Holding it together: rapid evolution and positive selection in the synaptonemal complex of Drosophila

ABSTRACT Plant pathogens utilize a portfolio of secreted effectors to successfully infect and manipulate their hosts. It is, however, still unclear whether changes in secretomes leading to host specialization involve mostly effector gene gains/losses or changes in their sequences. To test these hypotheses, we compared the secretomes of three host-specific castrating anther smut fungi (Microbotryum), two being sister species. To address within-species evolution, which might involve coevolution and local adaptation, we compared the secretomes of strains from differentiated populations. We experimentally validated a subset of signal peptides. Secretomes ranged from 321 to 445 predicted secreted proteins (SPs), including a few species-specific proteins (42 to 75), and limited copy number variation, i.e., little gene family expansion or reduction. Between 52% and 68% of the SPs did not match any Pfam domain, a percentage that reached 80% for the small secreted proteins, indicating rapid evolution. In comparison to background genes, we indeed found SPs to be more differentiated among species and strains, more often under positive selection, and highly expressed in planta; repeat-induced point mutations (RIPs) had no role in effector diversification, as SPs were not closer to transposable elements than background genes and were not more RIP affected. Our study thus identified both conserved core proteins, likely required for the pathogenic life cycle of all Microbotryum species, and proteins that were species specific or evolving under positive selection; these proteins may be involved in host specialization and/or coevolution. Most changes among closely related host-specific pathogens, however, involved rapid changes in sequences rather than gene gains/losses. IMPORTANCE Plant pathogens use molecular weapons to successfully infect their hosts, secreting a large portfolio of various proteins and enzymes. Different plant species are often parasitized by host-specific pathogens; however, it is still unclear whether the molecular basis of such host specialization involves species-specific weapons or different variants of the same weapons. We therefore compared the genes encoding secreted proteins in three plant-castrating pathogens parasitizing different host plants, producing their spores in plant anthers by replacing pollen. We validated our predictions for secretion signals for some genes and checked that our predicted secreted proteins were often highly expressed during plant infection. While we found few species-specific secreted proteins, numerous genes encoding secreted proteins showed signs of rapid evolution and of natural selection. Our study thus found that most changes among closely related host-specific pathogens involved rapid adaptive changes in shared molecular weapons rather than innovations for new weapons.

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Rapid Evolution by Positive Selection and Gene Gain and Loss: PLA2 Venom Genes in Closely Related Sistrurus Rattlesnakes with Divergent Diets

Journal of Molecular Evolution ◽

10.1007/s00239-008-9067-7 ◽

2008 ◽

Vol 66 (2) ◽

pp. 151-166 ◽

Cited By ~ 74

Author(s):

H. Lisle Gibbs ◽

Wayne Rossiter

Keyword(s):

Positive Selection ◽

Rapid Evolution ◽

Gene Gain ◽

Gain And Loss

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Conflicts with diarrheal pathogens trigger rapid evolution of an intestinal signaling axis

10.1101/2020.03.29.014761 ◽

2020 ◽

Author(s):

Clayton M. Carey ◽

Sarah E. Apple ◽

Zoё A. Hilbert ◽

Michael S. Kay ◽

Nels C. Elde

Keyword(s):

