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Immediate Genetic and Epigenetic Changes in F1 Hybrids Parented by Species with Divergent Genomes in the Rice Genus (Oryza).

Wu Y, Sun Y, Shen K, Sun S, Wang J, Jiang T, Cao S, Josiah SM, Pang J, Lin X, Liu B - PLoS ONE (2015)

Bottom Line: Transcriptional and transpositional activity of several transposable elements (TEs) and methylation stability of their flanking regions were also assessed.Artificially constructed inter-specific hybrids of remotely related species with divergent genomes in genus Oryza are chromosomally stable but show immediate and highly stochastic genetic and epigenetic instabilities at the molecular level.These novel hybrids might provide a rich resource of genetic and epigenetic diversities for potential utilization in rice genetic improvements.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Molecular Epigenetics of MOE and Institute of Genetics and Cytology, Northeast Normal University, Changchun, China.

ABSTRACT

Background: Inter-specific hybridization occurs frequently in higher plants, and represents a driving force of evolution and speciation. Inter-specific hybridization often induces genetic and epigenetic instabilities in the resultant homoploid hybrids or allopolyploids, a phenomenon known as genome shock. Although genetic and epigenetic consequences of hybridizations between rice subspecies (e.g., japonica and indica) and closely related species sharing the same AA genome have been extensively investigated, those of inter-specific hybridizations between more remote species with different genomes in the rice genus, Oryza, remain largely unknown.

Methodology/principal findings: We investigated the immediate chromosomal and molecular genetic/epigenetic instability of three triploid F1 hybrids produced by inter-specific crossing between species with divergent genomes of Oryza by genomic in situ hybridization (GISH) and molecular marker analysis. Transcriptional and transpositional activity of several transposable elements (TEs) and methylation stability of their flanking regions were also assessed. We made the following principle findings: (i) all three triploid hybrids are stable in both chromosome number and gross structure; (ii) stochastic changes in both DNA sequence and methylation occurred in individual plants of all three triploid hybrids, but in general methylation changes occurred at lower frequencies than genetic changes; (iii) alteration in DNA methylation occurred to a greater extent in genomic loci flanking potentially active TEs than in randomly sampled loci; (iv) transcriptional activation of several TEs commonly occurred in all three hybrids but transpositional events were detected in a genetic context-dependent manner.

Conclusions/significance: Artificially constructed inter-specific hybrids of remotely related species with divergent genomes in genus Oryza are chromosomally stable but show immediate and highly stochastic genetic and epigenetic instabilities at the molecular level. These novel hybrids might provide a rich resource of genetic and epigenetic diversities for potential utilization in rice genetic improvements.

No MeSH data available.


Related in: MedlinePlus

Schematic diagrams for three F1 rice hybrids, their genome compositions and several representative phenotypic traits.(A) Diagrams showing the parents and process for the construction of the three F1 hybrids, designated as Hybrid 1, Hybrid 2, and Hybrid 3, respectively. (B) Typical chromosomal constitutions of each of the three F1 hybrids, as revealed by multicolor GISH. The pink-, green-, and blue colored chromosomes represent the AA, CC, and the other genomes, respectively. The sphere-shaped clump is another intact nucleus in which though the chromosomes were not separated, their three coloration can also been seen. The photos from top to bottom are Hybrid1, Hybrid 2 and Hybrid 3, respectively. (C) Phenotypic characteristics of F1 hybrids and their parents; a, d, g are Hybrid 1, b, e, h are Hybrid 2, c, f, i are Hybrid 3. From left to right in Fig 1C were maternal Nipponbare, paternal wild rice and the corresponding F1 hybrids.
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pone.0132911.g001: Schematic diagrams for three F1 rice hybrids, their genome compositions and several representative phenotypic traits.(A) Diagrams showing the parents and process for the construction of the three F1 hybrids, designated as Hybrid 1, Hybrid 2, and Hybrid 3, respectively. (B) Typical chromosomal constitutions of each of the three F1 hybrids, as revealed by multicolor GISH. The pink-, green-, and blue colored chromosomes represent the AA, CC, and the other genomes, respectively. The sphere-shaped clump is another intact nucleus in which though the chromosomes were not separated, their three coloration can also been seen. The photos from top to bottom are Hybrid1, Hybrid 2 and Hybrid 3, respectively. (C) Phenotypic characteristics of F1 hybrids and their parents; a, d, g are Hybrid 1, b, e, h are Hybrid 2, c, f, i are Hybrid 3. From left to right in Fig 1C were maternal Nipponbare, paternal wild rice and the corresponding F1 hybrids.

