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Trans-chromosomal interactions resulting in changes in DNA methylation during hybridization have been observed in several plant species. However, little is known about the causes or consequences of these interactions. Here, we compared DNA methylomes of F1 hybrids that are mutant for a small RNA biogenesis gene, Mop1 (Mediator of paramutation1), with that of their parents, wild-type siblings, and backcrossed progeny in maize (Zea mays). Our data show that hybridization triggers global changes in both trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM), most of which involved changes in CHH methylation. In more than 60% of these TCM differentially methylated regions (DMRs) in which small RNAs are available, no significant changes in the quantity of small RNAs were observed. Methylation at the CHH TCM DMRs was largely lost in the mop1 mutant, although the effects of this mutant varied depending on the location of these DMRs. Interestingly, an increase in CHH at TCM DMRs was associated with enhanced expression of a subset of highly expressed genes and suppressed expression of a small number of lowly expressed genes. Examination of the methylation levels in backcrossed plants demonstrates that both TCM and TCdM can be maintained in the subsequent generation, but that TCdM is more stable than TCM. Surprisingly, although increased CHH methylation in most TCM DMRs in F1 plants required Mop1, initiation of a new epigenetic state of these DMRs did not require a functional copy of this gene, suggesting that initiation of these changes is independent of RNA-directed DNA methylation.

 

Genomic imprinting is an epigenetic phenomenon in which differential allele expression occurs in a parent-of-origin-dependent manner. Imprinting in plants is tightly linked to transposable elements (TEs), and it has been hypothesized that genomic imprinting may be a consequence of demethylation of TEs. Here, we performed high-throughput sequencing of ribonucleic acids from four maize (Zea mays) endosperms that segregated newly silenced Mutator (Mu) transposons and identified 110 paternally expressed imprinted genes (PEGs) and 139 maternally expressed imprinted genes (MEGs). Additionally, two potentially novel paternally suppressed MEGs are associated with de novo Mu insertions. In addition, we find evidence for parent-of-origin effects on expression of 407 conserved noncoding sequences (CNSs) in maize endosperm. The imprinted CNSs are largely localized within genic regions and near genes, but the imprinting status of the CNSs are largely independent of their associated genes. Both imprinted CNSs and PEGs have been subject to relaxed selection. However, our data suggest that although MEGs were already subject to a higher mutation rate prior to their being imprinted, imprinting may be the cause of the relaxed selection of PEGs. In addition, although DNA methylation is lower in the maternal alleles of both the maternally and paternally expressed CNSs (mat and pat CNSs), the difference between the two alleles in H3K27me3 levels was only observed in pat CNSs. Together, our findings point to the importance of both transposons and CNSs in genomic imprinting in maize.

 

Synopsis Evidence from across the tree of life suggests that epigenetic inheritance is more common than previously thought. If epigenetic inheritance is indeed as common as the data suggest, this finding has potentially important implications for evolutionary theory and our understanding of how evolution and adaptation progress. However, we currently lack an understanding of how common various epigenetic inheritance types are, and how they impact phenotypes. In this perspective, we review the open questions that need to be addressed to fully integrate epigenetic inheritance into evolutionary theory and to develop reliable predictive models for phenotypic evolution. We posit that addressing these challenges will require the collaboration of biologists from different disciplines and a focus on the exploration of data and phenomena without preconceived limits on potential mechanisms or outcomes. 

Abstract Transposable elements (TEs) are ubiquitous DNA segments capable of moving from one site to another within host genomes. The extant distributions of TEs in eukaryotic genomes have been shaped by both bona fide TE integration preferences in eukaryotic genomes and by selection following integration. Here, we compare TE target site distribution in host genomes using multiple de novo transposon insertion datasets in both plants and animals and compare them in the context of genome-wide transcriptional landscapes. We showcase two distinct types of transcription-associated TE targeting strategies that suggest a process of convergent evolution among eukaryotic TE families. The integration of two precision-targeting elements are specifically associated with initiation of RNA Polymerase II transcription of highly expressed genes, suggesting the existence of novel mechanisms of precision TE targeting in addition to passive targeting of open chromatin. We also highlight two features that can facilitate TE survival and rapid proliferation: tissue-specific transposition and minimization of negative impacts on nearby gene function due to precision targeting. 

