干旱条件下DCMU对高表达转C_4-pepc水稻的花青素合成基因及其相关信号的影响
|
摘要
为了揭示高表达转玉米C4-磷酸烯醇式丙酮酸羧化酶(PEPC,EC 4.1.1.31)基因水稻(PC)在耐旱中光合与花青素调节途径的内在联系,本研究以PC和未转基因野生型原种(WT)的水培苗为试验材料,在4~5叶期,通过50μmol·L-1光合抑制剂DCMU[3-(3’,4’-dich-lorophenyl)-1,1-dimethyl-urea]预处理1 h,观察其在12%PEG-6000模拟干旱处理下的表现。结果表明,在模拟干旱条件下,DCMU预处理使两种供试材料相对含水量显著下降,且PC相对含量显著高于WT;干旱处理下,两种材料的花青素含量显著升高,DCMU和干旱处理使两种材料的花青素含量下调,且PC水稻中始终伴随着较高的花青素含量。光合数据表明,与单独12%PEG-6000处理相比,DCMU联合12%PEG-6000处理显著抑制了两种水稻材料的净光合速率、气孔导度、胞间CO2含量及羧化效率,但PC的各指标显著高于WT。同时,DCMU联合12%PEG-6000处理显著下调两种供试材料的内源蔗糖含量,但PC中蔗糖含量显著高于WT。进一步研究发现PC中更高的蔗糖含量与花青素合成有关转录因子b HLH(Os B1,Os B2)、R2R3-MYB(Os C1)、COP1(constitutively photomorphogenic 1)、HY5(elongated hypocotyl 5)更高的转录水平同步,下游花青素合成相关基因Os PAL、Os CHI、Os CHS、Os F3H、Os F3’H、Os DFR、Os ANS的表达量增加。PC水稻可能通过诱导NO和Ca2(10)感受干旱信号,参与转录因子的调节,进而参与花青素合成基因的调控,合成较多的花青素,增强PC水稻对干旱逆境的响应,增强保水能力,最终表现耐旱。
Anthocyanins are important antioxidant materials that protects plant from damage by reactive oxygen species(ROS). Especially under adverse conditions, the regulation of sucrose in plants depends on its ability to induce anthocyanin accumulation. To determine the intrinsic relationship between photosynthetic and anthocyanin regulated pathways for C4-phosphoenolpyruvate carboxylate(PEPC, EC 4.1.1.31) gene overexpressed rice(PC) in drought conditions, PC and untransformed wild-type(WT) were treated with 50 μmol·L-1 photosynthetic inhibitor DCMU for 1 h and the performance of the rice seedlings at 4-5 leaf stage observed under 12% PEG-6000 simulated drought. The results showed that DCMU pretreatment significantly reduced relative water contents of WT and PC under simulated 12% PEG-6000 drought condition, and relative water content of PC was significantly higher than that of WT. The anthocyanin content was higher in PC than in WT under 12% PEG-6000 simulated drought or drought plus DCMU pretreatment. 12% PEG-6000 simulated drought decreased anthocyanin contents of PC and WT, while DCMU pretreatment alleviated this effect. Compared with 12% PEG-6000, DCMU plus 12% PEG-6000 significantly inhibited net photosynthetic rate, stomatal conductance, intercellular CO2 and carboxylation efficiency of the two rice lines, but these parameters of PC lines were significantly higher than those of WT lines. Then DCMU plus 12% PEG-6000 down-regulated endogenous sucrose content of the two materials, but sucrose content of PC lines was significantly higher than that of WT lines. Further studies showed that higher sucrose level in PC was associated with higher expression levels of transcriptional factors of b HLH(Os B1, Os B2), R2 R3-MYB(Os C1), COP1(constitutively photomorphogenic 1), HY5(elongated hypocotyl 5), Os PAL, Os CHI, Os CHS, Os F3 H, Os F3'H, Os DFR and Os ANS, which resulted in synthesizing more anthocyanin to improve water retention capacity. In addition, PC rice sensed drought signals through NO and Ca2+, which participated in the regulation of transcription factors, regulation of anthocyanin synthesis gene, synthesis of more anthocyanin and thereby enhanced PC rice response to drought stress. This enhanced water retention capacity, stabilized photosynthetic capacity and resisted drought. Therefore, it was beneficial in molecular breeding of "C4 Rice" to study the symphony between high yield and plant resistance.
