To Fight or to Grow: The Balancing Role of Ethylene in Plant Abiotic Stress Responses

Abstract

Plants often live in adverse environmental conditions and are exposed to various stresses, such as heat, cold, heavy metals, salt, radiation, poor lighting, nutrient deficiency, drought, or flooding. To adapt to unfavorable environments, plants have evolved specialized molecular mechanisms that serve to balance the trade-off between abiotic stress responses and growth. These mechanisms enable plants to continue to develop and reproduce even under adverse conditions. Ethylene, as a key growth regulator, is leveraged by plants to mitigate the negative effects of some of these stresses on plant development and growth. By cooperating with other hormones, such as jasmonic acid (JA), abscisic acid (ABA), brassinosteroids (BR), auxin, gibberellic acid (GA), salicylic acid (SA), and cytokinin (CK), ethylene triggers defense and survival mechanisms thereby coordinating plant growth and development in response to abiotic stresses. This review describes the crosstalk between ethylene and other plant hormones in tipping the balance between plant growth and abiotic stress responses.

Keywords: abiotic stress; ethylene; growth and defense tradeoff; hormone crosstalk.

Figure 1

Schematic overview of ethylene biosynthesis and signaling in Arabidopsis. (A) Ethylene biosynthetic pathway. Amino acid methionine is converted into hormone ethylene by three families of enzymes, SAM synthetases that produce S-adenosyl-methionine out of methionine, ACC synthases that make 1-aminocyclopropane-1-carboxylic acid, and ACC oxidases that generate ethylene. Ethylene then diffuses out of and into plant cells. (B) Ethylene signaling pathway in the absence of ethylene. Ethylene receptors ETR1, ETR2, ERS1, ERS2, and EIN4 localized in the ER membrane activate CTR1 kinase, which in turn phosphorylates the C-terminal end of EIN2 (EIN2-CEND) and turns EIN2 off. The mRNAs for F-box proteins EBF1 and EBF2 are translated and target the master transcriptional regulators of ethylene signaling, EIN3 and EIL1, to proteasomes for protein turnover, thus preventing ethylene responses. (C) Ethylene signaling pathway in the presence of ethylene. Ethylene binding to the receptors shuts them off, CTR1 is inactivated, EIN2 is dephosphorylated and is cleaved by an unknown protease, thus releasing EIN2-CEND that functions in the cytoplasm and in the nucleus. In the cytosol, EIN2-CEND recruits EBF1 and EBF2 mRNAs to the P-bodies and inhibits their translation. In the nucleus, EIN2-CEND directly or indirectly potentiates the activity of EIN3 and EIL1. Ethylene-triggered stabilization of the EIN3/EIL1 transcription factors leads to the transcriptional regulation of multiple target genes, including induction of several members of the ERF gene family that encode transcription factors of the second tier of the ethylene response that propagate the EIN3/EIL1-triggered transcriptional programs. Positive interactions such as activation, production, and stabilization are represented with lines that end in an arrowhead →. Negative interactions such as inactivation and repression are represented by lines that end in a hammerhead ⊣. Images were created with BioRender.

Figure 2

Simplified overview of the role of ethylene in mediating the tradeoff between abiotic stress and growth in plants. Abiotic stress induces ethylene biosynthesis and triggers ethylene accumulation in plants. Ethylene perception and signaling result in multiple physiological responses that not only inhibit plant growth, but also confer stress tolerance that maximizes plant survival in adverse conditions. Positive interactions such as activation, production, and stabilization are represented with lines that end in an arrowhead →. Negative interactions such as inactivation and repression are represented by lines that end in a hammerhead ⊣. The background image of balance was created with BioRender.

Figure 3

A model of stomatal closure regulation by crosstalk between ABA, BR, and ethylene in Arabidopsis. Endogenous ABA and ethylene accumulate in response to abiotic stress. The biosynthesis of ethylene is upregulated by BR but repressed by ABA due to the transcriptional regulation of ACS genes. The ABA biosynthesis is upregulated by ethylene through MHZ4/5. ABA induces ABI4 transcript levels and the ABI4 protein, in turn, represses the transcription of the ACS genes. Ethylene also regulates stomatal closure via two ROS-dependent pathways. One pathway is mediated by the ethylene-triggered activation of the Gα protein, which in turn promotes H₂O₂ production by activating the NADPH oxidase gene AtRbohF and by inducing NO accumulation via the transcriptional upregulation of the nitrate reductase gene NIA1. The increased ROS (H₂O₂ and NO) results in stomatal closure. The second pathway, vice versa, links ethylene with reduced ROS levels via EIN2-dependent synthesis of flavonols, secondary metabolites that serve as ROS scavengers. Conversely, high levels of ABA signaling lead to elevated ROS production and stomatal closure. Positive interactions such as activation, production, and stabilization are represented with lines that end in an arrowhead →. Negative interactions such as inactivation and repression are represented by lines that end in a hammerhead ⊣. The background image of stomata was created with BioRender.

Figure 4

A model of rice adaptation to partial and complete water submergence regulated by GA, ABA, BR, and ethylene. Upon full submergence of rice plants under water (left box), ethylene activates transcription of an ERF TF gene SUB1A, and the SUB1A protein then up-regulates anaerobic survival genes via the transcriptional induction and protein stabilization of ERF66/67 upon hypoxia stress. In addition, ethylene suppresses GA-mediated stem elongation by directly activating the transcription of DELLA protein genes, SLR1 and SLRL1, as well as by inhibiting BR signaling. Upon partial submergence under water (right box), ethylene acts via the EIL proteins to induce the transcript levels of ERF genes SK1 and SK2 bringing about the GA signaling-mediated stem elongation in rice. In deepwater wild rice, EIL-mediated signaling triggered by the hormone ethylene directly enhances GA production and induces shoot elongation by transcriptionally activating a GA biosynthesis gene SD1 that encodes a GA20-oxidase. Furthermore, ethylene promotes shoot elongation by relieving ABA-imposed shoot growth inhibition. Positive interactions such as activation, production, and stabilization are represented with lines that end in an arrowhead →. Negative interactions such as inactivation and repression are represented by lines that end in a hammerhead ⊣. The background image of a rice plant was created with BioRender.

Figure 5

A model of root growth regulation in Arabidopsis triggered by Al stress and mediated by the crosstalk between JA, CK, auxin, and ethylene. Under Al stress, enhanced ethylene production upregulates the local transcript levels of auxin biosynthesis genes TAA1 and YUCs promoted by the transcriptional upregulation of EIN3 and EIL1. The increased protein abundance of TAA1 and YUCs results in local auxin accumulation within the roots, suppressing primary root growth. Downstream of auxin, local accumulation of CK triggered by ARF7-mediated induction of the CK biosynthesis genes IPTs activates the CK response, which also contributes to root growth inhibition in response to Al stress. In parallel, COI1-mediated JA signaling downstream of ethylene is involved in Al stress-induced root growth inhibition through the transcriptional repression of PLT genes encoding AP2 TFs. Positive interactions such as activation, production, and stabilization are represented with lines that end in an arrowhead →. Negative interactions such as inactivation and repression are represented by lines that end in a hammerhead ⊣. The background image of an Arabidopsis root was created with BioRender.