Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids.

Polyploidy, or whole-genome duplication (WGD), is an important genomic feature for all eukaryotes, especially many plants and some animals. The common occurrence of polyploidy suggests an evolutionary advantage of having multiple sets of genetic material for adaptive evolution. However, increased gene and genome dosages in autopolyploids (duplications of a single genome) and allopolyploids (combinations of two or more divergent genomes) often cause genome instabilities, chromosome imbalances, regulatory incompatibilities, and reproductive failures. Therefore, new allopolyploids must establish a compatible relationship between alien cytoplasm and nuclei and between two divergent genomes, leading to rapid changes in genome structure, gene expression, and developmental traits such as fertility, inbreeding, apomixis, flowering time, and hybrid vigor. Although the underlying mechanisms for these changes are poorly understood, some themes are emerging. There is compelling evidence that changes in DNA sequence, cis- and trans-acting effects, chromatin modifications, RNA-mediated pathways, and regulatory networks modulate differential expression of homoeologous genes and phenotypic variation that may facilitate adaptive evolution in polyploid plants and domestication in crops.

[1]  J. Doebley,et al.  Pleiotropic Effects of the Duplicate Maize FLORICAULA/LEAFY Genes zfl1 and zfl2 on Traits Under Selection During Maize Domestication , 2006, Genetics.

[2]  G. Ledyard Stebbins,et al.  Chromosomal evolution in higher plants , 1971 .

[3]  M. Jakobsson,et al.  Chloroplast DNA indicates a single origin of the allotetraploid Arabidopsis suecica , 2003, Journal of evolutionary biology.

[4]  H. Muller Why Polyploidy is Rarer in Animals Than in Plants , 1925, The American Naturalist.

[5]  R. Jaenisch,et al.  The (epi)genetic control of mammalian X-chromosome inactivation. , 1997, Current opinion in genetics & development.

[6]  M. Navashin Chromosome Alterations Caused by Hybridization and Their Bearing upon Certain General Genetic Problems , 1934 .

[7]  C. Pikaard,et al.  Nucleolar dominance and silencing of transcription. , 1999, Trends in plant science.

[8]  R. Ojeda,et al.  Discovery of tetraploidy in a mammal , 1999, Nature.

[9]  L. Gottlieb Conservation and Duplication of Isozymes in Plants , 1982, Science.

[10]  R. Amasino,et al.  Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. , 2000, Science.

[11]  B. Bowen,et al.  Allelic Variation of Gene Expression in Maize Hybrids , 2004, The Plant Cell Online.

[12]  O. Riera-Lizarazu,et al.  Cytological and molecular characterization of oat×maize partial hybrids , 1996 .

[13]  Ronald W. Davis,et al.  Role of duplicate genes in genetic robustness against null mutations , 2003, Nature.

[14]  J. Cherry,et al.  Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: Rapid decay is associated with a group of touch- and specific clock-controlled genes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R. Martienssen,et al.  The role of RNA interference in heterochromatic silencing , 2004, Nature.

[16]  B. Mable ‘why polyploidy is rarer in animals than in plants’: myths and mechanisms , 2004 .

[17]  M. Nasrallah,et al.  Generation of Self-Incompatible Arabidopsis thaliana by Transfer of Two S Locus Genes from A. lyrata , 2002, Science.

[18]  G. Fink,et al.  Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of arabidopsis , 1995, Cell.

[19]  J. Nasrallah Cell-cell signaling in the self-incompatibility response. , 2000, Current opinion in plant biology.

[20]  S. Otto,et al.  Polyploid incidence and evolution. , 2000, Annual review of genetics.

[21]  R. Scott,et al.  The Basis of Natural and Artificial Postzygotic Hybridization Barriers in Arabidopsis Species Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010496. , 2003, The Plant Cell Online.

[22]  Jian-Min Zhou,et al.  Allopolyploidy alters gene expression in the highly stable hexaploid wheat , 2003, Plant Molecular Biology.

[23]  Brian C. Thomas,et al.  Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. , 2006, Genome research.

