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      The factors affecting the evolution of the anthocyanin biosynthesis pathway genes in monocot and dicot plant species

      research-article
      1 , , 1 , 2 , 1 , 2
      BMC Plant Biology
      BioMed Central
      Belyaev Conference
      07-10 August 2017
      Anthocyanin biosynthesis, Dicots, Monocots, Gene regulation, Pollination type, Selective constraint

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          Abstract

          Background

          The available data demonstrate that even in universal metabolic pathways, some species-specific regulatory features of structural genes are present. For instance, in the anthocyanin biosynthesis pathway (ABP), genes may be regulated by ABP-specific regulatory factors, and their expression levels may be strongly associated with anthocyanin pigmentation, or they may be expressed independently of pigmentation. A dataset of orthologous ABP genes ( Chs, Chi, F3h, F3’h, Dfr, Ans) from monocot and dicot plant species that have distinct gene regulation patterns and different types of pollination was constructed to test whether these factors affect the evolution of the genes.

          Results

          Using a maximum likelihood approach, we demonstrated that although the whole set of the ABP genes is under purifying selection, with greater selection acting on the upstream genes than on the downstream genes, genes from distinct groups of plant species experienced different strengths of selective pressure. The selective pressure on the genes was higher in dicots than in monocots ( F3h and further downstream genes) and in pollinator-dependent plants than in pollinator-independent species ( Chi and further downstream genes), suggesting an important role of pollination type in the evolution of the anthocyanin biosynthesis gene network. Contrasting effects of the regulation patterns on evolution were detected for the F3h and Dfr genes, with greater selective pressure on the F3h gene in plant species where the gene expression was not strongly associated with pigmentation and greater selective pressure on Dfr in plant species where the gene expression was associated with pigmentation.

          Conclusions

          We demonstrated the effects of pollination type and patterns of regulation on the evolution of the ABP genes, but the evolution of some of the genes could not be explained in the framework of these factors, such as the weaker selective pressure acting on Chs in species that attract pollinators or the stronger selective pressure on F3h in plant species where the gene expression was not associated with pigmentation. The observations suggest that additional factors could affect the evolution of these genes. One such factor could be an effect of gene duplication with further division of functions among gene copies and relaxed selective pressure acting on them. Additional tests with an appropriate dataset combining data on duplicated gene sequences and their functions in the flavonoid biosynthesis pathway are required to test this hypothesis.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-017-1190-4) contains supplementary material, which is available to authorized users.

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          Most cited references29

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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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            Estimating the pattern of nucleotide substitution.

            Z. Yang (1994)
            Knowledge of the pattern of nucleotide substitution is important both to our understanding of molecular sequence evolution and to reliable estimation of phylogenetic relationships. The method of parsimony analysis, which has been used to estimate substitution patterns in real sequences, has serious drawbacks and leads to results difficult to interpret. In this paper a model-based maximum likelihood approach is proposed for estimating substitution patterns in real sequences. Nucleotide substitution is assumed to follow a homogeneous Markov process, and the general reversible process model (REV) and the unrestricted model without the reversibility assumption are used. These models are also applied to examine the adequacy of the model of Hasegawa et al. (J. Mol. Evol. 1985;22:160-174) (HKY85). Two data sets are analyzed. For the psi eta-globin pseudogenes of six primate species, the REV models fits the data much better than HKY85, while, for a segment of mtDNA sequences from nine primates, REV cannot provide a significantly better fit than HKY85 when rate variation over sites is taken into account in the models. It is concluded that the use of the REV model in phylogenetic analysis can be recommended, especially for large data sets or for sequences with extreme substitution patterns, while HKY85 may be expected to provide a good approximation. The use of the unrestricted model does not appear to be worthwhile.
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              Expression of anthocyanin biosynthesis pathway genes in red and white grapes.

              The expression of seven genes from the anthocyanin biosynthesis pathway was determined in different tissues of Shiraz grapevines. All of the tissues contained proanthocyanidins, but only the berry skin accumulated anthocyanins. In most tissues, all of the flavonoid genes except UDP glucose-flavonoid 3-o-glucosyl transferase (UFGT) were expressed, but UFGT expression was only detected in berry skin. Similar patterns of expression were observed in the skin of other red grapes. In white grapes, UFGT expression was not detected. White grape cultivars appear to lack anthocyanins because they lack UFGT, although they also had decreased expression of other flavonoid pathway genes.
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                Author and article information

                Contributors
                olesya_ter@bionet.nsc.ru
                glagoleva@bionet.nsc.ru
                khlest@bionet.nsc.ru
                Conference
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                28 December 2017
                28 December 2017
                2017
                : 17
                Issue : Suppl 2 Issue sponsor : Publication of this supplement has not been supported by sponsorship. Information about the source of funding for publication charges can be found in the individual articles. The articles have undergone the journal's standard peer review process for supplements. The Supplement Editors declare that they have no competing interests.
                : 256
                Affiliations
                [1 ]GRID grid.418953.2, Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, ; Novosibirsk, Russia
                [2 ]ISNI 0000000121896553, GRID grid.4605.7, Novosibirsk State University, ; Novosibirsk, Russia
                Article
                1190
                10.1186/s12870-017-1190-4
                5751542
                29297327
                97f79fad-8e9f-48f8-952f-e5770b992aa6
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Belyaev Conference
                Novosibirsk, Russia
                07-10 August 2017
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                © The Author(s) 2017

                Plant science & Botany
                anthocyanin biosynthesis,dicots,monocots,gene regulation,pollination type,selective constraint

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