水稻响应缺铁的韧皮部汁液蛋白质组学分析
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摘要
为鉴定水稻(Oryzasativa)响应缺铁的根冠长距离信号转导物质,采用TMT标记技术分析了不同浓度铁处理下水稻韧皮部汁液的蛋白质组学变化,共鉴定出206个差异蛋白,其中54个蛋白表达丰度上调,152个蛋白表达丰度下调。差异蛋白的KEGG通路分类主要包括激素信号代谢、谷胱甘肽代谢、碳代谢以及mRNA转运等代谢途径。此外,对差异蛋白对应的生理指标进行测定,发现激素、蔗糖、谷胱甘肽和转运蛋白等在缺铁条件下变化显著,后续对这些差异蛋白的功能研究有助于揭示水稻响应铁素营养的长距离信号途径。
In order to identify long-distance signals under iron(Fe) deficiency in rice(Oryza sativa), TMT label technique was used to study the protein profile of phloem sap under different iron concentrations. A total of 206 differentially expressed proteins were identified: 54 were upregulated and 152 were downregulated. Most of these proteins are involved in hormone signal transduction, carbon metabolism, glutathione metabolism and mRNA transport. In addition, we measured the physiological indicators according to the differentially expressed proteins. It was found that phytohormones, sucrose, glutathione and transporters were significantly changed under iron deficiency. To further study the function of these proteins can help to reveal the long distance signaling pathway of rice in response to Fe deficiency.
In order to identify long-distance signals under iron(Fe) deficiency in rice(Oryza sativa), TMT label technique was used to study the protein profile of phloem sap under different iron concentrations. A total of 206 differentially expressed proteins were identified: 54 were upregulated and 152 were downregulated. Most of these proteins are involved in hormone signal transduction, carbon metabolism, glutathione metabolism and mRNA transport. In addition, we measured the physiological indicators according to the differentially expressed proteins. It was found that phytohormones, sucrose, glutathione and transporters were significantly changed under iron deficiency. To further study the function of these proteins can help to reveal the long distance signaling pathway of rice in response to Fe deficiency.
引文
傅友强,梁建平,于智卫,吴道铭,蔡昆争,沈宏(2011).不同铁形态对水稻根表铁膜及铁吸收的影响.植物营养与肥料学报17,1050-1057.
吴慧兰,王宁,凌宏清(2007).植物铁吸收、转运和调控的分子机制研究进展.植物学通报24,779-788.
熊长明,王晔,田晓莉(2014).植物矿质养分吸收的长距离反馈调节研究进展.植物营养与肥料学报20,737-746.
邹春琴,陈新平,张福锁,毛达如(1998).活性铁作为植物铁营养状况诊断指标的相关研究.植物营养与肥料学报4,399-406.
Agarwala SC,Sharma CP(1961).The relation of iron supply to the tissue concentration of iron,chlorophyll and catalase in barley plants grown in sand culture.Physiol Plant 14,275-283.
Aoyama T,Kobayashi T,Takahashi M,Nagasaka S,Usuda K,Kakei Y,Ishimaru Y,Nakanishi H,Mori S,Nishizawa NK(2009).Os YSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints.Plant Mol Biol70,681-692.
Bao F,Li JY(2002).Evidence that the auxin signaling pathway interacts with plant stress response.Acta Bot Sin 44,532-536.
Bashir K,Nagasaka S,Itai RN,Kobayashi T,Takahashi M,Nakanishi H,Mori S,Nishizawa NK(2007).Expression and enzyme activity of glutathione reductase is upregulated by Fe-deficiency in graminaceous plants.Plant Mol Biol 65,277-284.
Brown JC,Chaney RL(1971).Effect of iron on the transport of citrate into the xylem of soybeans and tomatoes.Plant Physiol 47,836-840.
Chen L,Ding CQ,Zhao XF,Xu JX,Mohammad AA,Wang SH,Ding YF(2015).Differential regulation of proteins in rice(Oryza sativa L.)under iron deficiency.Plant Cell Rep34,83-96.