[24]  J. Birchler,et al.  Dosage effects on gene expression in a maize ploidy series. , 1996, Genetics.

[25]  E. Lander,et al.  Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. , 1992, Genetics.

[26]  K. H. Wolfe Yesterday's polyploids and the mystery of diploidization , 2001, Nature Reviews Genetics.

[27]  M. Nasrallah,et al.  The male determinant of self-incompatibility in Brassica. , 1999, Science.

[28]  J. Paszkowski,et al.  Formation of stable epialleles and their paramutation-like interaction in tetraploid Arabidopsis thaliana , 2003, Nature Genetics.

[29]  R. Jorgensen,et al.  Altered gene expression in plants due to trans interactions between homologous genes. , 1990, Trends in biotechnology.

[30]  Greg Gibson,et al.  Extensive Sex-Specific Nonadditivity of Gene Expression in Drosophila melanogaster , 2004, Genetics.

[31]  J. Birchler,et al.  Nonadditive Gene Expression in Diploid and Triploid Hybrids of Maize , 2005, Genetics.

[32]  M. Stam,et al.  Paramutation: an encounter leaving a lasting impression. , 2005, Trends in plant science.

[33]  Brad A. Chapman,et al.  Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events , 2003, Nature.

[34]  J. Wendel,et al.  Non-Mendelian Phenomena in Allopolyploid Genome Evolution , 2002 .

[35]  T. Mitchell-Olds,et al.  Cis-regulatory Evolution of Chalcone-Synthase Expression in the Genus Arabidopsis , 2006, Genetics.

[36]  Douglas E. Soltis,et al.  Advances in the study of polyploidy since Plant speciation , 2003 .

[37]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[38]  Luca Comai,et al.  The advantages and disadvantages of being polyploid , 2005, Nature Reviews Genetics.

[39]  A. Force,et al.  The probability of duplicate gene preservation by subfunctionalization. , 2000, Genetics.

[40]  E. Selker Premeiotic instability of repeated sequences in Neurospora crassa. , 1990, Annual review of genetics.

[41]  C. Denis,et al.  The CCR4-NOT complex plays diverse roles in mRNA metabolism. , 2003, Progress in nucleic acid research and molecular biology.

[42]  S. Sze,et al.  Accumulation of genome-specific transcripts, transcription factors and phytohormonal regulators during early stages of fiber cell development in allotetraploid cotton. , 2006, The Plant journal : for cell and molecular biology.

[43]  M. Molnár-Láng,et al.  Production and meiotic pairing behaviour of new hybrids of winter wheat (Triticum aestivum) x winter barley (Hordeum vulgare). , 2000, Genome.

[44]  Scott A. Rifkin,et al.  Duplicate genes increase gene expression diversity within and between species , 2004, Nature Genetics.

[45]  D. Levin Polyploidy and Novelty in Flowering Plants , 1983, The American Naturalist.

[46]  W. Berg,et al.  Paramutation at the sulfurea locus of Lycopersicon esculentum Mill. , 1978, Theoretical and Applied Genetics.

[47]  J. Wendel,et al.  Polyploidy and the Evolutionary History of Cotton , 2003 .

[48]  D. Levin The Cytoplasmic Factor in Plant Speciation , 2009 .

[49]  J. Claverys,et al.  Mismatch repair genes of Streptococcus pneumoniae: HexA confers a mutator phenotype in Escherichia coli by negative complementation , 1991, Journal of Bacteriology.

[50]  J. Heslop-Harrison,et al.  The Transition to Flowering , 1964, Nature.

[51]  Z. Chen,et al.  Nonadditive Regulation of FRI and FLC Loci Mediates Flowering-Time Variation in Arabidopsis Allopolyploids , 2006, Genetics.

[52]  R W Doerge,et al.  Genomewide Nonadditive Gene Regulation in Arabidopsis Allotetraploids , 2006, Genetics.

[53]  B. Mcclintock,et al.  The significance of responses of the genome to challenge. , 1984, Science.

[54]  Andreas Madlung,et al.  Remodeling of DNA Methylation and Phenotypic and Transcriptional Changes in Synthetic Arabidopsis Allotetraploids1 , 2002, Plant Physiology.

