Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Four AUXIN RESPONSE FACTOR genes downregulated by microRNA167 are associated with growth and development in Oryza sativa

Hai Liu A , Shenghua Jia A , Defeng Shen A , Jin Liu A , Jie Li A , Heping Zhao A , Shengcheng Han A B and Yingdian Wang A B
+ Author Affiliations
- Author Affiliations

A Beijing Key Laboratory of Gene Resources and Molecular Development, College of Life Sciences, Beijing Normal University, 19, XinJieKouWai Avenue, Beijing 100875, China.

B Corresponding author. Email: gdbnu@bnu.edu.cn

Functional Plant Biology 39(9) 736-744 https://doi.org/10.1071/FP12106
Submitted: 5 April 2012  Accepted: 5 July 2012   Published: 6 August 2012

Abstract

MicroRNA167 (miR167), as a conserved miRNA, has been implicated in auxin signalling by regulating the expression of certain auxin response factor (ARF) genes to determine the plant developmental process. Among the 10 MIR167 genes of rice, the precursor structures derived from MIR167a, MIR167b and MIR167c produce miR167 with high efficiency. To explore the biological function of miR167 in rice, four of its predicted target genes, OsARF6, OsARF12, OsARF17 and OsARF25, were identified in vivo. Although the expression levels of miR167 and its target OsARFs did not show an obvious negative correlation, the enhanced miR167 level in transgenic rice overexpressing miR167 resulted in a substantial decrease in mRNA levels of the four OsARF genes. Moreover, the transgenic rice plants were small in stature with remarkably reduced tiller number. These results suggest that miR167 is important for the appropriate expression of at least four OsARFs, which mediate the auxin response, to contribute to the normal growth and development of rice.

Additional keywords: auxin response factor, auxin signal, microRNA167, rice.


References

Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207–221.
MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvV2jtb4%3D&md5=fd9447329dad57ec0b85f566d761956eCAS |

Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends in Plant Science 13, 343–349.
Evolution of plant microRNAs and their targets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlOjt7s%3D&md5=536dfb2ec8f2f342b097f44817962d26CAS |

Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297.
MicroRNAs: genomics, biogenesis, mechanism, and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVals7o%3D&md5=e83b7209b6889c35d5a766428f2bc818CAS |

Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301, 336–338.
Role of microRNAs in plant and animal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1yiu78%3D&md5=d7c492ca3377734c54961891aaa09dcbCAS |

Chaw SM, Chang CC, Chen HL, Li WH (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. Journal of Molecular Evolution 58, 424–441.
Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjslOrtr0%3D&md5=c3e33a4dc790d4a47158dcbeb9ca7fd6CAS |

English JJ, Davenport GF, Elmayan T, Vaucheret H, Baulcombe DC (1997) Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. The Plant Journal 12, 597–603.
Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntVCktb0%3D&md5=7fc8943f667d41395623844c3011173fCAS |

Ge L, Chen H, Jiang JF, Zhao Y, Xu ML, Xu YY, Tan KH, Xu ZH, Chong K (2004) Overexpression of OsRAA1 causes pleiotropic phenotypes in transgenic rice plants, including altered leaf, flower, and root development and root response to gravity. Plant Physiology 135, 1502–1513.
Overexpression of OsRAA1 causes pleiotropic phenotypes in transgenic rice plants, including altered leaf, flower, and root development and root response to gravity.Crossref | GoogleScholarGoogle Scholar |

Guilfoyle TJ, Hagen G (2007) Auxin response factors. Current Opinion in Plant Biology 10, 453–460.
Auxin response factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFekurvE&md5=95423bcd5897e9cd0c70adafb52fd81dCAS |

Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. The Plant Cell 21, 3119–3132.
Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOgsLvE&md5=cba1c6062fbe4e784a23760be10ee1a3CAS |

