Endogenous hydrogen sulfide regulated by calcium is involved in thermotolerance in tobacco Nicotiana tabacum L. suspension cell cultures

• Autorzy: Li Z.-G. , Long W.-B. , Yang S.-Z. , Wang Y.-C. , Tang J.-H. , Wen L. , Wen L. , Zhu B.-Y. , Min X.
• Języki publikacji: EN

Abstrakty

EN

Calcium (Ca2+)/calmodulin (CaM), a core component of calcium messenger system, is a multiple second messenger that is involved in multiple stress tolerance including heat tolerance in plants, hydrogen sulfide (H2S) is fast emerging similar functions, but Ca2+ and H2S crosstalk in the acquisition of thermotolerance is not completely understood. In this article, Ca2+ and CaM activated the activity of cysteine desulfhydrase (L-DES), followed by inducing endogenous H2S accumulation in tobacco suspension cultured cells, while treatment with Ca2+ chelator ethylene glycol-bis(b-aminoethylether)- N,N,N0,N0-tetraacetic acid and CaM antagonists chlorpromazine lowered L-DES activity and H2S accumulation. Interestingly, Ca2+- and CaM-activated L-DES activity and endogenous H2S accumulation were eliminated by H2S synthesis inhibitors DL-propargylglycine (PAG), aminooxy acetic acid (AOA), potassium pyruvate (PP) and hydroxylamine (HA), and the H2S scavenger hypotaurine (HT), indicating that Ca2+ and CaM regulated endogenous H2S generation via activating L-DES activity in tobacco cells. Furthermore, H2S donor NaHS, Ca2+ and CaM treatment alone significantly improved the thermotolerance of tobacco cells, and heat tolerance induced by Ca2+ and CaM was enhanced by exogenous NaHS, while weakened by PAG, AOA, PP, HA or HT. All above-mentioned results suggest that endogenous H2S generated by L-DES was involved, at least partly, in the thermotolerance induced by Ca2+ and CaM in tobacco suspension cell cultures.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 10
• Opis fizyczny: Article: 219 [11 p.], fig.,ref.

Twórcy

autor

Li Z.-G.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

autor

Long W.-B.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

autor

Yang S.-Z.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

autor

Wang Y.-C.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

autor

Tang J.-H.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

autor

Wen L.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

autor

Wen L.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

autor

Zhu B.-Y.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

autor

Min X.

• School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China
• Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China
• Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic of China

