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Biology subjects

Povilus, R. A.

Publications and source records attributed to Povilus, R. A..

4 recordsLinked to original sources

Imprinting and DNA methylation in water lily endosperm: implications for seed evolution

Endosperm is a key evolutionary innovation associated with the origin of angiosperms (flowering plants). This altruistic seed tissue supports the growth and development of the embryo by mediating the relationship of the mother plant as a nutrient source to the compatriot embryo as a nutrient sink. The endosperm is the primary site of gene imprinting in plants (where expression of an allele in offspring depends on which parent it was inherited from) and of parent-specific epigenetic modifications like DNA methylation, which are differentially patterned during male and female gamete development. Experimental results from a phylogenetically-wide array of monocot and eudicot plants suggest these parent-of-origin effects are a common feature across angiosperms. However, information about genetic imprinting and epigenetic modifications in seeds of angiosperm lineages whose origins predate the monocot-eudicot divergence (such as Nymphaeales, water lilies) is extremely limited. Additionally, Nymphaeales are an intriguing lineage in which to investigate seed genetic and epigenetic phenomena, as they are characterized by diploid endosperm and a maternal storage tissue (perisperm), both of which are unusual across angiosperm diversity. Here, we examined DNA methylation and genetic imprinting using two reproductively compatible water lily sister-species, Nymphaea thermarum and N. dimorpha. Our results suggest that maternally-expressed imprinted genes and differential DNA methylation of maternally and paternally inherited endosperm genomes are an ancestral condition for endosperm, while other seed characters like seed provisioning strategies, endosperm ploidy, and paternally-expressed imprinted genes might have evolved as coinciding, opposing strategies in the evolutionary dialogue over parental control of offspring development.

evolutionary biology↗

Transcriptomes across fertilization and seed development in the water lily Nymphaea thermarum (Nymphaeales) reveal dynamic expression of DNA and histone methylation modifiers

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, attention has mostly been focused on crop species or a small number of model systems. Information on gene expression during seed development is minimal for those angiosperm lineages whose origins predate the divergence of monocots and eudicots. In order to provide a new perspective on 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 general patterns of gene expression, beginning with mature ovules and continuing through fertilization into early- and mid-seed development. We then examine the expression of genes associated with DNA and histone methylation - processes known to be essential for development in distantly-related and structurally-divergent monocots and eudicots. Around 60% of transcripts putatively homologous to DNA and histone methylation modifiers are differentially expressed during seed development in N. thermarum, suggesting that the importance of dynamic epigenetic patterning during seed development dates to the earliest phases of angiosperm evolution. However, genes involved in establishing, maintaining, and removing methylation marks associated with genetic imprinting show a mix of conserved and unique expression patterns between N. thermarum and other flowering plants. Our data suggests that the regulation of imprinting has likely changed throughout angiosperm evolution, and furthermore identifies genes that merit further characterization in any angiosperm system.

plant biology↗

Single nucleus analysis of Arabidopsis seeds reveals new cell types and imprinting dynamics

Seeds are the basis of agriculture, yet their full transcriptional complexity has remained unknown. Here, we employ single-nucleus RNA-sequencing to characterize developing Arabidopsis thaliana seeds, with a focus on endosperm. Endosperm, the site of gene imprinting in plants, mediates the relationship between the maternal parent and embryo. We identify new cell types in the chalazal endosperm region, which interfaces with maternal tissue for nutrient unloading. We further demonstrate that the extent of parental bias of maternally expressed imprinted genes varies with cell cycle phase, and that imprinting of paternally expressed imprinted genes is strongest in chalazal endosperm. These data indicate imprinting in endosperm is heterogeneous and suggest that parental conflict, which is proposed to drive the evolution of imprinting, is fiercest at the boundary between filial and maternal tissues.

plant biology↗

Water lily (Nymphaea thermarum) draft genome reveals variable genomic signatures of ancient vascular cambium losses

For more than 225 million years, all seed plants were woody trees, shrubs, or vines (1-4). Shortly after the origin of angiosperms ~135 million years ago (MYA) (5), the Nymphaeales (water lilies) became one of the first lineages to deviate from their ancestral, woody habit by losing the vascular cambium (6), the meristematic population of cells that produces secondary xylem (wood) and phloem. Many of the genes and gene families that regulate differentiation of secondary tissues also regulate the differentiation of primary xylem and phloem (7-9), which are produced by apical meristems and retained in nearly all seed plants. Here we sequence and assemble a draft genome of the water lily Nymphaea thermarum, an emerging system for the study of early flowering plant evolution, and compare it to genomes from other cambium-bearing and cambium-less lineages (like monocots and Nelumbo). This reveals lineage-specific patterns of gene loss and divergence. Nymphaea is characterized by a significant contraction of the HD-ZIP III transcription factors, specifically loss of REVOLUTA, which influences cambial activity in other angiosperms. We also find the Nymphaea and monocot copies of cambium-associated CLE signaling peptides display unique substitutions at otherwise highly conserved amino acids. Nelumbo displays no obvious divergence in cambium-associated genes. The divergent genomic signatures of convergent vascular cambium loss reveals that even pleiotropic genes can exhibit unique divergence patterns in association with independent trait loss events. Our results shed light on the evolution of herbaceousness - one of the key biological innovations associated with the earliest phases of angiosperm evolution. Significance StatementFor ~225 million years, all seed plants were woody trees, shrubs, or vines. Shortly after the origin of flowering plants ~135 million years ago, Nymphaeales (water lilies) became one of the first seed plant lineages to become herbaceous through loss of the meristematic cell population known as the vascular cambium. We sequence and assemble the draft genome of the water lily Nymphaea thermarum, and compare it to genomes of other plants that have retained or lost the vascular cambium. By using both genome-wide and candidate-gene analysis, we find lineage-specific patterns of gene loss and divergence associated with cambium loss. Our reveal divergent genomic signatures of convergent trait loss in a system characterized by complex gene-trait relationships.

plant biology↗