Sorghum is an important food and feed crop globally; its production is hampered by anthracnose disease caused by the fungal pathogenColletotrichum sublineola(Cs). Here, we report identification and characterization ofANTHRACNOSE RESISTANCE GENE 2(ARG2) encoding a nucleotide‐binding leucine‐rich repeat (NLR) protein that confers race‐specific resistance toCsstrains.ARG2is one of a cluster of severalNLRgenes initially identified in the sorghum differential line SC328C that is resistant to someCsstrains. This cluster shows structural and copy number variations in different sorghum genotypes. Different sorghum lines carrying independentARG2alleles provided the genetic validation for the identity of theARG2gene.ARG2expression is induced byCs, and chitin inducesARG2expression in resistant but not in susceptible lines. ARG2‐mediated resistance is accompanied by higher expression of defense and secondary metabolite genes at early stages of infection, and anthocyanin and zeatin metabolisms are upregulated in resistant plants. Interestingly, ARG2 localizes to the plasma membrane when transiently expressed inNicotiana benthamiana. Importantly,ARG2plants produced higher shoot dry matter than near‐isogenic lines carrying the susceptible allele suggesting an absence of anARG2associated growth trade‐off. Furthermore, ARG2‐mediated resistance is stable at a wide range of temperatures. Our observations open avenues for resistance breeding and for dissecting mechanisms of resistance.

 

Meiotic recombination is a fundamental process that generates genetic diversity and ensures the accurate segregation of homologous chromosomes. While a great deal is known about genetic factors that regulate recombination, relatively little is known about epigenetic factors, such as DNA methylation. In maize, we examined the effects on meiotic recombination of a mutation in a component of the RNA-directed DNA methylation pathway,Mop1(Mediator of paramutation1), as well as a mutation in a component of thetrans-acting small interference RNA biogenesis pathway,Lbl1(Leafbladeless1). MOP1 is of particular interest with respect to recombination because it is responsible for methylation of transposable elements that are immediately adjacent to transcriptionally active genes. In themop1mutant, we found that meiotic recombination is uniformly decreased in pericentromeric regions but is generally increased in gene rich chromosomal arms. This observation was further confirmed by cytogenetic analysis showing that although overall crossover numbers are unchanged, they occur more frequently in chromosomal arms inmop1mutants. Using whole genome bisulfite sequencing, our data show that crossover redistribution is driven by loss of CHH (where H = A, T, or C) methylation within regions near genes. In contrast to what we observed inmop1mutants, no significant changes were observed in the frequency of meiotic recombination inlbl1mutants. Our data demonstrate that CHH methylation has a significant impact on the overall recombination landscape in maize despite its low frequency relative to CG and CHG methylation.

 

Sorghum (Sorghum bicolor), the fifth most widely grown cereal crop globally, provides food security for millions of people. Anthracnose caused by the fungus Colletotrichum sublineola is a major disease of sorghum worldwide. We discovered a major fungal resistance locus in sorghum composed of the nucleotide-binding leucine-rich repeat receptor gene ANTHRACNOSE RESISTANCE GENE1 (ARG1) that is completely nested in an intron of a cis-natural antisense transcript (NAT) gene designated CARRIER OF ARG1 (CARG). Susceptible genotypes express CARG and two alternatively spliced ARG1 transcripts encoding truncated proteins lacking the leucine-rich repeat domains. In resistant genotypes, elevated expression of an intact allele of ARG1, attributed to the loss of CARG transcription and the presence of miniature inverted-repeat transposable element sequences, resulted in broad-spectrum resistance to fungal pathogens with distinct virulence strategies. Increased ARG1 expression in resistant genotypes is also associated with higher histone H3K4 and H3K36 methylation. In susceptible genotypes, lower ARG1 expression is associated with reduced H3K4 and H3K36 methylation and increased expression of NATs of CARG. The repressive chromatin state associated with H3K9me2 is low in CARG-expressing genotypes within the CARG exon and higher in genotypes with low CARG expression. Thus, ARG1 is regulated by multiple mechanisms and confers broad-spectrum, strong resistance to fungal pathogens.