Role of ROS and auxin in plant response to metal-mediated stress

Abstract

Being unable to move away from their places of germination, in order to avoid excess metal-induced damages, plants have to evolve different strategies and complex regulatory mechanisms to survive harsh conditions. While both ROS and auxin are documented to be important in plant response to metal stress, the mechanisms underlying the crosstalk between ROS and auxin in metal stress are poorly understood. In this review, we provide an update on the regulation of plant responses to metal-stress by ROS and auxin signaling pathways, primarily, with a focus on the copper, aluminum and cadmium stress. We aim at surveying the mechanisms underlying how metal stress modulates the changes in auxin distribution and the network of ROS and auxin in plant response to metal stress based on recent studies.

Soils contain many kinds of heavy and trace metal elements, which interfere with numerous metabolic and physiological processes when at high concentrations, leading to reduced growth and serious negative environmental consequences.^1-3 Being unable to move away from their places of germination, in order to avoid excess metal-induced damages, plants have to evolve different strategies and complex regulatory mechanisms to survive harsh conditions, such as regulation of metal irons uptake, chelation and efflux, perception transduction and transmission of stress stimuli.^4-9 Recent research has revealed that metal-mediated stress seems to have a direct impact on accumulation of relative oxygen species (ROS), content of nitric oxide (NO) and hormone levels in organs and the plants can quickly adjust their growth to harsh environment by influencing the cellular redox state and hormone signaling.^10-16 This review provides an update on the regulation of plant responses to metal-stress by ROS and auxin signaling pathway, primarily, with a focus on the copper, aluminum and cadmium stress. The mechanisms underlying how metal stress modulates the changes in auxin distribution and the network of ROS and auxin in plant response to metal stress are discussed based on recent studies.

ROS Signaling in Metal Stress Response

ROS produced during normal cell metabolism has been shown to function as a key regulator in various physiological processes, such as seed germination, plant maturation and senescence and stomatal closure. Excess ROS accumulation leading to oxidative stress is also assayed in plants exposed to the adverse environmental conditions.^7,17-19 For metal stress, many metals such as Cd, Cu, Fe, Zn, Hg, Mn and Al can induce the ROS production^11,13,20-22 and ROS scavenging systems, including catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxide (APX) and glutathione reductase (GR) often work in the protection against excess ROS toxicity in plants.^{11,13,17,18,23} Hg has negative effect on algae growth and stimulates ROS production. To avoid the Hg-induced oxidative stress, antioxidative enzymes such as SOD, CAT and APX are upregulated to diminish the excess ROS.¹¹ A similar effect is also reported by Cd, in which the enzyme activities of CAT, APX and GR are increased both in the roots and leaves of Cd-exposed plants.¹³ However, APX activity was decreased in the roots of the plants under Cu stress.¹³ In addition, the antioxidative enzyme activities are differentially regulated in roots and leaves after Cu-exposure, for example, CAT activity is decreased in the roots, but increased in the leaves of Cu-treated plants.¹³

In addition to causing oxidative stress, ROS can also serve as a signal molecule for plants to survive in harsh conditions such as metal stress. It has been documented that mitogen-activated protein kinases (MAPKs) can perceive the changes of ROS content in signal transmission for a range of stresses²³ and the distinct MAPK pathways involve specifically to excess particular metal ions.^24-26 ROS induced by Cu triggers SIMK and SAMK activation via SIMKK, whereas Cd activates MMK2, MMK3 besides SIMK and SAMK.²⁴ Recently, MPK3 and MPK6 are also evidenced to be activated by Cd-induced ROS accumulation in Arabidopsis plants.²⁵ A similar effect is also shown in plant response to Al stress, in which a MAPK-like protein is modulated by toxic concentrations of aluminum.²⁶

Auxin Signaling in Metal Stress Response

Plants exposed to abiotic stress conditions can lead to a wide range of stress-induced phenotypes, such as inhibition of primary root elongation, increased formation of lateral roots and increased number of root hairs.¹⁸ Auxin, a key regulator controlling these phenotypes, directly affects plant responses to metal stresses by changes of auxin homeostasis including auxin redistribution, auxin transport and auxin stability.¹⁸ For example, Al alters both auxin accumulation and distribution in plants under Al stress.^12,27-29 These changes are mediated by Al-inhibited auxin transport form distal transition zone to elongation zone of the maize primary root, resulting in an arrest of root elongation.²⁷ Further studies demonstrate that the alteration of auxin transport for Al-induced auxin redistribution is modulated by auxin carriers AUX1 and PIN2.^12,29 In addition, the ethylene production leading to auxin redistribution is also evidenced in Al-mediated inhibition of root elongation.¹² In contrast to Al, Cd-impeded growth is associated with the decreased auxin concentration by elevating IAA oxidase activity for an increase in auxin degradation.³⁰ This Cd-induced growth inhibition can be alleviated by salt application through decreasing Cd-induced elevation of IAA oxidase activity.³¹ Auxin redistribution was also observed in Cd-treated roots,¹⁸ however, the mechanisms underlying how excess Cd modulates the auxin redistribution remain elusive. For the plant response to excess Cu, both auxin and NO regulate each other’s level during organ development under Cu excess.⁸ The observed Cu-mediated auxin redistribution responsible for the inhibition of primary root elongation is mediated by PIN1, but not PIN2 or AUX1, different from Al-modulated auxin transport.^10,12,29

Interactions Between ROS and Auxin Signaling in Plant Response to Metal Stress

Both ROS and auxin are the main players to avoid deleterious effects of stress on plant growth under metal stress and the crosstalk of these two molecules in plant response to metal stress has been explored. When the Arabidopsis seedlings were exposed to oxidative stress-inducing agents, the alterations in auxin homeostasis with physiological responses were observed, suggesting their possible crosstalk.³² This note is further re-enforced by the data that the increased ROS can regulate auxin transport by altering the expression of PIN genes, relocation of auxin exporters³³ and auxin conjugation.³⁴ In addition, H₂O₂ can activate a specific Arabidopsis MAPKKK, ANP1, which can suppress auxin signaling.³⁵ However, Tsukagoshi et al. report that ROS controls the transition from cell proliferation to differentiation in roots via a separate pathway different from auxin signaling.³⁶ Our recent studies also indicate that increased H₂O₂ in Cu-treated seedlings does not contribute to Cu-regulated auxin redistribution for the inhibition of primary root elongation.¹⁰ Thus, whether both ROS and auxin can crosstalk in plant response to different metal stresses needs to be further experimentally analyzed.

Glossary

Abbreviations:

APX

ascorbate peroxide

CAT

catalase

GR

glutathione reductase

MAPK

mitogen-activated protein kinase

NO

nitric oxide

POD

peroxidase

ROS

relative oxygen species

SOD

superoxide dismutase

Yuan HM, Xu HH, Liu WC, Lu YT. Copper regulates primary root elongation through PIN1-mediated auxin redistribution. Plant Cell Physiol. 2013 doi: 10.1093/pcp/pct030.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.