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      Genome-Wide Gene/Genome Dosage Imbalance Regulates Gene Expressions in Synthetic Brassica napus and Derivatives (AC, AAC, CCA, CCAA)

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          Abstract

          Gene/genome dosage balance is an essential evolutionary mechanism for organisms to ensure a normal function, but the underlying causes of dosage-imbalance regulation remain poorly understood. Herein, the serial Brassica hybrids/polyploids (AC, AAC, CCA, CCAA) with different copies of A and C subgenomes from the same two parents of Brassica rapa and Brassica oleracea were synthesized to investigate the effects of genome dosages on gene expressions and interactions by using RNA-Seq. The expression changes of A- and C-subgenome genes were consistent with dosage alterations. Dosage-dependent and -independent genes were grouped according to the correlations between dosage variations and gene expressions. Expression levels of dosage-dependent genes were strongly correlated with dosage changes and mainly contributed to dosage effects, while those of dosage-independent genes gave weak correlations with dosage variations and mostly facilitated dosage compensation. More protein–protein interactions were detected for dosage-independent genes than dosage-dependent ones, as predicted by the dosage balance hypothesis. Dosage-dependent genes more likely impacted the expressions by trans effects, whereas dosage-independent genes preferred to play by cis effects. Furthermore, dosage-dependent genes were mainly associated with the basic biological processes to maintain the stability of the growth and development, while dosage-independent genes were more enriched in the stress response related processes to accelerate adaptation. The present comprehensive analysis of gene expression dependent/independent on dosage alterations in Brassica polyploids provided new insights into gene/genome dosage-imbalance regulation of gene expressions.

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          Duplication and divergence: the evolution of new genes and old ideas.

          Over 35 years ago, Susumu Ohno stated that gene duplication was the single most important factor in evolution. He reiterated this point a few years later in proposing that without duplicated genes the creation of metazoans, vertebrates, and mammals from unicellular organisms would have been impossible. Such big leaps in evolution, he argued, required the creation of new gene loci with previously nonexistent functions. Bold statements such as these, combined with his proposal that at least one whole-genome duplication event facilitated the evolution of vertebrates, have made Ohno an icon in the literature on genome evolution. However, discussion on the occurrence and consequences of gene and genome duplication events has a much longer, and often neglected, history. Here we review literature dealing with the occurrence and consequences of gene duplication, beginning in 1911. We document conceptual and technological advances in gene duplication research from this early research in comparative cytology up to recent research on whole genomes, "transcriptomes," and "interactomes."
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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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              Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss.

              Ancient tetraploidies are found throughout the eukaryotes. After duplication, one copy of each duplicate gene pair tends to be lost (fractionate). For all studied tetraploidies, the loss of duplicated genes, known as homeologs, homoeologs, ohnologs, or syntenic paralogs, is uneven between duplicate regions. In maize, a species that experienced a tetraploidy 5-12 million years ago, we show that in addition to uneven ancient gene loss, the two complete genomes contained within maize are differentiated by ongoing fractionation among diverse inbreds as well as by a pattern of overexpression of genes from the genome that has experienced less gene loss. These expression differences are consistent over a range of experiments quantifying RNA abundance in different tissues. We propose that the universal bias in gene loss between the genomes of this ancient tetraploid, and perhaps all tetraploids, is the result of selection against loss of the gene responsible for the majority of total expression for a duplicate gene pair. Although the tetraploidy of maize is ancient, biased gene loss and expression continue today and explain, at least in part, the remarkable genetic diversity found among modern maize cultivars.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                23 September 2016
                2016
                : 7
                : 1432
                Affiliations
                [1] 1National Key Lab of Crop Genetic Improvement, National Center of Oil Crop Improvement (Wuhan), College of Plant Science and Technology, Huazhong Agricultural University Wuhan, China
                [2] 2Crop Research Institute, Sichuan Academy of Agricultural Sciences Chengdu, China
                Author notes

                Edited by: Xiaowu Wang, Chinese Academy of Agricultural Sciences, China

                Reviewed by: Guojia Ma, North Dakota State University, USA; Anne-Marie Chevre, French National Institute for Agricultural Research, France

                *Correspondence: Qi Pan 905681542@ 123456qq.com

                This article was submitted to Plant Genetics and Genomics, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2016.01432
                5033974
                27721820
                bf2201b2-0000-4366-947e-81c3d7d01652
                Copyright © 2016 Tan, Pan, Cui, Xiang, Ge and Li.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 04 July 2016
                : 08 September 2016
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 78, Pages: 14, Words: 9817
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: Grant No. 31371656
                Funded by: Ministry of Science and Technology of the People's Republic of China 10.13039/501100002855
                Award ID: 2014BAD11B03
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                dosage imbalance,gene expression,cis/trans effects,brassica,polyploids
                Plant science & Botany
                dosage imbalance, gene expression, cis/trans effects, brassica, polyploids

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