Abstract
Main conclusion
This study revealed novel insights into the function of MSP18 effector during root-knot nematode parasitism in rice roots. MSP18 may modulate host immunity and enhance plant susceptibility to Meloidogyne spp.
Abstract
Rice (Oryza sativa) production is seriously impacted by root-knot nematodes (RKN), including Meloidogyne graminicola, Meloidogyne incognita, and Meloidogyne javanica, in upland and irrigated culture systems. Successful plant infection by RKN is likely achieved by releasing into the host cells some effector proteins to suppress the activation of immune responses. Here, we conducted a series of functional analyses to assess the role of the Meloidogyne-secreted protein (MSP) 18 from M. incognita (Mi-MSP18) during rice infection by RKN. Developmental expression profiles of M. javanica and M. graminicola showed that the MSP18 gene is up-regulated throughout nematode parasitic stages in rice. Reproduction of M. javanica and M. graminicola is enhanced in rice plants overexpressing Mi-MSP18, indicating that the Mi-MSP18 protein facilitates RKN parasitism. Transient expression assays in onion cells suggested that Mi-MSP18 is localized to the cytoplasm of the host cells. In tobacco, Mi-MSP18 suppressed the cell death induced by the INF1 elicitin, suggesting that Mi-MSP18 can interfere with the plant defense pathways. The data obtained in this study highlight Mi-MSP18 as a novel RKN effector able to enhance plant susceptibility and modulate host immunity.
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Abbreviations
- DAI:
-
Days after inoculation
- HR:
-
Hypersensitive response
- J2/J3/J4:
-
Second/third/fourth stages of Meloidogyne juvenile
- MSP:
-
Meloidogyne-secreted protein
- Mg :
-
Meloidogyne graminicola
- Mi :
-
Meloidogyne incognita
- Mj :
-
Meloidogyne javanica
- PCD:
-
Programmed cell death
- RKN:
-
Root-knot nematodes
- SP:
-
Signal peptide
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Acknowledgements
We are grateful to Delphine Mieulet and Emmanuel Guiderdoni (CIRAD, Montpellier France) from the Rice Functional Genomics Platform (http://www.refuge-platform.org/) for assistance in rice transformation, and to Geert Smant and José Lozano-Torres (Wageningen University, Netherlands) for providing with INF1 constructs.
Funding
MGS received a Ph.D. grant, DXA received a junior post doc grant, and 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). MAB, IM and MELS received mobility grants from the Coordination for the Improvement of Higher Education Personnel (CAPES, Brazil). Part of this research was funded by Agropolis Fondation (Montpellier, France) under the reference ID “Identification of nematode (Meloidogyne spp.) effectors of pathogenicity in rice (O. sativa)” AA1002–003 and under the program “Investissement d’avenir” ANR-10-LABX-001-01, Labex Agro.
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Sequence data from this article can be found in the GenBank under accession numbers MK628545 and MK628546.
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Online Resource S2 Sources and platforms for genomic and transcriptomic analyses used for MSP18 BLAST searches (PDF 204 kb)
Online Resource S3 Meloidogyne javanica developmental stages at 21 days after infection (PDF 343 kb)
425_2019_3205_MOESM6_ESM.pdf
Online Resource S6 Root systems morphological and architectural comparison of independent transgenic rice lines (MB3-) and the wild-type Nipponbare (PDF 353 kb)
425_2019_3205_MOESM7_ESM.pdf
Online Resource S7 Meloidogyne graminicola MSP18 protein without the signal peptide (Mg-MSP18-SP) was not able to suppress PCD induced by INF1 elicitin from Phytophthora infestans in tobacco (PDF 275 kb)
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Grossi-de-Sa, M., Petitot, AS., Xavier, D.A. et al. Rice susceptibility to root-knot nematodes is enhanced by the Meloidogyne incognita MSP18 effector gene. Planta 250, 1215–1227 (2019). https://doi.org/10.1007/s00425-019-03205-3
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DOI: https://doi.org/10.1007/s00425-019-03205-3