HISTONE DEACETYLASE 9 represses seedling traits in Arabidopsis thaliana dry seeds

Plant Journal

Volumn 80, Issue 3, 2014, Pages 475-488

  Van Zanten, Martijn ^a,b   Zöll, Christian ^a   Wang, Zhi ^c   Philipp, Christina ^a   Carles, Annaick ^d,e   Li, Yong ^d,f   Kornet, Noortje G ^b,d   Liu, Yongxiu ^c   Soppe, Wim J J ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

^c INSTITUTE OF BOTANY   (China)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Arabidopsis thaliana; germination; HDA9; histone deacetylase; RuBisCO; seed dormancy

Indexed keywords

ACETYLATION; CULTIVATION; GENES; PLANTS (BOTANY);

ARABIDOPSIS THALIANA; GERMINATION; HDA9; HISTONE DEACETYLASES; RUBISCO; SEED DORMANCY;

SEED;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; HDA9 PROTEIN, ARABIDOPSIS; HISTONE DEACETYLASE; RIBULOSEBISPHOSPHATE CARBOXYLASE; TRANSCRIPTOME;

ARABIDOPSIS; CHROMATIN IMMUNOPRECIPITATION; DORMANCY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; META ANALYSIS; METABOLISM; PHYLOGENY; PHYSIOLOGY; PLANT SEED; SEEDLING; UPREGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, PLANT; GERMINATION; HISTONE DEACETYLASES; PHYLOGENY; PLANT DORMANCY; RIBULOSE-BISPHOSPHATE CARBOXYLASE; SEEDLING; SEEDS; TRANSCRIPTOME; UP-REGULATION;

EID: 84926507794     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12646     Document Type: Article

References (67)

