Glycine betaine increases salt tolerance in maize (Zea mays L.) by regulating Na+ homeostasis

Abstract

Improving crop salt tolerance is an adaptive measure to climate change for meeting future food demands. Previous studies have reported that glycine betaine (GB) plays critical roles as an osmolyte in enhancing plant salt resistance. However, the mechanism underlying the GB regulating plant Na+ homeostasis during response to salinity is poorly understood. In this study, hydroponically cultured maize with 125 mM NaCl for inducing salinity stress was treated with 100 μM GB. We found that treatment with GB improved the growth of maize plants under non-stressed (NS) and salinity-stressed (SS) conditions. Treatment with GB significantly maintained the properties of chlorophyll fluorescence, including Fv/Fm, ΦPSII, and ΦNPQ, and increased the activity of the antioxidant enzymes for mitigating salt-induced growth inhibition. Moreover, GB decreased the Na+/K+ ratio primarily by reducing the accumulation of Na+ in plants. The results of NMT tests further confirmed that GB increased Na+ efflux from roots under SS condition, and fluorescence imaging of cellular Na+ suggested that GB reduced the cellular allocation of Na+. GB additionally increased Na+ efflux in leaf protoplasts under SS condition, and treatment with sodium orthovanadate, a plasma membrane (PM) H+-ATPase inhibitor, significantly alleviated the positive effects of GB on Na+ efflux under salt stress. GB significantly improved the vacuolar activity of NHX but had no significant effects on the activity of V type H+-ATPases. In addition, GB significantly upregulated the expression of the PM H+-ATPase genes, ZmMHA2 and ZmMHA4, and the Na+/H+ antiporter gene, ZmNHX1. While, the V type H+-ATPases gene, ZmVP1, was not significantly regulated by GB. Altogether these results indicate that GB regulates cellular Na+ homeostasis by enhancing PM H+-ATPases gene transcription and protein activities to improve maize salt tolerance. This study provided an extended understanding of the functions of GB in plant responses to salinity, which can help the development of supportive measures using GB for obtaining high maize yield in saline conditions.

Unfolding molecular switches for salt stress resilience in soybean: recent advances and prospects for salt-tolerant smart plant production

“…GB has an excellent role in improving photosynthetic efficiency and antioxidant enzyme activity to mitigate salt-induced growth inhibition. Moreover, GB maintained the Na + /K + ratio mainly by plummeting the buildup of Na + in plants ( Zhu et al., 2022 ). GB reduces the membrane peroxidation and improves the photosynthesis and yield under stress conditions in soybean ( Khalid et al., 2022 ).…”

“…GB treatment increased Na + efflux in leaf protoplasts and reduced the cellular distribution of Na + . Furthermore, GB improved the vacuolar activity of NHX and V type H + -ATPases genes to improve salt tolerance ( Zhu et al., 2022 ). A previous study reported that GB biosynthesis in plant tissues is highly energy intensive ( Bai et al., 2022 ).…”

Enhancing the Biological Control of Mite Species Infesting Olive Trees through Application of Predatory Mite Agistemus exsertus Gonzalez (Acari: Stigmaeidae) and Eco‐Friendly Natural Compounds

“…It also protects enzymes, proteins and other molecules involved in disease resistance (Papageorgiou and Murata, 1995; Lavanya and Amruthesh, 2017). Moreover, GB improves plant tolerance to stresses, including drought (Raza et al ., 2014), salinity (Hasanuzzaman et al ., 2014; Zhu et al ., 2022) and heavy metals (Ahmad et al ., 2020). Lavanya and Amruthesh (2017) reported that GB has effectively controlled the downy mildew disease affecting pearl millet ( Pennisetum glaucum L.).…”

Reshifting Na+ from Shoots into Long Roots Is Associated with Salt Tolerance in Two Contrasting Inbred Maize (Zea mays L.) Lines

“…Trehalose is a nonreducing diglucoside elevated in plants under salt stress, probably protecting protein and membrane structures and regulating the antioxidant systems to ameliorate ROS scavenging, and trehalose-6-phosphate synthase (TPS) is one of the key enzymes in terms of trehalose biosynthesis [ 33 ]. Moreover, in maize, glycine betaine [ 34 , 35 ], trehalose [ 36 ], ascorbate–proline–glutathione [ 37 ], and phosphate [ 28 ], are applied to counter salt stress, which is favorable for the maintenance of Na + /K + balance and improvements in antioxidant defense. Recently, single or combined analyses of genomes [ 38 ], transcriptomes [ 34 , 39 ], proteomes [ 40 , 41 , 42 , 43 ], and metabolomes [ 44 , 45 ] and a genome-wide association study (GWAS) revealed differential expression genes, small RNAs, and regulatory networks in plants under salt stress [ 46 , 47 , 48 ], which provided valuable information to understand the mechanism of salt response.…”