Rice miR394 suppresses leaf inclination through targeting an F-box gene, LEAF INCLINATION 4
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摘要
Rice leaf inclination is an important agronomic trait, closely related to plant architecture and yield.Identification of genes controlling leaf inclination would assist in crop improvement. Although various factors,including the plant hormones auxin and brassinosteroids,have been shown to regulate lamina joint development,the role of microRNAs in regulating leaf inclination remains largely unknown. Here, we functionally characterize the role of rice miR394 and its target, LEAF INCLINCATION 4(LC4), which encodes an F-box protein, in the regulation of leaf inclination. We show that miR394 and LC4 work,antagonistically, to regulate leaf lamina joint development and rice architecture, by modulating expansion and elongation of adaxial parenchyma cells. Suppressed expression of miR394, or enhanced expression of LC4,results in enlarged leaf angles, whereas reducing LC4 expression by CRISPR/Cas9 leads to reduced leaf inclination, suggesting LC4 as candidate for use in rice architecture improvement. LC4 interacts with SKP1, a component of the SCF E3 ubiquitin ligase complex, and transcription of both miR394 and LC4 are regulated by auxin. Rice plants with altered expression of miR394 or LC4 have altered auxin responses, indicating that the miR394-LC4 module mediates auxin effects important for determining rice leaf inclination and architecture.
Rice leaf inclination is an important agronomic trait, closely related to plant architecture and yield.Identification of genes controlling leaf inclination would assist in crop improvement. Although various factors,including the plant hormones auxin and brassinosteroids,have been shown to regulate lamina joint development,the role of microRNAs in regulating leaf inclination remains largely unknown. Here, we functionally characterize the role of rice miR394 and its target, LEAF INCLINCATION 4(LC4), which encodes an F-box protein, in the regulation of leaf inclination. We show that miR394 and LC4 work,antagonistically, to regulate leaf lamina joint development and rice architecture, by modulating expansion and elongation of adaxial parenchyma cells. Suppressed expression of miR394, or enhanced expression of LC4,results in enlarged leaf angles, whereas reducing LC4 expression by CRISPR/Cas9 leads to reduced leaf inclination, suggesting LC4 as candidate for use in rice architecture improvement. LC4 interacts with SKP1, a component of the SCF E3 ubiquitin ligase complex, and transcription of both miR394 and LC4 are regulated by auxin. Rice plants with altered expression of miR394 or LC4 have altered auxin responses, indicating that the miR394-LC4 module mediates auxin effects important for determining rice leaf inclination and architecture.
Rice leaf inclination is an important agronomic trait, closely related to plant architecture and yield.Identification of genes controlling leaf inclination would assist in crop improvement. Although various factors,including the plant hormones auxin and brassinosteroids,have been shown to regulate lamina joint development,the role of microRNAs in regulating leaf inclination remains largely unknown. Here, we functionally characterize the role of rice miR394 and its target, LEAF INCLINCATION 4(LC4), which encodes an F-box protein, in the regulation of leaf inclination. We show that miR394 and LC4 work,antagonistically, to regulate leaf lamina joint development and rice architecture, by modulating expansion and elongation of adaxial parenchyma cells. Suppressed expression of miR394, or enhanced expression of LC4,results in enlarged leaf angles, whereas reducing LC4 expression by CRISPR/Cas9 leads to reduced leaf inclination, suggesting LC4 as candidate for use in rice architecture improvement. LC4 interacts with SKP1, a component of the SCF E3 ubiquitin ligase complex, and transcription of both miR394 and LC4 are regulated by auxin. Rice plants with altered expression of miR394 or LC4 have altered auxin responses, indicating that the miR394-LC4 module mediates auxin effects important for determining rice leaf inclination and architecture.
