.png){kind=logo}
Bacteriology
Host-Driven Selection, Revealed by Comparative Analysis of Xanthomonas Type III Secretion Effectoromes, Unveils Novel Recognized Effectors
AffiliationsAuthors and Affiliations
- Yao Xiao1 2
- Shatrupa Ray1
- Saul Burdman2
- Doron Teper1 †
- 1Department of Plant Pathology and Weed Research, Agricultural Research Organization–Volcani Institute, Rishon LeZion, Israel
- 2Department of Plant Pathology and Microbiology, The Hebrew University of Jerusalem, Rehovot, Israel
Published Online:16 Oct 2024https://doi.org/10.1094/PHYTO-04-24-0147-R
Abstract
Xanthomonas species are specialized plant pathogens, often exhibiting a narrow host range. They rely on the translocation of effector proteins through the type III secretion system to colonize their respective hosts. The effector arsenal varies among Xanthomonas spp., typically displaying species-specific compositions. This species-specific effector composition, collectively termed the effectorome, is thought to influence host specialization. We determined the plant host-derived effectoromes of more than 300 deposited genomes of Xanthomonas species associated with either Solanaceae or Brassicaceae hosts. Comparative analyses revealed clear species-specific effectorome signatures. However, Solanaceae or Brassicaceae host-associated effectorome signatures were not detected. Nevertheless, host biases in the presence or absence of specific effector classes were observed. To assess whether host-associated effector absence results from selective pressures, we introduced effectors unique to Solanaceae pathogens to X. campestris pv. campestris and effectors unique to Brassicaceae pathogens to X. euvesicatoria pv. euvesicatoria (Xeue) and evaluated if these introductions hindered virulence on their respective hosts. Introducing the effector XopI into X. campestris pv. campestris reduced virulence on white cabbage leaves without affecting localized or systemic colonization. Introducing the XopAC or XopJ5 effectors into Xeue reduced virulence and colonization on tomato but not on pepper. Additionally, XopAC and XopJ5 induced a hypersensitive response on tomato leaves when delivered by Xeue or through Agrobacterium-mediated transient expression, confirming recognition in tomato. This study demonstrates the role of host-derived selection in establishing species-specific effectoromes, identifying XopAC and XopJ5 as recognized effectors in tomato.
Literature Cited
- 2020. Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas. FEMS Microbiol. Rev. 44:1-32. https://doi.org/10.1093/femsre/fuz024 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2020. From effectors to effectomes: Are functional studies of individual effectors enough to decipher plant pathogen infectious strategies? PLoS Pathog. 16:e1009059. https://doi.org/10.1371/journal.ppat.1009059 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2019. The plant hypersensitive response: Concepts, control and consequences. Mol. Plant Pathol. 20:1163-1178. https://doi.org/10.1111/mpp.12821 CrossrefMedlineWeb of ScienceGoogle Scholar
- 1999. Gene-for-gene interactions: Bacterial avirulence proteins specify plant disease resistance. Curr. Opin. Microbiol. 2:94-98. https://doi.org/10.1016/S1369-5274(99)80016-2 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2022. Diversity, evolution, and function of Pseudomonas syringae effectoromes. Annu. Rev. Phytopathol. 60:211-236. https://doi.org/10.1146/annurev-phyto-021621-121935 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2010. Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol. Rev. 34:107-133. https://doi.org/10.1111/j.1574-6976.2009.00192.x CrossrefMedlineWeb of ScienceGoogle Scholar
- 2006. Targeting of two effector protein classes to the type III secretion system by a HpaC- and HpaB-dependent protein complex from Xanthomonas campestris pv. vesicatoria. Mol. Microbiol. 59:513-527. https://doi.org/10.1111/j.1365-2958.2005.04924.x CrossrefMedlineWeb of ScienceGoogle Scholar
