Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways

Abstract

Hydrogen sulfide (H2S) has been recently found to act as a potent priming agent. This study explored the hypothesis that hydroponic pretreatment of strawberry (Fragaria × ananassa cv. Camarosa) roots with a H2S donor, sodium hydrosulfide (NaHS; 100 μM for 48h), could induce long-lasting priming effects and tolerance to subsequent exposure to 100mM NaCI or 10% (w/v) PEG-6000 for 7 d. Hydrogen sulfide pretreatment of roots resulted in increased leaf chlorophyll fluorescence, stomatal conductance and leaf relative water content as well as lower lipid peroxidation levels in comparison with plants directly subjected to salt and non-ionic osmotic stress, thus suggesting a systemic mitigating effect of H2S pretreatment to cellular damage derived from abiotic stress factors. In addition, root pretreatment with NaHS resulted in the minimization of oxidative and nitrosative stress in strawberry plants, manifested via lower levels of synthesis of NO and H2O2 in leaves and the maintenance of high ascorbate and glutathione redox states, following subsequent salt and non-ionic osmotic stresses. Quantitative real-time RT-PCR gene expression analysis of key antioxidant (cAPX, CAT, MnSOD, GR), ascorbate and glutathione biosynthesis (GCS, GDH, GS), transcription factor (DREB), and salt overly sensitive (SOS) pathway (SOS2-like, SOS3-like, SOS4) genes suggests that H2S plays a pivotal role in the coordinated regulation of multiple transcriptional pathways. The ameliorative effects of H2S were more pronounced in strawberry plants subjected to both stress conditions immediately after NaHS root pretreatment, rather than in plants subjected to stress conditions 3 d after root pretreatment. Overall, H2S-pretreated plants managed to overcome the deleterious effects of salt and non-ionic osmotic stress by controlling oxidative and nitrosative cellular damage through increased performance of antioxidant mechanisms and the coordinated regulation of the SOS pathway, thus proposing a novel role for H2S in plant priming, and in particular in a fruit crop such as strawberry.

Hydrogen sulfide: a new endogenous player in an old mechanism of plant tolerance to high salinity

“…In addition, NaHS decreased in plants the activity of lipoxygenase, an enzyme implicated in the formation of lipid peroxides. Alleviation of NaCl-induced oxidative stress by H 2 S exogenous was also observed in alfalfa, bermudagrass, strawberry and cucumber (Wang et al 2012;Christou et al 2013;Shi et al 2013;Lai et al 2014;Sun & Luo 2014). The maintenance of high K + /Na + ratio in plant cells under salt-stress was also reported to be induced by H 2 S. Wheat seedlings treated with 50 µM NaHS, followed by 100 mM NaCl exposure exhibited increased K + /Na + ratio with augment of selective transport of K + over Na + through nonselective cation channels and salt overly sensitive 1 (SOS1), a plasma membrane Na + /H + antiporter (Deng et al 2016).…”

“…Induction of plasma membrane Na + /H + antiporter genes (e.g. SOS2-like, SOS3-like and SOS4) by NaHS was also described in strawberry plants under high salinity, indicating a role for H 2 S in K + uptake (Christou et al 2013). The K + /Na + homeostasis in salt-treated alfalfa was shown to be maintained by NaHS through the prevention of K + efflux likely triggered by lower expression of shaker-like K + outward-rectifying channel genes (Lai et al 2014).…”

“…Cucumis sativus (Yu et al 2013;Sun & Luo 2014) Cynodon dactylon (Shi et al 2013) Fragaria × ananassa (Christou et al 2013) Medicago sativa (Wang et al 2012;Lai et al 2014) Nicotiana tabacum (da-Silva et al 2017) Oryza sativa (Mostofa et al 2015) *Triticum aestivum (Khan et al 2017) Zea mays (Shan et al 2014) Increase of K + /Na + ratio…”

“…Fragaria × ananassa (Christou et al 2013) Hordeum vulgare (Chen et al 2015) Medicago sativa (Lai et al 2014) Triticum aestivum (Deng et al 2016) Protection of photosynthetic apparatus Fragaria × ananassa (Christou et al 2013) Oryza sativa (Mostofa et al 2015) Stimulation of seed germination and plant growth Arabidopsis thaliana Cucumis sativus (Sun & Luo 2014) Cynodon dactylon (Shi et al 2013) Medicago sativa (Wang et al 2012) Induction of osmoregulators accumulation…”

Exogenous Gibberellic Acid Ameliorates Salinity-Induced Morphological and Biochemical Alterations in Portulaca grandiflora

“…Over the past few years, many methods have been tested to overcome adverse effects of salinity stress on plants, namely mycorrhiza inoculation (Beltrano et al, 2013) hydrogen sulfide priming (Christou et al, 2013), ABA application (Osakabe et al, 2014) and salicylic acid treatment (LI et al, 2014). Previously, Ashraf et al (2002) reported the combining effects of gibberellic acid and salt stress on the photosynthetic capacity of wheat plants.…”