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The Arabidopsis AtAAE13.1 Gene Enhances Salt Stress Tolerance in Angiosperms and Gymnosperm Plant Cells

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Abstract

The Arabidopsis malonyl-CoA synthetase gene AAE13.1 (AtAAE13.1) plays important roles in cell metabolism, plant growth and development, and environmental stress responses. However, function of AtAAE13.1 in NaCl stress tolerance is not determined yet. Cell suspension cultures of different plant species including rice (Oryza sativa L.), cotton (Gossypium hirsutum L.), and white pine (Pinus strobus L.) were transformed using Agrobacterium tumefaciens strain GV3101 harboring pBI-AtAAE13.1. After confirmation of integration of the AtAAE13.1 gene into the genome by polymerase chain reaction (PCR), Southern and northern blot analyses, NaCl stress tolerance was examined in AtAAE13.1 transgenic cells of O. sativa, G. hirsutum, and P. strobus. AtAAE13.1 expression enhanced NaCl stress tolerance by increasing cell viability and growth rate, decreasing lipid peroxidation, increasing the oxidation rate, and elevating the content of amino acids, glycolate, and phosphoglycolate, as well as elevating the amount of sucrose, glucose, and fructose. In rice cells, AtAAE13.1 elevated expression of the Ca2+-dependent protein kinase (CPK) genes under NaCl stress. Overexpression of the AtAAE13.1 gene may be useful for engineering NaCl stress tolerance in different plant species.

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References

  • Ahmad R, Kim MD, Back KH, Kim HS, Lee HS, Kwon SY, Murata N, Chung WI, Kwak SS (2008) Stress-induced expression of choline oxidase in potato plant chloroplasts confers enhanced tolerance to oxidative, salt, and drought stresses. Plant Cell Rep 27:687–698

    CAS  PubMed  Google Scholar 

  • Arimura G, Sawasaki T (2010) Arabidopsis CPK3 plays extensive roles in various biological and environmental responses. Plant Signal Behav 5:1263–1265

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ashraf M, Ahmad S (2000) Influence of sodium chloride onion accumulation, yield components and fiber characteristics in salt-tolerant and salt sensitive lines of cotton (Gossypium hirsutum L.). Field Crop Res 66:115–127

    Google Scholar 

  • Bang VMJ, Aranao ALC, Nogueira BZ, Araujo AC, Bueno P, Barbalho SM, de Souza M, Guiguer EL (2019) Effects of Rhodiola rosea and Panax ginseng on the metabolic parameters of rats submitted to swimming. J Med Food 22:1–9

    Google Scholar 

  • Barajas-Lopez JD, Moreno JR, Gamez-Arjona FM, Pardo JM, Punkkinen M, Zhu JK, Quintero FJ, Fujii H (2018) Upstream kinases of plant SnRKs are involved in salt stress tolerance. Plant J 93:107–118

    CAS  PubMed  Google Scholar 

  • Barnawal D, Bharti N, Pandey SS, Pandey A, Chanotiya CS, Kalra A (2017) Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol Plant 161:502–514

    CAS  PubMed  Google Scholar 

  • Beckerman J, Lerner BR (2009) Salt damage in landscape plants. Purdue Extension Factsheet ID-412-W:1–11

  • Bertolacci R, Meza G, Sandell S (2018) Impact of pine allelopathy on seed germination. Purch Coll J Ecol 2:35–41

    Google Scholar 

  • Bhattacharjee S (2014) Membrane lipid peroxidation and its conflict of interest: the two faces of oxidative stress. Curr Sci 107:1811–1823

    CAS  Google Scholar 

  • Campos-Soriano L, Gomez-Ariza J, Bonfante P, San Segundo B (2011) A rice calcium-dependent protein kinase is expressed in cortical root cells during the presymbiotic phase of the arbuscular mycorrhizal symbiosis. BMC Plant Biol 11:90

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Yang M, Ma W, Sun Y, Chen G (2018) Overexpression of SSBXoc, a single-stranded DNA-binding protein from Xanthomonas oryzae pv. oryzicola, enhances plant growth and disease and salt stress tolerance in transgenic Nicotiana benthamiana. Front Plant Sci 9:953–965

