Brassinosteroid-regulated plant growth and development and gene expression in soybean
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摘要
Brassinosteroids(BRs) are endogenous phytohormones that play important roles in regulating plant growth and development.In this study, we evaluated the effects of brassinolide(BL, one of the active BRs) on soybean and identified roles of the hormone in regulating multiple aspects of plant growth and development.BL application promoted hypocotyl and epicotyl elongation in the light but blocked epicotyl elongation in the dark.High levels of castasterone and BL accumulated in light-grown plants.BL disrupted shoot negative gravitropism, whereas gibberellin did not.BL delayed leaf senescence.Transcriptome analysis showed that BL induced cell wall-modifying genes and auxin-associated genes but suppressed a class of WRKY genes involved in senescence and stress responses,showing the complex roles of BRs in multiple biological processes.
Brassinosteroids(BRs) are endogenous phytohormones that play important roles in regulating plant growth and development.In this study, we evaluated the effects of brassinolide(BL, one of the active BRs) on soybean and identified roles of the hormone in regulating multiple aspects of plant growth and development.BL application promoted hypocotyl and epicotyl elongation in the light but blocked epicotyl elongation in the dark.High levels of castasterone and BL accumulated in light-grown plants.BL disrupted shoot negative gravitropism, whereas gibberellin did not.BL delayed leaf senescence.Transcriptome analysis showed that BL induced cell wall-modifying genes and auxin-associated genes but suppressed a class of WRKY genes involved in senescence and stress responses,showing the complex roles of BRs in multiple biological processes.
Brassinosteroids(BRs) are endogenous phytohormones that play important roles in regulating plant growth and development.In this study, we evaluated the effects of brassinolide(BL, one of the active BRs) on soybean and identified roles of the hormone in regulating multiple aspects of plant growth and development.BL application promoted hypocotyl and epicotyl elongation in the light but blocked epicotyl elongation in the dark.High levels of castasterone and BL accumulated in light-grown plants.BL disrupted shoot negative gravitropism, whereas gibberellin did not.BL delayed leaf senescence.Transcriptome analysis showed that BL induced cell wall-modifying genes and auxin-associated genes but suppressed a class of WRKY genes involved in senescence and stress responses,showing the complex roles of BRs in multiple biological processes.
引文
[1]Z.Y.Wang,M.Y.Bai,E.Oh,J.Y.Zhu,Brassinosteroid signaling network and regulation of photomorphogenesis,Annu.Rev.Genet.46(2012)701-724.
[2]B.L.Zhao,J.Li,Regulation of brassinosteroid biosynthesis and inactivation,J.Integr.Plant Biol.54(2012)746-759.
[3]C.Vriet,E.Russinova,C.Reuzeau,From squalene to brassinolide:the steroid metabolic and signaling pathways across the plant kingdom,Mol.Plant 6(2013)1738-1757.
[4]Z.Y.Wang,H.Seto,S.Fujioka,S.Yoshida,J.Chory,BRI1 is a critical component of a plasma-membrane receptor for plant steroids,Nature 410(2001)380-383.
[5]K.H.Nam,J.Li,BRI1/BAK1,a receptor kinase pair mediating brassinosteroid signaling,Cell 110(2002)203-212.
[6]W.Tang,T.W.Kim,J.A.Oses-Prieto,Y.Sun,Z.Deng,S.Zhu,R.Wang,A.L.Burlingame,Z.Y.Wang,BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis,Science 321(2008)557-560.
[7]T.W.Kim,S.Guan,A.L.Burlingame,Z.Y.Wang,The CDG1kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2,Mol.Cell 43(2011)561-571.
[8]J.Li,K.H.Nam,Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase,Science 295(2002)1299-1301.
[9]J.X.He,J.M.Gendron,Y.Yang,J.Li,Z.Y.Wang,The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1,a positive regulator of the brassinosteroid signaling pathway in Arabidopsis,Proc.Natl.Acad.Sci.U.S.A.99(2002)10185-10190.
[10]Y.Yin,Z.Y.Wang,S.Mora-Garcia,J.Li,S.Yoshida,T.Asami,J.Chory,BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation,Cell 109(2002)181-191.
[11]X.F.Yu,L.Li,J.Zola,M.Aluru,H.X.Ye,A.Foudree,H.Q.Guo,S.Anderson,S.Aluru,P.Liu,S.Rodermel,Y.H.Yin,Abrassinosteroid transcriptional network revealed by genomewide identification of BES1 target genes in Arabidopsis thaliana,Plant J.65(2011)634-646.
