Abstract
Malonyl-CoA synthetases may modulate cell responses to abiotic stress by regulating stress-related signaling transduction pathways or activating expression of transcription factors. However, the molecular mechanism of cold stress tolerance enhanced by malonyl-CoA synthetase is not fully understood. Here, we report that overexpression of the Arabidopsis thaliana malonyl-CoA synthetase gene AAE13.1 resulted in increased cell viability and growth rate and decreased thiobarbituric acid reactive substances under cold stress in rice (Oryza sativa L.), tobacco (Nicotiana tabacum), and slash pine (Pinus elliottii Engelm.). AAE13.1 was associated with cold stress tolerance by increasing the activity of ascorbate peroxidase, catalase, polyphenol oxidase, and peroxidase and the accumulation of acid phosphatase and alkaline phosphatase. Among six rice mitogen-activated protein kinase (MAPK) genes examined, AAE13.1 overexpression increased the expression of OsMAPK genes during cold stress. AAE13.1 activated expression of stress-response genes OsMAPK1, OsMAPK2, and OsMAPK3, indicating that AAE13.1 enhances cold stress tolerance by regulating expression of MAPK genes in plant cells. These results increase our understanding of cold stress tolerance in species of monocotyledons, dicotyledons, and gymnosperms.
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Ahmed KZ, Sagi F (1993) Culture of and fertile plant regeneration from regenerable embryogenic suspension cell-derived protoplasts of wheat (Triticum aestivum L.). Plant Cell Rep 12:175–179
Arora P, Bhardwaj R, Kumar Kanwar M (2010) 24-Epibrassinolide induced antioxidative defense system of Brassica juncea L. under Zn metal stress. Physiol Mol Biol Plants 16:285–293
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
Chen GJ, Liu HP, Wei Q, Zhao HN, Liu JX, Yu YX (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
Correa-Aragunde N, Foresi N, Lamattina L (2015) Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. J Exp Bot 66:2913–2921
de Buanafina MMO, Iyer PR, Buanafina MF, Shearer EA (2017) Reducing cell wall feruloylation by expression of a fungal ferulic acid esterase in Festuca arundinacea modifies plant growth, leaf morphology and the turnover of cell wall arabinoxylans. PLoS ONE 12:e0185312
Deng X, Bashandy H, Ainasoja M, Kontturi J, Pietiainen M, Laitinen RA, Albert VA, Valkonen JP, Elomaa P, Teeri TH (2014) Functional diversification of duplicated chalcone synthase genes in anthocyanin biosynthesis of Gerbera hybrida. New Phytol 201:1469–1483
Dirks-Hofmeister ME, Kolkenbrock S, Moerschbacher BM (2013) Parameters that enhance the bacterial expression of active plant polyphenol oxidases. PLoS ONE 8:e77291
Erukainure OL, Mopuri R, Oyebode OA, Koorbanally NA, Islam MS (2017) Dacryodes edulis enhances antioxidant activities, suppresses DNA fragmentation in oxidative pancreatic and hepatic injuries; and inhibits carbohydrate digestive enzymes linked to type 2 diabetes. Biomed Pharmacother 96:37–47
Evers D, Legay S, Lamoureux D, Hausman JF, Hoffmann L, Renaut J (2012) Towards a synthetic view of potato cold and salt stress response by transcriptomic and proteomic analyses. Plant Mol Biol 78:503–514
Faltin Z, Holland D, Velcheva M, Tsapovetsky M, Roeckel-Drevet P, Handa AK, Abu-Abied M, Friedman-Einat M, Eshdat Y, Perl A (2010) Glutathione peroxidase regulation of reactive oxygen species level is crucial for in vitro plant differentiation. Plant Cell Physiol 51:1151–1162
Gapper NE, Hertog M, Lee J, Buchanan DA, Leisso RS, Fei ZJ, Qu GQ, Giovannoni JJ, Johnston JW, Schaffer RJ, Nicolai BM, Mattheis JP, Watkins CB, Rudell DR (2017) Delayed response to cold stress is characterized by successive metabolic shifts culminating in apple fruit peel necrosis. BMC Plant Biol 17:77
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
Gzyl J, Rymer K, Gwozdz EA (2009) Differential response of antioxidant enzymes to cadmium stress in tolerant and sensitive cell line of cucumber (Cucumis sativus L.). Acta Biochim Polonica 56:723–727
Herranz R, Medina FJ (2014) Cell proliferation and plant development under novel altered gravity environments. Plant Biol 16(Suppl 1):23–30
Johnson KL, Ramm S, Kappel C, Ward S, Leyser O, Sakamoto T, Kurata T, Bevan MW, Lenhard M (2015) The Tinkerbell (Tink) mutation identifies the dual-specificity MAPK phosphatase INDOLE-3-BUTYRIC ACID-RESPONSE5 (IBR5) as a novel regulator of organ size in Arabidopsis. PLoS ONE 10:e0131103
Jung JH, Park JH, Lee S, To TK, Kim JM, Seki M, Park CM (2013) The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 25:4378–4390
