乙烯参与钾对拟南芥缺铁响应的调控
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摘要
为了解乙烯是否作为信号分子参与钾对植物耐缺铁响应的调控,以拟南芥为研究材料,分析钾在调控植物缺铁响应过程中根中乙烯含量与缺铁响应的变化及其相互关系.结果表明:(1)与缺铁正常供钾(-Fe+K)相比,缺铁同时缺钾(-Fe-K)显著增加根中和根系质外体铁含量,降低植株地上部铁含量,加剧植株地上部缺铁,从而进一步增强根中铁还原酶活性,促进铁吸收相关基因表达.(2)在缺铁同时缺钾(-Fe-K)下添加不同浓度的钾则显著促进根系质外体铁的再利用,降低根中铁和根系质外体铁的含量,增加地上部铁含量,改善植株地上部铁营养状况,从而抑制根系铁还原酶活性.(3)与缺铁正常供钾(-Fe+K)相比,缺铁和缺钾共同胁迫(-Fe-K)显著增加根中乙烯含量,在-Fe+K和-Fe-K条件下外源添加乙烯合成前体均能进一步增加根中乙烯含量并增强铁还原酶活性,而外源添加乙烯合成抑制剂则进一步降低根中乙烯含量并抑制铁还原酶活性.(4)与对照相比,缺铁和缺钾共同胁迫(-Fe-K)下乙烯合成基因ACS4、ACS6和ACS7显著上调.本研究表明钾对拟南芥缺铁响应具有重要调控作用,ACS6、ACS4和ACS7基因介导合成的乙烯作为信号分子参与钾对拟南芥耐缺铁响应的调控.(图5表1参43)
To understand whether ethylene acts as a signal molecule involved in the regulation of potassium(K) on iron(Fe) deficiency-induced responses, the changes in ethylene levels and Fe deficiency responses and their relationship were analyzed under Fe and/or K deficiency stresses using Arabidopsis thaliana. The following results were obtained:(1) Fe and K deficiency(-Fe-K) significantly increased the Fe content both in the root and root apoplast, and decreased Fe content in the shoots, which aggravated the Fe deficiency in shoots, thus further increasing the ferric-chelate reductase(FCR) activity and Fe-uptake related gene expression as compared with Fe deficiency(-Fe+K).(2) Under Fe and K deficiency stress(-Fe-K), the exogenous application of various concentrations of K+ greatly promoted the reutilization of Fe in the root apoplast, hence the Fe content in both the root and root apoplast was decreased, which in turn increased the Fe content in the shoots, ameliorating the Fe deficiency in the shoots, and ultimately decreasing the FCR activity of the roots.(3) Ethylene levels were significantly higher in the roots of the-Fe-K treatment than in those of the-Fe+K treatment, and the exogenous application of the ethylene synthesis precursor greatly increased, whereas the ethylene synthesis inhibitor greatly decreased the FCR activity and ethylene levels under both Fe+K and-Fe-K stresses.(4) The higher accumulation of ethylene in the roots under Fe and K deficiency was accompanied by higher expression of ethylene synthesis genes ACS4, ACS6, and ACS7 compared to that in control. In conclusion, these results suggest that K plays an important role in the regulation of Fe-deficiency-induced responses, and ACS4,ACS6, and ACS7 mediate the accumulation of ethylene, which ultimately act as a signal molecule involved in the regulation of K on Fe-deficiency-induced responses.
