Influences of sea water on the ethylene-biosynthesis, senescence-associated gene expressions, and antioxidant characteristics of Arabidopsis plants

  • Kuan-Hung LIN Chinese Culture University, Department of Horticulture and Biotechnology, Taipei 11114
  • Meng-Yuan HUANG National Chung Hsing University, Department of Life Sciences, Taichung 40227
  • Wei-Jun XIE Ming Chuan University, Department of Biotechnology, Taoyuan 333
  • Shwu-Fen PAN Ming Chuan University, Department of Biotechnology, Taoyuan 333
  • Yi-Sheng CHEN Ming Chuan University, Department of Biotechnology, Taoyuan 333
  • Hui-Chung WU Ming Chuan University, Department of Biotechnology, Taoyuan 333
  • Hsin-Hung LIN Chinese Culture University, Department of Horticulture and Biotechnology, Taipei 11114
  • Chih-Ming CHIANG Ming Chuan University, Department of Biotechnology, Taoyuan 333
Keywords: calcium; ethylene; leaf senescence; salinity; sea water; signal transduction

Abstract

We evaluated the physiological and antioxidant characteristics of Arabidopsis thaliana (At) plants grown in different sea water (SW) products containing trace elements, namely RO3, 300K, and 340K, at various dilutions. The synthetic water (namely 300K-Test), a mixture of the main ions of SW including 143.08 mg L-1 Mg2+, 5.74 mg L-1 Na+, 170 mg L-1 K+, and 33.5 mg L-1 Ca2+ with equal concentrations to those in 300K SW without trace elements, was also used to culture At plants and study the influences that the major ions had on regulating ethylene production. The ethylene-biosynthesis (ACS7 and ACO2) and senescence-associated (NAP, SAG113, and WRKY6) gene expressions in SW- and ionic-treated At plants in response to transcriptional signaling pathways of ethylene response mechanisms were also investigated. Our results show that down-regulation of the ACS7 gene in 300K-treated plants significantly reduced the ethylene content but remarkably increased chlorophyll, total phenol, and DPPH radical scavenging accumulations and strengthened the salt tolerance of 300K-treated plants. The expression of the ACS7 gene of At plants under 300K, Ca2+, Mg2+, and Na+ treatments was correlated with decreases in NAP, SAG113, and WRKY6 gene expressions. The application of Ca2+ increased total phenol content and reduced the accumulation of superoxide, which in combination decreases plant aging brought on by ethylene. However, K+ treatment inhibited SGA113 gene expression, resulting in reducing ACS7 gene expression and ethylene content. The characterization and functional analysis of these genes should facilitate our understanding of ethylene response mechanisms in plants.

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References

Alet AI, Diego HS, Cuevas JC, Marina M, Carrasco P, Altabell T, … Ruiz OA (2012). Plant Science 182:94-100.

https://doi.org/10.1016/j.plantsci.2011.03.013

Alvarez-Aragon R, Rodriguez-Navarro A (2017). Nitrate-dependent shoot sodium accumulation and osmotic unctions of sodium in Arabidopsis under saline conditions. Plant Journal 91:208-219. https://doi.org/10.1111/tpj.13556

Arnon DI (1949). Copper enzymes in isolated chloroplasts, polyphenoxidase in Beta vulgaris. Plant Physiology 24:1-15.

https://doi.org/10.1104/pp.24.1.1

Aghdam MS, Hassanpouraghdam MB, Paliyath G, Farmani B (2012). The language of calcium in postharvest life of fruits, vegetables and flowers. Scientia Horticulturae 144:102-115. https://doi.org/10.1016/j.scienta.2012.07.007

Atzori G, Nissim WG, Caparrotta S, Masi E, Azzarello E, Pandolfi C, … Mancuso S (2016). Potential and constraints of different seawater and freshwater blendsas growing media for three vegetable crops. Agriculture Water Management 176:255-262. https://doi.org/10.1016/j.agwat.2016.06.016

Balal RM, Khan MM, Shahid M, Mattson NS, Abbas T, Ashfaq M, … Iqbal Z (2012). Comparative studies on the physiobiochemical, enzymatic, and ionic modifications in salt-tolerant and salt-sensitive citrus rootstocks under NaCl stress. Journal of American Society of Horticulture Science 137:86-95.

