Inheritance of Trans Chromosomal Methylation patterns from Arabidopsis F1 hybrids

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F1 hybrids can outperform their parents in yield and vegetative biomass, features of hybrid vigor that form the basis of the hybrid seed industry. The yield advantage of the F1 is lost in the F2 and subsequent generations. In Arabidopsis, from F2 plants that have a F1-like phenotype, we have by recurrent selection produced pure breeding F5/F6 lines, hybrid mimics, in which the characteristics of the F1 hybrid are stabilized. These hybrid mimic lines, like the F1 hybrid, have larger leaves than the parent plant, and the leaves have increased photosynthetic cell numbers, and in some lines, increased size of cells, suggesting an increased supply of photosynthate. A comparison of the differentially expressed genes in the F1 hybrid with those of eight hybrid mimic lines identified metabolic pathways altered in both; these pathways include down-regulation of defense response pathways and altered abiotic response pathways. F6 hybrid mimic lines are mostly homozygous at each locus in the genome and yet retain the large F1-like phenotype. Many alleles in the F6 plants, when they are homozygous, have expression levels different to the level in the parent. We consider this altered expression to be a consequence of transregulation of genes from one parent by genes from the other parent. Transregulation could also arise from epigenetic modifications in the F1. The pure breeding hybrid mimics have been valuable in probing the mechanisms of hybrid vigor and may also prove to be useful hybrid vigor equivalents in agriculture.I n Arabidopsis some ecotypes with similar genome sequences produce F1 hybrids with large increases in vegetative and reproductive yields (1, 2). These results appear to be at variance with the generalization that the larger the genetic distance between parents, the greater the hybrid vigor (3); however, the Arabidopsis ecotypes have different epigenomes that may be important for hybrid vigor (4). In hybrids between C24 and Ler, we found altered levels in two epigenetic systems: 24nt siRNAs and DNA methylation (4, 5). These epigenetic changes appear common among hybrid systems with similar observations being made in maize and rice hybrids (6). The epigenetic changes can correlate with changes in gene expression and contribute to the unique gene expression profile of the F1 hybrid (7). Not all crosses result in hybrid vigor (heterosis); some result in decreased vigor and yield referred to as "hybrid weakness" (8).Heterotic F1 hybrids are featured in agricultural and horticultural crops, and in all species, the yield gains are restricted to the F1 generation. The F2 and subsequent selfed generations are discarded because of reduced yields and heterogeneity of morphological and developmental traits. A hybrid crop system requires an efficient method of F1 hybrid seed production dependent on male sterility in the female parent and synchronous flowering of the male and female parents.QTL analysis in maize and rice has confirmed that hundreds of genome segments contribute to the heterotic phenotype, but the main m...

mentioning

confidence: 63%

Section: Genes and Metabolic Pathways Important In The F1 Hybrid Phenmentioning

confidence: 99%

Hybrid mimics and hybrid vigor in Arabidopsis

Wang

Greaves

Groszmann

et al. 2015

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“…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.…”

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confidence: 99%

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

Zhang

Wang

Lang

et al. 2016

110

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...

“…The TCM and TCdM events do not always occur in the early cell divisions of the developing embryo (9). A TCM event overlapping At3g43340 and At3g43350 results in a decrease in expression of both genes and is stably maintained through successive generations where it continues to correlate with altered levels of gene expression (9,10).…”

mentioning

confidence: 99%

“…A TCM event overlapping At3g43340 and At3g43350 results in a decrease in expression of both genes and is stably maintained through successive generations where it continues to correlate with altered levels of gene expression (9,10). The TCM characteristics defined at At3g43340/50 may not be representative of how all TCM events are established in the C24/ Ler F1 hybrid system.…”

mentioning

confidence: 99%

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

Greaves

Eichten

Groszmann

et al. 2016

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Hybrid Arabidopsis plants undergo epigenetic reprogramming producing decreased levels of 24-nt siRNAs and altered patterns of DNA methylation that can affect gene expression. Driving the changes in methylation are the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM). In TCM/TCdM the methylation state of one allele is altered to resemble the other allele. We show that Pol IV-dependent sRNAs are required to establish TCM events. The changes in DNA methylation and the associated changes in sRNA levels in the F1 hybrid can be maintained in subsequent generations and affect hundreds of regions in the F2 epigenome. The inheritance of these altered epigenetic states varies in F2 individuals, resulting in individuals with genetically identical loci displaying different epigenetic states and gene expression profiles. The change in methylation at these regions is associated with the presence of sRNAs. Loci without any sRNA activity can have altered methylation states, suggesting that a sRNA-independent mechanism may also contribute to the altered methylation state of the F1 and F2 generations.H ybrid vigor, heterosis, is important in agriculture due to the increased performance of hybrid plants over parental lines. The increase in performance is attributable to changes in gene expression (1, 2) but how these changes result in the increased performance of the hybrid is still not known. The level of hybrid vigor is believed to correlate with the genetic distance between parental lines; however, hybrid vigor can occur in progeny derived from crosses of genetically similar parents. An example is found in intraspecific crosses between Arabidopsis thaliana accessions. In crosses between C24 and Landsberg erecta (Ler), up to a 100% increase in plant biomass and seed yield is observed (3). The different epigenomes of the two parental accessions could provide the diversity required to initiate gene expression changes and vigor-related characteristics. A number of laboratories have investigated whether there are epigenetic changes in Arabidopsis hybrids, whether they affect gene expression, and whether they contribute to the hybrid vigor phenotype (1, 3-6).We have previously established that F1 hybrids between Arabidopsis accessions undergo some epigenetic reprogramming. We found that the abundance of 24-nt siRNAs is reduced in F1 hybrids and that a second epigenetic system, DNA methylation ( m C), is also altered in the hybrid genome (1, 3, 5). The altered m C patterns in the hybrids involve the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM), where the m C state of one parental allele is altered to resemble the other allele (reviewed in ref. 7). Due to the presence of siRNAs at regions that undergo TCM/TCdM, we have suggested that siRNAs are the initiating molecules that establish these TCM/TCdM events (reviewed in ref. 8). In the hybrid nucleus, the complement of 24-nt siRNAs can interact with homologous sequences from either parent.The TCM and TCdM...