To understand whether ethylene acts as a signal molecule involved in the regulation of potassium(K) on iron(Fe) deficiency-induced responses, the changes in ethylene levels and Fe deficiency responses and their relationship were analyzed under Fe and/or K deficiency stresses using Arabidopsis thaliana. The following results were obtained:(1) Fe and K deficiency(-Fe-K) significantly increased the Fe content both in the root and root apoplast, and decreased Fe content in the shoots, which aggravated the Fe deficiency in shoots, thus further increasing the ferric-chelate reductase(FCR) activity and Fe-uptake related gene expression as compared with Fe deficiency(-Fe+K).(2) Under Fe and K deficiency stress(-Fe-K), the exogenous application of various concentrations of K+ greatly promoted the reutilization of Fe in the root apoplast, hence the Fe content in both the root and root apoplast was decreased, which in turn increased the Fe content in the shoots, ameliorating the Fe deficiency in the shoots, and ultimately decreasing the FCR activity of the roots.(3) Ethylene levels were significantly higher in the roots of the-Fe-K treatment than in those of the-Fe+K treatment, and the exogenous application of the ethylene synthesis precursor greatly increased, whereas the ethylene synthesis inhibitor greatly decreased the FCR activity and ethylene levels under both Fe+K and-Fe-K stresses.(4) The higher accumulation of ethylene in the roots under Fe and K deficiency was accompanied by higher expression of ethylene synthesis genes ACS4, ACS6, and ACS7 compared to that in control. In conclusion, these results suggest that K plays an important role in the regulation of Fe-deficiency-induced responses, and ACS4,ACS6, and ACS7 mediate the accumulation of ethylene, which ultimately act as a signal molecule involved in the regulation of K on Fe-deficiency-induced responses.
引文
1 Ishimaru Y,Kim S,Tsukamoto T,Oki H,Kobayashi T,Watanabe S,Nishizawa NK.Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil[J].PNAS,2007,104(18):7373-7378
2陆景陵.植物营养学(上册)[M].北京:中国农业大学出版社,2003:261-263[Lu JL.Plant nutrition(volume One)[M].Beijing:China Agricultural University Press,2003:261-263]
3 Vose PB.Iron nutrition in plants:a world overview[J].J Plant Nutr,1982,5(4-7):233-249
4 Kabir AH,Rahman MM,Haider SA,Paul NK.Mechanisms associated with differential tolerance to Fe deficiency in okra(Abelmoschus esculentus Moench)[J].Environ Exp Bot,2015,112:16-26
5 Wang C,Yao X,Yu D,Liang G.Fe-deficiency-induced expression of bHLH104 enhances Fe-deficiency tolerance of Arabidopsis thaliana[J].Planta,2017,246(3):421-431
6 Hafsi C,Falleh H,Saada M,Ksouri R,Abdelly C.Potassium deficiency alters growth,photosynthetic performance,secondary metabolites content,and related antioxidant capacity in Sulla carnosa grown under moderate salinity[J].Plant Physiol Bioch,2017,118:609-617
7 Chen G,Feng H,Hu Q,Chen A,Yu L,Xu,G.Improving rice tolerance to potassium deficiency by enhancing OsHAK16:WOX11-controlled root development[J].Plant Biotechnol J,2015,13(6):833-848
8 Sakaguchi T,Nishizawa NK,Nakanishi H,Yoshimura E,Mori S.The role of Potassium in the secretion of mugineic acids family phytosiderophores from iron-deficient barley roots[J].Plant Soil,1999,215(2):221-227
