Interplay between Carotenoids, Abscisic Acid and Jasmonate Guides the Compatible Rice-Meloidogyne graminicola Interaction

Abstract

In this study, we have characterized the role of carotenoids and chlorophyll in the compatible interaction between the sedentary root knot nematode (RKN) Meloidogyne graminicola and the monocot model plant rice (Oryza sativa). Previous transcriptome data showed a differential expression of carotenoid and chlorophyll biosynthesis genes in nematode-induced giant cells and gall tissue. Metabolite measurement showed that galls indeed accumulate chlorophyll a, b and carotenoids, as well as the hormone abscisic acid (ABA). When ABA was externally applied on rice plants, or when ABA-biosynthesis was inhibited, a significant increase in gall formation and nematode development was found, showing the complex role of ABA in this interaction. ABA application suppressed jasmonic acid (JA) levels in the plants, while ABA-biosynthesis inhibition lead to increased JA levels confirming an antagonism between ABA and JA in rice roots. In addition, combined applications of ABA and JA showed that the ABA-effect can overcome JA-induced defense. Based on these observations, we hypothesized that the accumulation of chlorophyll and carotenoid precursors would be beneficial to nematode infection. Indeed, when chemically blocking the carotenoid biosynthesis pathway at different steps, which leads to differential accumulation of carotenoids and chlorophyll in the plants, a positive and clear link between accumulation of carotenoids and chlorophyll and rice susceptibility to RKN was detected.

Strigolactones enhance root‐knot nematode (Meloidogyne graminicola) infection in rice by antagonizing the jasmonate pathway

“…Because ABA and SLs share the same biosynthetic precursor, β‐carotene, we also investigated whether ABA plays a role in SL‐induced M. graminicola susceptibility. It is known that ABA plays a complex role in the interaction between rice and M. graminicola (Kyndt et al ., ). In our study, neither the exogenous GR24 treatment nor the TIS108 treatment or the d ‐mutants changed the contents of ABA in rice roots.…”

“…simultaneously influence plant cell differentiation and modulate the defense responses to establish a successful infection via feeding cell formation (Gheysen & Mitchum, 2011;Ji et al, 2013). The plant hormones JA, ethylene, SA, ABA, brassinosteroids (BR), gibberellic acid (GA), and auxin are known to be involved in the interactions between plant and root-knot nematodes (Karczmarek et al, 2004;Nahar et al, 2011Nahar et al, , 2013Kyndt et al, 2017;Yimer et al, 2018;Gheysen & Mitchum, 2019). For instance, the JA-based defense pathway plays a vital role in rice defense against M. graminicola infection, whereas SA is also involved in defense but to a lesser extent than JA (Nahar et al, 2011).…”

“…In addition, the JA-precursor cis-(+)-12-oxo-phytodienoic acid (cis-OPDA) acts as a signaling molecule in regulating Arabidopsis defense against M. hapla (Gleason et al, 2016). On the other hand, ABA, BR, and GA promote rice susceptibility to M. graminicola infection by interacting antagonistically with the JA pathway Kyndt et al, 2017;Yimer et al, 2018).…”

The Meloidogyne graminicola effector Mg16820 is secreted in the apoplast and cytoplasm to suppress plant host defense responses

“…In rice, galls induced by M. graminicola showed a two‐fold increased ABA level at 3 dai, whereas, at 7 dai, the ABA level was still increased, but lower than at 3 dai. The application of ABA, as well as ABA biosynthesis, promotes the susceptibility of rice to M. graminicola , indicating a complex role for ABA in this plant–nematode relation (Kyndt et al, ). The ABA level in the host during the migratory stage of the nematode is not known.…”

Aboveground herbivory induced jasmonates disproportionately reduce plant reproductive potential by facilitating root nematode infestation

“…Jasmonates have been suggested to regulate plant‐mediated interactions between above and below ground herbivores (Erb, Lenk, Degenhardt, & Turlings, ; Erb, Ton, Degenhardt, & Turlings, ; Papadopoulou & van Dam, ; van Dam & Heil, ; van Dam & Oomen, ). Foliar jasmonate treatments reduce gall formation by root parasitic nematodes in tomato (Bhattarai et al, ; Cooper, Jia, & Goggin, ; Fan et al, ; Fujimoto et al, ; Zinovieva, Vasyukova, Udalova, & Gerasimova, ), rice (Kyndt et al, ; Nahar, Kyndt, de Vleesschauwer, Höfte, & Gheysen, ), soybean (Hu, You, Li, Hua, & Wang, ), oat (Soriano, Asenstorfer, Schmidt, & Riley, ), and thale cress (Gleason, Leelarasamee, Meldau, & Feussner, ; Ozalvo et al, ). Genetic approaches also show that jasmonate signalling can decrease plant susceptibility to root nematodes (Kammerhofer et al, ; Nahar et al, ; Ozalvo et al, ), albeit with some exceptions (Gao et al, ).…”