Molecular characterization of a rice mutator-phenotype derived from an incompatible cross-pollination reveals transgenerational mobilization of multiple transposable elements and extensive epigenetic instability

Wang, Hongyan; Chai, Yimin; Chu, Xiucheng; Zhao, Yunyang; Wu, Ying; Zhao, Jihong; Ngezahayo, Frédéric; Xu, Chunming; B, Liu

doi:10.1186/1471-2229-9-63

Cited by 38 publications

(36 citation statements)

References 57 publications

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“…[36][37][38] For example, incompatible cross-pollination promotes the transgenerational mobilization of transposons that promote epigenetic instability. 39 This has led to the proposal that genetics drives epigenetics. 40 Although a genetic focus is predominant in the current concepts of biology, it will be an integration of epigenetics and genetics, with neither being dominant, that likely will provide a more accurate perspective on the molecular control of biological processes.…”

Section: Discussionmentioning

confidence: 99%

Environmentally induced epigenetic transgenerational inheritance of sperm epimutations promote genetic mutations

2015

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A variety of environmental factors have been shown to induce the epigenetic transgenerational inheritance of disease and phenotypic variation. This involves the germline transmission of epigenetic information between generations. Exposure specific transgenerational sperm epimutations have been previously observed. The current study was designed to investigate the potential role genetic mutations have in the process, using copy number variations (CNV). In the first (F1) generation following exposure, negligible CNV were identified; however, in the transgenerational F3 generation, a significant increase in CNV was observed in the sperm. The genome-wide locations of differential DNA methylation regions (epimutations) and genetic mutations (CNV) were investigated. Observations suggest the environmental induction of the epigenetic transgenerational inheritance of sperm epimutations promote genome instability, such that genetic CNV mutations are acquired in later generations. A combination of epigenetics and genetics is suggested to be involved in the transgenerational phenotypes. The ability of environmental factors to promote epigenetic inheritance that subsequently promotes genetic mutations is a significant advance in our understanding of how the environment impacts disease and evolution.

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Section: Discussionmentioning

confidence: 99%

Environmentally induced epigenetic transgenerational inheritance of sperm epimutations promote genetic mutations

2015

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“…Our previous studies have identified transpositional activation or mobilization of several TEs in the rice- Zizania introgression lines including RZ35 [30,33,34]. To further investigate if mobilization of additional TEs or mobilization sites of previously identified TEs in the RZ35 genome, we applied a PEM detection strategy (Figure S1) as employed previously by Sabot et al [42].…”

Section: Methodsmentioning

confidence: 99%

“…Apart from bona fide hybridization, the germinating alien pollens may constitute a "biological stress" to the recipient stigma genome due to its mechanistic resemblance to pathogen attack wherein the foreign DNA usually does not integrate into the host genome, yet its interaction with the host could provoke genetic and epigenetic instabilities of the host genome [27-30]. Therefore, in contrast to the hybridization and polyploidy, alien pollen-induced variations may represent an underlying mechanism that can also contribute to plant genome evolution.…”

Section: Introductionmentioning

confidence: 99%

“…japonica cv. Matsumae genome by the aforementioned method, these introgressants not only showed extensive de novo genetic changes but also exhibited morphological and physiological novelties [30-36]. These studies have provided compelling albeit circumstantial evidence showing that alien pollens can indeed provoke genetic and epigenetic instabilities of a recipient plant genome.…”

