Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus

New Phytologist

Volumn 191, Issue 1, 2011, Pages 251-263

  Scoville, Alison G ^a   Barnett, Laryssa L ^a   Bodbyl Roels, Sarah ^a   Kelly, John K ^a   Hileman, Lena C ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Maternal effects; Mimulus guttatus (yellow monkeyflower); MYB transcription factors; Phenotypic plasticity; Soft inheritance; Transgenerational epigenetic inheritance; Trichome density; Wound response

Indexed keywords

PROTEIN C MYB; VEGETABLE PROTEIN;

CHROMOSOME; DAMAGE; DICOTYLEDON; ENVIRONMENTAL FACTOR; GENE EXPRESSION; HERBIVORE; HERITABILITY; LIFE HISTORY TRAIT; MOLECULAR ANALYSIS; PARENTAGE; PHENOTYPIC PLASTICITY; TRICHOME; WOUNDING;

ARTICLE; CHEMISTRY; ENVIRONMENT; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HISTOLOGY; METABOLISM; MIMULUS; MOLECULAR EVOLUTION; PHENOTYPE; PHYLOGENY;

ENVIRONMENT; EPIGENESIS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; MIMULUS; PHENOTYPE; PHYLOGENY; PLANT PROTEINS; PROTO-ONCOGENE PROTEINS C-MYB;

MIMULUS (ANGIOSPERM); MIMULUS GUTTATUS;

EID: 79957914627     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.03656.x     Document Type: Article

References (95)

