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Fatty acid-and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes.

ABSTRACT: Plant-parasitic nematodes produce at least one structurally unique class of small helix-rich retinol- and fatty-acid-binding proteins that have no counterparts in their plant hosts. Herein we describe a protein of the plant-parasitic root-knot nematode Meloidogyne javanica, which is a member of the nematode-specific fatty-acid- and retinol-binding (Mj-FAR-1) family of proteins. The mj-far-1 mRNA was detected through M. javanica pre-parasitic J2s, migratory and sedentary parasitic stages by quantitative reverse transcriptase polymerase chain reaction (qRT-PCR). Immunolocalization assays demonstrate that the FAR protein of Meloidogyne is secreted during sedentary stages, as evidenced by the accumulation of FAR at the nematode cuticle surface and along the adjacent host root tissues. Tomato roots constitutively expressing mj-far-1 demonstrated an increased susceptibility to root-knot nematodes infection as observed by accelerated gall induction and expansion, accompanied by a higher percentage of nematodes developing into mature females compared to control roots. RNA interference assays that expressed double-stranded RNA complementary to mj-far-1 in transgenic tomato lines specifically reduced nematode infection levels. Histological analysis of nematode-infested roots indicated that in roots overexpressing mj-far-1, galls contained larger feeding cells and might support a faster nematode development and maturation. Roots overexpressing mj-far-1 suppressed jasmonic acid responsive genes such as the proteinase inhibitor (Pin2) and ?-thionin, illustrating the possible role of Mj-FAR-1 in manipulating the lipid based signaling in planta. This data, suggests that Meloidogyne FAR might have a strategic function during the interaction of the nematode with its plant host. Our study present the first demonstration of an in planta functional characterization and localization of FAR proteins secreted by plant-parasitic nematodes. It provides evidence that Mj-FAR-1 facilitates infection most likely via the manipulation of host lipid-based defenses, as critical components for a successful parasitism by plant-parasitic nematodes.

SUBMITTER: Iberkleid I

PROVIDER: S-EPMC3661543 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Fatty acid-and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes.

Iberkleid Ionit I Vieira Paulo P de Almeida Engler Janice J Firester Kalia K Spiegel Yitzhak Y Horowitz Sigal Brown SB

PloS one 20130522 5

Plant-parasitic nematodes produce at least one structurally unique class of small helix-rich retinol- and fatty-acid-binding proteins that have no counterparts in their plant hosts. Herein we describe a protein of the plant-parasitic root-knot nematode Meloidogyne javanica, which is a member of the nematode-specific fatty-acid- and retinol-binding (Mj-FAR-1) family of proteins. The mj-far-1 mRNA was detected through M. javanica pre-parasitic J2s, migratory and sedentary parasitic stages by quant ...[more]

PMID: 23717636

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Project description:BackgroundThe secreted Meloidogyne javanica fatty acid- and retinol-binding (FAR) protein Mj-FAR-1 is involved in nematode development and reproduction in host tomato roots. To gain further insight into the role of Mj-FAR-1 in regulating disease development, local transcriptional changes were monitored in tomato hairy root lines with constitutive mj-far-1 expression compared with control roots without inoculation, and 2, 5 and 15 days after inoculation (DAI), using mRNA sequencing analysis.ResultsGene-expression profiling revealed a total of 3970 differentially expressed genes (DEGs) between the two lines. Among the DEGs, 1093, 1039, 1959, and 1328 genes were up- or downregulated 2-fold with false discovery rate < 0.001 in noninoculated roots, and roots 2, 5, and 15 DAI compared with control roots, respectively. Four main groups of genes that might be associated with Mj-FAR-1-mediated susceptibility were identified: 1) genes involved in biotic stress responses such as pathogen-defense mechanisms and hormone metabolism; 2) genes involved in phenylalanine and phenylpropanoid metabolism; 3) genes associated with cell wall synthesis, modification or degradation; and 4) genes associated with lipid metabolism. All of these genes were overrepresented among the DEGs. Studying the distances between the treatments, samples from noninoculated roots and roots at 2 DAI clustered predominantly according to the temporal dynamics related to nematode infection. However, at the later time points (5 and 15 DAI), samples clustered predominantly according to mj-far-1 overexpression, indicating that at these time points Mj-FAR-1 is more important in defining a common transcriptome.ConclusionsThe presence of four groups of DEGs demonstrates a network of molecular events is mediated by Mj-FAR-1 that leads to highly complex manipulation of plant defense responses against nematode invasion. The results shed light on the in vivo role of secreted FAR proteins in parasitism, and add to the mounting evidence that secreted FAR proteins play a major role in nematode parasitism.

Project description:Beneficial microorganisms are generally known to activate plant defense against biotic challenges. However, the molecular mechanisms by which activated plants react more rapidly and actively to pests remain still largely unclear. Tomato plants pre-treated with a mixture of beneficial bio-control agents (BCAs), as soil-drenches, were less sensitive to infection of the root-knot nematode (RKN) Meloidogyne incognita. To unravel the molecular mechanisms of this induced resistance against RKNs, we used qRT-PCR to monitor the expression, in tomato roots and leaves, of 6 key defense genes. Gene transcripts were detected until the 12th day after BCA treatment(3, 7, 8, 12 dpt) and3 and 7 days after nematode inoculation of pre-treated plants. Early after BCA treatment, the salicylic acid (SA)-dependent pathogenesis related gene (PR-gene), PR-1b, marker of the systemic acquired resistance (SAR), was systemically over-expressed. Another PR-gene, PR-5, was over-expressed at later stages of BCA-plant interaction, and only in roots. Activation of defense against RKNs was attested by the early up-regulation of 4 genes (PR-1, PR-3, PR-5, ACO) in pre-treated plants after inoculation. Conversely, the expression of the JA/ET-dependent gene JERF3 did not increase after nematode inoculation in primed plants. A catalase gene (CAT)was highly over-expressed by nematode infection, however, this over-expression was annulled at the earliest stages or limited at the later stages of infection toBCA-treated roots. Enzyme activities, such as glucanase and endochitinase, were enhanced in roots of pre-treated inoculated plants with respect to plants left not inoculated as a control. These findings indicate that BCA interaction with roots primes plants against RKNs. BCA-mediated immunity seems to rely on SA-mediated SAR and to be associated with both the activation of chitinase and glucanase enzyme activities and the inhibition of the plant antioxidant enzyme system. Immunity is triggered at the penetration and movements inside the roots of the invading nematode juveniles but probably acts at the feeding site building stage of nematode infection.

Dataset Information

Fatty acid-and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes.

Publications

Fatty acid-and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes.

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