The endogenous L-cysteine desulfhydrase and hydrogen sulfide participate in supplemented phosphorus-induced tolerance to salinity stress in maize (Zea mays) plants

Although phosphorus supplementation (SP) has been shown to improve salinity tolerance in plants, crosstalk betweenhydrogen sulfide (H2S) or L-cysteine desulfhydrase (LDES) and SP-induced salinity tolerance needs to be elucidated. Thus, prior toinitiation of stress treatment, young seedlings were transferred to aqueous solution containing the scavenger of H2S, 0.1 mM hypotaurine(HT), or the inhibitor of LDES, 0.3 mM DL-propargylglycine (PAG), for 12 h. The plants grown under control (no NaCl added) orsalinity stress (SS; 100 mM NaCl) were then supplemented with SP (2.0 mM in total) as KH2PO4 for 5 weeks. SS caused a significantdecrease in plant growth, PSII maximum efficiency, chlorophyll a and b, leaf water potential, relative water content, mineral elementcontents, ascorbate, and glutathione, but a significant increase in hydrogen peroxide, malondialdehyde, electron leakage, proline, theactivities of different key antioxidant enzymes, Na+ contents, endogenous H2S, and LDES activity. The SP-induced tolerance to salinitystress of maize plants was found to be due to reduced leaf Na+ content and oxidative stress, as well as improved antioxidant defencesystem, leaf mineral nutrient contents, plant growth and photosynthetic traits, levels of H2S and proline, and LDES activity. However,HT significantly reversed the levels of H2S, but did not reduce LDES activity. The application of PAG reversed both H2S and LDES inthe salinity-stressed maize plants. Both HT and PAG reversed the positive effects of SP on oxidative stress and the antioxidant defencesystem, suggesting that H2S and LDES both jointly participated in P-induced salinity tolerance of maize plants.

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Ahanger MA, Agarwal RM (2017). Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L) as influenced by potassium supplementation. Plant Physiology and Biochemistry 115: 449- 460.
Ahmad Z, Waraich EA, Ahmad R, Shahbaz M (2017). Modulation in water relations, chlorophyll contents and antioxidants activity of maize by foliar phosphorus application under drought stress. Pakistan Journal of Botany 49: 11-9.
Al-Taey DK (2018). The role of GA and organic matter to reduce the salinity effect on growth and leaves contents of elements and antioxidant in pepper. Plant Archive 18: 479-488.
Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Bhardwaj R et al. (2018). Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma 255: 459-469.
Arshad M, Ali S, Noman A, Ali Q, Rizwan M et al. (2016). Phosphorus amendment decreased cadmium (Cd) uptake and ameliorates chlorophyll contents, gas exchange attributes, antioxidants, and mineral nutrients in wheat (Triticum aestivum L.) under Cd stress. Archives of Agronomy and Soil Science 62: 533-546.
Bargaz A, Nassar RMA, Rady MM, Gaballah MS,Thompson SM et al. (2016). Improved salinity tolerance by phosphorus fertilizer in two Phaseolus vulgaris recombinant inbred lines contrasting in their P‐efficiency. Journal of Agronomy and Crop Science 202: 497-507.
Bates LS, Waldren RP, Teare ID (1973). Rapid determination of free proline for water stress studies. Plant and Soil 39: 205-207.
Carstensen A, Herdean A, Schmidt SB, Sharma A, Spetea C et al. (2018). The impacts of phosphorus deficiency on the photosynthetic electron transport chain. Plant Physiology 177: 271-284.
Chance B, Maehly C (1955). Assay of catalase and peroxidases. Methods in Enzymology 2: 764-775.
Chapman HD, Pratt PF (1982). Methods of Plant Analysis I Methods of Analysis for Soils, Plants and Water. Riverside, CA, USA: Chapman Publishers.
Chen J, Wang WH, Wu FH, You CY, Liu TW et al. (2013). Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant and Soil 362: 301-318.
Çimrin KM, Türkmen Ö, Turan M, Tuncer B (2010). Phosphorus and humic acid application alleviate salinity stress of pepper seedling. African Journal of Biotechnology 9: 5845-5851.
Daei-hassani B, Chaparzadeh N, Sartibi L, Abedini M (2016). Effects of phosphorus on antioxidant system in pepper cultivars under saline conditions. Plant Physiology 7: 1935-1941.
Das P, Manna I, Biswas AK, Bandyopadhyay M (2018). Exogenous silicon alters ascorbate-glutathione cycle in two salt-stressed indica rice cultivars (MTU 1010 and Nonabokra). Environmental Science and Pollution Research 25: 26625-26642.
da-Silva CJ, Mollica DC, Vicente MH, Peres LE, Modolo LV (2018). NO, hydrogen sulfide does not come first during tomato response to high salinity. Nitric Oxide 76: 164-173.
