Title: Parental methylation mediates how progeny respond to environments of parents and of progeny themselves
AbstractBackground and Aims
Environments experienced by both parents and offspring influence progeny traits, but the epigenetic mechanisms that regulate the balance of parental vs. progeny control of progeny phenotypes are not known. We tested whether DNA methylation in parents and/or progeny mediates responses to environmental cues experienced in both generations.
Methods
Using Arabidopsis thaliana, we manipulated parental and progeny DNA methylation both chemically, via 5-azacytidine, and genetically, via mutants of methyltransferase genes, then measured progeny germination responses to simulated canopy shade in parental and progeny generations.
Key Results
We first found that germination of offspring responded to parental but not seed demethylation. We further found that parental demethylation reversed the parental effect of canopy in seeds with low (Cvi-1) to intermediate (Col) dormancy, but it obliterated the parental effect in seeds with high dormancy (Cvi-0). Demethylation did so by either suppressing germination of seeds matured under white-light (Cvi-1) or under canopy (Cvi-0), or by increasing the germination of seeds matured under canopy (Col). Disruption of parental methylation also prevented seeds from responding to their own light environment in one genotype (Cvi-0, most dormant), but it enabled seeds to respond to their own environment in another genotype (Cvi-1, least dormant). Using mutant genotypes, we found that both CG and non-CG DNA methylation were involved in parental effects on seed germination.
Conclusions
Parental methylation state influences seed germination more strongly than does the progeny’s own methylation state, and it influences how seeds respond to environments of parents and progeny in a genotype-specific manner.
Frost, Jennifer M.; Lee, Jaehoon; Hsieh, Ping-Hung; Lin, Samuel J. H.; Min, Yunsook; Bauer, Matthew; Runkel, Anne M.; Cho, Hyung-Taeg; Hsieh, Tzung-Fu; Fischer, Robert L.; et al(
, BMC Plant Biology)
AbstractBackground
H2A.X is an H2A variant histone in eukaryotes, unique for its ability to respond to DNA damage, initiating the DNA repair pathway. H2A.X replacement within the histone octamer is mediated by the FAcilitates Chromatin Transactions (FACT) complex, a key chromatin remodeler. FACT is required for DEMETER (DME)-mediated DNA demethylation at certain loci inArabidopsis thalianafemale gametophytes during reproduction. Here, we sought to investigate whether H2A.X is involved in DME- and FACT-mediated DNA demethylation during reproduction.
Results
H2A.X is encoded by two genes in Arabidopsis genome,HTA3andHTA5. We generatedh2a.xdouble mutants, which displayed a normal growth profile, whereby flowering time, seed development, and root tip organization, S-phase progression and proliferation were all normal. However,h2a.xmutants were more sensitive to genotoxic stress, consistent with previous reports. H2A.X fused to Green Fluorescent Protein (GFP) under theH2A.Xpromoter was highly expressed especially in newly developing Arabidopsis tissues, including in male and female gametophytes, where DME is also expressed. We examined DNA methylation inh2a.xdeveloping seeds and seedlings using whole genome bisulfite sequencing, and found that CG DNA methylation is decreased genome-wide inh2a.xmutant endosperm. Hypomethylation was most striking in transposon bodies, and occurred on both parental alleles in the developing endosperm, but not the embryo or seedling.h2a.x-mediated hypomethylated sites overlapped DME targets, but also included other loci, predominately located in heterochromatic transposons and intergenic DNA.
Conclusions
Our genome-wide methylation analyses suggest that H2A.X could function in preventing access of the DME demethylase to non-canonical sites. Overall, our data suggest that H2A.X is required to maintain DNA methylation homeostasis in the unique chromatin environment of the Arabidopsis endosperm.
