Abstract
Epigenetic changes in chromatin can be induced upon hybridization, but their contribution to phenotypic changes in F1 hybrids is not known. In this study, we examined the effect of genome-wide alteration of epigenetic chromatin status on the growth of inbreds and their F1 hybrid by large-scale fine-time-lapse growth monitoring of rice (Oryza sativa L.) under a controlled environment. This allowed us to dissect seedling growth of inbreds and their hybrid into separate growth parameters, and to analyze the effect of disturbance of inert chromatin states on these parameters. We found that superior growth parameters are generally more sensitive to global inhibition of the activities of histone deacetylases (HDACs), but this higher sensitivity is not directly correlated to heterosis in F1. Unexpectedly, however, the rate of the initial exponential growth of shoots is sensitive to HDAC inhibition only in inbreds, but not in F1, irrespective of phenotypic superiority. Our phenomics approach has detected an inbred-specific dependence of basic growth on the inert state of chromatin that is lost in F1 hybrids.
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References
Bustamante CD, Nielsen R, Sawyer SA, Olsen KM, Purugganan MD, Hartl DL (2002) The cost of inbreeding in Arabidopsis. Nature 416:531–534
Causton DR, Venus JC (1981) The biometry of plant growth. Edward Arnold, London
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796
Chen ZJ, Pikaard CS (1997) Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev 11:2124–2136
Comai L, Tyagi AP, Winter K, Holmes-Davis R, Reynolds SH, Stevens Y et al (2000) Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12:1551–1567
Hunt R (1982) Plant growth curves. The functional approach to plant growth analysis. Edward Arnold, London
Ishizuka T, Tanabata T, Takano M, Shinomura T (2005) Kinetic measuring method of rice growth in tillering stage using auto digital imaging system. Environ Control Biol 43:83–96
Jang I-C, Pahk Y-M, Song SI, Kwon HJ, Nahm BH, Kim J-K (2003) Structure and expression of the rice class-I type histone deacetylase genes OsHDAC1-3: OsHDAC1 overexpression in transgenic plants leads to increased growth rate and altered architecture. Plant J 33:531–541
Jonckheere RA (1954a) A distribution-free k-sample test against ordered alternatives. Biometrika 41:133–145
Jonckheere RA (1954b) A test of significance for the relation between m rankings and k ordered categories. Br J Statist Psychol 7:93–100
Li Y, Butenko Y, Grafi G (2005) Histone deacetylation is required for progression through mitosis in tobacco cells. Plant J 41:346–352
Liu B, Wendel JF (2003) Epigenetic phenomena and the evolution of plant allopolyploids. Mol Phylogenet Evol 29:365–379
Loidl P (2004) A plant dialect of the histone language. Trends Plant Sci 9:84–90
Lu J, Tang T, Tang H, Huang J, Shi S, Wu C-I (2006) The accumulation of deleterious mutations in rice genomes: a hypothesis on the cost of domestication. Trends Genet 22:126–131
Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y et al (2009) Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids. Nature 457:327–331
Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624
Shaked H, Kasukush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749–1759
Sollars V, Lu X, Xiao L, Wang X, Garfinkel MD, Ruden DM (2003) Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nat Genet 33:70–74
Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible models of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci USA 103:6805–6810
Taddei A, Roche D, Bickmore WA, Almouzni G (2005) The effects of histone deacetylases inhibitors on heterochromatin: implications for anticancer therapy? EMBO Rep 6:520–524
Tanabata T, Shimizu H, Shimnomura T, Takano M, Nakamura-Miyamura H, Saito T (2008) An image measurement system for phenotype analysis of rice seedlings growth. IEEJ Transact Electr Info Sys 128:962–969 (in Japanese with English abstract)
True HL, Berlin I, Lindquist SL (2004) Epigenetic regulation of translation reveales hidden genetic variation to produce complex traits. Nature 431:184–187
Wei G, Tao Y, Liu G, Chen C, Luo R, Xia H et al (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc Natl Acad Sci USA 106:7695–9701
Acknowledgments
We thank Keiko Hioki, Reiko Nigorikawa, Rie Takahashi, Kumiko Nissaka, Tomoko Watanabe and Hisayo Shimizu for technical assistance, and Helen Rothnie, Kentaro Ohigashi and Tetsuhisa Niwa for comments on the manuscript. This work was supported by the Ministry of Agriculture, Forestry and Fisheries of Japan (Integrated research project for plant, insect and animal using genome technology Japan, IP-1013 to Y.H. and IP-1006 T.S.; Genomics for Agricultural Innovation, NVR-0006 to Y.H.).
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Tanabata, T., Taguchi-Shiobara, F., Kishimoto, N. et al. A phenomics approach detected differential epigenetic growth regulation between inbreds and their hybrid in Oryza sativa . Mol Breeding 26, 729–734 (2010). https://doi.org/10.1007/s11032-010-9484-3
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DOI: https://doi.org/10.1007/s11032-010-9484-3