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      Comparative transcriptomics among floral organs of the basal eudicot Eschscholzia californica as reference for floral evolutionary developmental studies

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          Abstract

          Background

          Molecular genetic studies of floral development have concentrated on several core eudicots and grasses (monocots), which have canalized floral forms. Basal eudicots possess a wider range of floral morphologies than the core eudicots and grasses and can serve as an evolutionary link between core eudicots and monocots, and provide a reference for studies of other basal angiosperms. Recent advances in genomics have enabled researchers to profile gene activities during floral development, primarily in the eudicot Arabidopsis thaliana and the monocots rice and maize. However, our understanding of floral developmental processes among the basal eudicots remains limited.

          Results

          Using a recently generated expressed sequence tag (EST) set, we have designed an oligonucleotide microarray for the basal eudicot Eschscholzia californica (California poppy). We performed microarray experiments with an interwoven-loop design in order to characterize the E. californica floral transcriptome and to identify differentially expressed genes in flower buds with pre-meiotic and meiotic cells, four floral organs at pre-anthesis stages (sepals, petals, stamens and carpels), developing fruits, and leaves.

          Conclusions

          Our results provide a foundation for comparative gene expression studies between eudicots and basal angiosperms. We identified whorl-specific gene expression patterns in E. californica and examined the floral expression of several gene families. Interestingly, most E. californica homologs of Arabidopsis genes important for flower development, except for genes encoding MADS-box transcription factors, show different expression patterns between the two species. Our comparative transcriptomics study highlights the unique evolutionary position of E. californica compared with basal angiosperms and core eudicots.

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          Most cited references82

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          Small RNAs and their roles in plant development.

          Small RNAs of 20-30 nucleotides guide regulatory processes at the DNA or RNA level in a wide range of eukaryotic organisms. Many, although not all, small RNAs are processed from double-stranded RNAs or single-stranded RNAs with local hairpin structures by RNase III enzymes and are loaded into argonaute-protein-containing effector complexes. Many eukaryotic organisms have evolved multiple members of RNase III and the argonaute family of proteins to accommodate different classes of small RNAs with specialized molecular functions. Some small RNAs cause transcriptional gene silencing by guiding heterochromatin formation at homologous loci, whereas others lead to posttranscriptional gene silencing through mRNA degradation or translational inhibition. Small RNAs are not only made from and target foreign nucleic acids such as viruses and transgenes, but are also derived from endogenous loci and regulate a multitude of developmental and physiological processes. Here I review the biogenesis and function of three major classes of endogenous small RNAs in plants: microRNAs, trans-acting siRNAs, and heterochromatic siRNAs, with an emphasis on the roles of these small RNAs in developmental regulation.
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            Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms.

            Although great progress has been made in clarifying deep-level angiosperm relationships, several early nodes in the angiosperm branch of the Tree of Life have proved difficult to resolve. Perhaps the last great question remaining in basal angiosperm phylogeny involves the branching order among the five major clades of mesangiosperms (Ceratophyllum, Chloranthaceae, eudicots, magnoliids, and monocots). Previous analyses have found no consistent support for relationships among these clades. In an effort to resolve these relationships, we performed phylogenetic analyses of 61 plastid genes ( approximately 42,000 bp) for 45 taxa, including members of all major basal angiosperm lineages. We also report the complete plastid genome sequence of Ceratophyllum demersum. Parsimony analyses of combined and partitioned data sets varied in the placement of several taxa, particularly Ceratophyllum, whereas maximum-likelihood (ML) trees were more topologically stable. Total evidence ML analyses recovered a clade of Chloranthaceae + magnoliids as sister to a well supported clade of monocots + (Ceratophyllum + eudicots). ML bootstrap and Bayesian support values for these relationships were generally high, although approximately unbiased topology tests could not reject several alternative topologies. The extremely short branches separating these five lineages imply a rapid diversification estimated to have occurred between 143.8 +/- 4.8 and 140.3 +/- 4.8 Mya.
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              Widespread genome duplications throughout the history of flowering plants.

              Genomic comparisons provide evidence for ancient genome-wide duplications in a diverse array of animals and plants. We developed a birth-death model to identify evidence for genome duplication in EST data, and applied a mixture model to estimate the age distribution of paralogous pairs identified in EST sets for species representing the basal-most extant flowering plant lineages. We found evidence for episodes of ancient genome-wide duplications in the basal angiosperm lineages including Nuphar advena (yellow water lily: Nymphaeaceae) and the magnoliids Persea americana (avocado: Lauraceae), Liriodendron tulipifera (tulip poplar: Magnoliaceae), and Saruma henryi (Aristolochiaceae). In addition, we detected independent genome duplications in the basal eudicot Eschscholzia californica (California poppy: Papaveraceae) and the basal monocot Acorus americanus (Acoraceae), both of which were distinct from duplications documented for ancestral grass (Poaceae) and core eudicot lineages. Among gymnosperms, we found equivocal evidence for ancient polyploidy in Welwitschia mirabilis (Gnetales) and no evidence for polyploidy in pine, although gymnosperms generally have much larger genomes than the angiosperms investigated. Cross-species sequence divergence estimates suggest that synonymous substitution rates in the basal angiosperms are less than half those previously reported for core eudicots and members of Poaceae. These lower substitution rates permit inference of older duplication events. We hypothesize that evidence of an ancient duplication observed in the Nuphar data may represent a genome duplication in the common ancestor of all or most extant angiosperms, except Amborella.
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                Author and article information

                Journal
                Genome Biol
                Genome Biology
                BioMed Central
                1465-6906
                1465-6914
                2010
                15 October 2010
                : 11
                : 10
                : R101
                Affiliations
                [1 ]Department of Biology, The Pennsylvania State University, University Park, PA 16802, USA
                [2 ]The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA
                [3 ]The Intercollege Graduate Program in Cell and Developmental Biology, The Pennsylvania State University, University Park, PA 16802, USA
                [4 ]Department of Statistics, The Pennsylvania State University, University Park, PA 16802, USA
                [5 ]Department of Bioinformatics and Genomics, The University of North Carolina at Charlotte, 9201 University City Boulevard, Charlotte, NC 28223, USA
                [6 ]State Key Laboratory of Genetic Engineering and School of Life Sciences, Fudan University, 220 Handan Road, Shanghai 200433, China
                [7 ]Institutes of Biomedical Sciences, Fudan University, 138 Yixueyuan Road, Shanghai 200032, China
                [8 ]Current address: American Association for the Advancement of Science, 1200 New York Avenue NW, Washington DC 20005, USA
                [9 ]Current address: 2367 Setter Run Lane, State College, PA 16802, USA
                [10 ]Current address: BASF Plant Science, 26 Davis Drive, Research Triangle Park, NC 27709, USA
                [11 ]Current address: Department of Entomology, The Pennsylvania State University, University Park, PA 16802, USA
                [12 ]Current address: Department of Plant Biology, University of Georgia, 120 Carlton Street, Athens, GA 30602, USA
                Article
                gb-2010-11-10-r101
                10.1186/gb-2010-11-10-r101
                3218657
                20950453
                47aa6f4d-51de-45f4-a5e6-9ef24e0f113c
                Copyright ©2010 Zahn et al.; licensee BioMed Central Ltd.

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 June 2010
                : 3 August 2010
                : 15 October 2010
                Categories
                Research

                Genetics
                Genetics

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