CDPKs enhance Cd tolerance through intensifying H2S signal in Arabidopsis thaliana

Plant and Soil

Volumn 398, Issue 1-2, 2016, Pages 99-110

  Qiao, Zengjie ^a   Jing, Tao ^b   Jin, Zhuping ^a   Liang, Yali ^a   Zhang, Liping ^a   Liu, Zhiqiang ^a   Liu, Danmei ^a   Pei, Yanxi ^a  

^a SHANXI UNIVERSITY   (China)

^b OHIO UNIVERSITY   (United States)

Author keywords

Cadmium; Calcium dependent protein kinases; Glutathione persulfide; Hydrogen sulfide; L cysteine desulfhydrase; Protein S sulfhydration

Indexed keywords

CADMIUM; ENZYME; ENZYME ACTIVITY; EXPERIMENTAL STUDY; GENE EXPRESSION; HERB; HYDROGEN SULFIDE; MUTATION; POLLUTION TOLERANCE; PROTEIN; TOXICITY TEST;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84955194762     PISSN: 0032079X     EISSN: 15735036     Source Type: Journal    
DOI: 10.1007/s11104-015-2643-x     Document Type: Article

References (49)

1. Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669
2. Aroca A, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a new post-translational modification in plant systems. Plant Physiol. doi:10.1104/pp. 15.00009
3. Becana M, Aparicio-Tejo P, Irigoyen JJ, Sanchez-Diaz M (1986) Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of medicago sativa. Plant Physiol 82:1169–1171
4. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605
5. Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493
6. Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485
7. DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5:663–667
8. Dawood M, Cao F, Jahangir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209–210:121–128
9. Dooley FD, Nair SP, Ward PD (2013) Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One 8, e62048
10. Fang H, Jing T, Liu Z, Zhang L, Jin Z, Pei Y (2014) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481
11. Finkel T (2012) From sulfenylation to sulfhydration: what a thiolate needs to tolerate. Sci Signal 5:pe10
12. Garcia-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
13. Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 57:715S–724S, discussion 724S-725S
14. Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420
15. Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486
16. Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46
17. 2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal 4:ra86
18. Krussel L, Junemann J, Wirtz M, Birke H, Thornton JD, Browning LW, Poschet G, Hell R, Balk J, Braun HP, Hildebrandt TM (2014) The mitochondrial sulfur dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 is required for amino acid catabolism during carbohydrate starvation and embryo development in Arabidopsis. Plant Physiol 165:92–104
19. Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51:169–187
20. Li L, Wang Y, Shen W (2012a) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631
21. 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 Ca(2+) and calmodulin. Plant Sci 185–186:185–189
22. Li ZG, Ding XJ, Du PF (2013a) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747
23. Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013b) Hydrogen sulphide 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
24. Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36:1607–1616
25. 2S and NO. Methods 62:177–181
26. Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol 4, e327
27. Munaron L, Avanzato D, Moccia F, Mancardi D (2013) Hydrogen sulfide as a regulator of calcium channels. Cell Calcium 53:77–84
28. 2S signals through protein S-sulfhydration. Sci Signal 2:ra72
29. 2S-releasing enzymes of higher plants - from the field to the test tube and back. Plant Biol (Stuttg) 9:582–588
30. 2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13:499–507
31. Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548
32. 2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis. Plant Soil 393:137–146
33. Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005) Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. Febs J 272:1291–1304
34. Romeroa LC, Ángeles Arocaa M, Sernab A, Gotora C (2013) Proteomic analysis of endogenous S-sulfhydration in Arabidopsis thaliana. Nitric Oxide 31:S23
35. Sambrook J, Manistis T (1987) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
36. Schaedle M (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012
37. Sen N, Paul BD, Gadalla MM, Mustafa AK, Sen T, Xu R, Kim S, Snyder SH (2012) Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions. Mol Cell 45:13–24
38. 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
39. Shi H, Ye T, Chan Z (2014a) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74C:99–107
40. Shi H, Ye T, Han N, Bian H, Liu X, Chan Z (2014b) Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J Integr Plant Biol 57:628–640
41. Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signal Behav 2:79–85
42. Vandiver MS, Paul BD, Xu R, Karuppagounder S, Rao F, Snowman AM, Ko HS, Lee YI, Dawson VL, Dawson TM, Sen N, Snyder SH (2013) Sulfhydration mediates neuroprotective actions of parkin. Nat Commun 4:1626
43. Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896
44. Yang G, Zhao K, Ju Y, Mani S, Cao Q, Puukila S, Khaper N, Wu L, Wang R (2013) Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal 18:1906–1919
45. Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529
46. Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094
47. Zhang H, Ye Y, Wang S, Luo J, Tang J, Ma D (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250
48. Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567
49. Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036