9 Hughes DF,Jolley VD,Brown JC.Role for potassium in the iron-stress response mechanism of iron-efficient oat[J].Soil Sci Soc Am J,1992,56(3):830-835
10 Wang YH,Garvin DF,Kochian LV.Rapid induction of regulatory and transporter genes in response to phosphorus,potassium,and iron deficiencies in tomato roots.Evidence for cross talk and root/rhizosphere-mediated signals[J].Plant Physiol,2002,130(3):1361-1370
11 Nieves-Cordones M,Miller AJ,Alemán F,Martínez V,Rubio F.Aputative role for the plasma membrane potential in the control of the expression of the gene encoding the tomato high-affinity potassium transporter HAK5[J].Plant Mol Biol,2008,68(6):521
12 Ivanov R,Br umbarova T,Bauer P.Fitting into the harsh reality:regulation of iron-deficiency responses in dicotyledonous plants[J].Mol Plant,2012,5(1):27-42
13 Santi S,Schmidt W.Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots[J].New Phytol,2009,183(4):1072-1084
14 Walker EL,Connolly EL.Time to pump iron:iron-deficiency-signaling mechanisms of higher plants[J].Curr Opin Plant Biol,2008,11(5):530-535
15 Connolly EL,Campbell NH,Grotz N,Prichard CL,Guerinot ML.Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control[J].Plant Physiol,2003,133(3):1102-1110
16 Robinson NJ,Procter CM,Connolly EL,Guerinot ML.A ferric-chelate reductase for iron uptake from soils[J].Nature,1999,397:694-697
17 Vert G,Grotz N,Dédaldéchamp F,Gaymard F,Guerinot ML,Briat JF,Curie C.IRT1,an Arabidopsis transporter essential for iron uptake from the soil and for plant growth[J].Plant Cell,2002,14:1223-1233
18 Bauer P,Ling HQ,Guerinot ML.FIT,the FER-like iron deficiency induced transcription factor in Arabidopsis[J].Plant Physiol Biochem,2007,45(5):260-261
19 Hafsi C,Debez A,Abdelly C.Potassium deficiency in plants:effects and signaling cascades[J].Acta Physiol Plant,2014,36(5):1055-1070
20 Kim MJ,Ciani S,Schachtman DP.A peroxidase contributes to ROSproduction during Arabidopsis root response to potassium deficiency[J].Mol Plant,2010,3(2):420-427
21 Jung JY,Shin R,Schachtman DP.Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis[J].Plant Cell,2009,21(2):607-621
22 Chen WW,Yang JL,Qin C,Jin CW,Mo JH,Ye T,Zheng SJ.Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis thaliana[J].Plant Physiol,2010,154:810-819
23 García MJ,Suárez V,Romera FJ,Alcántara E,Pérez-Vicente R.A new model involving ethylene,nitric oxide and Fe to explain the regulation of Fe-acquisition genes in strategy I plants[J].Plant Physiol Bioch,2011,49(5):537-544
24 Merchante C,Alonso JM,Stepanova AN.Ethylene signaling:simple ligand,complex regulation[J].Curr Opin Plant Biol,2013,16(5):554-560
25 Iqbal N,Trivellini A,Masood A,Ferrante A,Khan NA.Current understanding on ethylene signaling in plants:the influence of nutrient availability[J].Plant Physiol Biochem,2013,73:128-138
26叶义全.蔗糖和一氧化氮对植物缺铁响应的调控作用及其机制[D].杭州:浙江大学,2015[Ye YQ.The roles and mechanisms of sucrose and nitric oxide in regulating plants iron-deficiency-induced response[D].Hangzhou:Zhejiang University,2015]
27何小林.铁、磷营养降低植物Cd积累的机制[D].杭州:浙江大学,2017[He XL.The mechanisms of Fe and P on decreasing cadmium accumulation in plants[D].Hangzhou:Zhejiang University,2017]
28 Grusak MA.Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L.(Fabaceae):relevance to the iron nutrition of developing seeds[J].Planta,1995,197(1):111-117
