Meloidogyne incognita - rice (Oryza sativa) interaction: a new model system to study plant-root-knot nematode interactions in monocotyledons

Abstract

BackgroundPlant-parasitic nematodes developed strategies to invade and colonize their host plants, including expression of immune suppressors to overcome host defenses. Meloidogyne graminicola and M. incognita are root-knot nematode (RKN) species reported to damage rice (Oryza sativa L.) cultivated in upland and irrigated systems. Despite M. incognita wide host range, study of the molecular plant - RKN interaction has been so far limited to a few dicotyledonous model plants. The aim of this study was to investigate if the rice cv. Nipponbare widely used in rice genomic studies could be used as a suitable monocotyledon host plant for studying M. incognita pathogenicity mechanisms. Here we compared the ability of M. graminicola and M. incognita to develop and reproduce in Nipponbare roots. Next, we tested if RKNs modulates rice immunity-related genes expression in galls during infection and express the Mi-crt gene encoding an immune suppressor.ResultsRoot galling, mature females, eggs and newly formed J2s nematodes were obtained for both species in rice cultivated in hydroponic culture system after 4-5 weeks. Meloidogyne graminicola reproduced at higher rates than M. incognita on Nipponbare and the timing of infection was shorter. In contrast, the infection characteristics compared by histological analysis were similar for both nematode species. Giant cells formed from 2 days after infection (DAI) with M. graminicola and from 6 DAI with M. incognita. Real-time PCR (qRT-PCR) data indicated that RKNs are able to suppress transcription of immune regulators genes, such as OsEDS1, OsPAD4 and OsWRKY13 in young galls. Four M. incognita reference genes (Mi-eif-3, Mi-GDP-2, Mi-Y45F10D.4, and Mi-actin) were selected for normalizing nematode gene expression studies in planta and in pre-parasitic J2s. Meloidogyne incognita expressed the immune suppressor calreticulin gene (Mi-crt) in rice roots all along its infection cycle.ConclusionRKNs repress the transcription of key immune regulators in rice, likely in order to lower basal defence in newly-formed galls. The calreticulin Mi-CRT can be one of the immune-modulator effectors secreted by M. incognita in rice root tissues. Together, these data show that rice is a well suited model system to study host- M. incognita molecular interactions in monocotyledons.Electronic supplementary materialThe online version of this article (doi:10.1186/s12284-014-0023-4) contains supplementary material, which is available to authorized users.

Transcriptomic and histological responses of African rice (Oryza glaberrima) to Meloidogyne graminicola provide new insights into root-knot nematode resistance in monocots

“…Meloidogyne graminicola may infect rice roots and complete its life cycle in < 3 weeks under favourable temperatures (Fernandez et al, 2014;Nguyen et al, 2014). Meloidogyne spp.…”

“…Nematode stage 2 juveniles (J2) enter roots close to the apex at the elongation zone, and then reach the root central cylinder, where they initiate a feeding site from a set of parenchyma cells. This process may be observed as soon as 2 d post-infection (dpi) (Nguyen et al, 2014). In response to nematode signals, the parenchyma cells differentiate into multinucleate and metabolically active giant cells (GCs), resembling transfer cells Rodiuc et al, 2014), enabling M. graminicola to withdraw nutrients from the plant's vascular system.…”

“…A gall may contain several feeding sites and nematodes. The juvenile then goes through several developmental stages (J3, J4) to finally differentiate into a female (from 14 dpi), which will lay numerous eggs inside the root tissue (Nguyen et al, 2014). During root invasion, M. graminicola juveniles express a high number of genes encoding cell wall-degrading enzymes and virulence effectors to enter, migrate into roots and induce GC formation (Haegeman et al, 2013;Petitot et al, 2015).…”

Gene expression analysis inMusa acuminataduring compatible interactions withMeloidogyne incognita

“…Recent transcriptome analysis of gall tissues induced by the biotrophic RKN M. graminicola has revealed suppression of ETI, SA and ET/JA defence pathways, together with activation of gibberellic acid and BR biosynthesis and signalling (Kyndt et al, 2012a;Ji et al, 2013;Nahar et al, 2013;Nguyên et al, 2014). The phytohormone ABA, although more typically associated with abiotic stress responses, together with auxins, BRs, cytokinins and gibberellins, which are known regulators of plant developmental, also all appear to play overlapping roles in plant immune responses to RKNs (Kyndt et al, 2014).…”

“…Most research to date on host gene expression in response to RKNs has focused on interactions in dicotyledonous host plants (e.g. Jammes et al, 2005;Alkharouf et al, 2006;Ithal et al, 2007a;Klink et al, 2007;Szakasits et al, 2009;Barcala et al, 2010;Bagnaresi et al, 2013;Guimaraes et al, 2015), with relatively few studies on monocotyledonous hosts (Kyndt et al, 2012a;Ji et al, 2013;Nguyên et al, 2014). Analysis of the transcriptome of compatible interactions between nematodes and monocotyledonous hosts has so far been limited to studies only on rice.…”