Anthocyanins are important antioxidant materials that protects plant from damage by reactive oxygen species(ROS). Especially under adverse conditions, the regulation of sucrose in plants depends on its ability to induce anthocyanin accumulation. To determine the intrinsic relationship between photosynthetic and anthocyanin regulated pathways for C4-phosphoenolpyruvate carboxylate(PEPC, EC 4.1.1.31) gene overexpressed rice(PC) in drought conditions, PC and untransformed wild-type(WT) were treated with 50 μmol·L-1 photosynthetic inhibitor DCMU for 1 h and the performance of the rice seedlings at 4-5 leaf stage observed under 12% PEG-6000 simulated drought. The results showed that DCMU pretreatment significantly reduced relative water contents of WT and PC under simulated 12% PEG-6000 drought condition, and relative water content of PC was significantly higher than that of WT. The anthocyanin content was higher in PC than in WT under 12% PEG-6000 simulated drought or drought plus DCMU pretreatment. 12% PEG-6000 simulated drought decreased anthocyanin contents of PC and WT, while DCMU pretreatment alleviated this effect. Compared with 12% PEG-6000, DCMU plus 12% PEG-6000 significantly inhibited net photosynthetic rate, stomatal conductance, intercellular CO2 and carboxylation efficiency of the two rice lines, but these parameters of PC lines were significantly higher than those of WT lines. Then DCMU plus 12% PEG-6000 down-regulated endogenous sucrose content of the two materials, but sucrose content of PC lines was significantly higher than that of WT lines. Further studies showed that higher sucrose level in PC was associated with higher expression levels of transcriptional factors of b HLH(Os B1, Os B2), R2 R3-MYB(Os C1), COP1(constitutively photomorphogenic 1), HY5(elongated hypocotyl 5), Os PAL, Os CHI, Os CHS, Os F3 H, Os F3'H, Os DFR and Os ANS, which resulted in synthesizing more anthocyanin to improve water retention capacity. In addition, PC rice sensed drought signals through NO and Ca2+, which participated in the regulation of transcription factors, regulation of anthocyanin synthesis gene, synthesis of more anthocyanin and thereby enhanced PC rice response to drought stress. This enhanced water retention capacity, stabilized photosynthetic capacity and resisted drought. Therefore, it was beneficial in molecular breeding of "C4 Rice" to study the symphony between high yield and plant resistance.
引文
[1]CHAVES M M,FLEXAS J,PINHEIRO C.Photosynthesis under drought and salt stress:regulation mechanisms from whole plant to cell[J].Annals of Botany,2009,103(4):551-560
[2]ZHU X G,LONG S P,ORT D R.Improving photosynthetic efficiency for greater yield[J].Annual Review of Plant Biology,2010,61:235-261
[3]KARKI S,RIZAL G,QUICK W P.Improvement of photosynthesis in rice(Oryza sativa L.)by inserting the C4 pathway[J].Rice,2013,6(1):28
[4]O′LEARY B,PARK J,PLAXTON W C.The remarkable diversity of plant PEPC(phosphoenolpyruvate carboxylase):recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs[J].Biochemical Journal,2011,436(1):15-34
[5]KU M S B,AGARIE S,NOMURA M,et al.High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants[J].Nature Biotechnology,1999,17:76-80
[6]JEANNEAU M,GERENTES D,FOUEILLASSAR X,et al.Improvement of drought tolerance in maize:towards the functional validation of the Zm-Asr1 gene and increase of water use efficiency by over-expressing C4-PEPC[J].Biochimie,2002,84:1127-1135
[7]JIAO D M,KUANG T Y,LI X,et al.Physiological characteristics of the primitive CO2 concentrating mechanism in PEPC transgenic rice[J].Science in China Series C:Life Sciences,2003,46(4):438-446