Chen L,Wang GP,Chen PF,Zhu HL,Wang SH,Ding YF(2018a).Shoot-root communication plays a key role in physiological alterations of rice(Oryza sativa)under iron deficiency.Front Plant Sci 9,757.
Chen PF,Chen L,Jiang ZR,Wang GP,Wang SH,Ding YF(2018b).Sucrose is involved in the regulation of iron deficiency responses in rice(Oryza sativa L.).Plant Cell Rep37,789-798.
Cheng LJ,Wang F,Shou HX,Huang FL,Zheng LQ,He F,Li JH,Zhao FJ,Ueno D,Ma JF,Wu P(2007).Mutation in nicotianamine aminotransferase stimulated the Fe(II)acquisition system and led to iron accumulation in rice.Plant Physiol 145,1647-1657.
Connolly EL,Campbell N,Grotz N,Prichard CL,Guerinot ML(2003).Overexpression of the FRO2 iron reductase confers tolerance to growth on low iron and uncovers post-transcriptional control.Plant Physiol 133,1102-1110.
Curie C,Cassin G,Counch D,Divol F,Higuchi K,Jean ML,Misson J,Schikora A,Czernic P,Mari S(2009).Metal movement within the plant:contribution of nicotianamine and yellow stripe 1-like transporters.Ann Bot103,1-11.
Curie C,Panaviene Z,Loulergue C,Dellaporta SL,Briat JF,Walker EL(2001).Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III)uptake.Nature 409,346-349.
Dean M,Hamon Y,Chimini G(2001).The human ATP-binding cassette(ABC)transporter superfamily.J Lipid Res 42,1007-1017.
Dong J,Pi?eros MA,Li X,Yang H,Liu Y,Murphy AS,Kochian LV,Liu D(2017).An Arabidopsis ABC transporter mediates phosphate deficiency-induced remodeling of root architecture by modulating iron homeostasis in roots.Mol Plant 10,244-259.
Eide D,Broderius M,Fett J,Guerinot ML(1996).A novel iron-regulated metal transporter from plants identified by functional expression in yeast.Proc Natl Acad Sci USA 93,5624-5628.
Enomoto Y,Hodoshima H,Shimada H,Shoji K,Yoshihara T,Goto F(2007).Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots.Planta 227,81-89.
Espen L,Dell'Orto M,Nisi PD,Zocchi G(2000).Metabolic responses in cucumber(Cucumis sativus L.)roots under Fe-deficiency:a 31P-nuclear magnetic resonance in-vivo study.Planta 210,985-992.
Falka J,Andersena G,Kernebeckb B,Krupinskaa K(2003).Constitutive overexpression of barley 4-hydroxyp henylpyruvate dioxygenase in tobacco results in elevation of the vitamin E content in seeds but not in leaves.FEBSLett 540,35-40.
Forde BG(2002).The role of long-distance signaling in plant responses to nitrate and other nutrients.J Exp Bot 53,39-43.
García MJ,Romera FJ,Stacey MG,Stacey G,Villar E,Alcántara E,Pérez-Vicente R(2013).Shoot to root communication is necessary to control the expression of ironacquisition genes in Strategy I plants.Planta 237,65-75.
Green LS,Rogers EE(2004).FRD3 controls iron localization in Arabidopsis.Plant Physiol 136,2523-2531.
Hagen G,Uhrhammer N,Guilfoyle TJ(1988).Regulation of expression of an auxin-induced soybean sequence by cadmium.J Biol Chem 263,6442-6446.
Haydon MJ,Cobbett CS(2007).Transporters of ligands for essential metal ions in plants.New Phytol 174,499-506.
Hell R,Stephan UW(2003).Iron uptake,trafficking and homeostasis in plants.Planta 216,541-551.
Hindt MN,Guerinot ML(2012).Getting a sense for signals:regulation of the plant iron deficiency response.Biochim Biophys Acta 1823,1521-1530.
