Changes in histone methylation and acetylation during microspore reprogramming to embryogenesis occur concomitantly with bnHKMT and BnHAT expression and are associated with cell totipotency, proliferation, and differentiation in brassica napus

Cytogenetic and Genome Research

Volumn 143, Issue 1-3, 2014, Pages 209-218

  Rodríguez Sanz, Héctor ^a   Moreno Romero, Jordi ^b   Solís, María Teresa ^a   Köhler, Claudia ^b   Risueño, María C ^a   Testillano, Pilar S ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Chromatin; Epigenetics; H3Ac; H3K9me2; H4Ac; Histone acetyl transferases; Histone methyl transferases; Pollen embryogenesis

Indexed keywords

HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE H3; HISTONE H3K9; HISTONE H4; HISTONE LYSINE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

APICAL MERISTEM; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO CELL; EMBRYO DEVELOPMENT; EPIGENETICS; HISTONE ACETYLATION; HISTONE METHYLATION; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE TEST; MICROSPORE; MICROSPORE CULTURE; NONHUMAN; NUCLEAR REPROGRAMMING; PLANT CELL; PLANT DEVELOPMENT; PLANT GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAPESEED; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TOTIPOTENT STEM CELL; TRANSCRIPTION INITIATION; UPREGULATION; WESTERN BLOTTING; BNHAT GENE; BNHKMT GENE; GENE EXPRESSION PROFILING;

BRASSICA NAPUS;

ACETYLATION; BRASSICA NAPUS; CELL DIFFERENTIATION; CELL PROLIFERATION; HAPLOIDY; HISTONE ACETYLTRANSFERASES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LYSINE; METHYLATION; POLLEN; SEEDS; TOTIPOTENT STEM CELLS;

EID: 84906794830     PISSN: 14248581     EISSN: 1424859X     Source Type: Journal    
DOI: 10.1159/000365261     Document Type: Article

References (42)