    PubMed  PubMed Central  Google Scholar 

  • Chen H, Kim HU, Weng H, Browse J (2011) Malonyl-CoA synthetase, encoded by acyl activating enzyme13, is essential for growth and development of Arabidopsis. Plant Cell 23:2247–2262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen G, Liu H, Wei Q, Zhao H, Liu J, Yu Y (2017) The acyl-activating enzyme PhAAE13 is an alternative enzymatic source of precursors for anthocyanin biosynthesis in petunia flowers. J Exp Bot 68:457–467

    CAS  PubMed  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2006) Salt stress signaling and mechanisms of plant salt tolerance. Genet Eng 27:141–177

    CAS  Google Scholar 

  • Davey JF, Ersser RS (1990) Amino acid analysis of physiological fluids by highperformance liquid chromatography with phenylisothiocyanate derivatization and comparison with ion-exchange chromatography. J Chromatogr 8:9–23

  • Foyer CH, Bloom AJ, Queval G, Noctor G (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60:455–484

  • Gao W, Xu FC, Guo DD, Zhao JR, Liu J, Guo YW, Singh PK, Ma XN, Long L, Botella JR, Song CP (2018) Calcium-dependent protein kinases in cotton: insights into early plant responses to salt stress. BMC Plant Biol 18:15–26

    PubMed  PubMed Central  Google Scholar 

  • Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KA, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci U S A 107:8023–8028

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geng S, Li A, Tang L, Yin L, Wu L, Lei C, Guo X, Zhang X, Jiang G, Zhai W, Wei Y, Zheng Y, Lan X, Mao L (2013) TaCPK2-A, a calcium-dependent protein kinase gene that is required for wheat powdery mildew resistance enhances bacterial blight resistance in transgenic rice. J Exp Bot 64:3125–3136

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghassemi F, Jakeman AJ, Nix HA (1995) Salinisation of land and water resources: human causes, extent, management and case studies. Sydney, Australia, and CAB international. UNSW Press, Wallingford

    Google Scholar 

  • Guan X, Nikolau BJ (2016) AAE13 encodes a dual-localized malonyl-CoA synthetase that is crucial for mitochondrial fatty acid biosynthesis. Plant J 85:581–593

    CAS  PubMed  Google Scholar 

  • Gupta PK, Durzan DJ (1985) Shoot multiplication from mature Douglas fir and sugar pine. Plant Cell Rep 4:177–179

    CAS  PubMed  Google Scholar 

  • Higbie SM, Wang F, Stewart JM, Sterling TM, Lindemann WC, Hughs E, Zhang J (2010) Physiological response to salt (NaCl) stress in selected cultivated tetraploid cottons. Int J Agron 1:1–12

    Google Scholar 

  • Holmes RP (1995) Measurement of urinary oxalate and citrate by capillary electrophoresis and indirect ultraviolet absorbance. Clinical Chem 41:1297–1301

  • Hu W, Xia Z, Yan Y, Ding Z, Tie W, Wang L, Zou M, Wei Y, Lu C, Hou X, Wang W, Peng M (2015) Genome-wide gene phylogeny of CIPK family in cassava and expression analysis of partial drought-induced genes. Front Plant Sci 6:914–925

    PubMed  PubMed Central  Google Scholar 

  • Hussain S, Bai Z, Huang J, Cao X, Zhu L, Zhu C et al (2019) 1-Methylcyclopropene modulates physiological, biochemical, and antioxidant responses of rice to different salt stress levels. Front Plant Sci 10:124–136

    PubMed  PubMed Central  Google Scholar 

  • James RA, Blake C, Byrt CS, Munns R (2011) Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5), decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. J Exp Bot 62:2939–2947

    CAS  PubMed  Google Scholar 

  • Kanchiswamy CN, Mohanta TK, Capuzzo A, Occhipinti A, Verrillo F, Maffei ME, Malnoy M (2013) Differential expression of CPKs and cytosolic Ca2+ variation in resistant and susceptible apple cultivars (Malus x domestica) in response to the pathogen Erwinia amylovora and mechanical wounding. BMC Genomics 14:760–772