https://doi.org/10.21273/JASHS.137.2.86

Caparrotta S, Masi E, Atzori G, Diamanti I, Azzarello E, Mancuso S, Pandolfi C (2019). Growing spinach (Spinacia oleracea) with different seawater concentrations: Effects on fresh, boiled and steamed leaves. Scientia Horticulturae 256:108540. https://doi.org/10.1016/j.scienta.2019.05.067

Ceusters J, Van de Poel B (2018). Ethylene exerts species-specific and age-dependent control of photosynthesis. Plant Physiology 176:2601-2612. https://doi.org/10.1104/pp.17.01706

Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007). Modulation of ethylene responses affects plant salt-stress responses. Plant Physiology 143:707-719. https://doi.org/10.1104/pp.106.094292

Chiang CM, Kuo WS, Lin KH (2014). Cloning and gene expression analysis of sponge gourd ascorbate peroxidase gene and winter squash superoxide dismutase gene under respective flooding and chilling stresses. Horticulture, Environment and Biotechnology 55:129-137. https://doi.org/10.1007/s13580-014-0116-4

Ding J, Yang T, Feng H, Dong M, Slavin M, Xiong S, Zhao S (2016). Enhancing contents of r-aminobutyric acid (GABA) and other micronutrients in dehulled rice during germination under normoxic and hypoxic conditions. Journal of Agriculture and Food Chemistry 64:1094-1102. https://doi.org/10.1021/acs.jafc.5b04859

Dewanto V, Wu X, Adom KK, Hai L, Liu R (2002). Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. Journal of Agriculture and Food Chemistry 50:3010-3014.

https://doi.org/10.1021/jf0115589

Dong H, Zhen Z, Peng J, Chang L, Gong Q, Wang NN (2011). Loss of ACS7 confers abiotic stress tolerance by modulating ABA sensitivity and accumulation in Arabidopsis. Journal of Experimental Botany 62:4875-4887.

https://doi.org/10.1093/jxb/err143

Errabii T, Gandonou CB, Essalmani H, Abrini J, Idaomar M, Skali-Senhaji N (2006). Growth, proline and ion accumulation in sugarcane callus cultures under drought-induced osmotic stress and its subsequent relief. African Journal of Biotechnology 5(16):1488-1493. https://doi.org/10.4314/ajb.v5i16.43144

Foyer CH, Lopez DH, Date JF, Scott IM (1997). Hydrogen peroxide and glutathione associated mechanisms of acclamatory stress tolerance and signaling. Physiologia Plantarum 100:241-254.

https://doi.org/10.1034/j.1399-3054.1997.1000205.x

Gao Q, Xiong T, Li X, Chen W, Zhu X (2019). Calcium and calcium sensors in fruit development and ripening. Scitifia Horticulturae 253:412-421. https://doi.org/10.1016/j.scienta.2019.04.069

Garcia-Sanchez F, Syvertsen JP (2009). Substrate type and salinity affect growth allocation, tissue ion concentrations, and physiological responses of Carrizo citrange seedlings. HortScience 44:1432-1437.

https://doi.org/10.21273/HORTSCI.44.5.1432

Gonzalez P, Syvertsen JP, Etxeberria JP (2012). Sodium distribution in salt-stressed citrus rootstock seedlings. HortScience 47:1504-1511. https://doi.org/10.21273/HORTSCI.47.10.1504

Gu L, Ma Q, Zhang C, Wang C, Wei H, Wang H, Yu S (2019). The cotton GhWRKY91 transcription factor mediates leaf senescence and responses to drought stress in transgenic Arabidopsis thaliana. Frontiers in Plant Science 10:1352. https://doi.org/10.3389/fpls.2019.01352

Higgins MF, Rudkin B, Kuo CH (2019). Oral ingestion of deep ocean minerals increases high-intensity intermittent running capacity in soccer players after short-term post-exercise recovery: A double-blind, placebo-controlled crossover trial. Marine Drugs 17:309. https://doi.org/10.3390/md17050309