Association between seed dormancy (SD) and flowering time (FT) may generate a synergy in plant adaptation. This research aimed to identify patterns and underlying genes of the association in rice (Oryza sativa). Four F2and two BC1F1populations from crosses of weedy/cultivated rice, and two families of progeny lines from backcrosses were evaluated for variations in time to flowering and germination ability. The two measurements were correlated negatively in the F2and BC1F1populations, but positively in advanced generations of the progeny lines. The negative correlations were resulted from linkage disequilibria between SD and FT loci at 7–40 cM apart. The positive correlations arose from co-located SD and FT loci undetectable in the BC1F1population. Two independent sets of co-localized loci were isolated as single Mendelian factors, and haplotypes that promote flowering and reduce germination derived from weedy and cultivated rice, respectively. The presence of negative and positive correlations indicates that the rice complex has maintained two contrasting patterns of SD-FT coadaptation, with the positive being “recessive” to the negative pattern. Modeling with isogenic lines suggests that a negative pattern could generate a greater synergy (difference between haplotype variants) than the positive one for seedbank persistence, or enhanced plant adaptation to seasonal changes in temperature or moisture. However, the early-flowering dormant genotype of a positive pattern could also have a selective advantage over its counterpart for weeds to avoid harvesting. The isolated haplotypes could be used to manipulate cultivars simultaneously for germination ability and growth duration.
Nihranz, Chad T.; Walker, William S.; Brown, Steven J.; Mescher, Mark C.; De Moraes, Consuelo M.; Stephenson, Andrew G.(
, American Journal of Botany)
Premise
Plant maternal effects on offspring phenotypes are well documented. However, little is known about how herbivory on maternal plants affects offspring fitness. Furthermore, while inbreeding is known to reduce plant reproductive output, previous studies have not explored whether and how such effects may extend across generations. Here, we addressed the transgenerational consequences of herbivory and maternal plant inbreeding on the reproduction of Solanum carolinenseoffspring.
Methods
Manduca sextacaterpillars were used to inflict weekly damage on inbred and outbredS. carolinensematernal plants. Cross‐pollinations were performed by hand to produce seed from herbivore‐damaged outbred plants, herbivore‐damaged inbred plants, undamaged outbred plants, and undamaged inbred plants. The resulting seeds were grown in the greenhouse to assess emergence rate and flower production in the absence of herbivores. We also grew offspring in the field to examine reproductive output under natural conditions.
Results
We found transgenerational effects of herbivory and maternal plant inbreeding on seedling emergence and reproductive output. Offspring of herbivore‐damaged plants had greater emergence, flowered earlier, and produced more flowers and seeds than offspring of undamaged plants. Offspring of outbred maternal plants also had greater seedling emergence and reproductive output than offspring of inbred maternal plants, even though all offspring were outbred. Moreover, the effects of maternal plant inbreeding were more severe when plant offspring were grown in field conditions.
Conclusions
This study demonstrates that both herbivory and inbreeding have fitness consequences that extend across generations even in outbred progeny.
Vahsen, Megan L.; Gentile, Rachel M.; Summers, Jennifer L.; Kleiner, Helena S.; Foster, Benjamin; McCormack, Regina M.; James, Evan W.; Koch, Rachel A.; Metts, Dailee L.; Saunders, Colin; et al(
, Evolutionary Applications)
Abstract
There has been a steady rise in the use of dormant propagules to study biotic responses to environmental change over time. This is particularly important for organisms that strongly mediate ecosystem processes, as changes in their traits over time can provide a unique snapshot into the structure and function of ecosystems from decades to millennia in the past. Understanding sources of bias and variation is a challenge in the field of resurrection ecology, including those that arise because often‐used measurements like seed germination success are imperfect indicators of propagule viability. Using a Bayesian statistical framework, we evaluated sources of variability and tested for zero‐inflation and overdispersion in data from 13 germination trials of soil‐stored seeds ofSchoenoplectus americanus, an ecosystem engineer in coastal salt marshes in the Chesapeake Bay. We hypothesized that these two model structures align with an ecological understanding of dormancy and revival: zero‐inflation could arise due to failed germinations resulting from inviability or failed attempts to break dormancy, and overdispersion could arise by failing to measure important seed traits. A model that accounted for overdispersion, but not zero‐inflation, was the best fit to our data. Tetrazolium viability tests corroborated this result: most seeds that failed to germinate did so because they were inviable, not because experimental methods failed to break their dormancy. Seed viability declined exponentially with seed age and was mediated by seed provenance and experimental conditions. Our results provide a framework for accounting for and explaining variability when estimating propagule viability from soil‐stored natural archives which is a key aspect of using dormant propagules in eco‐evolutionary studies.
In Mediterranean climates, the timing of seasonal rains determines germination, flowering phenology and fitness. As climate change alters seasonal precipitation patterns, it is important to ask how these changes will affect the phenology and fitness of plant populations. We addressed this question experimentally with the annual plant speciesArabidopsis thaliana.
