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Molecular Diagnosis and Diversity for Regulated Xanthomonas


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bacteria:t3e:xopl

XopL

Author: Joana G. Vicente
Internal reviewer: Joël F. Pothier
Expert reviewer: FIXME

Class: XopL
Family: XopL
Prototype: XCV3220 (Xanthomonas euvesicatoria pv. euvesicatoria, ex Xanthomonas campestris pv. vesicatoria; strain 85-10)
RefSeq ID: CAJ24951 (660 aa)
Examples of other sequences: XopLXcv85-10 CAJ24951.1 (X. euvesicatoria pv. euvesicatoria); XopKXcc306 21109412 (X. citri pv. citri); XopLXcc8004 66575899 (X. campestris pv. campestris)
3D structure: 4FC9, 4FCG (Singer et al., 2013). Full-length XopLXcv85-10 did not crystallize but fragments XopL[aa 144–450] and XopL[aa 474–660] yielded crystals (Singer et al., 2013). The crystal structure of the N-terminal region of XopL showed the presence of a leucine-rich repeat (LRR) domain, that might serve as a protein-protein interaction module for ubiquitination target recognition (Singer et al., 2013). The protein represents a new class of E3 ubiquitin ligases.

Biological function

How discovered?

XopL was first identified in X. campestris pv. campestris (Xcc) strain 8004 as a candidate T3E due to the presence of a plant-inducible promoter (PIP) box in its gene, XC_4273 (Jiang et al., 2009). The CDS XC_4273, re-called XopXccLR (LR = leucine-rich repeat), in X. campestris pv. campestris 8004 was suggested to be a T3E has it harboured a N-terminal region possessing translocation signal with the functionality to target proteins into plant cells (Jiang et al., 2009). It was also shown to be required for X. campestris pv. campestris to proliferate well in hosts plant and thus essential for virulence (Jiang et al., 2009). It's only a few years later that the analysis of the genome sequence of Xcv strain 85-10 led to the identification of XCV3220 (xopL) as a new T3E candidate gene and to its more complete characterization (Singer et al., 2013).

(Experimental) evidence for being a T3E

Using an AvrBs1 reporter fusion, XopLXcc8004 was shown to be translated into plant cells in a hrpF- and hpaB-dependent manner (Jiang et al., 2009).

XopLXcv85-10 contains a PIP box (plant inducible promoter) in its promoter (TTCG-N16-TTCG; genome position 3669238-261); co-regulation with the T3S system was confirmed by RT-PCR (Singer et al., 2013). Contains leucine-rich repeats (LRRs). Type III-dependent secretion and translocation was confirmed by in vitro secretion and in vivo translocation assays (Singer et al., 2013). Mutation of amino acids in the central cavity of the XL-box disrupts E3 ligase activity and prevents XopL-induced plant cell death. The lack of cysteine residues in the XL-box suggests the absence of thioester-linked ubiquitin-E3 ligase intermediates and a non-catalytic mechanism for XopL-mediated ubiquitination. The E3 ligase activity is required to provoke plant cell death, suppression of PAMP responses solely depends on the N-terminal LRR domain (Singer et al., 2013). XopLXcc8004 possesses features that are typical of T3Es: the promoter region of xopLXcc8004 gene contains a perfect plant inducible promoter (PIP) box followed by a 10 box similar sequence (TTCGC-N15-TTCGC-N31-ACGACA) and LRRs motif is characteristic of specific T3Es in pathogenic bacteria (Yan et al., 2019).

Regulation

The xopL Xcc8004 gene contains a PIP box and was shown to be controlled by hrpG and hrpX (Jiang et al., 2009).

qRT-PCR revealed that transcript levels of 15 out of 18 tested non-TAL effector genes (as well as the regulatory genes hrpG and hrpX), including xopL, were significantly reduced in the Xanthomonas oryzae pv. oryzae ΔxrvC mutant compared with those in the wild-type strain PXO99A (Liu et al., 2016).

The expression of xopL Xcc8004 gene is positively regulated by HrpG/HrpX (Yan et al., 2019).

