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Title: Water lily ( Nymphaea thermarum ) genome reveals variable genomic signatures of ancient vascular cambium losses
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 lilyNymphaea 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 andNelumbo). This revealed lineage-specific patterns of gene loss and divergence.Nymphaeais characterized by a significant contraction of the HD-ZIP III transcription factors, specifically loss ofREVOLUTA, which influences cambial activity in other angiosperms. We also found theNymphaeaand monocot copies of cambium-associated CLE signaling peptides display unique substitutions at otherwise highly conserved amino acids.Nelumbodisplays no obvious divergence in cambium-associated genes. The divergent genomic signatures of convergent loss of vascular cambium reveals more »
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.
Murphy, Chelsea L.; Yang, R.; Decker, T.; Cavalliere, C.; Andreev, V.; Bircher, N.; Cornell, J.; Dohmen, R.; Pratt, C. J.; Grinnell, A.; et al(
, Applied and Environmental Microbiology)
Nikel, Pablo Ivan
(Ed.)
ABSTRACT Cultured Myxococcota are predominantly aerobic soil inhabitants, characterized by their highly coordinated predation and cellular differentiation capacities. Little is currently known regarding yet-uncultured Myxococcota from anaerobic, nonsoil habitats. We analyzed genomes representing one novel order (o__JAFGXQ01) and one novel family (f__JAFGIB01) in the Myxococcota from an anoxic freshwater spring (Zodletone Spring) in Oklahoma, USA. Compared to their soil counterparts, anaerobic Myxococcota possess smaller genomes and a smaller number of genes encoding biosynthetic gene clusters (BGCs), peptidases, one- and two-component signal transduction systems, and transcriptional regulators. Detailed analysis of 13 distinct pathways/processes crucial to predation and cellular differentiation revealed severelymore »curtailed machineries, with the notable absence of homologs for key transcription factors (e.g., FruA and MrpC), outer membrane exchange receptor (TraA), and the majority of sporulation-specific and A-motility-specific genes. Further, machine learning approaches based on a set of 634 genes informative of social lifestyle predicted a nonsocial behavior for Zodletone Myxococcota . Metabolically, Zodletone Myxococcota genomes lacked aerobic respiratory capacities but carried genes suggestive of fermentation, dissimilatory nitrite reduction, and dissimilatory sulfate-reduction (in f_JAFGIB01) for energy acquisition. We propose that predation and cellular differentiation represent a niche adaptation strategy that evolved circa 500 million years ago (Mya) in response to the rise of soil as a distinct habitat on Earth. IMPORTANCE The phylum Myxococcota is a phylogenetically coherent bacterial lineage that exhibits unique social traits. Cultured Myxococcota are predominantly aerobic soil-dwelling microorganisms that are capable of predation and fruiting body formation. However, multiple yet-uncultured lineages within the Myxococcota have been encountered in a wide range of nonsoil, predominantly anaerobic habitats, and the metabolic capabilities, physiological preferences, and capacity of social behavior of such lineages remain unclear. Here, we analyzed genomes recovered from a metagenomic analysis of an anoxic freshwater spring in Oklahoma, USA, that represent novel, yet-uncultured, orders and families in the Myxococcota . The genomes appear to lack the characteristic hallmarks for social behavior encountered in Myxococcota genomes and displayed a significantly smaller genome size and a smaller number of genes encoding biosynthetic gene clusters, peptidases, signal transduction systems, and transcriptional regulators. Such perceived lack of social capacity was confirmed through detailed comparative genomic analysis of 13 pathways associated with Myxococcota social behavior, as well as the implementation of machine learning approaches to predict social behavior based on genome composition. Metabolically, these novel Myxococcota are predicted to be strict anaerobes, utilizing fermentation, nitrate reduction, and dissimilarity sulfate reduction for energy acquisition. Our results highlight the broad patterns of metabolic diversity within the yet-uncultured Myxococcota and suggest that the evolution of predation and fruiting body formation in the Myxococcota has occurred in response to soil formation as a distinct habitat on Earth.« less
Zumajo-Cardona, Cecilia; Pabón-Mora, Natalia; Ambrose, Barbara A(
, Molecular Biology and Evolution)
Purugganan, Michael
(Ed.)
