Evolution of Abscisic Acid Signaling for Stress Responses to Toxic Metals and Metalloids

Abstract

Toxic heavy metals and metalloids in agricultural ecosystems are crucial factors that limit global crop productivity and food safety. Industrial toxic heavy metals and metalloids such as cadmium, lead, and arsenic have contaminated large areas of arable land in the world and their accumulation in the edible parts of crops is causing serious health risks to humans and animals. Plants have co-evolved with various concentrations of these toxic metals and metalloids in soil and water. Some green plant species have significant innovations in key genes for the adaptation of abiotic stress tolerance pathways that are able to tolerate heavy metals and metalloids. Increasing evidence has demonstrated that phytohormone abscisic acid (ABA) plays a vital role in the alleviation of heavy metal and metalloid stresses in plants. Here, we trace the evolutionary origins of the key gene families connecting ABA signaling with tolerance to heavy metals and metalloids in green plants. We also summarize the molecular and physiological aspects of ABA in the uptake, rootto-shoot translocation, chelation, sequestration, reutilization, and accumulation of key heavy metals and metalloids in plants. The molecular evolution and interaction between the ABA signaling pathway and mechanisms for heavy metal and metalloid tolerance are highlighted in this review. Therefore, we propose that it is promising to manipulate ABA signaling in plant tissues to reduce the uptake and accumulation of toxic heavy metals and metalloids in crops through the application of ABA-producing bacteria or ABA analogues. This may lead to improvements in tolerance of major crops to heavy metals and metalloids.

Molecular Interaction and Evolution of Jasmonate Signaling With Transport and Detoxification of Heavy Metals and Metalloids in Plants

“…The ameliorating effects of jasmonates partially rely on the induced capacity of chelating and reactive oxygen species (ROS) scavenging. The thiol-contained peptides such as glutathione (GSH), PCs, and metallothioneins (MTs) play crucial roles in protecting plants from heavy metals and metalloids stress (Leszczyszyn et al, 2013;Hu et al, 2020;Deng et al, 2021). Both JA and heavy metals induced the transcription of genes for GSH synthesis including γ-glutamylcysteine synthetase (γ-ECS), glutathione synthetase (GSH), and glutathione reductase (GR; Xiang and Oliver, 1998).…”

“…Membrane-localized mineral transporters in the cellular and long-distance allocation of minerals play a significant role in the detoxification and accumulation of toxic heavy metals and metalloids in plants (Tomar et al, 2015;Clemens and Ma, 2016;Lindsay and Maathuis, 2017;Yamaji and Ma, 2017;Deng et al, 2019Deng et al, , 2021Hu et al, 2020;Sharma et al, 2020;Zhao and Wang, 2020;Liu et al, 2021;Tang and Zhao, 2021). For example, Arabidopsis (Arabidopsis thaliana) Iron Regulated Transporter 1 (AtIRT1), a members of the ZIP (zinc-regulated transporter) family, is the primary transporter for Cd uptake (Lux et al, 2011), while the translocation of Cd from roots (R) to shoots (SH) is mediated by two root pericycle-localized Heavy Metal ATPases (HMAs), AtHMA2, and AtHMA4 (Hussain et al, 2004;Mills et al, 2005).…”

“…The long-distance translocation and cellular mobility of toxic minerals can be regulated by signaling molecules through membrane transport systems. For example, ABA can inhibit Cd and Arsenate [As(V)] uptake through ABI5-MYB49-IRT1/HIPPs and WRKY6-PHT1;1 network, respectively (Hu et al, 2020). Additionally, ABA promotes the chelation and compartmentation of heavy metals through ABA-responsive transcriptional factors (Hu et al, 2020).…”

“…For example, ABA can inhibit Cd and Arsenate [As(V)] uptake through ABI5-MYB49-IRT1/HIPPs and WRKY6-PHT1;1 network, respectively (Hu et al, 2020). Additionally, ABA promotes the chelation and compartmentation of heavy metals through ABA-responsive transcriptional factors (Hu et al, 2020). Moreover, increasing pieces of evidence demonstrated the involvement of jasmonates consisting of JA and its derivatives such as jasmonoyl-l-isoleucine (JA-Ile) and methyl-JA in the detoxification and transport of toxic mineral stress (Maksymiec et al, 2005;Chen et al, 2014;Zhao et al, 2016;Wang et al, 2018;Bali et al, 2019;Lei et al, 2020b).…”

“…These regulatory mechanisms in algae and earlydivergent plants such as ferns may contribute to the removal of heavy metals from water and soil (Ma et al, 2001;Cheng et al, 2019;Manara et al, 2020). Physiological roles of the mineral transporters (Adem et al, 2020;Hu et al, 2020;Deng et al, 2021) and jasmonates signaling (Howe and Yoshida, 2019;Monte et al, 2019) may vary among plant species, but heavy metals and metalloids elevate endogenous JA levels in many plants. The growing number of plant genomes (Kersey, 2019) and transcriptomes (One Thousand Plant Transcriptomes Initiative, 2019) has enabled the comparative evolutionary analysis of key gene families relevant to the resistance of element contaminates in green plants, which will be helpful in searching for potential mitigation practices.…”