The Occurrence of the Holometabolous Pupal Stage Requires the Interaction between E93, Krüppel-Homolog 1 and Broad-Complex.

Abstract:

:Complete metamorphosis (Holometaboly) is a key innovation that underlies the spectacular success of holometabolous insects. Phylogenetic analyses indicate that Holometabola form a monophyletic group that evolved from ancestors exhibiting hemimetabolous development (Hemimetaboly). However, the nature of the changes underlying this crucial transition, including the occurrence of the holometabolan-specific pupal stage, is poorly understood. Using the holometabolous beetle Tribolium castaneum as a model insect, here we show that the transient up-regulation of the anti-metamorphic Krüppel-homolog 1 (TcKr-h1) gene at the end of the last larval instar is critical in the formation of the pupa. We find that depletion of this specific TcKr-h1 peak leads to the precocious up-regulation of the adult-specifier factor TcE93 and, hence, to a direct transformation of the larva into the adult form, bypassing the pupal stage. Moreover, we also find that the TcKr-h1-dependent repression of TcE93 is critical to allow the strong up-regulation of Broad-complex (TcBr-C), a key transcription factor that regulates the correct formation of the pupa in holometabolous insects. Notably, we show that the genetic interaction between Kr-h1 and E93 is also present in the penultimate nymphal instar of the hemimetabolous insect Blattella germanica, suggesting that the evolution of the pupa has been facilitated by the co-option of regulatory mechanisms present in hemimetabolan metamorphosis. Our findings, therefore, contribute to the molecular understanding of insect metamorphosis, and indicate the evolutionary conservation of the genetic circuitry that controls hemimetabolan and holometabolan metamorphosis, thereby shedding light on the evolution of complete metamorphosis.

journal_name

PLoS Genet

journal_title

PLoS genetics

authors

Ureña E,Chafino S,Manjón C,Franch-Marro X,Martín D

doi

10.1371/journal.pgen.1006020

subject

Has Abstract

pub_date

2016-05-02 00:00:00

pages

e1006020

issue

5

eissn

1553-7390

issn

1553-7404

pii

PGENETICS-D-15-02633

journal_volume

12

pub_type

杂志文章
  • Time dependent genetic analysis links field and controlled environment phenotypes in the model C4 grass Setaria.

    abstract::Vertical growth of plants is a dynamic process that is influenced by genetic and environmental factors and has a pronounced effect on overall plant architecture and biomass composition. We have performed six controlled growth trials of an interspecific Setaria italica x Setaria viridis recombinant inbred line populati...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1006841

    authors: Feldman MJ,Paul RE,Banan D,Barrett JF,Sebastian J,Yee MC,Jiang H,Lipka AE,Brutnell TP,Dinneny JR,Leakey ADB,Baxter I

    更新日期:2017-06-23 00:00:00

  • Genomic variation predicts adaptive evolutionary responses better than population bottleneck history.

    abstract::The relationship between population size, inbreeding, loss of genetic variation and evolutionary potential of fitness traits is still unresolved, and large-scale empirical studies testing theoretical expectations are surprisingly scarce. Here we present a highly replicated experimental evolution setup with 120 lines o...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1008205

    authors: Ørsted M,Hoffmann AA,Sverrisdóttir E,Nielsen KL,Kristensen TN

    更新日期:2019-06-12 00:00:00

  • Molecular basis of hemoglobin adaptation in the high-flying bar-headed goose.

    abstract::During the adaptive evolution of a particular trait, some selectively fixed mutations may be directly causative and others may be purely compensatory. The relative contribution of these two classes of mutation to adaptive phenotypic evolution depends on the form and prevalence of mutational pleiotropy. To investigate ...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1007331

    authors: Natarajan C,Jendroszek A,Kumar A,Weber RE,Tame JRH,Fago A,Storz JF

    更新日期:2018-04-02 00:00:00

  • High-throughput phenotypic characterization of Pseudomonas aeruginosa membrane transport genes.

    abstract::The deluge of data generated by genome sequencing has led to an increasing reliance on bioinformatic predictions, since the traditional experimental approach of characterizing gene function one at a time cannot possibly keep pace with the sequence-based discovery of novel genes. We have utilized Biolog phenotype Micro...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1000211

    authors: Johnson DA,Tetu SG,Phillippy K,Chen J,Ren Q,Paulsen IT

    更新日期:2008-10-03 00:00:00

  • Metabolites of lactic acid bacteria present in fermented foods are highly potent agonists of human hydroxycarboxylic acid receptor 3.

