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      A Parthenogenesis Gene Candidate and Evidence for Segmental Allopolyploidy in Apomictic Brachiaria decumbens

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          Abstract

          Apomixis, asexual reproduction through seed, enables breeders to identify and faithfully propagate superior heterozygous genotypes by seed without the disadvantages of vegetative propagation or the expense and complexity of hybrid seed production. The availability of new tools such as genotyping by sequencing and bioinformatics pipelines for species lacking reference genomes now makes the construction of dense maps possible in apomictic species, despite complications including polyploidy, multisomic inheritance, self-incompatibility, and high levels of heterozygosity. In this study, we developed saturated linkage maps for the maternal and paternal genomes of an interspecific Brachiaria ruziziensis (R. Germ. and C. M. Evrard) × B. decumbens Stapf. F 1 mapping population in order to identify markers linked to apomixis. High-resolution molecular karyotyping and comparative genomics with Setaria italica (L.) P. Beauv provided conclusive evidence for segmental allopolyploidy in B. decumbens, with strong preferential pairing of homologs across the genome and multisomic segregation relatively more common in chromosome 8. The apospory-specific genomic region (ASGR) was mapped to a region of reduced recombination on B. decumbens chromosome 5. The Pennisetum squamulatum (L.) R.Br. PsASGR-BABY BOOM-like ( psASGR–BBML)-specific primer pair p779/p780 was in perfect linkage with the ASGR in the F 1 mapping population and diagnostic for reproductive mode in a diversity panel of known sexual and apomict Brachiaria (Trin.) Griseb. and P. maximum Jacq. germplasm accessions and cultivars. These findings indicate that ASGR–BBML gene sequences are highly conserved across the Paniceae and add further support for the postulation of the ASGR–BBML as candidate genes for the apomictic function of parthenogenesis.

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          Most cited references34

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          The genetic control of apomixis: asexual seed formation.

          Apomixis (asexual seed formation) is the result of a plant gaining the ability to bypass the most fundamental aspects of sexual reproduction: meiosis and fertilization. Without the need for male fertilization, the resulting seed germinates a plant that develops as a maternal clone. This dramatic shift in reproductive process has been documented in many flowering plant species, although no major seed crops have been shown to be capable of apomixis. The ability to generate maternal clones and therefore rapidly fix desirable genotypes in crop species could accelerate agricultural breeding strategies. The potential of apomixis as a next-generation breeding technology has contributed to increasing interest in the mechanisms controlling apomixis. In this review, we discuss the progress made toward understanding the genetic and molecular control of apomixis. Research is currently focused on two fronts. One aims to identify and characterize genes causing apomixis in apomictic species that have been developed as model species. The other aims to engineer or switch the sexual seed formation pathway in non-apomictic species, to one that mimics apomixis. Here we describe the major apomictic mechanisms and update knowledge concerning the loci that control them, in addition to presenting candidate genes that may be used as tools for switching the sexual pathway to an apomictic mode of reproduction in crops.
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            Mendelian genetics of apomixis in plants.

            Apomixis, asexual reproduction through seeds, has the potential to revolutionize agriculture if its genetic basis can be elucidated. However, the genetic control of natural apomixis has remained obscure until quite recently, owing to all the complications of Mendelian genetics, such as epistatic gene interactions, components that are expressed sporophytically and gametophytically, expression modifiers, polyploidy, aneuploidy, segregation distortion, suppressed recombination, etc., that seem to have accumulated during the evolution of apomixis. In this review we show how molecular markers and superior phenotypic methods have been used to clarify the genetics of apomixis in monocots as well as dicots during the past 15 years. Many of the complexities in the genetics of apomixis are likely secondary and have evolved as a consequence of the reproductive process. New mapping techniques, such as comparative mapping, linkage disequilibrium mapping, and deletion mapping, and new high-throughput sequencing methods, will help to penetrate the core of apomixis chromosomal regions. If the evolutionary genetic load can be exposed and removed, the apomixis genes may be used in agriculture as a tool to fix elite genotypes.
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              A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant.

              Apomixis is a naturally occurring mode of asexual reproduction in flowering plants that results in seed formation without the involvement of meiosis or fertilization of the egg. Seeds formed on an apomictic plant contain offspring genetically identical to the maternal plant. Apomixis has significant potential for preserving hybrid vigor from one generation to the next in highly productive crop plant genotypes. Apomictic Pennisetum/Cenchrus species, members of the Poaceae (grass) family, reproduce by apospory. Apospory is characterized by apomeiosis, the formation of unreduced embryo sacs derived from nucellar cells of the ovary and, by parthenogenesis, the development of the unreduced egg into an embryo without fertilization. In Pennisetum squamulatum (L.) R.Br., apospory segregates as a single dominant locus, the apospory-specific genomic region (ASGR). In this study, we demonstrate that the PsASGR-BABY BOOM-like (PsASGR-BBML) gene is expressed in egg cells before fertilization and can induce parthenogenesis and the production of haploid offspring in transgenic sexual pearl millet. A reduction of PsASGR-BBML expression in apomictic F1 RNAi transgenic plants results in fewer visible parthenogenetic embryos and a reduction of embryo cell number compared with controls. Our results endorse a key role for PsASGR-BBML in parthenogenesis and a newly discovered role for a member of the BBM-like clade of APETALA 2 transcription factors. Induction of parthenogenesis by PsASGR-BBML will be valuable for installing parthenogenesis to synthesize apomixis in crops and will have further application for haploid induction to rapidly obtain homozygous lines for breeding.
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                Author and article information

                Journal
                Genetics
                Genetics
                genetics
                genetics
                genetics
                Genetics
                Genetics Society of America
                0016-6731
                1943-2631
                July 2016
                20 May 2016
                20 May 2016
                : 203
                : 3
                : 1117-1132
                Affiliations
                [* ]International Center for Tropical Agriculture (CIAT), Cali 763537, Colombia
                []Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520
                []The Genome Analysis Centre, Norwich Research Park, Colney, Norwich NR4 7UH, United Kingdom
                Author notes
                [1 ]Corresponding author: International Center for Tropical Agriculture, Tropical Forages, Km 17 Recta Cali-Palmira, Valle del Cauca 763537, Colombia. E-mail: m.worthington@ 123456cgiar.org
                [2]

                Present address: Department of Chemistry and Chemical Biology, Northeastern University, Boston, MA 02115.

                Author information
                http://orcid.org/0000-0001-8019-165X
                http://orcid.org/0000-0003-2847-5158
                Article
                190314
                10.1534/genetics.116.190314
                4937464
                27206716
                d217c102-2759-4696-81b9-88a75677ea4b
                Copyright © 2016 by the Genetics Society of America

                Available freely online through the author-supported open access option.

                History
                : 11 April 2016
                : 14 May 2016
                Page count
                Figures: 6, Tables: 3, Equations: 0, References: 80, Pages: 16
                Categories
                Investigations
                Genome Integrity and Transmission

                Genetics
                polyploidy,genetic linkage map,apospory,genotyping by sequencing,molecular karyotyping
                Genetics
                polyploidy, genetic linkage map, apospory, genotyping by sequencing, molecular karyotyping

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