引文
Attia KA,Abdelkhalik AF,Ammar MH,Wei C,Yang J,Lightfoot DA,El-Sayed WM,El-Shemy HA(2009)Antisense phenotypes reveal a functional expression of OsARF1,an auxin response factor,in transgenic rice.Curr Issues Mol Biol 11:i29-i34
Bai C,Sen P,Hofmann K,Ma L,Goebl M,Harper JW,Elledge SJ(1996)SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif,the F-box.Cell 86:263-274
Bian H,Xie Y,Guo F,Han N,Ma S,Zeng Z,Wang J,Yang Y,Zhu M(2012)Distinctive expression patterns and roles of the miRNA393/TIR1 homolog module in regulating flag leaf inclination and primary and crown root growth in rice(Oryza sativa).New Phytol 196:149-161
Chono M,Honda I,Zeniya H,Yoneyama K,Saisho D,Takeda K,Takatsuto S,Hoshino T,Watanabe Y(2003)A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor.Plant Physiol 133:1209-1219
Depuydt S,Hardtke CS(2011)Hormone signalling crosstalk in plant growth regulation.Curr Biol 21:R365-R373
De Vleesschauwer D,Van Buyten E,Satoh K,Balidion J,Mauleon R,Choi IR,Vera-Cruz C,Kikuchi S,H€ofte M(2012)Brassinosteroids antagonize gibberellin-and salicylatemediated root immunity in rice.Plant Physiol 158:1833-1846
Du H,Wu N,Fu J,Wang S,Li X,Xiao J,Xiong L(2012)A GH3family member,OsGH3-2,modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice.J Exp Bot 63:6467-6480
Hong Z,Ueguchi-Tanaka M,Matsuoka M(2004)Brassinosteroids and rice architecture.J Pestic Sci 29:184-188
Moon J,Parry G,Estelle M(2004)The ubiquitin-proteasome pathway and plant development.Plant Cell 16:3181-3195
Nakamura A,Fujioka S,Sunohara H,Kamiya N,Hong Z,Inukai Y,Miura K,Takatsuto S,Yoshida S,Ueguchi-Tanaka M,Hasegawa Y,Kitano H,Matsuoka M(2006)The role of OsBRI1 and its homologous genes,OsBRL1 and OsBRL3,in rice.Plant Physiol 140:580-590
Nakamura A,Fujioka S,Takatsuto S,Tsujimoto M,Kitano H,Yoshida S,Asami T,Nakano T(2009)Involvement of C-22-hydroxylated brassinosteroids in auxin-induced lamina joint bending in rice.Plant Cell Physiol 50:1627-1635
Sakamoto T,Morinaka Y,Ohnishi T,Sunohara H,Fujioka S,Ueguchi-Tanaka M,Mizutani M,Sakata K,Takatsuto S,Yoshida S,Tanaka H,Kitano H,Matsuoka M(2006)Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice.Nat Biotechnol24:105-109
Sinclair TR,Sheehy JE(1999)Erect leaves and photosynthesis in rice.Science 283:1455
Song JB,Gao S,Sun D,Li H,Shu XX,Yang ZM(2013)miR394and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner.BMCPlant Biol 13:210
Song Y,You J,Xiong L(2009)Characterization of OsIAA1 gene,a member of rice Aux/IAA family involved in auxin and brassinosteroid hormone responses and plant morphogenesis.Plant Mol Biol 70:297-309
Tang J,Chu C(2017)MicroRNAs in crop improvement:Finetuners for complex traits.Nat Plants 3:17077
Tang Y,Liu H,Guo S,Wang B,Li Z,Chong K,Xu Y(2017)OsmiR396d miRNA affects gibberellin and brassinosteroid signaling to regulate plant architecture.Plant Physiol 176:946-959
Tong H,Liu L,Jin Y,Du L,Yin Y,Qian Q,Zhu L,Chu C(2012)DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice.Plant Cell 24:2562-2577
Wada K,Marumo S,Ikekawa N,Morisaki M,Mori K(1981)Brassinolide and homobrassinolide promotion of lamina inclination of rice seedlings.Plant Cell Physiol 22:323-325
Xue LJ,Zhang JJ,Xue HW(2009)Characterization and expression profiles of miRNAs in rice seeds.Nucleic Acids Res 37:916-930
Yan J,Gu Y,Jia X,Kang W,Pan S,Tang X,Chen X,Tang G(2012)Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis.Plant Cell 24:415-427
Yang GX,Jan A,Shen SH,Yazaki J,Ishikawa M,Shimatani Z,Kishimoto N,Kikuchi S,Matsumoto H,Komatsu S(2004)Microarray analysis of brassinosteroids-and gibberellinregulated gene expression in rice seedlings.Mol Genet Genom 271:468-478
Yoshikawa T,Ito M,Sumikura T,Nakayama A,Nishimura T,Kitano H,Yamaguchi I,Koshiba T,Hibara K,Nagato Y,Itoh J(2014)The rice FISH BONE gene encodes a tryptophan aminotransferase,which affects pleiotropic auxin-related processes.Plant J 78:927-936
Zhang B,Pan X,Cobb GP,Anderson TA(2006)Plant microRNA:A small regulatory molecule with big impact.Dev Biol 289:3-16
Zhang S,Wang S,Xu Y,Yu C,Shen C,Qian Q,Geisler M,Jiang DA,Qi Y(2015)The auxin response factor,OsARF19,controls rice leaf angles through positively regulating OsGH3-5 and OsBRI1.Plant Cell Environ 38:638-654
Zhao SQ,Xiang JJ,Xue HW(2013)Studies on the rice LEAFINCLINATION1(LC1),an IAA-amino synthetase,reveal the effects of auxin in leaf inclination control.Mol Plant 6:174-187