    PubMed  PubMed Central  Google Scholar 

  • Kim JY, Kwak KJ, Jung HJ, Lee HJ, Kang H (2010) MicroRNA402 affects seed germination of Arabidopsis thaliana under stress conditions via targeting DEMETER-LIKE Protein3 mRNA. Plant Cell Physiol 51:1079–1083

    CAS  PubMed  Google Scholar 

  • Knight ZA, Tan K, Birsoy K, Schmidt S, Garrison JL, Wysocki RW, Emiliano A, Ekstrand MI, Friedman JM (2012) Molecular profiling of activated neurons by phosphorylated ribosome capture. Cell 151:11226–1137

  • Kontturi J, Osama R, Deng X, Bashandy H, Albert VA, Teeri TH (2017) Functional characterization and expression of GASCL1 and GASCL2, two anther-specific chalcone synthase like enzymes from Gerbera hybrida. Phytochemistry 134:38–45

    CAS  PubMed  Google Scholar 

  • Kumar V, Khare T, Shriram V, Wani SH (2018) Plant small RNAs: the essential epigenetic regulators of gene expression for salt-stress responses and tolerance. Plant Cell Rep 37:61–75

    CAS  PubMed  Google Scholar 

  • Li H, Liang J, Chen H, Ding G, Ma B, He N (2016) Evolutionary and functional analysis of mulberry type III polyketide synthases. BMC Genomics 17:540–553

    PubMed  PubMed Central  Google Scholar 

  • Li Z, Takahashi Y, Scavo A, Brandt B, Nguyen D, Rieu P, Schroeder JI (2018) Abscisic acid-induced degradation of Arabidopsis guanine nucleotide exchange factor requires calcium-dependent protein kinases. Proc Natl Acad Sci U S A 115:E4522–E4531

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Yang Y, Sun K, Chen Y, Chen X, Li X (2019) Exogenous melatonin enhances cold, salt and drought stress tolerance by improving antioxidant defense in tea plant (Camellia sinensis (L.) O. Kuntze). Molecules 24:1837–1847

    PubMed Central  Google Scholar 

  • Loka DM, Derrick M, Oosterhuis DM, Ritchie GL (2011) Water-deficit stress in cotton. In: Oosterhuis DM (ed) Number Seven the Cotton Foundation Book SeriesStress physiology in cotton. Natl Cotton Council Amer, Cordova, pp 37–72

    Google Scholar 

  • Ma NL, Che Lah WA, Abd Kadir N, Mustaqim M, Rahmat Z, Ahmad A et al (2018) Susceptibility and tolerance of rice crop to salt threat: physiological and metabolic inspections. PLoS One 13:192732–192743

    Google Scholar 

  • Mahjoubi H, Tamari Y, Takeda S, Bouchabke-Coussa O, Hanin M, Herzog E, Schmit AC, Chaboute ME, Ebel C (2018) The wheat TdRL1 is the functional homolog of the rice RSS1 and promotes plant salt stress tolerance. Plant Cell Rep 37:1625–1637

    CAS  PubMed  Google Scholar 

  • Maierhofer T, Diekmann M, Offenborn JN, Lind C, Bauer H, Hashimoto K, KA SA-R, Luan S, Kudla J, Geiger D, Hedrich R (2014) Site- and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Sci Signal 7:86–97

    Google Scholar 

  • Mannaerts GP, Debeer LJ, Thomas J, De Schepper PJ (1979) Mitochondrial and peroxisomal fatty acid oxidation in liver homogenates and isolated hepatocytes from control and clofibrate-treated rats. J Biol Chem 254:4585–4595

    CAS  PubMed  Google Scholar 

  • Mimouni H, Wasti S, Manaa A, Gharbi E, Chalh A, Vandoorne B, Lutts S, Ben Ahmed H (2016) Does salicylic acid (SA) improve tolerance to salt stress in plants? A study of SA effects on tomato plant growth, water dynamics, photosynthesis, and biochemical parameters. Omics 20:180–190

    CAS  PubMed  Google Scholar 

  • Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    CAS  PubMed  Google Scholar 

  • Park SR, Ahn MS, Han AR, Park JW, Yoon YJ (2011) Enhanced flavonoid production in Streptomyces venezuelae via metabolic engineering. J Microbiol Biotechnol 21:1143–1146

