Allopolyploidization Lays the Foundation for Evolution of Distinct Populations: Evidence From Analysis of Synthetic Arabidopsis Allohexaploids

Polyploidization is an important mechanism for introducing diversity into a population and promoting evolutionary change. It is believed that most, if not all, angiosperms have undergone whole genome duplication events in their evolutionary history, which has led to changes in genome structure, gene regulation, and chromosome maintenance. Previous studies have shown that polyploidy can coincide with meiotic abnormalities and somatic cytogenetic mosaics in Arabidopsis allotetraploids, but it is unclear whether this phenomenon can contribute to novel diversity or act as a mechanism for speciation. In this study we tested the hypothesis that mosaic aneuploidy contributes to the formation of incipient diversity in neoallopolyploids. We generated a population of synthesized Arabidopsis allohexaploids and monitored karyotypic and phenotypic variation in this population over the first seven generations. We found evidence of sibling line-specific chromosome number variations and rapidly diverging phenotypes between lines, including flowering time, leaf shape, and pollen viability. Karyotypes varied between sibling lines and between cells within the same tissues. Cytotypic variation correlates with phenotypic novelty, and, unlike in allotetraploids, remains a major genomic destabilizing factor for at least the first seven generations. While it is still unclear whether new stable aneuploid lines will arise from these populations, our data are consistent with the notion that somatic aneuploidy, especially in higher level allopolyploids, can act as an evolutionary relevant mechanism to induce rapid variation not only during the initial allopolyploidization process but also for several subsequent generations. This process may lay the genetic foundation for multiple, rather than just a single, new species.

[1]  A. Madlung,et al.  Natural variation and persistent developmental instabilities in geographically diverse accessions of the allopolyploid Arabidopsis suecica. , 2012, Physiologia plantarum.

[2]  Pamela S Soltis,et al.  Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae) , 2012, Proceedings of the National Academy of Sciences.

[3]  Claude W. dePamphilis,et al.  Ancestral polyploidy in seed plants and angiosperms , 2011, Nature.

[4]  J. Pires,et al.  Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus , 2011, Proceedings of the National Academy of Sciences.

[5]  Patrick S. Schnable,et al.  Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant , 2011, Current Biology.

[6]  G. Moore,et al.  Genetic regulation of meiosis in polyploid species: new insights into an old question. , 2010, The New phytologist.

[7]  W. Rickoll,et al.  Photoperiod-dependent floral reversion in the natural allopolyploid Arabidopsis suecica. , 2010, The New phytologist.

[8]  J. Chris Pires,et al.  Homoeologous recombination in allopolyploids: the polyploid ratchet. , 2010, The New phytologist.

[9]  L. F. Viccini,et al.  Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus. , 2010, The New phytologist.

[10]  Lex E. Flagel,et al.  Homoeologous nonreciprocal recombination in polyploid cotton. , 2010, The New phytologist.

[11]  J. Birchler,et al.  Reflections on studies of gene expression in aneuploids. , 2010, The Biochemical journal.

[12]  Z. Chen,et al.  Molecular mechanisms of polyploidy and hybrid vigor. , 2010, Trends in plant science.

[13]  J. Pires,et al.  Mitotic instability in resynthesized and natural polyploids of the genus Arabidopsis (Brassicaceae). , 2009, American journal of botany.

[14]  D. Soltis,et al.  Synthetic polyploids of Tragopogon miscellus and T. mirus (Asteraceae): 60 Years after Ownbey's discovery. , 2009, American journal of botany.

[15]  Pamela S Soltis,et al.  The role of hybridization in plant speciation. , 2009, Annual review of plant biology.

[16]  D. Soltis,et al.  Rapid Chromosome Evolution in Recently Formed Polyploids in Tragopogon (Asteraceae) , 2008, PloS one.

[17]  Z. Chen,et al.  Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids , 2008, Nature.

[18]  David P. Kreil,et al.  Effects of Aneuploidy on Genome Structure, Expression, and Interphase Organization in Arabidopsis thaliana , 2008, PLoS genetics.

[19]  S. Hiscock,et al.  Review Genomic Clues to the Evolutionary Success of Polyploid Plants , 2022 .

[20]  A. Leitch,et al.  Genomic Plasticity and the Diversity of Polyploid Plants , 2008, Science.

[21]  C. Lister,et al.  Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization , 2008, Proceedings of the National Academy of Sciences.

