Pseudomonas syringae pv. actinidiae Type III Effectors Localized at Multiple Cellular Compartments Activate or Suppress Innate Immune Responses in Nicotiana benthamiana

Choi, Si Hwan; Jayaraman, Jay; Segonzac, Cécile; Park, Hye-Jee; Park, Hanbi; Han, Sang-Wook; Sohn, Kee Hoon

doi:10.3389/fpls.2017.02157

Cited by 42 publications

(66 citation statements)

References 91 publications

(131 reference statements)

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“…Five effectors including hopM1 Pto DC3000 , hopAD1 Pto DC3000 , hopT1-1 Pta 11528 , avrE1 Pta 11528 , and hopW1 -1 Pta 11528 strongly elicited necrosis whereas two effectors, hopAA1-1 Pto DC3000 and hopQ1-1 Pto DC3000 displayed mild chlorosis when expressed transiently in N. benthamiana leaves. This supports previous observations indicating that multiple P. syringae effectors trigger cell death in N. benthamiana ( Vinatzer et al, 2006 ; Wei et al, 2007 ; Wroblewski et al, 2009 ; Choi et al, 2017 ). For example, hopM1 Pto DC3000 , hopAA1-1 Pto DC3000 , hopQ1-1 Pto DC3000 , avrE1 Pto DC3000 , hopT1-1 Pto DC3000 , and hopAD1 Pto DC3000 effectors elicit cell death in N. benthamiana when delivered by Pseudomonas fluorescens heterologously expressing a P. syringae TTSS ( Wei et al, 2007 ) or though Pto DC3000 secretion effector polymutants ( Wei et al, 2007 , 2015 ).…”

Section: Discussionsupporting

confidence: 92%

“…Firstly, necrosis induced by hopM1 Pto DC3000 , hopAD1 Pto DC3000 , hopT1-1 Pta 11528 , avrE1 Pta 11528 , and hopW1-1 Pta 11528 effector genes was not dependent on NbSgt1 , which is typically required for R gene function ( McDowell and Dangl, 2000 ). The NbSgt1 -independence of avrE1 induced cell death has been reported previously ( Choi et al, 2017 ). However, cell death induced by the Psy B728a effector hopM1 and the Psa effectors hopT1-1 and hopW1-1 were reported to be at least partially dependent on NbSgt1 ( Vinatzer et al, 2006 ; Choi et al, 2017 ).…”

Section: Discussionsupporting

confidence: 77%

“…The NbSgt1 -independence of avrE1 induced cell death has been reported previously ( Choi et al, 2017 ). However, cell death induced by the Psy B728a effector hopM1 and the Psa effectors hopT1-1 and hopW1-1 were reported to be at least partially dependent on NbSgt1 ( Vinatzer et al, 2006 ; Choi et al, 2017 ). Therefore, further analyses are required to determine to what extent the cell death caused by these effectors is dependent on NbSgt1 in N. benthamiana.…”

Section: Discussionsupporting

confidence: 77%

“…actinidiae ( Psa ), and P. syringae pv. syringae ( Psy ) B728a, showed the ability of hopQ1-1, avrE1, hopT1-1, hopM1 , and hopAA1-1 to induce cell death in N. benthamiana ( Vinatzer et al, 2006 ; Wroblewski et al, 2009 ; Choi et al, 2017 ). It is noteworthy that in our assays, hopT1-1 PtoDC3000 did not trigger cell death in N. benthamiana , although this has been previously reported ( Wei et al, 2007 ; Wroblewski et al, 2009 ).…”

Section: Discussionmentioning

confidence: 99%

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Differential Suppression of Nicotiana benthamiana Innate Immune Responses by Transiently Expressed Pseudomonas syringae Type III Effectors