[8]BANDYOPADHYAY A,DATTA K,ZHANG J,et al.Enhanced photosynthesis rate in genetically engineered indica rice expressing PEPC gene cloned from maize[J].Plant Science,2007,172(6):1204-1209
[9]LIAN L,WANG X W,ZHU Y S,et al.Physiological and photosynthetic characteristics of indica Hang2 expressing the sugarcane PEPC gene[J].Molecular Biology Reports,2014,41:2189-2197
[10]REN C G,LI X,LIU X L,et al.Hydrogen peroxide regulated photosynthesis in C4-pepc transgenic rice[J].Plant Physiology and Biochemistry,2014,74:218-229
[11]DING Z S,SUN X F,HUANG S H,et al.Response of photosynthesis to short-term drought stress in rice seedlings overexpressing C4 phosphoenolpyruvate carboxylase from maize and millet[J].Photosynthetica,2015,53(4):481-488
[12]钱宝云,刘小龙,李霞.钙肥对不同内源钙含量水稻品种光合参数的影响[J].江苏农业学报,2014,30(3):467-473QIAN B Y,LIU X L,LI X.Photosynthesis of rice cultivars with various endogenous calcium contents in response to calcium fertilizer application[J].Jiangsu Journal of Agricultural Sciences,2014,30(3):467-473
[13]霍垲,陆巍,李霞.干旱胁迫下调节ATP的含量对提高转玉米C4型pepc水稻光合速率的影响[J].中国生态农业学报,2015,23(5):605-613HUO K,LU W,LI X.Effect of regulating ATP on improving photosynthetic rate of transgenic rice with overexpressing maize C4 pepc under drought stress[J].Chinese Journal of Eco-Agriculture,2015,23(5):605-613
[14]唐玉婷,李霞,陆巍,等.高表达转C4型PEPC基因水稻在低氮下诱导碳氮酶稳定光合作用[J].华北农学报,2015,30(4):95-100TANG Y T,LI X,LU W,et al.Transgenic rice with high expression of C4-PEPC genes induced higher carbon and nitrogen key enzyme to maintain photosynthesis under low nitrogen conditions[J].Acta Agriculturae Boreali-Sinica,2015,30(4):95-100
[15]JIAO D M,XIA L,HUANG X Q,et al.The characteristics of CO2 assimilation of photosynthesis and chlorophyll fluorescence in transgenic PEPC rice[J].Science Bulletin,2001,46(13):1080-1084
[16]DOUBNEROVáV,RY?LAVáH.What can enzymes of C4,photosynthesis do for C3,plants under stress?[J].Plant Science,2011,180(4):575-583
[17]JIAO D M,LI X,JI B H.Photoprotective effects of high level expression of C4,phosphoenolpyruvate carboxylase in transgenic rice during photoinhibition[J].Photosynthetica,2005,43(4):501-508
[18]李霞,任承钢.ABA、BA及DPI对高表达玉米C4 pepc基因的水稻光合特性及叶绿素荧光特性的影响[J].植物生理学报,2012,48(6):549-556LI X,REN C G.Effects on photosynthetic and fluorescence characteristics under treatments of ABA,BA or DPI in transgenic rice with over-expression C4-pepc gene[J].Plant Physiology Journal,2012,48(6):549-556
[19]LIU X,LI X,ZHANG C,et al.Phosphoenolpyruvate carboxylase regulation in C4-PEPC-expressing transgenic rice during early responses to drought stress[J].Physiologia Plantarum,2017,159(2):178-200
[20]HUO K,LI X,HE Y F,et al.Exogenous ATP enhance signal response of suspension cells of transgenic rice(Oryza sativa L.)expressing maize C4-pepc encoded phosphoenolpyruvate carboxylase under PEG treatment[J].Plant Growth Regulation,2016,82(1):55–67
[21]QIAN B Y,LI X,LIU X L,et al.Enhanced drought tolerance in transgenic rice over-expressing of maize C4 phosphoenolpyruvate carboxylase gene via NO and Ca2(10)[J].Journal of Plant Physiology,2015,175:9–20
[22]QIAN B Y,LI X,LIU X L,et al.Improved oxidative tolerance in suspension-cultured cells of C4-pepc transgenic rice by H2O2 and Ca2(10)under PEG-6000[J].Journal of Integrative Plant Biology,2015,57(6):534–549
[23]NAKASHIMA K,TRAN L S P,DONG V N,et al.Functional analysis of a NAC-type transcription factor Os NAC6 involved in abiotic and biotic stress-responsive gene expression in rice[J].Plant Journal,2007,51:617-630
[24]NIJHAWAN A,JAIN M,TYAGI A K,et al.Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice[J].Plant Physiology,2008,146(2):333-350