Inoue H,Kobayashi T,Nozoye T,Takahashi M,Kakei Y,Suzuki K,Nakazono M,Nakanishi H,Mori S,Nishizawa NK(2009).Rice Os YSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings.J Biol Chem 284,3470-3479.
Ishimaru Y,Kim SA,Tsukamoto T,Oki H,Kobayashi T,Watanabe S,Matsuhashi S,Takahashi M,Nakanishi H,Mori S,Nishizawa NK(2007).Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil.Proc Natl Acad Sci USA 104,7373-7378.
Ishimaru Y,Suzuki M,Tsukamoto T,Suzuki K,Nakazono M,Kobayashi T,Wada Y,Watanabe S,Matsuhashi S,Takahashi M,Nakanishi H,Mori S,Nishizawa NK(2006).Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+.Plant J 45,335-346.
Jiang CF,Gao XH,Liao LL,Harberd NP,Fu XD(2007).Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellinDELLA signaling pathway in Arabidopsis.Plant Physiol145,1460-1470.
Kakei Y,Yamaguchi I,Kobayashi T,Takahashi M,Nakanishi H,Yamakawa T,Nishizawa NK(2009).A highly sensitive,quick and simple quantification method for nicotianamine and 2’-deoxymugineic acid from minimum samples using LC/ESI-TOF-MS achieves functional analysis of these components in plants.Plant Cell Physiol 50,1988-1993.
Kerk D,Bulgrien J,Smith DW,Barsam B,Veretnik S,Gribskov M(2002).The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis.Plant Physiol 129,908-925.
Lee S,Chiecko JC,Kim SA,Walker EL,Lee Y,Guerinot ML,An G(2009).Disruption of OsYSL15 leads to iron inefficiency in rice plants.Plant Physiol 150,786-800.
Lei GJ,Zhu XF,Wang ZW,Dong F,Dong NY,Zheng SJ(2014).Abscisic acid alleviates iron deficiency by promoting root iron reutilization and transport from root to shoot in Arabidopsis.Plant Cell Environ 37,852-863.
Li J,Wu XD,Hao ST,Wang XJ,Ling HQ(2008).Proteomic response to iron deficiency in tomato root.Proteomics 8,2299-2311.
Liu KD,Yue RQ,Yuan CC,Liu JX,Zhang L,Sun T,Yang YJ,Tie SG,Shen CJ(2015).Auxin signaling is involved in iron deficiency-induced photosynthetic inhibition and shoot growth defect in rice(Oryza sativa L.).J Plant Biol 58,391-401.
López-Millán AF,Morales F,Andaluz S,Gogorcena Y,Abadía A,De Las Rivas J,Abadía J(2000).Responses of sugar beet roots to iron deficiency.Changes in carbon assimilation and oxygen use.Plant Physiol 124,885-897.
Lucas WJ,Groover A,Lichtenberger R,Furuta K,Yadav SR,Helariutta Y,He XQ,Fukuda H,Kang JL,Brady SM,Patrick JW,Sperry J,Yoshida A,López-Millán AF,Grusak MA,Kachroo P(2013).The plant vascular system:evolution,development and functions.J Integr Plant Biol 55,294-388.
Lucas WJ,Yoo BC,Kragler F(2001).RNA as a longdistance information macromolecule in plants.Nat Rev Mol Cell Biol 2,849-857.
Majerus V,Bertin P,Lutts S(2009).Abscisic acid and oxidative stress implications in overall ferritin synthesis by African rice(Oryza glaberrima Steud.)seedlings exposed to short term iron toxicity.Plant Soil 324,253-265.
Matsuoka K,Furukawa J,Bidadi H,Asahina M,Yamaguchi S,Satoh S(2014).Gibberellin-induced expression of Fe uptake-related genes in Arabidopsis.Plant Cell Physiol 55,87-98.
Mol PC,Park HM,Mullins JT,Cabib E(1994).A GTP-binding protein regulates the activity of(1→3)-β-glucan synthase,an enzyme directly involved in yeast cell wall morphogenesis.J Biol Chem 269,31267-31274.