In a first experiment, we manipulated the date of rainfall onset and recorded germination phenology on sand and soil substrates. In a second experiment, we manipulated germination date, growing season length and mid‐season drought to measure their effects on flowering time and fitness. Within each experiment, we manipulated seed dormancy and flowering time using multilocus near‐isogenic lines segregating strong and weak alleles of the seed dormancy geneDOG1and the flowering time geneFRI. We synthesized germination phenology data from the first experiment with fitness functions from the second experiment to project population fitness under different seasonal rainfall scenarios.
Germination phenology tracked rainfall onset but was slower and more variable on sand than on soil. Many seeds dispersed on sand in spring and summer delayed germination until the cooler temperatures of autumn. The high‐dormancyDOG1allele also prevented immediate germination in spring and summer. Germination timing strongly affected plant fitness. Fecundity was highest in the October germination cohort and declined in spring germinants. The late floweringFRIallele had lower fecundity, especially in early fall and spring cohorts. Projections of population fitness revealed that: (1) Later onset of autumn rains will negatively affect population fitness. (2) Slow, variable germination on sand buffers populations against fitness impacts of variable spring and summer rainfall. (3) Seasonal selection favours high dormancy and early flowering genotypes in a Mediterranean climate with hot dry summers. The high‐dormancyDOG1allele delayed germination of spring‐dispersed fresh seeds until more favourable early fall conditions, resulting in higher projected population fitness.
These findings suggest that Mediterranean annual plant populations are vulnerable to changes in seasonal precipitation, especially in California where rainfall onset is already occurring later. The fitness advantage of highly dormant, early flowering genotypes helps explain the prevalence of this strategy in Mediterranean populations.
Read the freePlain Language Summaryfor this article on the Journal blog.
Morgan, Britany L., and Donohue, Kathleen. Parental methylation mediates how progeny respond to environments of parents and of progeny themselves. Annals of Botany 130.6 Web. doi:10.1093/aob/mcac125.
Morgan, Britany L., & Donohue, Kathleen. Parental methylation mediates how progeny respond to environments of parents and of progeny themselves. Annals of Botany, 130 (6). https://doi.org/10.1093/aob/mcac125
Morgan, Britany L., and Donohue, Kathleen.
"Parental methylation mediates how progeny respond to environments of parents and of progeny themselves". Annals of Botany 130 (6). Country unknown/Code not available: Oxford University Press. https://doi.org/10.1093/aob/mcac125.https://par.nsf.gov/biblio/10386043.
@article{osti_10386043,
place = {Country unknown/Code not available},
title = {Parental methylation mediates how progeny respond to environments of parents and of progeny themselves},
url = {https://par.nsf.gov/biblio/10386043},
DOI = {10.1093/aob/mcac125},
abstractNote = {Abstract Background and AimsEnvironments experienced by both parents and offspring influence progeny traits, but the epigenetic mechanisms that regulate the balance of parental vs. progeny control of progeny phenotypes are not known. We tested whether DNA methylation in parents and/or progeny mediates responses to environmental cues experienced in both generations. MethodsUsing Arabidopsis thaliana, we manipulated parental and progeny DNA methylation both chemically, via 5-azacytidine, and genetically, via mutants of methyltransferase genes, then measured progeny germination responses to simulated canopy shade in parental and progeny generations. Key ResultsWe first found that germination of offspring responded to parental but not seed demethylation. We further found that parental demethylation reversed the parental effect of canopy in seeds with low (Cvi-1) to intermediate (Col) dormancy, but it obliterated the parental effect in seeds with high dormancy (Cvi-0). Demethylation did so by either suppressing germination of seeds matured under white-light (Cvi-1) or under canopy (Cvi-0), or by increasing the germination of seeds matured under canopy (Col). Disruption of parental methylation also prevented seeds from responding to their own light environment in one genotype (Cvi-0, most dormant), but it enabled seeds to respond to their own environment in another genotype (Cvi-1, least dormant). Using mutant genotypes, we found that both CG and non-CG DNA methylation were involved in parental effects on seed germination. ConclusionsParental methylation state influences seed germination more strongly than does the progeny’s own methylation state, and it influences how seeds respond to environments of parents and progeny in a genotype-specific manner.},
journal = {Annals of Botany},
volume = {130},
number = {6},
publisher = {Oxford University Press},
author = {Morgan, Britany L. and Donohue, Kathleen},
}
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