Hoque A, Banu NA, Okuma E, Amakpo K, Nakamura Y, Shimoishi Y, Murata Y (2007). Exogenous proline and glycinebetaine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco bright yellow-2 suspension-cultured cells. Journal of Plant Physiology 164:1457-1468. https://doi.org/10.1016/j.jplph.2006.10.004

Hua J, Meyerowitz EM (1998). Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261-271. https://doi.org/10.1016/S0092-8674(00)81425-7

Hussain MI, Reigosaa MJ (2014). Higher peroxidase activity, leaf nutrient contents and carbon isotope composition changes in Arabidopsis thaliana are related to rutin stress. Journal of Plant Physiology 171:1325-1333.

https://doi.org/10.1016/j.jplph.2014.05.009

Hwang SY, VanToai TT (1991). Abscisic acid induces anaerobiosis tolerance in corn. Plant Physiology 97:593-597.

https://doi.org/10.1104/pp.97.2.593

Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR (2017). Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Frontiers in Plant Science 8:475. https://doi.org/10.3389/fpls.2017.00475

Janicka-Russak M, Kabała K, Wdowikowska A, Kłobus G (2013). Modification of plasma membrane proton pumps in cucumber roots as an adaptation mechanism to salt stress. Journal of Plant Physiology 170(10):915-922.

https://doi.org/10.1016/j.jplph.2013.02.002

Julkowska MM, Testerink C (2015). Tuning plant signaling and growth to survive salt. Trends in Plant Science 20:586-594. https://doi.org/10.1016/j.tplants.2015.06.008

Islam S, Hagimine T, Ishikawa K, Takeda N, Azad MAK, Miyauchi K (2010). Growth and fruit quality responses of hydroponically cultivated eggplants to mineral controlled deep-sea water. Journal of Plant Nutrition 33:1970-1979. https://doi.org/10.1080/01904167.2010.512055

Jung SJ, Joo EJ (2006). Effect of the supply of natural water from deep sea rock on the immune response and antioxidant activity in rats. Journal of Animal Science 48:211-215. https://doi.org/10.5187/JAST.2006.48.2.211

Kang SM, Jhoo J W, Pak JI, Kwon IK, Lee SK, Kim GY (2015). Effect of yogurt containing deep sea water on health-related serum parameters and intestinal microbiota in mice. Journal of Dairy Science 98(9):5967-5973. https://doi.org/10.3168/jds.2015-9492

Kim CY, Liu Y, Thorne ET, Yang H, Fukushige H, Gassmann W, … Zhang S (2003). Activation of a stress-responsive mitogen activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15:2707-2718.

https://doi.org/10.1105/tpc.011411

Krishnan S, Emily B, Merewitz B (2015). Phytohormone responses and cell viability during salinity stress in two creeping Bent grass cultivars differing in salt tolerance. Journal of American Society of Horticultural Science 140:346-355.

https://doi.org/10.21273/JASHS.140.4.346

Kosugi H, Kikugawa K (1985). Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. Lipids 20:915-920. https://doi.org/10.1007/BF02534777

Kou X, Watkins CB, Gan SS (2012). Arabidopsis AtNAP regulates fruit senescence. Journal of Experimental Botany 63:6139-6147. https://doi.org/10.1093/jxb/ers266

Lin KH, Chiou YK, Hwang SY, Chen LFO, Lo HF (2008). Calcium chloride enhances the antioxidative system of sweet potato (Ipomoea batatas) under flooding stress. Annals of Applied Biology 152:157-168. https://doi.org/10.1111/j.1744-7348.2007.00211.x

Lin KH, Seib SC, Su YH, Chiang CM (2019). Overexpression of the Arabidopsis and winter squash superoxide dismutase genes enhances chilling tolerance via ABA-sensitive transcriptional regulation in transgenic Arabidopsis. Plant Signaling & Behavior 14(12):1685728. https://doi.org/10.1080/15592324.2019.1685728

Lin KH, Pu SF (2010). Tissue- and genotype-specific ascorbate peroxidase expression in sweet potato in response to salt stress. Biologia Plantarum 54:664-670. https://doi.org/10.1007/s10535-010-0118-8

Linkies A, Müller K, Morris K, Turečková V, Wenk M, Cadman CS, Leubner-Metzger G (2009). Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803-3822. https://doi.org/10.1105/tpc.109.070201

Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta DeltaC(T)) method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262

Lyzenga WJ, Judith KB, Stone SL (2012). The Arabidopsis RING-type E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane-1-carboxylate synthase 7. The Plant Journal 71:23-34. https://doi.org/10.1111/j.1365-313X.2012.04965.x

Maathuis FJM (2006). The role of monovalent cation transporters in plant responses to salinity. Journal of Experimental Botany 57:1137-1147. https://doi.org/10.1093/jxb/erj001

Millero FJ, Feistel R, Wright DG, McDougall TJ (2008). The composition of standard seawater and the definition of the reference-composition salinity scale. Deep Sea Research Part I: Oceanographic Research Papers 55(1):50-72.

https://doi.org/10.1016/j.dsr.2007.10.001

Munns R (2002). Comparative physiology of salt and water stress. Plant, Cell and Environment 25:239-250.

https://doi.org/10.1046/j.0016-8025.2001.00808.x

Nakagawa K, Yokoyama Y, Nakajima H, Ikegami Y (2000). Application of minerals in deep sea water. JADOWA Deep Ocean Water Research 1:1-4. https://doi.org/10.1016/0146-6291(78)90619-7

Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology 22:67-880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

Nani M, Zura S, Majid FAA, Jaafar AB, Mahdzir A, Musa MN (2016). Potential health benefits of deep-sea water: a review. Evidence-Based Complementary and Alternative Medicine https://doi.org/10.1155/2016/6520475

Nguyen HC, Lin KH, Ho SL, Chiang CM, Yang CM (2018). Enhancing the abiotic stress tolerance of plants: from chemical treatment to biotechnological approaches. Physiologia Plantarum 164:452-466.

https://doi.org/10.1111/ppl.12812

Niu Y, Chen P, Zhang Y, Wang Z, Hu S, Jin G, Tang C, Guo L (2018). Natural variation among Arabidopsis thaliana accessions in tolerance to high magnesium supply. Scientific Report 8:13640.

https://doi.org/10.1038/s41598-018-31950-0

Parida AK, Das AB (2005). Salt tolerance and salinity effects on plants: A review. Ecotoxicology and Environmental Safety 60:324-349. https://doi.org/10.1016/j.ecoenv.2004.06.010

Peng J, Li Z, Wen X, Li W, Shi H, Yang L (2014). Salt-induced stabilization of EIN3/EIL1 confers salinity tolerance by deterring ROS accumulation in Arabidopsis. PLoS Genetics 10:e1004664.

https://doi.org/10.1371/journal.pgen.1004664

Pérez-López U, Miranda-Apodaca J, Muñoz-Rueda A, Mena-Petite A (2013). Lettuce production and antioxidant capacity are differentially modified by salt stress and light intensity under ambient and elevated CO2. Journal of Plant Physiology 170(17):1517-1525. https://doi.org/10.1016/j.jplph.2013.06.004

Robatzek S, Somssich IE (2002). Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genetic Development 16:1139-1149. https://doi.org/10.1101/gad.222702

Sakamoto K, Kogi M, Yanagisawa T (2014). Effects of salinity and nutrients in seawater on hydroponic culture of red leaf lettuce. Environmental Control in Biology 52:189-195. https://doi.org/10.2525/ecb.52.189

Saito T, Fukuda N, Matsukura C, Nishimura S (2009). Effects of salinity on distribution of photosynthates and carbohydrate metabolism in tomato grown using nutrient film technique. Journal of Japanese Society of Horticultural Sciences 78:90-96. https://doi.org/10.2503/jjshs1.78.90

Sekeli R, Abdullah JO, Namasivayam P, Muda P, Bakar UK, Yeong WC, Pillai V (2014). RNA interference of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO1 and ACO2) genes expression prolongs the shelf life of eksotika (Carica papaya L.) papaya fruit. Molecules 19:8350-8362. https://doi.org/10.3390/molecules19068350

Shafi A, Dogra V, Gill T, Ahuja PS, Sreenivasulu Y (2014). Simultaneous over-expression of PaSOD and RaAPX in transgenic Arabidopsis thaliana confers cold stress tolerance through increase in vascular lignification. PLos ONE 9: e110302. https://doi.org/10.1371/journal.pone.0110302

