MicroRNAs as regulators of root development and architecture

Plant Molecular Biology

Volumn 77, Issue 1, 2011, Pages 47-58

  Khan, Ghazanfar A ^a   Declerck, Marie ^a   Sorin, Céline ^a,b   Hartmann, Caroline ^a,b   Crespi, Martin ^a   Lelandais Brière, Christine ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Abiotic stress; Auxin; MicroRNA; Nodulation; Root development

Indexed keywords

INDOLEACETIC ACID DERIVATIVE; MICRORNA; PLANT RNA; VEGETABLE PROTEIN;

ARTICLE; CELL DIFFERENTIATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; NITROGEN FIXATION; NODULATION; PHYSIOLOGY; PLANT ROOT; SEEDLING; SIGNAL TRANSDUCTION;

CELL DIFFERENTIATION; HOMEOSTASIS; INDOLEACETIC ACIDS; MICRORNAS; NITROGEN FIXATION; PLANT PROTEINS; PLANT ROOT NODULATION; PLANT ROOTS; RNA, PLANT; SEEDLING; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 80051932344     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-011-9793-x     Document Type: Article

References (108)

1. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109-120.
2. Arenas-Huertero C, Pérez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sanchez F, Covarrubias AA, Reyes JL (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70: 385-401.
3. Arnaud C, Bonnot C, Desnos T, Nussaume L (2010) The root cap at the forefront. C R Biol 333: 335-343.
4. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141: 988-999.
5. Becraft PW, Bongard-Pierce DK, Sylvester AW, Poethig RS, Freeling M (1990) The LIGULELESS-1 gene acts tissue specifically in maize leaf development. Dev Biol 141: 220-232.
6. Benfey PN, Scheres B (2000) Root development. Curr Biol 10: R813-R815.
7. Benková E, Hejátko J (2009) Hormone interactions at the root apical meristem. Plant Mol Biol 69: 383-396.
8. Berleth T, Jürgens G (1993) The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118: 575-587.
9. Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54: 876-887.
10. Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A, Schauser L, Scheible WR, Krajinski F (2010) Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol Plant Microbe Interact 23: 915-926.
11. Brechenmacher L, Kim MY, Benitez M, Li M, Joshi T, Calla B, Lee MP, Libault M, Vodkin LO, Xu D, Lee SH, Clough SJ, Stacey G (2008) Transcription profiling of soybean nodulation by Bradyrhizobium japonicum. Mol Plant Microbe Interact 21: 631-645.
12. Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10: 64.
13. Byrne ME (2006) Shoot meristem function and leaf polarity: the role of class III HD-ZIP genes. PLoS Genet 2: e89.
14. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465: 316-321.
15. Casimiro I, Beeckman T, Graham N, Rishikesh Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting arabidopsis lateral root development. Trends Plant Sci 8: 165-171.
16. Chen H, Xiong L (2010) The bifunctional abiotic stress signalling regulator and endogenous RNA silencing suppressor FIERY1 is required for lateral root formation. Plant Cell Environ 33: 2180-2190.
17. Chiou TJ (2008) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30: 323-332.
18. Chuck G, Candela H, Hake S (2009) Big impacts by small RNAs in plant development. Curr Opin Plant Biol 12: 81-86.
19. Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernié T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20: 3084-3088.
20. Coudert Y, Périn C, Courtois B, Khong NG, Gantet P (2010) Genetic control of root development in rice, the model cereal. Trends Plant Sci 15: 219-226.
21. Crespi M, Frugier F (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Sci Signal 9: 1(49): re11.
22. de Dorlodot S, Forster B, Pagès L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12: 474-481.
23. Desnos T (2008) Root branching responses to phosphate and nitrate. Current Opin Plant Biol 11: 82-87.
24. Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci 9: 302-308.
25. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
26. Ding Y, Oldroyd GE (2009) Positioning the nodule, the hormone dictum. Plant Signal Behav 4: 89-93.
27. Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16: 939-944.
28. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39: 1033-1037.
29. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15: 2038-2043.
30. Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 256: 111-137.
31. Gallagher KL, Paquette AJ, Nakajima K, Benfey PN (2004) Mechanisms regulating SHORT-ROOT intercellular movement. Curr Biol 14: 1847-1851.
32. Gazzani S, Lawrenson T, Woodward C, Headon D, Sablowski R (2004) A link between mRNA turnover and RNA interference in Arabidopsis. Science 306: 1046-1048.
33. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105: 803-808.
34. Godiard L, Niebel A, Micheli F, Gouzy J, Ott T, Gamas P (2007) Identification of new potential regulators of the Medicago truncatula-Sinorhizobium meliloti symbiosis using a large-scale suppression subtractive hybridization approach. Mol Plant Microbe Interact 20: 321-332.
35. Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby L, Yang M, Ma H, Estelle M (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev 13: 1678-1691.
36. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF (TIR1)-dependent degradation of AUX/IAA proteins. Nature 414: 271-276.
37. Gregory BD, O'Malley RC, Lister R, Urich MA, Tonti-Filippini J, Chen H, Millar AH, Ecker JR (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Developmental Cell 14: 854-866.
38. Grigg SP, Canales C, Hay A, Tsiantis M (2005) SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437: 1022-1026.
39. Grigg SP, Galinha C, Kornet N, Canales C, Scheres B, Tsiantis M (2009) Repression of apical homeobox genes is required for embryonic root development in arabidopsis. Curr Biol 19: 1485-1490.
40. Grimsrud PA, den Os D, Wenger CD, Swaney DL, Schwartz D, Sussman MR, Ané JM, Coon JJ (2010) Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol 152: 19-28.
41. Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138: 226-237.
42. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10: 453-460.
43. Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17: 1376-1386.
44. 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. Plant Cell 21: 3119-3132.
45. Gy I, Gasciolli V, Lauressergues D, Morel JB, Gombert J, Proux F, Proux C, Vaucheret H, Mallory AC (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19: 3451-3461.
46. Hamann T, Mayer U, Jürgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation andapical-basal patterning in the Arabidopsis embryo. Development 126: 1387-1395.
47. Hennig L, Taranto P, Walser M, Schönrock N, Gruissem W (2003) Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130: 2555-2565.
48. Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144: 752-767.
49. Hernández G, Valdés-López O, Ramírez M, Goffard N, Weiller G, Aparicio-Fabre R, Fuentes SI, Erban A, Kopka J, Udvardi MK, Vance CP (2009) Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiol 151: 1221-1238.
50. Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2007) The auxin-regulated AP2/EREBP gene PUCHI is required foorphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19: 2156-2168.
51. Hochholdinger F, Zimmermann R (2008) Conserved and diverse mechanisms in root development. Curr Opin Plant Biol 11: 70-74.
52. Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151: 2120-2132.
53. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42: 541-544.
54. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787-799.
55. Joshi T, Yan Z, Libault M, Jeong DH, Park S, Green PJ, Sherrier DJ, Farmer A, May G, Meyers BC, Xu D, Stacey G (2010) Prediction of novel miRNAs and associated target genes in Glycine max. BMC Bioinformatics 11(1): S14.
56. Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004) Root-to- shoot transport of sulphate in Arabidopsis: evidence for the role of SULTR3; 5 as a component of low-affinity sulphate transport system in the root vasculature. Plant Physiol 136: 4198-4204.
57. Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57: 313-321.
58. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435: 446-451.
59. Kutz A, Muller A, Henning P, Kaiser WM, Piotrowsky M, Weiler EW (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J 30: 95-106.
60. Laux T, Würschum T, Breuninger H (2004) Genetic regulation of embryonic pattern formation. Plant Cell 16: S190-S202.
61. Lelandais-Brière C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M (2009) Genome-wide small RNA analysis revealed differentially regulated miRNA isoforms in Medicago truncatula roots and nodules. Plant Cell 21: 2780-2796.
62. Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou, Hassan H, Nakajima K, Matsumoto N, Lohmann JU, Scheres B, Benfey PN (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol 4: e143.
63. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20: 2238-2251.
64. Li H, Deng Y, Wu T, Subramanian S, Yu O (2010) Misexpression of miR482, miR1512, and miR1515 increases soybean nodulation. Plant Physiol 153: 1759-1770.
65. Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62: 1046-1057.
66. Linkohr BI, Williamson LC, Fitter AH, Leyser HM (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29: 751-760.
67. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280-287.
68. Lundmark M, Kørner CJ, Nielsen TH (2010) Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol Plant 140: 57-68.
69. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33-44.
70. 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. Plant Cell 17: 1360-1375.
71. Maraschin FS, Memelink J, Offringa R (2009) Auxin induced, SCFTIR1-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. Plant J 59: 100-109.
72. Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume CrespiM, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22: 1104-1117.
73. Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de La Peña A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24: 559-567.
74. 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.
75. Meng Y, Ma X, Chen D, Wu P, Chen M (2010) MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun 393: 345-349.
76. Naya L, Khan GA, Sorin C, Hartmann C, Crespi M, Lelandais-Brière C (2010) Cleavage of a non-conserved target by a specific miR156 isoform in root apexes of Medicago truncatula. Plant Signal Behav 5: 328-331.
77. Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev of Plant Bio 59: 519-546.
78. Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58: 93-113.
79. Overvoorde P, Fukaki H, Beeckman T. (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2(6): a001537.
80. Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53: 731-738.
81. Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14: 399-408.
82. Petricka JJ, Benfey PN (2008) Root layers: complex regulation of developmental patterning. Curr Opin Genet Dev 18: 354-361.
83. Prigge MJ, Wagner DR (2001) The Arabidopsis SERRATE gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 13: 1263-1279.
84. Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137: 103-112.
85. Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of the Arabidopsis primary root and root-meristem initials. Development 120: 2475-2487.
86. Simon SA, Meyers BC, Sherrier DJ (2009) MicroRNAs in the rhizobia legume symbiosis. Plant Physiol 151: 1002-1008.
87. Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, Geiss G, McKhann H, Garcion C, Vaucheret H, Sandberg G, Bellini C (2005) Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17: 1343-1359.
88. Stone J, Liang X, Nekl E, Stiers J (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41: 744-754.
89. Subramanian S, Fu Y, Sunkar R, Barbazuk BW, Zhu JK, Yu O (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9: 160.
90. Takahashi H (2010) Regulation of sulfate transport and assimilation in plants. Int Rev Cell Mol Biol 281: 129-159.
91. Thole JM, Vermeer JE, Zhang Y, Gadella TW, Nielsen E (2008) Root hair defective4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20: 381-395.
92. Tian CE, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J 40: 333-343.
93. Ueda M, Koshino-Kimura Y, Okada K (2005) Stepwise understanding of root development. Curr Opin Plant Biol 8: 71-76.
94. Ulmasov T, Hagen G, Guilfoyle TJ (1999) Dimerization and DNA binding of auxin response factors. Plant J 19: 309-319.
95. Valdés-López O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187: 805-818.
96. Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci 107: 4477-4482.
97. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669-687.
98. 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. Plant Cell 17: 2204-2216.
99. Wang Y, Li P, Cao X, Wang X, Zhang A, Li X (2009) Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochem Biophys Res Commun 378: 799-803.
100. Wang J, Gao X, Li L, Shi X, Zhang J, Shi Z (2010) Overexpression of Osta-siR2141 caused abnormal polarity establishment and retarded growth in rice. J Exp Bot 61: 1885-1895.
101. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126: 875-882.
102. Xiong L, Lee Bh, Ishitani M, Lee H, Zhang C, Zhu JK (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev 15: 1971-1984.
103. Xiong L, Wang RG, Mao G, Koczan JM (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic Acid. Plant Physiol 142: 1065-1074.
104. Yang L, Liu ZQ, Lu F, Dong AW, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47: 841-850.
105. Zeng CJ, Lee YR, Liu B (2009) The WD40 repeat protein NEDD1 Functions in microtubule organization during cell division in Arabidopsis thaliana. Plant Cell 21: 1129-1140.
106. Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J Plant Physiol 167: 1289-1297.
107. Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10: 29.
108. Zhou GK, Kubo M, Zhong R, Demura T, Ye ZH (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48: 391-404.