Positive Selection ◽

Rapid Evolution ◽

Genetic Conflict ◽

Selective Pressures ◽

Heat Stable ◽

Guanylate Cyclase C ◽

Signaling Axis ◽

History Of ◽

Water Secretion

AbstractThe pathogenesis of infectious diarrheal diseases is largely attributed to enterotoxin proteins that disrupt intestinal water absorption, causing severe dehydration. Despite profound health consequences, the impacts of diarrhea-causing microbes on the evolutionary history of host species are largely unknown. We investigated patterns of genetic variation in mammalian Guanylate Cyclase-C (GC-C), an intestinal receptor frequently targeted by bacterial enterotoxins, to determine how hosts might adapt in response to diarrheal infections. Under normal conditions, GC-C interacts with endogenous guanylin peptides to promote water secretion in the intestine, but signaling can be hijacked by bacterially-encoded heat-stable enterotoxins (STa) during infection, which leads to overstimulation of GC-C and diarrhea. Phylogenetic analysis in mammals revealed evidence of recurrent positive selection in the GC-C ligand-binding domain in primates and bats, consistent with selective pressures to evade interactions with STa. Using in vitro assays and transgenic intestinal organoids to model STa-mediated diarrhea, we show that GC-C diversification in these lineages results in substantial variation in toxin susceptibility. In bats, we observe a unique pattern of compensatory coevolution in the endogenous GC-C ligand uroguanylin, reflecting intense bouts of positive selection at the receptor-ligand interface. These findings demonstrate control of water physiology as a previously unrecognized interface for genetic conflict and reveal diarrheal pathogens as a source of selective pressure among diverse mammals.

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Rapid Evolution of Plethodontid Modulating Factor, a Hypervariable Salamander Courtship Pheromone, is Driven by Positive Selection

Journal of Molecular Evolution ◽

10.1007/s00239-010-9342-2 ◽

2010 ◽

Vol 70 (5) ◽

pp. 427-440 ◽

Cited By ~ 26

Author(s):

Catherine A. Palmer ◽

Richard A. Watts ◽

Amy P. Hastings ◽

Lynne D. Houck ◽

Stevan J. Arnold

Keyword(s):

Positive Selection ◽

Rapid Evolution ◽

Courtship Pheromone

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The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors

eLife ◽

10.7554/elife.21455 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 69

Author(s):

Ofer Rog ◽

Simone Köhler ◽

Abby F Dernburg

Keyword(s):

Signal Transduction ◽

Synaptonemal Complex ◽

Meiotic Recombination ◽

Liquid Crystalline ◽

Hydrophobic Interactions ◽

Rapid Evolution ◽

Three Dimensional ◽

Homologous Chromosomes ◽

Meiotic Progression ◽

Meiotic Chromosomes

The synaptonemal complex (SC) is a polymer that spans ~100 nm between paired homologous chromosomes during meiosis. Its striated, periodic appearance in electron micrographs led to the idea that transverse filaments within this structure ‘crosslink’ the axes of homologous chromosomes, stabilizing their pairing. SC proteins can also form polycomplexes, three-dimensional lattices that recapitulate the periodic structure of SCs but do not associate with chromosomes. Here we provide evidence that SCs and polycomplexes contain mobile subunits and that their assembly is promoted by weak hydrophobic interactions, indicative of a liquid crystalline phase. We further show that in the absence of recombination intermediates, polycomplexes recapitulate the dynamic localization of pro-crossover factors during meiotic progression, revealing how the SC might act as a conduit to regulate chromosome-wide crossover distribution. Properties unique to liquid crystals likely enable long-range signal transduction along meiotic chromosomes and underlie the rapid evolution of SC proteins.

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Adaptation Insights from Comparative Transcriptome Analysis of Two Opisthopappus Species in the Taihang Mountains

10.21203/rs.3.rs-1023687/v1 ◽

2021 ◽

Author(s):

Ning Chen ◽

Hao Zhang ◽

En Zang ◽

Zhi-Xia Liu ◽

Ya-Fei Lan ◽

...

Keyword(s):