Shimada K, Fujikawa K, Yahara K, Nakamura T (1992). Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion. Journal of Agriculture Food Chemistry 40:945-948. https://doi.org/10.1021/jf00018a005

Shiraishi H, Fujino M, Shirakawa N, Ishida N, Funato H, Hirata A, … Miyamura M (2017). Effect of minerals on intestinal IgA production using deep sea water drinks. Biological and Pharmaceutical Bulletin 40(10):1700-1705.

https://doi.org/10.1021/jf00018a005

Sohrin Y, Iwamoto SI, Akiyama S, Fujita T, Kugii T, Obata H, Matsui M (1998). Determination of trace elements in seawater by fluorinated metal alkoxide glass-immobilized 8-hydroxyquinoline concentration and high-resolution inductively coupled plasma mass spectrometry detection. Analytica Chimica Acta 363(1):11-19.

https://doi.org/10.1016/S0003-2670(98)00074-9

Sun G, Mei Y, Deng D, Xiong L, Sun L, Zhang X, … Wang NN (2017). N-t erminus-mediated degradation of ACS7 is negatively regulated by senescence signaling to allow optimal ethylene production during leaf development in Arabidopsis. Frontiers in Plant Science 8:2066. https://doi.org/10.3389/fpls.2017.02066

Tenhaken R (2014). Cell wall remodeling under abiotic stress. Frontiers in Plant Science 5:771. https://doi.org/10.3389/fpls.2014.00771

Turhan A, Kuscu H, Ozmen, N, Serbeci MS, Demir AO (2014). Effect of different concentrations of diluted seawater on yield and quality of lettuce. Chilean Journal of Agriculture Research 74:111-116.

https://doi.org/10.4067/S0718-58392014000100017

Wen CK, Tucker M (2015). Research tool: ethylene preparation: treatment with ethylene and its replacements. In: Ethylene in Plants. Springer, Dordrecht pp 245-261. https://doi.org/10.1007/978-94-017-9484-8_1

.Xie WJ, Chen YS, Wu HV, Pan SF, Lin KH, Chiang CM (2020). Analysis the cell viability activity and antioxidant ability of pakchoi and tomato by deep ocean water. Ming Chung-Transaction in Biotechnology 11:e1.

https://doi.org/10.1201/9781439843390-c6

Yang SF, Hoffman NE (1984). Ethylene biosynthesis and its regulation in higher plants. Annual Review of Plant Physiology 35:155-189. https://doi.org/10.1146/annurev.pp.35.060184.001103

Yamada H, Takimoto S, Toshinari D, Kataoka K, Habu T (2015). Effect of seawater irrigation on water relations and fruit quality in potted citrus trees. Horticulture Journal 84:195-201. https://doi.org/10.2503/hortj.MI-022

Yudi C, Takahisa M, Suhardiyanto, H, Susila AD (2007). Application of deep-sea water for nutrient supplement in hydroponics cultivation of tomato: Effect of supplemented DSW at different EC levels on fruit properties. Indonesian Journal of Agronomy 35:118-126. https://doi.org/10.17660/ActaHortic.2007.761.61

Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C, … Pei ZM (2014). OSCA1 mediates osmotic- stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514(7522):367-371. https://doi.org/10.1038/nature13593

Zhang Z, Gan SS (2012). An abscisic acid- AtNAP transcription factor- SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiology 158:961-969.

https://doi.org/10.1104/pp.111.190876

Zhang Y, Yang L, Chen G, Ren D, Guo L (2018). Sensing of abiotic stress and ionic stress responses in plants. International Journal of Molecular Science 19:3298. https://doi.org/10.1002/9781118764374.ch8

Published
2021-02-10
How to Cite
LIN, K.-H., HUANG, M.-Y., XIE, W.-J., PAN, S.-F., CHEN, Y.-S., WU, H.-C., LIN, H.-H., & CHIANG, C.-M. (2021). Influences of sea water on the ethylene-biosynthesis, senescence-associated gene expressions, and antioxidant characteristics of Arabidopsis plants. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(1), 12205. https://doi.org/10.15835/nbha49112205
Section
Research Articles
CITATION
DOI: 10.15835/nbha49112205