Crosstalk among nitric oxide, calcium and reactive oxygen species during triterpenoid biosynthesis in Betula platyphylla
Fansuo Zeng A B , Kun Liu B , Sida Li B and Yaguang Zhan A B C
+ Author Affiliations
- Author Affiliations
A State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.
B College of Life Science, Northeast Forestry University, Harbin 150040, China.
C Corresponding author. Email: youpractise@126.com
Functional Plant Biology 42(7) 643-654 https://doi.org/10.1071/FP14352
Submitted: 14 December 2014 Accepted: 13 March 2015 Published: 10 April 2015
Abstract
We analysed NO, reactive oxygen species (ROS) and Ca2+ crosstalk during triterpenoid biosynthesis in white birch (Betula platyphylla Suk.) cells. Cells were pretreated with diphenyleneiodonium, sodium diethyldithiocarbamate (DDTC) or catalase (CAT), or a Ca2+ channel blocker or chelator before sodium nitroprusside treatment. Changes in triterpenoid, malondialdehyde and proline levels, cell viability, and CAT, ascorbate peroxidase and peroxidase activity were recorded. Furthermore, enzyme gene expression levels related to triterpene biosynthesis, endogenous signalling and antioxidase activity, and cell apoptosis and death rates were measured. Sodium nitroprusside elevated ROS and Ca2+ levels. Oleanolic acid levels in cells pretreated with diphenyleneiodonium and CAT reduced significantly, but it increased with DDTC pretreatment. ROS inhibition downregulated BpDXR, BpCALM and BpNIA expression. Oleanolic acid, BpMnSOD expression, and CAT, ascorbate peroxidase and peroxidase activities reduced when the Ca2+ signalling pathway was blocked. The apoptosis rates of cells pretreated with DDTC and CAT decreased significantly; cell death rates also reduced in groups Ca2+ pretreated with channel blocker and chelator . Thus ROS and Ca2+ participate in triterpenoid biosynthesis, cell apoptosis and death induced by exogenous NO application. Further, NO causes oxidative stress and restricts the level of intracellular ROS through the Ca2+ signalling pathway.
Additional keywords: apoptosis, Ca2+, cell death, enzymes, oxidative stress, white birch.
References
Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. Journal of Plant Biology 51, 167–173.| Reactive oxygen species, antioxidants and signaling in plants.Crossref | GoogleScholarGoogle Scholar |
Astier J, Besson-Bard A, Wawer I, Parent C, Rasul S, Jeandroz S, Dat JF, Wendehenne D (2010) Nitric oxide signalling in plants: cross-talk with Ca2+, protein kinases and reactive oxygen species. In ‘Annual Plant Reviews Volume 42: Nitrogen Metabolism in Plants in the Post-Genomic Era’. (Eds C. H. Foyer and H. Zhang) pp. 147–170. (Wiley-Blackwell: Oxford, UK)
Bai S, Li M, Yao T, Wang H, Zhang Y, Xiao L, Wang J, Zhang Z, Hu Y, Liu W, He Y (2012) Nitric oxide restrain root growth by DNA damage induced cell cycle arrest in Arabidopsis thaliana. Nitric Oxide 26, 54–60.
| Nitric oxide restrain root growth by DNA damage induced cell cycle arrest in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 22197746PubMed |
Bates LS, Waldron RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant and Soil 39, 205–207.
| Rapid determination of free proline for water stress studies.Crossref | GoogleScholarGoogle Scholar |
Catalá A (2009) Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chemistry and Physics of Lipids 157, 1–11.
| Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions.Crossref | GoogleScholarGoogle Scholar | 18977338PubMed |
Chappell J, Wolf F, Proulx J, Cuellar R, Saunders C (1995) Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase a rate-limiting step for isoprenoid biosynthesis in plants? Plant Physiology 109, 1337–1343.
Chintharlapalli S, Papineni S, Ramaiah SK, Safe S (2007) Betulinic acid inhibits prostate cancer growth through inhibition of specificity protein transcription factors. Cancer Research 67, 2816–2823.
| Betulinic acid inhibits prostate cancer growth through inhibition of specificity protein transcription factors.Crossref | GoogleScholarGoogle Scholar | 17363604PubMed |
Csuk R, Barthel A, Kluge R, Strohl D, Kommera H, Paschke R (2010) Synthesis and biological evaluation of antitumour-active betulin derivatives. Bioorganic & Medicinal Chemistry 18, 1344–1355.
| Synthesis and biological evaluation of antitumour-active betulin derivatives.Crossref | GoogleScholarGoogle Scholar |
Dat JF, Pellinen R, Beeckman T, Van De Cotte B, Langebartels C, Kangasjarvi J, Inze D, Van Breusegem F (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. The Plant Journal 33, 621–632.
| Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco.Crossref | GoogleScholarGoogle Scholar | 12609037PubMed |
Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585–588.
| Nitric oxide functions as a signal in plant disease resistance.Crossref | GoogleScholarGoogle Scholar | 9707120PubMed |
Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences of the United States of America 98, 13 454–13 459.
| Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response.Crossref | GoogleScholarGoogle Scholar |
Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany 32, 93–101.
| Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase.Crossref | GoogleScholarGoogle Scholar |
Dickerson DP, Pascholati SF, Hagerman AE, Butler LG, Nicholson RL (1984) Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiological Plant Pathology 25, 111–123.
| Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum.Crossref | GoogleScholarGoogle Scholar |
Du F, Shi H, Zhang X, Xu X (2014) Responses of reactive oxygen scavenging enzymes, proline and malondialdehyde to water deficits among six secondary successional seral species in Loess Plateau. PLoS ONE 9, e98872
| Responses of reactive oxygen scavenging enzymes, proline and malondialdehyde to water deficits among six secondary successional seral species in Loess Plateau.Crossref | GoogleScholarGoogle Scholar | 24914928PubMed |
Fan JP, He CH (2006) Simultaneous quantification of three major bioactive triterpene acids in the leaves of Diospyros kaki by high-performance liquid chromatography method. Journal of Pharmaceutical and Biomedical Analysis 41, 950–956.
| Simultaneous quantification of three major bioactive triterpene acids in the leaves of Diospyros kaki by high-performance liquid chromatography method.Crossref | GoogleScholarGoogle Scholar | 16527439PubMed |
Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446.
| Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Crossref | GoogleScholarGoogle Scholar | 12660786PubMed |
Fukushima EO, Seki H, Ohyama K, Ono E, Umemoto N, Mizutani M, Saito K, Muranaka T (2011) CYP716A subfamily members are multifunctional oxidases in triterpenoid biosynthesis. Plant & Cell Physiology 52, 2050–2061.
| CYP716A subfamily members are multifunctional oxidases in triterpenoid biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.
| Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.Crossref | GoogleScholarGoogle Scholar | 20870416PubMed |
Gonzalez A, Cabrera Mde L, Henriquez MJ, Contreras RA, Morales B, Moenne A (2012) Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess. Plant Physiology 158, 1451–1462.
| Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess.Crossref | GoogleScholarGoogle Scholar | 22234999PubMed |
Gupta KJ, Fernie AR, Kaiser WM, Van Dongen JT (2011) On the origins of nitric oxide. Trends in Plant Science 16, 160–168.
| On the origins of nitric oxide.Crossref | GoogleScholarGoogle Scholar | 21185769PubMed |
Han RB, Yuan YJ (2004) Oxidative burst in suspension culture of Taxus cuspidata induced by a laminar shear stress in short-term. Biotechnology Progress 20, 507–513.
| Oxidative burst in suspension culture of Taxus cuspidata induced by a laminar shear stress in short-term.Crossref | GoogleScholarGoogle Scholar | 15058996PubMed |
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604–611.
| Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.Crossref | GoogleScholarGoogle Scholar |
Huang C, Qian ZG, Zhong JJ (2013) Enhancement of ginsenoside biosynthesis in cell cultures of Panax ginseng by N,Nʹ-dicyclohexylcarbodiimide elicitation. Journal of Biotechnology 165, 30–36.
| Enhancement of ginsenoside biosynthesis in cell cultures of Panax ginseng by N,Nʹ-dicyclohexylcarbodiimide elicitation.Crossref | GoogleScholarGoogle Scholar | 23467002PubMed |
Kim BJ, Gibson DM, Shuler ML (2005) Relationship of viability and apoptosis to taxol production in Taxus sp. suspension cultures elicited with methyl jasmonate. Biotechnology Progress 21, 700–707.
| Relationship of viability and apoptosis to taxol production in Taxus sp. suspension cultures elicited with methyl jasmonate.Crossref | GoogleScholarGoogle Scholar | 15932245PubMed |
Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. The Plant Cell 22, 541–563.
| Calcium signals: the lead currency of plant information processing.Crossref | GoogleScholarGoogle Scholar | 20354197PubMed |
Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annual Review of Plant Biology 54, 109–136.
| Nitric oxide: the versatility of an extensive signal molecule.Crossref | GoogleScholarGoogle Scholar | 14502987PubMed |
Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiology 135, 516–529.
| Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein.Crossref | GoogleScholarGoogle Scholar | 15122020PubMed |
Leite M, Quinta-Costa M, Leite PS, Guimaraes JE (1999) Critical evaluation of techniques to detect and measure cell death – study in a model of UV radiation of the leukaemic cell line HL60. Analytical Cellular Pathology 19, 139–151.
| Critical evaluation of techniques to detect and measure cell death – study in a model of UV radiation of the leukaemic cell line HL60.Crossref | GoogleScholarGoogle Scholar | 10866276PubMed |
Li X, Bonawitz ND, Weng JK, Chapple C (2010) The growth reduction associated with repressed lignin biosynthesis in Arabidopsis thaliana is independent of flavonoids. Plant Cell 22, 1620–1632.
| The growth reduction associated with repressed lignin biosynthesis in Arabidopsis thaliana is independent of flavonoids.Crossref | GoogleScholarGoogle Scholar | 20511296PubMed |
Liang ZS, Yang DF, Liang X, Zhang YJ, Liu Y, Liu FH (2012) Roles of reactive oxygen species in methyl jasmonate and nitric oxide-induced tanshinone production in Salvia miltiorrhiza hairy roots. Plant Cell Reports 31, 873–883.
| Roles of reactive oxygen species in methyl jasmonate and nitric oxide-induced tanshinone production in Salvia miltiorrhiza hairy roots.Crossref | GoogleScholarGoogle Scholar | 22189441PubMed |
Lima MR, Dias AC (2012) Phaeomoniella chlamydospora‐induced oxidative burst in Vitis vinifera cell suspensions: role of NADPH oxidase and Ca2+. Journal of Phytopathology 160, 129–134.
| Phaeomoniella chlamydospora‐induced oxidative burst in Vitis vinifera cell suspensions: role of NADPH oxidase and Ca2+.Crossref | GoogleScholarGoogle Scholar |
Lu D, Dong J, Jin H, Sun L, Xu X, Zhou T, Zhu Y, Xu M (2011a) Nitrate reductase-mediated nitric oxide generation is essential for fungal elicitor-induced camptothecin accumulation of Camptotheca acuminata suspension cell cultures. Applied Microbiology and Biotechnology 90, 1073–1081.
| Nitrate reductase-mediated nitric oxide generation is essential for fungal elicitor-induced camptothecin accumulation of Camptotheca acuminata suspension cell cultures.Crossref | GoogleScholarGoogle Scholar | 21336687PubMed |
Lu H, Zhu Z, Dong L, Jia X, Sun X, Yan L, Chai Y, Jiang Y, Cao Y (2011b) Lack of trehalose accelerates H2O2-induced Candida albicans apoptosis through regulating Ca2+ signaling pathway and caspase activity. PLoS ONE 6, e15808
| Lack of trehalose accelerates H2O2-induced Candida albicans apoptosis through regulating Ca2+ signaling pathway and caspase activity.Crossref | GoogleScholarGoogle Scholar | 21246042PubMed |
Moreau M, Lindermayr C, Durner J, Klessig DF (2010) NO synthesis and signaling in plants – where do we stand? Physiologia Plantarum 138, 372–383.
| NO synthesis and signaling in plants – where do we stand?Crossref | GoogleScholarGoogle Scholar | 19912564PubMed |
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.
Newman JD, Chappell J (1999) Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway. Critical Reviews in Biochemistry and Molecular Biology 34, 95–106.
| Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway.Crossref | GoogleScholarGoogle Scholar | 10333387PubMed |
Pedroso MC, Magalhaes JR, Durzan D (2000) A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues. Journal of Experimental Botany 51, 1027–1036.
| A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues.Crossref | GoogleScholarGoogle Scholar | 10948230PubMed |
Pennell RI, Lamb C (1997) Programmed cell death in plants. The Plant Cell 9, 1157–1168.
| Programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar | 12237381PubMed |
Petõ A, Lehotai N, Feigl G, Tugyi N, Ördög A, Gémes K, Tari I, Erdei L, Kolbert Z (2013) Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis. Plant Cell Reports 32, 1913–1923.
| Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24013762PubMed |
Ranieri A, Castagna A, Lorenzini G, Soldatini GF (1997) Changes in thylakoid protein patterns and antioxidant levels in two wheat cultivars with different sensitivity to sulfur dioxide. Environmental and Experimental Botany 37, 125–135.
| Changes in thylakoid protein patterns and antioxidant levels in two wheat cultivars with different sensitivity to sulfur dioxide.Crossref | GoogleScholarGoogle Scholar |
Rohmer M, Knani M, Simonin P, Sutter B, Sahm H (1993) Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. The Biochemical Journal 295, 517–524.
