Changes in micro RNA expression in a wild tuber-bearing Solanum species induced by 5-Azacytidine treatment

Plant Cell Reports

Volumn 31, Issue 8, 2012, Pages 1449-1461

  Marfil, Carlos F ^a   Asurmendi, Sebastian ^b   Masuelli, Ricardo W ^a,c  

^a Inst de Biologia Agricola de Mendoza Consejo Nacional de Investigaciones Cientificas y Tecnicas   (Argentina)

^b INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA   (Argentina)

^c INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

Author keywords

DNA methylation; Epigenetics; Micro RNAs; Phenotypic plasticity; Wild potato species

Indexed keywords

AZACITIDINE; CYTOSINE; MICRORNA;

ARTICLE; DNA METHYLATION; DRUG EFFECT; FLOWER; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; METABOLISM; PHENOTYPE; PHYSIOLOGY; PLANT GENE; PLANT LEAF; PLANT TUBER; SOLANUM; SPECIES DIFFERENCE;

AZACITIDINE; CYTOSINE; DNA METHYLATION; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MICRORNAS; PHENOTYPE; PLANT LEAVES; PLANT TUBERS; SOLANUM; SPECIES SPECIFICITY;

SOLANUM; SOLANUM JAMESII; SOLANUM RUIZ-LEALII; SOLANUM TUBEROSUM;

EID: 84864364957     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-012-1260-x     Document Type: Article

References (63)