[12]Y.Sun,X.Y.Fan,D.M.Cao,W.Q.Tang,K.He,J.Y.Zhu,J.X.He,M.Y.Bai,S.W.Zhu,E.Oh,S.Patil,T.W.Kim,H.K.Ji,W.H.Wong,S.Y.Rhee,Z.Y.Wang,Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis,Dev.Cell 19(2010)765-777.
[13]M.Szekeres,K.Nemeth,Z.Koncz-Kalman,J.Mathur,A.Kauschmann,T.Altmann,G.P.Redei,F.Nagy,J.Schell,C.Koncz,Brassinosteroids rescue the deficiency of CYP90,a cytochrome P450,controlling cell elongation and deetiolation in Arabidopsis,Cell 85(1996)171-182.
[14]T.Noguchi,S.Fujioka,S.Takatsuto,A.Sakurai,S.Yoshida,J.Li,J.Chory,Arabidopsis det2 is defective in the conversion of(24R)-24-methylcholest-4-En-3-one to(24R)-24-methyl-5alpha-cholestan-3-one in brassinosteroid biosynthesis,Plant Physiol.120(1999)833-840.
[15]C.Yamamuro,Y.Ihara,X.Wu,T.Noguchi,S.Fujioka,S.Takatsuto,M.Ashikari,H.Kitano,M.Matsuoka,Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint,Plant Cell 12(2000)1591-1606.
[16]S.Tanabe,M.Ashikari,S.Fujioka,S.Takatsuto,S.Yoshida,M.Yano,A.Yoshimura,H.Kitano,M.Matsuoka,Y.Fujisawa,H.Kato,Y.Iwasaki,A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant,dwarf11,with reduced seed length,Plant Cell17(2005)776-790.
[17]X.Yu,L.Li,M.Guo,J.Chory,Y.Yin,Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis,Proc.Natl.Acad.Sci.U.S.A.105(2008)7618-7623.
[18]Y.J.Jeong,Y.Shang,B.H.Kim,S.Y.Kim,J.H.Song,J.S.Lee,M.M.Lee,J.Li,K.H.Nam,BAK7 displays unequal genetic redundancy with BAK1 in brassinosteroid signaling and early senescence in Arabidopsis,Mol.Cell 29(2010)259-266.
[19]Q.Ye,W.Zhu,L.Li,S.Zhang,Y.Yin,H.Ma,X.Wang,Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development,Proc.Natl.Acad.Sci.U.S.A.107(2010)6100-6105.
[20]C.Mussig,G.H.Shin,T.Altmann,Brassinosteroids promote root growth in Arabidopsis,Plant Physiol.133(2003)1261-1271.
[21]H.Nakashita,M.Yasuda,T.Nitta,T.Asami,S.Fujioka,Y.Arai,K.Sekimata,S.Takatsuto,I.Yamaguchi,S.Yoshida,Brassinosteroid functions in a broad range of disease resistance in tobacco and rice,Plant J.33(2003)887-898.
[22]F.Cui,L.Liu,Q.Zhao,Z.Zhang,Q.Li,B.Lin,Y.Wu,S.Tang,Q.Xie,Arabidopsis ubiquitin conjugase UBC32 is an ERADcomponent that functions in brassinosteroid-mediated salt stress tolerance,Plant Cell 24(2012)233-244.
[23]Z.Hong,M.Ueguchi-Tanaka,M.Matsuoka,Brassinosteroids and rice architecture,J.Pestic.Sci.29(2004)184-188.
[24]C.Y.Wu,A.Trieu,P.Radhakrishnan,S.F.Kwok,S.Harris,K.Zhang,J.Wang,J.Wan,H.Zhai,S.Takatsuto,S.Matsumoto,S.Fujioka,K.A.Feldmann,R.I.Pennell,Brassinosteroids regulate grain filling in rice,Plant Cell 20(2008)2130-2145.
[25]T.Sakamoto,Y.Morinaka,T.Ohnishi,H.Sunohara,S.Fujioka,M.Ueguchi-Tanaka,M.Mizutani,K.Sakata,S.Takatsuto,S.Yoshida,H.Tanaka,H.Kitano,M.Matsuoka,Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice,Nat.Biotechnol.24(2006)105-109.
