MicroRNAs in trees

Plant Molecular Biology

Volumn 80, Issue 1, 2012, Pages 37-53

  Sun, Ying Hsuan ^a   Shi, Rui ^a   Zhang, Xing Hai ^a,b   Chiang, Vincent L ^a   Sederoff, Ronald R ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

Artificial microRNA; Gene regulation; MicroRNA; Plant development; Plant stress response; Woody plant

Indexed keywords

MESSENGER RNA; MICRORNA; PLANT RNA;

ARTICLE; BIOLOGICAL MODEL; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYLOGENY; TRANSGENIC PLANT; TREE;

GENE EXPRESSION REGULATION, PLANT; MICRORNAS; MODELS, GENETIC; PHYLOGENY; PLANTS, GENETICALLY MODIFIED; RNA, MESSENGER; RNA, PLANT; TREES;

EID: 84865414595     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-011-9864-z     Document Type: Article

References (127)

1. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18(10): 758-762.
2. Ahuja MR, Neale DB (2005) Evolution of genome size in conifers. Silvae Genet 54(3): 126-138.
3. Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36(12): 1282-1290.
4. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2): 207-221.
5. Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18(5): 1134-1151.
6. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T (2003) A uniform system for microRNA annotation. RNA 9(3): 277-279.
7. Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17(6): 1658-1673.
8. Barakat A, Wall K, Leebens-Mack J, Wang YJ, Carlson JE, Depamphilis CW (2007a) Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant J 51(6): 991-1003.
9. Barakat A, Wall PK, Diloreto S, Depamphilis CW, Carlson JE (2007b) Conservation and divergence of microRNAs in Populus. BMC Genom 8: 481.
10. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2): 281-297.
11. Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125(4): 655-664.
12. Beck CB (1988) Origin and evolution of gymnosperms. Columbia University Press, New York.
13. Böhle UR, Hilger HH, Martin WF (1996) Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proc Natl Acad Sci USA 93(21): 11740-11745.
14. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218(5): 683-692.
15. Bradshaw HD, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19(3): 306-313.
16. Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9(1): 49-56.
17. Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8(11): 884-896.
18. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303(5666): 2022-2025.
19. Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP, Flannigan MD, Hanson PJ, Irland LC, Lugo AE, Peterson CJ, Simberloff D, Swanson FJ, Stocks BJ, Wotton BM (2001) Climate change and forest disturbances. Bioscience 51(9): 723-734.
20. Darwin C (1859) The origin of species, Reprint edition. Random House, New York.
21. Dolgosheina EV, Morin RD, Aksay G, Sahinalp SC, Magrini V, Mardis ER, Mattsson J, Unrau PJ (2008) Conifers have a unique small RNA silencing signature. RNA 14(8): 1508-1515.
22. Du J, Mansfield SD, Groover AT (2009) The Populus homeobox gene ARBORKNOX2 regulates cell differentiation during secondary growth. Plant J 60(6): 1000-1014.
23. Du J, Miura E, Robischon M, Martinez C, Groover A (2011) The Populus Class III HD ZIP transcription factor POPCORONA affects cell differentiation during secondary growth of woody stems. PLoS ONE 6(2): e17458.
24. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2(2): e219.
25. Floyd SK, Bowman JL (2004) Gene regulation: ancient microRNA target sequences in plants. Nature 428(6982): 485-486.
26. Fornara F, Coupland G (2009) Plant phase transitions make a SPLash. Cell 138(4): 625-627.
27. German MA, Pillay M, Jeong DH, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R, De Paoli E, Lu C, Schroth G, Meyers BC, Green PJ (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26(8): 941-946.
28. Gleave AP, Ampomah-Dwamena C, Berthold S, Dejnoprat S, Karunairetnam S, Nain B, Wang Y-Y, Crowhurst RN, MacDiarmid RM (2008) Identification and characterisation of primary microRNAs from apple (Malus domestica cv. Royal Gala) expressed sequence tags. Tree Genet Genom 4(2): 343-358.
29. Groover AT (2005) What genes make a tree a tree? Trends Plant Sci 10(5): 210-214.
30. 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(5): 1376-1386.
31. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286(5441): 950-952.
32. Heisel SE, Zhang Y, Allen E, Guo L, Reynolds TL, Yang X, Kovalic D, Roberts JK (2008) Characterization of unique small RNA populations from rice grain. PLoS One 3(8): e2871.