[55]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[56]  J. Paszkowski,et al.  A change of ploidy can modify epigenetic silencing. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Phillip D. Zamore,et al.  Ribo-gnome: The Big World of Small RNAs , 2005, Science.

[58]  B. Gaut Patterns of chromosomal duplication in maize and their implications for comparative maps of the grasses. , 2001, Genome research.

[59]  Pawel Michalak,et al.  Genome-wide patterns of expression in Drosophila pure species and hybrid males. , 2003, Molecular biology and evolution.

[60]  Dan Nettleton,et al.  All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[61]  J. Tainer,et al.  Subunit-destabilizing mutations in Drosophila copper/zinc superoxide dismutase: neuropathology and a model of dimer dysequilibrium. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[62]  A. Paterson,et al.  Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. , 2001, Genetics.

[63]  Jonathan F Wendel,et al.  Organ-Specific Silencing of Duplicated Genes in a Newly Synthesized Cotton Allotetraploid , 2004, Genetics.

[64]  Cathal Seoighe,et al.  Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. , 2004, Trends in genetics : TIG.

[65]  Eric S. Lander,et al.  Genetic evidence for complex speciation of humans and chimpanzees , 2006, Nature.

[66]  M. A. Koch,et al.  Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). , 2000, Molecular biology and evolution.

[67]  J. Harlan,et al.  Chromosome Pairing within Genomes in Maize-Tripsacum Hybrids , 1970, Science.

[68]  K. Hokamp,et al.  A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. , 2003, Genome research.

[69]  R. Doerge,et al.  The development of an Arabidopsis model system for genome-wide analysis of polyploidy effects. , 2004, Biological journal of the Linnean Society. Linnean Society of London.

[70]  M. Feldman,et al.  Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. , 2002, Genetics.

[71]  Dawei Li,et al.  The Genomes of Oryza sativa: A History of Duplications , 2005, PLoS biology.

[72]  M. Adams,et al.  Recent Segmental Duplications in the Human Genome , 2002, Science.

[73]  M. Ainouche,et al.  Molecular phylogeny of hybridizing species from the genus Spartina Schreb. (Poaceae). , 2002, Molecular phylogenetics and evolution.

[74]  A. Bruce THE MENDELIAN THEORY OF HEREDITY AND THE AUGMENTATION OF VIGOR. , 1910, Science.

[75]  Z. Jeffrey Chen,et al.  Stochastic and Epigenetic Changes of Gene Expression in Arabidopsis Polyploids , 2004, Genetics.

[76]  R. Grant-Downton,et al.  Epigenetics and its implications for plant biology 2. The 'epigenetic epiphany': epigenetics, evolution and beyond. , 2006, Annals of botany.

[77]  R. Amasino,et al.  FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering , 1999, Plant Cell.

[78]  James A. Birchler,et al.  In Search of the Molecular Basis of Heterosis , 2003, The Plant Cell Online.

[79]  J. Heslop-Harrison Gene expression and parental dominance in hybrid plants. , 1990, Development (Cambridge, England). Supplement.

[80]  O. Riera-Lizarazu,et al.  Cytological and molecular characterization of oat x maize partial hybrids , 1996, Theoretical and Applied Genetics.

[81]  J. Crow Alternative Hypotheses of Hybrid Vigor. , 1948, Genetics.

[82]  Z. Chen,et al.  Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[83]  P. Lu,et al.  Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[84]  K. Hilu,et al.  Polyploidy and the evolution of domesticated plants , 1993 .

[85]  C. Pikaard,et al.  Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. , 2006, Genes & development.

[86]  M. Feldman,et al.  The Impact of Polyploidy on Grass Genome Evolution , 2002, Plant Physiology.

[87]  R. Reeder Mechanisms of nucleolar dominance in animals and plants , 1985, The Journal of cell biology.

[88]  D. Schemske,et al.  PATHWAYS, MECHANISMS, AND RATES OF POLYPLOID FORMATION IN FLOWERING PLANTS , 1998 .