Abstract The field of evolutionary developmental biology can help address how morphological novelties evolve, a key question in evolutionary biology. In Arabidopsis thaliana, APETALA2 (AP2) plays a role in the development of key plant innovations including seeds, flowers, and fruits. AP2 belongs to the AP2/ETHYLENE RESPONSIVE ELEMENT BINDING FACTOR family which has members in all viridiplantae, making it one of the oldest and most diverse gene lineages. One key subclade, present across vascular plants is the euAPETALA2 (euAP2) clade, whose founding member is AP2. We reconstructed the evolution of the euAP2 gene lineage in vascular plants to better understand itsmore »impact on the morphological evolution of plants, identifying seven major duplication events. We also performed spatiotemporal expression analyses of euAP2/TOE3 genes focusing on less explored vascular plant lineages, including ferns, gymnosperms, early diverging angiosperms and early diverging eudicots. Altogether, our data suggest that euAP2 genes originally contributed to spore and sporangium development, and were subsequently recruited to ovule, fruit and floral organ development. Finally, euAP2 protein sequences are highly conserved; therefore, changes in the role of euAP2 homologs during development are most likely due to changes in regulatory regions.« less
Abstract Although the seed is a key morphological innovation, its origin remains unknown and molecular data outside angiosperms is still limited. Ginkgo biloba, with a unique place in plant evolution, being one of the first extant gymnosperms where seeds evolved, can testify to the evolution and development of the seed. Initially, to better understand the development of the ovules in Ginkgo biloba ovules, we performed spatio-temporal expression analyses in seeds at early developing stages, of six candidate gene homologues known in angiosperms: WUSCHEL, AINTEGUMENTA, BELL1, KANADI, UNICORN, and C3HDZip . Surprisingly, the expression patterns of most these ovule homologues indicatemore »that they are not wholly conserved between angiosperms and Ginkgo biloba . Consistent with previous studies on early diverging seedless plant lineages, ferns, lycophytes, and bryophytes, many of these candidate genes are mainly expressed in mega- and micro-sporangia. Through in-depth comparative transcriptome analyses of Ginkgo biloba developing ovules, pollen cones, and megagametophytes we have been able to identify novel genes, likely involved in ovule development. Finally, our expression analyses support the synangial or neo-synangial hypotheses for the origin of the seed, where the sporangium developmental network was likely co-opted and restricted during integument evolution.« less
Mohanasundaram, Boominathan; Dodds, Audrey; Kukshal, Vandna; Jez, Joseph M; Pandey, Sona(
, Plant Physiology)
Abstract Heterotrimeric G-protein complexes comprising Gα-, Gβ-, and Gγ-subunits and the regulator of G-protein signaling (RGS) are conserved across most eukaryotic lineages. Signaling pathways mediated by these proteins influence overall growth, development, and physiology. In plants, this protein complex has been characterized primarily from angiosperms with the exception of spreading-leaved earth moss (Physcomitrium patens) and Chara braunii (charophytic algae). Even within angiosperms, specific G-protein components are missing in certain species, whereas unique plant-specific variants—the extra-large Gα (XLGα) and the cysteine-rich Gγ proteins—also exist. The distribution and evolutionary history of G-proteins and their function in nonangiosperm lineages remain mostly unknown. Wemore »explored this using the wealth of available sequence data spanning algae to angiosperms representing extant species that diverged approximately 1,500 million years ago, using BLAST, synteny analysis, and custom-built Hidden Markov Model profile searches. We show that a minimal set of components forming the XLGαβγ trimer exists in the entire land plant lineage, but their presence is sporadic in algae. Additionally, individual components have distinct evolutionary histories. The XLGα exhibits many lineage-specific gene duplications, whereas Gα and RGS show several instances of gene loss. Similarly, Gβ remained constant in both number and structure, but Gγ diverged before the emergence of land plants and underwent changes in protein domains, which led to three distinct subtypes. These results highlight the evolutionary oddities and summarize the phyletic patterns of this conserved signaling pathway in plants. They also provide a framework to formulate pertinent questions on plant G-protein signaling within an evolutionary context.« less