1. Agrawal AA, Laforsch C, Tollrian R. 1999. Transgenerational induction of defences in animals and plants. Nature 401: 60-63.
2. Agren J, Schemske DW. 1993. The cost of defense against herbivores: an experimental study of trichome production in Brassica rapa. American Naturalist 141: 338-350.
3. Almeida J, Rocheta M, Galego L. 1997. Genetic control of flower shape in Antirrhinum majus. Development 124: 1387-1392.
4. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped Blast and Psi-Blast: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
5. Anway MD, Cupp AS, Uzumcu M, Skinner MK. 2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308: 1466-1469.
6. Arathi HS, Kelly JK. 2004. Corolla morphology facilitates both autogamy and bumble bee pollination in Mimulus Guttatus. International Journal of Plant Sciences 165: 1039-1045.
7. Ariel FD, Manavella PA, Dezar CA, Chan RL. 2007. The true story of the HD-Zip family. Trends in Plant Science 12: 419-426.
8. Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin HL, Koes R, Roberts K, Martin C. 2007. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134: 1691-1701.
9. Becskei A, Seraphin B, Serrano L. 2001. Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion. EMBO Journal 20: 2528-2535.
10. 3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 49: 1117-1119.
11. Bonduriansky R, Day T. 2009. Nongenetic inheritance and its evolutionary implications. Annual Review of Ecology, Evolution, and Systematics 40: 103-125.
12. 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. Evolutionary Ecology 24: 541-553.
13. Bossdorf O, Richards CL, Pigliucci M. 2008. Epigenetics for ecologists. Ecology Letters 11: 106-115.
14. Chandler VL. 2007. Paramutation: from maize to mice. Cell 128: 641-645.
15. Chandler VL, Eggleston WB, Dorweiler JE. 2000. Paramutation in maize. Plant Molecular biology 43: 121-145.
16. Chen YH, Yang XY, He K, Liu MH, Li JG, Gao ZF, Lin ZQ, Zhang YF, Wang XX, Qiu XM et al. 2006. The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Molecular biology 60: 107-124.
17. Crews D, Gore AC, Hsu TS, Dangleben NL, Spinetta M, Schallert T, Anway MD, Skinner MK. 2007. Transgenerational epigenetic imprints on mate preference. Proceedings of the National Academy of Sciences, USA 104: 5942-5946.
18. vy allele by nutritional supplementation. Proceedings of the National Academy of Sciences, USA 103: 17308-17312.
19. Cubas P, Vincent C, Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157-161.
20. Daxinger L, Whitelaw E. 2010. Transgenerational epigenetic inheritance: more questions than answers. Genome Research 20: 1623-1628.
21. Edgar RC. 2004a. Muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 1-19.
22. Edgar RC. 2004b. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797.
23. Elle E, Hare JD. 2000. No benefit of glandular trichome production in natural populations of Datura wrightii? Oecologia 123: 57-65.
24. Fieldes MA. 1994. Heritable effects of 5-azacytidine treatments on the growth and development of flax (Linum usitatissimum) genotrophs and genotypes. Genome 37: 1-11.
25. Fieldes MA, Schaeffer SM, Krech MJ, Brown JCL. 2005. DNA hypomethylation in 5-azacytidine-induced early-flowering lines of flax. Theoretical and Applied Genetics 111: 136-149.
26. Fyvie MJ, Murray JAH, Kilby NJ. 2000. Mosaic analysis of GL2 gene expression and cell layer autonomy during the specification of Arabidopsis leaf trichomes. Genesis 28: 68-74.
27. Galego L, Almeida J. 2002. Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes and Development 16: 880-891.
28. Gilding EK, Marks MD. 2010. Analysis of purified glabra3-shapeshifter trichomes reveals a role for NOECK in regulating early trichome morpholgenic events. Plant Journal 64: 304-317.
29. Glover BJ, Perez-Rodriguez M, Martin C. 1998. Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development 125: 3497-3508.
30. Guan XY, Li QJ, Shan CM, Wang S, Mao YB, Wang LJ, Chen XY. 2008. The HD-Zip IV Gene GaHOX1 from cotton is a functional homologue of the Arabidopsis GLABRA2. Physiologia Plantarum 134: 174-182.
31. Hall MC, Basten CJ, Willis JH. 2006. Pleiotropic quantitative trait loci contribute to population divergence in traits associated with life-history variation in Mimulus guttatus. Genetics 172: 1829-1844.
32. Hall MC, Willis JH. 2006. Divergent selection on flowering time contributes to local adaptation in Mimulus guttatus populations. Evolution 60: 2466-2477.
33. Holeski LM. 2007. Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus. Journal of Evolutionary Biology 20: 2092-2100.
34. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: bayesian inference of phylogeny. Bioinformatics 17: 754-755.
35. Hülskamp M. 2004. Plant trichomes: a model for cell differentiation. Nature Reviews Molecular Cell Biology 5: 471-480.
36. Humphries JA, Walker AR, Timmis JN, Orford SJ. 2005. Two WD-repeat genes from cotton are functional homologues of the Arabidopsis thaliana TRANSPARENT TESTA GLABRA1 (TTG1) gene. Plant Molecular biology 57: 67-81.
37. Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S et al. 2007. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19: 2531-2543.
38. Ishida T, Kurata T, Okada K, Wada T. 2008. A genetic regulatory network in the development of trichomes and root hairs. Annual Review of Plant Biology 59: 365-386.
39. Jablonka E, Lamb MJ. 2008. Soft inheritance: challenging the modern synthesis. Genetics and Molecular Biology 31: 389-395.
40. Jablonka E, Oborny B, Molnar I, Kisdi E, Hofbauer J, Czaran T. 1995. The adaptive advantage of phenotypic memory in changing environments. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 350: 133-141.
41. Jablonka E, Raz G. 2009. Transgenerational epigenetic inheritance: prevelence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology 84: 131-176.
42. Jacobsen SE, Meyerowitz EM. 1997. Hypermethylated superman epigenetic alleles in Arabidopsis. Science 277: 1100-1103.
43. Jaffe FW, Tattersall A, Glover BJ. 2007. A truncated MYB transcription factor from Antirrhinum majus regulates epidermal cell outgrowth. Journal of Experimental Botany 58: 1515-1524.
44. Jakoby MJ, Falkenhan D, Mader MT, Brininstool G, Wischnitzki E, Platz N, Hudson A, Hulskamp M, Larkin J, Schnittger A. 2008. Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-like transcriptional regulator MYB106. Plant Physiology 148: 1583-1602.
45. Johannes F, Colot C, Jansen RC. 2008. Epigenome dynamics: a quantitative genetics perspective. Nature Reviews Genetics 9: 883-890.
46. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P. 2009. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genetics 5: 1-11.
47. Kakutani T, Munakata K, Richards EJ, Hirochika H. 1999. Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics 151: 831-838.