1. Banaei-Moghaddam AM, Schubert V, Kumke K, Weib O, Klemme S, et al: Non-disjunction in favor of a chromosome: the mechanism of rye B chromosome drive during pollen mitosis. Plant Cell 24: 4124-4134 (2012).
2. Bárány I, González-Melendi P, Mityko J, Fadón B, Risueño MC, Testillano PS: Microspore-derived embryogenesis in Capsicum annuum : subcellular rearrangements through development. Biol Cell 97: 709-722 (2005).
3. Bárány I, Fadón B, Risueño MC, Testillano PS: Cell wall components and pectin esterification levels as markers of proliferation and differentiation events during pollen development and embryogenesis. J Exp Bot 61: 1159-1175 (2010).
4. Costa M, Nobre MS, Becker JD, Masiero S, Amorim MI, et al: Expression-based and co-localization detection of arabinogalactan protein 6 and arabinogalactan protein 11 interactors in Arabidopsis pollen and pollen tubes. BMC Plant Biol 13: 7 (2013).
5. Earley KW, Shook MS, Brower-Toland B, Hicks L, Pikaard CS: In vitro specificities of Arabidopsis co-activator histone acetyltransferases: implications for histone hyperacetylation in gene activation. Plant J 52: 615-626 (2007).
6. El-Tantawy AA, Solís MT, Da Costa ML, Coimbra S, Risueño MC, Testillano PS: Arabinogalactan protein profiles and distribution patterns during microspore embryogenesis and pollen development in Brassica napus. Plant Reprod 26: 231-243 (2013).
7. González-Melendi P, Testillano PS, Ahmadian P, Fadón B, Vicente O, Risueño MC: In situ characterization of the late vacuolate microspore as a convenient stage to induce embryogenesis in Capsicum. Protoplasma 187: 60-71 (1995).
8. Grafi G, Florentin A, Ransbotyn V, Morgenstern Y: The stem cell state in plant development and in response to stress. Front Plant Sci 2: 53 (2011).
9. Hezroni H, Tzchori I, Davidi A, Mattout A, Biran A, et al: H3K9 histone acetylation predicts pluripotency and reprogramming capacity of ES cells. Nucleus 2: 300-309 (2011).
10. Hoffmann RD, Palmgren MG: Epigenetic repression of male gametophyte-specific genes in the Arabidopsis sporophyte. Mol Plant 6: 1176-1186 (2013).
11. Houben A, Kumke K, Nagaki K, Hause G: CENH3 distribution and differential chromatin modifications during pollen development in rye ( Secale cereale L.). Chromosome Res 19: 471-480 (2011).
12. Köhler C, Wolff P, Spillane C: Epigenetic mechanisms underlying genomic imprinting in plants. Annu Rev Plant Biol 63: 331-352 (2012).
13. Kouzarides T: Chromatin modifications and their function. Cell 128: 693-705 (2007).
14. Latrasse D, Benhamed M, Henry Y, Domenichini S, Kim W, et al: The MYST histone acetyltransferases are essential for gametophyte development in Arabidopsis. BMC Plant Biol 8: 121 (2008).
15. Law DR, Shuttle JC: Changes in histone H3 and H4 multi-acetylation during natural and forced dormancy break in potato tubers. Physiol Plant 120: 642-649 (2004).
16. Leeb M, Wutz A: Establishment of epigenetic patterns in development. Chromosoma 121: 251-262 (2012).
17. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, et al: Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471-476 (2004).
18. Liu C, Lu F, Cui X, Cao X: Histone methylation in higher plants. Annu Rev Plant Biol 61: 395-420 (2010).
19. Liu C, Xu D, Han H, Fan Y, Schain F, et al: Transcriptional regulation of 15-lipoxygenase expression by histone H3 lysine 4 methylation/demethylation. PLoS One 7:e52703 (2012).
20. Liu X, Luo M, Zhang W, Zhao J, Zhang J, et al: Histone acetyltransferases in rice ( Oryza sativa L.): phylogenetic analysis, subcellular localization and expression. BMC Plant Biol 12: 145 (2012).
21. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2 CT method. Methods 25: 402-408 (2001).
22. Maluszynski M, Kasha KJ, Forster BP, Szarejko I: Doubled Haploid Production in Crop Plants-A Manual (Kluwer Academic Publisher, Dordrecht 2003).
23. Meijón M, Valledor L, Santamaría E, Testillano PS, Risueño MC, et al: Epigenetic characterization of the vegetative and floral stages of azalea buds: dynamics of DNA methylation and histone H4 acetylation. J Plant Physiol 166: 1624-1636 (2009).
24. Nelissen H, Fleury D, Bruno L, Robles P, De Veylder L, et al: The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc Natl Acad Sci USA 102: 7754-7759 (2005).
25. Onder TT, Kara N, Cherry A, Sinha AU, Zhu N, et al: Chromatin-modifying enzymes as modulators of reprogramming. Nature 483: 508-602 (2012).
26. Pandey R, Muller A, Napoli CA, Selinger DA, Pikaard CS, et al: Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30: 5036-5055 (2002).
27. Prem D, Solís MT, Bárány I, Rodríguez-Sanz H, Risueño MC, Testillano PS: A new microspore embryogenesis system under low temperature which mimics zygotic embryogenesis initials, expresses auxin and efficiently regenerates doubled-haploid plants in Brassica napus. BMC Plant Biol 12: 127 (2012).
28. Rodríguez-Serrano M, Bárány I, Prem D, Coronado MJ, Risueño MC, Testillano PS: NO, ROS and cell death associated with caspaselike activity increase in stress-induced microspore embryogenesis of barley. J Exp Bot 63: 2007-2024 (2012).
29. Rybaczek D, Maszewski J: Phosphorylation of H2AX histones in response to double-strand breaks and induction of premature chromatin condensation in hydroxyurea-treated root meristem cells of Raphanus sativus , Vicia faba , and Allium porrum. Protoplasma 230: 31-39 (2007).
30. Saze H, Tsugane K, Kanno T, Nishimura T: DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol 53: 766-784 (2012).
31. Seguí-Simarro JM, Corral-Martínez P, Corredor E, Raska I, Testillano PS, Risueño MC: A change of developmental program induces the remodelling of the interchromatin domain during microspore embryogenesis in Brassica napus L. J Plant Physiol 168: 746-757 (2011).
32. Servet C, Conde-Silva N, Zhou DX: Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Mol Plant 3: 670-677 (2010).
33. Solís MT, Rodríguez-Serrano M, Meijón M, Cañal MJ, Cifuentes A, et al: DNA methylation dynamics and MET1a-like gene expression changes during stress-induced pollen reprogramming to embryogenesis. J Exp Bot 63: 6431-6444 (2012).
34. Solís MT, Chakrabarti N, Corredor E, Cortés-Eslava J, Rodríguez-Serrano M, et al: Epigenetic changes accompany developmental programmed cell death in tapetum cells. Plant Cell Physiol 55: 16-29 (2014).
35. Stancheva I: Caught in conspiracy: cooperation between DNA methylation and histone H3K9 methylation in the establishment and maintenance of heterochromatin. Biochem Cell Biol 83: 385-395 (2005).
36. Testillano PS, Coronado MJ, Seguí JM, Domenech J, González-Melendi P, et al: Defined nuclear changes accompany the reprogramming of the microspore to embryogenesis. J Struct Biol 129: 223-232 (2000).
37. Testillano PS, González-Melendi P, Coronado MJ, Seguí JM, Moreno MA, Risueño MC: Differentiating plant cells switched to proliferation remodel the functional organization of nuclear domains. Cytogenet Genome Res 109: 166-174 (2005).
38. Testillano PS, Solís MT, Risueño MC: The 5-methyl-deoxy-cytidine (5mdC) localization to reveal in situ the dynamics of DNA methylation chromatin pattern in a variety of plant organ and tissue cells during development. Physiol Plant 149: 104-113 (2013).
39. Thorstensen T, Fischer A, Sandvik SV, Johnsen SS, Grini PE, et al: The Arabidopsis SUVR4 protein is a nucleolar histone methyltransferase with preference for monomethylated H3K9. Nucleic Acid Res 34: 5461-5470 (2006).
40. Xu CR, Liu C, Wang YL, Li LC, Chen WQ, et al: Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis. Proc Natl Acad Sci USA 102: 14469-14474 (2005).
41. Yaish MW, Colasanti J, Rothstein SJ: The role of epigenetic processes in controlling flowering time in plants exposed to stress. J Exp Bot 62: 3727-3735 (2011).
42. Zhou J, Wang X, He K, Charron JB, Elling AA, Deng XW: Genome-wide profiling of histone H3 lysine 9 acetylation and dimethylation in Arabidopsis reveals correlation between multiple histone marks and gene expression. Plant Mol Biol 72: 585-595 (2010).