[25]HUANG G T,MA S L,BAI L P,et al.Signal transduction during cold,salt,and drought stresses in plants[J].Molecular Biology Reports,2012,39:969-987
[26]朱素琴,季本华,焦德茂.亚硫酸氢钠对转PEPC基因水稻叶片光合作用的促进作用[J].科技通报,2004,20(6):523-528ZHU S Q,JI B H,JIAO D M.Promotive effect of Na HSO3 on photosynthesis in PEPC transgenic rice leaves[J].Bulletin of Science and Technology,2004,20(6):523-528
[27]BISWAL A K,DILNAWAZ F,DAVID K A V,et al.Increase in the intensity of thermoluminescence Q-band during leaf ageing is due to a block in the electron transfer from QA to QB[J].Luminescence,2001,16(5):309-313
[28]SUZUKI K,OHMORI Y,RATEL E.High root temperature blocks both linear and cyclic electron transport in the dark during chilling of the leaves of rice seedlings[J].Plant and Cell Physiology,2011,52(9):1697-1707
[29]VAN DEN ENDE W,EL-ESAWE S K.Sucrose signaling pathways leading to fructan and anthocyanin accumulation:A dual function in abiotic and biotic stress responses?[J].Environmental and Experimental Botany,2014,108:4-13
[30]TENG S,KEURENTJES J,BENTSINK L,et al.Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene[J].Plant Physiology,2005,139(4):1840-1852
[31]SANYAL S K,PANDEY A,PANDEY G K.The CBL–CIPK signaling module in plants:a mechanistic perspective[J].Physiologia Plantarum,2015,155:89-108
[32]SHIN D H,CHOI M G,KANG C S,et al.A wheat R2R3-MYB protein PURPLE PLANT1(Ta PL1)functions as a positive regulator of anthocyanin biosynthesis[J].Biochemical&Biophysical Research Communications,2016,469(3):686-691
[33]YASUDA S,AOYAMA S,HASEGAWA Y,et al.Arabidopsis CBL-interacting protein kinases regulate carbon/nitrogen-nutrient response by phosphorylating ubiquitin ligase ATL31[J].Molecular Plant,2017,4(10):537-658
[34]SANYAL S K,KANWAR P,YADAV A K,et al.Arabidopsis CBL interacting protein kinase 3 interacts with ABR1,an APETALA2 domain transcription factor,to regulate ABA responses[J].Plant Science,2017,254:48-59
[35]YOSHIDA S,FORNO D A,COCK J H,et al.Laboratory Manual for Physiological Studies of Rice[M].Philippines:International Rice Research Institute,1976:61–64
[36]LI X,WANG C,REN C G.Effects of 1-butanol,neomycin and calcium on the photosynthetic characteristics of PEPC transgenic rice[J].African Journal of Biotechnology,2011,10:17466-17476
[37]AMBAVARAM M M R,BASU S,KRISHNAN A,et al.Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress[J].Nature Communications,2014,5:1-14
[38]RABINO I,MANCINELLI A L.Light,temperature,and anthocyanin production[J].Plant Physiology,1986,81(3):922-924
[39]MURPHY M E,NOACK E.Nitric oxide assay using hemoglobin method[J].Methods in Enzymology,1994,233:240–250
[40]YANG C Q,LIU W N,ZHAO Z H,et al.Determination of the content of serum calcium with methylthymol blue as chromogenic reagent[J].Spectroscopy&Spectral Analysis,1998,18:485–487
[41]JUNG H,KIM J K,HA S W.Use of animal viral IRES sequence makes multiple truncated transcripts without mediating polycistronic expression in rice[J].Journal of the Korean Society for Applied Biological Chemistry,2011,54:678–684
[42]CHEN P B,LI X,HUO K,et al.Promotion of photosynthesis in transgenic rice over-expressing of maize C4 phosphoenolpyruvate carboxylase gene by nitric oxide donors[J].Journal of Plant Physiology,2014,171:458–466
[43]JIA X H,ZHANG P P,SHI D J,et al.Regulation of PEPC gene expression in Anabaena sp.PCC 7120 and its effects on cyclic electron flow around photosystem I and tolerances to environmental stresses[J].Journal of Integrative Plant Biology,2015,57(5):468-476
[44]KEUNEN E,PESHEV D,VANGRONSVELD J,et al.Plant sugars are crucial players in the oxidative challenge during abiotic stress:extending the traditional concept[J].Plant Cell&Environment,2013,36(7):1242-1255
