Analyses of the Root-Knot Nematode (Meloidogyne graminicola) Transcriptome during Host Infection Highlight Specific Gene Expression Profiling in Resistant Rice Plants

Abstract

The plant-parasitic nematode Meloidogyne graminicola causes considerable damages to rice (Oryza sativa) culture. Resistance to M. graminicola in the related species Oryza glaberrima reduces root penetration by juveniles and stops further nematode development. M. graminicola genes expressed during O. sativa infection were previously characterized but no information is available about the molecular dialogue established with a resistant plant. We compared the M. graminicola transcriptomes of stage-two juveniles (J2s) before and during infection of susceptible or resistant rice. Among 36,121 M. graminicola genes surveyed, 367 were differentially expressed during infection of resistant or susceptible plants. Genes encoding cell wall-degrading enzymes, peptidases and neuropeptides were expressed for a longer time in resistant plants compared to susceptible plants. Conversely, genes related to nematode development were not activated in the resistant host. The majority of M. graminicola effector genes had similar expression patterns, whatever the host genotype. However, two venom allergen-like protein (VAP)-encoding genes were specifically induced in resistant plants and Mg-VAP1 silencing in J2s reduced their ability to colonize roots. This study highlighted that M. graminicola adapts its gene expression to the host susceptibility. Further investigation is required to assess the role of Mg-VAPs in the rice–nematode interaction.

Genome expression dynamics reveals parasitism regulatory landscape of the root-knot nematodeMeloidogyne incognitaand a promoter motif associated with effector genes

“…At early stages (transition from eggs to ppJ2), M. incognita expresses genes involved in chemosensation and movement, supporting the host recognition and attraction. Induction of these groups of genes correlated with the preparation of parasitism have been reported in other PPNs, for example Meloidogyne graminicola [48], Globodera pallida [49] and the migratory endoparasite Radopholus similis [50]. RNAi mediated down-regulation of such chemosensory (e.g odr genes) or neuropeptide genes (e.g npl-3 or npl-12 genes) displayed a significant alteration of attraction and penetration of M. incognita ppJ2 to host roots, supporting their importance at early events of plant parasitism [51,52].…”

“…To explore the transcriptional regulation of parasitism, we first identified loci that encode previously known effectors with experimental evidence of expression in the two sets of pharyngeal glands: sub-ventral (SvG) or dorsal pharyngeal gland (DG) cells. From the literature, we identified 48 Two anomalies are noted. Firstly, the effector 35A02 (msp25) described as specifically expressed in the SvG in [39] is 97% identical to Minc02097, conversely detected in the DG in [40].…”

Genome Expression Dynamics Reveal the Parasitism Regulatory Landscape of the Root-Knot Nematode Meloidogyne incognita and a Promoter Motif Associated with Effector Genes

“…These observations make sense with the particular time point of the pre-parasitic life stages of the animal, in which the triggering of signaling pathways accompanies hatched ppJ2s that actively sense root exudates and move towards their host, supporting host recognition and attraction. The induction of these groups of genes correlated with the preparation of parasitism and have been reported in other PPNs, including Meloidogyne graminicola [ 48 ], Globodera pallida [ 49 ], and the migratory endoparasite Radopholus similis [ 50 ]. The RNAi mediated downregulation of such chemosensory (e.g., odr genes) or neuropeptide genes (e.g., npl-3 or npl-12 genes) resulted in a significant alteration in the attraction and penetration of M. incognita ppJ2 to host roots, supporting their importance at early events of plant parasitism [ 51 , 52 ].…”

Meloidogyne graminicola—A Threat to Rice Production: Review Update on Distribution, Biology, Identification, and Management

“…Over the past years, novel Mg effectors playing a role in nematode parasitism were functionally characterized, including pioneer genes [ 167 , 168 ], a C-type lectin [ 169 ], and a protein disulfide isomerase [ 170 ]. In 2020, Petitot et al [ 171 ] analyzed mRNA-seq data derived from nematode-infected rice tissue to identify nematode transcripts specifically expressed when the nematode resides inside the plant, through a comprehensive transcriptome analyses of J2 and rice infected tissues until the development of young adult females. Dash et al [ 172 ] delivered a transcriptome comparison of nematode-resistant and -susceptible rice plants in the same genetic background.…”