1. Alinsug, M.V., Yu, C.W., and, Wu, K., (2009) Phylogenetic analysis, subcellular localization, and expression patterns of RPD3/HDA1 family histone deacetylases in plants. BMC Plant Biol. 9, 37.
2. Bedbrook, J.R., Coen, D.M., Beaton, A.R., Bogorad, L., and, Rich, A., (1979) Location of the single gene for the large subunit of ribulosebisphosphate carboxylase on the maize chloroplast chromosome. J. Biol. Chem. 254, 905-910.
3. Bentsink, L., Jowett, J., Hanhart, C.J., and, Koornneef, M., (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc. Natl Acad. Sci. USA, 103, 17042-17047.
4. Bentsink, L., Hanson, J., Hanhart, C.J., et al,. (2010) Natural variation for seed dormancy in Arabidopsis is regulated by additive genetic and molecular pathways. Proc. Natl Acad. Sci. USA, 107, 4264-4269.
5. Bowler, C., Benvenuto, G., Laflamme, P., Molino, D., Probst, A.V., Tariq, M., and, Paszkowski, J., (2004) Chromatin techniques for plant cells. Plant J. 39, 776-789.
6. Cadman, C.S., Toorop, P.E., Hilhorst, H.W., and, Finch-Savage, W.E., (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J. 46, 805-822.
7. Charron, J.B., He, H., Elling, A.A., and, Deng, X.W., (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell, 21, 3732-3748.
8. Chen, Z.J., and, Pikaard, C.S., (1997) Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev. 11, 2124-2136.
9. Cigliano, R.A., Cremona, G., Paparo, R., Termolino, P., Perrella, G., Gutzat, R., Consiglio, M.F., and, Conicella, C., (2013) Histone deacetylase AtHDA7 is required for female gametophyte and embryo development in Arabidopsis. Plant Physiol. 163, 431-440.
10. Colville, A., Alhattab, R., Hu, M., Labbé, H., Xing, T., and, Miki, B., (2011) Role of HD2 genes in seed germination and early seedling growth in Arabidopsis. Plant Cell Rep. 30, 1969-1979.
11. Comai, L., and, Harada, J.J., (1990) Transcriptional activities in dry seed nuclei indicate the timing of the transition from embryogeny to germination. Proc. Natl Acad. Sci. USA, 87, 2671-2674.
12. De Menezes, R.X., Boer, J.M., and, Van Houwelingen, J.C., (2004) Microarray data analysis: a hierarchical T-test to handle heteroscedasticity. Appl. Bioinformatics, 3, 229-235.
13. Demarsy, E., Buhr, F., Lambert, E., and, Lerbs-Mache, S., (2012) Characterization of the plastid-specific germination and seedling establishment transcriptional programme. J. Exp. Bot. 63, 925-939.
14. Fait, A., Angelovici, R., Less, H., Ohad, I., Urbanczyk-Wochniak, E., Fernie, A.R., and, Galili, G., (2006) Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol. 142, 839-854.
15. Finch-Savage, W.E., and, Leubner-Metzger, G., (2006) Seed dormancy and the control of germination. New Phytol. 171, 501-523.
16. Finch-Savage, W.E., Cadman, C.S., Toorop, P.E., Lynn, J.R., and, Hilhorst, H.W., (2007) Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J. 51, 60-78.
17. Finkelstein, R., Reeves, W., Ariizumi, T., and, Steber, C., (2008) Molecular aspects of seed dormancy. Annu. Rev. Plant Biol. 59, 387-415.
18. Finkemeier, I., Laxa, M., Miguet, L., Howden, A.J., and, Sweetlove, L.J., (2011) Proteins of diverse function and subcellular location are lysine acetylated in Arabidopsis. Plant Physiol. 155, 1779-1790.
19. Gardarin, A., Dürr, C., and, Colbach, N., (2011) Prediction of germination rates of weed species: relationships between germination speed parameters and species traits. Ecol. Modell. 222, 626-636.
20. Goda, H., Sasaki, E., Akiyama, K., et al. (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J. 55, 526-542.
21. Graeber, K., Nakabayashi, K., Miatton, E., Leubner-Metzger, G., and, Soppe, W.J.J., (2012) Molecular mechanisms of seed dormancy. Plant Cell Environ. 35, 1769-1786.
22. Grasser, M., Kane, C.M., Merkle, T., Melzer, M., Emmersen, J., and, Grasser, K.D., (2009) Transcript elongation factor TFIIS is involved in Arabidopsis seed dormancy. J. Mol. Biol. 386, 598-611.
23. Gu, X., Wang, Y., and, He, Y., (2013) Photoperiodic regulation of flowering time through periodic histone deacetylation of the florigen gene FT. PLoS Biol. 11, e1001649.
24. Guo, L., Zhou, J., Elling, A.A., Charron, J.B., and, Deng, X.W., (2008) Histone modifications and expression of light-regulated genes in Arabidopsis are cooperatively influenced by changing light conditions. Plant Physiol. 147, 2070-2083.
25. He, X. J., Chen, T., and, Zhu, J. K., (2011) Regulation and function of DNA methylation in plants and animals. Cell Res. 21, 442-465.
26. He, Y., Michaels, S.D., and, Amasino, R.M., (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science, 302, 1751-1754.
27. Holdsworth, M.J., Bentsink, L., and, Soppe, W.J.J., (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol. 179, 33-54.
28. Hollender, C., and, Liu, Z., (2008) Histone deacetylase genes in Arabidopsis development. J. Integr. Plant Biol. 50, 875-885.
29. Hong, F., Breitling, R., McEntee, C.W., Wittner, B.S., Nemhauser, J.L., and, Chory, J., (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics, 22, 2825-2827.
30. Izumi, M., Tsunoda, H., Suzuki, Y., Makino, A., and, Ishida, H., (2012) RBCS1A and RBCS3B, two major members within the Arabidopsis RBCS multigene family, function to yield sufficient Rubisco content for leaf photosynthetic capacity. J. Exp. Bot. 63, 2159-2170.
31. Joosen, R.V.L., Kodde, J., Willems, L.A.J., Ligterink, W., Van Der Plas, L.H.W., and, Hilhorst, H.W., (2010) GERMINATOR: a software package for high-throughput scoring and curve fitting of Arabidopsis seed germination. Plant J. 62, 148-159.
32. Kim, W., Latrasse, D., Servet, C., and, Zhou, D.X., (2012) Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19. Biochem. Biophys. Res. Commun. 432, 394-398.
33. Liu, Y., Koornneef, M., and, Soppe, W.J.J., (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell, 19, 433-444.
34. Liu, Y., Geyer, R., van Zanten, M., Carles, A., Li, Y., Hörold, A., Van Nocker, S., and, Soppe, W.J.J., (2011) Identification of the Arabidopsis REDUCED DORMANCY2 gene uncovers a role for the polymerase associated factor 1 complex in seed dormancy. PLoS ONE, 6, e22241.