CABI . 2022. Xanthomonas campestris pv. campestris (black rot). PlantwisePlus Knowledge Bank. https://doi.org/10.1079/pwkb.species.56919 Google Scholar- 2017. Immunity at cauliflower hydathodes controls systemic infection by Xanthomonas campestris pv. campestris. Plant Physiol. 174:700-716. https://doi.org/10.1104/pp.16.01852 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2024. Exploring the genetic makeup of Xanthomonas species causing bacterial spot in Taiwan: Evidence of population shift and local adaptation. Front. Microbiol. 15:1408885. https://doi.org/10.3389/fmicb.2024.1408885 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2014. AvrBsT Acetylates Arabidopsis ACIP1, a protein that associates with microtubules and is required for immunity. PLoS Pathog. 10:e1003952. https://doi.org/10.1371/journal.ppat.1003952 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2014. Eggplant and related species are promising genetic resources to dissect the plant immune response to Pseudomonas syringae and Xanthomonas euvesicatoria and to identify new resistance determinants. Mol. Plant Pathol. 15:814-822. https://doi.org/10.1111/mpp.12140 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2024. A community-curated DokuWiki resource on diagnostics, diversity, pathogenicity and genetic control of Xanthomonads. Mol. Plant-Microbe Interact. 37:347-353. https://doi.org/10.1094/MPMI-11-23-0184-FI LinkWeb of ScienceGoogle Scholar
- 2019. Phylogenetic analyses of xanthomonads causing bacterial leaf spot of tomato and pepper: Xanthomonas euvesicatoria revealed homologous populations despite distant geographical distribution. Microorganisms 7:462. https://doi.org/10.3390/microorganisms7100462 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2021. Genomic insights advance the fight against black rot of crucifers. J. Gen. Plant Pathol. 87:127-136. https://doi.org/10.1007/s10327-021-00987-x CrossrefWeb of ScienceGoogle Scholar
- 2022. Cruciferous weed isolates of Xanthomonas campestris yield insight into pathovar genomic relationships and genetic determinants of host and tissue specificity. Mol. Plant-Microbe Interact. 35:791-802. https://doi.org/10.1094/MPMI-01-22-0024-R LinkWeb of ScienceGoogle Scholar
- 2022. Identification of genes in Xanthomonas euvesicatoria pv. rosa that are host limiting in tomato. Plants 11:796. https://doi.org/10.3390/plants11060796 CrossrefGoogle Scholar
- 1998. Recognition specificity for the bacterial avirulence protein AvrPto is determined by Thr-204 in the activation loop of the tomato Pto kinase. Mol. Cell 2:241-245. https://doi.org/10.1016/S1097-2765(00)80134-3 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2022. The origin and evolution of a plant resistosome. Plant Cell 34:1600-1620. https://doi.org/10.1093/plcell/koac053 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2013. xopAC-triggered Immunity against Xanthomonas depends on Arabidopsis receptor-like cytoplasmic kinase genes PBL2 and RIPK. PLoS One 8:e73469. https://doi.org/10.1371/journal.pone.0073469 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2022. A vector system for fast-forward studies of the HOPZ-ACTIVATED RESISTANCE1 (ZAR1) resistosome in the model plant Nicotiana benthamiana. Plant Physiol. 188:70-80. https://doi.org/10.1093/plphys/kiab471 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2016. Using ecology, physiology, and genomics to understand host specificity in Xanthomonas. Annu. Rev. Phytopathol. 54:163-187. https://doi.org/10.1146/annurev-phyto-080615-100147 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2013. Complete genome sequence of Xanthomonas citri subsp. citri Strain Aw12879, a restricted-host-range citrus canker-causing bacterium. Genome Announc. 1:e00235-13. https://doi.org/10.1128/genomeA.00235-13 CrossrefMedlineGoogle Scholar
- 2020. A bacterial F-box effector suppresses SAR immunity through mediating the proteasomal degradation of OsTrxh2 in rice. Plant J. 104:1054-1072. https://doi.org/10.1111/tpj.14980 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2013. Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host Microbe 13:143-154. https://doi.org/10.1016/j.chom.2013.01.006 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2010. Xanthomonas campestris pv. vesicatoria effector AvrBsT induces cell death in pepper, but suppresses defense responses in tomato. Mol. Plant-Microbe Interact. 23:1069-1082. https://doi.org/10.1094/MPMI-23-8-1069 LinkWeb of ScienceGoogle Scholar
- 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176. https://doi.org/10.1016/0378-1119(95)00584-1 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2023. Discovery of the Hrp Type III secretion system in phytopathogenic bacteria: How investigation of hypersensitive cell death in plants led to a novel protein injector system and a world of inter-organismal molecular interactions within plant cells. Phytopathology 113:626-636. https://doi.org/10.1094/PHYTO-08-22-0292-KD LinkWeb of ScienceGoogle Scholar
