Exogenous hydrogen sulfide mediates Na+ and K+ fluxes of salt gland in salt-secreting mangrove plant Avicennia marina

Abstract

Hydrogen sulfide (H2S), is a crucial biological player in plants. Here, we primarily explored the interaction between sodium hydrosulfide (NaHS, a H2S donor) and the fluxes of Na+ and K+ from the salt glands of mangrove species Avicennia marina with non-invasive micro-test technology (NMT) and quantitative real-time PCR (qRT-PCR) approaches under salinity treatments. The results showed that under 400 mM NaCl treatment, the addition of 200 μM NaHS markedly increased the quantity of salt crystals in the adaxial epidermis of A. marina leaves, accompanied by an increase in the K+/Na+ ratio. Meanwhile, the endogenous content of H2S was dramatically elevated in this process. NMT result revealed that the Na+ efflux was increased from salt glands, while K+ efflux was decreased with NaHS application. On the contrary, the effects of NaHS were reversed by H2S scavenger hypotaurine (HT), and DL-propargylglycine (PAG), an inhibitor of cystathionine-γ-lyase (CES, a H2S synthase). Moreover, enzymic assay revealed that NaHS increased the activities of plasma membrane and tonoplast H+-ATPase. qRT-PCR analysis revealed that NaHS significantly increased the genes transcript levels of tonoplast Na+/H+ antiporter (NHX1), plasma membrane Na+/H+ antiporter (SOS1), plasma membrane H+-ATPase (AHA1), and tonoplast H+-ATPase subunit c (VHA-c1), while suppressed above-mentioned gene expressions by the application of HT and PAG. Overall, H2S promotes Na+ secretion from the salt glands of A. marina by up-regulating the plasma membrane and tonoplast Na+/H+ antiporter and H+-ATPase.

Overexpression of ZmDUF1644 from Zoysia matrella enhances salt tolerance in Arabidopsis thaliana

“…In addition, excessive Na + /K + also caused plant cellular dehydration, membrane dysfunction, and ion toxicity (Gupta et al 2021;Zhang et al 2021c). To alleviate ion stress, plants mainly reduce salt ion concentration in the cytoplasm through reduced uptake (Sofy et al 2020), increased exclusion (Wei et al 2022), or compartmentalized salt ions in the vesicles (Lang et al 2017). Consequently, the salt tolerance of plants is associated with the ability to exclude sodium ions from excess uptake and maintain low sodium to potassium ratio (Xie et al 2021).…”

Bracelet salt glands of the recretohalophyte Limonium bicolor: Distribution, morphology, and induction

“…Normally, a salt gland in L. bicolor contains 16 cells composed of four groups of secretory cells, accessory cells, inner cup cells, and outer cup cells in a radially symmetric structure (Leng et al, 2018). This symmetric pattern is also observed in the eight-cell salt glands of salt cedar (Tamarix) (Thomson and Liu, 1967;Wilson et al, 2017) and the 20-cell salt glands of Avicennia (Tan et al, 2015;Wei et al, 2022).…”

“…To date, 68 of the 370 known recretohalophyte species were shown to have salt glands (Yuan et al, 2016b), such as the bicellular salt glands in S. foliosa (Arisz et al, 1995) and the multicellular salt glands in grey mangrove ( Avicennia marina ) (Wei et al, 2022) and Indian mangrove ( Avicennia officinalis ) (Tan et al, 2015). However, few reports have focused on salt gland development due to the lack of genome information or a transformation system.…”

RNA-sequencing transcriptome analysis of Avicennia marina (Forsk.) Vierh. leaf epidermis defines tissue-specific transcriptional response to salinity treatment

“…A. marina , as a pioneer tree species of the mangrove ecosystem and a typical salt-secreting mangrove plant, shows great advantages in salt resistance. Our previous studies showed that the salt crystals on the leaf surface of A. marina increased significantly after 400 mM NaCl treatment 4 , 6 . Further proteomic analysis revealed that the abundances of proteins related to photosynthesis were sharply decreased, and the stomatal and nonstomatal limitations could account for the photosynthetic reduction 2 .…”

“…As typical halophytes, mangroves can be divided into the following types: nonsalt-secreting and salt-secreting plants. Mangroves have formed sets of unique characteristics to adapt well to high salinity conditions 4 . It is generally accepted that nonsalt-secreting mangrove plants are capable of extruding excess salt through ultrafiltration at the roots 5 .…”