XopD SUMO Protease Affects Host Transcription, Promotes Pathogen Growth, and Delays Symptom Development in<i>Xanthomonas</i>-Infected Tomato Leaves

Kim, Jung‐Gun; Taylor, Kristie; Hotson, Andrew; Keegan, Mark T.; Schmelz, Eric A.; Mudgett, Mary Beth

doi:10.1105/tpc.108.058529

Cited by 155 publications

(199 citation statements)

References 58 publications

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“…These authors found a widespread suppression of photosynthetic gene expression caused by bacterial effector proteins, indicating that bacterial infection itself influences photosynthesis. In agreement with these results, Mudgett and colleagues (Kim et al, 2008) recently demonstrated that the Xcv effector protein XopD contributes to a delayed development of tissue chlorosis and necrosis. Thus, the effector-mediated effect on photosynthesis was most likely responsible for the reduced rate of photosynthesis and the expression of corresponding genes observed in both wild-type and transgenic plants in our experiments.…”

Section: Discussionsupporting

confidence: 67%

Cell Wall-Bound Invertase Limits Sucrose Export and Is Involved in Symptom Development and Inhibition of Photosynthesis during Compatible Interaction between Tomato andXanthomonas campestrispvvesicatoria

2008

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Cell wall-bound invertase (cw-Inv) plays an important role in carbohydrate partitioning and regulation of sink-source interaction. There is increasing evidence that pathogens interfere with sink-source interaction, and induction of cw-Inv activity has frequently been shown in response to pathogen infection. To investigate the role of cw-Inv, transgenic tomato (Solanum lycopersicum) plants silenced for the major leaf cw-Inv isoforms were generated and analyzed during normal growth and during the compatible interaction with Xanthomonas campestris pv vesicatoria. Under normal growth conditions, activities of sucrolytic enzymes as well as photosynthesis and respiration were unaltered in the transgenic plants compared with wild-type plants. However, starch levels of source leaves were strongly reduced, which was most likely caused by an enhanced sucrose exudation rate. Following X. campestris pv vesicatoria infection, cw-Inv-silenced plants showed an increased sucrose to hexose ratio in the apoplast of leaves. Symptom development, inhibition of photosynthesis, and expression of photosynthetic genes were clearly delayed in transgenic plants compared with wild-type plants. In addition, induction of senescence-associated and pathogenesis-related genes observed in infected wild-type plants was abolished in cw-Inv-silenced tomato lines. These changes were not associated with decreased bacterial growth. In conclusion, cw-Inv restricts carbon export from source leaves and regulates the sucrose to hexose ratio in the apoplast. Furthermore, an increased apoplastic hexose to sucrose ratio can be linked to inhibition of photosynthesis and induction of pathogenesis-related gene expression but does not significantly influence bacterial growth. Indirectly, bacteria may benefit from low invertase activity, since the longevity of host cells is raised and basal defense might be dampened.

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Section: Discussionsupporting

confidence: 67%

Cell Wall-Bound Invertase Limits Sucrose Export and Is Involved in Symptom Development and Inhibition of Photosynthesis during Compatible Interaction between Tomato andXanthomonas campestrispvvesicatoria

2008

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“…Among the ;35 T3Es injected by Xcv into the plant cell, XopD is a modular protein of 760 amino acids that contains (1) a recently identified N-terminal domain of 215 amino acids , (2) a helix-loop-helix domain (HLH), (3) two tandemly repeated ERF-associated amphiphillic repression (EAR) motifs, previously described in plant transcriptional repressors during defense responses (Kazan, 2006), and (4) a C-terminal Cys protease domain with structural similarity to the yeast ubiquitin-like protease 1. Consistent with its protein structure, XopD displays small ubiquitin-like modifier (SUMO) protease (Hotson et al, 2003) and nonspecific DNA binding activities (Kim et al, 2008). In plant cells, XopD is localized in nuclear foci, indicating that host targets are likely nuclear SUMOylated proteins (Hotson et al, 2003;Canonne et al, 2010).…”