C. Silva, Mónica; Chibucos, Marcus; Munro, James B.; Daugherty, Sean; Coelho, M. Manuela; C. Silva, Joana(
, Scientific Reports)
Abstract
Olfactory receptors (ORs), encoded by the largest vertebrate multigene family, enable the detection of thousands of unique odorants in the environment and consequently play a critical role in species survival. Here, we advance our knowledge of OR gene evolution in procellariiform seabirds, an avian group which relies on the sense of olfaction for critical ecological functions. We built a cosmid library of Cory’s Shearwater (Calonectris borealis) genomic DNA, a model species for the study of olfaction-based navigation, and sequence OR gene-positive cosmid clones with a combination of sequencing technologies. We identified 220 OR open reading frames, 20 of whichmore »are full length, intact OR genes, and found a large ratio of partial and pseudogenes to intact OR genes (2:1), suggestive of a dynamic mode of evolution. Phylogenetic analyses revealed that while a few genes cluster with those of other sauropsid species in aγ(gamma) clade that predates the divergence of different avian lineages, most genes belong to an avian-specificγ-c clade, within which sequences cluster by species, suggesting frequent duplication and/or gene conversion events. We identified evidence of positive selection on full lengthγ-c clade genes. These patterns are consistent with a key role of adaptation in the functional diversification of olfactory receptor genes in a bird lineage that relies extensively on olfaction.
Povilus, Rebecca A., DaCosta, Jeffrey M., Grassa, Christopher, Satyaki, Prasad R. V., Moeglein, Morgan, Jaenisch, Johan, Xi, Zhenxiang, Mathews, Sarah, Gehring, Mary, Davis, Charles C., and Friedman, William E. Water lily ( Nymphaea thermarum ) genome reveals variable genomic signatures of ancient vascular cambium losses. Proceedings of the National Academy of Sciences 117.15 Web. doi:10.1073/pnas.1922873117.
Povilus, Rebecca A., DaCosta, Jeffrey M., Grassa, Christopher, Satyaki, Prasad R. V., Moeglein, Morgan, Jaenisch, Johan, Xi, Zhenxiang, Mathews, Sarah, Gehring, Mary, Davis, Charles C., & Friedman, William E. Water lily ( Nymphaea thermarum ) genome reveals variable genomic signatures of ancient vascular cambium losses. Proceedings of the National Academy of Sciences, 117 (15). https://doi.org/10.1073/pnas.1922873117
Povilus, Rebecca A., DaCosta, Jeffrey M., Grassa, Christopher, Satyaki, Prasad R. V., Moeglein, Morgan, Jaenisch, Johan, Xi, Zhenxiang, Mathews, Sarah, Gehring, Mary, Davis, Charles C., and Friedman, William E.
"Water lily ( Nymphaea thermarum ) genome reveals variable genomic signatures of ancient vascular cambium losses". Proceedings of the National Academy of Sciences 117 (15). Country unknown/Code not available: Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1922873117.https://par.nsf.gov/biblio/10142453.
@article{osti_10142453,
place = {Country unknown/Code not available},
title = {Water lily ( Nymphaea thermarum ) genome reveals variable genomic signatures of ancient vascular cambium losses},
url = {https://par.nsf.gov/biblio/10142453},
DOI = {10.1073/pnas.1922873117},
abstractNote = {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 lilyNymphaea 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 andNelumbo). This revealed lineage-specific patterns of gene loss and divergence.Nymphaeais characterized by a significant contraction of the HD-ZIP III transcription factors, specifically loss ofREVOLUTA, which influences cambial activity in other angiosperms. We also found theNymphaeaand monocot copies of cambium-associated CLE signaling peptides display unique substitutions at otherwise highly conserved amino acids.Nelumbodisplays 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.},
journal = {Proceedings of the National Academy of Sciences},
volume = {117},
number = {15},
publisher = {Proceedings of the National Academy of Sciences},
author = {Povilus, Rebecca A. and DaCosta, Jeffrey M. and Grassa, Christopher and Satyaki, Prasad R. V. and Moeglein, Morgan and Jaenisch, Johan and Xi, Zhenxiang and Mathews, Sarah and Gehring, Mary and Davis, Charles C. and Friedman, William E.},
}