Mentions: Three sets of triploid hybrids all with Oryza sativa ssp. japonica, cv. Nipponbare (genome AA, 2n = 2x = 24) as the maternal parent and three different wild tetraploid rice species as the paternal parents were produced. Specifically, (1) crossing Nipponbare with O. alta (genome CCDD, 2n = 4x = 48) to produce Hybrid 1 (genome ACD, 2n = 3x = 36); (2) crossing Nipponbare with O. punctata (genome BBCC, 2n = 4x = 48), to produce Hybrid 2 (genome ABC, 2n = 3x = 36); and (3) crossing Nipponbare with O. officinalis (genome CCC’C’, 2n = 4x = 48), to produce Hybrid 3 (genome ACC’, 2n = 3x = 36). Hybrid plants of all three crosses were obtained by embryo rescue (Fig 1A). Hybrid nature of these plants was validated by genomic in situ hybridization (GISH) and chromosome counting (Fig 1B). No change in either chromosome number or gross structure was detected, indicating the hybrids were karyotypically stable. The hybrids were completely male sterile and showed overall intermediate plant statue between the parental species. However, in several traits, such as tiller number, panicle shape, spikelet shape and fragility etc., the hybrids showed more resemblance to the wild tetraploid paternal species than to the maternal parent (Nipponbare) (Fig 1C), as expected given the 2:1 subgenome contributions to each hybrid by the two parental species for each triploid hybrid. All three hybrids are vigorous and can be maintained asexually by regeneration from nod-cuttings.


Immediate Genetic and Epigenetic Changes in F1 Hybrids Parented by Species with Divergent Genomes in the Rice Genus (Oryza).

Wu Y, Sun Y, Shen K, Sun S, Wang J, Jiang T, Cao S, Josiah SM, Pang J, Lin X, Liu B - PLoS ONE (2015)

Schematic diagrams for three F1 rice hybrids, their genome compositions and several representative phenotypic traits.(A) Diagrams showing the parents and process for the construction of the three F1 hybrids, designated as Hybrid 1, Hybrid 2, and Hybrid 3, respectively. (B) Typical chromosomal constitutions of each of the three F1 hybrids, as revealed by multicolor GISH. The pink-, green-, and blue colored chromosomes represent the AA, CC, and the other genomes, respectively. The sphere-shaped clump is another intact nucleus in which though the chromosomes were not separated, their three coloration can also been seen. The photos from top to bottom are Hybrid1, Hybrid 2 and Hybrid 3, respectively. (C) Phenotypic characteristics of F1 hybrids and their parents; a, d, g are Hybrid 1, b, e, h are Hybrid 2, c, f, i are Hybrid 3. From left to right in Fig 1C were maternal Nipponbare, paternal wild rice and the corresponding F1 hybrids.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4514751&req=5