[89]  A. Fire,et al.  Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans , 1998, Nature.

[90]  Andrew G. Clark,et al.  Evolutionary changes in cis and trans gene regulation , 2004, Nature.

[91]  Zhongfu Ni,et al.  Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[92]  Dominance of Linked Factors as a Means of Accounting for Heterosis. , 1917, Genetics.

[93]  I. Leitch,et al.  Polyploidy in angiosperms , 1997 .

[94]  R. Aramayo,et al.  Meiotic Transvection in Fungi , 1996, Cell.

[95]  B. Mcclintock The relation of a particular chromosomal element to the development of the nucleoli in Zea mays , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[96]  A. Lowe,et al.  Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles , 2004 .

[97]  Lee Hs,et al.  Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. , 2001 .

[98]  Z. Chen,et al.  Protein-coding genes are epigenetically regulated in Arabidopsis polyploids , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[99]  W. Lewis Polyploidy : biological relevance , 1980 .

[100]  L. Gottlieb,et al.  A recently silenced, duplicate PgiC locus in Clarkia. , 1997, Molecular biology and evolution.

[101]  B. McKee Homologous pairing and chromosome dynamics in meiosis and mitosis. , 2004, Biochimica et biophysica acta.

[102]  D. Pellman,et al.  From polyploidy to aneuploidy, genome instability and cancer , 2004, Nature Reviews Molecular Cell Biology.

[103]  J. Fossella,et al.  Genetic and epigenetic incompatibilities underlie hybrid dysgenesis in Peromyscus , 2000, Nature Genetics.

[104]  S. Tilghman The Sins of the Fathers and Mothers Genomic Imprinting in Mammalian Development , 1999, Cell.

[105]  D. G. Brown,et al.  The origins of genomic duplications in Arabidopsis. , 2000, Science.

[106]  Jane Masterson,et al.  Stomatal Size in Fossil Plants: Evidence for Polyploidy in Majority of Angiosperms , 1994, Science.

[107]  A. Levy,et al.  Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat , 2003, Nature Genetics.

[108]  Tamim H. Shaikh,et al.  Segmental duplications: an 'expanding' role in genomic instability and disease , 2001, Nature Reviews Genetics.

[109]  P. Gounon,et al.  RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse , 2006, Nature.

[110]  Jonathan F. Wendel,et al.  Genome evolution in polyploids , 2004, Plant Molecular Biology.

[111]  Wen-Hsiung Li,et al.  External factors accelerate expression divergence between duplicate genes. , 2007, Trends in genetics : TIG.

[112]  A. Tyagi,et al.  FISH analysis of meiosis in Arabidopsis allopolyploids , 2004, Chromosome Research.

[113]  D. Soltis,et al.  Defective chlorophyll a/b-binding protein genes in the genome of a homosporous fern. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[114]  W. Peacock,et al.  The FLF MADS Box Gene: A Repressor of Flowering in Arabidopsis Regulated by Vernalization and Methylation , 1999, Plant Cell.

[115]  Vincent Colot,et al.  Understanding mechanisms of novel gene expression in polyploids. , 2003, Trends in genetics : TIG.

[116]  M. Matzke,et al.  How and Why Do Plants Inactivate Homologous (Trans)genes? , 1995, Plant physiology.

[117]  J. Birchler,et al.  Dosage-dependent gene regulation in multicellular eukaryotes: implications for dosage compensation, aneuploid syndromes, and quantitative traits. , 2001, Developmental biology.

[118]  S. Langlois,et al.  Parental origin of triploidy in human fetuses: evidence for genomic imprinting , 1993, Human Genetics.

[119]  M. Matzke,et al.  Rapid structural and epigenetic changes in polyploid and aneuploid genomes , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[120]  S. Henikoff,et al.  Trans-Sensing Effects: The Ups and Downs of Being Together , 1998, Cell.

[121]  T. Kao,et al.  Molecular recognition and response in pollen and pistil interactions. , 2000, Annual review of cell and developmental biology.

[122]  Joshua P. White,et al.  An RNA-dependent RNA polymerase is required for paramutation in maize , 2006, Nature.