[45]LORETI E,POVERO G,NOVI G,et al.Gibberellins,jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis[J].New Phytologist,2008,179(4):1004-1016
[46]ZHANG Y C,GONG S F,LI Q H,et al.Functional and signaling mechanism analysis of rice CRYPTOCHROME 1[J].Plant Journal,2006,46(6):971-983
[47]SHIN D H,CHOI M,KIM K,et al.HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis[J].FEBS letters,2013,587(10):1543-1547
[48]丁在松,周宝元,孙雪芳,等.干旱胁迫下PEPC过表达增强水稻的耐强光能力[J].作物学报,2012,38(2):285-292DING Z S,ZHOU B Y,SUN X F,et al.High light tolerance is enhanced by overexpressed PEPC in rice under drought stress[J].Acta Agronomica Sinica,2012,38(2):285-292
[49]SANTOS M G,RIBEIRO R V,MACHADO E C,et al.Photosynthetic parameters and leaf water potential of five common bean genotypes under mild water deficit[J].Biologia Plantarum,2009,53(2):229-236
[50]VAVASSEUR A,RAGHAVENDRA A S.Guard cell metabolism and CO2 sensing[J].New Phytologist,2005,16:665-682
[51]ZHANG C,LI X,HE Y F,et al.Physiological investigation of C4-phosphoenolpyruvate-carboxylase-introduced rice line shows that sucrose metabolism is involved in the improved drought tolerance[J].Plant Physiology and Biochemistry,2017,115:328-342
[52]JENKINS C L D.Effects of the phosphoenolpyruvate carboxylase inhibitor 3,3-dichloro-2-(dihydroxy phosphinoyl methyl)propenoate on photosynthesis.C4 selectivity and studies on C4 photosynthesis[J].Plant Physiology,1989,89(4):1231-1237
[53]AGBARIAH K T,ROTHBEJERANO N.The effect of blue light on energy levels in epidermal strips[J].Physiologia Plantarum,1990,78(1):100-104
[54]TOMINAGA M,KINOSHITA T,SHIMAZAKI K.Guard-cell chloroplasts provide ATP required for H(10)pumping in the plasma membrane and stomatal opening[J].Plant&Cell Physiology,2001,42(8):795-802
[55]MENG L S,LI Y Q,LIU M Q,et al.The arabidopsis ANGUSTIFOLIA3-YODA gene cascade induces anthocyanin accumulation by regulating sucrose levels[J].Frontiers in Plant Science,2016,7:1728
[56]SAKAMOTO W,OHMORI T,KAGEYAMA K,et al.The purple leaf(Pl)locus of rice:The Pl(w)allele has a complex organization and includes two genes encoding basic helix-loop-helix proteins involved in anthocyanin biosynthesis[J].Plant&Cell Physiology,2001,42(9):982-991
[57]DONG W,NIU L L,GU J T,et al.Isolation of a WD40-repeat gene regulating anthocyanin biosynthesis in storage roots of purple-fleshed sweet potato[J].Acta Physiologiae Plantarum,2014,36(5):1123-1132
[58]TOSSI V,AMENTA M,LAMATTINA L,et al.Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway[J].Plant,Cell&Environment,2011,34(6):909-921
[59]YIN R H,SKVORTSOVA M Y,LOUBéRY S,et al.COP1 is required for UV-B-induced nuclear accumulation of the UVR8 photoreceptor[J].Proceedings of the National Academy of Sciences of the United States of America,2016,113(30):E4415-E4422
[60]SRIVASTAVA A K,SENAPATI D,SRIVASTAVA A,et al.Short hypocotyl in white light1 interacts with elongated hypocotyl5(HY5)and constitutive photomorphogenic1(COP1)and promotes COP1-mediated degradation of HY5 during arabidopsis seedling development[J].Plant Physiology,2015,169(4):2922-2934
[2]ZHU X G,LONG S P,ORT D R.Improving photosynthetic efficiency for greater yield[J].Annual Review of Plant Biology,2010,61:235-261
[3]KARKI S,RIZAL G,QUICK W P.Improvement of photosynthesis in rice(Oryza sativa L.)by inserting the C4 pathway[J].Rice,2013,6(1):28
[4]O′LEARY B,PARK J,PLAXTON W C.The remarkable diversity of plant PEPC(phosphoenolpyruvate carboxylase):recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs[J].Biochemical Journal,2011,436(1):15-34