1. Ahluwalia JK, Hariharan M, Bargaje R, Pillai B, Brahmachari V (2009) Incomplete penetrance and variable expressivity: is there a microRNA connection? BioEssays 31: 981-992.
2. Alvarez NMB, Peralta IE, Salas A, Spooner DM (2008) A morphological study of species boundaries of the wild potato Solanum brevicaule complex: replicated field trials in Peru. Plant Syst Evol 274: 37-45.
3. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15: 2730-2741.
4. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
5. Bazzini AA, Almasia NI, Manacorda CA, Mongelli VC, Conti G, Maroniche GA, Rodriguez MC, Distéfano AJ, Hopp HE, del Vas M, Asurmendi S (2009) Virus infection alters transcriptional activity of miR164a promoter in plants. BMC Plant Biol 9: 152s. ISSN: 1471-2229.
6. Bazzini AA, Manacorda CA, Tohge T, Conti G, Rodriguez MC, Nunes-Nesi A, Villanueva S, Fernie AR, Carrari F, Asurmendi S (2011) Metabolic and miRNA profiling of TMV infected plants reveals biphasic temporal changes. Plos One 6: e28466.
7. Bedogni MC, Camadro EL (2009) Morphological and molecular evidence of natural interspecific hybridization in the diploid potato Solanum kurtzianum from Argentina. Botany 87: 78-87.
8. Benetti R, Gonzalo S, Jaco I, Muñoz P, Gonzalez S, Schoeftner S, Murchison E, Andl T, Chen T, Klatt P, Li E, Serrano M, Millar S, Hannon G, Blasco MA (2008) A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat Struct Mol Biol 15: 268-279.
9. Berger Y, Harpaz-Saad S, Brand A, Melnik H, Sirding N, Alvarez JP, Zinder M, Samach A, Eshed Y, Ori N (2009) The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136: 823-832.
10. Bossdorf O, Arcuri D, Richards CL, Pigliucci M (2010) Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol Ecol 24: 541-553.
11. Brown JCL, De Decker MM, Fieldes MA (2008) A comparative analysis of developmental profiles for DNA methylation in 5-azacytidine-induced early-flowering flax lines and their control. Plant Sci 175: 217-225.
12. Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ (1993) DNA methylation, vernalization, and the initiation of flowering. Proc Natl Acad Sci USA 90: 287-291.
13. Cocciolone SM, Chopra S, Flint-Garcia SA, McMullen MD, Peterson T (2001) Tissue-specific patterns of a maize Myb transcription factor are epigenetically regulated. Plant J 5: 467-478.
14. Correll DS (1962) The potato and its wild relatives. Contributions from the Texas Research Foundation, Botanical Studies 4: 1-606.
15. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157-161.
16. Di Rienzo JA (2009) fgStatistics, version 2009. Córdoba, Argentina. http://sites. google. com/site/fgstatistics.
17. Egger G, Liang G, Aparicio A, Jones PA (2004) Epigenetics in human disease and prospects for epigenetic therapy. Nature 429: 457-463.
18. Erazzú LE, Camadro EL, Clausen AM (2009) Persistence over time, overlapping distribution and molecular indications of interspecific hybridization in wild potato populations of Northwest Argentina. Euphytica 168: 249-262.
19. Eriksson S, Böhlenius H, Moritz T, Nilsson O (2006) GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell 18: 2172-2181.
20. Fieldes MA, Amyot LM (1999) Epigenetic control of early flowering in flax lines induced by 5-azacytidine applied to germinating seed. J Heredity 90: 199-206.
21. Fieldes MA, Schaeffer SM, Krech MJ, Brown JCL (2005) DNA hypomethylation in 5-azacytidine-induced early-flowering lines of flax. Theor Appl Genet 111: 136-149.
22. Gutierrez L, Bussell JD, Pǎcurar DI, Schwambach J, Pǎcurar 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.
23. Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, Carrington JC, Chen X, Wang XJ, Chen ZJ (2009) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci USA 106: 17835-17840.
24. Hijmans RJ, Spooner DM, Salas AR, Guarino L, de la Cruz J (2002) Atlas of wild potatoes. International Plant Genetic Resources Institute, Rome.
25. Iwase Y, Shiraya T, Takeno K (2010) Flowering and dwarfism induced by DNA demethylation in Pharbitis nil. Physiol Plant 139: 118-127.
26. Jacobs MMJ, van den Berg RG, Vleeshouwers VGAA, Visser M, Mank R, Sengers M, Hoekstra R, Vosman B (2008) AFLP analysis reveals a lack of phylogenetic structure within Solanum section Petota. BMC Evol Biol 8: 145.
27. Jacobsen SE, Meyerowitz EM (1997) Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277: 1100-1103.
28. Janoušek B, Široký J, Vyskot B (1996) Epigenetic control of sexual phenotype in a dioecious plant, Melandrium album. Mol Gen Genet 250: 483-490.
29. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57: 19-53.
30. Jung J-H, Seo Y-H, Pil JS, Reyes JL, Yun J, Chua NH, Park CM (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19: 2736-2748.
31. Kalisz S, Purugganan MD (2004) Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol Evol 19: 309-314.
32. Khraiwesh B, Zhu J-K, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819: 137-148.
