硫化氢信号能够通过生物钟调控拟南芥对冷胁迫的响应
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摘要
硫化氢(hydrogen sulfide, H_2S)是继一氧化氮(nitric oxide, NO)与一氧化碳(carbon oxide, CO)之后的第3种气体信号分子,在动植物中均发挥着重要的生理功能。生物钟是生物体的内在计时器,对动植物适应环境和生长发育至关重要。鉴于H_2S与生物钟调控的生理过程有较大的相关性,本文以拟南芥(Arabidopsis thaliana)为实验材料,对二者之间的关系进行了探索。结果发现,外源NaHS(H_2S供体)处理能够上调生物钟相关基因CCA1(circadian clock associated 1)和PRR9(pseudo-response regulator 9)的表达,而且在H_2S生成关键酶编码基因缺失的双突变体lcd/des1中,CCA1与PRR9的峰值表达时间明显滞后。CBFs(c-repeat binding factors)是受CCA1调控的冷胁迫响应基因,其表达也受H_2S的调控。lcd/des1中CBF1和CBF3的峰值表达时间延迟,同时在lcd/des1中CBF1、CBF2和CBF3都下调表达。lcd/des1幼苗对冷胁迫表现出更高的敏感性。本文也对拟南芥内源H_2S生成关键酶L-半胱氨酸脱硫基酶(L-cysteine desulfhydrase, LCD)与脱硫基酶1(desulfhydrase 1, DES1)编码基因的转录水平节律性进行了初步的探索。LCD的表达在1 d内未见明显的变化,而DES1的表达有明显的节律性,在早上8:00达到峰值。综上所述,H_2S能够通过调节CCA1与PRR9基因的表达调控生物钟,进而影响下游靶标CBFs基因的表达以增加拟南芥对冷胁迫的耐受性。
Hydrogen sulfide(H_2S), the third gasotransmitter after nitric oxide and carbon oxide, performs important functions in both animals and plants. Circadian clock is internal timekeeper of organisms, which is crucial for environment adaption, growth and development. The relationship between H_2S and circadian clock in Arabidopsis thaliana was explored because they have many overlap functions. The results showed that NaHS(H_2S donor) could up-regulated the gene expression levels of CCA1(circadian clock associated 1) and PRR9(pseudo-response regulator 9) which are core circadian clock genes. The peak expression levels of CCA1 and PRR9 were delayed in H_2S synthesis mutant lcd/des1. The expression of CBFs(c-repeat binding factors), the cold stress response genes that are the downstream target of CCA1, was also regulated by H_2S. In lcd/des1, the peak expression of CBF1 and CBF3 was delayed and the expression levels of CBF1, CBF2 and CBF3 were decreased. The seedlings of lcd/des1 were more sensitivity to cold stress than WT. The diurnal change of LCD(L-cysteine desulfhydrase) and DES1(desulfhydrase 1), which encode H_2S production enzymes in Arabidopsis, was also analyzed. The expression of LCD did not change significantly during 1 d, however, the expression of DES1 showed diurnal change with peak at 8 in the morning. In summary, H_2S can regulate the expression levels of clock genes CCA1 and PRR9, as well as its downstream genes CBFs to increase resistance to cold stress in Arabidopsis thaliana.
Hydrogen sulfide(H_2S), the third gasotransmitter after nitric oxide and carbon oxide, performs important functions in both animals and plants. Circadian clock is internal timekeeper of organisms, which is crucial for environment adaption, growth and development. The relationship between H_2S and circadian clock in Arabidopsis thaliana was explored because they have many overlap functions. The results showed that NaHS(H_2S donor) could up-regulated the gene expression levels of CCA1(circadian clock associated 1) and PRR9(pseudo-response regulator 9) which are core circadian clock genes. The peak expression levels of CCA1 and PRR9 were delayed in H_2S synthesis mutant lcd/des1. The expression of CBFs(c-repeat binding factors), the cold stress response genes that are the downstream target of CCA1, was also regulated by H_2S. In lcd/des1, the peak expression of CBF1 and CBF3 was delayed and the expression levels of CBF1, CBF2 and CBF3 were decreased. The seedlings of lcd/des1 were more sensitivity to cold stress than WT. The diurnal change of LCD(L-cysteine desulfhydrase) and DES1(desulfhydrase 1), which encode H_2S production enzymes in Arabidopsis, was also analyzed. The expression of LCD did not change significantly during 1 d, however, the expression of DES1 showed diurnal change with peak at 8 in the morning. In summary, H_2S can regulate the expression levels of clock genes CCA1 and PRR9, as well as its downstream genes CBFs to increase resistance to cold stress in Arabidopsis thaliana.