Zhou LJ,Xiao LT,Xue HW(2017)Dynamic cytology and transcriptional regulation of rice lamina joint development.Plant Physiol 174:1728-1746
Bai C,Sen P,Hofmann K,Ma L,Goebl M,Harper JW,Elledge SJ(1996)SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif,the F-box.Cell 86:263-274
Bian H,Xie Y,Guo F,Han N,Ma S,Zeng Z,Wang J,Yang Y,Zhu M(2012)Distinctive expression patterns and roles of the miRNA393/TIR1 homolog module in regulating flag leaf inclination and primary and crown root growth in rice(Oryza sativa).New Phytol 196:149-161
Chono M,Honda I,Zeniya H,Yoneyama K,Saisho D,Takeda K,Takatsuto S,Hoshino T,Watanabe Y(2003)A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor.Plant Physiol 133:1209-1219
Depuydt S,Hardtke CS(2011)Hormone signalling crosstalk in plant growth regulation.Curr Biol 21:R365-R373
De Vleesschauwer D,Van Buyten E,Satoh K,Balidion J,Mauleon R,Choi IR,Vera-Cruz C,Kikuchi S,H€ofte M(2012)Brassinosteroids antagonize gibberellin-and salicylatemediated root immunity in rice.Plant Physiol 158:1833-1846
Du H,Wu N,Fu J,Wang S,Li X,Xiao J,Xiong L(2012)A GH3family member,OsGH3-2,modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice.J Exp Bot 63:6467-6480
Hong Z,Ueguchi-Tanaka M,Matsuoka M(2004)Brassinosteroids and rice architecture.J Pestic Sci 29:184-188
Moon J,Parry G,Estelle M(2004)The ubiquitin-proteasome pathway and plant development.Plant Cell 16:3181-3195
Nakamura A,Fujioka S,Sunohara H,Kamiya N,Hong Z,Inukai Y,Miura K,Takatsuto S,Yoshida S,Ueguchi-Tanaka M,Hasegawa Y,Kitano H,Matsuoka M(2006)The role of OsBRI1 and its homologous genes,OsBRL1 and OsBRL3,in rice.Plant Physiol 140:580-590
Nakamura A,Fujioka S,Takatsuto S,Tsujimoto M,Kitano H,Yoshida S,Asami T,Nakano T(2009)Involvement of C-22-hydroxylated brassinosteroids in auxin-induced lamina joint bending in rice.Plant Cell Physiol 50:1627-1635
Sakamoto T,Morinaka Y,Ohnishi T,Sunohara H,Fujioka S,Ueguchi-Tanaka M,Mizutani M,Sakata K,Takatsuto S,Yoshida S,Tanaka H,Kitano H,Matsuoka M(2006)Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice.Nat Biotechnol24:105-109
Sinclair TR,Sheehy JE(1999)Erect leaves and photosynthesis in rice.Science 283:1455
Song JB,Gao S,Sun D,Li H,Shu XX,Yang ZM(2013)miR394and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner.BMCPlant Biol 13:210
Song Y,You J,Xiong L(2009)Characterization of OsIAA1 gene,a member of rice Aux/IAA family involved in auxin and brassinosteroid hormone responses and plant morphogenesis.Plant Mol Biol 70:297-309
Tang J,Chu C(2017)MicroRNAs in crop improvement:Finetuners for complex traits.Nat Plants 3:17077
Tang Y,Liu H,Guo S,Wang B,Li Z,Chong K,Xu Y(2017)OsmiR396d miRNA affects gibberellin and brassinosteroid signaling to regulate plant architecture.Plant Physiol 176:946-959
Tong H,Liu L,Jin Y,Du L,Yin Y,Qian Q,Zhu L,Chu C(2012)DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice.Plant Cell 24:2562-2577
Wada K,Marumo S,Ikekawa N,Morisaki M,Mori K(1981)Brassinolide and homobrassinolide promotion of lamina inclination of rice seedlings.Plant Cell Physiol 22:323-325
Xue LJ,Zhang JJ,Xue HW(2009)Characterization and expression profiles of miRNAs in rice seeds.Nucleic Acids Res 37:916-930
Yan J,Gu Y,Jia X,Kang W,Pan S,Tang X,Chen X,Tang G(2012)Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis.Plant Cell 24:415-427
Yang GX,Jan A,Shen SH,Yazaki J,Ishikawa M,Shimatani Z,Kishimoto N,Kikuchi S,Matsumoto H,Komatsu S(2004)Microarray analysis of brassinosteroids-and gibberellinregulated gene expression in rice seedlings.Mol Genet Genom 271:468-478
Yoshikawa T,Ito M,Sumikura T,Nakayama A,Nishimura T,Kitano H,Yamaguchi I,Koshiba T,Hibara K,Nagato Y,Itoh J(2014)The rice FISH BONE gene encodes a tryptophan aminotransferase,which affects pleiotropic auxin-related processes.Plant J 78:927-936
Zhang B,Pan X,Cobb GP,Anderson TA(2006)Plant microRNA:A small regulatory molecule with big impact.Dev Biol 289:3-16
Zhang S,Wang S,Xu Y,Yu C,Shen C,Qian Q,Geisler M,Jiang DA,Qi Y(2015)The auxin response factor,OsARF19,controls rice leaf angles through positively regulating OsGH3-5 and OsBRI1.Plant Cell Environ 38:638-654
Zhao SQ,Xiang JJ,Xue HW(2013)Studies on the rice LEAFINCLINATION1(LC1),an IAA-amino synthetase,reveal the effects of auxin in leaf inclination control.Mol Plant 6:174-187
Zhou LJ,Xiao LT,Xue HW(2017)Dynamic cytology and transcriptional regulation of rice lamina joint development.Plant Physiol 174:1728-1746
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