Huang SQ, Peng J, Qiu CX, Yang ZM (2009) Heavy metal-regulated new microRNAs from rice. Journal of Inorganic Biochemistry 103, 282–287.
Heavy metal-regulated new microRNAs from rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntlyktA%3D%3D&md5=8fef438afdf6c11f71a9cd503160cd73CAS |

Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochemical and Biophysical Research Communications 345, 646–651.
Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVert70%3D&md5=646c480d06661372995c264990623bc5CAS |

Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 57, 19–53.
MicroRNAs and their regulatory roles in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhsb0%3D&md5=71719087e5a5085af3f1900e0faf2c80CAS |

Jung JH, Seo PJ, Park CM (2009) MicroRNA biogenesis and function in higher plants. Plant Biotechnology Reports 3, 111–126.
MicroRNA biogenesis and function in higher plants.Crossref | GoogleScholarGoogle Scholar |

Kozomara A, Griffiths-Jones S (2011) MiRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Research 39, D152–D157.
MiRBase: integrating microRNA annotation and deep-sequencing data.Crossref | GoogleScholarGoogle Scholar |

Larue CT, Wen J, Walker JC (2009) A microRNA-transcription factor module regulates lateral organ size and patterning in Arabidopsis. The Plant Journal 58, 450–463.
A microRNA-transcription factor module regulates lateral organ size and patterning in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVGjur8%3D&md5=913a58e993bb57e839fe6f1c0da3ab6aCAS |

Li T, Li H, Zhang YX, Liu JY (2011) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Research 39, 2821–2833.
Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvFansrk%3D&md5=0b78d9cf2b72bee5d74a05bc6b122363CAS |

Liu Q, Zhang YC, Wang CY, Luo YC, Huang QJ, Chen SY, Zhou H, Qu LH, Chen YQ (2009) Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Letters 583, 723–728.
Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitFSlsrg%3D&md5=be991ca5fdc360a301cc40e7662e1fc2CAS |

Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053–2056.
Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xnt1ansLo%3D&md5=eb4dca0784b982350bdc0b63269880eeCAS |

Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Current Biology 14, 1035–1046.
MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVOgtLg%3D&md5=8a292366480cc751173b0c921cfe8542CAS |

Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. The Plant Cell 17, 1360–1375.
MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKksrg%3D&md5=105ba033ce45d26b86edefd88cb09949CAS |

Meng Y, Huang F, Shi Q, Cao J, Chen D, Zhang J, Ni J, Wu P, Chen M (2009) Genome-wide survey of rice microRNAs and microRNA-target pairs in the root of a novel auxin-resistant mutant. Planta 230, 883–898.
Genome-wide survey of rice microRNAs and microRNA-target pairs in the root of a novel auxin-resistant mutant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOiurrE&md5=6e09bae0af05c49554aadf9cbe1d43eaCAS |

Meng Y, Chen D, Ma X, Mao C, Cao J, Wu P, Chen M (2010a) Mechanisms of microRNA-mediated auxin signaling inferred from the rice mutant osaxr. Plant Signaling & Behavior 5, 252–254.
Mechanisms of microRNA-mediated auxin signaling inferred from the rice mutant osaxr.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXps1ekur8%3D&md5=63ef3a27374707c8f29799188e969a74CAS |

Meng Y, Ma X, Chen D, Wu P, Chen M (2010b) MicroRNA-mediated signaling involved in plant root development. Biochemical and Biophysical Research Communications 393, 345–349.
MicroRNA-mediated signaling involved in plant root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1GrsL0%3D&md5=8df4a6aae8084aef42efffe9dd27bdd7CAS |

Nakamura A, Umemura I, Gomi K, Hasegawa Y, Kitano H, Sazuka T, Matsuoka M (2006) Production and characterization of auxin-insensitive rice by overexpression of a mutagenized rice IAA protein. The Plant Journal 46, 297–306.
Production and characterization of auxin-insensitive rice by overexpression of a mutagenized rice IAA protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVWnt7w%3D&md5=d089de7dd9fd0b7659906f7b110b9625CAS |

Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436–439.
A plant miRNA contributes to antibacterial resistance by repressing auxin signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslSktbw%3D&md5=284f2273b35d71d30d74cee2318ce4cfCAS |

Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. The Plant Cell 18, 2929–2945.
The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1ClsA%3D%3D&md5=5dc4cc96b323c6716ec3fc4d420867f1CAS |

Qi Y, Wang S, Shen C, Zhang S, Chen Y, Xu Y, Liu Y, Wu Y, Jiang D (2012) OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytologist 193, 109–120.
OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitVKgtrc%3D&md5=783e02a1a49cdfd090dfb2a59064965cCAS |

Quint M, Gray WM (2006) Auxin signaling. Current Opinion in Plant Biology 9, 448–453.
Auxin signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFCntbw%3D&md5=5678d042ae59b5c57a154a0ae95ec411CAS |

Ramkissoon SH, Mainwaring LA, Sloand EM, Young NS, Kajigaya S (2006) Nonisotopic detection of microRNA using digoxigenin labeled RNA probes. Molecular and Cellular Probes 20, 1–4.
Nonisotopic detection of microRNA using digoxigenin labeled RNA probes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFyhurk%3D&md5=2a007698282962cf696eb487365bf4edCAS |

Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes & Development 16, 1616–1626.
MicroRNAs in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVSmt7c%3D&md5=654f80872853c1d5e173e0e33e6f5ab7CAS |

Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. The Plant Journal 49, 592–606.
ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlGmsbs%3D&md5=ce72b09ae1883f6ccc90232d4fa2d33fCAS |

Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110, 513–520.
Prediction of plant microRNA targets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmslyjt7s%3D&md5=c2eb3f69b3a947203f1111f8eb82876cCAS |

Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Research 16, 457–465.
Plant fertility defects induced by the enhanced expression of microRNA167.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFSgu7Y%3D&md5=bac63d21716e9ae41f5ea07e0314e10cCAS |

Schmidt GW, Delaney SK (2010) Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Molecular Genetics and Genomics 283, 233–241.
Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvVKit74%3D&md5=1ad69ce243dc44e5000d6854969afa6eCAS |

Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Molecular Biology 67, 183–195.
The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXks1Krt7s%3D&md5=89779e79ac07bbca9a48f21e2e8db68dCAS |

Shen C, Wang S, Bai Y, Wu Y, Zhang S, Chen M, Guilfoyle TJ, Wu P, Qi Y (2010) Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L.). Journal of Experimental Botany 61, 3971–3981.
Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFGhtrvK&md5=07b9bc17fa14129c6ec57a658d4e6b53CAS |

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 Molecular Biology 70, 297–309.
Characterization of OsIAA1 gene, a member of rice Aux/IAA family involved in auxin and brassinosteroid hormone responses and plant morphogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltlygtLs%3D&md5=8e8a0b9de7f954ee3d8f3d98c49252e6CAS |

Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. The Plant Cell 17, 1397–1411.
Cloning and characterization of microRNAs from rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKksrc%3D&md5=2296307ada137c21feefcc4a335d374cCAS |

Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nature Reviews. Molecular Cell Biology 7, 847–859.
Auxin in action: signalling, transport and the control of plant growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSms77M&md5=2863e5fb0bd9507c6d4dfcc9be7cd7aeCAS |

Válóczi A, Hornyik C, Varga N, Burgyán J, Kauppinen S, Havelda Z (2004) Sensitive and specific detection of microRNAs by northern blot analysis using LNA-modified oligonucleotide probes. Nucleic Acids Research 32, e175
Sensitive and specific detection of microRNAs by northern blot analysis using LNA-modified oligonucleotide probes.Crossref | GoogleScholarGoogle Scholar |

