Genetics, Vol. 167, 1961-1973, August 2004, Copyright © 2004
doi:10.1534/genetics.104.027896

Stochastic and Epigenetic Changes of Gene Expression in Arabidopsis Polyploids

Jianlin Wang^*, Lu Tian^*, Andreas Madlung^,, Hyeon-Se Lee^*, Meng Chen^*, Jinsuk J. Lee^*, Brian Watson, Trevor Kagochi, Luca Comai and Z. Jeffrey Chen^*,1

^* Genetics Program and Department of Soil and Crop Sciences, Texas A&M University, College Station, Texas 77843-2474
Department of Biology, University of Washington, Seattle, Washington 98195-5325
Department of Biology, University of Puget Sound, Tacoma, Washington 98416

¹ Corresponding author: Molecular Genetics/MS 2474, Department of Soil and Crop Sciences, Texas A&M University, College Station, TX 77843-2474.
E-mail: zjchen{at}tamu.edu

Polyploidization is an abrupt speciation mechanism for eukaryotes and is especially common in plants. However, little is known about patterns and mechanisms of gene regulation during early stages of polyploid formation. Here we analyzed differential expression patterns of the progenitors' genes among successive selfing generations and independent lineages. The synthetic Arabidopsis allotetraploid lines were produced by a genetic cross between A. thaliana and A. arenosa autotetraploids. We found that some progenitors' genes are differentially expressed in early generations, whereas other genes are silenced in late generations or among different siblings within a selfing generation, suggesting that the silencing of progenitors' genes is rapidly and/or stochastically established. Moreover, a subset of genes is affected in autotetraploid and multiple independent allotetraploid lines and in A. suecica, a natural allotetraploid derived from A. thaliana and A. arenosa, indicating locus-specific susceptibility to ploidy-dependent gene regulation. The role of DNA methylation in silencing progenitors' genes is tested in DNA-hypomethylation transgenic lines of A. suecica using RNA interference (RNAi). Two silenced genes are reactivated in both ddm1- and met1-RNAi lines, consistent with the demethylation of centromeric repeats and gene-specific regions in the genome. A rapid and stochastic process of differential gene expression is reinforced by epigenetic regulation during polyploid formation and evolution.

This article has been cited by other articles:

				S. A. Church and E. J. Spaulding Gene Expression in a Wild Autopolyploid Sunflower Series J. Hered., July 1, 2009; 100(4): 491 - 495. [Abstract] [Full Text] [PDF]

				S. Anssour, T. Krugel, T. F. Sharbel, H. P. Saluz, G. Bonaventure, and I. T. Baldwin Phenotypic, genetic and genomic consequences of natural and synthetic polyploidization of Nicotiana attenuata and Nicotiana obtusifolia Ann. Bot., June 1, 2009; 103(8): 1207 - 1217. [Abstract] [Full Text] [PDF]

				B. Chaudhary, L. Flagel, R. M. Stupar, J. A. Udall, N. Verma, N. M. Springer, and J. F. Wendel Reciprocal Silencing, Transcriptional Bias and Functional Divergence of Homeologs in Polyploid Cotton (Gossypium) Genetics, June 1, 2009; 182(2): 503 - 517. [Abstract] [Full Text] [PDF]

				M. Stam Paramutation: A Heritable Change in Gene Expression by Allelic Interactions In Trans Mol Plant, April 8, 2009; (2009) ssp020v1. [Abstract] [Full Text] [PDF]

				M. Throude, S. Bolot, M. Bosio, C. Pont, X. Sarda, U. M. Quraishi, F. Bourgis, P. Lessard, P. Rogowsky, A. Ghesquiere, et al. Structure and expression analysis of rice paleo duplications Nucleic Acids Res., March 1, 2009; 37(4): 1248 - 1259. [Abstract] [Full Text] [PDF]

				M. Pumphrey, J. Bai, D. Laudencia-Chingcuanco, O. Anderson, and B. S. Gill Nonadditive Expression of Homoeologous Genes Is Established Upon Polyploidization in Hexaploid Wheat Genetics, March 1, 2009; 181(3): 1147 - 1157. [Abstract] [Full Text] [PDF]

