Figure - uploaded by Nathan Springer
Content may be subject to copyright.
Figure S5 Association between DMR inheritance patterns and DMR types (A) or different genomic features (B). (A) Percentage of DMRs with different methylation contexts for each DMR inheritance pattern. We classified DMRs with Whole-Genome Bisulfite Sequencing data into 5 context categories: CG, CHG, CHH, CGCHG and CGCHGCHH based on the methylation difference between B73 and Mo17. For CG and CHG, we used a cutoff of 20% difference; and for CHH, we used a cutoff of 5% difference. DMRs that have methylation difference greater than the cutoff of the respective sequence context (i.e., CG, CHG, and CHH) are defined as DMRs of that sequence context. For example, CG-DMRs showed more than 20% methylation difference in CG, less than 20% in CHG and less than 5% in CHH. (B) Percentage of DMRs overlapping different genomic features for each DMR inheritance pattern. The DMR position was compared with the gene annotation (version: 5b) or transposable element (TE) annotation (version: 5a_MTEC). DMRs that don't overlap any of these annotated features were classified into the "none" group.
Source publication
DNA methylation is a chromatin modification that contributes to epigenetic regulation of gene expression. The inheritance patterns and trans-generational stability of 962 differentially methylated regions (DMRs) were assessed in a panel of 71 near-isogenic lines (NILs) derived from maize (Zea mays) inbred lines B73 and Mo17. The majority of DMRs ex...
Similar publications
Histone modifications regulate key processes of eukaryotic genomes. Misregulation of the enzymes that place these modifications can lead to disease. An example of this is DOT1L, the enzyme that can mono-, di-, and trimethylate the nucleosome core on lysine 79 of histone H3 (H3K79). DOT1L plays a role in development and its misregulation has been im...
Base editing events in eukaryote require a compatible chromatin environment, but there is little research on how chromatin factors contribute to the editing efficiency or window. By engineering BEs (base editors) fused with various pioneer factors, the authors found that SOX2 substantially increased the editing efficiency for GBE and CBE. While Sox...
The detailed principles of the hierarchical folding of eukaryotic chromosomes have been revealed during the last two decades. Along with structures composing three-dimensional (3D) genome organization (chromatin compartments, topologically associating domains, chromatin loops, etc.), the molecular mechanisms that are involved in their establishment...
Data-driven machine learning is the method of choice for predicting molecular phenotypes from nucleotide sequence, modeling gene expression events including protein-DNA binding, chromatin states as well as mRNA and protein levels. Deep neural networks automatically learn informative sequence representations and interpreting them enables us to impro...
Genes are not randomly distributed on eukaryotic chromosomes. Some neighboring genes show order conservation among species, while some neighboring genes separate during evolution even though their neighborhoods are conserved in some species. Here, I investigated whether after-separation gene repositioning is under natural selection for evolutionary...
Citations
... Several studies have used epiRILs to study the role of epigenetic modifications in gene expression and phenotypic variation [117][118][119][120][121][122][123]. For example, Zhang et al. [124] used epiRILs to study the role of DNA methylation in gene expression and drought tolerance in Arabidopsis thaliana. ...
Mendelian heredity is the cornerstone of plant breeding and has been used to develop new varieties of plants since the 19th century. However, there are several breeding cases, such as cytoplasmic inheritance, methylation, epigenetics, hybrid vigour, and loss of heterozygosity (LOH), where Mendelian heredity is not applicable, known as non-Mendelian heredity. This type of inheritance can be influenced by several factors besides the genetic architecture of the plant and its breeding potential. Therefore, exploring various non-Mendelian heredity mechanisms, their prevalence in plants, and the implications for plant breeding is of paramount importance to accelerate the pace of crop improvement. In this review, we examine the current understanding of non-Mendelian heredity in plants, including the mechanisms, inheritance patterns, and applications in plant breeding, provide an overview of the various forms of non-Mendelian inheritance (including epigenetic inheritance, cytoplasmic inheritance, hybrid vigour, and LOH), explore insight into the implications of non-Mendelian heredity in plant breeding, and the potential it holds for future research.