et al. 2018

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The plant pathogen Pseudomonas syringae injects about 30 different virulence proteins, so-called effectors, via a type III secretion system into plant cells to promote disease. Although some of these effectors are known to suppress either pattern-triggered immunity (PTI) or effector-triggered immunity (ETI), the mode of action of most of them remains unknown. Here, we used transient expression in Nicotiana benthamiana, to test the abilities of type III effectors of Pseudomonas syringae pv. tomato (Pto) DC3000 and Pseudomonas syringae pv. tabaci (Pta) 11528 to interfere with plant immunity. We monitored the sequential and rapid bursts of cytoplasmic Ca2+ and reactive oxygen species (ROS), the subsequent induction of defense gene expression, and promotion of cell death. We found that several effector proteins caused cell death, but independently of the known plant immune regulator NbSGT1, a gene essential for ETI. Furthermore, many effectors delayed or blocked the cell death-promoting activity of other effectors, thereby potentially contributing to pathogenesis. Secondly, a large number of effectors were able to suppress PAMP-induced defense responses. In the majority of cases, this resulted in suppression of all studied PAMP responses, suggesting that these effectors target common elements of PTI. However, effectors also targeted different steps within defense pathways and could be divided into three major groups based on their suppressive activities. Finally, the abilities of effectors of both Pto DC3000 and Pta 11528 to suppress plant immunity was conserved in most but not all cases. Overall, our data present a comprehensive picture of the mode of action of these effectors and indicate that most of them suppress plant defenses in various ways.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 77%

Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

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Differential Suppression of Nicotiana benthamiana Innate Immune Responses by Transiently Expressed Pseudomonas syringae Type III Effectors

et al. 2018

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“…shcM from Pto DC3000 (shcMPto) was cloned under the same avrRps4 promoter to 174 control expression of the plasmid-borne hopM1 operon used to assess shcMPsa 175 described earlier (Jayaraman et al, 2017). shcMPto was cloned as a cis-176 complementation construct ahead of hopM1Psa and transformed into Pfo Pf0-1 or 177…”

Section: Hopm1 Function In Psa3 Is Affected By Truncation Of Its Chapmentioning

confidence: 99%

AvrE1 and HopR1 fromPseudomonas syringaepv.actinidiaeare additively required for full virulence on kiwifruit

Jayaraman

Yoon

Applegate

et al. 2020

Preprint

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21Pseudomonas syringae pv. actinidiae ICMP 18884 biovar 3 (Psa3) produces 22 necrotic lesions during infection of its kiwifruit host. Bacterial growth in planta 23 and lesion formation are dependent upon a functional type III secretion system 24 (T3S), which translocates multiple effector proteins into host cells. Associated 25 with the T3S locus is the conserved effector locus (CEL), which has been 26 characterised and shown to be essential for the full virulence in other P. syringae 27 pathovars. Two effectors at the CEL, hopM1 and avrE1, as well as an avrE1-related 28 non-CEL effector, hopR1, have been shown to be redundant in the model pathogen 29 P. syringae pv. tomato DC3000 (Pto), a close relative of Psa. However, it is not 30 known whether CEL-related effectors are required for Psa pathogenicity. The Psa3 31 allele of hopM1, and its associated chaperone, shcM, have diverged significantly 32 from their orthologs in Pto. Furthermore, the CEL effector hopAA1-1, as well as a 33 related non-CEL effector, hopAA1-2, have both been pseudogenised. We have 34shown that HopM1 does not contribute to Psa3 virulence due to a truncation in 35 shcM, a truncation conserved in the Psa lineage, likely due to the need to evade 36 HopM1-triggered immunity in kiwifruit. We characterised the virulence 37 contribution of CEL and related effectors in Psa3 and found that only avrE1 and 38 hopR1, additively, are required for in planta growth and lesion production. This is 39 unlike the redundancy described for these effectors in Pto and indicates that these 40

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Using Bioinformatics and Molecular Biology to Streamline Construction of Effector Libraries for Phytopathogenic Pseudomonas syringae Strains

Jayaraman¹,

Halane²,

Choi³

et al. 2019

Methods in Molecular Biology

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Pseudomonas syringae pv. actinidiae Type III Effectors Localized at Multiple Cellular Compartments Activate or Suppress Innate Immune Responses in Nicotiana benthamiana

Cited by 42 publications

References 91 publications

Differential Suppression of Nicotiana benthamiana Innate Immune Responses by Transiently Expressed Pseudomonas syringae Type III Effectors

Differential Suppression of Nicotiana benthamiana Innate Immune Responses by Transiently Expressed Pseudomonas syringae Type III Effectors

AvrE1 and HopR1 fromPseudomonas syringaepv.actinidiaeare additively required for full virulence on kiwifruit

Using Bioinformatics and Molecular Biology to Streamline Construction of Effector Libraries for Phytopathogenic Pseudomonas syringae Strains

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