    abstract::The interplay of microbiota and the human host is physiologically crucial in health and diseases. The beneficial effects of lactic acid bacteria (LAB), permanently colonizing the human intestine or transiently obtained from food, have been extensively reported. However, the molecular understanding of how LAB modulate ...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1008145

    authors: Peters A,Krumbholz P,Jäger E,Heintz-Buschart A,Çakir MV,Rothemund S,Gaudl A,Ceglarek U,Schöneberg T,Stäubert C

    更新日期:2019-05-23 00:00:00

  • Pre-mRNA secondary structures influence exon recognition.

    abstract::The secondary structure of a pre-mRNA influences a number of processing steps including alternative splicing. Since most splicing regulatory proteins bind to single-stranded RNA, the sequestration of RNA into double strands could prevent their binding. Here, we analyzed the secondary structure context of experimentall...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.0030204

    authors: Hiller M,Zhang Z,Backofen R,Stamm S

    更新日期:2007-11-01 00:00:00

  • Mismatch repair balances leading and lagging strand DNA replication fidelity.

    abstract::The two DNA strands of the nuclear genome are replicated asymmetrically using three DNA polymerases, α, δ, and ε. Current evidence suggests that DNA polymerase ε (Pol ε) is the primary leading strand replicase, whereas Pols α and δ primarily perform lagging strand replication. The fact that these polymerases differ in...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1003016

    authors: Lujan SA,Williams JS,Pursell ZF,Abdulovic-Cui AA,Clark AB,Nick McElhinny SA,Kunkel TA

    更新日期:2012-01-01 00:00:00

  • Loss of hepatocyte cell division leads to liver inflammation and fibrosis.

    abstract::The liver possesses a remarkable regenerative capacity based partly on the ability of hepatocytes to re-enter the cell cycle and divide to replace damaged cells. This capability is substantially reduced upon chronic damage, but it is not clear if this is a cause or consequence of liver disease. Here, we investigate wh...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1009084

    authors: Dewhurst MR,Ow JR,Zafer G,van Hul NKM,Wollmann H,Bisteau X,Brough D,Choi H,Kaldis P

    更新日期:2020-11-04 00:00:00

  • Developmental transcriptional networks are required to maintain neuronal subtype identity in the mature nervous system.

    abstract::During neurogenesis, transcription factors combinatorially specify neuronal fates and then differentiate subtype identities by inducing subtype-specific gene expression profiles. But how is neuronal subtype identity maintained in mature neurons? Modeling this question in two Drosophila neuronal subtypes (Tv1 and Tv4),...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1002501

    authors: Eade KT,Fancher HA,Ridyard MS,Allan DW

    更新日期:2012-01-01 00:00:00

  • Interplay between mitochondria and diet mediates pathogen and stress resistance in Caenorhabditis elegans.

    abstract::Diet is a crucial determinant of organismal biology; interactions between the host, its diet, and its microbiota are critical to determining the health of an organism. A variety of genetic and biochemical means were used to assay stress sensitivity in C. elegans reared on two standard laboratory diets: E. coli OP50, t...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1008011

    authors: Revtovich AV,Lee R,Kirienko NV

    更新日期:2019-03-13 00:00:00

  • Two modes of transvection at the eyes absent gene of Drosophila demonstrate plasticity in transcriptional regulatory interactions in cis and in trans.

    abstract::For many genes, proper gene expression requires coordinated and dynamic interactions between multiple regulatory elements, each of which can either promote or silence transcription. In Drosophila, the complexity of the regulatory landscape is further complicated by the tight physical pairing of homologous chromosomes,...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1008152

    authors: Tian K,Henderson RE,Parker R,Brown A,Johnson JE,Bateman JR

    更新日期:2019-05-10 00:00:00

  • Coronary artery disease genes SMAD3 and TCF21 promote opposing interactive genetic programs that regulate smooth muscle cell differentiation and disease risk.

    abstract::Although numerous genetic loci have been associated with coronary artery disease (CAD) with genome wide association studies, efforts are needed to identify the causal genes in these loci and link them into fundamental signaling pathways. Recent studies have investigated the disease mechanism of CAD associated gene SMA...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1007681

    authors: Iyer D,Zhao Q,Wirka R,Naravane A,Nguyen T,Liu B,Nagao M,Cheng P,Miller CL,Kim JB,Pjanic M,Quertermous T