Phenotypes

  • XopLXcv85-10 displays E3 ubiquitin ligase activity and inhibits expression of the elf18- and flg22-induced defense gene pNHL10 in Arabidopsis mesophyll protoplasts, triggers cell death in Nicotiana benthamiana and suppresses PTI in host plants (Singer et al., 2013; Popov et al., 2016).
  • In contrast, XopLXoc does not induce cell death in N. benthamiana. FIXME
  • XopLXcc8004 is required for full virulence and growth of X. campestris pv. campestris in the host plant Chinese radish (Jiang et al., 2009).
  • XopLXcv85-10 suppresses PAMP-related defense gene expression and is an E3 ubiquitin ligase (Singer et al., 2013).
  • Transient expression of XopL, led to a nearly complete elimination of stromules and the relocation of plastids to the nucleus and further characterization of XopL revealed that the E3 ligase activity is essential for two plastid phenotypes (Erickson et al., 2016).
  • XopLXap is a T3E which supports X. axonopodis pv. punicae for multiplication in pomegranate by suppressing plant immune responses including plant cell death (Soni et al., 2017).
  • XopLXcc8004 interferes with innate immunity of Arabidopsis (Yan et al., 2019).

Localization

Possibly plasma membrane. The transiently expressed XopLXap::EYFP fusion protein was localized to the plasma membrane, indicating the possible site of its action (Soni et al., 2017).

Enzymatic function

E3 ubiquitin ligase activity (Singer et al., 2013).

Interaction partners

Unknown.

Conservation

In xanthomonads

Yes (e.g., X. euvesicatoria, X. citri, X. axonopodis, X. oryzae, X. oryzicola, X. fragariae, X. perforans, X. gardneri, X. campestris pv. campestris, but not X. campestris pv. raphani, in some X. arboricola pathovars). See for example Table 2 in Jiang et al. (2009) and Figure S1 in Singer et al. (2013).

In other plant pathogens/symbionts

No.

References

Adlung N (2016). Charakterisierung der Avirulenzaktivität von XopQ und Identifizierung möglicher Interaktoren von XopL aus Xanthomonas campestris pv. vesicatoria. Doctoral Thesis. Martin-Luther-Universität Halle-Wittenberg, Germany. PDF: d-nb.info/1116951061/34 FIXME

Erickson JL, Adlung N, Lampe C, Bonas U, Schattat MH (2018). The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana. Plant J. 93: 856-870. DOI:10.1111/tpj.13813

Jiang W, Jiang BL, Xu RQ, Huang JD, Wei HY, Jiang GF, Cen WJ, Liu J, Ge YY, Li GH, Su LL, Hang XH, Tang DJ, Lu GT, Feng JX, He YQ, Tang JL (2009). Identification of six type III effector genes with the PIP box in Xanthomonas campestris pv campestris and five of them contribute individually to full pathogenicity. Mol. Plant Microbe Interact. 22: 1401-1411. DOI: 10.1094/MPMI-22-11-1401

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

Popov G, Fraiture M, Brunner F, Sessa G (2016). Multiple Xanthomonas euvesicatoria type III effectors inhibit flg22-triggered immunity. Mol. Plant Microbe Interact. 29: 651-660. DOI: 10.1094/MPMI-07-16-0137-R

Singer AU, Schulze S, Skarina T, Xu X, Cui H, Eschen-Lippold L, Egler M, Srikumar T, Raught B, Lee J, Scheel D, Savchenko A, Bonas U (2013). A pathogen type III effector with a novel E3 ubiquitin ligase architecture. PLoS Pathog. 9: e1003121. DOI: 10.1371/journal.ppat.1003121

Soni M, Mondal KK. (2017). Xanthomonas axonopodis pv. punicae employs XopL effector to suppress pomegranate immunity. J. Integr. Plant Biol. 60: 341-357. DOI: 10.1111/jipb.12615

Yan X, Tao J, Luo HL, Tan LT, Rong W, Li HP, He CZ (2019). A type III effector XopLXcc8004 is vital for Xanthomonas campestris pathovar campestris to regulate plant immunity. Res. Microbiol. 170: 138-146. DOI: 10.1016/j.resmic.2018.12.001

bacteria/t3e/xopl.txt · Last modified: 2020/10/28 12:23 by rkoebnik