Comparative Analysis ◽

Positive Selection ◽

Molecular Mechanisms ◽

Rapid Evolution ◽

Model Systems ◽

Perennial Herb ◽

Starch Degradation ◽

Adaptive Divergence ◽

Nucleotide Synthesis ◽

Opisthopappus Taihangensis

Abstract Opisthopappus is a major wild source of Asteraceae with good cold and drought resistance. Two species of this genus (Opisthopappus taihangensis and Opisthopappus longilobus) have been employed as model systems to address the evolutionary history of perennial herb biomes in the Taihang Mountains of China. However, further studies on the adaptive divergence processes of these two species are currently impeded by the lack of genomic resources. To elucidate the molecular mechanisms involved, a comparative analysis of these two species was conducted. Among the identified transcription factors, the bHLH members were most prevalent, which exhibited significantly different expression levels in the terpenoid metabolic pathway. O. longilobus revealed a higher expression than did O. taihangensis in terms of terpenes biosynthesis and metabolism, particularly regarding monoterpenoids and diterpenoids. Analyses of the positive selection genes (PSGs) identified from O. taihangensis and O. longilobus, 1203 genes were found that related to adaptative divergence, which were under rapid evolution and/or have signs of positive selection. Different PSG expressions occurred primarily in the mitochondrial electron transport, starch degradation, secondary metabolism, as well as nucleotide synthesis and S-metabolism pathway processes. Two PSGs were obviously differentially expressed in terpenes biosynthesis that might result in the fragrances divergence between O. longilobus and O. taihangensis, which would provide insights as to how the two species adapted to different environments, characterized by sub-humid warm temperate and temperate continental monsoon climates. The comparative analysis for these two species of Opisthopappus not only revealed how the divergence occurred from molecular perspective, but also provided novel insights into how differential adaptations occurred in Taihang Mountains.

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Tissue-specific transcriptome for Poeciliopsis prolifica reveals evidence for genetic adaptation related to the evolution of a placental fish

10.1101/289488 ◽

2018 ◽

Author(s):

Nathaniel K. Jue ◽

Robert J. Foley ◽

David N. Reznick ◽

Rachel J. O’Neill ◽

Michael J. O’Neill

Keyword(s):

Positive Selection ◽

Rapid Evolution ◽

Duplication Event ◽

Detailed Examination ◽

Sequence Evolution ◽

Genome Duplication Event ◽

Genetic Components ◽

Maternal Provisioning ◽

Stage Embryo ◽

Adaptive Complexity

ABSTRACTThe evolution of the placenta is an excellent model to examine the evolutionary processes underlying adaptive complexity due to the recent, independent derivation of placentation in divergent animal lineages. In fishes, the family Poeciliidae offers the opportunity to study placental evolution with respect to variation in degree of post-fertilization maternal provisioning among closely related sister species. In this study, we present a detailed examination of a new reference transcriptome sequence for the live-bearing, matrotrophic fish, Poeciliopsis prolifica, from multiple-tissue RNA-seq data. We describe the genetic components active in liver, brain, late-stage embryo, and the maternal placental/ovarian complex, as well as associated patterns of positive selection in a suite of orthologous genes found in fishes. Results indicate the expression of many signaling transcripts, “non-coding” sequences and repetitive elements in the maternal placental/ovarian complex. Moreover, patterns of positive selection in protein sequence evolution were found associated with live-bearing fishes, generally, and the placental P. prolifica, specifically, that appear independent of the general live-bearer lifestyle. Much of the observed patterns of gene expression and positive selection are congruent with the evolution of placentation in fish functionally converging with mammalian placental evolution and with the patterns of rapid evolution facilitated by the teleost-specific whole genome duplication event.

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Innovation of heterochromatin functions drives rapid evolution of essential ZAD-ZNF genes in Drosophila

10.1101/2020.07.08.192740 ◽

2020 ◽

Cited By ~ 1

Author(s):

Bhavatharini Kasinathan ◽

Serafin U. Colmenares ◽

Hannah McConnell ◽

Janet M. Young ◽

Gary H. Karpen ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Transcription Factors ◽

Positive Selection ◽

Larval Development ◽

Rapid Evolution ◽

Strong Positive Selection ◽

General Explanation

AbstractContrary to prevailing dogma, evolutionarily young and dynamic genes can encode essential functions. Here, we investigate genetic innovation in ZAD-ZNF genes, which encode the most abundant class of insect transcription factors. We find that evolutionarily dynamic ZAD-ZNF genes are more likely to encode essential functions in Drosophila melanogaster than ancient, conserved ZAD-ZNF genes. To understand the basis of this unexpected correlation, we focus on the Nicknack ZAD-ZNF gene. Nicknack is an evolutionarily young, poorly retained in Drosophila species, and evolves under strong positive selection, yet we find that it is necessary for larval development in D. melanogaster. We show that Nicknack encodes a heterochromatin-localizing protein like its closely related paralog Oddjob, also an evolutionarily dynamic, essential ZAD-ZNF gene. We find that the divergent D. simulans Nicknack protein can still localize to D. melanogaster heterochromatin and rescue viability of female but not male Nicknack-null D. melanogaster. Our findings suggest that innovation for rapidly changing heterochromatin functions might provide a general explanation for the essential functions of many evolutionarily dynamic ZAD-ZNF genes in insects.

