<i>Nicotiana </i>species as surrogate host for studying the pathogenicity of <i>Acidovorax citrulli</i>, the causal agent of bacterial fruit blotch of cucurbits

Traore, Sy M.; Eckshtain‐Levi, Noam; Miao, Jiamin; Sparks, A. C.; Wang, Zhibo; Wang, Kunru; Li, Qi; Burdman, Saul; Walcott, R. R.; Welbaum, Gregory E.; Zhao, Bingyu

doi:10.1111/mpp.12792

Cited by 18 publications

(35 citation statements)

References 58 publications

(86 reference statements)

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“…Similar to most plant pathogenic bacteria, Ac uses the type III secretion system (T3SS) to inject type III effector (T3E) proteins into the host to cause disease (Jimenez-Guerrero et al, 2020). However, unlike other well-studied T3SS-dependent pathogenic bacteria, how T3Es perturb innate plant immunity remains mostly unknown for Ac (Traore et al, 2019;Jimenez-Guerrero et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Acidovorax citrulli Type III Effector AopP Suppresses Plant Immunity by Targeting the Watermelon Transcription Factor WRKY6

et al. 2020

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Acidovorax citrulli (Ac) is the causal agent of bacterial fruit blotch (BFB), and BFB poses a threat to global watermelon production. Despite its economic importance, the molecular mechanisms underlying Ac pathogenicity and virulence are not well understood, particularly with regard to its type III secreted effectors. We identify a new effector, AopP, in Ac and confirm its secretion and translocation. AopP suppresses reactive oxygen species burst and salicylic acid (SA) content and significantly contributes to virulence. Interestingly, AopP interacts with a watermelon transcription factor, ClWRKY6, in vivo and in vitro. ClWRKY6 shows typical nuclear localization, and AopP and ClWRKY6 co-localize in the nucleus. Ac infection, SA, and the pathogen-associated molecular pattern flg22Ac promote ClWRKY6 production, suggesting that ClWRKY6 is involved in plant immunity and SA signaling. Furthermore, ClWRKY6 positively regulates PTI and SA production when expressed in Nicotiana benthamiana. Importantly, AopP reduces ClWRKY6 mRNA and ClWRKY6 protein levels, suggesting that AopP suppresses plant immunity by targeting ClWRKY6. In summary, we identify a novel effector associated with the virulence mechanism of Ac, which interacts with the transcription factor of the natural host, watermelon. The findings of this study provide insights into the mechanisms of watermelon immune responses and may facilitate molecular breeding for bacterial fruit blotch resistance.

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Section: Introductionmentioning

confidence: 99%

Acidovorax citrulli Type III Effector AopP Suppresses Plant Immunity by Targeting the Watermelon Transcription Factor WRKY6

et al. 2020

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“…To assess this hypothesis, we first carried out inoculation experiments of melon and Nicotiana benthamiana leaves using the syringe infiltration method. N. benthamiana was included in these assays since it was recently shown that this plant can be used as a surrogate host for studying pathogenicity aspects of A. citrulli (Traore et al, 2019). These experiments showed no differences in the progress of symptom appearance and in symptom severity among the tested cured strains, non-cured strains and wild-type M6 (Figure 5A and Supplementary Figure S6).…”

Section: Resultsmentioning

confidence: 99%

Complete Assembly of the Genome of an Acidovorax citrulli Strain Reveals a Naturally Occurring Plasmid in This Species

et al. 2019

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Acidovorax citrulli is the causal agent of bacterial fruit blotch (BFB), a serious threat to cucurbit crop production worldwide. Based on genetic and phenotypic properties, A. citrulli strains are divided into two major groups: group I strains have been generally isolated from melon and other non-watermelon cucurbits, while group II strains are closely associated with watermelon. In a previous study, we reported the genome of the group I model strain, M6. At that time, the M6 genome was sequenced by MiSeq Illumina technology, with reads assembled into 139 contigs. Here, we report the assembly of the M6 genome following sequencing with PacBio technology. This approach not only allowed full assembly of the M6 genome, but it also revealed the occurrence of a ∼53 kb plasmid. The M6 plasmid, named pACM6, was further confirmed by plasmid extraction, Southern-blot analysis of restricted fragments and obtention of M6-derivative cured strains. pACM6 occurs at low copy numbers (average of ∼4.1 ± 1.3 chromosome equivalents) in A. citrulli M6 and contains 63 open reading frames (ORFs), most of which (55.6%) encoding hypothetical proteins. The plasmid contains several genes encoding type IV secretion components, and typical plasmid-borne genes involved in plasmid maintenance, replication and transfer. The plasmid also carries an operon encoding homologs of a Fic-VbhA toxin-antitoxin (TA) module. Transcriptome data from A. citrulli M6 revealed that, under the tested conditions, the genes encoding the components of this TA system are among the highest expressed genes in pACM6. Whether this TA module plays a role in pACM6 maintenance is still to be determined. Leaf infiltration and seed transmission assays revealed that, under tested conditions, the loss of pACM6 did not affect the virulence of A. citrulli M6. We also show that pACM6 or similar plasmids are present in several group I strains, but absent in all tested group II strains of A. citrulli .

