Evolutionarily conserved plant genes responsive to root-knot nematodes identified by comparative genomics

Abstract

Root-knot nematodes (RKNs, genus Meloidogyne) affect a large number of crops causing severe yield losses worldwide, more specifically in tropical and sub-tropical regions. Several plant species display high resistance levels to Meloidogyne, but a general view of the plant immune molecular responses underlying resistance to RKNs is still lacking. Combining comparative genomics with differential gene expression analysis may allow the identification of widely conserved plant genes involved in RKN resistance. To identify genes that are evolutionary conserved across plant species, we used OrthoFinder to compared the predicted proteome of 22 plant species, including important crops, spanning 214 Myr of plant evolution. Overall, we identified 35,238 protein orthogroups, of which 6,132 were evolutionarily conserved and universal to all the 22 plant species (PLAnts Common Orthogroups—PLACO). To identify host genes responsive to RKN infection, we analyzed the RNA-seq transcriptome data from RKN-resistant genotypes of a peanut wild relative (Arachis stenosperma), coffee (Coffea arabica L.), soybean (Glycine max L.), and African rice (Oryza glaberrima Steud.) challenged by Meloidogyne spp. using EdgeR and DESeq tools, and we found 2,597 (O. glaberrima), 743 (C. arabica), 665 (A. stenosperma), and 653 (G. max) differentially expressed genes (DEGs) during the resistance response to the nematode. DEGs’ classification into the previously characterized 35,238 protein orthogroups allowed identifying 17 orthogroups containing at least one DEG of each resistant Arachis, coffee, soybean, and rice genotype analyzed. Orthogroups contain 364 DEGs related to signaling, secondary metabolite production, cell wall-related functions, peptide transport, transcription regulation, and plant defense, thus revealing evolutionarily conserved RKN-responsive genes. Interestingly, the 17 DEGs-containing orthogroups (belonging to the PLACO) were also universal to the 22 plant species studied, suggesting that these core genes may be involved in ancestrally conserved immune responses triggered by RKN infection. The comparative genomic approach that we used here represents a promising predictive tool for the identification of other core plant defense-related genes of broad interest that are involved in different plant–pathogen interactions.

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Acknowledgements

This work was supported by grants/fellowships from EMBRAPA, UCB, CNPq-INCT, CAPES, and FAPDF. We are grateful to Dr. Regina Carneiro (Embrapa Cenargen, Brazil) for valuable contributions and for providing and characterizing Meloidogyne spp. We would like to thank the SPIBOC (INRA, Sophia-Antipolis) and CENARGEN (Embrapa, Brasília) Bioinformatics platform for technical help and advices.

Funding

APZM, BPMA, and FBMA received a PhD grant from the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES, Brazil), and APZM and FBMA also received CAPES mobility grants to France. DF was supported by a visiting scientist grant from the Science without Boarders program (project no. 400328/2012-7) from the Brazilian National Council for Scientific and Technological Development (CNPq, Brasil). ED was supported by a visiting scientist grant. Part of this research was funded by project 002/14 from the Agropolis Fondation (Montpellier, France), Embrapa and CAPES (Brazil) under the reference ID (1402-004) and under the program "Investissement d'avenir" ANR-10-LABX-001-01, Labex Agro, by the INCT PlantStress Biotech (project number 465480/2014-4); and the FAPDF-Distrito Federal Research Foundation (project number no.193001265/2017).

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ACBM, PMG, MFGS, EVSA, ASP, PG, and DF conceived the project. APZM, ACBM, PMG, EVSA, DF, PG, and MFGS designed the experiments. APZM and ED conceived, designed, and performed the bioinformatics pipelines, and analyzed the results. APZM, MAPS, ASP, BPM, DF, and EVSA executed the qPCR experiments. ACBM, PMG, MAPS, ASP, DF, EVSA, and MELS produced the plant samples for transcriptomics. APZM, EGJD, ACMB, PMG, EVSA, ASP, DF, and MFGS wrote and revised the manuscript. All authors have read and approved the final manuscript.

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Correspondence to Maria Fatima Grossi-de-Sa.

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Mota, A.P.Z., Fernandez, D., Arraes, F.B.M. et al. Evolutionarily conserved plant genes responsive to root-knot nematodes identified by comparative genomics. Mol Genet Genomics 295, 1063–1078 (2020). https://doi.org/10.1007/s00438-020-01677-7

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Keywords

  • Transcriptome
  • Meloidogyne
  • Arachis
  • Soybean
  • Coffee
  • Rice