Perturbation of Parentally Biased Gene Expression during Interspecific Hybridization

Burkart‐Waco, Diana; Ngo, Kathie J.; Lieberman, Meric; Comai, Luca

doi:10.1371/journal.pone.0117293

Cited by 30 publications

(41 citation statements)

References 49 publications

(88 reference statements)

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“…We created an inventory of published IGs identified in A. thaliana ( At ; Köhler et al ., ; Spillane et al ., ; Gehring et al ., ; Hsieh et al ., ; McKeown et al ., ; Wolff et al ., ; Bratzel et al ., ; Pignatta et al ., ; Burkart‐Waco et al ., ; Jeong et al ., ), A. lyrata ( Al ; Klosinska et al ., ), C. rubella ( Cr ; Hatorangan et al ., ), rice ( Os ; Luo et al ., ; Yuan et al ., ), maize ( Zm ; Gutiérrez‐Marcos et al ., ; Zhang et al ., , ; Waters et al ., ; Xin et al ., ), S. bicolor ( Sb ; Zhang et al ., ) and castor bean ( Rc ; Xu et al ., ). Sequences were retrieved from public databases: At , The Arabidopsis Information Resource (TAIR; Swarbreck et al ., ) at http://www.arabidopsis.org; Al and Cr , Phytozome v11.0 (Goodstein et al ., ) at https://phytozome.jgi.doe.gov; maize, MaizeGDB (Lawrence, ) at http://www.maizegdb.org; rice and Sb , PlantGDB (Duvick et al ., ) at http://www.plantgdb.org; and Rc , Castor Bean Genome Project (Chan et al ., ) at http://castorbean.jcvi.org.…”

Section: Methodsmentioning

confidence: 99%

Wild tomato endosperm transcriptomes reveal common roles of genomic imprinting in both nuclear and cellular endosperm

et al. 2018

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Genomic imprinting is a conspicuous feature of the endosperm, a triploid tissue nurturing the embryo and synchronizing angiosperm seed development. An unknown subset of imprinted genes (IGs) is critical for successful seed development and should have highly conserved functions. Recent genome-wide studies have found limited conservation of IGs among distantly related species, but there is a paucity of data from closely related lineages. Moreover, most studies focused on model plants with nuclear endosperm development, and comparisons with properties of IGs in cellular-type endosperm development are lacking. Using laser-assisted microdissection, we characterized parent-specific expression in the cellular endosperm of three wild tomato lineages (Solanum section Lycopersicon). We identified 1025 candidate IGs and 167 with putative homologs previously identified as imprinted in distantly related taxa with nuclear-type endosperm. Forty-two maternally expressed genes (MEGs) and 17 paternally expressed genes (PEGs) exhibited conserved imprinting status across all three lineages, but differences in power to assess imprinted expression imply that the actual degree of conservation might be higher than that directly estimated (20.7% for PEGs and 10.4% for MEGs). Regardless, the level of shared imprinting status was higher for PEGs than for MEGs, indicating dissimilar evolutionary trajectories. Expression-level data suggest distinct epigenetic modulation of MEGs and PEGs, and gene ontology analyses revealed MEGs and PEGs to be enriched for different functions. Importantly, our data provide evidence that MEGs and PEGs interact in modulating both gene expression and the endosperm cell cycle, and uncovered conserved cellular functions of IGs uniting taxa with cellular- and nuclear-type endosperm.

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Section: Methodsmentioning

confidence: 99%

Wild tomato endosperm transcriptomes reveal common roles of genomic imprinting in both nuclear and cellular endosperm

et al. 2018

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“…There is growing evidence for a role for imprinted genes in hybrid inviability in both mammals and seed plants (e.g., Brekke & Good, ; Brekke, Henry, & Good, ; Burkart‐Waco, Ngo, Lieberman, & Comai, ; Florez‐Rueda et al., ; Garner, Kenney, Fishman, & Sweigart, ; Josefsson, Dilkes, & Comai, ; Loschiavo, Nguyen, Duselis, & Vrana, ; Vrana et al., ), and dysregulation of imprinted genes caused by trans effects has been suggested as a possible source of this incompatibility (Wolf, Oakey, & Feil, ). Intriguingly for the X‐autosome conflict hypothesis, Vrana et al.…”

Section: Other Selfish Aspects Of X Chromosomes and How They Might Comentioning

confidence: 99%

Selfish X chromosomes and speciation

Patten

2018

Molecular Ecology

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In two papers published at about the same time almost thirty years ago, Frank (Evolution, 45, 1991a, 262) and Hurst and Pomiankowski (Genetics, 128, 1991, 841) independently suggested that divergence of meiotic drive systems-comprising genes that cheat meiosis and genes that suppress this cheating-might provide a general explanation for Haldane's rule and the large X-effect in interspecific hybrids. Although at the time, the idea was met with skepticism and a conspicuous absence of empirical support, the tide has since turned. Some of the clearest mechanistic explanations we have for hybrid male sterility involve meiotic drive systems, and several other cases of hybrid sterility are suggestive of a role for meiotic drive. In this article, I review these ideas and their descendants and catalog the current evidence for the meiotic drive model of speciation. In addition, I suggest that meiotic drive is not the only intragenomic conflict to involve the X chromosome and contribute to hybrid incompatibility. Sexually and parentally antagonistic selection pressures can also pit the X chromosome and autosomes against each other. The resulting intragenomic conflicts should lead to co-evolution within populations and divergence between them, thus increasing the likelihood of incompatibilities in hybrids. I provide a sketch of these ideas and interpret some empirical patterns in the light of these additional X-autosome conflicts.

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“…Supporting this view, imprinted genes are deregulated in interspecific hybrid endosperm resulting from Arabidopsis thaliana and Arabidopsis arenosa hybridization (Burkart‐Waco et al . , ; Kirkbride et al . ).…”

Section: Interploidy and Interspecific Hybridization Barriers May Shamentioning

confidence: 99%

“…Interestingly, interspecific hybridization of A. thaliana and A. arenosa parents particularly affects PEG regulation and causes activation of the maternal alleles of PEGs (Burkart‐Waco et al . ; Kirkbride et al . ), suggesting deregulated PEGs generate interspecific hybridization barriers.…”

Section: Interploidy and Interspecific Hybridization Barriers May Shamentioning

confidence: 99%

Endosperm‐based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers

2016

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The endosperm is a nourishing tissue that serves to support embryo growth. Failure of endosperm development will ultimately cause embryo arrest and seed lethality, a phenomenon that is frequently observed upon hybridization of related plant species or species that differ in ploidy. Endosperm-based interspecies or interploidy hybridization barriers depend on the direction of the hybridization, causing nonreciprocal seed defects. This reveals that the parental genomes are not equivalent, implicating parent-of-origin specific genes generating this type of hybridization barrier. Recent work revealed that endosperm-based hybridization barriers are rapidly evolving. In this review, we discuss the developmental mechanisms causing hybrid seed lethality in angiosperms as well as the evolutionary forces establishing endosperm-based postzygotic hybridization barriers.

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Perturbation of Parentally Biased Gene Expression during Interspecific Hybridization

Cited by 30 publications

References 49 publications

Wild tomato endosperm transcriptomes reveal common roles of genomic imprinting in both nuclear and cellular endosperm

Wild tomato endosperm transcriptomes reveal common roles of genomic imprinting in both nuclear and cellular endosperm

Selfish X chromosomes and speciation

Endosperm‐based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers

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