Large-Scale Identification and Characterization of Heterodera avenae Putative Effectors Suppressing or Inducing Cell Death in Nicotiana benthamiana

Chen, Changlong; Chen, Yongpan; Jian, Heng; Yang, Dan; Dai, Yiran; Pan, Lingling; Shi, Fengwei; Yang, Shanshan; Liu, Qian

doi:10.3389/fpls.2017.02062

Cited by 32 publications

(27 citation statements)

References 65 publications

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“…Hypersensitivity elicitation ability of parasite effectors is often verified in the nonhost plant N. benthamiana (Naessens et al, 2015;Chen et al, 2018;Shangguan et al, 2018). In this study, temporary expression of the effector SSGP-1A2 in N. benthamiana resulted in moderate elicitation of hypersensitive responses (Figure 6; Figure S7), suggesting that the effector could trigger defense reactions under certain conditions.…”

Section: Discussionmentioning

confidence: 52%

Differential localization of Hessian fly candidate effectors in resistant and susceptible wheat plants

et al. 2020

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Hessian fly Mayetiola destructor is a notorious pest of wheat. Previous studies suggest that Hessian fly uses effector‐based mechanisms to attack wheat plants during parasitism, but no direct evidence has been reported to support this postulation. Here, we produced recombinant proteins for five Family‐1 candidate effectors and antibodies. Indirect immunostaining and western blots were carried out to examine the localization of Hessian fly Family‐1 proteins in plant and insect tissues. Confocal images revealed that Family‐1 putative effectors were exclusively produced in the basal region of larval salivary glands, which are directly linked to the mandibles’ ducts for effector injection. The five Family‐1 proteins were detected in infested host plants on western blots. Indirect immunostaining of sectioned host tissues around the feeding site revealed strikingly different localization patterns between resistant and susceptible plants. In susceptible plants, the Family‐1 proteins penetrated from the feeding cell into deep tissues, indicative of movement between cells during nutritive cell formation. In contrast, the Hessian fly proteins were primarily limited to the initially attacked cells in resistant plants. The limitation of effectors’ spread in resistant plants was likely due to wall strengthening and rapid hypersensitive cell death. Cell death was found in Nicotiana benthamiana in association with hypersensitive reaction triggered by the Family‐1 effector SSGP‐1A2. Our finding represents a significant progress in visualizing insect effectors in host tissues and mechanisms of plant resistance and susceptibility to gall midge pests.

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Section: Discussionmentioning

confidence: 52%

Differential localization of Hessian fly candidate effectors in resistant and susceptible wheat plants

et al. 2020

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“…In addition, expressing candidate effectors in N. benthamiana using other expression vectors can be used to evaluate cell death with effector genes. For example, after 7 candidate effectors of Heterodera avenae were constructed into the pND108 expression vector, the infiltration assay showed induced cell death in N. benthamiana (Chen et al., 2018). Although different expression vectors were used, the effectors were identified by transient expression of proteins.…”

Section: Discussionmentioning

confidence: 99%

A key effector, BxSapB2, plays a role in the pathogenicity of the pine wood nematode Bursaphelenchus xylophilus

Zhao

et al. 2020

Forest Pathology

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The pine wood nematode (PWN), Bursaphelenchus xylophilus, causes huge economic losses in pine forests. The plant‐parasitic nematodes have a complex life cycle that includes the secretion of effector proteins through a stylet into the host cell to promote parasitism. In this study, SignalP 4.1 and TMHMM 2.0 were used in preliminary screens for candidate effectors and were expressed in Nicotiana benthamiana through the PVX virus expression vector. The yeast signal sequence trap system was used to further study the function of the signal peptide of an effector, BxSapB2. In situ hybridization was conducted to investigate the localization of BxSapB2, followed by RNA interference technology (RNAi) to assess the functions of BxSapB2. The results demonstrate that BxSapB2 is a secreted protein that induces cell death in N. benthamiana and is highly expressed in esophageal gland cells and amphids of B. xylophilus. BxSapB2 was determined to be related to the pathogenicity of B. xylophilus. The results of this work indicate that BxSapB2 plays an important role in the interactions between B. xylophilus and the hosts.

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“…This assay were conducted as previously described (Chen C. et al, 2018). Coding sequences (without SPs) of each gene of H. avenae were constructed into the PVX vector pGR107 (Jones et al, 1999), fused with the 3× flag-tag at the N-terminus by an In-Fusion HD Cloning Kit (Clontech, United States).…”

Section: Methodsmentioning

confidence: 99%

A Novel G16B09-Like Effector From Heterodera avenae Suppresses Plant Defenses and Promotes Parasitism

et al. 2019

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Plant parasitic nematodes secrete effectors into host plant tissues to facilitate parasitism. In this study, we identified a G16B09-like effector protein family from the transcriptome of Heterodera avenae, and then verified that most of the members could suppress programmed cell death triggered by BAX in Nicotiana benthamiana. Ha18764, the most homologous to G16B09, was further characterized for its function. Our experimental evidence suggested that Ha18764 was specifically expressed in the dorsal gland and was dramatically upregulated in the J4 stage of nematode development. A Magnaporthe oryzae secretion system in barley showed that the signal peptide of Ha18764 had secretion activity to deliver mCherry into plant cells. Arabidopsis thaliana overexpressing Ha18764 or Hs18764 was more susceptible to Heterodera schachtii. In contrast, BSMV-based host-induced gene silencing (HIGS) targeting Ha18764 attenuated H. avenae parasitism and its reproduction in wheat plants. Transient expression of Ha18764 suppressed PsojNIP, Avr3a/R3a, RBP-1/Gpa2, and MAPK kinases (MKK1 and NPK1Nt)-related cell death in Nicotiana benthamiana. Co-expression assays indicated that Ha18764 also suppressed cell death triggered by four H. avenae putative cell-death-inducing effectors. Moreover, Ha18764 was also shown strong PTI suppression such as reducing the expression of plant defense-related genes, the burst of reactive oxygen species, and the deposition of cell wall callose. Together, our results indicate that Ha18764 promotes parasitism, probably by suppressing plant PTI and ETI signaling in the parasitic stages of H. avenae.

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Large-Scale Identification and Characterization of Heterodera avenae Putative Effectors Suppressing or Inducing Cell Death in Nicotiana benthamiana

Cited by 32 publications

References 65 publications

Differential localization of Hessian fly candidate effectors in resistant and susceptible wheat plants

Differential localization of Hessian fly candidate effectors in resistant and susceptible wheat plants

A key effector, BxSapB2, plays a role in the pathogenicity of the pine wood nematode Bursaphelenchus xylophilus

A Novel G16B09-Like Effector From Heterodera avenae Suppresses Plant Defenses and Promotes Parasitism

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