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“…In a previous study, it was found that the YopJ homologous protein from A. citrulli Aac5 induced PCD symptoms [ 17 ]. Traore et al [ 16 ] also reported that the YopJ homologous protein from A. citrulli AAC00-1 induced PCD symptoms in N. benthamiana . ROS burst is a key event in the PTI response [ 11 ].…”

Section: Discussionmentioning

confidence: 99%

“…Recently, three putative effectors of A. citrulli were found to induce PCD in N. benthamiana leaves. Among them, A. citrulli strains M6 and AAC00-1 mutated in the Aave_1548 effector gene and displayed reduced virulence in N. benthamiana [ 16 ], which was the first detailed report of a putative PCD-inducing effector in A. citrulli . In a previous study, we found that the YopJ homologous effectors in A. citrulli Aac5 strain also induced PCD in N. benthamiana [ 17 ].…”

Section: Introductionmentioning

confidence: 99%

“…As one of the natural hosts of A. citrulli is watermelon, and the immune pathway of watermelon is not well-studied, it is difficult to analyze the functions of A. citrulli effector proteins in watermelon. Recent studies have shown that the interaction system of A. citrulli and N. benthamiana can be used for the functional analysis of A. citrulli effector proteins [ 16 ]. HrpG and HrpX were previously identified as key regulatory factors of the type III secretion system (T3SS) in A. citrulli [ 17 ].…”

Section: Introductionmentioning

confidence: 99%

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Identification and Functional Analysis of AopN, an Acidovorax Citrulli Effector that Induces Programmed Cell Death in Plants

Zhang

Zhao

Jiang

et al. 2020

IJMS

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Bacterial fruit blotch (BFB), caused by Acidovorax citrulli, seriously affects watermelon and other cucurbit crops, resulting in significant economic losses. However, the pathogenicity mechanism of A. citrulli is not well understood. Plant pathogenic bacteria often suppress the plant immune response by secreting effector proteins. Thus, identifying A. citrulli effector proteins and determining their functions may improve our understanding of the underlying pathogenetic mechanisms. In this study, a novel effector, AopN, which is localized on the cell membrane of Nicotiana benthamiana, was identified. The functional analysis revealed that AopN significantly inhibited the flg22-induced reactive oxygen species burst. AopN induced a programmed cell death (PCD) response. Unlike its homologous protein, the ability of AopN to induce PCD was dependent on two motifs of unknown functions (including DUP4129 and Cpta_toxin), but was not dependent on LXXLL domain. More importantly, the virulence of the aopN mutant of A. citrulli in N. benthamiana significantly decreased, indicating that it was a core effector. Further analysis revealed that AopN interacted with watermelon ClHIPP and ClLTP, which responds to A. citrulli strain Aac5 infection at the transcription level. Collectively, these findings indicate that AopN suppresses plant immunity and activates the effector-triggered immunity pathway.

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Nicotiana species as surrogate host for studying the pathogenicity of Acidovorax citrulli, the causal agent of bacterial fruit blotch of cucurbits

Cited by 18 publications

References 58 publications

Acidovorax citrulli Type III Effector AopP Suppresses Plant Immunity by Targeting the Watermelon Transcription Factor WRKY6

Acidovorax citrulli Type III Effector AopP Suppresses Plant Immunity by Targeting the Watermelon Transcription Factor WRKY6

Complete Assembly of the Genome of an Acidovorax citrulli Strain Reveals a Naturally Occurring Plasmid in This Species

Identification and Functional Analysis of AopN, an Acidovorax Citrulli Effector that Induces Programmed Cell Death in Plants

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