[26]Y.Morinaka,T.Sakamoto,Y.Inukai,M.Agetsuma,H.Kitano,M.Ashikari,M.Matsuoka,Morphological alteration caused by brassinosteroid insensitivity increases the biomass and grain production of rice,Plant Physiol.141(2006)924-931.
[27]J.Ding,L.J.Mao,S.T.Wang,B.F.Yuan,Y.Q.Feng,Determination of endogenous brassinosteroids in plant tissues using solidphase extraction with double layered cartridge followed by high-performance liquid chromatography-tandem mass spectrometry,Phytochem.Anal.24(2013)386-394.
[28]Y.Meng,H.Li,Q.Wang,B.Liu,C.Lin,Blue light-dependent interaction between cryptochrome2 and CIB1 regulates transcription and leaf senescence in soybean,Plant Cell 25(2013)4405-4420.
[29]M.H.Oh,W.G.Romanow,R.C.Smith,E.Zamskiue,J.Sasse,S.D.Clouse,Soybean BRU1 encodes a functional xyloglucan endotransglycosylase that is highly expressed in inner epicotyl tissues during brassinosteroid-promoted elongation,Plant Cell Physiol.39(1998)124-130.
[30]T.S.Yao,X.F.Zhu,J.H.Jung,Y.H.Xuan,Qa-SNARE protein SYP22 negatively regulates brassinosteroid signaling in the dark,Acta Biol.Cracov.Ser.Bot.57(2015)79-88.
[31]F.Vandenbussche,D.Suslov,L.de Grauwe,O.Leroux,K.Vissenberg,D.van der Straeten,The role of brassinosteroids in shoot gravitropism,Plant Physiol.156(2011)1331-1336.
[32]L.Armengot,M.M.Marquès-Bueno,Y.Jaillais,Regulation of polar auxin transport by protein and lipid kinases,J.Exp.Bot.67(2016)4015-4037.
[33]S.L.Harmer,C.J.Brooks,Growth-mediated plant movements:hidden in plain sight,Curr.Opin.Plant Biol.41(2018)89-94.
[34]N.Zhang,H.Yu,H.Yu,Y.Y.Cai,L.Z.Huang,C.Xu,G.S.Xiong,X.B.Meng,J.Y.Wang,H.F.Chen,G.F.Liu,Y.H.Jing,Y.D.Yuan,Y.Liang,S.J.Li,S.M.Smith,J.Y.Li,Y.H.Wang,A core regulatory pathway controlling rice tiller angle mediated by the LAZY1-dependent asymmetric distribution of auxin,Plant Cell 30(2018)1461-1475.
[35]F.Chen,Y.Hu,A.Vannozzi,K.Wu,H.Cai,Y.Qin,A.Mullis,Z.Lin,L.Zhang,The WRKY transcription factor family in model plants and crops,Crit.Rev.Plant Sci.36(2017)311-335.
[36]X.Tian,X.Li,W.Zhou,Y.Ren,Z.Wang,Z.Liu,J.Tang,H.Tong,J.Fang,Q.Bu,Transcription factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture,Plant Physiol.175(2017)1337-1349.
[37]J.Chen,T.M.Nolan,H.Ye,M.Zhang,H.Tong,P.Xin,J.Chu,C.Chu,Z.Li,Y.Yin,Arabidopsis WRKY46,WRKY54,and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses,Plant Cell 29(2017)1425-1439.
[2]B.L.Zhao,J.Li,Regulation of brassinosteroid biosynthesis and inactivation,J.Integr.Plant Biol.54(2012)746-759.
[3]C.Vriet,E.Russinova,C.Reuzeau,From squalene to brassinolide:the steroid metabolic and signaling pathways across the plant kingdom,Mol.Plant 6(2013)1738-1757.
[4]Z.Y.Wang,H.Seto,S.Fujioka,S.Yoshida,J.Chory,BRI1 is a critical component of a plasma-membrane receptor for plant steroids,Nature 410(2001)380-383.
[5]K.H.Nam,J.Li,BRI1/BAK1,a receptor kinase pair mediating brassinosteroid signaling,Cell 110(2002)203-212.
[6]W.Tang,T.W.Kim,J.A.Oses-Prieto,Y.Sun,Z.Deng,S.Zhu,R.Wang,A.L.Burlingame,Z.Y.Wang,BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis,Science 321(2008)557-560.