[123]  R. Doerge,et al.  Genomic changes in synthetic Arabidopsis polyploids. , 2004, The Plant journal : for cell and molecular biology.

[124]  E S Lander,et al.  Ploidy regulation of gene expression. , 1999, Science.

[125]  David P. Bartel,et al.  MicroRNAs: At the Root of Plant Development?1 , 2003, Plant Physiology.

[126]  Chris D. Jiggins,et al.  Speciation by hybridization in Heliconius butterflies , 2006, Nature.

[127]  Jonathan F. Wendel,et al.  Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[128]  L. Rieseberg,et al.  Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization , 2003, Science.

[129]  A. Tyagi,et al.  Phenotypic Instability and Rapid Gene Silencing in Newly Formed Arabidopsis Allotetraploids , 2000, Plant Cell.

[130]  Z. Chen,et al.  Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. , 1997, Genes & development.

[131]  Hans Lassmann,et al.  The Widespread Impact of Mammalian MicroRNAs on mRNA Repression and Evolution , 2005 .

[132]  Colin D. Meiklejohn,et al.  Sex-Dependent Gene Expression and Evolution of the Drosophila Transcriptome , 2003, Science.

[133]  D. Charlesworth,et al.  Breeding systems and genome evolution. , 2001, Current opinion in genetics & development.

[134]  M. Feldman,et al.  Sequence Elimination and Cytosine Methylation Are Rapid and Reproducible Responses of the Genome to Wide Hybridization and Allopolyploidy in Wheat , 2001, The Plant Cell Online.

[135]  R. Stanyon,et al.  Molecular cytogenetics discards polyploidy in mammals. , 2005, Genomics.

[136]  Dosage effects on gene expression in a maize ploidy series. , 1996 .

[137]  X. Gu,et al.  Expression divergence between duplicate genes. , 2005, Trends in genetics : TIG.

[138]  Z. Chen,et al.  Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[139]  Z. Chen,et al.  A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. , 2004, Molecular cell.

[140]  J. Birchler,et al.  RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. , 2002, Molecular cell.

[141]  D. Barbash,et al.  A rapidly evolving MYB-related protein causes species isolation in Drosophila , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[142]  G. Barker,et al.  Development of anonymous cDNA microarrays to study changes to the Senecio floral transcriptome during hybrid speciation , 2005, Molecular ecology.

[143]  Caroline Josefsson,et al.  Parent-Dependent Loss of Gene Silencing during Interspecies Hybridization , 2006, Current Biology.

[144]  Andreas Madlung,et al.  Sensitivity of 70-mer oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species. , 2004, Plant biotechnology journal.

[145]  Mattias Jakobsson,et al.  A unique recent origin of the allotetraploid species Arabidopsis suecica: Evidence from nuclear DNA markers. , 2006, Molecular biology and evolution.

[146]  David Briggs,et al.  Plant Variation and Evolution , 1970 .

[147]  V. Chandler,et al.  Chromatin conversations: mechanisms and implications of paramutation , 2004, Nature Reviews Genetics.

[148]  D. Soltis,et al.  Evolution and Expression of Homeologous Loci in Tragopogon miscellus (Asteraceae), a Recent and Reciprocally Formed Allopolyploid , 2006, Genetics.

[149]  G. S. Whitt,et al.  Loss of duplicate gene expression after polyploidisation , 1977, Nature.

[150]  G. Segal,et al.  Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. , 1997, Genetics.

[151]  Nathan M. Springer,et al.  Cis-transcriptional Variation in Maize Inbred Lines B73 and Mo17 Leads to Additive Expression Patterns in the F1 Hybrid , 2006, Genetics.

[152]  A. Force,et al.  The probability of preservation of a newly arisen gene duplicate. , 2001, Genetics.

[153]  C. Pikaard,et al.  Restricted chromosomal silencing in nucleolar dominance , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[154]  O. Borsani,et al.  Endogenous siRNAs Derived from a Pair of Natural cis-Antisense Transcripts Regulate Salt Tolerance in Arabidopsis , 2005, Cell.