Deng YQ, Bao J, Yuan F, Liang X, Feng ZT et al. (2016). Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na+ content. Plant Growth Regulation 79: 391-399.
Dionisio-Sese ML, Tobita S (1998). Antioxidant responses of rice seedlings to salinity stress. Plant Science 135: 1-9.
Ellman GL (1959). Tissue sulphydryl groups. Archives of Biochemistry and Biophysics 82: 70‐77.
Gandonou CB, Prodjinoto H, Zanklan SEA, Wouyou AD, Lutts S et al. (2018). Effects of salinity stress on growth in relation to gas exchanges parameters and water status in amaranth (Amaranthus cruentus). International Journal of Plant Physiology and Biochemistry 10: 19-27.
Ghani MNO, Awang Y, Ismail MF (2018). Effects of NaCl salinity on leaf water status, proline and mineral ion content of four Cucurbitaceae species. Australian Journal of Crop Science 12: 1434.
Guo H, Zhou H, Zhang J, Guan W, Xu S et al. (2017).L‐cysteine desulfhydrase‐related H2 S production is involved in OsSE5‐ promoted ammonium tolerance in roots of Oryza sativa. Plant, Cell, and Environment 40: 1777-1790.
Isayenkov SV and Maathuis FJM (2019). Plant salinity stress: many unanswered questions remain. Frontiers in Plant Science 10: 80. doi: 10.3389/fpls.2019.00080
Kabała K, Zboińska M, Głowiak D, Reda M, Jakubowska D et al. (2018). Interaction between the signaling molecules hydrogen sulfide and hydrogen peroxide and their role in vacuolar H+‐ATPase regulation in cadmium‐stressed cucumber roots. Physiologia Plantarum 166: 688-704.
Kaya C, Ashraf M (2015). Exogenous application of nitric oxide promotes growth and oxidative defense system in highly boron stressed tomato plants bearing fruit. Scientia Horticulturae (Amsterdam) 185: 43-47.
Kaya C, Ashraf M (2019).The mechanism of hydrogen sulfide mitigation of iron deficiency induced chlorosis in strawberry (Fragaria × ananassa) plants. Protoplasma 56: 371-382.
Kaya C, Tuna AL, Dikilitas M, Ashraf M, Koskeroglu S et al. (2009). Supplementary phosphorus can alleviate boron toxicity in tomato. Scientia Horticulturae 121: 284-288.
Li ZG, Gong M, Liu P (2012). Hydrogen sulfide is a mediator in H2 O2-induced seed germination in Jatropha curcas. Acta Physiologia Plantarum 34: 2207-2213.
Liang C, Ma C, Zhang Z, Wei Z, Gao T, Zhao Q et al. (2018) Longterm exogenous application of melatonin improves nutrient uptake fluxes in apple plants under moderate drought stress. Environment and Experimental Botany 155: 650–661
Ma Y, Zhang W, Niu J, Ren Y, Zhang F (2019). Hydrogen sulfide may function downstream of hydrogen peroxide in salt stress-induced stomatal closure in Vicia faba. Functional Plant Biology 46: 136- 145. Milosevic N, Slusarenko AJ (1996). Active oxygen metabolism and lignification in the hypersensitive response in bean. Physiological and Molecular Plant Pathology 49: 143-158.
Mohammad M, Shibli R, Ajlouni M, Nimri L (1998). Tomato root and shoot responses to salt stress under different levels of phosphorus nutrition. Journal of Plant Nutrition 21: 1667-1680.
Mostofa MG, Saegusa D, Fujita M, Tran LSP (2015). Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Frontiers in Plant Science 6: 1055. doi: 10.3389/ fpls.2015.01055
Mukherjee SP, Choudhuri MA (1983). Implications of water stressinduced changes in the leaves of indigenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiologia Plantarum 58: 166-170.
Negrão S, Schmöckel SM, Tester M (2017). Evaluating physiological responses of plants to salinity stress. Annals of Botany 119: 1-11.
Poudyal D, Rosenqvist E, Ottosen CO (2019). Phenotyping from lab to field–tomato lines screened for heat stress using Fv/Fm maintain high fruit yield during thermal stress in the field. Functional Plant Biology 46: 44-55.
Qiao Z, Jing T, Liu Z, Zhang L, Jin Z, Liu D, Pei Y (2015) H2 S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis. Plant Soil 393:137-146.
Rady MM, El-Shewy AA, El-Yazal MAS, Abdelaal KE (2018). Response of salt-stressed common bean plant performances to foliar application of phosphorus (MAP). International Letters of Natural Sciences 72: 7-20.
Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016). Calcium supplementation improves Na+/K+ ratio, antioxidant defense and glyoxalase systems in salt-stressed rice seedlings. Frontiers in Plant Science 7: 609.
Rahneshan Z, Nasibi F, Moghadam AA (2018). Effects of salinity stress on some growth, physiological, biochemical parameters and nutrients in two pistachio (Pistacia vera L.) rootstocks. Journal of Plant Interactions 13: 73-82.
Sacala E, Demczuk A, Grzys E (2016). The response of maize seedlings to salt stress under increasing levels of phosphorus. Journal of Elementology 21: 185-194.
Sadji-Ait Kaci H, Chaker-Haddadj A, Aid F (2017). Interactive effects of salinity and two phosphorus fertilizers on growth and grain yield of Cicer arietinum L. Acta Agriculturae Scandinavica, Section B— Soil & Plant Science 67: 208-216.
Scheible WR, Rojas‐Triana M (2018). Sensing, signalling, and control of phosphate starvation in plants: molecular players and applications. Annual Plant Reviews Online, 23-63.
Strain HH, Svec WA (1966). Extraction separation estimation and isolation of the chlorophylls. In: Vernon LP, Seely GR, editors. The Chlorophylls. New York: Academic Press.
Tariq A, Pan K, Olatunji OA, Graciano C, Li Z et al. (2018). Impact of phosphorus application on drought resistant responses of Eucalyptus grandis seedlings. Physiologia Plantarum 166: 894- 908. doi.org/10.1111/ppl.12868
Tian Z, Li J, Jia X, Yang F, Wang Z (2016). Assimilation and translocation of dry matter and phosphorus in rice genotypes affected by saltalkaline stress. Sustainability 8: 568.
Vandamme E, Rose T, Saito K, Jeong K, Wissuwa M (2016). Integration of P acquisition efficiency, P utilization efficiency and low grain P concentrations into P-efficient rice genotypes for specific target environments. Nutrient Cycling in Agroecosystems 104: 413-427.
Van Rossum MWPC, Alberda M, Van Der Plas LHW (1997). Role of oxidative damage in tulip bulb scale micropropagation. Plant Science 130: 207-216.
Velikova V, Yordanov I, Edreva A (2000). Oxidative stress and some antioxidant system in acid rain treated bean plants: protective role of exogenous polyamines. Plant Science 151: 59-66.
Verma E, Singh S, Mishra AK (2019). Salinity-induced oxidative stressmediated change in fatty acids composition of cyanobacterium Synechococcus sp. PCC7942. International Journal of Environmental Science and Technology 16: 875-886.
Wang BL, Shi L, Li Y X, Zhang WH (2010). Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231: 1301-1309.
Wang Y, Li L, Cui W, Xu S, Shen W et al. (2012). Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant and Soil 351: 107-119.
Wang Y, Li X, Li J, Bao Q, Zhang F, Tulaxi G et al. (2016). Salt-induced hydrogen peroxide is involved in modulation of antioxidant enzymes in cotton. The Crop Journal 4: 490-498.
Wei G, Zhang W, Cao H, Yue S, Li P, Yang H (2019). Effects hydrogen sulfide on the antioxidant system and membrane stability in mitochondria of Malus hupehensis under NaCl stress. Biologia Plantarum 63: 228-236.
Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2012). Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L). Plant Omics Journal 5: 60-67.
Yamasaki S, Dillenburg LR (1999). Measurements of leaf relative water content in Araucaria angustifolia. Revista Brasileira de Fisiologia Vegetal 11: 69-75.
Zeng Y, Li Q, Wang H, Zhang J, Du J et al. (2018). Two NHX‐type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress. Plant Biotechnology Journal 16: 310-321.
Zhang H, Hu LY, Hu KD, He YD, Wang SH et al. (2008). Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. Journal of Integrative Plant Biology 50: 1518-1529.
Zhang B, Zhang H, Wang H, Wang P, Wu Y et al. (2018). Effect of phosphorus additions and arbuscular mycorrhizal fungal inoculation on the growth, physiology, and phosphorus uptake of wheat under two water regimes. Communications in Soil Science and Plant Analysis 49: 862-874.
Zhang J, Ma X, Chen B, Xu Z, Wang Y (2018). Effects of exogenous hydrogen sulfide on physiological and biochemical characteristics of tobacco seedlings under drought stress. Journal of Agricultural Science and Technology (Beijing) 20: 112-119.
Zhang X, Zhang Y, Zhang L, Zhao H, Li H (2017). Hydrogen sulphide improves iron homeostasis in wheat under irondeficiency. Journal of Plant Sciences 5: 170-176.