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      Near-Absent Levels of Segregational Variation Suggest Limited Opportunities for the Introduction of Genetic Variation Via Homeologous Chromosome Pairing in Synthetic Neoallotetraploid Mimulus

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          Abstract

          Genetic variation is the fundamental medium of evolution. In allopolyploids, which are the product of hybridization and whole genome duplication, if homologous chromosomes always pair, then all descendants of a single diploid F 1 hybrid lineage will be genetically identical. Contrarily, genetic variation among initially isogenic lineages is augmented when homeologous chromosomes pair; this added variation may contribute to phenotypic evolution. Mimulus sookensis is a naturally occurring, small-flowered allotetraploid derived from the large-flowered Mimulus guttatus and small-flowered Mimulus nasutus. Because diploid F 1 hybrids between M. guttatus and M. nasutus have large flowers, phenotypic evolution post-polyploidization is implied in M. sookensis. Here, we present genetic and phenotypic analyses of synthetic neoallotetraploid Mimulus derived from a cross between M. guttatus and M. nasutus. Genetic marker data from S 2 and BC 1N progeny suggest that chromosomes regularly pair with their homologous counterpart. By measuring the phenotype of synthetic neoallotetraploids, we demonstrate that polyploidization per se does not induce the small flowers of M. sookensis. Moreover, phenotypic measurements of synthetic allotetraploid F 2s and S 4 families suggest that rare homeologous recombination events have a negligible phenotypic effect in the first few generations. In total, the results are consistent with either exceedingly rare homeologous pairing and recombination or spontaneous fragment loss. The low levels of fragment loss and phenotypic variation in neoallotetraploids suggest that homeologous recombination after polyploidization is not a major mechanism of phenotypic evolution in M. sookensis. Rather, it may be that spontaneous mutations or epigenetic changes after allopolyploidization have driven phenotypic evolution in M. sookensis.

          Most cited references33

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          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.
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            Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms.

            Three published estimates of the frequency of polyploidy in angiosperms (30 to 35 percent, 47 percent, and 70 to 80 percent) were tested by estimating the genome size of extinct woody angiosperms with the use of fossil guard cell size as a proxy for cellular DNA content. The inferred chromosome numbers of these extinct species suggest that seven to nine is the primitive haploid chromosome number of angiosperms and that most angiosperms (approximately 70 percent) have polyploidy in their history.
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              Widespread genome duplications throughout the history of flowering plants.

              Genomic comparisons provide evidence for ancient genome-wide duplications in a diverse array of animals and plants. We developed a birth-death model to identify evidence for genome duplication in EST data, and applied a mixture model to estimate the age distribution of paralogous pairs identified in EST sets for species representing the basal-most extant flowering plant lineages. We found evidence for episodes of ancient genome-wide duplications in the basal angiosperm lineages including Nuphar advena (yellow water lily: Nymphaeaceae) and the magnoliids Persea americana (avocado: Lauraceae), Liriodendron tulipifera (tulip poplar: Magnoliaceae), and Saruma henryi (Aristolochiaceae). In addition, we detected independent genome duplications in the basal eudicot Eschscholzia californica (California poppy: Papaveraceae) and the basal monocot Acorus americanus (Acoraceae), both of which were distinct from duplications documented for ancestral grass (Poaceae) and core eudicot lineages. Among gymnosperms, we found equivocal evidence for ancient polyploidy in Welwitschia mirabilis (Gnetales) and no evidence for polyploidy in pine, although gymnosperms generally have much larger genomes than the angiosperms investigated. Cross-species sequence divergence estimates suggest that synonymous substitution rates in the basal angiosperms are less than half those previously reported for core eudicots and members of Poaceae. These lower substitution rates permit inference of older duplication events. We hypothesize that evidence of an ancient duplication observed in the Nuphar data may represent a genome duplication in the common ancestor of all or most extant angiosperms, except Amborella.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                March 2014
                27 January 2014
                : 4
                : 3
                : 509-522
                Affiliations
                [1]Department of Biology, Duke University, Durham, North Carolina 27708
                Author notes

                Supplemental information for raw phenotypic data is available online at http://dx.doi.org/10.6084/m9.figshare.904927.

                Supporting information is available online at http://www.g3journal.org/lookup/suppl/doi:10.1534/g3.113.008441/-/DC1.

                [1]

                Present address: Department of Biology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599.

                [2 ]Corresponding author: Department of Biology, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599. E-mail: jenmod@ 123456live.unc.edu
                Article
                GGG_008441
                10.1534/g3.113.008441
                3962489
                24470218
                359b18ac-8ead-4433-8e47-80021663e5eb
                Copyright © 2014 Modliszewski and Willis

                This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License ( http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 06 September 2013
                : 17 January 2014
                Page count
                Pages: 14
                Categories
                Investigations
                Custom metadata
                v1

                Genetics
                mimulus,neoallotetraploid,segregational variation,homeologous recombination,colchicine
                Genetics
                mimulus, neoallotetraploid, segregational variation, homeologous recombination, colchicine

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