29 Tian QY,Sun P,Zhang WH.Ethylene is involved in nitrate-dependent root growth and branching in Arabidopsis thaliana[J].New Phytol,2009,184(4):918-931
30 Hughes DF,Jolley VD,Brown JC.Roles for potassium in the iron-stress response mechanisms of strategy I and strategy II plants[J].J Plant Nutr,1992,15(10):1821-1839
31 Jin CW,You GY,He YF,Tang C,Wu P,Zheng SJ.Iron deficiencyinduced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover[J].Plant Physiol,2007,144(1):278-285
32 Bienfait HF,Briel WVD,Mesland-Mul NT.Free space iron pools in roots:generation and mobilization[J].Plant Physiol,1985,78:596-600
33 Pavlovic J,Samardzic J,Maksimovi?V,Timotijevic G,Stevic N,Laursen KH,Nikolic M.Silicon alleviates iron deficiency in cucumber by promoting mobilization of iron in the root apoplast[J].New Phytol,2013,198(4):1096-1107
34 Zhang FS,Romheld V,Marschner H.Role of the toot apoplasm for Iron acquisition by wheat plants[J].Plant Physiol,1991,97:1302-1305
35 Lucena C,Waters BM,Romera FJ,García MJ,Morales M,Alcántara E,Pérez-Vicente R.Ethylene could inf luence ferric reductase,iron transporter,and H+-ATPase gene expression by affecting FER(or FER-like)gene activity[J].J Exp Bot,2006,57(15):4145-4154
36 Shin R,Schachtman DP.Hydrogen peroxide mediates plant root cell response to nutrient deprivation[J].P Natl Acad Sci USA,2004,101(23):8827-8832
37 Graziano M,Lamattina L.Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots[J].Plant J,2007,52(5):949-960
38徐昌杰,陈昆松.乙烯生物合成及其控制研究进展[J].植物学通报,1998,15(S):54-61[Xu CJ,Chen KS.Advances in ethylene biosynthesis and its control[J].Chin Bull Bot,1998,15(S):54-61]
39王爱勤,王自章,杨丽涛,韦宇拓,李杨瑞.乙烯生物合成途径中的两个关键酶基因的研究进展[J].广西农业生物科学,2004,23(2):164-169[Wang AQ,Wang ZZ,Yang LP,Wei YT,Li YR.Research progress of two key enzyme genes on the ethylene biosynthesis[J].J Guangxi Agric Biol Sci,2004,23(2):164-169]
40 Yamagami T,Tsuchisaka A,Yamada K,Haddon WF,Harden LA,Theologis A.Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family[J].J Biol Chem,2003,278(49):49102-49112
41 Liu M,Liu XX,He XL,Liu LJ,Wu H,Tang CX,Jin CW.Ethylene and nitric oxide interact to regulate the magnesium deficiency-induced root hair development in Arabidopsis[J].New Phytol,2017,213(3):1242-1256
42 Schellingen K,Van Der Straeten D,Vandenbussche F,Prinsen E,Remans T,Vangronsveld J,Cuypers A.Cadmium-induced ethylene production and responses in Arabidopsis thaliana rely on ACS2 and ACS6 gene expression[J].BMC Plant Biol,2014,14(1):214-227
43陈新建,刘国顺,陈占宽,郅玉宝,易明林,刘鸿先.乙烯生物合成途径及其相关基因工程的研究进展[J].热带亚热带植物学报,2002,10(1):83-98[Chen XJ,Liu GS,Chen ZK,Zhi YB,Yi ML,Liu HX.Areview of the pathway of ethylene biosynthesis and the relevant genetic engineering[J].J Trop Subtrop Bot,2002,10(1):83-98]
2陆景陵.植物营养学(上册)[M].北京:中国农业大学出版社,2003:261-263[Lu JL.Plant nutrition(volume One)[M].Beijing:China Agricultural University Press,2003:261-263]
3 Vose PB.Iron nutrition in plants:a world overview[J].J Plant Nutr,1982,5(4-7):233-249
4 Kabir AH,Rahman MM,Haider SA,Paul NK.Mechanisms associated with differential tolerance to Fe deficiency in okra(Abelmoschus esculentus Moench)[J].Environ Exp Bot,2015,112:16-26
5 Wang C,Yao X,Yu D,Liang G.Fe-deficiency-induced expression of bHLH104 enhances Fe-deficiency tolerance of Arabidopsis thaliana[J].Planta,2017,246(3):421-431