... Genetic inheritance is the phenomenon in which an individual's underlying DNA sequence affects epigenetic state. 86 The inheritance of DNA methylation can be intergenerational and transgenerational. Intergenerational transmission refers to the transfer of epigenetic marks from one generation to the next whereas the passage of information from grandparents to a grandchild is defined as transgenerational. ...
Epigenetics is the field of science that deals with the study of changes in gene function that do not involve changes in DNA sequence and are heritable while epigenetics inheritance is the process of transmission of epigenetic modifications to the next generation. It can be transient, intergenerational, or transgenerational. There are various epigenetic modifications involving mechanisms such as DNA methylation, histone modification, and noncoding RNA expression, all of which are inheritable. In this chapter, we summarize the information on epigenetic inheritance, its mechanism, inheritance studies on various organisms, factors affecting epigenetic modifications and their inheritance, and the role of epigenetic inheritance in the heritability of diseases.
... There are dramatic differences in DNA methylation levels among species. In maize, the average level of cytosine methylation is ~90% at CG sites, ~70% at CHG sites, and ~3% at CHH sites (60). In comparison, genome-wide DNA methylation levels in Arabidopsis at CG, CHG, and CHH sites are 24%, 6.7%, and 1.7%, respectively (56). ...
Plant breeding relies on crossing-over to create novel combinations of alleles needed to confer increased productivity and other desired traits in new varieties. However, crossover (CO) events are rare, as usually only one or two of them occur per chromosome in each generation. In addition, COs are not distributed evenly along chromosomes. In plants with large genomes, which includes most crops, COs are predominantly formed close to chromosome ends, and there are few COs in the large chromosome swaths around centromeres. This situation has created interest in engineering CO landscape to improve breeding efficiency. Methods have been developed to boost COs globally by altering expression of anti-recombination genes and increase CO rates in certain chromosome parts by changing DNA methylation patterns. In addition, progress is being made to devise methods to target COs to specific chromosome sites. We review these approaches and examine using simulations whether they indeed have the capacity to improve efficiency of breeding programs. We found that the current methods to alter CO landscape can produce enough benefits for breeding programs to be attractive. They can increase genetic gain in recurrent selection and significantly decrease linkage drag around donor loci in schemes to introgress a trait from unimproved germplasm to an elite line. Methods to target COs to specific genome sites were also found to provide advantage when introgressing a chromosome segment harboring a desirable quantitative trait loci. We recommend avenues for future research to facilitate implementation of these methods in breeding programs.
... In model plant organisms, quantitative genetic studies also indicate that many variations in methylation of DNA between individuals are correlated with underlying differences in genetics. For instance, most differentially methylated regions (DMRs) were segregated stably in maize with the local allele DNA sequence (Li et al., 2014). In comparison, among 142 natural A. thaliana accessions, DMRs of only 35% were associated with polymorphisms of DNA sequence (Schmitz et al., 2013). ...
... In crop species, different results have been reported even for the same species. For instance, generally stable inheritance with rare examples of unexpected patterns has been shown in recombinant inbred populations of maize (Eichten et al. 2013;Li et al. 2014). Still, non-Mendelian epi-inheritance was reported in maize (Zhao et al. 2008), rice (Peng et al. 2013) and soybean (Schmitz et al. 2013). ...
Crop wild relatives (CWRs) are recognized as the best potential source of traits for crop improvement. However, successful crop improvement using CWR relies on identifying variation in genes controlling desired traits in plant germplasms and subsequently incorporating them into cultivars. Epigenetic diversity may provide an additional layer of variation within CWR and can contribute novel epialleles for key traits for crop improvement. There is emerging evidence that epigenetic variants of functional and/or agronomic importance exist in CWR gene pools. This provides a rationale for the conservation of epigenotypes of interest, thus contributing to agrobiodiversity preservation through conservation and (epi)genetic monitoring. Concepts and techniques of classical and modern breeding should consider integrating recent progress in epigenetics, initially by identifying their association with phenotypic variations and then by assessing their heritability and stability in subsequent generations. New tools available for epigenomic analysis offer the opportunity to capture epigenetic variation and integrate it into advanced (epi)breeding programmes. Advances in -omics have provided new insights into the sources and inheritance of epigenetic variation and enabled the efficient introduction of epi-traits from CWR into crops using epigenetic molecular markers, such as epiQTLs.
