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. 2025 Apr 14;6(4):101237.
doi: 10.1016/j.xplc.2024.101237. Epub 2024 Dec 30.

Herbivory-triggered JA signaling suppresses photosynthesis by inducing photoinhibition in tomato

Chaoyi Hu  1 , Hannah Rae Thomas  2 , Chunyu Wei  2 , Shaofang Wu  2 , Changan Zhu  2 , Yanhong Zhou  1 , Christine H Foyer  3 , Jingquan Yu  4
Affiliations

Herbivory-triggered JA signaling suppresses photosynthesis by inducing photoinhibition in tomato

Chaoyi Hu et al. Plant Commun. .
No abstract available

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Figures

Figure 1
Figure 1
Jasmonates suppress cyclic electron flow, contributing to the photoinhibition-associated reduction of photosynthesis in tomato response to herbivory. (A and B) Effects of herbivory by H. armigera(A), wounding, or simulated herbivory (B) on the maximal photochemical efficiency of PSII (Fv/Fm) and maximum P700 photooxidation level (ΔP700max) in WT plants. Data represent the mean ± SD (n = 3). Statistically significant differences between treatment and mock were determined using Student’s t-test and are indicated with asterisks (∗∗P < 0.01). W, wounding; OS, oral secretion. (C and D) Effects of herbivory by H. armigera(C), wounding, or simulated herbivory (D) on the cyclic electron flow (CEF) of PSI in WT plants. Representative images of post-illumination transient induction curves are shown (n = 3), with values representing the slopes of red lines. (E and F) Effects of herbivory by H. armigera(E), wounding, or simulated herbivory (F) on JA-Ile content in WT plants. Data represent the mean ± SD (n = 3). Statistically significant differences between treatment and mock were determined using Student’s t-test and are indicated with asterisks (∗P < 0.05 and ∗∗P < 0.01). (G) Representative wound-induced surface potential changes in WT and glr3.3/3.5 mutants (n = 5). (H) JA-Ile content in WT and glr3.3/3.5 plants 1 hour after W+OS treatment. Data represent the mean ± SD (n = 3). Statistically significant differences between treatments are represented by compact letter display (P < 0.05; two-way ANOVA followed by post hoc Tukey’s test). (I–L) Effects of simulated herbivory on Fv/Fm (I), ΔP700max(J), CEF on PSI (K), and the expression of PGR5(L) in glr3.3/3.5, jai1, or myc2 mutants 1 hour after treatment. Data represent the mean ± SD (n = 3) in (I), (J), and (L). Representative images of post-illumination transient induction curves are shown (n = 3), with the slopes of red lines indicated by values (K). ACTIN2 and UBI3 served as internal reference genes, and the relative expression of PGR5 was normalized to that in WT under mock treatment (L). Statistically significant differences in treatments are represented by compact letter display (P < 0.05; two-way ANOVA followed by post hoc Tukey’s test). (M) Schematic of the PGR5 promoter showing the MYC2 binding motif CACATG, probe, primers, and fragment used for electrophoretic mobility shift assays (EMSAs), chromatin immunoprecipitation (ChIP)‒qPCR, and yeast one-hybrid (Y1H) assays, respectively. (N) Y1H analysis of MYC2 binding to the promoter of PGR5. The interaction was determined on synthetic dextrose (SD) medium lacking Leu in the presence of 150 ng ml−1 AbA (−Leu+AbA150). (O) Regulation of the PGR5 promoter by MYC2 assessed by dual-luciferase assays in N. benthamiana. The ratio of firefly luciferase to Renilla luciferase (LUC/REN) of the empty vector (EV) plus promoter was set as 1. Data represent the mean ± SD (n = 4). Statistically significant differences from EV were determined using Student’s t-test and are indicated by asterisks (∗∗P < 0.01). (P) ChIP–qPCR results showing the enrichment of MYC2-HA at the PGR5 promoter (n = 3). Tomato ACTIN2 was used as a nonspecific target. Statistically significant differences between PGR5 and ACTIN2 were determined using Student’s t-test and are indicated with asterisks (∗P < 0.05). (Q) EMSA showing the direct binding of MBP-MYC2 to the PGR5 promoter. Competitors and mutant competitors were used at 100-fold molar concentration. Mut, mutated probe. (R) CEF of PSI in WT and pgr5 after simulated herbivory and exposure to 1000 μmol m−2 s−1 Photosynthetic Photon Flux Density (PPFD) light for 30 min. Representative images of post-illumination transient induction curves are shown (n = 3), and the values represent the slopes of red lines. (S) Fv/Fm and ΔP700max of WT and pgr5 after simulated herbivory followed by exposure to 1000 μmol m−2 s−1 PPFD light for 30 min. Data represent the mean ± SD (n = 3). Statistically significant differences between treatments are represented by a compact letter display (P < 0.05; two-way ANOVA followed by post hoc Tukey’s test). (T) Proposed model for herbivory-induced reduction in CO2 assimilation. Herbivory induces GLR3.3/3.5-dependent accumulation of JA and activation of MYC2. MYC2 functions as a transcriptional suppressor for PGR5, which plays a crucial role in regulating CEF and alleviating NPQ-related photoinhibition. ES, electrical signaling.
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