scholarly journals Evidence for parent-of-origin effects and interparental conflict in seeds of an ancient flowering plant lineage

2018 ◽  
Vol 285 (1872) ◽  
pp. 20172491 ◽  
Author(s):  
Rebecca A. Povilus ◽  
Pamela K. Diggle ◽  
William E. Friedman

Theoretical and empirical studies have long connected the evolutionary innovation of endosperm, a genetically biparental product of a double fertilization process unique to flowering plants (angiosperms), to conflicting parental interests over offspring provisioning. Yet, none of these studies examined interparental conflict in representatives of any of the most ancient angiosperm lineages. We performed reciprocal interploidy crosses in the water lily Nymphaea thermarum , a member of one of the most ancient angiosperm lineages, Nymphaeales. We find that an excess of paternal genomes is associated with an increase in endosperm growth. By contrast, maternal ploidy negatively influences development or growth of all seed components, regardless of paternal genome dosage. Most relevant to the conflict over distribution of maternal resources, however, is that growth of the perisperm (seed storage tissue derived from the maternal sporophyte, found in all Nymphaeales) is unaffected by paternal genome dosage—ensuring maternal control of maternal resources. We conclude that the evolutionary transfer of embryo-nourishing function from a genetically biparental endosperm to a genetically maternal perisperm can be viewed as an effective maternal strategy to recapture control of resource distribution among progeny, and thus that interparental conflict has influenced the evolution of seed development in this ancient angiosperm lineage.

Development ◽  
1994 ◽  
Vol 120 (4) ◽  
pp. 797-802 ◽  
Author(s):  
J.P. Renard ◽  
P. Baldacci ◽  
V. Richoux-Duranthon ◽  
S. Pournin ◽  
C. Babinet

Normal development of the mouse embryo requires the presence of both paternal and maternal genomes. This is due to functional differences having their origin in a differential imprinting of parental genomes. Furthermore, several lines of evidence show that the very early interactions between egg cytoplasm and pronuclei may influence the programming of the embryonic genome and modulate the functional inequality of the parental contribution even during preimplantation stages. In this paper, we show that a factor present in ovulated oocytes of the mouse mutant strain DDK and therefore of maternal origin prevents the formation of the blastocyst. This factor, which acts via an interaction with the paternal genome, is present in oocytes as an RNA and is still active in preimplantation embryos. This is the first direct evidence of such a maternal control in the mouse.


eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Mia T Levine ◽  
Helen M Vander Wende ◽  
Harmit S Malik

Sperm-packaged DNA must undergo extensive reorganization to ensure its timely participation in embryonic mitosis. Whereas maternal control over this remodeling is well described, paternal contributions are virtually unknown. In this study, we show that Drosophila melanogaster males lacking Heterochromatin Protein 1E (HP1E) sire inviable embryos that undergo catastrophic mitosis. In these embryos, the paternal genome fails to condense and resolve into sister chromatids in synchrony with the maternal genome. This delay leads to a failure of paternal chromosomes, particularly the heterochromatin-rich sex chromosomes, to separate on the first mitotic spindle. Remarkably, HP1E is not inherited on mature sperm chromatin. Instead, HP1E primes paternal chromosomes during spermatogenesis to ensure faithful segregation post-fertilization. This transgenerational effect suggests that maternal control is necessary but not sufficient for transforming sperm DNA into a mitotically competent pronucleus. Instead, paternal action during spermiogenesis exerts post-fertilization control to ensure faithful chromosome segregation in the embryo.


2007 ◽  
Vol 403 (3) ◽  
pp. e13-e14 ◽  
Author(s):  
Tatjana Kleine ◽  
Dario Leister

The term ‘evolutionary tinkering’ refers to evolutionary innovation by recombination of functional units, and includes the creation of novel proteins from pre-existing modules. A novel instance of evolutionary tinkering was recently discovered in the flowering plant genus Nicotiana: the conversion of a nuclear transcription factor into the plastid-resident protein WIN4 (wound-induced clone 4) involved in environmental stress responses. In this issue of the Biochemical Journal, Kodama and Sano now show that two steps are necessary for the establishment of the novel plastid protein: the acquisition of an internal translation initiation site and the use of multiple transcription starts to produce short mRNA variants that encode the plastid-targeted protein form.


2020 ◽  
Vol 117 (15) ◽  
pp. 8649-8656 ◽  
Author(s):  
Rebecca A. Povilus ◽  
Jeffrey M. DaCosta ◽  
Christopher Grassa ◽  
Prasad R. V. Satyaki ◽  
Morgan Moeglein ◽  
...  

For more than 225 million y, all seed plants were woody trees, shrubs, or vines. Shortly after the origin of angiosperms ∼140 million y ago (MYA), the Nymphaeales (water lilies) became one of the first lineages to deviate from their ancestral, woody habit by losing the vascular cambium, 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, which are produced by apical meristems and retained in nearly all seed plants. Here, we sequenced and assembled a draft genome of the water lily Nymphaea thermarum, an emerging system for the study of early flowering plant evolution, and compared it to genomes from other cambium-bearing and cambium-less lineages (e.g., monocots and Nelumbo). This revealed 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 found 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 loss of vascular cambium reveals that even pleiotropic genes can exhibit unique divergence patterns in association with independent events of trait loss. Our results shed light on the evolution of herbaceousness—one of the key biological innovations associated with the earliest phases of angiosperm evolution.