Válóczi A, Várallyay É, Kauppinen S, Burgyán J, Havelda Z (2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. The Plant Journal 47, 140–151.
Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues.Crossref | GoogleScholarGoogle Scholar |

Wang M, Chen C, Xu YY, Jiang RX, Han Y, Xu ZH, Chong K (2004) A practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.). Plant Molecular Biology Reporter 22, 409–417.
A practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFertLg%3D&md5=cea9cd0366c64d0a13edabbaadd55c18CAS |

Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. The Plant Cell 17, 2204–2216.
Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFGjs7c%3D&md5=80b0294118e78ac5a5ede7fdf88cb072CAS |

Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394, 13–24.
Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVelur8%3D&md5=18c697ca6c91bc22413bc09a93f22436CAS |

Weijers D, Benkova E, Jager KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jurgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO Journal 24, 1874–1885.
Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1Smtr8%3D&md5=e547c8fa3c8385d7f829c8de7b824c1eCAS |

Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proceedings of the National Academy of Sciences of the United States of America 102, 9703–9708.
A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsVaktbg%3D&md5=d276c9014d150e0e5fe8d5acd6a51d64CAS |

Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211–4218.
Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlSmt73E&md5=d868abca1a0e3ca9494cbf1b293b9e1cCAS |

Xue LJ, Zhang JJ, Xue HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Research 37, 916–930.
Characterization and expression profiles of miRNAs in rice seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFekuro%3D&md5=d262741d2f288452e10e7b2d5833e8cdCAS |

Yang JH, Han SJ, Yoon EK, Lee WS (2006) Evidence of an auxin signal pathway, microRNA167–ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Research 34, 1892–1899.
Evidence of an auxin signal pathway, microRNA167–ARF8-GH3, and its response to exogenous auxin in cultured rice cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslOjsr4%3D&md5=8e0e89762b107027b27e64cbb0ca8408CAS |

Yoon EK, Yang JH, Lim J, Kim SH, Kim SK, Lee WS (2010) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Research 38, 1382–1391.
Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1WrtL0%3D&md5=c9315c4aea83defdebc4890dc3088e81CAS |

Zhang Y (2005) MiRU: an automated plant miRNA target prediction server. Nucleic Acids Research 33, W701–W704.
MiRU: an automated plant miRNA target prediction server.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslyrtbg%3D&md5=abd0b18e7a4c2536555c548cc251fb0fCAS |

Zhao BT, Liang RQ, Ge LF, Li W, Xiao HS, Lin HX, Ruan KC, Jin YX (2007) Identification of drought-induced microRNAs in rice. Biochemical and Biophysical Research Communications 354, 585–590.
Identification of drought-induced microRNAs in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOgtb4%3D&md5=7ed61ecfdbd6c6dec7eefdee17c5e1e0CAS |

Zhou X, Li J, Cheng W, Liu H, Li M, Zhang Y, Li W, Han S, Wang Y (2010) Gene structure analysis of rice ADP-ribosylation factors (OsARFs) and their mRNA expression in developing rice plants. Plant Molecular Biology Reporter 28, 692–703.
Gene structure analysis of rice ADP-ribosylation factors (OsARFs) and their mRNA expression in developing rice plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGksb%2FF&md5=940cb2f6a5275f80e3c909dfef268c63CAS |

Zhu QH, Spriggs A, Matthew L, Fan LJ, Kennedy G, Gubler F, Helliwell C (2008) A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Research 18, 1456–1465.
A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtV2qsr3P&md5=b39a9379092fe6d7830bb1d73439c601CAS |

Zhu ZX, Liu Y, Liu SJ, Mao CZ, Wu YR, Wu P (2012) A gain-of-function mutation in OsIAA11 affects lateral root development in rice. Molecular Plant 5, 154–161.
A gain-of-function mutation in OsIAA11 affects lateral root development in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Smt7Y%3D&md5=a9fcb7bd27474d76305201bc8d6187f1CAS |