    更新日期:2018-10-11 00:00:00

  • The ABI4-induced Arabidopsis ANAC060 transcription factor attenuates ABA signaling and renders seedlings sugar insensitive when present in the nucleus.

    abstract::Seedling establishment is inhibited on media containing high levels (∼ 6%) of glucose or fructose. Genetic loci that overcome the inhibition of seedling growth on high sugar have been identified using natural variation analysis and mutant selection, providing insight into sugar signaling pathways. In this study, a qua...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1004213

    authors: Li P,Zhou H,Shi X,Yu B,Zhou Y,Chen S,Wang Y,Peng Y,Meyer RC,Smeekens SC,Teng S

    更新日期:2014-03-13 00:00:00

  • Cellular variability of RpoS expression underlies subpopulation activation of an integrative and conjugative element.

    abstract::Conjugative transfer of the integrative and conjugative element ICEclc in the bacterium Pseudomonas knackmussii is the consequence of a bistable decision taken in some 3% of cells in a population during stationary phase. Here we study the possible control exerted by the stationary phase sigma factor RpoS on the bistab...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1002818

    authors: Miyazaki R,Minoia M,Pradervand N,Sulser S,Reinhard F,van der Meer JR

    更新日期:2012-01-01 00:00:00

  • Correction: Pleiotropic Mechanisms Indicated for Sex Differences in Autism.

    abstract::[This corrects the article DOI: 10.1371/journal.pgen.1006425.]. ...

    journal_title:PLoS genetics

    pub_type: 杂志文章,已发布勘误

    doi:10.1371/journal.pgen.1006831

    authors: Mitra I,Tsang K,Ladd-Acosta C,Croen LA,Aldinger KA,Hendren RL,Traglia M,Lavillaureix A,Zaitlen N,Oldham MC,Levitt P,Nelson S,Amaral DG,Hertz-Picciotto I,Fallin MD,Weiss LA

    更新日期:2017-06-07 00:00:00

  • Genome-wide physical activity interactions in adiposity - A meta-analysis of 200,452 adults.

    abstract::Physical activity (PA) may modify the genetic effects that give rise to increased risk of obesity. To identify adiposity loci whose effects are modified by PA, we performed genome-wide interaction meta-analyses of BMI and BMI-adjusted waist circumference and waist-hip ratio from up to 200,452 adults of European (n = 1...

    journal_title:PLoS genetics

    pub_type: 杂志文章,meta分析

    doi:10.1371/journal.pgen.1006528

    authors: Graff M,Scott RA,Justice AE,Young KL,Feitosa MF,Barata L,Winkler TW,Chu AY,Mahajan A,Hadley D,Xue L,Workalemahu T,Heard-Costa NL,den Hoed M,Ahluwalia TS,Qi Q,Ngwa JS,Renström F,Quaye L,Eicher JD,Hayes JE,Corneli

    更新日期:2017-04-27 00:00:00

  • Inflammation-mediated genetic and epigenetic alterations drive cancer development in the neighboring epithelium upon stromal abrogation of TGF-β signaling.

    abstract::Deletion of tumor suppressor genes in stromal fibroblasts induces epithelial cancer development, suggesting an important role of stroma in epithelial homoeostasis. However, the underlying mechanisms remain to be elucidated. Here we report that deletion of the gene encoding TGFβ receptor 2 (Tgfbr2) in the stromal fibro...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1003251

    authors: Achyut BR,Bader DA,Robles AI,Wangsa D,Harris CC,Ried T,Yang L

    更新日期:2013-01-01 00:00:00

  • Specificity of the STAT4 genetic association for severe disease manifestations of systemic lupus erythematosus.

    abstract::Systemic lupus erythematosus (SLE) is a genetically complex disease with heterogeneous clinical manifestations. A polymorphism in the STAT4 gene has recently been established as a risk factor for SLE, but the relationship with specific SLE subphenotypes has not been studied. We studied 137 SNPs in the STAT4 region gen...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1000084

    authors: Taylor KE,Remmers EF,Lee AT,Ortmann WA,Plenge RM,Tian C,Chung SA,Nititham J,Hom G,Kao AH,Demirci FY,Kamboh MI,Petri M,Manzi S,Kastner DL,Seldin MF,Gregersen PK,Behrens TW,Criswell LA

