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Transcriptomes across fertilization and seed development in the water lily Nymphaea thermarum (Nymphaeales): evidence for epigenetic patterning during reproduction

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The first record of gene expression during seed development within the Nymphaeales provides evidence for a variety of biological processes, including dynamic epigenetic patterning during sexual reproduction in the water lily Nymphaea thermarum.

Abstract

Studies of gene expression during seed development have been performed for a growing collection of species from a phylogenetically broad sampling of flowering plants (angiosperms). However, angiosperm lineages whose origins predate the divergence of monocots and eudicots have been largely overlooked. In order to provide a new resource for understanding the early evolution of seed development in flowering plants, we sequenced transcriptomes of whole ovules and seeds from three key stages of reproductive development in the waterlily Nymphaea thermarum, an experimentally tractable member of the Nymphaeales. We first explore patterns of gene expression, beginning with mature ovules and continuing through fertilization into early- and mid-stages of seed development. We find patterns of gene expression that corroborate histological/morphological observations of seed development in this species, such as expression of genes involved in starch synthesis and transcription factors that have been associated with embryo and endosperm development in other species. We also find evidence for processes that were previously not known to be occurring during seed development in this species, such as epigenetic modification. We then examine the expression of genes associated with patterning DNA and histone methylation—processes that are essential for seed development in distantly related and structurally diverse monocots and eudicots. Around 89% of transcripts putatively homologous to DNA and histone methylation modifiers are expressed during seed development in N. thermarum, including homologs of genes known to pattern imprinting-related epigenetic modifications. Our results suggest that dynamic epigenetic patterning is a deeply conserved aspect of angiosperm seed development.

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Data availability

Raw sequence data of N. thermarum have been submitted to the National Center for Biotechnology Information (NCBI) database under BioProject PRJNA718528. Genome assembly and annotation (Povilus et al. 2020) is available as part of NCBI BioProject PRJNA508901. Biological material and all other data are available as Supplemental Data, or from the corresponding authors upon request.

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Acknowledgements

We thank the Botanische Gärten der Universität Bonn for providing original plant material for propagation.

Funding

We acknowledge support from the National Science Foundation: IOS-0919986 awarded to W.E.F., and DEB-1500963 and IOS-1812116 awarded to R.A.P.

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Correspondence to William E. Friedman.

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The authors declare no conflicts of interest or competing interests.

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Communicated by Claudia Köhler.

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Povilus, R.A., Friedman, W.E. Transcriptomes across fertilization and seed development in the water lily Nymphaea thermarum (Nymphaeales): evidence for epigenetic patterning during reproduction. Plant Reprod 35, 161–178 (2022). https://doi.org/10.1007/s00497-022-00438-3

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  • DOI: https://doi.org/10.1007/s00497-022-00438-3

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