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

Abstract

Background and Aims The root-knot nematode Meloidogyne graminicola is responsible for production losses in rice (Oryza sativa) in Asia and Latin America. The accession TOG5681 of African rice, O. glaberrima, presents improved resistance to several biotic and abiotic factors, including nematodes. The aim of this study was to assess the cytological and molecular mechanisms underlying nematode resistance in this accession.Methods Penetration and development in M. graminicola in TOG5681 and the susceptible O. sativa genotype 'Nipponbare' were compared by microscopic observation of infected roots and histological analysis of galls. In parallel, host molecular responses to M. graminicola were assessed by root transcriptome profiling at 2, 4 and 8 d postinfection (dpi). Specific treatments with hormone inhibitors were conducted in TOG5681 to assess the impact of the jasmonic acid and salicylic acid pathways on nematode penetration and reproduction.Key Results Penetration and development of M. graminicola juveniles were reduced in the resistant TOG5681 in comparison with the susceptible accession, with degeneration of giant cells observed in the resistant genotype from 15 dpi onwards. Transcriptome changes were observed as early as 2 dpi, with genes predicted to be involved in defence responses, phenylpropanoid and hormone pathways strongly induced in TOG5681, in contrast to 'Nipponbare'. No specific hormonal pathway could be identified as the major determinant of resistance in the ricenematode incompatible interaction. Candidate genes proposed as involved in resistance to M. graminicola in TOG5681 were identified based on their expression pattern and quantitative trait locus (QTL) position, including chalcone synthase, isoflavone reductase, phenylalanine ammonia lyase, WRKY62 transcription factor, thionin, stripe rust resistance protein, thaumatins and ATPase3.Conclusions This study provides a novel set of candidate genes for O. glaberrima resistance to nematodes and highlights the rice-M. graminicola pathosystem as a model to study plant-nematode incompatible interactions.

Gene expression analysis inMusa acuminataduring compatible interactions withMeloidogyne incognita

“…Although RKN infection has been associated with suppression of ET responses (Barcala et al, 2010;Nahar et al, 2011;Kyndt et al, 2012b), patterns of repression or activation have also been observed in both incompatible and compatible interactions between rice and M. graminicola (Petitot et al, 2017). Our data revealed similar patterns, with numerous ET signalling-related proteins and ERF activators up-or downregulated amongst the DEGs.…”

Cereal Root Interactions with Soilborne Pathogens—From Trait to Gene and Back

“…Six defense genes were induced in the resistant wheat, but only three were induced in the susceptible cultivar, suggesting that the latter had an attenuated jasmonate signal pathway. A number of studies have linked changes in lignin to both the nematode infection process and to host-nematode interactions [4,6,13,58,76]. Thompson et al [25] found that the resistant landrace IWA8608077 had higher lignin content than the susceptible Louise [77].…”

“…Of the 16 target genes, 12 resulted in reduction in nematode egg masses and/or gall counts in root infection assays when gene function was disrupted. This approach identified novel pathogenicity proteins and narrowed the candidate gene pool to a feasible number for further testing A transcriptome study of root responses to M. graminicola infection was carried out using the resistant African rice, Oryza glaberrima, and a susceptible japonica cultivar of O. sativa [6]. In the resistant rice, nematode penetration was reduced, and females were smaller and laid fewer eggs compared to the susceptible rice.…”

“…Smith) Sacc., Pratylenchus neglectus (Rensch, 1924) Filijev and Stuurmans Stekhoven, 1941, P. thornei Scher and Allen, 1953, Hereodera avenae Wollenweber, 1924, and Meloidogyne graminicola. These pathogens are problems in the dryland production regions of the Pacific Northwest, USA (PNW), Australia, Europe, China, Southeast Asia, India, and other parts of the world [2][3][4][5][6][7]. Furthermore, a body of knowledge is accumulating about the cellular and molecular interactions between these hosts and pathogens that are helping to elucidate the basis of susceptibility and resistance, e.g., References [8][9][10][11][12][13].…”

Proteome-Wide Analyses Provide New Insights into the Compatible Interaction of Rice with the Root-Knot Nematode Meloidogyne graminicola

“…Analyses of the transcriptome of NPB giant cells at 7 and 14 dpi by using both laser-capture microdissection and RNA-seq indicated that the expression of genes associated with chloroplast biogenesis and tetrapyrrole synthesis was notably changed, while the majority of defense-related genes were extremely suppressed by infection of M. graminicola [11]. Through comparison of the transcriptomes of rice accessions compatibly and incompatibly interacting with M. graminicola at 2, 4 and 8 dpi, 32 potential M. graminicola-resistance-associated genes such as phenylalanine ammonia lyase, thionin and chalcone synthase genes were identified [12]. However, the rice genes underlying resistance to M. graminicola are not yet clear.…”