE | Bradyrhizobium diazoefficiens USDA110–Vigna spp. Glycine max. Macroptilium atropurpureum | Calcium binding protein | Rhizobium-specific | Promotes nodulation on G. max, M. atropurpureum, and V. radiata cv. KPS1, but has negative effect on V. radiata cv. KPS2 via SA-mediated ETI-responses | Wenzel et al.2010; Piromyou et al.2021 | ||
| 13 | NopL | Sinorhizobium fredii NGR234–Phaseolus vulgaris, Flemingia congesta | Protein phosphorylation | Rhizobium-specific | Nucleus | MAP Kinase | Suppresses the expression of pathogenesis-related (PR) proteins on L. japonicus, inhibits P. vulgaris nodule-senescence, promotes nodulation of F. congesta | Marie et al.2003; Bartsev et al.2004; Zhang et al.2011; |
| Bradyrhizobium elkanii USDA61–nfr1 mutant soybean | Positively affects nodulation on nfr1 mutant soybean | Ratu et al.2021a | ||||||
| 14 | NopP | Rhizobium sp. NGR234–Vigna unguiculata, Flemingia congesta, Tephrosia vogelii | Protein phosphorylation | Rhizobium-specific | Promotes nodulation on F. congesta and T. vogelii but inhibits nodulation on V. unguiculata | Ausmees et al.2004; Skorpil et al.2005 | ||
| Bradyrhizobium USDA110–Glycine max | Endoplasmic reticulum (ER) | GmNNL1 | Inhibits root hair infection on soybean carrying GmNNL1 | Zhang et al.2021 | ||||
| Bradyrhizobium diazoefficiens USDA122–Glycine max | Severely restricts nodulation with Rj2-soybean via ETI-like responses | Sugawara et al.2018 | ||||||
| Sinorhizobium fredii HH103–Glycine max | Associated with pathogenesis-related 5 (PR5) family (Glyma.12g031200) and mitogen-activated protein kinase 3 (MAPK3) (Glyma.12g073000)* | Regulates nodulation either positively or negatively on 10 soybean germplasms tested in QTL analysis | Wang et al.2018 | |||||
| Mesorhizobium amorphae—Robinia pseudoacacia | Plasma membrane | Trafficking protein particle complex subunit 13–like protein (TRAPPC13) | Plays roles at the early stage of M. amorphae infection. Minor positive effect on nodule biomass, but significantly promotes N-fixing activity of M. amorphae on R. pseudoacacia | Liu D et al.2021 | ||||
* means putative associated-host gene/host target of effector was identified by the Quantitative trait locus (QTL) analysis on the respective host
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