Kaida R, Satoh Y, Bulone V, Yamada Y, Kaku T, Hayashi T, Kaneko TS (2009) Activation of beta-glucan synthases by wall-bound purple acid phosphatase in tobacco cells. Plant Physiol 150:1822–1830
Kampatsikas I, Bijelic A, Pretzler M, Rompel A (2017) Three recombinantly expressed apple tyrosinases suggest the amino acids responsible for mono- versus diphenolase activity in plant polyphenol oxidases. Sci Rep 7:8860
Kim HS, Oh JM, Luan S, Carlson JE, Ahn SJ (2013) Cold stress causes rapid but differential changes in properties of plasma membrane H+-ATPase of camelina and rapeseed. J Plant Physiol 170:828–837
Kuijpers TF, van Herk T, Vincken JP, Janssen RH, Narh DL, van Berkel WJ, Gruppen H (2014) Potato and mushroom polyphenol oxidase activities are differently modulated by natural plant extracts. J Agric Food Chem 62:214–221
Lee DJ, Choi HJ, Moon ME, Chi YT, Ji KY, Choi D (2017) Superoxide serves as a putative signal molecule for plant cell division: overexpression of CaRLK1 promotes the plant cell cycle via accumulation of O2(−) and decrease in H2O2. Physiol Plant 159:228–243
Leyva A, Hernandez N, Gonzalez T, Sanchez JC, Franco A, Delgado I, Montanez M, Valdes R (2004) Standardization and validation of an alkaline phosphatase-linked immunoassay to quantify a plant-derived antibody directed against the hepatitis B virus surface antigen. Biochem Biophys Res Commun 325:1438–1442
Ma HR, Wei HB, Chen Z et al (2013) The estrogenic activity of isoflavones extracted from chickpea Cicer arietinum L sprouts in vitro. Phytother Res 27:1237–1242
Majda M, Grones P, Sintorn IM, Vain T, Milani P, Krupinski P, Zagorska-Marek B, Viotti C, Jonsson H, Mellerowicz EJ, Hamant O, Robert S (2017) Mechanochemical polarization of contiguous cell walls shapes plant pavement cells. Develop Cell 43(290–304):e294
Malik CP, Sethi RS (1975) Histochemical studies in stomatal apparatus of Phaseolus mungo linn. IV. Mechanism of stomatal action. Acta Histochem 53:1–11
Matia I, Gonzalez-Camacho F, Herranz R, Kiss JZ, Gasset G, van Loon JJ, Marco R, Javier Medina F (2010) Plant cell proliferation and growth are altered by microgravity conditions in spaceflight. J Plant Physiol 167:184–193
Matos AR, Hourton-Cabassa C, Cicek D, Reze N, Arrabaca JD, Zachowski A, Moreau F (2007) Alternative oxidase involvement in cold stress response of Arabidopsis thaliana fad2 and FAD3 + cell suspensions altered in membrane lipid composition. Plant Cell Physiol 48:856–865
Molitor C, Mauracher SG, Rompel A (2016) Aurone synthase is a catechol oxidase with hydroxylase activity and provides insights into the mechanism of plant polyphenol oxidases. Proc Natl Acad Sci USA 113:E1806–E1815
Murota K, Shimura H, Takeshita M, Masuta C (2017) Interaction between Cucumber mosaic virus 2b protein and plant catalase induces a specific necrosis in association with proteasome activity. Plant Cell Rep 36:37–47
Nautiyal CS, Govindarajan R, Lavania M, Pushpangadan P (2008) Novel mechanism of modulating natural antioxidants in functional foods: involvement of plant growth promoting Rhizobacteria NRRL B-30488. J Agric Food Chem 56:4474–4481
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
Pasquali G, Biricolti S, Locatelli F, Baldoni E, Mattana M (2008) Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep 27:1677–1686
Poiatti VA, Dalmas FR, Astarita LV (2009) Defense mechanisms of Solanum tuberosum L. in response to attack by plant-pathogenic bacteria. Biol Res 42:205–215
Ray M, Mishra P, Das P, Sabat SC (2012) Expression and purification of soluble bio-active rice plant catalase-A from recombinant Escherichia coli. J Biotechnol 157:12–19
Sakthivel KM, Guruvayoorappan C (2013) Acacia ferruginea inhibits tumor progression by regulating inflammatory mediators-(TNF-a, iNOS, COX-2, IL-1beta, IL-6, IFN-gamma, IL-2, GM-CSF) and pro-angiogenic growth factor- VEGF. Asian Pac J Cancer Prevent 14:3909–3919
Sang MK, Kim KD (2011) Biocontrol activity and primed systemic resistance by compost water extracts against anthracnoses of pepper and cucumber. Phytopathol 101:732–740
Selin-Rani S, Senthil-Nathan S, Revathi K, Chandrasekaran R, Thanigaivel A, Vasantha-Srinivasan P, Ponsankar A, Edwin ES, Pradeepa V (2016) Toxicity of Alangium salvifolium Wang chemical constituents against the tobacco cutworm Spodoptera litura Fab. Pesticide Biochem Physiol 126:92–101
Sessions A (2008) Immunohistochemistry on sections of plant tissues using alkaline-phosphatase-coupled secondary antibody. CSH Protoc 2008:pdb prot4946
Shahryar N, Maali-Amiri R (2016) Metabolic acclimation of tetraploid and hexaploid wheats by cold stress-induced carbohydrate accumulation. J Plant Physiol 204:44–53
