Diproline-induced resistance to parasitic nematodes in the same and subsequent rice generations: Roles of iron, nitric oxide and ethylene

Jonas De Kesel; Eli Bonneure; Michael Frei; Tim De Meyer; Sven Mangelinckx; Tina Kyndt

doi:10.3389/fpls.2023.1112007

Diproline-induced resistance to parasitic nematodes in the same and subsequent rice generations: Roles of iron, nitric oxide and ethylene

Front Plant Sci. 2023 Feb 7:14:1112007. doi: 10.3389/fpls.2023.1112007. eCollection 2023.

Authors

Jonas De Kesel¹, Eli Bonneure², Michael Frei³, Tim De Meyer⁴, Sven Mangelinckx², Tina Kyndt¹

Affiliations

¹ Department of Biotechnology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
² Department of Green Chemistry and Technology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
³ Department of Agronomy and Crop Physiology, Institute for Agronomy and Plant Breeding, Justus Liebig University Giessen, Giessen, Germany.
⁴ Department of Data Analysis and Mathematical Modelling, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.

Abstract

Induced resistance (IR) is a plant phenotype characterized by lower susceptibility to biotic challenges upon elicitation by so-called IR stimuli. Earlier, we identified diproline (cyclo(l-Pro-l-Pro)) as IR stimulus that protects rice (Oryza sativa) against the root-knot nematode Meloidogyne graminicola (Mg). In the current study, detailed transcriptome analyses at different time points, and under uninfected and nematode-infected conditions revealed that this rice IR phenotype is correlated with induction of genes related to iron (Fe), ethylene (ET) and reactive oxygen species (ROS)/reactive nitrogen species (RNS) metabolism. An infection experiment under Fe limiting conditions confirmed that diproline-IR is only effective under optimal Fe supply. Although total root Fe levels were not affected in diproline-treated plants, phytosiderophore secretion was found to be induced by this treatment. Experiments on mutant and transgenic rice lines impaired in ET or ROS/RNS metabolism confirmed that these metabolites are involved in diproline-IR. Finally, we provide evidence for transgenerational inheritance of diproline-IR (diproline-TIR), as two successive generations of diproline-treated ancestors exhibited an IR phenotype while themselves never being exposed to diproline. Transcriptome analyses on the offspring plants revealed extensive overlap between the pathways underpinning diproline-IR and diproline-TIR. Although diproline induces significant systemic changes in global DNA methylation levels early after treatment, such changes in DNA methylation were not detected in the descendants of these plants. To our knowledge, this is the first report of TIR in rice and the first transcriptional assessment of TIR in monocots.

Keywords: Fe homeostasis; defense priming; diproline (cyclo(L-Pro-L-Pro)); induced resistance (IR); rice (Oryza sativa); rice root-knot nematode (Meloidogyne graminicola); transgenerational IR.

Grants and funding

Part of this research was funded by Ghent University via a Bijzonder Onderzoeksfonds (BOF) starting grant to TK, a BOF-BAS grant (01B02720) and a BOF-GOA grant (BOF-GOA No. 01G01715). The DNA methylation assays were financed by Fonds Wetenschappelijk Onderzoek Vlaanderen (FWO grant G007417N). We thank Maarten Claes for his contribution to the practical execution of some analytical experiments. We also thank Lien De Smet for technical support. The authors declare no conflict of interest.