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Duplication and Loss of Function of Genes Encoding RNA Polymerase III Subunit C4 Causes Hybrid Incompatibility in Rice

Reproductive barriers are commonly observed in both animals and plants, in which they maintain species integrity and contribute to speciation. This report shows that a combination of loss-of-function alleles at two duplicated loci, DUPLICATED GAMETOPHYTIC STERILITY 1 (DGS1) on chromosome 4 and DGS2 on chromosome 7, causes pollen sterility in hybrid progeny derived from an interspecific cross between cultivated rice, Oryza sativa, and an Asian annual wild rice, O. nivara.

Giao Ngoc Nguyen, Y Yamagata, Y Shigenmatsu, M Watanabe, Y Miyazaki, K Doi, K Tashiro, S Kuhara, H Kanamori, J Wu, T Matsumoto, H Yasui and A Yoshimura

G3: Genes, Genomes, Genetics August 1, 2017 vol. 7 no. 8 2565-2575; https://doi.org/10.1534/g3.117.043943

Abstract

Reproductive barriers are commonly observed in both animals and plants, in which they maintain species integrity and contribute to speciation. This report shows that a combination of loss-of-function alleles at two duplicated loci, DUPLICATED GAMETOPHYTIC STERILITY 1 (DGS1) on chromosome 4 and DGS2 on chromosome 7, causes pollen sterility in hybrid progeny derived from an interspecific cross between cultivated rice, Oryza sativa, and an Asian annual wild rice, O. nivara. Male gametes carrying the DGS1 allele from O. nivara (DGS1-nivaras) and the DGS2 allele from O. sativa (DGS2-T65s) were sterile, but female gametes carrying the same genotype were fertile. We isolated the causal gene, which encodes a protein homologous to DNA-dependent RNA polymerase (RNAP) III subunit C4 (RPC4). RPC4 facilitates the transcription of 5S rRNAs and tRNAs. The loss-of-function alleles at DGS1-nivaras and DGS2-T65s were caused by weak or nonexpression of RPC4 and an absence of RPC4, respectively. Phylogenetic analysis demonstrated that gene duplication of RPC4 at DGS1 and DGS2 was a recent event that occurred after divergence of the ancestral population of Oryza from other Poaceae or during diversification of AA-genome species.

 

See http://www.g3journal.org/content/7/8/2565?etoc=

Figure 2: Linkage mapping and map-based cloning of DGS1 and DGS2. (A and B) Linkage mapping of (A) DGS1 and (B) DGS2. (C and D) High-resolution mapping of (C) DGS1 and (D) DGS2. The number in parentheses beneath each marker represents the number of recombinants between that marker and the DGS gene. (E) Diagrams of the BAC clones in the DGS1 and DGS2 regions of T65 and O. nivara. Segmental duplications (white boxes) were found in the DGS1-T65+, DGS1-nivaras, and DGS2-nivara+ alleles, but not in the DGS2-T65s allele. Black pentagons represent the predicted RPC4 genes. Dotted lines represent the EcoRI fragments used for the transgenic complementation tests. Homologous genomic regions are connected by translucent gray areas. Black arrowhead indicates site where segmental duplication was not found or deleted in DGS2-T65s. (F) Structure of RPC4. White boxes represent 5′- and 3′-untranslated regions. Black boxes indicate coding sequences within exons. Arrows indicate the positions of amino acid polymorphisms among the copies of RPC4. Horizontal bars indicate position of the RNA polymerase III subunit C4 domain. BAC, bacterial artificial chromosome; Chr., chromosome.

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