- 2020. The pan-genome effector-triggered immunity landscape of a host-pathogen interaction. Science 367:763-768. https://doi.org/10.1126/science.aax4079 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2024. Bacterial host adaptation through sequence and structural variations of a single type III effector gene. iScience 27:109224. https://doi.org/10.1016/j.isci.2024.109224 CrossrefMedlineGoogle Scholar
- 1982. Heme biosynthesis in rhizobium: Identification of a cloned gene coding for delta-aminolevulinic acid synthetase from Rhizobium meliloti. J. Biol. Chem. 257:8724-8730. https://doi.org/10.1016/S0021-9258(18)34188-7 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2011. The YopJ superfamily in plant-associated bacteria. Mol. Plant Pathol. 12:928-937. https://doi.org/10.1111/j.1364-3703.2011.00719.x CrossrefMedlineWeb of ScienceGoogle Scholar
- 2016. YopJ family effectors promote bacterial infection through a unique acetyltransferase activity. Microbiol. Mol. Biol. Rev. 80:1011-1027. https://doi.org/10.1128/MMBR.00032-16 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2021. The ETS-ETI cycle: Evolutionary processes and metapopulation dynamics driving the diversification of pathogen effectors and host immune factors. Curr. Opin. Plant Biol. 62:102011. https://doi.org/10.1016/j.pbi.2021.102011 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2021. Recent advances in effector-triggered immunity in plants: new pieces in the puzzle create a different paradigm. Int. J. Mol. Sci. 22:4709. https://doi.org/10.3390/ijms22094709 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2002. Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J. Bacteriol. 184:1340-1348. https://doi.org/10.1128/JB.184.5.1340-1348.2002 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2021. A centenary for bacterial spot of tomato and pepper. Mol. Plant Pathol. 22:1500-1519. https://doi.org/10.1111/mpp.13125 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2021. Ralstonia solanacearum type III effector RipJ triggers bacterial wilt resistance in Solanum pimpinellifolium. Mol. Plant-Microbe Interact. 34:962-972. https://doi.org/10.1094/MPMI-09-20-0256-R LinkWeb of ScienceGoogle Scholar
- 2024. Phenotypic and genetic diversity of xanthomonads isolated from pepper (Capsicum spp.) in Taiwan from 1989 to 2019. Phytopathology 114:2033-2044. https://doi.org/10.1094/PHYTO-11-23-0449-R LinkWeb of ScienceGoogle Scholar
- 2021. Harnessing eco-evolutionary dynamics of xanthomonads on tomato and pepper to tackle new problems of an old disease. Annu. Rev. Phytopathol. 59:289-310. https://doi.org/10.1146/annurev-phyto-020620-101612 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2015. Bacterial spot of tomato and pepper: Diverse Xanthomonas species with a wide variety of virulence factors posing a worldwide challenge. Mol. Plant Pathol. 16:907-920. https://doi.org/10.1111/mpp.12244 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2015. The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci. Adv. 1:e1500245. https://doi.org/10.1126/sciadv.1500245 CrossrefMedlineWeb of ScienceGoogle Scholar
- 1998. Counterselectable markers: Untapped tools for bacterial genetics and pathogenesis. Infect. Immun. 66:4011-4017. https://doi.org/10.1128/IAI.66.9.4011-4017.1998 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2018. Identification of Xanthomonas species associated with bacterial leaf spot of tomato, capsicum and chilli crops in eastern Australia. Eur. J. Plant Pathol. 150:595-608. https://doi.org/10.1007/s10658-017-1303-9 CrossrefWeb of ScienceGoogle Scholar
- 2004. Characterization of the Xanthomonas AvrXv4 Effector, a SUMO protease translocated into plant cells. Mol. Plant-Microbe Interact. 17:633-643. https://doi.org/10.1094/MPMI.2004.17.6.633 LinkWeb of ScienceGoogle Scholar
- 2022. Comparative genomic analysis of the lettuce bacterial leaf spot pathogen, Xanthomonas hortorum pv. vitians, to investigate race specificity. Front. Microbiol. 13:840311. https://doi.org/10.3389/fmicb.2022.840311 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2018. Suppression of hopz effector-triggered plant immunity in a natural pathosystem. Front. Plant Sci. 9:977. https://doi.org/10.3389/fpls.2018.00977 CrossrefMedlineWeb of ScienceGoogle Scholar