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The Vertebrate TLR Supergene Family Evolved Dynamically by Gene Gain/Loss and Positive Selection Revealing a Host–Pathogen Arms Race in Birds

Diversity ◽

10.3390/d11080131 ◽

2019 ◽

Vol 11 (8) ◽

pp. 131 ◽

Cited By ~ 4

Author(s):

Imran Khan ◽

Emanuel Maldonado ◽

Liliana Silva ◽

Daniela Almeida ◽

Warren E. Johnson ◽

...

Keyword(s):

Positive Selection ◽

Rapid Evolution ◽

Immune Defense ◽

Arms Race ◽

Gene Gain ◽

Toll Like Receptor ◽

Viral Pathogens ◽

Host Pathogen ◽

Gain Loss ◽

Supergene Family

The vertebrate toll-like receptor (TLRs) supergene family is a first-line immune defense against viral and non-viral pathogens. Here, comparative evolutionary-genomics of 79 vertebrate species (8 mammals, 48 birds, 11 reptiles, 1 amphibian, and 11 fishes) revealed differential gain/loss of 26 TLRs, including 6 (TLR3, TLR7, TLR8, TLR14, TLR21, and TLR22) that originated early in vertebrate evolution before the diversification of Agnatha and Gnathostomata. Subsequent dynamic gene gain/loss led to lineage-specific diversification with TLR repertoires ranging from 8 subfamilies in birds to 20 in fishes. Lineage-specific loss of TLR8-9 and TLR13 in birds and gains of TLR6 and TLR10-12 in mammals and TLR19-20 and TLR23-27 in fishes. Among avian species, 5–10% of the sites were under positive selection (PS) (omega 1.5–2.5) with radical amino-acid changes likely affecting TLR structure/functionality. In non-viral TLR4 the 20 PS sites (posterior probability PP > 0.99) likely increased ability to cope with diversified ligands (e.g., lipopolysaccharide and lipoteichoic). For viral TLR7, 23 PS sites (PP > 0.99) possibly improved recognition of highly variable viral ssRNAs. Rapid evolution of the TLR supergene family reflects the host–pathogen arms race and the coevolution of ligands/receptors, which follows the premise that birds have been important vectors of zoonotic pathogens and reservoirs for viruses.

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Rapid evolution and biogeographic spread in a colorectal cancer

Nature Communications ◽

10.1038/s41467-019-12926-8 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 15

Author(s):

Joao M. Alves ◽

Sonia Prado-López ◽

José Manuel Cameselle-Teijeiro ◽

David Posada

Keyword(s):

Colorectal Cancer ◽

Lymph Nodes ◽

Positive Selection ◽

Rapid Evolution ◽

Population Expansion ◽

Metastatic Colonization ◽

Biogeographic History ◽

History Of ◽

Tumoral Cells ◽

Over Time

Abstract How and when tumoral clones start spreading to surrounding and distant tissues is currently unclear. Here we leveraged a model-based evolutionary framework to investigate the demographic and biogeographic history of a colorectal cancer. Our analyses strongly support an early monoclonal metastatic colonization, followed by a rapid population expansion at both primary and secondary sites. Moreover, we infer a hematogenous metastatic spread under positive selection, plus the return of some tumoral cells from the liver back to the colon lymph nodes. This study illustrates how sophisticated techniques typical of organismal evolution can provide a detailed, quantitative picture of the complex tumoral dynamics over time and space.

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