Section: Introductionmentioning

confidence: 99%

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Genomewide Variation in an Introgression Line of Rice-Zizania Revealed by Whole-Genome re-Sequencing

et al. 2013

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BackgroundHybridization between genetically diverged organisms is known as an important avenue that drives plant genome evolution. The possible outcomes of hybridization would be the occurrences of genetic instabilities in the resultant hybrids. It remained under-investigated however whether pollination by alien pollens of a closely related but sexually "incompatible" species could evoke genomic changes and to what extent it may result in phenotypic novelties in the derived progenies.Methodology/Principal FindingsIn this study, we have re-sequenced the genomes of Oryza sativa ssp. japonica cv. Matsumae and one of its derived introgressant RZ35 that was obtained from an introgressive hybridization between Matsumae and Zizania latifolia Griseb. in general, 131 millions 90 base pair (bp) paired-end reads were generated which covered 13.2 and 21.9 folds of the Matsumae and RZ35 genomes, respectively. Relative to Matsumae, a total of 41,724 homozygous single nucleotide polymorphisms (SNPs) and 17,839 homozygous insertions/deletions (indels) were identified in RZ35, of which 3,797 SNPs were nonsynonymous mutations. Furthermore, rampant mobilization of transposable elements (TEs) was found in the RZ35 genome. The results of pathogen inoculation revealed that RZ35 exhibited enhanced resistance to blast relative to Matsumae. Notably, one nonsynonymous mutation was found in the known blast resistance gene Pid3/Pi25 and real-time quantitative (q) RT-PCR analysis revealed constitutive up-regulation of its expression, suggesting both altered function and expression of Pid3/Pi25 may be responsible for the enhanced resistance to rice blast by RZ35.Conclusions/SignificanceOur results demonstrate that introgressive hybridization by Zizania has provoked genomewide, extensive genomic changes in the rice genome, and some of which have resulted in important phenotypic novelties. These findings suggest that introgressive hybridization by alien pollens of even a sexually incompatible species may represent a potent means to generate novel genetic diversities, and which may have played relevant roles in plant evolution and can be manipulated for crop improvements.

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“…Actually, some mutator-phenotype might derive from an incompatible cross-pollination and selfing instead of compatibility. It was reported that transgenerational epigenetic instability in the form of altered cytosine methylation and its associated TE activity occurred in a rice mutator-phenotype produced by pollinating the rice stigma with pollen grains of Oenothera biennis (Wang et al 2009). Whether the hybrids contain genomeic material of the paternal hybrid or not, need to be analyzed by genomic in situ hybridization (GISH).…”

Section: Discussionmentioning

confidence: 99%

Possible intergeneric hybridization between Cancrinia maximowiczii C. Winkl. and Chrysanthemum naktongense (Nakai) Tzvel. × C. ×morifolium Ramat. ‘Aifen’

XiaoBo

Liu

et al. 2014

Genet Resour Crop Evol

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Two possible intergeneric putative hybrids between Cancrinia maximowiczii and an interspecific hybrid (Chrysanthemum naktongense 9 Chrysanthemum 9morifolium 'Aifen') were produced without emasculation. The putative hybrids could be identified by ITS sequences and morphological characteristics. The distinct trait of the putative hybrids presented itself by 7-13 white tubular florets bursting out in the outer capitula. Results of flow cytometry analysis and chromosome counting did not support the nature of the putative hybrids. It was found that the ploidy levels of the putative hybrids and parents are diploid, hexaploid and diploid respectively. Whether the paternal parent is a donor of the genome or not, need to be analyzed further by GISH. We propose that C. maximowiczii may be transferred to the subtribe Artemisiinae based on ITS phylogenetic analysis, although the position of the species and the genus Cancrinia could not be confirmed here.

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Molecular characterization of a rice mutator-phenotype derived from an incompatible cross-pollination reveals transgenerational mobilization of multiple transposable elements and extensive epigenetic instability

Cited by 38 publications

References 57 publications

Environmentally induced epigenetic transgenerational inheritance of sperm epimutations promote genetic mutations

Environmentally induced epigenetic transgenerational inheritance of sperm epimutations promote genetic mutations

Genomewide Variation in an Introgression Line of Rice-Zizania Revealed by Whole-Genome re-Sequencing

Possible intergeneric hybridization between Cancrinia maximowiczii C. Winkl. and Chrysanthemum naktongense (Nakai) Tzvel. × C. ×morifolium Ramat. ‘Aifen’

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