Negishi T,Nakanishi H,Yazaki J,Kishimoto N,Fujii F,Shimbo K,Yamamoto K,Sakata K,Sasaki T,Kikuchi S,Mori S,Nishizawa NK(2002).cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore secretion in Fe-deficient barley roots.Plant J 30,83-94.
Nguyen VNT,Moon S,Jung KH(2014).Genome-wide expression analysis of rice ABC transporter family across spatio-temporal samples and in response to abiotic stressses.J Plant Physiol 171,1276-1288.
Qi YH,Wang SK,Shen CJ,Zhang SN,Chen Y,Xu YX,Liu Y,Wu YR,Jiang DA(2012).Os ARF12,a transcription activator on auxin response gene,regulates root elongation and affects iron accumulation in rice(Oryza sativa).New Phytol 193,109-120.
Robinson NJ,Procter CM,Connolly EL,Guerinot ML(1999).A ferric-chelate reductase for iron uptake from soils.Nature 397,694-697.
Shanmugam V,Wang YW,Tsednee M,Karunakaran K,Yeh KC(2015).Glutathione plays an essential role in nitric oxide-mediated iron-deficiency signaling and iron-deficiency tolerance in Arabidopsis.Plant J 84,464-477.
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吴慧兰,王宁,凌宏清(2007).植物铁吸收、转运和调控的分子机制研究进展.植物学通报24,779-788.
熊长明,王晔,田晓莉(2014).植物矿质养分吸收的长距离反馈调节研究进展.植物营养与肥料学报20,737-746.
邹春琴,陈新平,张福锁,毛达如(1998).活性铁作为植物铁营养状况诊断指标的相关研究.植物营养与肥料学报4,399-406.
Agarwala SC,Sharma CP(1961).The relation of iron supply to the tissue concentration of iron,chlorophyll and catalase in barley plants grown in sand culture.Physiol Plant 14,275-283.
Aoyama T,Kobayashi T,Takahashi M,Nagasaka S,Usuda K,Kakei Y,Ishimaru Y,Nakanishi H,Mori S,Nishizawa NK(2009).Os YSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints.Plant Mol Biol70,681-692.
Bao F,Li JY(2002).Evidence that the auxin signaling pathway interacts with plant stress response.Acta Bot Sin 44,532-536.
Bashir K,Nagasaka S,Itai RN,Kobayashi T,Takahashi M,Nakanishi H,Mori S,Nishizawa NK(2007).Expression and enzyme activity of glutathione reductase is upregulated by Fe-deficiency in graminaceous plants.Plant Mol Biol 65,277-284.
Brown JC,Chaney RL(1971).Effect of iron on the transport of citrate into the xylem of soybeans and tomatoes.Plant Physiol 47,836-840.
Chen L,Ding CQ,Zhao XF,Xu JX,Mohammad AA,Wang SH,Ding YF(2015).Differential regulation of proteins in rice(Oryza sativa L.)under iron deficiency.Plant Cell Rep34,83-96.
Chen L,Wang GP,Chen PF,Zhu HL,Wang SH,Ding YF(2018a).Shoot-root communication plays a key role in physiological alterations of rice(Oryza sativa)under iron deficiency.Front Plant Sci 9,757.
Chen PF,Chen L,Jiang ZR,Wang GP,Wang SH,Ding YF(2018b).Sucrose is involved in the regulation of iron deficiency responses in rice(Oryza sativa L.).Plant Cell Rep37,789-798.
Cheng LJ,Wang F,Shou HX,Huang FL,Zheng LQ,He F,Li JH,Zhao FJ,Ueno D,Ma JF,Wu P(2007).Mutation in nicotianamine aminotransferase stimulated the Fe(II)acquisition system and led to iron accumulation in rice.Plant Physiol 145,1647-1657.
Connolly EL,Campbell N,Grotz N,Prichard CL,Guerinot ML(2003).Overexpression of the FRO2 iron reductase confers tolerance to growth on low iron and uncovers post-transcriptional control.Plant Physiol 133,1102-1110.