48. Kalisz S, Purugganan MD. 2004. Epialleles via DNA methylation: consequences for plant evolution. Trends in Ecology and Evolution 19: 309-314.
49. Larkin JC, Brown ML, Schiefelbein J. 2003. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annual Review of Plant Biology 54: 403-430.
50. Levin DA. 1973. The role of trichomes in plant defense. Quarterly Review of Biology 48: 3-15.
51. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD. 2004. Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471-476.
52. Lippman Z, May B, Yordan C, Singer T, Martienssen R. 2003. Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biology 1: 420-428.
53. Lynch M, Walsh JB. 1998. Genetics and analysis of quantitative traits. Sunderland, MA, USA: Sinauer Associates.
54. Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES. 2009. The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant Journal 59: 52-62.
55. Maddison DR, Maddison WP. 2003. MacClade, version 4.06. Sunderland, MA, USA: Sinauer Associates.
56. Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB. 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-Box transcription factor inhibits tomato fruit ripening. Nature Genetics 38: 948-952.
57. Matzke MA, Birchler JA. 2005. RNAi-mediated pathways in the nucleus. Nature Reviews Genetics 6: 24-35.
58. Mauricio R. 1998. Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. American Naturalist 151: 20-28.
59. Mayr E. 1980. Prologue: Some thoughts on the history of the evolutionary synthesis. In: Mayr E, Provine WB, eds. The evolutionary synthesis: perspectives on the unification of biology. Cambridge, MA, USA: Harvard University Press, 1-48.
60. Mayr E. 1982. The growth of biological thought. Cambridge, MA, USA: Harvard University Press.
61. Newbold RR, Padilla-Banks E, Jefferson WN. 2006. Adverse effects of the model environmental estrogen Diethylstilbestrol are transmitted to subsequent generations. Endocrinology 147: S11-S17.
62. Ohashi Y, Oka A, Ruberti I, Morelli G, Aoyama T. 2002. Entopically additive expression of GLABRA2 alters the frequency and spacing of trichome initiation. Plant Journal 29: 359-369.
63. Payne T, Clement J, Arnold D, Lloyd A. 1999. Heterologous MYB genes distinct from GL1 enhance trichome production when overexpressed in Nicoliana tabacum. Development 126: 671-682.
64. Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C. 2005. Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132: 359-370.
65. Pesch M, Hulskamp M. 2004. Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. Current Opinion in Genetics & Development 14: 422-427.
66. Ramsay NA, Glover BJ. 2005. MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends in Plant Science 10: 63-70.
67. Rangwala SH, Elumalai R, Vanier C, Ozkan H, Galbraith DW, Richards EJ. 2006. Meiotically stable natural epialleles of Sadhu, a novel Arabidopsis retroposon. PLoS Genetics 2: 270-281.
68. Rapp RA, Wendel JF. 2005. Epigenetics and plant evolution. New Phytologist 168: 81-91.
69. Rasmussen R. 2000. Quantification on the lightcycler. In: Meuer S, Wittwer C, Nakagawara K, eds. Rapid cycle real-time PCR, methods and applications. Heidelberg: Springer Press, 21-34.
70. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, Cuzin F. 2006. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441: 469-474.
71. Rerie WG, Feldmann KA, Marks MD. 1994. The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes & Development 8: 1388-1399.
72. Richards EJ. 2006. Inherited epigenetic variation - revisiting soft inheritance. Nature Reviews Genetics 7: 395-401.
73. Richards EJ. 2008. Population epigenetics. Current Opinion in Genetics & Development 18: 221-226.
74. Richards CL, Bossdorf O, Pigliucci M. 2010. What role does heritable epigenetic variation play in phenotypic evolution? BioScience 60: 232-237.
75. Romeis J, Shanower TG, Peter AJ. 1999. Trichomes on pigeonpea (Cajanus Cajan (L.) Millsp.) and two wild Cajanus spp. Crop Science 39: 564-569.
76. Rossiter MC. 1996. Incidence and consequences of inherited environmental effects. Annual Review of Ecology & Systematics 27: 451-476.
77. 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. Molecular and General Genetics 220: 441-447.
78. Schiefelbein J. 2003. Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Current Opinion in Plant Biology 6: 74-78.
79. Serna L. 2004. A network of interacting factors triggering different cell fates. Plant Cell 16: 2258-2263.
80. Serna L, Martin C. 2006. Trichomes: different regulatory networks lead to convergent structures. Trends in Plant Science 11: 274-280.
81. Simon M, Lee MM, Lin Y, Gish L, Schiefelbein J. 2007. Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Developmental Biology 311: 566-578.
82. Suo JF, Liang XO, Pu L, Zhang YS, Xue YB. 2003. Identification of GhMYB109 encoding a R2R3 MYB transcription factor that expressed specifically in fiber initials and elongating fibers of cotton (Gossypium hirsutum L.). Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 1630: 25-34.
83. Szymanski DB, Jilk RA, Pollock SM, Marks MD. 1998. Control of GL2 expression in Arabidopsis leaves and trichomes. Development 125: 1161-1171.
84. Szymanski DB, Lloyd AM, Marks MD. 2000. Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis. Trends in Plant Science 5: 214-219.
85. Team RDC. 2008. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
86. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: 1-12.
87. Vaughn MW, Tanurdzic M, Lippman Z, Jiang H, Carrasquillo R, Rabinowicz PD, Dedhia N, McCombie WR, Agier N, Bulski A. 2007. Epigenetic natural variation in Arabidopsis thaliana. PLoS Biology 5: 1617-1629.
88. Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A. 2010. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytologist 185: 1108-1118.
89. Wang SC, Chen JG. 2008. Arabidopsis transient expression analysis reveals the activation of GLABRA2 may require concurrent binding of GLABRA1 and GLABRA3 to the promoter of GLABRA2. Plant and Cell Physiology 49: 1792-1804.
90. Wang SC, Kwak SH, Zeng QN, Ellis BE, Chen XY. 2007. TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134: 3873-3882.
91. Wang S, Wang JW, Yu N, Li CH, Luo B, Gou JY, Wang LJ, Chen XY. 2004. Control of plant trichome development by a cotton fiber MYB gene. Plant Cell 16: 2323-2334.
92. Willis JH. 1999. The role of genes of large effect on inbreeding depression in Mimulus guttatus. Evolution 53: 1678-1691.
93. Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW, Willis JH. 2008. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100: 220-230.
94. Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd A. 2008. The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135: 1991-1999.
95. Zwickl DJ. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, University of Texas, Austin, TX, USA.