				M. Ha, E.-D. Kim, and Z. J. Chen Duplicate genes increase expression diversity in closely related species and allopolyploids PNAS, February 17, 2009; 106(7): 2295 - 2300. [Abstract] [Full Text] [PDF]

				M. G. Sawchuk, T. J. Donner, P. Head, and E. Scarpella Unique and Overlapping Expression Patterns among Members of Photosynthesis-Associated Nuclear Gene Families in Arabidopsis Plant Physiology, December 1, 2008; 148(4): 1908 - 1924. [Abstract] [Full Text] [PDF]

				A. Guggisberg, C. Baroux, U. Grossniklaus, and E. Conti Genomic Origin and Organization of the Allopolyploid Primula egaliksensis Investigated by in situ Hybridization Ann. Bot., May 1, 2008; 101(7): 919 - 927. [Abstract] [Full Text] [PDF]

				M. Chen, M. Ha, E. Lackey, J. Wang, and Z. J. Chen RNAi of met1 Reduces DNA Methylation and Induces Genome-Specific Changes in Gene Expression and Centromeric Small RNA Accumulation in Arabidopsis Allopolyploids Genetics, April 1, 2008; 178(4): 1845 - 1858. [Abstract] [Full Text] [PDF]

				R. T. Gaeta, J. C. Pires, F. Iniguez-Luy, E. Leon, and T. C. Osborn Genomic Changes in Resynthesized Brassica napus and Their Effect on Gene Expression and Phenotype PLANT CELL, November 1, 2007; 19(11): 3403 - 3417. [Abstract] [Full Text] [PDF]

				E. W. Ganko, B. C. Meyers, and T. J. Vision Divergence in Expression between Duplicated Genes in Arabidopsis Mol. Biol. Evol., October 1, 2007; 24(10): 2298 - 2309. [Abstract] [Full Text] [PDF]

				R. M. Stupar, P. B. Bhaskar, B. S. Yandell, W. A. Rensink, A. L. Hart, S. Ouyang, R. E. Veilleux, J. S. Busse, R. J. Erhardt, C. R. Buell, et al. Phenotypic and Transcriptomic Changes Associated With Potato Autopolyploidization Genetics, August 1, 2007; 176(4): 2055 - 2067. [Abstract] [Full Text] [PDF]

				J. Dubcovsky and J. Dvorak Genome Plasticity a Key Factor in the Success of Polyploid Wheat Under Domestication Science, June 29, 2007; 316(5833): 1862 - 1866. [Abstract] [Full Text] [PDF]

				N. Shitsukawa, C. Tahira, K.-i. Kassai, C. Hirabayashi, T. Shimizu, S. Takumi, K. Mochida, K. Kawaura, Y. Ogihara, and K. Murai Genetic and Epigenetic Alteration among Three Homoeologous Genes of a Class E MADS Box Gene in Hexaploid Wheat PLANT CELL, June 1, 2007; 19(6): 1723 - 1737. [Abstract] [Full Text] [PDF]

				K. L. Adams Evolution of Duplicate Gene Expression in Polyploid and Hybrid Plants J. Hered., March 1, 2007; 98(2): 136 - 141. [Abstract] [Full Text] [PDF]

				J. de Meaux, A. Pop, and T. Mitchell-Olds Cis-regulatory Evolution of Chalcone-Synthase Expression in the Genus Arabidopsis Genetics, December 1, 2006; 174(4): 2181 - 2202. [Abstract] [Full Text] [PDF]

				J. A. Udall and J. F. Wendel Polyploidy and Crop Improvement Crop Sci., November 1, 2006; 46(Supplement_1): S-3 - S-14. [Abstract] [Full Text] [PDF]

				E. Jablonka Commentary: Induction and selection of variations during cancer development Int. J. Epidemiol., October 1, 2006; 35(5): 1163 - 1165. [Full Text] [PDF]

				J. A. Tate, Z. Ni, A.-C. Scheen, J. Koh, C. A. Gilbert, D. Lefkowitz, Z. J. Chen, P. S. Soltis, and D. E. Soltis Evolution and Expression of Homeologous Loci in Tragopogon miscellus (Asteraceae), a Recent and Reciprocally Formed Allopolyploid Genetics, July 1, 2006; 173(3): 1599 - 1611. [Abstract] [Full Text] [PDF]

