Isoprene Acts as a Signaling Molecule in Gene Networks Important for Stress Responses and Plant Growth

Abstract

Isoprene synthase converts dimethylallyl diphosphate to isoprene and appears to be necessary and sufficient to allow plants to emit isoprene at significant rates. Isoprene can protect plants from abiotic stress but is not produced naturally by all plants; for example, Arabidopsis (Arabidopsis thaliana) and tobacco (Nicotiana tabacum) do not produce isoprene. It is typically present at very low concentrations, suggesting a role as a signaling molecule; however, its exact physiological role and mechanism of action are not fully understood. We transformed Arabidopsis with a Eucalyptus globulus isoprene synthase. The regulatory mechanisms of photosynthesis and isoprene emission were similar to those of native emitters, indicating that regulation of isoprene emission is not specific to isoprene-emitting species. Leaf chlorophyll and carotenoid contents were enhanced by isoprene, which also had a marked positive effect on hypocotyl, cotyledon, leaf, and inflorescence growth in Arabidopsis. By contrast, leaf and stem growth was reduced in tobacco engineered to emit isoprene. Expression of genes belonging to signaling networks or associated with specific growth regulators (e.g. gibberellic acid that promotes growth and jasmonic acid that promotes defense) and genes that lead to stress tolerance was altered by isoprene emission. Isoprene likely executes its effects on growth and stress tolerance through direct regulation of gene expression. Enhancement of jasmonic acid-mediated defense signaling by isoprene may trigger a growth-defense tradeoff leading to variations in the growth response. Our data support a role for isoprene as a signaling molecule.

Shoot Characterization of Isoprene and Ocimene-Emitting Transgenic Arabidopsis Plants under Contrasting Environmental Conditions

“…Conversely, significant positive effects were recorded for dry weight under heat stress only. Indeed, our data are in line with most of the literature showing the efficacy of hemi-and monoterpenes at protecting the photosynthetic apparatus under high temperatures [25,30,34]. Somehow surprisingly, however, these results indicate relatively minor phenotypic variations consequent to VOCs' emission under the stress conditions tested.…”

“…However, independent studies demonstrated that the emission of isoprenoids led to an increased biomass, leaf area, and pigment content in several species (e.g., [25,34]), which is consistent with our data, suggesting the existence of a tight but complex relationship between isoprene/monoterpene emission and growth. In Zuo et al [34], Arabidopsis plants transformed with a Eucalyptus globulus IspS gene had a higher leaf area, leaf number, and final dry weight than the wild-type Col-0, consistent with our data on both isoprene and ocimene emitters. Similarly, in Loivamäki et al [25], Arabidopsis lines transformed with an IspS gene from gray poplar had higher growth rates under optimal growth conditions.…”

“…Under optimal conditions, isoprenoids' emission is a metabolically expensive trait, with high energy and photosynthetic carbon requirements [15]. However, independent studies demonstrated that the emission of isoprenoids led to an increased biomass, leaf area, and pigment content in several species (e.g., [25,34]), which is consistent with our data, suggesting the existence of a tight but complex relationship between isoprene/monoterpene emission and growth. In Zuo et al [34], Arabidopsis plants transformed with a Eucalyptus globulus IspS gene had a higher leaf area, leaf number, and final dry weight than the wild-type Col-0, consistent with our data on both isoprene and ocimene emitters.…”

“…An interesting output of our work is the enhanced photosynthetic capacity and CO 2 assimilation per unit of leaf area (A) in emitters compared with Col-0 under optimal conditions. It was previously reported that isoprene and monoterpene emission might increase the chlorophyll content in leaves, and potentially enhance A [25,34]. This increase in A can also partially explain the higher PLA and biomass of the emitters compared with Col-0, suggesting a higher carbon availability that can sustain growth.…”

“…Similarly, in Loivamäki et al [25], Arabidopsis lines transformed with an IspS gene from gray poplar had higher growth rates under optimal growth conditions. The role of isoprene as a signaling molecule has recently been shown, with a significant upregulation in the expression of genes belonging to signaling networks or associated with specific growth regulators (e.g., gibberellic acid, cytokinins, and jasmonic acid) in Arabidopsis engineered to emit isoprene [34]. In particular, greater accumulation of gibberellic acid, potentially through an enhanced expression level of genes encoding for zinc fingers proteins (e.g., TZF5), has been suggested as a potential explanation of these phenotypes with an enhanced leaf area.…”