6 Hafsi C,Falleh H,Saada M,Ksouri R,Abdelly C.Potassium deficiency alters growth,photosynthetic performance,secondary metabolites content,and related antioxidant capacity in Sulla carnosa grown under moderate salinity[J].Plant Physiol Bioch,2017,118:609-617
7 Chen G,Feng H,Hu Q,Chen A,Yu L,Xu,G.Improving rice tolerance to potassium deficiency by enhancing OsHAK16:WOX11-controlled root development[J].Plant Biotechnol J,2015,13(6):833-848
8 Sakaguchi T,Nishizawa NK,Nakanishi H,Yoshimura E,Mori S.The role of Potassium in the secretion of mugineic acids family phytosiderophores from iron-deficient barley roots[J].Plant Soil,1999,215(2):221-227
9 Hughes DF,Jolley VD,Brown JC.Role for potassium in the iron-stress response mechanism of iron-efficient oat[J].Soil Sci Soc Am J,1992,56(3):830-835
10 Wang YH,Garvin DF,Kochian LV.Rapid induction of regulatory and transporter genes in response to phosphorus,potassium,and iron deficiencies in tomato roots.Evidence for cross talk and root/rhizosphere-mediated signals[J].Plant Physiol,2002,130(3):1361-1370
11 Nieves-Cordones M,Miller AJ,Alemán F,Martínez V,Rubio F.Aputative role for the plasma membrane potential in the control of the expression of the gene encoding the tomato high-affinity potassium transporter HAK5[J].Plant Mol Biol,2008,68(6):521
12 Ivanov R,Br umbarova T,Bauer P.Fitting into the harsh reality:regulation of iron-deficiency responses in dicotyledonous plants[J].Mol Plant,2012,5(1):27-42
13 Santi S,Schmidt W.Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots[J].New Phytol,2009,183(4):1072-1084
14 Walker EL,Connolly EL.Time to pump iron:iron-deficiency-signaling mechanisms of higher plants[J].Curr Opin Plant Biol,2008,11(5):530-535
15 Connolly EL,Campbell NH,Grotz N,Prichard CL,Guerinot ML.Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control[J].Plant Physiol,2003,133(3):1102-1110
16 Robinson NJ,Procter CM,Connolly EL,Guerinot ML.A ferric-chelate reductase for iron uptake from soils[J].Nature,1999,397:694-697
17 Vert G,Grotz N,Dédaldéchamp F,Gaymard F,Guerinot ML,Briat JF,Curie C.IRT1,an Arabidopsis transporter essential for iron uptake from the soil and for plant growth[J].Plant Cell,2002,14:1223-1233
18 Bauer P,Ling HQ,Guerinot ML.FIT,the FER-like iron deficiency induced transcription factor in Arabidopsis[J].Plant Physiol Biochem,2007,45(5):260-261
19 Hafsi C,Debez A,Abdelly C.Potassium deficiency in plants:effects and signaling cascades[J].Acta Physiol Plant,2014,36(5):1055-1070
20 Kim MJ,Ciani S,Schachtman DP.A peroxidase contributes to ROSproduction during Arabidopsis root response to potassium deficiency[J].Mol Plant,2010,3(2):420-427
21 Jung JY,Shin R,Schachtman DP.Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis[J].Plant Cell,2009,21(2):607-621
22 Chen WW,Yang JL,Qin C,Jin CW,Mo JH,Ye T,Zheng SJ.Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis thaliana[J].Plant Physiol,2010,154:810-819
23 García MJ,Suárez V,Romera FJ,Alcántara E,Pérez-Vicente R.A new model involving ethylene,nitric oxide and Fe to explain the regulation of Fe-acquisition genes in strategy I plants[J].Plant Physiol Bioch,2011,49(5):537-544
24 Merchante C,Alonso JM,Stepanova AN.Ethylene signaling:simple ligand,complex regulation[J].Curr Opin Plant Biol,2013,16(5):554-560
25 Iqbal N,Trivellini A,Masood A,Ferrante A,Khan NA.Current understanding on ethylene signaling in plants:the influence of nutrient availability[J].Plant Physiol Biochem,2013,73:128-138