Bibliografia

• Batistic O, Kim KN, Kleist T, Kudla J, Luan S (2011) The CBL–CIPK network for decoding calcium signals in plants. In: Luan S (ed) Coding and decoding of calcium signals in plants. Springer, Berlin, pp 235–258
• Calderwood A, Kopriva S (2014) Hydrogen sulfide in plants: from dissipation of excess sulfur to signalling molecule. Nitric Oxide 41:72–78
• Christou A, Manganaris GA, Papadopoulos I, Fotopouls V (2013) Hydrogen sulfide induces systemic tolerance to salinity and nonionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64:1953–1966
• Christou A, Filippou P, Manganaris GA, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 149:42
• Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:4.1–4.28
• Dubrovina AS, Kiselev KV, Khristenko VS (2013) Expression of calcium-dependent protein kinase (CDPK) genes under abiotic stress conditions in wild-growing grapevine Vitis amurensis. J Plant Physiol 170:1491–1500
• Fang T, Cao ZY, Li JL, Shen WB, Huang LQ (2014a) Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol Biochem 76:44–51
• Fang HH, Jing T, Liu ZQ, Zhang LP, Jin ZP, Pei YX (2014b) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481
• Fu PN, Wang WJ, Hou LX, Liu X (2013) Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Soc Bot Pol 82:295–302
• García-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201(202):66–73
• Gong M, Chen SN, Song YQ, Li ZG (1997) Effect of calcium and calmodulin on intrinsic heat tolerance in relation to antioxidant systems in maize seedlings. Aust J Plant Physiol 24:371–379
• Gong M, van der Luit AH, Knight MR, Trewavas AJ (1998) Heat shockinduced changes of intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116:429–437
• Hancock JT, Whiteman M (2014) Hydrogen sulfide and cell signaling: team player or referee+ Plant Physiol Biochem 78:37–42
• Knight H (2000) Calcium signaling during abiotic stress in plants. Inter Rev Cytol 195:269–324
• Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563
• Kump LR, Pavlov A, Arthur MA (2005) Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia. Geology 33:397–400
• Larkindale J, Knight MR (2002) Protection against heat stressinduced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:628–695
• Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defencesignalling pathways. New Phytol 171:249–269
• Lee SW, Hu YS, Hu LF, Lu Q, Dawe GS, Moore PK, Wong PTH, Bian JS (2006) Hydrogen sulphide regulates calcium homeostasis in microglial cells. Glia 54:116–124
• Li ZG (2013) Hydrogen sulfide: a multifunctional gaseous molecule in plants. Russ J Plant Physiol 60:733–740
• Li ZG (2015a) Analysis of some enzymes activities of hydrogen sulfide metabolism in plants. Methods Enzymol 555:253–269
• Li ZG (2015b) Quantification of hydrogen sulfide concentration using methylene blue and 5,50-dithiobis(2-nitrobenzoic acid) methods in Plants. Methods Enzymol 554:101–110
• Li ZG, Gong M (2009) Involvement of calcium and calmodulin in mechanical stimulation-induced heat tolerance in tobacco (Nicotiana Tabacum L.) suspension cultured cells. Plant Physiol J 45:363–366
• Li ZG, Zhu LP (2015) Hydrogen sulfide donor sodium hydrosulfideinduced accumulation of betaine is involved in the acquisition of heat tolerance in maize seedlings. Br J Bot 38:31–38
• Li ZG, Du CK, Gong M (2005) Involvement of Ca2+ and calmodulin in the regulation of H2O2-induced heat tolerance in maize seedlings. J Plant Physiol Mol Biol 31:515–519
• Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51:169–187
• Li ZG, Gong M, Liu P (2012a) Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha Curcas. Acta Physiol Plant 34:2207–2213
• Li ZG, Gong M, Xie H, Yang L, Li J (2012b) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185(186):185–189
• Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013a) Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564–1572
• Li ZG, Ding XJ, Du PF (2013b) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747
• Li ZG, Luo LJ, Zhu LP (2014a) Involvement of trehalose in hydrogen sulfide donor sodium hydrosulfide-induced the acquisition of heat tolerance in maize (Zea mays L.) seedlings. Bot Stud 55:20
• Li ZG, Yi XY, Li YT (2014b) Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings. Biologia 69:1001–1009
• Li ZG, Xie LR, Li XJ (2015) Hydrogen sulfide acts as a downstream signal molecule in salicylic acid-induced heat tolerance in maize (Zea mays L.) seedlings. J Plant Physiol 177:121–127
• Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935
• Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule+ Plant Cell Environ 36:1607–1616
• McAinsh RM, Pittman JK (2009) Shaping the calcium signature. N Phytol 181:275–294
• Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–479
• Nagain Y, Tsugane M, Oka JI, Kimura H (2004) Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18:557–559
• Reddy ASN (2001) Calcium: silver bullet in signaling. Plant Sci 160:381–404
• Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:62010–62032
• Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Overexpression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327
• Shi H, Ye T, Chan Z (2013) Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 71:226–234
• Shi H, Ye T, Chan Z (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74:99–107
• Shi H, Ye T, Han N, Bian H, Liu X, Chan Z (2015) Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J Int Plant Biol 57:628–640
• Takahashi Y, Ito T (2011) Structure and function of CDPK: a sensor responder of calcium. In: Luan S (ed) Coding and decoding of calcium signals in plants. Springer, Berlin, pp 129–146
• Yang GD, Wu LY, Jiang B, Yang W, Qi JS, Cao K, Meng QH, Mustafa AK, Mu WD, Zhang SM, Snyder SH, Wang R (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine c-lyase. Science 322:587–590
• Zhang H, Hua SL, Zhang ZJ, Hua LY, Jiang CX, Wei ZJ, Liu L, Wang HL, Jiang ST (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharv Biol Technol 60:251–257

Identyfikatory

DOI

10.1007/s11738-015-1971-z