Curie C,Cassin G,Counch D,Divol F,Higuchi K,Jean ML,Misson J,Schikora A,Czernic P,Mari S(2009).Metal movement within the plant:contribution of nicotianamine and yellow stripe 1-like transporters.Ann Bot103,1-11.
Curie C,Panaviene Z,Loulergue C,Dellaporta SL,Briat JF,Walker EL(2001).Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III)uptake.Nature 409,346-349.
Dean M,Hamon Y,Chimini G(2001).The human ATP-binding cassette(ABC)transporter superfamily.J Lipid Res 42,1007-1017.
Dong J,Pi?eros MA,Li X,Yang H,Liu Y,Murphy AS,Kochian LV,Liu D(2017).An Arabidopsis ABC transporter mediates phosphate deficiency-induced remodeling of root architecture by modulating iron homeostasis in roots.Mol Plant 10,244-259.
Eide D,Broderius M,Fett J,Guerinot ML(1996).A novel iron-regulated metal transporter from plants identified by functional expression in yeast.Proc Natl Acad Sci USA 93,5624-5628.
Enomoto Y,Hodoshima H,Shimada H,Shoji K,Yoshihara T,Goto F(2007).Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots.Planta 227,81-89.
Espen L,Dell'Orto M,Nisi PD,Zocchi G(2000).Metabolic responses in cucumber(Cucumis sativus L.)roots under Fe-deficiency:a 31P-nuclear magnetic resonance in-vivo study.Planta 210,985-992.
Falka J,Andersena G,Kernebeckb B,Krupinskaa K(2003).Constitutive overexpression of barley 4-hydroxyp henylpyruvate dioxygenase in tobacco results in elevation of the vitamin E content in seeds but not in leaves.FEBSLett 540,35-40.
Forde BG(2002).The role of long-distance signaling in plant responses to nitrate and other nutrients.J Exp Bot 53,39-43.
García MJ,Romera FJ,Stacey MG,Stacey G,Villar E,Alcántara E,Pérez-Vicente R(2013).Shoot to root communication is necessary to control the expression of ironacquisition genes in Strategy I plants.Planta 237,65-75.
Green LS,Rogers EE(2004).FRD3 controls iron localization in Arabidopsis.Plant Physiol 136,2523-2531.
Hagen G,Uhrhammer N,Guilfoyle TJ(1988).Regulation of expression of an auxin-induced soybean sequence by cadmium.J Biol Chem 263,6442-6446.
Haydon MJ,Cobbett CS(2007).Transporters of ligands for essential metal ions in plants.New Phytol 174,499-506.
Hell R,Stephan UW(2003).Iron uptake,trafficking and homeostasis in plants.Planta 216,541-551.
Hindt MN,Guerinot ML(2012).Getting a sense for signals:regulation of the plant iron deficiency response.Biochim Biophys Acta 1823,1521-1530.
Inoue H,Kobayashi T,Nozoye T,Takahashi M,Kakei Y,Suzuki K,Nakazono M,Nakanishi H,Mori S,Nishizawa NK(2009).Rice Os YSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings.J Biol Chem 284,3470-3479.
Ishimaru Y,Kim SA,Tsukamoto T,Oki H,Kobayashi T,Watanabe S,Matsuhashi S,Takahashi M,Nakanishi H,Mori S,Nishizawa NK(2007).Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil.Proc Natl Acad Sci USA 104,7373-7378.
Ishimaru Y,Suzuki M,Tsukamoto T,Suzuki K,Nakazono M,Kobayashi T,Wada Y,Watanabe S,Matsuhashi S,Takahashi M,Nakanishi H,Mori S,Nishizawa NK(2006).Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+.Plant J 45,335-346.
Jiang CF,Gao XH,Liao LL,Harberd NP,Fu XD(2007).Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellinDELLA signaling pathway in Arabidopsis.Plant Physiol145,1460-1470.
