Involvement of ethylene receptors in the salt tolerance response of Cucurbita pepo

Abstract

Abiotic stresses have a negative effect on crop production, affecting both vegetative and reproductive development. Ethylene plays a relevant role in plant response to environmental stresses, but the specific contribution of ethylene biosynthesis and signalling components in the salt stress response differs between Arabidopsis and rice, the two most studied model plants. In this paper, we study the effect of three gain-of-function mutations affecting the ethylene receptors CpETR1B, CpETR1A, and CpETR2B of Cucurbita pepo on salt stress response during germination, seedling establishment, and subsequent vegetative growth of plants. The mutations all reduced ethylene sensitivity, but enhanced salt tolerance, during both germination and vegetative growth, demonstrating that the three ethylene receptors play a positive role in salt tolerance. Under salt stress, etr1b, etr1a, and etr2b germinate earlier than WT, and the root and shoot growth rates of both seedlings and plants were less affected in mutant than in WT. The enhanced salt tolerance response of the etr2b plants was associated with a reduced accumulation of Na+ in shoots and leaves, as well as with a higher accumulation of compatible solutes, including proline and total carbohydrates, and antioxidant compounds, such as anthocyanin. Many membrane monovalent cation transporters, including Na+/H+ and K+/H+ exchangers (NHXs), K+ efflux antiporters (KEAs), high-affinity K+ transporters (HKTs), and K+ uptake transporters (KUPs) were also highly upregulated by salt in etr2b in comparison with WT. In aggregate, these data indicate that the enhanced salt tolerance of the mutant is led by the induction of genes that exclude Na+ in photosynthetic organs, while maintaining K+/Na+ homoeostasis and osmotic adjustment. If the salt response of etr mutants occurs via the ethylene signalling pathway, our data show that ethylene is a negative regulator of salt tolerance during germination and vegetative growth. Nevertheless, the higher upregulation of genes involved in Ca2+ signalling (CpCRCK2A and CpCRCK2B) and ABA biosynthesis (CpNCED3A and CpNCED3B) in etr2b leaves under salt stress likely indicates that the function of ethylene receptors in salt stress response in C. pepo can be mediated by Ca2+ and ABA signalling pathways.

Ethylene signaling in salt-stressed Arabidopsis thaliana ein2-1 and ctr1-1 mutants – A dissection of molecular mechanisms involved in acclimation

“…The latter is supported by the observation that constitutive ethylene signaling promotes germination during salt stress, whereas most ethylene insensitive mutants perform worse (Achard et al, 2006;Wang et al, 2007). However, detailed genetic analyses of loss-of-function mutants of ethylene receptors have demonstrated distinct roles for different receptors in the regulation of salt stress (Wilson et al, 2014;Cebrián et al, 2021). Ethylene is perceived by a group of five receptors ETHYLENE RESPONSE1 (ETR1), ETR2, ETHYLENE INSENSITIVE4 (EIN4), ETHYLENE RESPONSE SENSOR1 (ERS1), with ETR1 and EIN4 operating as negative regulators of germination under salt stress, and ETR2 acting as a positive regulator (Depaepe et al, 2021).…”

“…Ethylene is perceived by a group of five receptors ETHYLENE RESPONSE1 (ETR1), ETR2, ETHYLENE INSENSITIVE4 (EIN4), ETHYLENE RESPONSE SENSOR1 (ERS1), with ETR1 and EIN4 operating as negative regulators of germination under salt stress, and ETR2 acting as a positive regulator (Depaepe et al, 2021). Furthermore, the action of ETR1 and ETR2 are independent of ethylene signaling and mediate the salt stress response through ABA and Ca 2+ pathways (Wilson et al, 2014;Cebrián et al, 2021). When ethylene is absent the canonical signaling cascade is suppressed via CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1), a Raf kinase which inhibits the endoplasmic reticulum protein ETHYLENE INSEN-SITIVE 2 (EIN2) by direct phosphorylation.…”

Role of Ethylene Biosynthesis Genes in the Regulation of Salt Stress and Drought Stress Tolerance in Petunia

“…The involvement of ethylene in the abiotic stress tolerance mechanism has been reported in many plant species, however, the role of its involvement in the mechanism remains unclear because it can act as a positive or negative regulator of the stress tolerance depending on its concentrations, plant species, and plant growth stages ( Albacete et al, 2009 ; Wi et al, 2010 ; Dong et al, 2011 ; Freitas et al, 2017 ; Xu et al, 2019 ; Cebrián et al, 2021 ). In this study, we examined how ethylene affects salt and drought stress tolerance in Petunia hybrida cv.…”

“…However, a decisive conclusion on whether ethylene plays a positive role in plant response to abiotic stress could not be reached at this time. While many researchers reported a positive role of ethylene or its precursor 1-aminocyclopropane-1-carboxylate (ACC) in stress tolerance of various plant species, such as corn, Arabidopsis , tomato, grapevines ( Lin et al, 2012 ; Yang et al, 2013 ; Freitas et al, 2017 ; Gharbi et al, 2017 ; Xu et al, 2019 ), other researchers claimed a negative role of ethylene in some plant growth (such as Cucurbita pepo , tomato, Arabidopsis , and tobacco) under abiotic stress ( Albacete et al, 2009 ; Wi et al, 2010 ; Dong et al, 2011 ; Cebrián et al, 2021 ). The role of ethylene in the response regulation to abiotic stress depends on its level in plant tissue and plants’ sensitivity to it, as the optimal ethylene level for normal plant growth may vary at different stages and in different plant species ( Khan et al, 2008 ; Tao et al, 2015 ).…”

Tolerance Screening for Phytophthora capsici and Fusarium solani f. sp. cucurbitae in Cucurbita spp. and Gene Expression Responses in Mutant Families

“…Within Cucurbita spp. EMS-mutant collections, individuals with higher tolerances to abiotic [25,26] and biotic stresses [27] have been identified via screening, and the function of the altered genes with phenotypes has been obtained [28]. However, this has never been undertaken for soil-borne pathogen tolerance.…”