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A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of Radopholus similis That Inhibits Plant Defense and Facilitates Parasitism.

ABSTRACT: Radopholus similis is a migratory endoparasitic nematode that is extremely harmful to host plants. Venom allergen-like proteins (VAPs) are members of the cysteine-rich secretory protein family that are widely present in plants and animals. In this study, we cloned a VAP gene from R. similis, designated as RsVAP. RsVAP contains an open reading frame of 1089 bp encoding 362 amino acids. RsVAP is specifically expressed in the esophageal gland, and the expression levels of RsVAP are significantly higher in juveniles than in other life stages of R. similis. This expression pattern of RsVAP was consistent with the biological characteristics of juveniles of R. similis, which have the ability of infection and are the main infection stages of R. similis. The pathogenicity and reproduction rate of R. similis in tomato was significantly attenuated after RsVAP was silenced. In tobacco leaves transiently expressing RsVAP, the pathogen-associated molecular pattern-triggered immunity (PTI) induced by a bacterial flagellin fragment (flg22) was inhibited, while the cell death induced by two sets of immune elicitors (BAX and Gpa2/RBP-1) was repressed. The RsVAP-interacting, ras-related protein RABA1d (LeRabA1d) was identified in tomato hosts by yeast two-hybrid and co-immunoprecipitation assays. RsVAP may interact with LeRabA1d to affect the host defense response, which in turn facilitates nematode infection. This study provides the first evidence for the inhibition of plant defense response by a VAP from migratory plant-parasitic nematodes, and, for the first time, the target protein of R. similis in its host was identified.

SUBMITTER: Li J

PROVIDER: S-EPMC8125365 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Banana (Musa spp. L.) is an important staple food and cash crop for about 30% of the population in Tanzania; however, the burrowing plant-parasitic nematode Radopholus similis causes black head disease and toppling in banana plants, which results in yield losses. We collected and identified 80 specimens of R. similis from four agro-ecological zones in Tanzania using morphological characters. We then used universal and specific R. similis primers to amplify the small subunit, internal transcribed spacer and large subunit of ribosomal DNA regions of these specimens. The amplicons were subsequently sequenced and analyzed using Bayesian inference. We identified two major clades, one that comprised all R. similis sequences derived from this study and another that included R. similis and Radopholus spp. sequences obtained from GenBank, indicating the separation of this species from congeneric sequences. Our findings provide a useful, simple and rapid method for identifying burrowing nematodes. This outcome could contribute to the development of permanent, integrated pest management strategies for the control of R. similis in banana and other crops in order to reduce associated yield losses in Tanzania. To our knowledge, this is the first study of nematodes to use combined morphological and molecular methods for the identification of R. similis in Tanzania.Banana (Musa spp. L.) is an important staple food and cash crop for about 30% of the population in Tanzania; however, the burrowing plant-parasitic nematode Radopholus similis causes black head disease and toppling in banana plants, which results in yield losses. We collected and identified 80 specimens of R. similis from four agro-ecological zones in Tanzania using morphological characters. We then used universal and specific R. similis primers to amplify the small subunit, internal transcribed spacer and large subunit of ribosomal DNA regions of these specimens. The amplicons were subsequently sequenced and analyzed using Bayesian inference. We identified two major clades, one that comprised all R. similis sequences derived from this study and another that included R. similis and Radopholus spp. sequences obtained from GenBank, indicating the separation of this species from congeneric sequences. Our findings provide a useful, simple and rapid method for identifying burrowing nematodes. This outcome could contribute to the development of permanent, integrated pest management strategies for the control of R. similis in banana and other crops in order to reduce associated yield losses in Tanzania. To our knowledge, this is the first study of nematodes to use combined morphological and molecular methods for the identification of R. similis in Tanzania.

Project description:Radopholus similis is a destructive, migratory, and endophytoparasitic nematode. It has two morphologically indistinguishable pathotypes (or physiological races): banana and citrus pathotypes. At present, the only reliable method to differentiate the two pathotypes is testing the infestation and parasitism of nematodes on Citrus spp. via inoculation. However, differences in inoculation methods and conditions adopted by different researchers complicate obtaining consistent results. In this study, the parasitism and pathogenicity of 10 R. similis populations on rough lemon (Citrus limon) seedlings and the tropism and invasion of rough lemon roots were tested. It revealed that populations SWK, GJ, FZ, GZ, DBSR, and YJ were citrus pathotypes, which showed parasitism and pathogenicity on rough lemon and could invade rough lemon roots, whereas populations XIN, ML, HN6, and HL were banana pathotypes, having no parasitism and pathogenicity on rough lemon and they did not invade the rough lemon roots. Four pectate lyase genes (Rs-pel-2, Rs-pel-3, Rs-pel-4, and Rs-pel-5) belonging to the Class III family from these populations were amplified and analysed. The gene Rs-pel-3 could be amplified from six citrus pathotype populations and was stably expressed in the four developmental stages of the nematode, whereas it could not be amplified from the four banana pathotypes. Rs-pel-3 expression may be related to the parasitism and pathogenicity of R. similis on rough lemon. Hence, it can be used as a molecular marker to distinguish between banana and citrus pathotypes and as a target gene for the molecular identification of these two pathotypes. KEY POINTS: • Four pectate lyase genes (Rs-pels) from Radopholus similis were cloned and analysed. • The expression of Rs-pels is different in two pathotypes of Radopholus similis. • A molecular identification method for two pathotypes of Radopholus similis using pectate lyase gene Rs-pel-3 as the target gene was established.

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A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of Radopholus similis That Inhibits Plant Defense and Facilitates Parasitism.

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