[5]KU M S B,AGARIE S,NOMURA M,et al.High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants[J].Nature Biotechnology,1999,17:76-80
[6]JEANNEAU M,GERENTES D,FOUEILLASSAR X,et al.Improvement of drought tolerance in maize:towards the functional validation of the Zm-Asr1 gene and increase of water use efficiency by over-expressing C4-PEPC[J].Biochimie,2002,84:1127-1135
[7]JIAO D M,KUANG T Y,LI X,et al.Physiological characteristics of the primitive CO2 concentrating mechanism in PEPC transgenic rice[J].Science in China Series C:Life Sciences,2003,46(4):438-446
[8]BANDYOPADHYAY A,DATTA K,ZHANG J,et al.Enhanced photosynthesis rate in genetically engineered indica rice expressing PEPC gene cloned from maize[J].Plant Science,2007,172(6):1204-1209
[9]LIAN L,WANG X W,ZHU Y S,et al.Physiological and photosynthetic characteristics of indica Hang2 expressing the sugarcane PEPC gene[J].Molecular Biology Reports,2014,41:2189-2197
[10]REN C G,LI X,LIU X L,et al.Hydrogen peroxide regulated photosynthesis in C4-pepc transgenic rice[J].Plant Physiology and Biochemistry,2014,74:218-229
[11]DING Z S,SUN X F,HUANG S H,et al.Response of photosynthesis to short-term drought stress in rice seedlings overexpressing C4 phosphoenolpyruvate carboxylase from maize and millet[J].Photosynthetica,2015,53(4):481-488
[12]钱宝云,刘小龙,李霞.钙肥对不同内源钙含量水稻品种光合参数的影响[J].江苏农业学报,2014,30(3):467-473QIAN B Y,LIU X L,LI X.Photosynthesis of rice cultivars with various endogenous calcium contents in response to calcium fertilizer application[J].Jiangsu Journal of Agricultural Sciences,2014,30(3):467-473
[13]霍垲,陆巍,李霞.干旱胁迫下调节ATP的含量对提高转玉米C4型pepc水稻光合速率的影响[J].中国生态农业学报,2015,23(5):605-613HUO K,LU W,LI X.Effect of regulating ATP on improving photosynthetic rate of transgenic rice with overexpressing maize C4 pepc under drought stress[J].Chinese Journal of Eco-Agriculture,2015,23(5):605-613
[14]唐玉婷,李霞,陆巍,等.高表达转C4型PEPC基因水稻在低氮下诱导碳氮酶稳定光合作用[J].华北农学报,2015,30(4):95-100TANG Y T,LI X,LU W,et al.Transgenic rice with high expression of C4-PEPC genes induced higher carbon and nitrogen key enzyme to maintain photosynthesis under low nitrogen conditions[J].Acta Agriculturae Boreali-Sinica,2015,30(4):95-100
[15]JIAO D M,XIA L,HUANG X Q,et al.The characteristics of CO2 assimilation of photosynthesis and chlorophyll fluorescence in transgenic PEPC rice[J].Science Bulletin,2001,46(13):1080-1084
[16]DOUBNEROVáV,RY?LAVáH.What can enzymes of C4,photosynthesis do for C3,plants under stress?[J].Plant Science,2011,180(4):575-583
[17]JIAO D M,LI X,JI B H.Photoprotective effects of high level expression of C4,phosphoenolpyruvate carboxylase in transgenic rice during photoinhibition[J].Photosynthetica,2005,43(4):501-508
[18]李霞,任承钢.ABA、BA及DPI对高表达玉米C4 pepc基因的水稻光合特性及叶绿素荧光特性的影响[J].植物生理学报,2012,48(6):549-556LI X,REN C G.Effects on photosynthetic and fluorescence characteristics under treatments of ABA,BA or DPI in transgenic rice with over-expression C4-pepc gene[J].Plant Physiology Journal,2012,48(6):549-556
[19]LIU X,LI X,ZHANG C,et al.Phosphoenolpyruvate carboxylase regulation in C4-PEPC-expressing transgenic rice during early responses to drought stress[J].Physiologia Plantarum,2017,159(2):178-200
[20]HUO K,LI X,HE Y F,et al.Exogenous ATP enhance signal response of suspension cells of transgenic rice(Oryza sativa L.)expressing maize C4-pepc encoded phosphoenolpyruvate carboxylase under PEG treatment[J].Plant Growth Regulation,2016,82(1):55–67
[21]QIAN B Y,LI X,LIU X L,et al.Enhanced drought tolerance in transgenic rice over-expressing of maize C4 phosphoenolpyruvate carboxylase gene via NO and Ca2(10)[J].Journal of Plant Physiology,2015,175:9–20