35. (-ΔΔCT) method. Methods, 25, 402-408.
36. Loidl, P., (2004) A plant dialect of the histone language. Trends Plant Sci. 9, 84-90.
37. Lottaz, C., Yang, X., Scheid, S., and, Spang, R., (2006) OrderedList-a bioconductor package for detecting similarity in ordered gene lists. Bioinformatics, 22, 2315-2316.
38. Mathieu, O., Jasencakova, Z., Vaillant, I., Gendrel, A.V., Colot, V., Schubert, I., and, Tourmente, S., (2003) Changes in 5S rDNA chromatin organization and transcription during heterochromatin establishment in Arabidopsis. Plant Cell, 15, 2929-2939.
39. Müller, K., Bouyer, D., Schnittger, A., and, Kermode, A.R., (2012) Evolutionary conserved histone methylation dynamics during seed life-cycle transitions. PLoS ONE, 7, e51532.
40. Mutskov, V., Gerber, D., Angelov, D., Ausio, J., Workman, J., and, Dimitrov, S., (1998) Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding. Mol. Cell. Biol. 18, 6293-6304.
41. Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y., and, Nambara, E., (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J. 41, 697-709.
42. Nakabayashi, K., Bartsch, M., Xiang, Y., Miatton, E., Pellengahr, S., Yano, R., Seo, M., and, Soppe, W.J.J., (2012) The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION 1 protein levels in freshly harvested seeds. Plant Cell, 24, 2826-2838.
43. Nguyen, T.P., Keizer, P., van Eeuwijk, F., Smeekens, S., and, Bentsink, L., (2012) Natural variation for seed longevity and seed dormancy are negatively correlated in Arabidopsis. Plant Phys. 160, 2083-2092.
44. Pandey, R., Müller, A., Napoli, C.A., Selinger, D.A., Pikaard, C.S., Richards, E.J., Bender, J., Mount, D.W., and, Jorgensen, R.A., (2002) 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.
45. Paul, M.J., and, Pellny, T.K., (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J. Exp. Bot. 54, 539-547.
46. Portis, A.R. Jr, (2003) Rubisco activase-Rubisco's catalytic chaperone. Photosynth. Res. 75, 11-27.
47. Portis, A.R. Jr, Li, C., Wang, D., and, Salvucci, M.E., (2008) Regulation of Rubisco activase and its interaction with Rubisco. J. Exp. Bot. 59, 1597-1604.
48. Preston, J., Tatematsu, K., Kanno, Y., Hobo, T., Kimura, M., Jikumaru, Y., Yano, R., Kamiya, Y., and, Nambara, E., (2009) Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: a comparative study on dormant and non-dormant accessions. Plant Cell Physiol. 50, 1786-1800.
49. Sawchuk, M.G., Donner, T.J., Head, P., and, Scarpella, E., (2008) Unique and overlapping expression patterns among members of photosynthesis-associated nuclear gene families in Arabidopsis. Plant Physiol. 148, 1908-1924.
50. Smyth, G.K., (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 3.
51. Sridha, S., and, Wu, K., (2006) Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J. 46, 124-133.
52. Tai, H.H., Tai, G.C., and, Beardmore, T., (2005) Dynamic histone acetylation of late embryonic genes during seed germination. Plant Mol. Biol. 59, 909-925.
53. Tanaka, M., Kikuchi, A., and, Kamada, H., (2008) The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol. 146, 149-161.
54. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L.A., Rhee, S.Y., and, Stitt, M., (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939.
55. To, T.K., Nakaminami, K., Kim, J.M., Morosawa, T., Ishida, J., Tanaka, M., Yokoyama, S., Shinozaki, K., and, Seki, M., (2011) Arabidopsis HDA6 is required for freezing tolerance. Biochem. Biophys. Res. Commun. 406, 414-419.
56. Van Zanten, M., Koini, M.A., Geyer, R., Liu, Y., Brambilla, V., Bartels, D., Koornneef, M., Fransz, P., and, Soppe, W.J.J., (2011) Seed maturation in Arabidopsis thaliana is characterized by nuclear size reduction and increased chromatin condensation. Proc. Natl Acad. Sci. USA, 108, 20219-20224.
57. Van Zanten, M., Liu, Y., and, Soppe, W.J.J., (2013) Epigenetic signaling during the life of seeds. In Epigenetic Memory and Control in Plants (, Grafi, G., and, Ohad, N., eds). Heidelberg, New York, Dordrecht, London: Springer, pp. 127-153.
58. Wang, Z., Cao, H., Sun, Y., et al. (2013) Arabidopsis thaliana paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via the ABA-ethylene antagonism mediated by histone deacetylation. Plant Cell, 25, 149-166.
59. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and, Provart, N.J., (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analysing large-scale biological data sets. PLoS ONE, 2, e718.
60. Wu, X., Oh, M.H., Schwarz, E.M., Larue, C.T., Sivaguru, M., Imai, B.S., Yau, P.M., Ort, D.R., and, Huber, S.C., (2011) Lysine acetylation is a widespread protein modification for diverse proteins in Arabidopsis. Plant Physiol. 155, 1769-1778.
61. Yang, X., Bentink, S., Scheid, S., and, Spang, R., (2006) Similarities of ordered gene lists. J. Bioinform. Comput. Biol. 4, 693-708.
62. Yano, R., Takebayashi, Y., Nambara, E., Kamiya, Y., and, Seo, M., (2013) Combining association mapping and transcriptomics identify HD2B histone deacetylase as a genetic factor associated with seed dormancy in Arabidopsis thaliana. Plant J. 74, 815-828.
63. Yoshida, M., Horinouchi, S., and, Beppu, T., (1995) Trichostatin A and trapoxin: novel chemical probes for the role of histone acetylation in chromatin structure and function. BioEssays, 17, 423-430.
64. Yun, J., Kim, Y.S., Jung, J.H., Seo, P.J., and, Park, C.M., (2012) The AT-hook motif-containing protein AHL22 regulates flowering initiation by modifying FLOWERING LOCUS T chromatin in Arabidopsis. J. Biol. Chem. 287, 15307-15316.
65. Zhang, L., Qiu, Z., Hu, Y., et al. (2011) ABA treatment of germinating maize seeds induces VP1 gene expression and selective promoter-associated histone acetylation. Physiol. Plant. 143, 287-296.
66. Zheng, J., Chen, F., Wang, Z., Cao, H., Li, X., Deng, X., Soppe, W.J., Li, Y., and, Liu, Y., (2012) A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy. New Phytol. 193, 605-616.
67. Zhou, J., Wang, X., He, K., Charron, J.B.F., Elling, A.A., and, Deng, X.W., (2010) 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.