Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs

Shivaprasad, P. V.; Dunn, Ruth M.; Santos, Bruno; Bassett, Andrew; Baulcombe, David C.

doi:10.1038/emboj.2011.458

Cited by 192 publications

(162 citation statements)

References 71 publications

Supporting

Mentioning

148

Contrasting

Unclassified

Order By: Relevance

“…Similarly, DNA methylation interactions in rice F1 hybrids were shown to be strongly associated with regions where siRNA production is unequal in the two parents (11). An association between changes in DNA methylation levels and transgressive siRNAs has also been observed in tomato hybrids (19). These observations…”

supporting

confidence: 52%

Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation

Zhang

Wang

Lang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

110

View full text Add to dashboard Cite

DNA methylation is a conserved epigenetic mark in plants and many animals. How parental alleles interact in progeny to influence the epigenome is poorly understood. We analyzed the DNA methylomes of Arabidopsis Col and C24 ecotypes, and their hybrid progeny. Hybrids displayed nonadditive DNA methylation levels, termed methylation interactions, throughout the genome. Approximately 2,500 methylation interactions occurred at regions where parental DNA methylation levels are similar, whereas almost 1,000 were at differentially methylated regions in parents. Methylation interactions were characterized by an abundance of 24-nt small interfering RNAs. Furthermore, dysfunction of the RNA-directed DNA methylation pathway abolished methylation interactions but did not affect the increased biomass observed in hybrid progeny. Methylation interactions correlated with altered genetic variation within the genome, suggesting that they may play a role in genome evolution.D NA methylation is a conserved epigenetic mark in many eukaryotes (1-6). In plants and mammals, DNA methylation plays important roles in genome stability, genomic imprinting, paramutation, and gene regulation during development and diseases (1-6). Parental genetic alleles interact in the filial 1 (F1) progeny in a Mendelian manner. DNA methylation may affect this interaction such that methylated epialleles may show nonadditive interactions. This notion is supported by recent observations that hybridization results in nonadditive changes in the F1 plant DNA methylome (7,8). It has been proposed that genome-wide interactions between parental epialleles in F1 hybrids are critical for hybrid vigor, the superior performance of hybrids compared with their parents (8-13). Epigenome interactions may confer nonadditive transcriptional and epigenetic activities in hybrid offspring compared with the parental lines. In contrast to additive regulation, which leads to midparent value (MPV) levels equal to the average of the two parental lines, nonadditive regulation results in a deviation from the MPV, such that the F1 hybrid resembles the high-or low-expression parent. In addition, nonadditive regulation can be transgressive, which is beyond the range of the parental levels (14).Studies in rice and Arabidopsis have identified nonadditive changes in DNA methylation levels at loci where parental methylation levels are different [differentially methylated regions (DMRs)] (7,8,11,12,15,16). These "methylation interactions" were attributed to two mechanisms, transchromosomal methylation (TCM) and transchromosomal demethylation (TCdM), whereby the methylation level of one parental allele is altered to resemble the methylation level of the other parental allele (7,8,17). At some genomic loci, the transmethylation events in F1 were shown to be inherited to the next generation, as observed for paramutation (17). Nonetheless, a thorough profile of DNA methylation interactions across the whole Arabidopsis genome has yet to be determined. In particular, it remains unclear whether DNA m...

show abstract

supporting

confidence: 52%

Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation

Zhang

Wang

Lang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

110

View full text Add to dashboard Cite

show abstract

“…We speculate that there could be a direct or indirect epistatic interaction between the nonoverlapping IL 2-4 region and PME2.5. However, there are many factors that could be involved after the hybridization of genomes, including regulatory divergence and the epigenetic state of the loci of interest (Udall and Wendel, 2006;Shivaprasad et al, 2012), and these factors may also account for the transgressive firmness phenotypes observed in this study. For example, the prominent firm F2 line 301 was consistently firmer than the parental line IL 2-3.…”

Section: Discussionmentioning

confidence: 90%

High-Resolution Mapping of a Fruit Firmness-Related Quantitative Trait Locus in Tomato Reveals Epistatic Interactions Associated with a Complex Combinatorial Locus