[22]QIAN B Y,LI X,LIU X L,et al.Improved oxidative tolerance in suspension-cultured cells of C4-pepc transgenic rice by H2O2 and Ca2(10)under PEG-6000[J].Journal of Integrative Plant Biology,2015,57(6):534–549
[23]NAKASHIMA K,TRAN L S P,DONG V N,et al.Functional analysis of a NAC-type transcription factor Os NAC6 involved in abiotic and biotic stress-responsive gene expression in rice[J].Plant Journal,2007,51:617-630
[24]NIJHAWAN A,JAIN M,TYAGI A K,et al.Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice[J].Plant Physiology,2008,146(2):333-350
[25]HUANG G T,MA S L,BAI L P,et al.Signal transduction during cold,salt,and drought stresses in plants[J].Molecular Biology Reports,2012,39:969-987
[26]朱素琴,季本华,焦德茂.亚硫酸氢钠对转PEPC基因水稻叶片光合作用的促进作用[J].科技通报,2004,20(6):523-528ZHU S Q,JI B H,JIAO D M.Promotive effect of Na HSO3 on photosynthesis in PEPC transgenic rice leaves[J].Bulletin of Science and Technology,2004,20(6):523-528
[27]BISWAL A K,DILNAWAZ F,DAVID K A V,et al.Increase in the intensity of thermoluminescence Q-band during leaf ageing is due to a block in the electron transfer from QA to QB[J].Luminescence,2001,16(5):309-313
[28]SUZUKI K,OHMORI Y,RATEL E.High root temperature blocks both linear and cyclic electron transport in the dark during chilling of the leaves of rice seedlings[J].Plant and Cell Physiology,2011,52(9):1697-1707
[29]VAN DEN ENDE W,EL-ESAWE S K.Sucrose signaling pathways leading to fructan and anthocyanin accumulation:A dual function in abiotic and biotic stress responses?[J].Environmental and Experimental Botany,2014,108:4-13
[30]TENG S,KEURENTJES J,BENTSINK L,et al.Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene[J].Plant Physiology,2005,139(4):1840-1852
[31]SANYAL S K,PANDEY A,PANDEY G K.The CBL–CIPK signaling module in plants:a mechanistic perspective[J].Physiologia Plantarum,2015,155:89-108
[32]SHIN D H,CHOI M G,KANG C S,et al.A wheat R2R3-MYB protein PURPLE PLANT1(Ta PL1)functions as a positive regulator of anthocyanin biosynthesis[J].Biochemical&Biophysical Research Communications,2016,469(3):686-691
[33]YASUDA S,AOYAMA S,HASEGAWA Y,et al.Arabidopsis CBL-interacting protein kinases regulate carbon/nitrogen-nutrient response by phosphorylating ubiquitin ligase ATL31[J].Molecular Plant,2017,4(10):537-658
[34]SANYAL S K,KANWAR P,YADAV A K,et al.Arabidopsis CBL interacting protein kinase 3 interacts with ABR1,an APETALA2 domain transcription factor,to regulate ABA responses[J].Plant Science,2017,254:48-59
[35]YOSHIDA S,FORNO D A,COCK J H,et al.Laboratory Manual for Physiological Studies of Rice[M].Philippines:International Rice Research Institute,1976:61–64
[36]LI X,WANG C,REN C G.Effects of 1-butanol,neomycin and calcium on the photosynthetic characteristics of PEPC transgenic rice[J].African Journal of Biotechnology,2011,10:17466-17476
[37]AMBAVARAM M M R,BASU S,KRISHNAN A,et al.Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress[J].Nature Communications,2014,5:1-14
[38]RABINO I,MANCINELLI A L.Light,temperature,and anthocyanin production[J].Plant Physiology,1986,81(3):922-924
[39]MURPHY M E,NOACK E.Nitric oxide assay using hemoglobin method[J].Methods in Enzymology,1994,233:240–250
[40]YANG C Q,LIU W N,ZHAO Z H,et al.Determination of the content of serum calcium with methylthymol blue as chromogenic reagent[J].Spectroscopy&Spectral Analysis,1998,18:485–487
[41]JUNG H,KIM J K,HA S W.Use of animal viral IRES sequence makes multiple truncated transcripts without mediating polycistronic expression in rice[J].Journal of the Korean Society for Applied Biological Chemistry,2011,54:678–684