[22]  J. Pires,et al.  Genomic Changes in Resynthesized Brassica napus and Their Effect on Gene Expression and Phenotype[W][OA] , 2007, The Plant Cell Online.

[23]  L. Rieseberg,et al.  Plant Speciation , 2007, Science.

[24]  J. Davison,et al.  Large-scale polymorphism of heterochromatic repeats in the DNA of Arabidopsis thaliana , 2007, BMC Plant Biology.

[25]  Z. Chen,et al.  Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. , 2007, Annual review of plant biology.

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

[27]  D. Soltis,et al.  Widespread genome duplications throughout the history of flowering plants. , 2006, Genome research.

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

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

[30]  J. Wendel,et al.  Novel patterns of gene expression in polyploid plants. , 2005, Trends in genetics : TIG.

[31]  B. Dilkes,et al.  Aneuploidy and Genetic Variation in the Arabidopsis thaliana Triploid Response , 2005, Genetics.

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

[33]  Colin N. Dewey,et al.  Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution , 2004, Nature.

[34]  J. Birchler,et al.  Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[36]  L. Lukens,et al.  Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae) , 2004 .

[37]  Guillaume Blanc,et al.  Widespread Paleopolyploidy in Model Plant Species Inferred from Age Distributions of Duplicate Genes , 2004, The Plant Cell Online.

[38]  O. Seehausen Hybridization and adaptive radiation. , 2004, Trends in ecology & evolution.

[39]  Y. Ueda,et al.  Cystic partially differentiated nephroblastoma, embryonal rhabdomyosarcoma, and multiple congenital anomalies associated with variegated mosaic aneuploidy and premature centromere division: a case report. , 2003, Journal of pediatric hematology/oncology.

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

[41]  Hao Yu,et al.  AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[43]  C. Halldén,et al.  Genetic variation in Arabidopsis suecica and its parental species A. arenosa and A. thaliana. , 2002, Hereditas.

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

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

[46]  D. Soltis,et al.  The Origins of Arabidopsis suecica (Brassicaceae) as Indicated by Nuclear rDNA Sequences , 1996 .

[47]  Lin Chao,et al.  GENETIC MOSAICISM IN PLANTS AND CLONAL ANIMALS , 1995 .

[48]  J. Ford,et al.  Chromosome elimination in micronuclei: a common cause of hypoploidy. , 1988, American journal of human genetics.

[49]  M. Nozzolini,et al.  Chromosomal variation on plants regenerated from twoNicotiana spp. , 1981, Protoplasma.

[50]  J. Hermsen,et al.  Somatic chromosome elimination and meiotic chromosome pairing in the triple hybrid 6x-(Solanum acaule × S. bulbocastanum) × 2×-S. phureja , 1971, Euphytica.

[51]  Dr. Susumu Ohno Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[52]  M. Rao,et al.  Chromosome numerical mosaicism in some hybrids of theSolanum nigrum complex , 1969, Genetica.

[53]  Maxine M. Thompson CYTOGENETICS OF RUBUS. III. MEIOTIC INSTABILITY IN SOME HIGHER POLYPLOIDS , 1962 .

[54]  G. Pohlendt Variabilität der Chromosomenzahlen und andere Kernpathologien in Aegilops Triuncialis×Triticum Aestivum-Bastarden , 1958, Zeitschrift für Vererbungslehre.

[55]  L. Sachs Chromosome mosaics in experimental amphiploids in the Triticinae , 1952, Heredity.

[56]  A. Blakeslee,et al.  CHROMOSOMAL DUPLICATION AND MENDELIAN PHENOMENA IN DATURA MUTANTS. , 1920 .

[57]  R. Amasino,et al.  The Timing of Flowering , 2010 .

[58]  J. Mallet Hybrid speciation , 2007, Nature.

[59]  J. Harper,et al.  Detailed FISH analysis of day 5 human embryos reveals the mechanisms leading to mosaic aneuploidy. , 2005, Human reproduction.

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

[61]  E. Finnegan,et al.  The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[63]  H. Harmaja,et al.  Three different chromosome numbers from Finnish Arabidopsis suecica (Brassicaceae) , 1990 .

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

[65]  W. Lewis,et al.  Cytogeography of Claytonia virginica and Its Allies , 1967 .

[66]  Yasuko Takahashi,et al.  Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events , 2022 .