Sabater-Jara A, Tudela L, Lopez-Perez A (2010) In vitro culture of Taxus sp.: strategies to increase cell growth and taxoid production. Phytochemistry Reviews 9, 343–356.
| In vitro culture of Taxus sp.: strategies to increase cell growth and taxoid production.Crossref | GoogleScholarGoogle Scholar |
Sapir-Mir M, Mett A, Belausov E, Tal-Meshulam S, Frydman A, Gidoni D, Eyal Y (2008) Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiology 148, 1219–1228.
| Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes.Crossref | GoogleScholarGoogle Scholar | 18988695PubMed |
Shang GM, Wu JC, Yuan YJ (2004) Improved cell growth and taxol production of suspension-cultured Taxus chinensis var. mairei in alternating and direct current magnetic fields. Biotechnology Letters 26, 875–878.
| Improved cell growth and taxol production of suspension-cultured Taxus chinensis var. mairei in alternating and direct current magnetic fields.Crossref | GoogleScholarGoogle Scholar | 15269533PubMed |
Vandelle E, Poinssot B, Wendehenne D, Bentejac M, Alain P (2006) Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Molecular Plant–Microbe Interactions 19, 429–440.
| Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses.Crossref | GoogleScholarGoogle Scholar | 16610746PubMed |
Verma K, Mehta SK, Shekhawat GS (2013) Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses. Biometals 26, 255–269.
| Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses.Crossref | GoogleScholarGoogle Scholar | 23322177PubMed |
Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. Plant & Cell Physiology 46, 923–930.
| Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells.Crossref | GoogleScholarGoogle Scholar |
Wang Y, Lin J, Wang G (2010) Role of calcium in nitric oxide-induced programmed cell death in tobacco protoplasts. Biologia Plantarum 54, 471–476.
| Role of calcium in nitric oxide-induced programmed cell death in tobacco protoplasts.Crossref | GoogleScholarGoogle Scholar |
Wang Q, Liang X, Dong Y, Xu L, Zhang X, Hou J, Fan Z (2013) Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regulation 69, 11–20.
| Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar |
Wentzinger LF, Bach TJ, Hartmann MA (2002) Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme a reductase. Plant Physiology 130, 334–346.
| Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme a reductase.Crossref | GoogleScholarGoogle Scholar | 12226513PubMed |
Yin J, Ren CL, Zhan YG, Li CX, Xiao JL, Qiu W, Li XY, Peng HM (2012) Distribution and expression characteristics of triterpenoids and OSC genes in white birch (Betula platyphylla Suk.). Molecular Biology Reports 39, 2321–2328.
| Distribution and expression characteristics of triterpenoids and OSC genes in white birch (Betula platyphylla Suk.).Crossref | GoogleScholarGoogle Scholar | 21647548PubMed |
Yuan YJ, Li C, Hu ZD, Wu JC, Zeng AP (2002) Fungal elicitor-induced cell apoptosis in suspension cultures of Taxus chinensis var. mairei for taxol production. Process Biochemistry 38, 193–198.
| Fungal elicitor-induced cell apoptosis in suspension cultures of Taxus chinensis var. mairei for taxol production.Crossref | GoogleScholarGoogle Scholar |
Zeng FS, Sun FK, Li LL, Liu K (2014) Genome-scale transcriptome analysis in response to nitric oxide in birch cells: implications of the triterpene biosynthetic pathway. PLoS ONE 9, e116157
| Genome-scale transcriptome analysis in response to nitric oxide in birch cells: implications of the triterpene biosynthetic pathway.Crossref | GoogleScholarGoogle Scholar |
Zhang WH, Rengel Z, Kuo J (1998) Determination of intracellular Ca2+ in cells of intact wheat roots: loading of acetoxymethyl ester of Fluo‐3 under low temperature. The Plant Journal 15, 147–151.
| Determination of intracellular Ca2+ in cells of intact wheat roots: loading of acetoxymethyl ester of Fluo‐3 under low temperature.Crossref | GoogleScholarGoogle Scholar |
Zhang B, Zheng LP, Wang JW (2012a) Nitric oxide elicitation for secondary metabolite production in cultured plant cells. Applied Microbiology and Biotechnology 93, 455–466.
| Nitric oxide elicitation for secondary metabolite production in cultured plant cells.Crossref | GoogleScholarGoogle Scholar | 22089384PubMed |
Zhang H, Wang W, Yin H, Zhao X, Du Y (2012b) Oligochitosan induces programmed cell death in tobacco suspension cells. Carbohydrate Polymers 87, 2270–2278.
| Oligochitosan induces programmed cell death in tobacco suspension cells.Crossref | GoogleScholarGoogle Scholar |