[42]CHEN P B,LI X,HUO K,et al.Promotion of photosynthesis in transgenic rice over-expressing of maize C4 phosphoenolpyruvate carboxylase gene by nitric oxide donors[J].Journal of Plant Physiology,2014,171:458–466
[43]JIA X H,ZHANG P P,SHI D J,et al.Regulation of PEPC gene expression in Anabaena sp.PCC 7120 and its effects on cyclic electron flow around photosystem I and tolerances to environmental stresses[J].Journal of Integrative Plant Biology,2015,57(5):468-476
[44]KEUNEN E,PESHEV D,VANGRONSVELD J,et al.Plant sugars are crucial players in the oxidative challenge during abiotic stress:extending the traditional concept[J].Plant Cell&Environment,2013,36(7):1242-1255
[45]LORETI E,POVERO G,NOVI G,et al.Gibberellins,jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis[J].New Phytologist,2008,179(4):1004-1016
[46]ZHANG Y C,GONG S F,LI Q H,et al.Functional and signaling mechanism analysis of rice CRYPTOCHROME 1[J].Plant Journal,2006,46(6):971-983
[47]SHIN D H,CHOI M,KIM K,et al.HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis[J].FEBS letters,2013,587(10):1543-1547
[48]丁在松,周宝元,孙雪芳,等.干旱胁迫下PEPC过表达增强水稻的耐强光能力[J].作物学报,2012,38(2):285-292DING Z S,ZHOU B Y,SUN X F,et al.High light tolerance is enhanced by overexpressed PEPC in rice under drought stress[J].Acta Agronomica Sinica,2012,38(2):285-292
[49]SANTOS M G,RIBEIRO R V,MACHADO E C,et al.Photosynthetic parameters and leaf water potential of five common bean genotypes under mild water deficit[J].Biologia Plantarum,2009,53(2):229-236
[50]VAVASSEUR A,RAGHAVENDRA A S.Guard cell metabolism and CO2 sensing[J].New Phytologist,2005,16:665-682
[51]ZHANG C,LI X,HE Y F,et al.Physiological investigation of C4-phosphoenolpyruvate-carboxylase-introduced rice line shows that sucrose metabolism is involved in the improved drought tolerance[J].Plant Physiology and Biochemistry,2017,115:328-342
[52]JENKINS C L D.Effects of the phosphoenolpyruvate carboxylase inhibitor 3,3-dichloro-2-(dihydroxy phosphinoyl methyl)propenoate on photosynthesis.C4 selectivity and studies on C4 photosynthesis[J].Plant Physiology,1989,89(4):1231-1237
[53]AGBARIAH K T,ROTHBEJERANO N.The effect of blue light on energy levels in epidermal strips[J].Physiologia Plantarum,1990,78(1):100-104
[54]TOMINAGA M,KINOSHITA T,SHIMAZAKI K.Guard-cell chloroplasts provide ATP required for H(10)pumping in the plasma membrane and stomatal opening[J].Plant&Cell Physiology,2001,42(8):795-802
[55]MENG L S,LI Y Q,LIU M Q,et al.The arabidopsis ANGUSTIFOLIA3-YODA gene cascade induces anthocyanin accumulation by regulating sucrose levels[J].Frontiers in Plant Science,2016,7:1728
[56]SAKAMOTO W,OHMORI T,KAGEYAMA K,et al.The purple leaf(Pl)locus of rice:The Pl(w)allele has a complex organization and includes two genes encoding basic helix-loop-helix proteins involved in anthocyanin biosynthesis[J].Plant&Cell Physiology,2001,42(9):982-991
[57]DONG W,NIU L L,GU J T,et al.Isolation of a WD40-repeat gene regulating anthocyanin biosynthesis in storage roots of purple-fleshed sweet potato[J].Acta Physiologiae Plantarum,2014,36(5):1123-1132
[58]TOSSI V,AMENTA M,LAMATTINA L,et al.Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway[J].Plant,Cell&Environment,2011,34(6):909-921
[59]YIN R H,SKVORTSOVA M Y,LOUBéRY S,et al.COP1 is required for UV-B-induced nuclear accumulation of the UVR8 photoreceptor[J].Proceedings of the National Academy of Sciences of the United States of America,2016,113(30):E4415-E4422
[60]SRIVASTAVA A K,SENAPATI D,SRIVASTAVA A,et al.Short hypocotyl in white light1 interacts with elongated hypocotyl5(HY5)and constitutive photomorphogenic1(COP1)and promotes COP1-mediated degradation of HY5 during arabidopsis seedling development[J].Plant Physiology,2015,169(4):2922-2934