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      Apomictic and Sexual Germline Development Differ with Respect to Cell Cycle, Transcriptional, Hormonal and Epigenetic Regulation

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          Abstract

          Seeds of flowering plants can be formed sexually or asexually through apomixis. Apomixis occurs in about 400 species and is of great interest for agriculture as it produces clonal offspring. It differs from sexual reproduction in three major aspects: (1) While the sexual megaspore mother cell (MMC) undergoes meiosis, the apomictic initial cell (AIC) omits or aborts meiosis (apomeiosis); (2) the unreduced egg cell of apomicts forms an embryo without fertilization (parthenogenesis); and (3) the formation of functional endosperm requires specific developmental adaptations. Currently, our knowledge about the gene regulatory programs underlying apomixis is scarce. We used the apomict Boechera gunnisoniana, a close relative of Arabidopsis thaliana, to investigate the transcriptional basis underlying apomeiosis and parthenogenesis. Here, we present the first comprehensive reference transcriptome for reproductive development in an apomict. To compare sexual and apomictic development at the cellular level, we used laser-assisted microdissection combined with microarray and RNA-Seq analyses. Conservation of enriched gene ontologies between the AIC and the MMC likely reflects functions of importance to germline initiation, illustrating the close developmental relationship of sexuality and apomixis. However, several regulatory pathways differ between sexual and apomictic germlines, including cell cycle control, hormonal pathways, epigenetic and transcriptional regulation. Enrichment of specific signal transduction pathways are a feature of the apomictic germline, as is spermidine metabolism, which is associated with somatic embryogenesis in various plants. Our study provides a comprehensive reference dataset for apomictic development and yields important new insights into the transcriptional basis underlying apomixis in relation to sexual reproduction.

          Author Summary

          In flowering plants, asexual reproduction through seeds (apomixis) likely evolved from sexual ancestors several times independently. Only three key developmental steps differ between sexual reproduction and apomixis. In contrast to sexual reproduction, in apomicts the first cell of the female reproductive lineage omits or aborts meiosis (apomeiosis) to initiate gamete formation. Subsequently, the egg cell develops into an embryo without fertilization (parthenogenesis), and endosperm formation can either be autonomous or depend on fertilization. Consequently, the offspring of apomicts is genetically identical to the mother plant. The production of clonal seeds bears great promise for agricultural applications. However, the targeted manipulation of reproductive pathways for seed production has proven difficult as knowledge about the underlying gene regulatory processes is limited. We performed cell type-specific transcriptome analyses to study apomictic germline development in Boechera gunnisoniana, an apomictic species closely related to Arabidopsis thaliana. To facilitate these analyses, we first characterized a floral reference transcriptome. In comparison, we identified several regulatory pathways, including core cell cycle regulation, protein degradation, transcription factor activity, and hormonal pathways to be differentially regulated between sexual and apomictic plants. Apart from new insights into the underlying transcriptional networks, our dataset provides a valuable starting point for functional investigations.

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          Most cited references 65

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          MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis.

          Arabidopsis embryos lacking DICER-LIKE1 (DCL1), which is required for microRNA (miRNA) biogenesis, arrest early in development. To assess the functions of embryonic miRNAs, we determined the developmental and molecular consequences of DCL1 loss. We found that DCL1 is required for cell differentiation events as early as the eight-cell stage and soon thereafter for proper division of the hypophysis and subprotoderm cells. By the early globular (∼32-cell) stage, dcl1-null mutant embryos overexpress ∼50 miRNA targets. In dcl1 eight-cell embryos, the two most up-regulated targets are those of miR156 and encode SPL10 and SPL11 transcription factors. SPL10 and SPL11 are derepressed >150-fold in dcl1 embryos and are redundantly required for the dcl1 early patterning defects. Moreover, as early as the eight-cell stage, miR156-mediated repression of zygotic SPL transcripts prevents premature accumulation of transcripts from genes normally induced during the embryonic maturation phase. Thus, the first perceptible molecular function of plant embryonic miRNAs is the opposite of that in vertebrates; in vertebrates, miRNAs sharpen the first developmental transition, whereas in plants, they forestall developmental transitions by repressing mRNAs that act later. We propose that, by preventing precocious expression of differentiation-promoting transcription factors, miRNAs enable proper embryonic patterning.
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            The natural polyamine spermine functions directly as a free radical scavenger.

            The polyamines are small organic cations that are absolutely required for eukaryotic cell growth. Although their growth requirements are well established, the molecular functions of the polyamines are ill-defined. Oxidative damage to DNA by reactive oxygen species is a continual problem that cells must guard against to survive. The polyamine spermine, which is normally found in millimolar concentrations in the nucleus, is shown here to function directly as a free radical scavenger, and adducts formed as a result of this function are identified. These data suggest that spermine is a major natural intracellular compound capable of protecting DNA from free radical attack.
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              Apomixis: a developmental perspective.

              The term apomixis encompasses a suite of processes whereby seeds form asexually in plants. In contrast to sexual reproduction, seedlings arising from apomixis retain the genotype of the maternal parent. The transfer of apomixis and its effective utilization in crop plants (where it is largely absent) has major advantages in agriculture. The hallmark components of apomixis include female gamete formation without meiosis (apomeiosis), fertilization-independent embryo development (parthenogenesis), and developmental adaptations to ensure functional endosperm formation. Understanding the molecular mechanisms underlying apomixis, a developmentally fascinating phenomenon in plants, is critical for the successful induction and utilization of apomixis in crop plants. This review draws together knowledge gained from analyzing ovule, embryo, and endosperm development in sexual and apomictic plants. It consolidates the view that apomixis and sexuality are closely interrelated developmental pathways where apomixis can be viewed as a deregulation of the sexual process in both time and space.
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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
                July 2014
                10 July 2014
                : 10
                : 7
                Affiliations
                [1 ]Institute of Plant Biology & Zürich-Basel Plant Science Center, University of Zürich, Zürich, Switzerland
                [2 ]Institute of Clinical Molecular Biology, Christian-Albrechts University, Kiel, Germany
                [3 ]Functional Genomics Center Zürich, UZH/ETH Zürich, Zürich, Switzerland
                CCMB, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AS UG. Performed the experiments: AS UCK CS DG MW. Analyzed the data: AS MWS UG UCK CS DG MW WQ. Contributed reagents/materials/analysis tools: WQ MWS AS PR UG. Wrote the paper: AS. Performed bioinformatic analyses: AS MWS WQ. Helped writing the paper: UG MWS. Participated in the design of RNA-Seq experiments and their analysis: PR. Revised and approved the manuscript: AS UG UCK CS DG MW MWS WQ.

                Article
                PGENETICS-D-13-03138
                10.1371/journal.pgen.1004476
                4091798
                25010342

                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.

                Page count
                Pages: 21
                Funding
                This project was supported by the University of Zürich, the Marie Curie project IDEAGENA (to AS), and grants from the “Staatssekretariat für Bildung und Forschung” in the framework of COST action FA0903 (to AS and UG) and the Swiss National Science Foundation (to UG). PR was supported by the DFG Cluster of excellence Inflammation at Interfaces (CL Nucleotide lab). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biotechnology
                Plant Biotechnology
                Plant Genomics
                Developmental Biology
                Genetics
                Gene Expression
                Genomics
                Molecular Genetics
                Plant Genetics
                Plant Science

                Genetics

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