[7]T.W.Kim,S.Guan,A.L.Burlingame,Z.Y.Wang,The CDG1kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2,Mol.Cell 43(2011)561-571.
[8]J.Li,K.H.Nam,Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase,Science 295(2002)1299-1301.
[9]J.X.He,J.M.Gendron,Y.Yang,J.Li,Z.Y.Wang,The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1,a positive regulator of the brassinosteroid signaling pathway in Arabidopsis,Proc.Natl.Acad.Sci.U.S.A.99(2002)10185-10190.
[10]Y.Yin,Z.Y.Wang,S.Mora-Garcia,J.Li,S.Yoshida,T.Asami,J.Chory,BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation,Cell 109(2002)181-191.
[11]X.F.Yu,L.Li,J.Zola,M.Aluru,H.X.Ye,A.Foudree,H.Q.Guo,S.Anderson,S.Aluru,P.Liu,S.Rodermel,Y.H.Yin,Abrassinosteroid transcriptional network revealed by genomewide identification of BES1 target genes in Arabidopsis thaliana,Plant J.65(2011)634-646.
[12]Y.Sun,X.Y.Fan,D.M.Cao,W.Q.Tang,K.He,J.Y.Zhu,J.X.He,M.Y.Bai,S.W.Zhu,E.Oh,S.Patil,T.W.Kim,H.K.Ji,W.H.Wong,S.Y.Rhee,Z.Y.Wang,Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis,Dev.Cell 19(2010)765-777.
[13]M.Szekeres,K.Nemeth,Z.Koncz-Kalman,J.Mathur,A.Kauschmann,T.Altmann,G.P.Redei,F.Nagy,J.Schell,C.Koncz,Brassinosteroids rescue the deficiency of CYP90,a cytochrome P450,controlling cell elongation and deetiolation in Arabidopsis,Cell 85(1996)171-182.
[14]T.Noguchi,S.Fujioka,S.Takatsuto,A.Sakurai,S.Yoshida,J.Li,J.Chory,Arabidopsis det2 is defective in the conversion of(24R)-24-methylcholest-4-En-3-one to(24R)-24-methyl-5alpha-cholestan-3-one in brassinosteroid biosynthesis,Plant Physiol.120(1999)833-840.
[15]C.Yamamuro,Y.Ihara,X.Wu,T.Noguchi,S.Fujioka,S.Takatsuto,M.Ashikari,H.Kitano,M.Matsuoka,Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint,Plant Cell 12(2000)1591-1606.
[16]S.Tanabe,M.Ashikari,S.Fujioka,S.Takatsuto,S.Yoshida,M.Yano,A.Yoshimura,H.Kitano,M.Matsuoka,Y.Fujisawa,H.Kato,Y.Iwasaki,A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant,dwarf11,with reduced seed length,Plant Cell17(2005)776-790.
[17]X.Yu,L.Li,M.Guo,J.Chory,Y.Yin,Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis,Proc.Natl.Acad.Sci.U.S.A.105(2008)7618-7623.
[18]Y.J.Jeong,Y.Shang,B.H.Kim,S.Y.Kim,J.H.Song,J.S.Lee,M.M.Lee,J.Li,K.H.Nam,BAK7 displays unequal genetic redundancy with BAK1 in brassinosteroid signaling and early senescence in Arabidopsis,Mol.Cell 29(2010)259-266.
[19]Q.Ye,W.Zhu,L.Li,S.Zhang,Y.Yin,H.Ma,X.Wang,Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development,Proc.Natl.Acad.Sci.U.S.A.107(2010)6100-6105.
[20]C.Mussig,G.H.Shin,T.Altmann,Brassinosteroids promote root growth in Arabidopsis,Plant Physiol.133(2003)1261-1271.
[21]H.Nakashita,M.Yasuda,T.Nitta,T.Asami,S.Fujioka,Y.Arai,K.Sekimata,S.Takatsuto,I.Yamaguchi,S.Yoshida,Brassinosteroid functions in a broad range of disease resistance in tobacco and rice,Plant J.33(2003)887-898.
[22]F.Cui,L.Liu,Q.Zhao,Z.Zhang,Q.Li,B.Lin,Y.Wu,S.Tang,Q.Xie,Arabidopsis ubiquitin conjugase UBC32 is an ERADcomponent that functions in brassinosteroid-mediated salt stress tolerance,Plant Cell 24(2012)233-244.