Section: Introductionmentioning

confidence: 73%

The Xanthomonas Type III Effector XopD Targets the Arabidopsis Transcription Factor MYB30 to Suppress Plant Defense

et al. 2011

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Plant and animal pathogens inject type III effectors (T3Es) into host cells to suppress host immunity and promote successful infection. XopD, a T3E from Xanthomonas campestris pv vesicatoria, has been proposed to promote bacterial growth by targeting plant transcription factors and/or regulators. Here, we show that XopD from the B100 strain of X. campestris pv campestris is able to target MYB30, a transcription factor that positively regulates Arabidopsis thaliana defense and associated cell death responses to bacteria through transcriptional activation of genes related to very-long-chain fatty acid (VLCFA) metabolism. XopD specifically interacts with MYB30, resulting in inhibition of the transcriptional activation of MYB30 VLCFA-related target genes and suppression of Arabidopsis defense. The helix-loop-helix domain of XopD is necessary and sufficient to mediate these effects. These results illustrate an original strategy developed by Xanthomonas to subvert plant defense and promote development of disease.

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“…Indeed, the effector protein XopD (Xanthomonas outer protein D) from the tomato (Solanum lycopersicum) pathogen Xanthomonas campestris pv vesicatoria is known to act as a SUMO isopeptidase in planta, and this activity enhances virulence of this pathogen on tomato (Hotson et al, 2003;Kim et al, 2008). Interestingly, XopD appears to have SUMO isopeptidase activity not only toward SUM1 and SUM2 conjugates, but also toward SUM3 conjugates (Colby et al, 2006).…”

Section: Sa-dependent Sum3 Expression Promotes Plant Defense Responsementioning

confidence: 99%

Arabidopsis Small Ubiquitin-Like Modifier Paralogs Have Distinct Functions in Development and Defense

et al. 2010

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Posttranslational modifications allow dynamic and reversible changes to protein function. In Arabidopsis thaliana, a small gene family encodes paralogs of the small ubiquitin-like posttranslational modifier. We studied the function of these paralogs. Single mutants of the SUM1 and SUM2 paralogs do not exhibit a clear phenotype. However, the corresponding double knockdown mutant revealed that SUM1 and SUM2 are essential for plant development, floral transition, and suppression of salicylic acid (SA)-dependent defense responses. The SUM1 and SUM2 genes are constitutively expressed, but their spatial expression patterns do not overlap. Tight transcriptional regulation of these two SUM genes appears to be important, as overexpression of either wild-type or conjugation-deficient mutants resulted in activation of SA-dependent defense responses, as did the sum1 sum2 knockdown mutant. Interestingly, expression of the paralog SUM3 is strongly and widely induced by SA and by the defense elicitor Flg22, whereas its expression is otherwise low and restricted to a few specific cell types. Loss of SUM3 does not result in an aberrant developmental phenotype except for late flowering, while SUM3 overexpression causes early flowering and activates plant defense. Apparently, SUM3 promotes plant defense downstream of SA, while SUM1 and SUM2 together prevent SA accumulation in noninfected plants.

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XopD SUMO Protease Affects Host Transcription, Promotes Pathogen Growth, and Delays Symptom Development inXanthomonas-Infected Tomato Leaves

Cited by 155 publications

References 58 publications

Cell Wall-Bound Invertase Limits Sucrose Export and Is Involved in Symptom Development and Inhibition of Photosynthesis during Compatible Interaction between Tomato andXanthomonas campestrispvvesicatoria

Cell Wall-Bound Invertase Limits Sucrose Export and Is Involved in Symptom Development and Inhibition of Photosynthesis during Compatible Interaction between Tomato andXanthomonas campestrispvvesicatoria

The Xanthomonas Type III Effector XopD Targets the Arabidopsis Transcription Factor MYB30 to Suppress Plant Defense

Arabidopsis Small Ubiquitin-Like Modifier Paralogs Have Distinct Functions in Development and Defense

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