    CAS  PubMed  Google Scholar 

  • Park YC, Chapagain S, Jang CS (2018) A negative regulator in response to salinity in rice: Oryza sativa salt-, ABA- and drought-induced RING finger protein 1 (OsSADR1). Plant Cell Physiol 59:575–589

    CAS  PubMed  Google Scholar 

  • Qin T, Xiong L (2019) Subcellular localization and functions of plant lncRNAs in drought and salt stress tolerance. Methods Mol Biol 1933:173–186

    CAS  PubMed  Google Scholar 

  • Rady MM, Elrys AS, Abo El-Maati MF, Desoky EM (2019) Interplaying roles of silicon and proline effectively improve salt and cadmium stress tolerance in Phaseolus vulgaris plant. Plant Physiol Biochem 139:558–568

    CAS  PubMed  Google Scholar 

  • Rajbanshi SL, Pandanaboina CS (2014) Alcohol stress on cardiac tissue–ameliorative effects of Thespesia populnea leaf extract. J Cardiol 63:449–459

    PubMed  Google Scholar 

  • Ranty B, Aldon D, Cotelle V, Galaud JP, Thuleau P, Mazars C (2016) Calcium sensors as key hubs in plant responses to biotic and abiotic stresses. Front Plant Sci 7:327–338

    PubMed  PubMed Central  Google Scholar 

  • Sartore G, Burlina S, Ragazzi E, Ferraresso S, Valentini R, Lapolla A (2013) Mediterranean diet and red yeast rice supplementation for the management of hyperlipidemia in statin-intolerant patients with or without type 2 diabetes. Evid-Based Compl Altern Med 2013:743473

    Google Scholar 

  • Singh RP, Jha PN (2016) A halotolerant bacterium Bacillus licheniformis HSW-16 augments induced systemic tolerance to salt stress in wheat plant (Triticum aestivum). Front Plant Sci 7:1890–1899

    PubMed  PubMed Central  Google Scholar 

  • Siringam K, Juntawong N, Chaum S, Kirdmanee C (2011) Salt stress induced ion accumulation, ion homeostasis, membrane injury and sugar contents in salt-sensitive rice (Oryza sajtiva L. spp. indica) roots under isosmotic conditions. Afr J Biotech 10:1340–1346

    CAS  Google Scholar 

  • South PF, Cavanagh AP, Liu HW, Ort DR (2019) Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363:9077–9088

    Google Scholar 

  • Stein O, Granot D (2019) An overview of sucrose synthases in plants. Front Plant Sci 10:95–106

    PubMed  PubMed Central  Google Scholar 

  • Stitt M, Lilley RM, Gerhardt R, Heldt HW (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. In: Fleischer S, Fleischer B (eds) Methods in Enzymology: Biomembranes, Vol 174. Academic Press, Amsterdam, pp 518–552

  • Sun XL, Yu QY, Tang LL, Ji W, Bai X, Cai H, Liu XF, Ding XD, Zhu YM (2013) GsSRK, a G-type lectin S-receptor-like serine/threonine protein kinase, is a positive regulator of plant tolerance to salt stress. J Plant Physiol 170:505–515

    CAS  PubMed  Google Scholar 

  • Sytar O, Brestic M, Zivcak M, Olsovska K, Kovar M, Shao H, He X (2017) Applying hyperspectral imaging to explore natural plant diversity towards improving salt stress tolerance. Sci Total Environ 578:90–99

    CAS  PubMed  Google Scholar 

  • Tang W, Page M (2013) Transcription factor AtbZIP60 regulates expression of Ca2+−dependent protein kinase genes in transgenic cells. Mol Biol Rep 40:2723–2732

    CAS  PubMed  Google Scholar 

  • Tang W, Charles TM, Newton RJ (2005a) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus Virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617

    CAS  PubMed  Google Scholar 

  • Tang W, Peng X, Newton RJ (2005b) Enhanced tolerance to salt stress in transgenic loblolly pine simultaneously expressing two genes encoding mannitol-1-phosphate dehydrogenase and glucitol-6-phosphate dehydrogenase. Plant Physiol Biochem 43:139–146

