Characterization of promoter elements of isoprene‐responsive genes and the ability of isoprene to bind START domain transcription factors

Abstract

Isoprene has recently been proposed to be a signaling molecule that can enhance tolerance of both biotic and abiotic stress. Not all plants make isoprene, but all plants tested to date respond to isoprene. We hypothesized that isoprene interacts with existing signaling pathways rather than requiring novel mechanisms for its effect on plants. We analyzed the cis‐regulatory elements (CREs) in promoters of isoprene‐responsive genes and the corresponding transcription factors binding these promoter elements to obtain clues about the transcription factors and other proteins involved in isoprene signaling. Promoter regions of isoprene‐responsive genes were characterized using the Arabidopsis cis‐regulatory element database. CREs bind ARR1, Dof, DPBF, bHLH112, GATA factors, GT‐1, MYB, and WRKY transcription factors, and light‐responsive elements were overrepresented in promoters of isoprene‐responsive genes; CBF‐, HSF‐, WUS‐binding motifs were underrepresented. Transcription factors corresponding to CREs overrepresented in promoters of isoprene‐responsive genes were mainly those important for stress responses: drought‐, salt/osmotic‐, oxidative‐, herbivory/wounding and pathogen‐stress. More than half of the isoprene‐responsive genes contained at least one binding site for TFs of the class IV (homeodomain leucine zipper) HD‐ZIP family, such as GL2, ATML1, PDF2, HDG11, ATHB17. While the HD‐zipper‐loop‐zipper (ZLZ) domain binds to the L1 box of the promoter region, a special domain called the steroidogenic acute regulatory protein‐related lipid transfer, or START domain, can bind ligands such as fatty acids (e.g., linolenic and linoleic acid). We tested whether isoprene might bind in such a START domain. Molecular simulations and modeling to test interactions between isoprene and a class IV HD‐ZIP family START‐domain‐containing protein were carried out. Without membrane penetration by the HDG11 START domain, isoprene within the lipid bilayer was inaccessible to this domain, preventing protein interactions with membrane bound isoprene. The cross‐talk between isoprene‐mediated signaling and other growth regulator and stress signaling pathways, in terms of common CREs and transcription factors could enhance the stability of the isoprene emission trait when it evolves in a plant but so far it has not been possible to say what how isoprene is sensed to initiate signaling responses.

Nanoscale simulation of the thylakoid membrane response to extreme temperatures

“…Instead, perhaps isoprene is a signaling molecule that activates metabolic pathways (Weraduwage et al, 2023; Zuo et al, 2019) that alter the membrane composition, thereby maintaining membrane homeostasis to support the embedded photosynthetic proteins (Martinière et al, 2011; Zheng et al, 2021). An important consideration is whether or not isoprene requires an active transport mechanism, as has been discussed for other volatile organic compounds (Adebesin et al, 2017; Widhalm et al, 2015).…”

Nanoscale Simulation of the Thylakoid Membrane Response to Extreme Temperatures

“…Instead, perhaps isoprene is a signaling molecule that activates metabolic pathways 69,70 that alter the membrane composition, thereby maintaining membrane homeostasis. 71,72 An important consideration is whether or not isoprene requires an active transport mechanism, as has been discussed for other volatile organic compounds.…”

The effect of constitutive root isoprene emission on root phenotype and physiology under control and salt stress conditions

“…It is thought that isoprene effects on the transcriptome, proteome, and metabolome accounts for improved stress tolerance (Dani & Loreto, 2022; Lantz et al, 2019; Monson et al, 2021). Indeed, isoprene has a hormone‐like activity (Pollastri et al, 2021), acting as a signal molecule for regulating gene expression and biosynthesis and signaling cascades of several plant hormones, including cytokinins (CKs), jasmonic acid (JA), and salicylic acid (SA) (Dani et al, 2022; Dani & Loreto, 2022; Weraduwage et al, 2023; Zuo et al, 2019). The control of isoprene over specific metabolite production and defense mechanisms indicates the roles of isoprene in growth‐defense tradeoffs (Frank et al, 2021; Monson et al, 2020; Xu et al, 2020; Zuo et al, 2019).…”