26叶义全.蔗糖和一氧化氮对植物缺铁响应的调控作用及其机制[D].杭州:浙江大学,2015[Ye YQ.The roles and mechanisms of sucrose and nitric oxide in regulating plants iron-deficiency-induced response[D].Hangzhou:Zhejiang University,2015]
27何小林.铁、磷营养降低植物Cd积累的机制[D].杭州:浙江大学,2017[He XL.The mechanisms of Fe and P on decreasing cadmium accumulation in plants[D].Hangzhou:Zhejiang University,2017]
28 Grusak MA.Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L.(Fabaceae):relevance to the iron nutrition of developing seeds[J].Planta,1995,197(1):111-117
29 Tian QY,Sun P,Zhang WH.Ethylene is involved in nitrate-dependent root growth and branching in Arabidopsis thaliana[J].New Phytol,2009,184(4):918-931
30 Hughes DF,Jolley VD,Brown JC.Roles for potassium in the iron-stress response mechanisms of strategy I and strategy II plants[J].J Plant Nutr,1992,15(10):1821-1839
31 Jin CW,You GY,He YF,Tang C,Wu P,Zheng SJ.Iron deficiencyinduced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover[J].Plant Physiol,2007,144(1):278-285
32 Bienfait HF,Briel WVD,Mesland-Mul NT.Free space iron pools in roots:generation and mobilization[J].Plant Physiol,1985,78:596-600
33 Pavlovic J,Samardzic J,Maksimovi?V,Timotijevic G,Stevic N,Laursen KH,Nikolic M.Silicon alleviates iron deficiency in cucumber by promoting mobilization of iron in the root apoplast[J].New Phytol,2013,198(4):1096-1107
34 Zhang FS,Romheld V,Marschner H.Role of the toot apoplasm for Iron acquisition by wheat plants[J].Plant Physiol,1991,97:1302-1305
35 Lucena C,Waters BM,Romera FJ,García MJ,Morales M,Alcántara E,Pérez-Vicente R.Ethylene could inf luence ferric reductase,iron transporter,and H+-ATPase gene expression by affecting FER(or FER-like)gene activity[J].J Exp Bot,2006,57(15):4145-4154
36 Shin R,Schachtman DP.Hydrogen peroxide mediates plant root cell response to nutrient deprivation[J].P Natl Acad Sci USA,2004,101(23):8827-8832
37 Graziano M,Lamattina L.Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots[J].Plant J,2007,52(5):949-960
38徐昌杰,陈昆松.乙烯生物合成及其控制研究进展[J].植物学通报,1998,15(S):54-61[Xu CJ,Chen KS.Advances in ethylene biosynthesis and its control[J].Chin Bull Bot,1998,15(S):54-61]
39王爱勤,王自章,杨丽涛,韦宇拓,李杨瑞.乙烯生物合成途径中的两个关键酶基因的研究进展[J].广西农业生物科学,2004,23(2):164-169[Wang AQ,Wang ZZ,Yang LP,Wei YT,Li YR.Research progress of two key enzyme genes on the ethylene biosynthesis[J].J Guangxi Agric Biol Sci,2004,23(2):164-169]
40 Yamagami T,Tsuchisaka A,Yamada K,Haddon WF,Harden LA,Theologis A.Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family[J].J Biol Chem,2003,278(49):49102-49112
41 Liu M,Liu XX,He XL,Liu LJ,Wu H,Tang CX,Jin CW.Ethylene and nitric oxide interact to regulate the magnesium deficiency-induced root hair development in Arabidopsis[J].New Phytol,2017,213(3):1242-1256
42 Schellingen K,Van Der Straeten D,Vandenbussche F,Prinsen E,Remans T,Vangronsveld J,Cuypers A.Cadmium-induced ethylene production and responses in Arabidopsis thaliana rely on ACS2 and ACS6 gene expression[J].BMC Plant Biol,2014,14(1):214-227
43陈新建,刘国顺,陈占宽,郅玉宝,易明林,刘鸿先.乙烯生物合成途径及其相关基因工程的研究进展[J].热带亚热带植物学报,2002,10(1):83-98[Chen XJ,Liu GS,Chen ZK,Zhi YB,Yi ML,Liu HX.Areview of the pathway of ethylene biosynthesis and the relevant genetic engineering[J].J Trop Subtrop Bot,2002,10(1):83-98]