				K. Y. Lim, K. Souckova-Skalicka, V. Sarasan, J. J. Clarkson, M. W. Chase, A. Kovarik, and A. R. Leitch A genetic appraisal of a new synthetic Nicotiana tabacum (Solanaceae) and the Kostoff synthetic tobacco Am. J. Botany, June 1, 2006; 93(6): 875 - 883. [Abstract] [Full Text] [PDF]

				J. Wang, L. Tian, H.-S. Lee, and Z. J. Chen Nonadditive Regulation of FRI and FLC Loci Mediates Flowering-Time Variation in Arabidopsis Allopolyploids Genetics, June 1, 2006; 173(2): 965 - 974. [Abstract] [Full Text] [PDF]

				W. Albertin, T. Balliau, P. Brabant, A.-M. Chevre, F. Eber, C. Malosse, and H. Thiellement Numerous and Rapid Nonstochastic Modifications of Gene Products in Newly Synthesized Brassica napus Allotetraploids Genetics, June 1, 2006; 173(2): 1101 - 1113. [Abstract] [Full Text] [PDF]

				R. T. GRANT-DOWNTON and H. G. DICKINSON Epigenetics and its Implications for Plant Biology 2. The 'Epigenetic Epiphany': Epigenetics, Evolution and Beyond Ann. Bot., January 1, 2006; 97(1): 11 - 27. [Abstract] [Full Text] [PDF]

				J. Wang, L. Tian, H.-S. Lee, N. E. Wei, H. Jiang, B. Watson, A. Madlung, T. C. Osborn, R. W. Doerge, L. Comai, et al. Genomewide Nonadditive Gene Regulation in Arabidopsis Allotetraploids Genetics, January 1, 2006; 172(1): 507 - 517. [Abstract] [Full Text] [PDF]

				L. N. Lukens, J. C. Pires, E. Leon, R. Vogelzang, L. Oslach, and T. Osborn Patterns of Sequence Loss and Cytosine Methylation within a Population of Newly Resynthesized Brassica napus Allopolyploids Plant Physiology, January 1, 2006; 140(1): 336 - 348. [Abstract] [Full Text] [PDF]

				C. R. Landry, P. J. Wittkopp, C. H. Taubes, J. M. Ranz, A. G. Clark, and D. L. Hartl Compensatory cis-trans Evolution and the Dysregulation of Gene Expression in Interspecific Hybrids of Drosophila Genetics, December 1, 2005; 171(4): 1813 - 1822. [Abstract] [Full Text] [PDF]

				T. Nomura, A. Ishihara, R. C. Yanagita, T. R. Endo, and H. Iwamura Three genomes differentially contribute to the biosynthesis of benzoxazinones in hexaploid wheat PNAS, November 8, 2005; 102(45): 16490 - 16495. [Abstract] [Full Text] [PDF]

				Y.-M. Wang, Z.-Y. Dong, Z.-J. Zhang, X.-Y. Lin, Y. Shen, D. Zhou, and B. Liu Extensive de Novo Genomic Variation in Rice Induced by Introgression From Wild Rice (Zizania latifolia Griseb.) Genetics, August 1, 2005; 170(4): 1945 - 1956. [Abstract] [Full Text] [PDF]

				R. Gorelick Theory for why dioecious plants have equal length sex chromosomes Am. J. Botany, June 1, 2005; 92(6): 979 - 984. [Abstract] [Full Text] [PDF]

				K. L. Adams, R. Percifield, and J. F. Wendel Organ-Specific Silencing of Duplicated Genes in a Newly Synthesized Cotton Allotetraploid Genetics, December 1, 2004; 168(4): 2217 - 2226. [Abstract] [Full Text] [PDF]

International Access Link

Online ISSN: 1943-2361  Print ISSN: 0016-6731
Copyright 2009 by the Genetics Society of America
phone: 412-268-1812   fax: 412-268-1813   email: genetics-gsa{at}andrew.cmu.edu