Isoprene: New insights into the control of emission and mediation of stress tolerance by gene expression

Abstract

Isoprene is a volatile compound produced in large amounts by some, but not all, plants by the enzyme isoprene synthase. Plants emit vast quantities of isoprene, with a net global output of 600 Tg per year, and typical emission rates from individual plants around 2% of net carbon assimilation. There is significant debate about whether global climate change resulting from increasing CO₂ in the atmosphere will increase or decrease global isoprene emission in the future. We show evidence supporting predictions of increased isoprene emission in the future, but the effects could vary depending on the environment under consideration. For many years, isoprene was believed to have immediate, physical effects on plants such as changing membrane properties or quenching reactive oxygen species. Although observations sometimes supported these hypotheses, the effects were not always observed, and the reasons for the variability were not apparent. Although there may be some physical effects, recent studies show that isoprene has significant effects on gene expression, the proteome, and the metabolome of both emitting and nonemitting species. Consistent results are seen across species and specific treatment protocols. This review summarizes recent findings on the role and control of isoprene emission from plants.

Keywords: CO2; climate change; growth; high temperature; signalling; stress tolerance; triose phosphate utilization limitation.

Figure 1:. The MEP pathway in plants.

Enzymes: PEPC = phosphoenolpyruvate carboxylase, DXS = 1-deoxy-d-xylulose-5-phosphate synthase, DXR = 1-deoxy-d-xylulose-5-phosphate reductoisomerase, CMS/MCT = 4-diphosphocytidyl-2-C-methylerythritol synthase/2-C-methyl-d-erythritol-4-phosphate cytidylyltransferase, CMK = 4-(cytidine 5’-diphospho)-2-C-methyl-d-erythritol kinase, MCS = 2-C-methyl-d-erythritol-2,4-cyclodiphosphate synthase, HDS = 4-hydroxy 3-methylbut-2-enyl-diphosphate synthase, HDR = 4-hydroxy-3-methylbut-2-enyl-diphosphate reductase, IDI = isopentenyl diphosphate isomerase. In isoprene emitting plants the conversion of DMADP to isoprene is catalyzed by isoprene synthase (ISPS).

Figure 2:. The post-burning burst from Glycine soja.

At time 0 one leaflet of a trifoliolate leaf was burned for 5 seconds with a butane lighter. Assimilation and isoprene emission were tracked in an adjacent leaflet. The effect when leaves were exposed to 150 ppm ambient CO₂ (A) and 1200 ppm ambient CO₂ (B) is shown. (Unpublished data by A.T.L. and T.D.S.)

Figure 3.. Leaf growth in Arabidopsis and tobacco expressing ISPS.

A comparison of Arabidopsis rosette size reflecting projected leaf area (A-C) and leaves after being separated from the rosettes reflecting apparent total leaf area (D-F) in 35-day old Arabidopsis non-emitting empty vector control (EV-B3) and isoprene emitting lines (expressing ISPS) (B2 and C4) is presented. For (A)-(F) all plants were grown in growth chambers under a light intensity of 200 μmol m⁻² s⁻¹. Photographs depicting the front and top views of tobacco plants taken during the 27^th day (G, H), 41^st day (I, J), and 54^th day (K) of plant growth are shown. NE: Non-emitting tobacco; IE: Isoprene-emitting tobacco. (Modified and reproduced from Zuo et al., 2019)

Figure 4.. Proposed model for how isoprene signaling can affect GA-mediated growth regulation and JA-mediated defense responses.

Transcriptomic data revealed that isoprene can alter genes required for both GA accumulation and JA synthesis (genes shown in green font) which can promote both GA-mediated growth and JA-mediated defense simultaneously. We speculate that the observed growth enhancement in Arabidopsis engineered to emit isoprene is likely a result of upregulation of PIF. However, interactions between GA and JA pathways occur through DELLA and JAZ proteins (Campos et al. 2016). JA synthesis leads to the degradation of JAZ proteins that release the inhibition of transcription factors to enhancing defense related processes (Campos et al. 2016). Antagonistic interactions between JAZ and DELLA proteins play a part in regulating the growth-defense trade-off mediated by GA and JA (Campos et al. 2016). Therefore, one possible explanation for the observed variations in isoprene mediated growth effects in different species is the likely effect of isoprene on growth-defense trade-off. Genes belonging to other signalling pathways whose expression was altered by isoprene were omitted from this diagram for the sake of simplicity. Dotted lines and genes written in green font denote isoprene responsive gene expression revealed during the present study. Asterisks (*) denote differentially expressed genes in both Arabidopsis expressing ISPS and Arabidopsis fumigated by isoprene, but, not differentially expressed in tobacco. Upregulation and down regulation of gene expression is denoted by pointed and blunt ended arrows, respectively (DFL2 and TEM1 expression was downregulated in the presence of isoprene in Arabidopsis). Solid lines denote signalling pathways that are well established. Abbreviations: BBD - Bifunctional nuclease in basal defense response; CBF - CRT/DRE binding factor; COP1 - Constitutively photomorphogenic 1, a ubiquitin ligase; CRPK1- Cold-responsive protein kinase 1; DELLA - PIF transcription factor repressors; DFL2 - Dwarf in light 2, a GH3-related (auxin response related) protein; FT - Flowering locus T; GA - gibberellic acid; HY5 - Elongated hypocotyl 5; JA - jasmonic acid; JAZ - Jasmonate ZIM-domain repressors; JMT - Jasmonic acid carboxyl methyltransferase; LOX - Lipoxygenase; MARD1 - Mediator of ABA (abscisic acid)-regulated dormancy 1, a novel zinc-finger protein; MYC2 - a basic helix-loop-helix transcription factor and a master regulator of JA signaling; MYB59 - MYB domain protein 59; OPR3 - Oxophytodienoate-reductase 3; PHYB - Phytochrome-B; PIF - Phytochrome-interacting factors, TEM1 - Tempranillo 1, a RAV transcription factor; TZF5 -Tandem CCCH zinc finger protein 5; 14-3-3 - highly conserved acidic proteins of the 14-3-3-protein family. (Reproduced from Zuo et al., 2019)