Sineshchekov V, Koppel L, Shor E, Kochetova G, Galland P, Zeidler M (2013) Protein phosphatase activity and acidic/alkaline balance as factors regulating the state of phytochrome A and its two native pools in the plant cell. Photochem Photobiol 89:83–96
Singh S, Braus-Stromeyer SA, Timpner C, Valerius O, von Tiedemann A, Karlovsky P, Druebert C, Polle A, Braus GH (2012) The plant host Brassica napus induces in the pathogen Verticillium longisporum the expression of functional catalase peroxidase which is required for the late phase of disease. Mol Plant Microbe Interact 25:569–581
Sirhindi G, Mir MA, Sharma P, Gill SS, Kaur H, Mushtaq R (2015) Modulatory role of jasmonic acid on photosynthetic pigments, antioxidants and stress markers of Glycine max L. under nickel stress. Physiol Mol Biol Plants 21:559–565
Spanou CI, Veskoukis AS, Stagos D, Liadaki K, Aligiannis N, Angelis A, Skaltsounis AL, Anastasiadi M, Haroutounian SA, Kouretas D (2012) Effects of Greek legume plant extracts on xanthine oxidase, catalase and superoxide dismutase activities. J Physiol Biochem 68:37–45
Steward N, Martin R, Engasser JM, Goergen JL (1999) Determination of growth and lysis kinetics in plant cell suspension cultures from the measurement of esterase release. Biotechnol Bioengineer 66:114–121
Tamirisa S, Vudem DR, Khareedu VR (2014) Overexpression of pigeonpea stress-induced cold and drought regulatory gene (CcCDR) confers drought, salt, and cold tolerance in Arabidopsis. J Exp Bot 65:4769–4781
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
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
Tang W, Peng XX, 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
Tang W, Newton RJ, Lin J, Charles TM (2006) Expression of a transcription factor from Capsicum annuum in pine calli counteracts the inhibitory effects of salt stress on adventitious shoot formation. Mol Genet Genom 276:242–253
Tang W, Newton RJ, Li C, Charles TM (2007a) Enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis. Plant Cell Rep 26:115–124
Tang W, Newton RJ, Weidner DA (2007b) Genetic transformation and gene silencing mediated by multiple copies of a transgene in eastern white pine. J Exp Bot 58:545–554
Vashisht AA, Pradhan A, Tuteja R, Tuteja N (2005) Cold- and salinity stress-induced bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. Plant J 44:76–87
Wagstaff C, Bramke I, Breeze E, Thornber S, Harrison E, Thomas B, Buchanan-Wollaston V, Stead T, Rogers H (2010) A specific group of genes respond to cold dehydration stress in cut Alstroemeria flowers whereas ambient dehydration stress accelerates developmental senescence expression patterns. J Exp Bot 61:2905–2921
Wan BL, Lin YJ, Mou TM (2007) Expression of rice Ca2+-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Lett 581:1179–1189
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
Widyowati R, Tezuka Y, Miyahara T, Awale S, Kadota S (2010) Alkaline phosphatase (ALP) enhancing iridoid glucosides from the Indonesian medicinal plant Barleria lupulina. Nat Product Commun 5:1711–1716
Yan Y, Peng L, Liu WX, Wan FH, Harris MK (2011) Host plant effects on alkaline phosphatase activity in the whiteflies, Bemisia tabaci Biotype B and Trialeurodes vaporariorum. J Insect Sci 11:9
Yang Z, Mhamdi A, Noctor G (2018) Analysis of catalase mutants underscores the essential role of CATALASE2 for plant growth and day length-dependent oxidative signalling. Plant Cell Environ 42:688–700
Yoshida K, Kaothien P, Matsui T, Kawaoka A, Shinmyo A (2003) Molecular biology and application of plant peroxidase genes. Appl Microbiol Biotechnol 60:665–670
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
Zou Y, Aboshora W, Li J, Xiao TC, Zhang LF (2017) Protective effects of Lepidium meyenii (Maca) Aqueous extract and lycopene on Testosterone Propionate-induced prostatic hyperplasia in mice. Phytother Res 31:1192–1198
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The authors are grateful to Dr. T. Bradshaw, Dr. R. Lischewski, and Dr. D. Thompson for their critical reading and suggestions during the preparation of this manuscript.
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Tang, W., Tang, A.Y. Overexpression of Arabidopsis thaliana malonyl-CoA synthetase gene enhances cold stress tolerance by activating mitogen-activated protein kinases in plant cells. J. For. Res. 32, 741–753 (2021). https://doi.org/10.1007/s11676-020-01140-8
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DOI: https://doi.org/10.1007/s11676-020-01140-8