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      Ploidy and Hybridity Effects on Growth Vigor and Gene Expression in Arabidopsis thaliana Hybrids and Their Parents

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          Abstract

          Both ploidy and hybridity affect cell size and growth vigor in plants and animals, but the relative effects of genome dosage and hybridization on biomass, fitness, and gene expression changes have not been systematically examined. Here we performed the first comparative analysis of seed, cell, and flower sizes, starch and chlorophyll content, biomass, and gene expression changes in diploid, triploid, and tetraploid hybrids and their respective parents in three Arabidopsis thaliana ecotypes: Columbia, C24, and Landsberg erecta (L er). Ploidy affects many morphological and fitness traits, including stomatal size, flower size, and seed weight, whereas hybridization between the ecotypes leads to altered expression of central circadian clock genes and increased starch and chlorophyll content, biomass, and seed weight. However, varying ploidy levels has subtle effects on biomass, circadian clock gene expression, and chlorophyll and starch content. Interestingly, biomass, starch content, and seed weight are significantly different between the reciprocal hybrids at all ploidy levels tested, with the lowest and highest levels found in the reciprocal triploid hybrids, suggesting parent-of-origin effects on biomass, starch content, and seed weight. These findings provide new insights into molecular events of polyploidy and heterosis, as well as complex agronomic traits that are important to biomass and seed production in hybrid and polyploid crops.

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          Most cited references51

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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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            Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids

            Segregating hybrids and stable allopolyploids display morphological vigor1,2,3, and Arabidopsis allotetraploids are larger than the parents Arabidopsis thaliana and A. arenosa 1,4. The mechanisms are unknown. Circadian clocks mediate metabolic pathways and increase fitness in animals and plants5,6,7,8. Here we report that epigenetic modifications of the circadian clock genes CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY)9,10 and their reciprocal regulators TIMING OF CAB EXPRESSION 1 (TOC1) and GIGANTEA (GI)10,11,12 mediate expression changes in downstream genes and pathways. During the day, epigenetic repression of CCA1 and LHY induced expression of TOC1, GI and downstream genes that contain CCA1 binding site (CBS)13 in chlorophyll and starch metabolic pathways in allotetraploids and F1 hybrids, which produced more chlorophyll and starch than the parents in the same environment. Mutations in cca1 and cca1 lhy and daily repression of cca1 in TOC1:cca1-RNAi transgenic plants increased expression of downstream genes and chlorophyll and starch content, whereas constitutively expressing CCA1 or ectopically expressing TOC1:CCA1 had the opposite effects. The causal effects of CCA1 on output traits suggest that hybrids and allopolyploids gain advantages from the control of circadian-mediated physiological and metabolic pathways, leading to growth vigor and increased biomass.
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              Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing.

              Most eukaryotes have genomes that exhibit high levels of gene redundancy, much of which seems to have arisen from one or more cycles of genome doubling. Polyploidy has been particularly prominent during flowering plant evolution, yielding duplicated genes (homoeologs) whose expression may be retained or lost either as an immediate consequence of polyploidization or on an evolutionary timescale. Expression of 40 homoeologous gene pairs was assayed by cDNA-single-stranded conformation polymorphism in natural (1- to 2-million-yr-old) and synthetic tetraploid cotton (Gossypium) to determine whether homoeologous gene pairs are expressed at equal levels after polyploid formation. Silencing or unequal expression of one homoeolog was documented for 10 of 40 genes examined in ovules of Gossypium hirsutum. Assays of homoeolog expression in 10 organs revealed variable expression levels and silencing, depending on the gene and organ examined. Remarkably, silencing and biased expression of some gene pairs are reciprocal and developmentally regulated, with one homoeolog showing silencing in some organs and the other being silenced in other organs, suggesting rapid subfunctionalization. Duplicate gene expression was examined in additional natural polyploids to characterize the pace at which expression alteration evolves. Analysis of a synthetic tetraploid revealed homoeolog expression and silencing patterns that sometimes mirrored those of the natural tetraploid. Both long-term and immediate responses to polyploidization were implicated. Data suggest that some silencing events are epigenetically induced during the allopolyploidization process.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                ggg
                ggg
                ggg
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                1 April 2012
                April 2012
                : 2
                : 4
                : 505-513
                Affiliations
                Section of Molecular Cell and Developmental Biology, Center for Computational Biology and Bioinformatics, and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, Texas 78712
                Author notes

                Supporting information is available online at http://www.g3journal.org/lookup/suppl/doi:10.1534/g3.112.002162/-/DC1

                [1 ]Corresponding author: Institute for Cellular and Molecular Biology, University of Texas at Austin, One University Station, A-4800, Austin, TX 78712. E-mail: zjchen@ 123456mail.utexas.edu
                Article
                GGG_002162
                10.1534/g3.112.002162
                3337479
                22540042
                6400848c-b815-41c9-9124-4761c054c9a9
                Copyright © 2012 Miller et al.

                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
                : 11 December 2011
                : 22 February 2012
                Categories
                Investigations

                Genetics
                heterosis,gene expression,hybrids,circadian clock,polyploidy
                Genetics
                heterosis, gene expression, hybrids, circadian clock, polyploidy

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