... In maize recombination inbred lines (RILs), DNA methylation variation in one eighthgeneration RIL switched from non-donor to the donor, which were guided by siRNAs [31]. However, in maize near isogenic lines, DNA methylation variation may correlate with cis-regulatory elements [63], independent of siRNAs. This is probably because the study using DNA methylC immunoprecipitation with microarray profiling may not effectively capture CHH methylation variation among these lines that are derived from three rounds of backcross. ...
Background
Hybridization and backcrossing are commonly used in animal and plant breeding to induce heritable variation including epigenetic changes such as paramutation. However, the molecular basis for hybrid-induced epigenetic memory remains elusive.
Results
Here, we report that hybridization between the inbred parents B73 and Mo17 induces trans-acting hypermethylation and hypomethylation at thousands of loci; several hundreds (~ 3%) are transmitted through six backcrossing and three selfing generations. Notably, many transgenerational methylation patterns resemble epialleles of the nonrecurrent parent, despite > 99% of overall genomic loci are converted to the recurrent parent. These epialleles depend on 24-nt siRNAs, which are eliminated in the isogenic hybrid Mo17xB73:mop1-1 that is defective in siRNA biogenesis. This phenomenon resembles paramutation-like events and occurs in both intraspecific (Mo17xB73) and interspecific (W22xTeosinte) hybrid maize populations. Moreover, siRNA abundance and methylation levels of these epialleles can affect expression of their associated epigenes, many of which are related to stress responses.
Conclusion
Divergent siRNAs between the hybridizing parents can induce trans-acting epialleles in the hybrids, while the induced epigenetic status is maintained for transgenerational inheritance during backcross and hybrid breeding, which alters epigene expression to enhance growth and adaptation. These genetic and epigenetic principles may apply broadly from plants to animals.
... For epigenetics to be useful in plant breeding, the most critical question is whether it provides a source of phenotypic variation not already captured in improvement programs. DNA methylation epialleles occupy a unique and useful position, by-and-large exhibiting highly stable mendelian inheritance, though they are less stable than genetic variants [36]. Beyond seminal work in Arabidopsis [22,37], we have a far from complete picture of inheritance in crops. ...
For millennia, natural and artificial selection has combined favourable alleles for desirable traits in crop species. While modern plant breeding has achieved steady increases in crop yields over the last century, on the current trajectory we will simply not meet demand by 2045. Novel breeding strategies and sources of genetic variation will be required to sustainably fill predicted yield gaps and meet new consumer preferences. Here, we highlight that stepping up to meet this grand challenge will increasingly require thinking ‘beyond the gene’. Significant progress has been made in understanding the contributions of both epigenetic variation and cis-regulatory variation to plant traits. This non-genic variation has great potential in future breeding, synthetic biology and biotechnology applications.
... Variations in the methylation patterns have also been identified across 83 soybean RILs [36] and across different wild soybean, landraces, and cultivars [37]. Similarly, thousands of DMRs were also observed in different genotypes and RILs of maize [26,[38][39][40] and in the model cereal Brachypodium distachyon RILs [41]. As found in A. thaliana, naturally occurring epialleles also serve diverse biological functions in other plant species, a classical example being epiallelic and transcriptional variations in the Lcyc gene in L. vulgaris that controls floral symmetry and the pericarp color1 (p1) locus in maize, which controls the kernel development and pigmentation [24,25]. ...
