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. 2021 Apr 1;8(1):73.
doi: 10.1038/s41438-021-00508-z.

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

Gustavo Cebrián  1 , Jessica Iglesias-Moya  1 , Alicia García  1 , Javier Martínez  1 , Jonathan Romero  1 , José Javier Regalado  1 , Cecilia Martínez  1 , Juan Luis Valenzuela  1 , Manuel Jamilena  2
Affiliations

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

Gustavo Cebrián et al. Hortic Res. .

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.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Effect of salt stress on germination parameters of WT and etr1b, etr1a, and etr2b.
A Germination rates of WT and etr1b, etr1a, and etr2b ethylene receptor mutants under control and NaCl conditions. The percentage of germination was analysed every 2 h at the indicated time points. The data represent means of three independent replicates with at least 50 seeds counted per replicate. B, C, and D Effect of NaCl stress treatment on germination initiation, time at which 50% of seed is germinated, and average germination time. The bottom graphs show the percentage of increase of each parameter in response to salt stress in WT and mutant plants with respect to plants of the same genotype grown under control conditions. Means were obtained from four independent replicates with at least 50 seeds per replicate. Different letters indicate statistically significant differences (P < 0.05) between samples
Fig. 2
Fig. 2. Effect of salt stress on growth parameters of WT and etr1b, etr1a, and etr2b seedlings.
A Effect of salt stress on radicle length at 48 h. B Effect of salt stress on hypocotyl length in seedlings growing in darkness for 72 h. The bottom graphs of each figure show the percentage of reduction of each parameter in response to salt stress in WT and mutant plants with respect to plants of the same genotype growing under control conditions. Different letters indicate statistically significant differences (P < 0.05) between samples
Fig. 3
Fig. 3. Effect of salt stress on the growth of WT and etr1b, etr1a, and etr2b plants grown for 20 days under control and NaCl conditions.
A WT and etr2b shoots and roots. B Root balls of WT and etr2b plants. C, D Effect of salt stress on leaf and root biomass. The bottom graphs of each figure show the percentage of reduction of each parameter in response to salt stress in WT and mutant plants with respect to plants of the same genotype growing under control conditions. Different letters indicate statistically significant differences (P < 0.05) between samples
Fig. 4
Fig. 4. Effect of salt stress on root and leaf development of WT and ethylene receptor etr2b mutant of C. pepo at different days after sowing (DAS).
The graphs at the top in A, B, C and D show the growth rates of root length and plant height, as well as root and leaf biomass, in plants growing under control and NaCl conditions. The graphs at the bottom show the percentage of reduction of the same parameters in response to salt stress in WT and mutant plants with respect to plants growing under control conditions. Different letters indicate statistically significant differences (P < 0.05) between samples
Fig. 5
Fig. 5. Content of stress metabolites in WT and etr2b mutant leaves of plants growing under control and NaCl conditions for a total of 45 days after sowing (DAS).
A, B and C shows the content of proline, total carbohydrates and anthocyanins, respectively. The bottom graphs show the increment in metabolite content in response to salt stress in WT and mutant plants. DW, dry weight. Different letters indicate statistically significant differences (P < 0.05) between samples
Fig. 6
Fig. 6. Relative expression of genes encoding for ion transporters, salt stress signalling and ABA biosynthesis in leaves of WT and etr2b plants grown for 45 days under control and NaCl conditions.
A Potassium transporters CpKUPs. B K+/H+ efflux antiporters CpKEAs. C Sodium transporter CpHKT1A and Na+/H+ exchanger CpNHX1-3B. D Calmodulin-binding receptor-like cytoplasmic kinase, CpCRCKs. E 9-cis-epoxycarotenoid dioxygenase CpNCEDs, involved in ABA biosynthesis. In each gene family, the number of each gene corresponds to that of Arabidopsis with the highest identity at the protein sequence level, and the A and B letters at the end of each gene corresponds to paralogs derived from the A and B subgenomes of C. pepo, respectively. The relative level of each transcript was assessed by qRT–PCR in three independent replicates and normalised by the ∆∆CT method. Different letters indicate statistically significant differences (P < 0.05) between samples
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