Chapman

Bonnet²,

Grivet³

et al. 2012

Plant Physiology

View full text Add to dashboard Cite

Fruit firmness in tomato (Solanum lycopersicum) is determined by a number of factors including cell wall structure, turgor, and cuticle properties. Firmness is a complex polygenic trait involving the coregulation of many genes and has proved especially challenging to unravel. In this study, a quantitative trait locus (QTL) for fruit firmness was mapped to tomato chromosome 2 using the Zamir Solanum pennellii interspecific introgression lines (ILs) and fine-mapped in a population consisting of 7,500 F2 and F3 lines from IL 2-3 and IL 2-4. This firmness QTL contained five distinct subpeaks, Fir s.p. QTL2.1 to Fir s.p. QTL2.5, and an effect on a distal region of IL 2-4 that was nonoverlapping with IL 2-3. All these effects were located within an 8.6-Mb region. Using genetic markers, each subpeak within this combinatorial locus was mapped to a physical location within the genome, and an ethylene response factor (ERF) underlying Fir s.p. QTL2.2 and a region containing three pectin methylesterase (PME) genes underlying Fir s.p. QTL2.5 were nominated as QTL candidate genes. Statistical models used to explain the observed variability between lines indicated that these candidates and the nonoverlapping portion of IL 2-4 were sufficient to account for the majority of the fruit firmness effects. Quantitative reverse transcription-polymerase chain reaction was used to quantify the expression of each candidate gene. ERF showed increased expression associated with soft fruit texture in the mapping population. In contrast, PME expression was tightly linked with firm fruit texture. Analysis of a range of recombinant lines revealed evidence for an epistatic interaction that was associated with this combinatorial locus.

show abstract

“…The enrichment for nonparental expression in trans to the introgression provides evidence of the existence of epistatically interacting mutations within each lineage that, when combined, result in unique expression phenotypes. An additional possible contributing factor is the recent discovery of transgressive siRNA expression patterns in tomato hybrids (44). These results point to introgression as a possible source of unique expression phenotypes in cultivated tomato.…”

Section: Effect Of Introgression On the Transcriptome Of Domesticatedmentioning

confidence: 97%

Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato

Koenig

Jiménez‐Gómez²,

Kimura

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

325

268

View full text Add to dashboard Cite

Although applied over extremely short timescales, artificial selection has dramatically altered the form, physiology, and life history of cultivated plants. We have used RNAseq to define both gene sequence and expression divergence between cultivated tomato and five related wild species. Based on sequence differences, we detect footprints of positive selection in over 50 genes. We also document thousands of shifts in gene-expression level, many of which resulted from changes in selection pressure. These rapidly evolving genes are commonly associated with environmental response and stress tolerance. The importance of environmental inputs during evolution of gene expression is further highlighted by large-scale alteration of the light response coexpression network between wild and cultivated accessions. Human manipulation of the genome has heavily impacted the tomato transcriptome through directed admixture and by indirectly favoring nonsynonymous over synonymous substitutions. Taken together, our results shed light on the pervasive effects artificial and natural selection have had on the transcriptomes of tomato and its wild relatives.domestication | biotic stress | abiotic stress D omestication has long served as an important example of severe phenotypic divergence in response to selection. Darwin recognized the parallel between the processes of domestication and adaptation in the wild and used this analogy to emphasize the power of selection in generating phenotypic diversity (1). The genetic basis of domestication-associated phenotypes has been examined in several instances, most notably in maize, rice, tomato, and dogs (reviewed in refs. 2-5). The clear conclusion from these studies is that the rapid phenotypic divergence associated with domestication is often attributable to very few genetic loci (6). Improvements to DNA sequence technologies have allowed studies of the effect of domestication at the whole-genome level. Early population genetic analyses in maize found that very few genes (∼5%) show evidence of positive selection during domestication of maize (7), and recent work using whole-genome resequencing has found a similar proportion of the genome was under positive selection (8). Evidence for strong selective sweeps at a limited number of loci has also been found in rice and dog genomes (9). Together with the previous genetic mapping work, these studies support the model that relatively few mutations experienced extremely strong selection by humans during domestication.Although not the target of direct positive selection, the rest of the genome still experiences a dramatic shift in evolutionary pressures during domestication. Most characterized domestication events are associated with an extreme genetic bottleneck and alleviation of selective constraints in the original niche (10). These factors are predicted to increase the relative rate of nonsynonymous to synonymous (dN/dS) substitution, potentially resulting in the fixation of deleterious alleles (11). Previous studies comparing the distribution ...

show abstract

Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs

Cited by 192 publications

References 71 publications

Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation

Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation

High-Resolution Mapping of a Fruit Firmness-Related Quantitative Trait Locus in Tomato Reveals Epistatic Interactions Associated with a Complex Combinatorial Locus

Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato

Contact Info

Product

Resources

About