引文
[1] Más P. Circadian clock function in Arabidopsis thaliana: time beyond transcription[J]. Trends Cell Biol, 2008, 18(6): 273-281
[2] McClung CR. Plant circadian rhythms[J]. Plant Cell, 2006, 18(4): 792-803
[3] Hsu PY, Harmer SL. Wheels within wheels: the plant circadian system[J]. Trends Plant Sci, 2014, 19(4): 240-249
[4] Nohales MA, Kay SA. Molecular mechanisms at the core of the plant circadian oscillator[J]. Nat Struct Mol Biol, 2016, 23(12): 1061-1069
[5] Covington MF, Maloof JN, Straume M, et al. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development[J]. Genome Biol, 2008, 9(8): R130
[6] Harmer SL, Hogenesch JB, Straume M, et al. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock[J]. Science, 2000, 290(5499): 2110-2113
[7] Shi Y, Ding Y, Yang S. Cold signal transduction and its interplay with phytohormones during cold acclimation[J]. Plant Cell Physiol, 2015, 56(1): 7-15
[8] Dong MA, Farré EM, Thomashow MF. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the c-repeat binding factor (CBF) pathway in Arabidopsis[J]. Proc Natl Acad Sci U S A, 2011, 108(17): 7241-7246
[9] Hotta CT, Gardner MJ, Hubbard KE, et al. Modulation of environmental responses of plants by circadian clocks[J]. Plant Cell Environ, 2007, 30(3): 333-349
[10] Harmer SL. The circadian system in higher plants[J].Annu Rev Plant Biol,2009, 60: 357- 377
[11] Wang R. Gasotransmitters: growing pains and joys[J]. Trends Biochem Sci, 2014, 39(5): 227-232
[12] Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed [J]. Physiol Rev, 2012, 92(2): 791-896
[13] Papenbrock J, Riemenschneider A, Kamp A, et al. Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants - from the field to the test tube and back[J]. Plant Biol(Stuttg), 2007, 9(5): 582-588
[14] Alvarez C, Calo L, Romero LC, et al. An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis[J]. Plant Physiol, 2010, 152(2): 656-669
[15] 裴雁曦. 植物中的气体信号分子硫化氢:无香而立,其臭如兰[J]. 中国生物化学与分子生物学报(Pei YX. Gasotransmitter hydrogen sulfide in plants: stinking to high heaven, but refreshing to fine life [J]. Chin J Biochem Mol Biol), 2016, 32(7): 721-733
[16] Guo HM, Xiao TY, Zhou H, et al. Hydrogen sulfide: a versatile regulator of environmental stress in plants[J]. Acta Physiol Plant, 2016, 38(1): 16
[17] Shi H, Ye T, Han N, et al. Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis[J]. J Integr Plant Biol, 2015, 57(7): 628-640
[18] Shi H, Ye T, Chan Z. Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.)[J]. Plant Physiol Biochem, 2013, 71: 226-234
[19] Ma L, Yang L, Zhao J, et al. Comparative proteomic analysis reveals the role of hydrogen sulfide in the adaptation of the alpine plant Lamiophlomis rotata to altitude gradient in the Northern Tibetan Plateau[J]. Planta, 2015, 241(4): 887-906
[20] Du X, Jin Z, Liu D, et al. Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana [J]. Plant Physiol Biochem, 2017, 120: 112-119
[21] Shen J, Xing T, Yuan H, et al. Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions[J]. PLoS One, 2013, 8(10): e77047
[2] McClung CR. Plant circadian rhythms[J]. Plant Cell, 2006, 18(4): 792-803
[3] Hsu PY, Harmer SL. Wheels within wheels: the plant circadian system[J]. Trends Plant Sci, 2014, 19(4): 240-249
[4] Nohales MA, Kay SA. Molecular mechanisms at the core of the plant circadian oscillator[J]. Nat Struct Mol Biol, 2016, 23(12): 1061-1069
[5] Covington MF, Maloof JN, Straume M, et al. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development[J]. Genome Biol, 2008, 9(8): R130
[6] Harmer SL, Hogenesch JB, Straume M, et al. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock[J]. Science, 2000, 290(5499): 2110-2113
[7] Shi Y, Ding Y, Yang S. Cold signal transduction and its interplay with phytohormones during cold acclimation[J]. Plant Cell Physiol, 2015, 56(1): 7-15
[8] Dong MA, Farré EM, Thomashow MF. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the c-repeat binding factor (CBF) pathway in Arabidopsis[J]. Proc Natl Acad Sci U S A, 2011, 108(17): 7241-7246
[9] Hotta CT, Gardner MJ, Hubbard KE, et al. Modulation of environmental responses of plants by circadian clocks[J]. Plant Cell Environ, 2007, 30(3): 333-349
[10] Harmer SL. The circadian system in higher plants[J].Annu Rev Plant Biol,2009, 60: 357- 377
[11] Wang R. Gasotransmitters: growing pains and joys[J]. Trends Biochem Sci, 2014, 39(5): 227-232
[12] Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed [J]. Physiol Rev, 2012, 92(2): 791-896
[13] Papenbrock J, Riemenschneider A, Kamp A, et al. Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants - from the field to the test tube and back[J]. Plant Biol(Stuttg), 2007, 9(5): 582-588
[14] Alvarez C, Calo L, Romero LC, et al. An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis[J]. Plant Physiol, 2010, 152(2): 656-669
[15] 裴雁曦. 植物中的气体信号分子硫化氢:无香而立,其臭如兰[J]. 中国生物化学与分子生物学报(Pei YX. Gasotransmitter hydrogen sulfide in plants: stinking to high heaven, but refreshing to fine life [J]. Chin J Biochem Mol Biol), 2016, 32(7): 721-733
[16] Guo HM, Xiao TY, Zhou H, et al. Hydrogen sulfide: a versatile regulator of environmental stress in plants[J]. Acta Physiol Plant, 2016, 38(1): 16
[17] Shi H, Ye T, Han N, et al. Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis[J]. J Integr Plant Biol, 2015, 57(7): 628-640
[18] Shi H, Ye T, Chan Z. Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.)[J]. Plant Physiol Biochem, 2013, 71: 226-234
[19] Ma L, Yang L, Zhao J, et al. Comparative proteomic analysis reveals the role of hydrogen sulfide in the adaptation of the alpine plant Lamiophlomis rotata to altitude gradient in the Northern Tibetan Plateau[J]. Planta, 2015, 241(4): 887-906
[20] Du X, Jin Z, Liu D, et al. Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana [J]. Plant Physiol Biochem, 2017, 120: 112-119
[21] Shen J, Xing T, Yuan H, et al. Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions[J]. PLoS One, 2013, 8(10): e77047