Kakei Y,Yamaguchi I,Kobayashi T,Takahashi M,Nakanishi H,Yamakawa T,Nishizawa NK(2009).A highly sensitive,quick and simple quantification method for nicotianamine and 2’-deoxymugineic acid from minimum samples using LC/ESI-TOF-MS achieves functional analysis of these components in plants.Plant Cell Physiol 50,1988-1993.
Kerk D,Bulgrien J,Smith DW,Barsam B,Veretnik S,Gribskov M(2002).The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis.Plant Physiol 129,908-925.
Lee S,Chiecko JC,Kim SA,Walker EL,Lee Y,Guerinot ML,An G(2009).Disruption of OsYSL15 leads to iron inefficiency in rice plants.Plant Physiol 150,786-800.
Lei GJ,Zhu XF,Wang ZW,Dong F,Dong NY,Zheng SJ(2014).Abscisic acid alleviates iron deficiency by promoting root iron reutilization and transport from root to shoot in Arabidopsis.Plant Cell Environ 37,852-863.
Li J,Wu XD,Hao ST,Wang XJ,Ling HQ(2008).Proteomic response to iron deficiency in tomato root.Proteomics 8,2299-2311.
Liu KD,Yue RQ,Yuan CC,Liu JX,Zhang L,Sun T,Yang YJ,Tie SG,Shen CJ(2015).Auxin signaling is involved in iron deficiency-induced photosynthetic inhibition and shoot growth defect in rice(Oryza sativa L.).J Plant Biol 58,391-401.
López-Millán AF,Morales F,Andaluz S,Gogorcena Y,Abadía A,De Las Rivas J,Abadía J(2000).Responses of sugar beet roots to iron deficiency.Changes in carbon assimilation and oxygen use.Plant Physiol 124,885-897.
Lucas WJ,Groover A,Lichtenberger R,Furuta K,Yadav SR,Helariutta Y,He XQ,Fukuda H,Kang JL,Brady SM,Patrick JW,Sperry J,Yoshida A,López-Millán AF,Grusak MA,Kachroo P(2013).The plant vascular system:evolution,development and functions.J Integr Plant Biol 55,294-388.
Lucas WJ,Yoo BC,Kragler F(2001).RNA as a longdistance information macromolecule in plants.Nat Rev Mol Cell Biol 2,849-857.
Majerus V,Bertin P,Lutts S(2009).Abscisic acid and oxidative stress implications in overall ferritin synthesis by African rice(Oryza glaberrima Steud.)seedlings exposed to short term iron toxicity.Plant Soil 324,253-265.
Matsuoka K,Furukawa J,Bidadi H,Asahina M,Yamaguchi S,Satoh S(2014).Gibberellin-induced expression of Fe uptake-related genes in Arabidopsis.Plant Cell Physiol 55,87-98.
Mol PC,Park HM,Mullins JT,Cabib E(1994).A GTP-binding protein regulates the activity of(1→3)-β-glucan synthase,an enzyme directly involved in yeast cell wall morphogenesis.J Biol Chem 269,31267-31274.
Negishi T,Nakanishi H,Yazaki J,Kishimoto N,Fujii F,Shimbo K,Yamamoto K,Sakata K,Sasaki T,Kikuchi S,Mori S,Nishizawa NK(2002).cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore secretion in Fe-deficient barley roots.Plant J 30,83-94.
Nguyen VNT,Moon S,Jung KH(2014).Genome-wide expression analysis of rice ABC transporter family across spatio-temporal samples and in response to abiotic stressses.J Plant Physiol 171,1276-1288.
Qi YH,Wang SK,Shen CJ,Zhang SN,Chen Y,Xu YX,Liu Y,Wu YR,Jiang DA(2012).Os ARF12,a transcription activator on auxin response gene,regulates root elongation and affects iron accumulation in rice(Oryza sativa).New Phytol 193,109-120.
Robinson NJ,Procter CM,Connolly EL,Guerinot ML(1999).A ferric-chelate reductase for iron uptake from soils.Nature 397,694-697.
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