Dataset Information

Heterodera avenae GLAND5 Effector Interacts With Pyruvate Dehydrogenase Subunit of Plant to Promote Nematode Parasitism.

ABSTRACT: Heterodera avenae mainly infects cereal crops and causes severe economic losses. Many studies have shown that parasitic nematodes can secrete effector proteins to suppress plant immune responses and then promote parasitism. In this study, we showed that HaGland5, a novel effector of H. avenae, was exclusively expressed in dorsal esophageal gland cell of nematode, and up-regulated in the early parasitic stage. Transgenic Arabidopsis thaliana lines expressing HaGland5 were significantly more susceptible to H. schachtii than wild-type control plants. Conversely, silencing of HaGland5 through barley stripe mosaic virus-medicated host-induced gene silencing technique substantially reduced the infection of H. avenae in wheat. Moreover, HaGland5 could suppress the plant defense responses, including the repression of plant defense-related genes, reducing deposition of cell wall callose and the burst of reactive oxygen species. Mass spectrometry, co-immunoprecipitation, and firefly luciferase complementation imaging assays confirmed that HaGland5 interacted specifically with Arabidopsis pyruvate dehydrogenase subunit (AtEMB3003).

SUBMITTER: Yang S

PROVIDER: S-EPMC6558007 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Heterodera avenae GLAND5 Effector Interacts With Pyruvate Dehydrogenase Subunit of Plant to Promote Nematode Parasitism.

Yang Shanshan S Pan Lingling L Chen Yongpan Y Yang Dan D Liu Qian Q Jian Heng H

Frontiers in microbiology 20190604

Heterodera avenae mainly infects cereal crops and causes severe economic losses. Many studies have shown that parasitic nematodes can secrete effector proteins to suppress plant immune responses and then promote parasitism. In this study, we showed that HaGland5, a novel effector of H. avenae, was exclusively expressed in dorsal esophageal gland cell of nematode, and up-regulated in the early parasitic stage. Transgenic Arabidopsis thaliana lines expressing HaGland5 w ...[more]

PMID: 31214156

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Project description:One of the reasons for the progressive yield decline observed in cereals production is the rapid build-up of populations of the cereal cyst nematode (CCN, Heterodera avenae). These nematodes secrete so-call effectors into their host plant to suppress the plant defense responses, alter plant signaling pathways and then induce the formation of syncytium after infection. However, little is known about its molecular mechanism and parasitism during incompatible infection. To gain insight into its repertoire of parasitism genes, we investigated the transcriptome of the early parasitic second-stage (30 hours, 3 days and 9 days post infection) juveniles of the CCN as well as the CCN infected tissue of the host Aegilops variabilis by Illumina sequencing. Among all assembled unigenes, 681 putative genes of parasitic nematode were found, in which 56 putative effectors were identified, including novel pioneer genes and genes corresponding to previously reported effectors. All the 681 CCN unigenes were mapped to 229 GO terms and 200 KEGG pathways, including growth, development and several stimulus-related signaling pathways. Sixteen clusters were involved in the CCN unigene expression atlas at the early stages during infection process, and three of which were significantly gene-enriched. Besides, the protein-protein interaction network analysis revealed 35 node unigenes which may play an important role in the plant-CCN interaction. Moreover, in a comparison of differentially expressed genes between the pre-parasitic juveniles and the early parasitic juveniles, we found that hydrolase activity was up-regulated in pre J2s whereas binding activity was upregulated in infective J2s. RT-qPCR analysis on some selected genes showed detectable expression, indicating possible secretion of the proteins and putative role in infection. This study provided better insights into the incompatible interaction between H. avenae and the host plant Ae. varabilis. Moreover, RNAi targets with potential lethality were screened out and primarily validated, which provide candidates for engineering-based control of cereal cyst nematode in crops breeding.

Project description:BACKGROUND:Cereal cyst nematode Heterodera avenae, an important soil-borne pathogen in wheat, causes numerous annual yield losses worldwide, and use of resistant cultivars is the best strategy for control. However, target genes are not readily available for breeding resistant cultivars. Therefore, comparative transcriptomic analyses were performed to identify more applicable resistance genes for cultivar breeding. METHODS:The developing nematodes within roots were stained with acid fuchsin solution. Transcriptome assemblies and redundancy filteration were obtained by Trinity, TGI Clustering Tool and BLASTN, respectively. Gene Ontology annotation was yielded by Blast2GO program, and metabolic pathways of transcripts were analyzed by Path_finder. The ROS levels were determined by luminol-chemiluminescence assay. The transcriptional gene expression profiles were obtained by quantitative RT-PCR. RESULTS:The RNA-sequencing was performed using an incompatible wheat cultivar VP1620 and a compatible control cultivar WEN19 infected with H. avenae at 24 h, 3 d and 8 d. Infection assays showed that VP1620 failed to block penetration of H. avenae but disturbed the transition of developmental stages, leading to a significant reduction in cyst formation. Two types of expression profiles were established to predict candidate resistance genes after developing a novel strategy to generate clean RNA-seq data by removing the transcripts of H. avenae within the raw data before assembly. Using the uncoordinated expression profiles with transcript abundance as a standard, 424 candidate resistance genes were identified, including 302 overlapping genes and 122 VP1620-specific genes. Genes with similar expression patterns were further classified according to the scales of changed transcript abundances, and 182 genes were rescued as supplementary candidate resistance genes. Functional characterizations revealed that diverse defense-related pathways were responsible for wheat resistance against H. avenae. Moreover, phospholipase was involved in many defense-related pathways and localized in the connection position. Furthermore, strong bursts of reactive oxygen species (ROS) within VP1620 roots infected with H. avenae were induced at 24 h and 3 d, and eight ROS-producing genes were significantly upregulated, including three class III peroxidase and five lipoxygenase genes. CONCLUSIONS:Large-scale identification of wheat resistance genes were processed by comparative transcriptomic analysis. Functional characterization showed that phospholipases associated with ROS production played vital roles in early defense responses to H. avenae via involvement in diverse defense-related pathways as a hub switch. This study is the first to investigate the early defense responses of wheat against H. avenae, not only provides applicable candidate resistance genes for breeding novel wheat cultivars, but also enables a better understanding of the defense mechanisms of wheat against H. avenae.

Dataset Information

Heterodera avenae GLAND5 Effector Interacts With Pyruvate Dehydrogenase Subunit of Plant to Promote Nematode Parasitism.

Publications

<i>Heterodera avenae</i> GLAND5 Effector Interacts With Pyruvate Dehydrogenase Subunit of Plant to Promote Nematode Parasitism.

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