33. Helfgott DM, Francisco-Ortega J, Santos-Guerra A, Jansen RK, Simpson BB (2000) Biogeography and breeding system evolution of the woody Bencomia alliance (Rosaceae) in Macaronesia based on ITS sequence data. Syst Bot 25(1): 82-97.
34. Jia X, Ren L, Chen Q-J, Li R, Tang G (2009a) UV-B-responsive microRNAs in Populus tremula. J Plant Physiol 166(18): 2046-2057.
35. Jia X, Wang WX, Ren L, Chen QJ, Mendu V, Willcut B, Dinkins R, Tang X, Tang G (2009b) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71(1-2): 51-59.
36. Jin H, Zhu JK (2010) A viral suppressor protein inhibits host RNA silencing by hooking up with Argonautes. Genes Dev 24(9): 853-856.
37. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14(6): 787-799.
38. 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(2): 313-321.
39. Kidner CA, Martienssen RA (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428(6978): 81-84.
40. Kirst M, Johnson AF, Baucom C, Ulrich E, Hubbard K, Staggs R, Paule C, Retzel E, Whetten R, Sederoff R (2003) Apparent homology of expressed genes from wood-forming tissues of loblolly pine (Pinus taeda L.) with Arabidopsis thaliana. Proc Natl Acad Sci USA 100(12): 7383-7388.
41. Klevebring D, Street NR, Fahlgren N, Kasschau KD, Carrington JC, Lundeberg J, Jansson S (2009) Genome-wide profiling of Populus small RNAs. BMC Genom 10: 620.
42. Ko J-H, Prassinos C, Han K-H (2006) Developmental and seasonal expression of PtaHB1, a Populus gene encoding a class III HD-Zip protein, is closely associated with secondary growth and inversely correlated with the level of microRNA (miR166). New Phytol 169(3): 469-478.
43. Lauter N, Kampani A, Carlson S, Goebel M, Moose SP (2005) MicroRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci USA 102(26): 9412-9417.
44. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5): 843-854.
45. Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res 38(9): 3081-3093.
46. Lev-Yadun S (1997) Fibres and fibre-sclereids in wild-type Arabidopsis thaliana. Ann Bot 80: 125-129.
47. Li B, Yin W, Xia X (2009) Identification of microRNAs and their targets from Populus euphratica. Biochem Biophys Res Commun 388(2): 272-277.
48. Li B, Qin Y, Duan H, Yin W, Xia X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62(11): 3765-3779.
49. Lin SI, Wang JG, Poon SY, Su CL, Wang SS, Chiou TJ (2005) Differential regulation of FLOWERING LOCUS C expression by vernalization in cabbage and Arabidopsis. Plant Physiol 137(3): 1037-1048.
50. Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52(1): 133-146.
51. Liu JQ, Allan DL, Vance CP (2010) Systemic signaling and local sensing of phosphate in common bean: cross-talk between photosynthate and microRNA399. Mol Plant 3(2): 428-437.
52. Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14(7): 1605-1619.
53. Lu S, Sun Y-H, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17(8): 2186-2203.
54. Lu C, Kulkarni K, Souret FF, MuthuValliappan R, Tej SS, Poethig RS, Henderson IR, Jacobsen SE, Wang W, Green PJ, Meyers BC (2006) MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res 16(10): 1276-1288.
55. Lu S, Sun Y-H, Amerson H, Chiang VL (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J 51(6): 1077-1098.
56. Lu S, Sun Y-H, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55(1): 131-151.
57. Lu S, Sun Y-H, Chiang VL (2009) Adenylation of plant miRNAs. Nucleic Acids Res 37(6): 1878-1885.
58. Martienssen RA (2010) Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis. New Phytol 186(1): 46-53.
59. Mathieu J, Yant LJ, Murdter F, Kuttner F, Schmid M (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol 7(7): e1000148.
60. Matzke M, Kanno T, Huettel B, Daxinger L, Matzke AJ (2007) Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10(5): 512-519.
61. Melzer S, Lens F, Gennen J, Vanneste S, Rohde A, Beeckman T (2008) Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nat Genet 40(12): 1489-1492.
62. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20(12): 3186-3190.
63. Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER, Sahinalp SC, Unrau PJ (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res 18(4): 571-584.
64. Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2(4): 279-289.
65. 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. Plant Cell 18(11): 2929-2945.
66. Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW, Yeh SD, Chua NH (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24(11): 1420-1428.
67. Oh TJ, Wartell RM, Cairney J, Pullman GS (2008) Evidence for stage-specific modulation of specific microRNAs (miRNAs) and miRNA processing components in zygotic embryo and female gametophyte of loblolly pine (Pinus taeda). New Phytol 179(1): 67-80.
68. Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I, Alvarez JP, Blum E, Zamir D, Eshed Y (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39(6): 787-791.
69. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955): 257-263.
70. 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(5): 731-738.
71. Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18(18): 2237-2242.
72. Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12(17): 1484-1495.
73. Pavy N, Johnson JJ, Crow JA, Paule C, Kunau T, MacKay J, Retzel EF (2007) ForestTreeDB: a database dedicated to the mining of tree transcriptomes. Nucleic Acids Res 35(Database issue): D888-D894.
74. Piriyapongsa J, Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14(5): 814-821.
75. Poethig RS (2010) The past, present, and future of vegetative phase change. Plant Physiol 154(2): 541-544.
76. Prabu GR, Mandal AKA (2010) Computational identification of miRNAs and their target genes from expressed sequence tags of tea (Camellia sinensis). Genom Proteom Bioinform 8(2): 113-121.
77. Qiu D, Pan X, Wilson IW, Li F, Liu M, Teng W, Zhang B (2009) High throughput sequencing technology reveals that the taxoid elicitor methyl jasmonate regulates microRNA expression in Chinese yew (Taxus chinensis). Gene 436(1-2): 37-44.
78. Ralph SG, Chun HJ, Kolosova N, Cooper D, Oddy C, Ritland CE, Kirkpatrick R, Moore R, Barber S, Holt RA, Jones SJ, Marra MA, Douglas CJ, Ritland K, Bohlmann J (2008) A conifer genomics resource of 200, 000 spruce (Picea spp.) ESTs and 6, 464 high-quality, sequence-finished full-length cDNAs for Sitka spruce (Picea sitchensis). BMC Genom 9: 484.
79. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16(13): 1616-1626.
80. Ridge CR, Hinckley TM, Stettler RF, van Volkenburgh E (1986) Leaf growth characteristics of fast-growing poplar hybrids Populus trichocarpa × P. deltoides. Tree Physiol 1(2): 209-216.
81. Robinson LW, Wareing PF (1969) Experiments on the juvenile-adult phase change in some woody species. New Phytol 68: 2.
82. Robischon M, Du J, Miura E, Groover A (2011) The Populus Class III HD ZIP, popREVOLUTA, influences cambium initiation and patterning of woody stems. Plant Physiol 155(3): 1214-1225.
83. Samish RM (1954) Dormancy in woody plants. Annu Rev Plant Physiol 5: 183-204.
84. Scheckler SE (2001) Afforestation - the first forest. In: Briggs DEG, Crowther PR (eds) Palaeobiology II. Blackwell Science, Oxford, pp 67-71.
85. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18(5): 1121-1133.
86. Sederoff R, Myburg A, Kirst M (2009) Genomics, domestication and evolution of forest trees. Cold Spring Harbor Symp Quantitat Biol 74: 303-317.
87. Shi R, Yang C, Lu S, Sederoff R, Chiang VL (2010) Specific down-regulation of PAL genes by artificial microRNAs in Populus trichocarpa. Planta 232(6): 1281-1288.
88. Simon SA, Meyers BC, Sherrier DJ (2009) MicroRNAs in the rhizobia legume symbiosis. Plant Physiol 151(3): 1002-1008.
89. Sinnott EW, Bailey IW (1915) Investigations on the phylogeny of the Angiosperms 5: Foliar evidence as to the ancestry and early climatic environment of the Angiosperms. Am J Bot 2(1): U1-U6.
90. Song C, Fang J, Li X, Liu H, Thomas Chao C (2009) Identification and characterization of 27 conserved microRNAs in citrus. Planta 230(4): 671-685.
91. Song C, Fang J, Wang C, Guo L, Nicholas KK, Ma Z (2010a) MiR-RACE, a new efficient approach to determine the precise sequences of computationally identified trifoliate orange (Poncirus trifoliata) microRNAs. PLoS ONE 5(6): e10861.
92. Song C, Wang C, Zhang C, Korir NK, Yu H, Ma Z, Fang J (2010b) Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genom 11: 431.
93. Stokstad E (2006) Genomics. Poplar tree sequence yields genome double take. Science 313(5793): 1556.
94. Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8): 2001-2019.
95. Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18(8): 2051-2065.
96. Talmor-Neiman M, Stav R, Frank W, Voss B, Arazi T (2006) Novel micro-RNAs and intermediates of micro-RNA biogenesis from moss. Plant J 47(1): 25-37.