[23]Z.Hong,M.Ueguchi-Tanaka,M.Matsuoka,Brassinosteroids and rice architecture,J.Pestic.Sci.29(2004)184-188.
[24]C.Y.Wu,A.Trieu,P.Radhakrishnan,S.F.Kwok,S.Harris,K.Zhang,J.Wang,J.Wan,H.Zhai,S.Takatsuto,S.Matsumoto,S.Fujioka,K.A.Feldmann,R.I.Pennell,Brassinosteroids regulate grain filling in rice,Plant Cell 20(2008)2130-2145.
[25]T.Sakamoto,Y.Morinaka,T.Ohnishi,H.Sunohara,S.Fujioka,M.Ueguchi-Tanaka,M.Mizutani,K.Sakata,S.Takatsuto,S.Yoshida,H.Tanaka,H.Kitano,M.Matsuoka,Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice,Nat.Biotechnol.24(2006)105-109.
[26]Y.Morinaka,T.Sakamoto,Y.Inukai,M.Agetsuma,H.Kitano,M.Ashikari,M.Matsuoka,Morphological alteration caused by brassinosteroid insensitivity increases the biomass and grain production of rice,Plant Physiol.141(2006)924-931.
[27]J.Ding,L.J.Mao,S.T.Wang,B.F.Yuan,Y.Q.Feng,Determination of endogenous brassinosteroids in plant tissues using solidphase extraction with double layered cartridge followed by high-performance liquid chromatography-tandem mass spectrometry,Phytochem.Anal.24(2013)386-394.
[28]Y.Meng,H.Li,Q.Wang,B.Liu,C.Lin,Blue light-dependent interaction between cryptochrome2 and CIB1 regulates transcription and leaf senescence in soybean,Plant Cell 25(2013)4405-4420.
[29]M.H.Oh,W.G.Romanow,R.C.Smith,E.Zamskiue,J.Sasse,S.D.Clouse,Soybean BRU1 encodes a functional xyloglucan endotransglycosylase that is highly expressed in inner epicotyl tissues during brassinosteroid-promoted elongation,Plant Cell Physiol.39(1998)124-130.
[30]T.S.Yao,X.F.Zhu,J.H.Jung,Y.H.Xuan,Qa-SNARE protein SYP22 negatively regulates brassinosteroid signaling in the dark,Acta Biol.Cracov.Ser.Bot.57(2015)79-88.
[31]F.Vandenbussche,D.Suslov,L.de Grauwe,O.Leroux,K.Vissenberg,D.van der Straeten,The role of brassinosteroids in shoot gravitropism,Plant Physiol.156(2011)1331-1336.
[32]L.Armengot,M.M.Marquès-Bueno,Y.Jaillais,Regulation of polar auxin transport by protein and lipid kinases,J.Exp.Bot.67(2016)4015-4037.
[33]S.L.Harmer,C.J.Brooks,Growth-mediated plant movements:hidden in plain sight,Curr.Opin.Plant Biol.41(2018)89-94.
[34]N.Zhang,H.Yu,H.Yu,Y.Y.Cai,L.Z.Huang,C.Xu,G.S.Xiong,X.B.Meng,J.Y.Wang,H.F.Chen,G.F.Liu,Y.H.Jing,Y.D.Yuan,Y.Liang,S.J.Li,S.M.Smith,J.Y.Li,Y.H.Wang,A core regulatory pathway controlling rice tiller angle mediated by the LAZY1-dependent asymmetric distribution of auxin,Plant Cell 30(2018)1461-1475.
[35]F.Chen,Y.Hu,A.Vannozzi,K.Wu,H.Cai,Y.Qin,A.Mullis,Z.Lin,L.Zhang,The WRKY transcription factor family in model plants and crops,Crit.Rev.Plant Sci.36(2017)311-335.
[36]X.Tian,X.Li,W.Zhou,Y.Ren,Z.Wang,Z.Liu,J.Tang,H.Tong,J.Fang,Q.Bu,Transcription factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture,Plant Physiol.175(2017)1337-1349.
[37]J.Chen,T.M.Nolan,H.Ye,M.Zhang,H.Tong,P.Xin,J.Chu,C.Chu,Z.Li,Y.Yin,Arabidopsis WRKY46,WRKY54,and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses,Plant Cell 29(2017)1425-1439.