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      A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant

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      Proceedings of the National Academy of Sciences

      Proceedings of the National Academy of Sciences

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          Abstract

          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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          Most cited references 17

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          PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development.

          Factors with a graded distribution can program fields of cells in a dose-dependent manner, but no evidence has hitherto surfaced for such mechanisms in plants. In the Arabidopsis thaliana root, two PLETHORA (PLT) genes encoding AP2-domain transcription factors have been shown to maintain the activity of stem cells. Here we show that a clade of four PLT homologues is necessary for root formation. Promoter activity and protein fusions of PLT homologues display gradient distributions with maxima in the stem cell area. PLT activities are largely additive and dosage dependent. High levels of PLT activity promote stem cell identity and maintenance; lower levels promote mitotic activity of stem cell daughters; and further reduction in levels is required for cell differentiation. Our findings indicate that PLT protein dosage is translated into distinct cellular responses.
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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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              Phylogeny and domain evolution in the APETALA2-like gene family.

              The combined processes of gene duplication, nucleotide substitution, domain duplication, and intron/exon shuffling can generate a complex set of related genes that may differ substantially in their expression patterns and functions. The APETALA2-like (AP2-like) gene family exhibits patterns of both gene and domain duplication, coupled with changes in sequence, exon arrangement, and expression. In angiosperms, these genes perform an array of functions including the establishment of the floral meristem, the specification of floral organ identity, the regulation of floral homeotic gene expression, the regulation of ovule development, and the growth of floral organs. To determine patterns of gene diversification, we conducted a series of broad phylogenetic analyses of AP2-like sequences from green plants. These studies indicate that the AP2 domain was duplicated prior to the divergence of the two major lineages of AP2-like genes, euAP2 and AINTEGUMENTA (ANT). Structural features of the AP2-like genes as well as phylogenetic analyses of nucleotide and amino acid (aa) sequences of the AP2-like gene family support the presence of the two major lineages. The ANT lineage is supported by a 10-aa insertion in the AP2-R1 domain and a 1-aa insertion in the AP2-R2 domain, relative to all other members of the AP2-like family. MicroRNA172-binding sequences, the function of which has been studied in some of the AP2-like genes in Arabidopsis, are restricted to the euAP2 lineage. Within the ANT lineage, the euANT lineage is characterized by four conserved motifs: one in the 10-aa insertion in the AP2-R1 domain (euANT1) and three in the predomain region (euANT2, euANT3, and euANT4). Our expression studies show that the euAP2 homologue from Amborella trichopoda, the putative sister to all other angiosperms, is expressed in all floral organs as well as leaves.
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                Author and article information

                Journal
                Proceedings of the National Academy of Sciences
                Proc Natl Acad Sci USA
                Proceedings of the National Academy of Sciences
                0027-8424
                1091-6490
                September 08 2015
                September 08 2015
                September 08 2015
                August 24 2015
                : 112
                : 36
                : 11205-11210
                Article
                10.1073/pnas.1505856112
                4568661
                26305939
                © 2015

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