In plants, the gene expression and associated phenotypes can be modulated by dynamic changes in DNA methylation, occasionally being fixed in certain genomic loci and inherited stably as epialleles. Epiallelic variations in a population can occur as methylation changes at an individual cytosine position, methylation changes within a stretch of genomic regions, and chromatin changes in certain loci. Here, we focus on methylated regions, since it is unclear whether variations at individual methylated cytosines can serve any regulatory function, and the evidence for heritable chromatin changes independent of genetic changes is limited. While DNA methylation is known to affect and regulate wide arrays of plant phenotypes, most epialleles in the form of methylated regions have not been assigned any biological function. Here, we review how epialleles can be established in plants, serve a regulatory function, and are involved in adaptive processes. Recent studies suggest that most epialleles occur as byproducts of genetic variations, mainly from structural variants and Transposable Element (TE) activation. Nevertheless, epialleles that occur spontaneously independent of any genetic variations have also been described across different plant species. Here, we discuss how epialleles that are dependent and independent of genetic architecture are stabilized in the plant genome and how methylation can regulate a transcription relative to its genomic location.
... For instance, epigenetic differences in Arabidopsis thaliana have been linked to heritability in flowering time and primary root length (Cortijo et al., 2014), response to temperature (Kawakatsu et al., 2016), and biotic stressors (Dowen et al., 2012) reviewed in Zogli and Libault (2017). Additionally, inheritance of environmentally induced epigenetic variation has been observed in A. thaliana (Blevins et al., 2014;Lang-Mladek et al., 2010), as well as in several crop species (Bilichak et al., 2015;De Kort et al., 2020;Li et al., 2014) and dandelions (Verhoeven et al., 2010). However, our understanding of how epigenetic variation behaves in a variety of species and ecological contexts is growing Neinavaie et al., 2021;Richards & Pigliucci, 2020;Richards et al., 2017). ...
The capacity to respond to environmental challenges ultimately relies on phenotypic variation which manifests from complex interactions of genetic and nongenetic mechanisms through development. While we know something about genetic variation and structure of many species of conservation importance, we know very little about the nongenetic contributions to variation. Rhizophora mangle is a foundation species that occurs in coastal estuarine habitats throughout the neotropics where it provides critical ecosystem functions and is potentially threatened by anthropogenic environmental changes. Several studies have documented landscape-level patterns of genetic variation in this species, but we know virtually nothing about the inheritance of nongenetic variation. To assess one type of nongenetic variation, we examined the patterns of DNA sequence and DNA methylation in maternal plants and offspring from natural populations of R. mangle from the Gulf Coast of Florida. We used a reduced representation bisulfite sequencing approach (epi-genotyping by sequencing; epiGBS) to address the following questions: (a) What are the levels of genetic and epigenetic diversity in natural populations of R. mangle? (b) How are genetic and epigenetic variation structured within and among populations? (c) How faithfully is epigenetic variation inherited? We found low genetic diversity but high epigenetic diversity from natural populations of maternal plants in the field. In addition, a large portion (up to ~25%) of epigenetic differences among offspring grown in common garden was explained by maternal family. Therefore, epigenetic variation could be an important source of response to challenging environments in the genetically depauperate populations of this foundation species.
... DNA methylation in maize can be heritable [36,37] and changes under stress may influence subsequent generations [38]. We also found that the DNA methylation status in the offspring was more similar to that of the sequence-origin parents and the inheritance increased under drought stress, highlighting the potential function of DNA methylation. ...
DNA methylation is important for plant growth, development, and stress response. To understand DNA methylation dynamics in maize roots under water stress (WS), we reanalyzed DNA methylation sequencing data to profile DNA methylation and the gene expression landscape of two inbred lines with different drought sensitivities, as well as two of their derived recombination inbred lines (RILs). Combined with genotyping-by-sequencing, we found that the inheritance pattern of DNA methylation between RILs and parental lines was sequence-dependent. Increased DNA methylation levels were observed under WS and the methylome of drought-tolerant inbred lines were much more stable than that of the drought-sensitive inbred lines. Distinctive differentially methylated genes were found among diverse genetic backgrounds, suggesting that inbred lines with different drought sensitivities may have responded to stress in varying ways. Gene body DNA methylation showed a negative correlation with gene expression but a positive correlation with exon splicing events. Furthermore, a positive correlation of a varying extent was observed between small interfering RNA (siRNA) and DNA methylation, which at different genic regions. The response of siRNAs under WS was consistent with the differential DNA methylation. Taken together, our data can be useful in deciphering the roles of DNA methylation in plant drought-tolerance variations and in emphasizing its function in alternative splicing.
