Distinct methylome patterns contribute to ecotypic differentiation in the growth of the storage organ of a flowering plant (sacred lotus)

Abstract

DNA methylation is an epigenetic modification involved in phenotypic diversity, plant development, and environmental responses. However, the mechanisms of DNA methylation underpinning the adaption of lotus (Nelumbo nucifera) ecotypes to high and low latitudes remain unsolved, especially adaptive evolution of their storage organs. Tropical and temperate lotus ecotypes have thin and enlarged rhizomes which are adapted to low and high latitudes, respectively. Here, we investigated the DNA methylomes and transcriptomes of rhizomes of the temperate and tropical lotus to address this issue. Compared with that of the tropical lotus, the DNA of the temperate lotus was significantly more hypermethylated, indicating an increase in global DNA methylation in the lotus, with rhizome enlargement. Meanwhile, genes associated with differentially methylated regions in their promoters tended to be differentially expressed between the two ecotypes. Interestingly, the genes with their expression negatively correlated with methylation levels in their promoters and genomic regions displayed significantly higher transposon coverage, while the genes showing a significant positive correlation between expression and methylation showed lesser transposon coverage. Further, we identified that DNA methylation, especially in the promoter region, was significantly correlated with the expression of many starch‐biosynthetic, gibberellin‐, and brassinosteroid‐signalling genes associated with rhizome differentiation. Overall, our study unveiled that distinct global and local methylation patterns between the two lotus ecotypes contribute to their expression differences and adaptive phenotypic divergence of their storage organs, highlighting the role of DNA methylation in shaping the ecotypic differentiation of lotus.

Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed

“…Recent studies have found that some hyperaccumulators with limited genetic variation among populations still have a wide range of phenotypes in different metalliferous habitats ( Chen et al, 2015 ). Epigenetic variation which can regulate phenotypic variation could be one potentially important way for plant in response to environmental changes ( Niederhuth and Schmitz, 2014 ; Wibowo et al, 2016 ; Li et al, 2021 ). DNA methylation is one of the main epigenetic mechanisms enabling adaptation of plants in complex environments ( Niederhuth and Schmitz, 2014 ; Chang et al, 2019 ; Perrone and Martinelli, 2020 ; Li et al, 2021 ; Chen et al, 2022 ).…”

“…Epigenetic variation which can regulate phenotypic variation could be one potentially important way for plant in response to environmental changes ( Niederhuth and Schmitz, 2014 ; Wibowo et al, 2016 ; Li et al, 2021 ). DNA methylation is one of the main epigenetic mechanisms enabling adaptation of plants in complex environments ( Niederhuth and Schmitz, 2014 ; Chang et al, 2019 ; Perrone and Martinelli, 2020 ; Li et al, 2021 ; Chen et al, 2022 ). Changes of DNA methylation in response to environmental stresses can be relatively stable, and establish a DNA methylation-dependent stress memory to the offspring ( Wibowo et al, 2016 ; Williams and Gehring, 2017 ; Sudan et al, 2018 ).…”

Genomic variation reveals demographic history and biological adaptation of the ancient relictual, lotus (Nelumbo Adans.)

“…[ 12 ] studied the genetic diversity of the wild Asian lotus from Northern China and provided essential resources for the Chinese wild lotus. Recently, research on DNA methylation in the lotus genome has been greatly promoted and conducted successfully [ 13 , 14 ]. However, studies on the mutation rate and demographic history of lotus are relatively few and evolutionary questions related to extinction, competition, and adaptation in lotus remain unclear.…”

Interactive Regulations of Dynamic Methylation and Transcriptional Responses to Recurring Environmental Stresses During Biological Invasions

“…Despite the fact that the functions of phenotypic plasticity in rapid environmental response have been well-accepted, its downstream regulatory roles are still under hot debates (Foret et al, 2012;Neri et al, 2017;Li et al, 2018Li et al, , 2021Smith et al, 2020). In a "standard" model, the methylation of CpG islands within promoter region is generally correlated with the transcriptional repression (Halpern et al, 2014).…”

“…During the endodermal development, hypermethylation of one CpG island within Forkhead box A2 (FOXA2) promoter might contribute to the active transcription of this gene (Halpern et al, 2014). In contrast to the widely studied functions of promoter methylation, the role of gene body methylation is still uncertain and perplexing, as it has been reported to be involved in negative/positive regulations at the transcript levels, alternative splicing, mitigation of transcriptional noise, and maintenance of transcriptional homeostasis (Foret et al, 2012;Neri et al, 2017;Li et al, 2018Li et al, , 2021. Collectively, these results suggest that the regulatory roles of DNA methylation in transcription might be far more complicated than what we have known.…”