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      An Interspecific Fungal Hybrid Reveals Cross-Kingdom Rules for Allopolyploid Gene Expression Patterns

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          Abstract

          Polyploidy, a state in which the chromosome complement has undergone an increase, is a major force in evolution. Understanding the consequences of polyploidy has received much attention, and allopolyploids, which result from the union of two different parental genomes, are of particular interest because they must overcome a suite of biological responses to this merger, known as “genome shock.” A key question is what happens to gene expression of the two gene copies following allopolyploidization, but until recently the tools to answer this question on a genome-wide basis were lacking. Here we utilize high throughput transcriptome sequencing to produce the first genome-wide picture of gene expression response to allopolyploidy in fungi. A novel pipeline for assigning sequence reads to the gene copies was used to quantify their expression in a fungal allopolyploid. We find that the transcriptional response to allopolyploidy is predominantly conservative: both copies of most genes are retained; over half the genes inherit parental gene expression patterns; and parental differential expression is often lost in the allopolyploid. Strikingly, the patterns of gene expression change are highly concordant with the genome-wide expression results of a cotton allopolyploid. The very different nature of these two allopolyploids implies a conserved, eukaryote-wide transcriptional response to genome merger. We provide evidence that the transcriptional responses we observe are mostly driven by intrinsic differences between the regulatory systems in the parent species, and from this propose a mechanistic model in which the cross-kingdom conservation in transcriptional response reflects conservation of the mutational processes underlying eukaryotic gene regulatory evolution. This work provides a platform to develop a universal understanding of gene expression response to allopolyploidy and suggests that allopolyploids are an exceptional system to investigate gene regulatory changes that have evolved in the parental species prior to allopolyploidization.

          Author Summary

          Organisms are complex biological systems that must continue to function even as their genomes evolve. While evolution is usually gradual, the formation of new species by the hybridization of different parents—allopolyploidization—occurs nearly instantaneously. A key question is what happens to expression of the two parental gene copies following genome merger. To determine this, we focused on a fungal allopolyploid from a group that dominates many of the world's pastoral economies. To investigate the fate of gene expression in this system, we developed a novel pipeline to assign high throughput RNA sequence reads to the two parental gene copies, thus allowing quantification of expression. We found transcriptional responses to be predominantly conservative: most gene copies either inherit parental expression patterns, or if differentially expressed in the parents, that difference is lost in the hybrid. Moreover, we identified an extraordinary level of concordance in the fate of genome-wide allopolyploid gene expression with that seen in cotton. The very different nature of these two allopolyploids suggests that there is a set of universal rules for the transcriptional response to genome merger. We propose a mechanistic model whereby this conserved response reflects similarities in mutational processes that underlie gene regulatory evolution.

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          The significance of responses of the genome to challenge.

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            Evolutionary changes in cis and trans gene regulation.

            Differences in gene expression are central to evolution. Such differences can arise from cis-regulatory changes that affect transcription initiation, transcription rate and/or transcript stability in an allele-specific manner, or from trans-regulatory changes that modify the activity or expression of factors that interact with cis-regulatory sequences. Both cis- and trans-regulatory changes contribute to divergent gene expression, but their respective contributions remain largely unknown. Here we examine the distribution of cis- and trans-regulatory changes underlying expression differences between closely related Drosophila species, D. melanogaster and D. simulans, and show functional cis-regulatory differences by comparing the relative abundance of species-specific transcripts in F1 hybrids. Differences in trans-regulatory activity were inferred by comparing the ratio of allelic expression in hybrids with the ratio of gene expression between species. Of 29 genes with interspecific expression differences, 28 had differences in cis-regulation, and these changes were sufficient to explain expression divergence for about half of the genes. Trans-regulatory differences affected 55% (16 of 29) of genes, and were always accompanied by cis-regulatory changes. These data indicate that interspecific expression differences are not caused by select trans-regulatory changes with widespread effects, but rather by many cis-acting changes spread throughout the genome.
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              Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia.

              The duplication of entire genomes has long been recognized as having great potential for evolutionary novelties, but the mechanisms underlying their resolution through gene loss are poorly understood. Here we show that in the unicellular eukaryote Paramecium tetraurelia, a ciliate, most of the nearly 40,000 genes arose through at least three successive whole-genome duplications. Phylogenetic analysis indicates that the most recent duplication coincides with an explosion of speciation events that gave rise to the P. aurelia complex of 15 sibling species. We observed that gene loss occurs over a long timescale, not as an initial massive event. Genes from the same metabolic pathway or protein complex have common patterns of gene loss, and highly expressed genes are over-retained after all duplications. The conclusion of this analysis is that many genes are maintained after whole-genome duplication not because of functional innovation but because of gene dosage constraints.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                March 2014
                6 March 2014
                : 10
                : 3
                : e1004180
                Affiliations
                [1 ]Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand
                [2 ]Institute of Natural and Mathematical Sciences, Massey University, Auckland, New Zealand
                University of California-Riverside, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ARDG MPC DBS. Performed the experiments: MPC GS YD ARDG. Analyzed the data: MPC TD ARDG. Contributed reagents/materials/analysis tools: ARDG MPC DBS. Wrote the paper: ARDG MPC. Designed the software used in analysis: MPC. Obtained permission for use of the reference genome: DBS MPC.

                [¤]

                Current address: Department of Botany, University of Pune, Ganeshkhind, Pune, India.

                Article
                PGENETICS-D-13-01805
                10.1371/journal.pgen.1004180
                3945203
                24603805
                12541c37-d93c-4edc-b240-7f02b3cfbce0
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 8 July 2013
                : 2 January 2014
                Page count
                Pages: 15
                Funding
                The Tertiary Education Commission supported this research via BioProtection Research Center ( http://bioprotection.org.nz) grants to DBS (3–10-MU) and MPC (3–11-MU). The Royal Society of New Zealand also provided support via a Rutherford Fellowship ( http://www.royalsociety.org.nz) to MPC (RDF-10-MAU-001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Computational Biology
                Genomics
                Genome Expression Analysis
                Evolutionary Biology
                Genomic Evolution
                Genetics
                Gene expression
                DNA transcription
                Molecular Genetics
                Gene Regulation
                Microbiology
                Mycology
                Fungi

                Genetics
                Genetics

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