pone.0132911.g001: Schematic diagrams for three F1 rice hybrids, their genome compositions and several representative phenotypic traits.(A) Diagrams showing the parents and process for the construction of the three F1 hybrids, designated as Hybrid 1, Hybrid 2, and Hybrid 3, respectively. (B) Typical chromosomal constitutions of each of the three F1 hybrids, as revealed by multicolor GISH. The pink-, green-, and blue colored chromosomes represent the AA, CC, and the other genomes, respectively. The sphere-shaped clump is another intact nucleus in which though the chromosomes were not separated, their three coloration can also been seen. The photos from top to bottom are Hybrid1, Hybrid 2 and Hybrid 3, respectively. (C) Phenotypic characteristics of F1 hybrids and their parents; a, d, g are Hybrid 1, b, e, h are Hybrid 2, c, f, i are Hybrid 3. From left to right in Fig 1C were maternal Nipponbare, paternal wild rice and the corresponding F1 hybrids.
Mentions: Three sets of triploid hybrids all with Oryza sativa ssp. japonica, cv. Nipponbare (genome AA, 2n = 2x = 24) as the maternal parent and three different wild tetraploid rice species as the paternal parents were produced. Specifically, (1) crossing Nipponbare with O. alta (genome CCDD, 2n = 4x = 48) to produce Hybrid 1 (genome ACD, 2n = 3x = 36); (2) crossing Nipponbare with O. punctata (genome BBCC, 2n = 4x = 48), to produce Hybrid 2 (genome ABC, 2n = 3x = 36); and (3) crossing Nipponbare with O. officinalis (genome CCC’C’, 2n = 4x = 48), to produce Hybrid 3 (genome ACC’, 2n = 3x = 36). Hybrid plants of all three crosses were obtained by embryo rescue (Fig 1A). Hybrid nature of these plants was validated by genomic in situ hybridization (GISH) and chromosome counting (Fig 1B). No change in either chromosome number or gross structure was detected, indicating the hybrids were karyotypically stable. The hybrids were completely male sterile and showed overall intermediate plant statue between the parental species. However, in several traits, such as tiller number, panicle shape, spikelet shape and fragility etc., the hybrids showed more resemblance to the wild tetraploid paternal species than to the maternal parent (Nipponbare) (Fig 1C), as expected given the 2:1 subgenome contributions to each hybrid by the two parental species for each triploid hybrid. All three hybrids are vigorous and can be maintained asexually by regeneration from nod-cuttings.

Bottom Line: Transcriptional and transpositional activity of several transposable elements (TEs) and methylation stability of their flanking regions were also assessed.Artificially constructed inter-specific hybrids of remotely related species with divergent genomes in genus Oryza are chromosomally stable but show immediate and highly stochastic genetic and epigenetic instabilities at the molecular level.These novel hybrids might provide a rich resource of genetic and epigenetic diversities for potential utilization in rice genetic improvements.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Molecular Epigenetics of MOE and Institute of Genetics and Cytology, Northeast Normal University, Changchun, China.

ABSTRACT

Background: Inter-specific hybridization occurs frequently in higher plants, and represents a driving force of evolution and speciation. Inter-specific hybridization often induces genetic and epigenetic instabilities in the resultant homoploid hybrids or allopolyploids, a phenomenon known as genome shock. Although genetic and epigenetic consequences of hybridizations between rice subspecies (e.g., japonica and indica) and closely related species sharing the same AA genome have been extensively investigated, those of inter-specific hybridizations between more remote species with different genomes in the rice genus, Oryza, remain largely unknown.

Methodology/principal findings: We investigated the immediate chromosomal and molecular genetic/epigenetic instability of three triploid F1 hybrids produced by inter-specific crossing between species with divergent genomes of Oryza by genomic in situ hybridization (GISH) and molecular marker analysis. Transcriptional and transpositional activity of several transposable elements (TEs) and methylation stability of their flanking regions were also assessed. We made the following principle findings: (i) all three triploid hybrids are stable in both chromosome number and gross structure; (ii) stochastic changes in both DNA sequence and methylation occurred in individual plants of all three triploid hybrids, but in general methylation changes occurred at lower frequencies than genetic changes; (iii) alteration in DNA methylation occurred to a greater extent in genomic loci flanking potentially active TEs than in randomly sampled loci; (iv) transcriptional activation of several TEs commonly occurred in all three hybrids but transpositional events were detected in a genetic context-dependent manner.

Conclusions/significance: Artificially constructed inter-specific hybrids of remotely related species with divergent genomes in genus Oryza are chromosomally stable but show immediate and highly stochastic genetic and epigenetic instabilities at the molecular level. These novel hybrids might provide a rich resource of genetic and epigenetic diversities for potential utilization in rice genetic improvements.

No MeSH data available.


Related in: MedlinePlus