97. Taylor G (2002) Populus: arabidopsis for forestry. Do we need a model tree? Ann Bot 90(6): 681-689.
98. Tomari Y, Matranga C, Haley B, Martinez N, Zamore PD (2004) A protein sensor for siRNA asymmetry. Science 306(5700): 1377-1380.
99. Tuskan GA (1998) Short-rotation woody crop supply systems in the United States: What do we know and what do we need to know? Biomass Bioenergy 14(4): 307-315.
100. Tuskan GA, Walsh ME (2001) Short-rotation woody crop systems, atmospheric carbon dioxide and carbon management: a US case study. Forestry Chronicle 77(2): 259-264.
101. Tuskan GA, DiFazio SP, Teichmann T (2004) Poplar genomics is getting popular: the impact of the poplar genome project on tree research. Plant Biol 6(1): 2-4.
102. Tuskan GA, Difazio S, Jansson S et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793): 1596-1604.
103. Varkonyi-Gasic E, Gould N, Sandanayaka M, Sutherland P, MacDiarmid RM (2010) Characterisation of microRNAs from apple (Malus domestica 'Royal Gala') vascular tissue and phloem sap. BMC Plant Biol 10: 159.
104. Vazquez F, Legrand S, Windels D (2010) The biosynthetic pathways and biological scopes of plant small RNAs. Trends Plant Sci 15(6): 337-345.
105. Victor M (2006) MicroRNAs in differentiating tissues of Populus and Eucalyptus trees. Thesis, University of Pretoria, Pretoria.
106. Voinnet O (2005) Non-cell autonomous RNA silencing. FEBS Lett 579(26): 5858-5871.
107. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4): 669-687.
108. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416(6879): 389-395.
109. 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(8): 2204-2216.
110. Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459(7245): 423-427.
111. Wang JW, Park MY, Wang LJ, Koo Y, Chen XY, Weigel D, Poethig S (2011) MiRNA control of vegetative phase change in trees. PLoS Genet 7(2): e1002012.
112. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18): 3539-3547.
113. Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4): 750-759.
114. Wullschleger SD, Jansson S, Taylor G (2002) Genomics and forest biology: Populus emerges as the perennial favorite. Plant Cell 14(11): 2651-2655.
115. Wullschleger S, Yin TM, DiFazio SP, Tschaplinski TJ, Gunter LE, Davis MF, Tuskan GA (2005) Phenotypic variation in growth and biomass distribution for two advanced-generation pedigrees of hybrid poplar. Can J For Res 35(8): 1779-1789.
116. Xu Q, Liu Y, Zhu A, Wu X, Ye J, Yu K, Guo W, Deng X (2010) Discovery and comparative profiling of microRNAs in a sweet orange red-flesh mutant and its wild type. BMC Genom 11: 246.
117. Yakovlev IA, Fossdal CG, Johnsen Ø (2010) MicroRNAs, the epigenetic memory and climatic adaptation in Norway spruce. New Phytol 187(4): 1154-1169.
118. Yu H, Song C, Jia Q, Wang C, Li F, Nicholas KK, Zhang X, Fang J (2011) Computational identification of microRNAs in apple expressed sequence tags and validation of their precise sequences by miR-RACE. Physiol Plant 141(1): 56-70.
119. Zeng Y, Wagner EJ, Cullen BR (2002) Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol Cell 9(6): 1327-1333.
120. Zeng C, Wang W, Zheng Y, Chen X, Bo W, Song S, Zhang W, Peng M (2010) Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants. Nucleic Acids Res 38(3): 981-995.
121. Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46(2): 243-259.
122. Zhang S, Zhou J, Han S, Yang W, Li W, Wei H, Li X, Qi L (2010) Four abiotic stress-induced miRNA families differentially regulated in the embryogenic and non-embryogenic callus tissues of Larix leptolepis. Biochem Biophys Res Commun 398(3): 355-360.
123. Zhang Y, Yu M, Yu H, Han J, Song C, Ma R, Fang J (2011) Computational identification of microRNAs in peach expressed sequence tags and validation of their precise sequences by miR-RACE. Mol Biol Rep, doi: 10. 1007/s11033-011-0944-6.
124. Zhebentyayeva TN, Swire-Clark G, Georgi LL, Garay L, Jung S, Forrest S, Blenda AV, Blackmon B, Mook J, Horn R, Howad W, Arús P, Main D, Tomkins JP, Sosinski B, Baird WB, Reighard GL, Abbott AG (2008) A framework physical map for peach, a model Rosaceae species. Tree Genet Genom 4(4): 745-756.
125. Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20(10): 2763-2782.
126. Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779(11): 780-788.
127. Zhou J, Zhuo R, Liu M, Qiao G, Jiang J, Li H, Qiu W, Zhang X, Lin S (2011) Identification and characterization of novel microRNAs from Populus cathayana Rehd. Plant Mol Biol Rep 29(1): 242-251.