Open Biology ◽  
2014 ◽  
Vol 4 (6) ◽  
pp. 140027 ◽  
Author(s):  
Grazyna E. Ptak ◽  
Paola Toschi ◽  
Antonella Fidanza ◽  
Marta Czernik ◽  
Federica Zacchini ◽  
...  

Functional genomic imprinting is necessary for the transfer of maternal resources to mammalian embryos. Imprint-free embryos are unable to establish a viable placental vascular network necessary for the transfer of resources such as nutrients and oxygen. How the parental origin of inherited genes influences cellular response to resource limitation is currently not well understood. Because such limitations are initially realized by the placenta, we studied how maternal and paternal genomes influence the cellular self-destruction responses of this organ specifically. Here, we show that cellular autophagy is prevalent in androgenetic (i.e. having only a paternal genome) placentae, while apoptosis is prevalent in parthenogenetic (i.e. having only a maternal genome) placentae. Our findings indicate that the parental origin of inherited genes determines the placenta's cellular death pathway: autophagy for androgenotes and apoptosis for parthenogenotes. The difference in time of arrest between androgenotes and parthenogenotes can be attributed, at least in part, to their placentae's selective use of these two cell death pathways. We anticipate our findings to be a starting point for general studies on the parent-of-origin regulation of autophagy. Furthermore, our work opens the door to new studies on the involvement of autophagy in pathologies of pregnancy in which the restricted transfer of maternal resources is diagnosed.


2021 ◽  
Author(s):  
Toby Buttress ◽  
Shengbo He ◽  
Liang Wang ◽  
Shaoli Zhou ◽  
Lei Sun ◽  
...  

Sperm chromatin is typically transformed by protamines into a compact and transcriptionally inactive state. Flowering plant sperm cells lack protamines, yet have small, transcriptionally active nuclei with chromatin condensed by an unknown mechanism. Here we show that a histone variant, H2B.8, mediates sperm chromatin and nuclear condensation in Arabidopsis thaliana. Loss of H2B.8 causes enlarged sperm nuclei with dispersed chromatin, whereas ectopic expression in somatic cells produces smaller nuclei with aggregated chromatin, demonstrating that H2B.8 is sufficient for chromatin condensation. H2B.8 aggregates transcriptionally inactive AT-rich chromatin into phase-separated condensates, thus achieving nuclear compaction without reducing transcription. H2B.8 also intermixes inactive AT-rich chromatin and GC-rich pericentromeric heterochromatin, altering higher-order chromatin architecture. Altogether, our results reveal a novel mechanism of nuclear compaction via global aggregation of unexpressed chromatin. We propose that H2B.8 is a flowering plant evolutionary innovation that achieves nuclear condensation compatible with active transcription.


2019 ◽  
Author(s):  
Rebecca A. Povilus ◽  
Jeffery M. DaCosta ◽  
Christopher Grassa ◽  
Prasad R. V. Satyaki ◽  
Morgan Moeglein ◽  
...  

AbstractFor 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.


2015 ◽  
Vol 112 (52) ◽  
pp. 15952-15957 ◽  
Author(s):  
Sarah P. Otto ◽  
Michael F. Scott ◽  
Simone Immler

Diploid organisms manipulate the extent to which their haploid gametes experience selection. Animals typically produce sperm with a diploid complement of most proteins and RNA, limiting selection on the haploid genotype. Plants, however, exhibit extensive expression in pollen, with actively transcribed haploid genomes. Here we analyze models that track the evolution of genes that modify the strength of haploid selection to predict when evolution intensifies and when it dampens the “selective arena” within which male gametes compete for fertilization. Considering deleterious mutations, evolution leads diploid mothers to strengthen selection among haploid sperm/pollen, because this reduces the mutation load inherited by their diploid offspring. If, however, selection acts in opposite directions in haploids and diploids (“ploidally antagonistic selection”), mothers evolve to reduce haploid selection to avoid selectively amplifying alleles harmful to their offspring. Consequently, with maternal control, selection in the haploid phase either is maximized or reaches an intermediate state, depending on the deleterious mutation rate relative to the extent of ploidally antagonistic selection. By contrast, evolution generally leads diploid fathers to mask mutations in their gametes to the maximum extent possible, whenever masking (e.g., through transcript sharing) increases the average fitness of a father’s gametes. We discuss the implications of this maternal–paternal conflict over the extent of haploid selection and describe empirical studies needed to refine our understanding of haploid selection among seemingly diploid organisms.


Author(s):  
Debi A. LaPlante ◽  
Heather M. Gray ◽  
Pat M. Williams ◽  
Sarah E. Nelson

Abstract. Aims: To discuss and review the latest research related to gambling expansion. Method: We completed a literature review and empirical comparison of peer reviewed findings related to gambling expansion and subsequent gambling-related changes among the population. Results: Although gambling expansion is associated with changes in gambling and gambling-related problems, empirical studies suggest that these effects are mixed and the available literature is limited. For example, the peer review literature suggests that most post-expansion gambling outcomes (i. e., 22 of 34 possible expansion outcomes; 64.7 %) indicate no observable change or a decrease in gambling outcomes, and a minority (i. e., 12 of 34 possible expansion outcomes; 35.3 %) indicate an increase in gambling outcomes. Conclusions: Empirical data related to gambling expansion suggests that its effects are more complex than frequently considered; however, evidence-based intervention might help prepare jurisdictions to deal with potential consequences. Jurisdictions can develop and evaluate responsible gambling programs to try to mitigate the impacts of expanded gambling.


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