Author: Laurent D. Noël
Internal reviewer: Ralf Koebnik
Expert reviewer: Jian-Min Zhou

Class: XopAC
Family: XopAC
Prototype: XopAC (Xanthomonas campestris pv. campestris; strain 8004)
RefSeq ID: AFP74845.1 (536 aa)
3D structure: Unknown

xopAC is present in many Xcc strains as well as several Xanthomonas campestris pv. raphani (Guy et al., 2013a). To date, all allelic variants of XopAC conferred avirulence in Arabidopsis accession Col-0 (Guy et al., 2013b).

Yes, Ralstonia solanacearum (Tan et al., 2019).

XopAC/AvrAC was identified as a putative type III effector because of the presence of seven prokaryotic-type leucine-rich repeats in its C-terminal domain and a PIP-box motif in the xopAC promoter suggestive of a hrpX-dependent expression (Xu et al., 2008).

The N-terminal region of XopAC (XopAC_1-217) mediates secretion and translocation of an AvrBs1 reporter domain (AvrBs1_59-445) into pepper leaves in a hrpF-dependent manner (Xu et al., 2008).

xopAC promoters possess a PIP-box motif (Xu et al., 2008). Expression of xopAC is induced in the hrp-inducing medium XVM2 in a hrpG- and hrpX-dependent manner (Xu et al., 2008).

• xopAC, also named avrAC, confers avirulence to Xanthomonas campestris pv. campestris (Xcc) on Arabidopsis accession Col-0 but not on Kas (Xu et al., 2008).
• xopAC avirulence is weak in mesophyll tissue but strong upon inoculation of hydathodes or vascular tissues (Xu et al., 2008; Cerutti et al., 2017).
• xopAC contributes to Xcc pathogenicity on Brassica oleracea and Arabidopsis in a BIK1-dependent manner (Feng et al., 2012).
• XopAC inhibits BIK1 kinase activity and blocks flg22-induced PTI responses (Feng et al., 2012).
• XopAC was found to be associated with variations in disease symptoms when testing a set of 45 Xcc strains on two natural accessions of Arabidopsis (Guy et al., 2013a).
• Mutagenesis of type III effectors in Xcc confirmed that xopAC functions as both a virulence and an avirulence gene in Arabidopsis (Guy et al., 2013).
• When heterologously expressed in virulent Ralstonia solanacearum or Pseudomonas syringae pv. tomato, XopAC confers avirulence on the Arabidopsis accession Col-0 (Guy et al., 2013b).
• Transgenic expression of xopAC in Arabidopsis accession Col-0 induces early growth arrest at both apical and root meristems (Wang et al., 2015).
• AvrAC recognition requires the RKS1 pseudokinase of the ZRK family and the NLR protein ZAR1, which also recognizes the Pseudomonas syringae effectors HopZ1a, HopBA1, HopF1, HopO1, and HopX1 and the Xanthomonas perforanseffector XopJ4 (Wang et al., 2015; Laflamme et al., 2020; Schultink et al., 2019).

XopAC was localized to the plant plasma membrane upon Agrobacterium-mediated transient expression in Nicotiana benthamiana (Guy et al., 2013b). This localization depends on its LRR domain suggesting that XopAC localization is dependent on its interacting partner(s) (Guy et al., 2013b).

XopAC presents an uridylyl transferase activity, which depends on residue H₄₆₉ (Feng et al., 2012). XopAC is able to uridylylate both conserved S₂₃₆ and T₂₃₇ in BIK1. Similar activity was demonstrated for all other RLCK VIIa tested including PBL2, which acts as a decoy and enables AvrAC detection (Feng et al., 2012; Wang et al., 2015).

Nine Arabidopsis RLCKs (receptor-like cytoplasmic kinases, subfamily VIIa) were described as putative interactors of XopAC using yeast-two hybrid assays (Guy et al., 2013b). Importantly, PBL2 RLCK is essential for the XopAC avirulence function and BIK1 RLCK is required for the XopAC virulence functions (Guy et al., 2013b; Feng et al., 2012; Wang et al., 2015).

xopAC is present in many Xcc strains as well as several Xanthomonas campestris pv. raphani (Guy et al., 2013a). To date, all allelic variants of XopAC conferred avirulence in Arabidopsis accession Col-0 (Guy et al., 2013b).

Yes, Ralstonia solanacearum (Tan et al., 2019).

Cerutti A, Jauneau A, Auriac M-C, Lauber E, Martinez Y, Chiarenza S, Leonhardt N, Berthomé R, Noël LD (2017). Immunity at cauliflower hydathodes controls infection by Xanthomonas campestris pv. campestris. Plant Physiol. 174: 700-712. DOI: 10.1104/pp.16.01852

Feng F, Yang F, Rong W, Wu X, Zhang J, Chen S, He C, Zhou JM (2012). A Xanthomonas uridine 5'-monophosphate transferase inhibits plant immune kinases. Nature 485: 114-118. DOI: 10.1038/nature10962

Guy E, Genissel A, Hajri A, Chabannes M, David P, Carrère S, Lautier M, Roux B, Boureau T, Arlat M, Poussier S, Noël LD (2013a). Natural genetic variation of Xanthomonas campestris pv. campestris pathogenicity on Arabidopsis revealed by association and reverse genetics. MBio 4: e00538-12. DOI: 10.1128/mBio.00538-12. Erratum in: MBio (2013) 4: e00978-13.

Guy E, Lautier M, Chabannes M, Roux B, Lauber E, Arlat M, Noël LD (2013b). xopAC-triggered immunity against Xanthomonas depends on Arabidopsis receptor-like cytoplasmic kinase genes PBL2 and RIPK. PLoS One 8: e73469. DOI: 10.1371/journal.pone.0073469

Laflamme B, Dillon MM, Martel A, Almeida RND, Desveaux D, Guttman DS (2020). The pan-genome effector-triggered immunity ladscape of a host-pathogen interaction. Science 367: 763-768. http://doi.org/10.1126/science.aax4079

Schultink A, Qi T, Bally J, Staskawicz B (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. http://doi.org/doi: 10.1111/nph.15411

Tan X, Qiu H, Li F, Cheng D, Zheng X, Wang B, Huang M, Li W, Li Y, Sang K, Song B, Du J, Chen H, Xie C (2019). Complete genome sequence of sequevar 14M Ralstonia solanacearum strain HA4-1 reveals novel type III effectors acquired through horizontal gene transfer. Front. Microbiol. 10: 1893. DOI: 10.3389/fmicb.2019.01893

Wang G, Roux B, Feng F, Guy E, Li L, Li N, Zhang X, Lautier M, Jardinaud MF, Chabannes M, Arlat M, Chen S, He C, Noël LD, J.M. Zhou JM (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. DOI: 10.1016/j.chom.2015.08.004

Xu RQ, Blanvillain S, Feng JX, Jiang BL, Li XZ, Wei HY, Kroj T, Lauber E, Roby D, Chen B, He YQ, Lu GT, Tang DJ, Vasse J, Arlat M, Tang JL (2008). AvrAC_Xcc8004, 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. DOI: 10.1128/JB.00978-07