33. King GJ (1995) Morphological development in Brassica oleracea is modulated by in vivo treatment with 5-azacytidine. J Hort Sci 70: 333-342.
34. Kondo H, Miura T, Wada KC, Takeno K (2007) Induction of flowering by 5-azacytidine in some plant species: Relationship between the stability of photoperiodically induced flowering and flower-inducing effect of DNA demethylation. Physiol Plant 131: 462-469.
35. Kondo H, Shiraya T, Wada KC, Takeno K (2010) Induction of flowering by DNA demethylation in Perilla frutescens and Silene armeria: heritability of 5-azacytidine-induced effects and alteration of the DNA methylation state by photoperiodic conditions. Plant Sci 178: 321-326.
36. Li C, Zhang K, Zeng X, Jackson S, Zhou Y, Hong Y (2009) A cis element within Flowering Locus T mRNA determines its mobility and facilitates trafficking of heterologous viral RNA. J Virol 83: 3540-3548.
37. Lin MK, Belanger H, Lee YJ, Varkonyi-Gasic E, Taoka K, Miura E, Xoconostle-Cázares B, Gendler K, Jorgensen RA, Phinney B, Lough TJ, Lucas WJ (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the Cucurbits. Plant Cell 19: 1488-1506.
38. Marfil CF, Camadro EL, Masuelli RW (2009) Phenotypic instability and epigenetic variability in a diploid potato of hybrid origin, Solanum ruiz-lealii. BMC Plant Biol 9: 21.
39. Martin A, Adam H, Díaz-Mendoza M, Źurczak M, González-Schain ND, Suárez-López P (2009) Graft-transmissible induction of potato tuberization by the microRNA miR172. Development 136: 2873-2881.
40. Masuelli RW, Camadro EL, Erazzú LE, Bedogni MC, Marfil CF (2009) Homoploid hybridization in the origin and evolution of wild diploid potato species. Plant Syst Evol 277: 143-151.
41. Mathieu J, Yant LJ, Mürdter F, Küttner F, Schmid M (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol 7: e1000148.
42. McClelland M, Nelson M, Raschke E (1994) Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nuc Acids Res 22: 3640-3659.
43. Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG (2006) MicroRNA promoter element discovery in Arabidopsis. RNA 12: 1612-1619.
44. Miller JT, Spooner DM (1999) Collapse of species boundaries in the wild potato Solanum brevicaule complex (Solanaceae, sect. Petota): Molecular data. Plant Syst Evol 214: 103-130.
45. Mlotshwa S, Yang Z, Kim Y, Chen X (2006) Floral patterning defects induced by ArabidopsisAPETALA2 and microRNA172 expression in Nicotiana benthamiana. Plant Mol Biol 61: 781-793.
46. Nicot N, Hausman J-F, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56: 2907-2914.
47. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nuc Acids Res 30: e36.
48. Raimondi JP, Peralta IE, Masuelli RW, Feingold S, Camadro EL (2005) Examination of the hybrid origin of the wild potato Solanum ruiz-lealii Brücher. Plant Syst Evol 253: 33-51.
49. Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
50. Sano H, Kamada I, Youssefian S, Katsumi M, Wabiko H (1990) A single treatment of rice seedlings with 5-azacytidine induces heritable dwarfism and undermethylation of genomic DNA. Mol Gen Genet 220: 441-447.
51. Sato F, Tsuchiya S, Meltzer SJ, Shimizu K (2011) MicroRNAs and epigenetics. FEBS J 278: 1598-1609.
52. Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130: 6001-6012.
53. Sinkkonen L, Hugenschmidt T, Berninger P, Gaidatzis D, Mohn F, Artus-Revel CG, Zavolan M, Svoboda P, Filipowicz W (2008) MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nat Struct Mol Biol 15: 259-267.
54. Solis JS, Ulloa DM, Rodríguez LA (2007) Molecular description and similarity relationships among native germplasm potatoes (Solanum tuberosum ssp. tuberosum L.) using morphological data and AFLP markers. Elect J Biot 10: 436-443.
55. Soppe WJJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, Peeters AJ (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6: 791-802.
56. Spooner DM, Castillo RT (1997) Reexamination of series relationships of South American wild potatoes (Solanaceae: Solanum sect. Petota): evidence from chloroplast DNA restriction site variation. Amer J Bot 84: 671-685.
57. Spooner DM, McLean K, Ramsay G, Waugh R, Bryan GJ (2005) A single domestication for potato based on multilocus amplified fragment length polymorphism genotyping. Proc Natl Acad Sci USA 102: 14694-14699.
58. Stokes TL, Kunkel BN, Richards EJ (2002) Epigenetic variation in Arabidopsis disease resistance. Genes Dev 16: 171-182.
59. Stresemann C, Lyko F (2008) Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int J Cancer 123: 8-13.
60. Vyskot B, Koukalová B, Kovařík A, Sachambula L, Reynolds D, Bezděk M (1995) Meiotic transmission of a hypomethylated repetitive DNA family in tobacco. Theor Appl Genet 91: 659-664.
61. Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends Genet 26: 519-527.
62. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38: 465-475.
63. Zhang W, Luo Y, Gong X, Zeng W, Li S (2009) Computational identification of 48 potato microRNAs and their targets. Comput Biol Chem 33: 84-93.