Elevated CO₂ Reduces the Resistance and Tolerance of Tomato Plants to <em>Helicoverpa armigera</em> by Suppressing the JA Signaling Pathway

<div><p>Both resistance and tolerance, which are two strategies that plants use to limit biotic stress, are affected by the abiotic environment including atmospheric CO₂ levels. We tested the hypothesis that elevated CO₂ would reduce resistance (i.e., the ability to prevent damage) but enhance tolerance (i.e., the ability to regrow and compensate for damage after the damage has occurred) of tomato plants to the cotton bollworm, <em>Helicoverpa armigera</em>. The results showed that elevated CO₂ reduced resistance by decreasing the jasmonic acid (JA) level and activities of lipoxygenase, proteinase inhibitors, and polyphenol oxidase in wild-type (WT) plants infested with <em>H. armigera</em>. Consequently, the activities of total protease, trypsin-like enzymes, and weak and active alkaline trypsin-like enzymes increased in the midgut of <em>H. armigera</em> when fed on WT plants grown under elevated CO₂. Unexpectedly, the tolerance of the WT to <em>H. armigera</em> (in terms of photosynthetic rate, activity of sucrose phosphate synthases, flower number, and plant biomass and height) was also reduced by elevated CO₂. Under ambient CO₂, the expression of resistance and tolerance to <em>H. armigera</em> was much greater in wild type than in <em>spr2</em> (a JA-deficient genotype) plants, but elevated CO₂ reduced these differences of the resistance and tolerance between WT and <em>spr2</em> plants. The results suggest that the JA signaling pathway contributes to both plant resistance and tolerance to herbivorous insects and that by suppressing the JA signaling pathway, elevated CO₂ will simultaneously reduce the resistance and tolerance of tomato plants.</p> </div

Activities of digestive proteases in the guts of <i>H. armigera</i> that fed for 2 days on tomato genotypes grown under ambient and elevated CO₂.

<p>(A) total protease, (B) chymotrypsin (CTE) activity, (C) weak alkaline trypsin-like enzyme (WATE) activity, and (D) active alkaline trypsin-like enzyme (AATE) activity. Each value represents the average (±SE) of four replicates. Different lowercase letters indicate significant differences between ambient CO₂ and elevated CO₂ treatment. Different uppercase letters indicate significant differences between feeding on the WT plants and <i>spr2</i> plants within the same CO₂.</p

Activity of sugar transport enzymes in leaves of two tomato genotypes grown under ambient and elevated CO₂ without <i>H. armigera</i>.

<p>(A) sucrose phosphate synthase (SPS) activity, and (B) sucrose synthase (SS) activity. Each value represents the average (±SE) of four replicates. Different lowercase letters indicate significant differences between CO₂ level within the same tomato genotype (LSD test: d.f. = 3.12; <i>P</i><0.05). Different uppercase letters indicate significant differences between WT plants and <i>spr2</i> plants within the same CO₂ level (LSD test: d.f. = 2.9; <i>P</i><0.05).</p

Mean relative growth rate (MRGR) of <i>H. armigera</i> that fed for 2 days on tomato genotypes grown under ambient and elevated CO₂.

<p>Each value represents the average (±SE) of 85 replicates. Different lowercase letters indicate significant differences between ambient CO₂ and elevated CO₂ treatment. Different uppercase letters indicate significant differences between feeding on WT plants and <i>spr2</i> plants within the same CO₂ treatment.</p

Experimental design and replications.

<p>A flow diagram of the design used for the plant treatments, tissue collection and replications. There were two CO₂ levels, two plant genotypes, two insect treatments and four OTC replications for plant treatments.</p

The major results and conclusion of this study were summarized.

<p>Elevated CO₂ decreased resistance and tolerance of WT to <i>H. armigera</i>. In contrast, the resistance and tolerance of <i>spr2</i> were not changed by elevated CO₂. Elevated CO₂ reduces the resistance and tolerance of WT plants by suppressing the JA signaling pathway.</p

Tolerance (as indicated by differences in values of growth traits or enzyme activities between damaged plants and undamaged plants) of two tomato genotypes grown under ambient and elevated CO₂.

<p>Damaged plants are those that were fed on by <i>H. armigera</i>. (A) photosynthetic rate (<i>A</i>), (B) sucrose phosphate synthase (SPS), (C) sucrose synthase (SS), (D) biomass, (E) root biomass: shoot biomass (R∶S), (F) cumulative flower number, (G) plant height, and (H) total branch length. Each value represents the average (±SE) of 20 replicates. Symbols above columns indicate levels of significant differences between variables of damaged and undamaged plants (*, P<0.05). Positive differences indicate that values were greater for damaged plants than for undamaged plants.</p

Chemical defensive components in two tomato genotypes grown under ambient (AM) and elevated CO₂ (EL) without and with <i>H. Armigera</i> (+HA).

<p>(A) JA content, and the activity of (B) lipoxygenase (LOX), (C) proteinase inhibitors (PIs), (D) polyphenol oxidase (PPO), (E) peroxidase (POD), and (F) phenylalanine ammonia lyase (PAL). Each value represents the average (±SE) of four replicates. Different lowercase letters indicate significant differences among combinations of <i>H. armigera</i> and CO₂ level within the same tomato genotype (LSD test: d.f. = 3.12; <i>P</i><0.05). Different uppercase letters indicate significant differences between WT plants and <i>spr2</i> plants within the same CO₂ (LSD test: d.f. = 2.9; <i>P</i><0.05).</p