    CAS  PubMed  Google Scholar 

  • Tang W, Newton RJ, Weidner DA (2007) Genetic transformation and gene silencing mediated by multiple copies of a transgene in eastern white pine. J Exp Bot 58:545–554

    CAS  PubMed  Google Scholar 

  • Tong X, Cao A, Wang F, Chen X, Xie S, Shen H, Jin X, Li H (2019) Calcium-dependent protein kinase genes in Glycyrrhiza Uralensis appear to be involved in promoting the biosynthesis of glycyrrhizic acid and flavonoids under salt stress. Molecules 24:1837–1848

    CAS  PubMed Central  Google Scholar 

  • Valmonte GR, Arthur K, Higgins CM, MacDiarmid RM (2014) Calcium-dependent protein kinases in plants: evolution, expression and function. Plant Cell Physiol 55:551–569

    CAS  PubMed  Google Scholar 

  • von Arnold S, Eriksson T (1979) Bud induction on isolated needles of Norway spruce (Picea abies L. Kast.) grown in vitro. Plant Sci Lett 15:363–372

    Google Scholar 

  • Wan B, Lin Y, Mou T (2007) Expression of rice Ca2+-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Lett 581:1179–1189

    CAS  PubMed  Google Scholar 

  • Wang C, Zhang LJ, Huang RD (2011) Cytoskeleton and plant salt stress tolerance. Plant Signal Behav 6:29–31

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Chen H, Yu O (2014) A plant malonyl-CoA synthetase enhances lipid content and polyketide yield in yeast cells. Appl Microbiol Biotechnol 98:5435–5447

    CAS  PubMed  Google Scholar 

  • Wei M, Wang S, Dong H, Cai B, Tao J (2016) Characterization and comparison of the CPK gene family in the apple (Malus x domestica) and other rosaceae species and its response to Alternaria alternata infection. PLoS One 11:155590–155599

    Google Scholar 

  • Weinberg JM, Bienholz A, Venkatachalam MA (2016) The role of glycine in regulated cell death. Cell Mol Life Sci 73:2285–2308

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada A, Sekiguchi M, Mimura T, Ozeki Y (2002) The role of plant CCTalpha in salt- and osmotic-stress tolerance. Plant Cell Physiol 43:1043–1048

    CAS  PubMed  Google Scholar 

  • Yang L, Ji W, Zhu Y, Gao P, Li Y, Cai H, Bai X, Guo D (2010) GsCBRLK, a calcium/calmodulin-binding receptor-like kinase, is a positive regulator of plant tolerance to salt and ABA stress. J Exp Bot 61:2519–2533

    CAS  PubMed  Google Scholar 

  • Yang W, Liu XD, Chi XJ, Wu CA, Li YZ, Song LL, Liu XM, Wang YF, Wang FW, Zhang C, Liu Y, Zong JM, Li HY (2011) Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233:219–229

    CAS  PubMed  Google Scholar 

  • Yu HN, Wang L, Sun B, Gao S, Cheng AX, Lou HX (2015) Functional characterization of a chalcone synthase from the liverwort Plagiochasma appendiculatum. Plant Cell Rep 34:233–245

    CAS  PubMed  Google Scholar 

  • Zhang H, Yang B, Liu WZ, Li H, Wang L, Wang B, Deng M, Liang W, Deyholos MK, Jiang YQ (2014) Identification and characterization of CBL and CIPK gene families in canola (Brassica napus L.). BMC Plant Biol 14:8–19

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou M, Tang W (2019) MicroRNA156 amplifies transcription factor-associated cold stress tolerance in plant cells. Mol Gen Genomics 294:379–393

    CAS  Google Scholar 

  • Zhu N, Cheng S, Liu X, Du H, Dai M, Zhou DX, Yang W, Zhao Y (2015) The R2R3-type MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance in rice. Plant Sci 236:146–156

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Prasad, Dr. Lischewski, and Dr. Page for their critical reading and suggestions during the preparation of this manuscript.

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Zhou, M., Thompson, W.A. & Tang, W. The Arabidopsis AtAAE13.1 Gene Enhances Salt Stress Tolerance in Angiosperms and Gymnosperm Plant Cells. In Vitro Cell.Dev.Biol.-Plant 56, 750–764 (2020). https://doi.org/10.1007/s11627-020-10083-y

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