Suppression of XopQ-XopX-induced Immune Responses of Rice by the Type III Effector XopG

Overview

Journal Mol Plant Pathol

Specialty Molecular Biology

Date 2022 Feb 12

PMID 35150038

Authors

Sohini Deb

C G Gokulan

Rajkanwar Nathawat

Hitendra K Patel

Ramesh V Sonti

Affiliations

Soon will be listed here.

Abstract

Effectors that suppress effector-triggered immunity (ETI) are an essential part of the arms race in the co-evolution of bacterial pathogens and their host plants. Xanthomonas oryzae pv. oryzae uses multiple type III secretion system (T3SS) secreted effectors such as XopU, XopV, XopP, XopG, and AvrBs2 to suppress rice immune responses that are induced by the interaction of two other effectors, XopQ and XopX. Here we show that each of these five suppressors can interact individually with both XopQ and XopX. One of the suppressors, XopG, is a predicted metallopeptidase that appears to have been introduced into X. oryzae pv. oryzae by horizontal gene transfer. XopQ and XopX interact with each other in the nucleus while interaction with XopG sequesters them in the cytoplasm. The XopG E76A and XopG E85A mutants are defective in interaction with XopQ and XopX, and are also defective in suppression of XopQ-XopX-mediated immune responses. Both mutations individually affect the virulence-promoting ability of XopG. These results indicate that XopG is important for X. oryzae pv. oryzae virulence and provide insights into the mechanisms by which this protein suppresses ETI in rice.

Citing Articles

Pangenome insights into the diversification and disease specificity of worldwide outbreaks.

Agarwal V, Stubits R, Nassrullah Z, Dillon M Front Microbiol. 2023; 14:1213261.

PMID: 37476668 PMC: 10356107. DOI: 10.3389/fmicb.2023.1213261.

Suppression of XopQ-XopX-induced immune responses of rice by the type III effector XopG.

Deb S, Gokulan C, Nathawat R, Patel H, Sonti R Mol Plant Pathol. 2022; 23(5):634-648.

PMID: 35150038 PMC: 8995061. DOI: 10.1111/mpp.13184.

References

Rohmer L, Guttman D, Dangl J . Diverse evolutionary mechanisms shape the type III effector virulence factor repertoire in the plant pathogen Pseudomonas syringae. Genetics. 2004; 167(3):1341-60. PMC: 1470954. DOI: 10.1534/genetics.103.019638. View

Gupta M, Nathawat R, Sinha D, Haque A, Sankaranarayanan R, Sonti R . Mutations in the Predicted Active Site of Xanthomonas oryzae pv. oryzae XopQ Differentially Affect Virulence, Suppression of Host Innate Immunity, and Induction of the HR in a Nonhost Plant. Mol Plant Microbe Interact. 2014; 28(2):195-206. DOI: 10.1094/MPMI-09-14-0288-R. View

Hajri A, Brin C, Hunault G, Lardeux F, Lemaire C, Manceau C . A "repertoire for repertoire" hypothesis: repertoires of type three effectors are candidate determinants of host specificity in Xanthomonas. PLoS One. 2009; 4(8):e6632. PMC: 2722093. DOI: 10.1371/journal.pone.0006632. View

Gehl C, Waadt R, Kudla J, Mendel R, Hansch R . New GATEWAY vectors for high throughput analyses of protein-protein interactions by bimolecular fluorescence complementation. Mol Plant. 2009; 2(5):1051-8. DOI: 10.1093/mp/ssp040. View

Sinha D, Gupta M, Patel H, Ranjan A, Sonti R . Cell wall degrading enzyme induced rice innate immune responses are suppressed by the type 3 secretion system effectors XopN, XopQ, XopX and XopZ of Xanthomonas oryzae pv. oryzae. PLoS One. 2013; 8(9):e75867. PMC: 3784402. DOI: 10.1371/journal.pone.0075867. View

Ma W, Dong F, Stavrinides J, Guttman D . Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genet. 2006; 2(12):e209. PMC: 1713259. DOI: 10.1371/journal.pgen.0020209. View

James P, Halladay J, Craig E . Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics. 1996; 144(4):1425-36. PMC: 1207695. DOI: 10.1093/genetics/144.4.1425. View

Block A, Toruno T, Elowsky C, Zhang C, Steinbrenner J, Beynon J . The Pseudomonas syringae type III effector HopD1 suppresses effector-triggered immunity, localizes to the endoplasmic reticulum, and targets the Arabidopsis transcription factor NTL9. New Phytol. 2013; 201(4):1358-1370. DOI: 10.1111/nph.12626. View

Madeira F, Park Y, Lee J, Buso N, Gur T, Madhusoodanan N . The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019; 47(W1):W636-W641. PMC: 6602479. DOI: 10.1093/nar/gkz268. View

10.

Hauck P, Thilmony R, He S . A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci U S A. 2003; 100(14):8577-82. PMC: 166271. DOI: 10.1073/pnas.1431173100. View

11.

Gietz R, Schiestl R . High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007; 2(1):31-4. DOI: 10.1038/nprot.2007.13. View

12.

Kosugi S, Hasebe M, Tomita M, Yanagawa H . Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A. 2009; 106(25):10171-6. PMC: 2695404. DOI: 10.1073/pnas.0900604106. View

13.

Midha S, Bansal K, Kumar S, Girija A, Mishra D, Brahma K . Population genomic insights into variation and evolution of Xanthomonas oryzae pv. oryzae. Sci Rep. 2017; 7:40694. PMC: 5233998. DOI: 10.1038/srep40694. View

14.

Deb S, Gupta M, Patel H, Sonti R . Xanthomonas oryzae pv. oryzae XopQ protein suppresses rice immune responses through interaction with two 14-3-3 proteins but its phospho-null mutant induces rice immune responses and interacts with another 14-3-3 protein. Mol Plant Pathol. 2019; 20(7):976-989. PMC: 6856769. DOI: 10.1111/mpp.12807. View

15.

Wei C, Kvitko B, Shimizu R, Crabill E, Alfano J, Lin N . A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J. 2007; 51(1):32-46. DOI: 10.1111/j.1365-313X.2007.03126.x. View

16.

Deb S, Gokulan C, Nathawat R, Patel H, Sonti R . Suppression of XopQ-XopX-induced immune responses of rice by the type III effector XopG. Mol Plant Pathol. 2022; 23(5):634-648. PMC: 8995061. DOI: 10.1111/mpp.13184. View

17.

Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R . SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018; 46(W1):W296-W303. PMC: 6030848. DOI: 10.1093/nar/gky427. View

18.

Jones J, Dangl J . The plant immune system. Nature. 2006; 444(7117):323-9. DOI: 10.1038/nature05286. View

19.

Pierce B, Wiehe K, Hwang H, Kim B, Vreven T, Weng Z . ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers. Bioinformatics. 2014; 30(12):1771-3. PMC: 4058926. DOI: 10.1093/bioinformatics/btu097. View

20.

Liu Y, Long J, Shen D, Song C . Xanthomonas oryzae pv. oryzae requires H-NS-family protein XrvC to regulate virulence during rice infection. FEMS Microbiol Lett. 2016; 363(10). DOI: 10.1093/femsle/fnw067. View