- 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: Selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73. https://doi.org/10.1016/0378-1119(94)90324-7 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675. https://doi.org/10.1038/nmeth.2089 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2021. What the wild things do: Mechanisms of plant host manipulation by bacterial type III-secreted effector proteins. Microorganisms 9:1029. https://doi.org/10.3390/microorganisms9051029 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2019. Using forward genetics in Nicotiana benthamiana to uncover the immune signaling pathway mediating recognition of the Xanthomonas perforans effector XopJ4. New Phytol. 221:1001-1009. https://doi.org/10.1111/nph.15411 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2015. Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front. Microbiol. 6:535. https://doi.org/10.3389/fmicb.2015.00535 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2023. Comparative genomic analysis and rapid molecular detection of Xanthomonas euvesicatoria using unique ATP-Dependent DNA Helicase recQ, hrpB1, and hrpB2 Genes Isolated from Physalis pubescens in China. Plant Pathol. J. 39:191-206. https://doi.org/10.5423/PPJ.OA.08.2022.0119 CrossrefMedlineGoogle Scholar
- 2024. Natural variation of immune epitopes reveals intrabacterial antagonism. Proc. Natl. Acad. Sci. U.S.A. 121:e2319499121. https://doi.org/10.1073/pnas.2319499121 CrossrefMedlineGoogle Scholar
- 2018. The Xanthomonas euvesicatoria type III effector XopAU is an active protein kinase that manipulates plant MAP kinase signaling. PLoS Pathog. 14:e1006880. https://doi.org/10.1371/journal.ppat.1006880 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2015. Five Xanthomonas type III effectors suppress cell death induced by components of immunity-associated MAP kinase cascades. Plant Signal. Behav. 10:e1064573. https://doi.org/10.1080/15592324.2015.1064573 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2013. The Xanthomonas campestris type III effector XopJ targets the host cell proteasome to suppress salicylic-acid mediated plant defence. PLoS Pathog. 9:e1003427. https://doi.org/10.1371/journal.ppat.1003427 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2020. Single gene enables plant pathogenic Pectobacterium to overcome host-specific chemical defence. Mol. Plant Pathol. 21:349-359. https://doi.org/10.1111/mpp.12900 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2022. Immune recognition of the secreted serine protease ChpG restricts the host range of Clavibacter michiganensis from eggplant varieties. Mol. Plant Pathol. 23:933-946. https://doi.org/10.1111/mpp.13215 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2006. Identification of isolates that cause a leaf spot disease of brassicas as Xanthomonas campestris pv. raphani and pathogenic and genetic comparison with related pathovars. Phytopathology 96:735-745. https://doi.org/10.1094/PHYTO-96-0735 LinkWeb of ScienceGoogle Scholar
- 2013. Xanthomonas campestris pv. campestris (cause of black rot of crucifers) in the genomic era is still a worldwide threat to brassica crops. Mol. Plant Pathol. 14:2-18. https://doi.org/10.1111/j.1364-3703.2012.00833.x CrossrefMedlineWeb of ScienceGoogle Scholar
- 2015. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:285-295. https://doi.org/10.1016/j.chom.2015.08.004 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2015. Rice OsFLS2-mediated perception of bacterial flagellins is evaded by Xanthomonas oryzae pvs. oryzae and oryzicola. Mol. Plant 8:1024-1037. https://doi.org/10.1016/j.molp.2015.01.012 CrossrefMedlineWeb of ScienceGoogle Scholar
- 1993. Avirulence gene avrRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii 7998. Mol. Plant-Microbe Interact. 6:616-627. https://doi.org/10.1094/MPMI-6-616 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2009. The type III effectors of Xanthomonas. Mol. Plant Pathol. 10:749-766. https://doi.org/10.1111/j.1364-3703.2009.00590.x CrossrefMedlineWeb of ScienceGoogle Scholar
- 2008. AvrACXcc8004, a type III effector with a leucine-rich repeat domain from Xanthomonas campestris pathovar campestris confers avirulence in vascular tissues of Arabidopsis thaliana ecotype Col-0. J. Bacteriol. 190:343-355. https://doi.org/10.1128/JB.00978-07 CrossrefMedlineWeb of ScienceGoogle Scholar
- 2023. A novel biosynthetic gene cluster across the Pantoea species complex is important for pathogenicity in onion. Mol. Plant-Microbe Interact. 36:176-188. https://doi.org/10.1094/MPMI-08-22-0165-R LinkWeb of ScienceGoogle Scholar
