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      Resolving deep relationships of PACMAD grasses: a phylogenomic approach

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          Abstract

          Background

          Plastome sequences for 18 species of the PACMAD grasses (subfamilies Panicoideae, Aristidoideae, Chloridoideae, Micrairoideae, Arundinoideae, Danthonioideae) were analyzed phylogenomically. Next generation sequencing methods were used to provide complete plastome sequences for 12 species. Sanger sequencing was performed to determine the plastome of one species, Hakonechloa macra, to provide a reference for annotation. These analyses were conducted to resolve deep subfamilial relationships within the clade. Divergence estimates were assessed to determine potential factors that led to the rapid radiation of this lineage and its dominance of warmer open habitats.

          Results

          New plastomes were completely sequenced and characterized for 13 PACMAD species. An autapomorphic ~1140 bp deletion was found in Hakonechloa macra putatively pseudogenizing rpl14 and eliminating rpl16 from this plastome. Phylogenomic analyses support Panicoideae as the sister group to the ACMAD clade. Complete plastome sequences provide greater support at deep nodes within the PACMAD clade. The initial diversification of PACMAD subfamilies was estimated to occur at 32.4 mya.

          Conclusions

          Phylogenomic analyses of complete plastomes provides resolution for deep relationships of PACMAD grasses. The divergence estimate of 32.4 mya at the crown node of the PACMAD clade coincides with the Eocene-Oligocene Transition (EOT). The Eocene was a period of global cooling and drying, which led to forest fragmentation and the expansion of open habitats now dominated by these grasses. Understanding how these grasses are related and determining a cause for their rapid radiation allows for future predictions of grassland distribution in the face of a changing global climate.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12870-015-0563-9) contains supplementary material, which is available to authorized users.

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          Most cited references34

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          Sequence and comparative analysis of the maize NB mitochondrial genome.

          The NB mitochondrial genome found in most fertile varieties of commercial maize (Zea mays subsp. mays) was sequenced. The 569,630-bp genome maps as a circle containing 58 identified genes encoding 33 known proteins, 3 ribosomal RNAs, and 21 tRNAs that recognize 14 amino acids. Among the 22 group II introns identified, 7 are trans-spliced. There are 121 open reading frames (ORFs) of at least 300 bp, only 3 of which exist in the mitochondrial genome of rice (Oryza sativa). In total, the identified mitochondrial genes, pseudogenes, ORFs, and cis-spliced introns extend over 127,555 bp (22.39%) of the genome. Integrated plastid DNA accounts for an additional 25,281 bp (4.44%) of the mitochondrial DNA, and phylogenetic analyses raise the possibility that copy correction with DNA from the plastid is an ongoing process. Although the genome contains six pairs of large repeats that cover 17.35% of the genome, small repeats (20-500 bp) account for only 5.59%, and transposable element sequences are extremely rare. MultiPip alignments show that maize mitochondrial DNA has little sequence similarity with other plant mitochondrial genomes, including that of rice, outside of the known functional genes. After eliminating genes, introns, ORFs, and plastid-derived DNA, nearly three-fourths of the maize NB mitochondrial genome is still of unknown origin and function.
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            Oligocene CO2 decline promoted C4 photosynthesis in grasses.

            C4 photosynthesis is an adaptation derived from the more common C3 photosynthetic pathway that confers a higher productivity under warm temperature and low atmospheric CO2 concentration [1, 2]. C4 evolution has been seen as a consequence of past atmospheric CO2 decline, such as the abrupt CO2 fall 32-25 million years ago (Mya) [3-6]. This relationship has never been tested rigorously, mainly because of a lack of accurate estimates of divergence times for the different C4 lineages [3]. In this study, we inferred a large phylogenetic tree for the grass family and estimated, through Bayesian molecular dating, the ages of the 17 to 18 independent grass C4 lineages. The first transition from C3 to C4 photosynthesis occurred in the Chloridoideae subfamily, 32.0-25.0 Mya. The link between CO2 decrease and transition to C4 photosynthesis was tested by a novel maximum likelihood approach. We showed that the model incorporating the atmospheric CO2 levels was significantly better than the null model, supporting the importance of CO2 decline on C4 photosynthesis evolvability. This finding is relevant for understanding the origin of C4 photosynthesis in grasses, which is one of the most successful ecological and evolutionary innovations in plant history.
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              The age of the grasses and clusters of origins of C4photosynthesis

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                Author and article information

                Contributors
                joebtcotton@gmail.com
                wwysoc2@gmail.com
                lgclark@iastate.edu
                kelchner@isu.edu
                piresjc@missouri.edu
                pedger@gmail.com
                dmayfield-jones@danforthcenter.org
                mel-duvall@niu.edu
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                11 July 2015
                11 July 2015
                2015
                : 15
                : 178
                Affiliations
                [ ]Biological Sciences, Northern Illinois University, 1425 W. Lincoln Hwy, DeKalb, Illinois 60115-2861 U.S.A
                [ ]Ecology, Evolution and Organismal Biology, Iowa State University, 251 Bessey Hall, Ames, Iowa 50011-1020 U.S.A
                [ ]Division of Biological Sciences, Bond Life Sciences Center, University of Missouri, Columbia, MO 65211-7310 U.S.A
                [ ]Department of Plant and Microbial Biology, University of California, Berkeley, California, 94720 U.S.A
                [ ]Biological Sciences, Idaho State University, 921 S. 8th Ave, Pocatello, Idaho 83209 U.S.A
                [ ]Donald Danforth Plant Science Center, 975 North Warson Rd, St. Louis, Missouri 63132 U.S.A
                Article
                563
                10.1186/s12870-015-0563-9
                4498559
                26160195
                2d2f87ad-0470-4d6a-b14e-9986f080cb17
                © Cotton et al. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.

                History
                : 20 January 2015
                : 25 June 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Plant science & Botany
                complete plastome,divergence estimates,pacmad clade,panicoideae,phylogenomics,rapid radiation

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