    更新日期:2008-05-30 00:00:00

  • SAS-1 is a C2 domain protein critical for centriole integrity in C. elegans.

    abstract::Centrioles are microtubule-based organelles important for the formation of cilia, flagella and centrosomes. Despite progress in understanding the underlying assembly mechanisms, how centriole integrity is ensured is incompletely understood, including in sperm cells, where such integrity is particularly critical. We id...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1004777

    authors: von Tobel L,Mikeladze-Dvali T,Delattre M,Balestra FR,Blanchoud S,Finger S,Knott G,Müller-Reichert T,Gönczy P

    更新日期:2014-11-20 00:00:00

  • Pedigree- and SNP-Associated Genetics and Recent Environment are the Major Contributors to Anthropometric and Cardiometabolic Trait Variation.

    abstract::Genome-wide association studies have successfully identified thousands of loci for a range of human complex traits and diseases. The proportion of phenotypic variance explained by significant associations is, however, limited. Given the same dense SNP panels, mixed model analyses capture a greater proportion of phenot...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1005804

    authors: Xia C,Amador C,Huffman J,Trochet H,Campbell A,Porteous D,Generation Scotland.,Hastie ND,Hayward C,Vitart V,Navarro P,Haley CS

    更新日期:2016-02-02 00:00:00

  • HSPB7 prevents cardiac conduction system defect through maintaining intercalated disc integrity.

    abstract::HSPB7 is a member of the small heat-shock protein (HSPB) family and is expressed in the cardiomyocytes from cardiogenesis onwards. A dramatic increase in HSPB7 is detected in the heart and blood plasma immediately after myocardial infarction. Additionally, several single-nucleotide polymorphisms of HSPB7 have been ide...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1006984

    authors: Liao WC,Juo LY,Shih YL,Chen YH,Yan YT

    更新日期:2017-08-21 00:00:00

  • New insight into bacterial social communication in natural host: Evidence for interplay of heterogeneous and unison quorum response.

    abstract::Many microbes exhibit quorum sensing (QS) to cooperate, share and perform a social task in unison. Recent studies have shown the emergence of reversible phenotypic heterogeneity in the QS-responding pathogenic microbial population under laboratory conditions as a possible bet-hedging survival strategy. However, very l...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1008395

    authors: Samal B,Chatterjee S

    更新日期:2019-09-17 00:00:00

  • The genetic architecture of the genome-wide transcriptional response to ER stress in the mouse.

    abstract::Endoplasmic reticulum (ER) stress occurs when misfolded proteins accumulate in the ER. The cellular response to ER stress involves complex transcriptional and translational changes, important to the survival of the cell. ER stress is a primary cause and a modifier of many human diseases. A first step to understanding ...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1004924

    authors: Chow CY,Wang X,Riccardi D,Wolfner MF,Clark AG

    更新日期:2015-02-04 00:00:00

  • An estimator of first coalescent time reveals selection on young variants and large heterogeneity in rare allele ages among human populations.

    abstract::Allele age has long been a focus of population genetic research, primarily because it can be an important clue to the fitness effects of an allele. By virtue of their effects on fitness, alleles under directional selection are expected to be younger than neutral alleles of the same frequency. We developed a new coales...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1008340

    authors: Platt A,Pivirotto A,Knoblauch J,Hey J

    更新日期:2019-08-19 00:00:00

  • Oxidative stress and replication-independent DNA breakage induced by arsenic in Saccharomyces cerevisiae.

    abstract::Arsenic is a well-established human carcinogen of poorly understood mechanism of genotoxicity. It is generally accepted that arsenic acts indirectly by generating oxidative DNA damage that can be converted to replication-dependent DNA double-strand breaks (DSBs), as well as by interfering with DNA repair pathways and ...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1003640

    authors: Litwin I,Bocer T,Dziadkowiec D,Wysocki R

    更新日期:2013-01-01 00:00:00

  • Genomic analysis of natural selection and phenotypic variation in high-altitude mongolians.

    abstract::Deedu (DU) Mongolians, who migrated from the Mongolian steppes to the Qinghai-Tibetan Plateau approximately 500 years ago, are challenged by environmental conditions similar to native Tibetan highlanders. Identification of adaptive genetic factors in this population could provide insight into coordinated physiological...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1003634

    authors: Xing J,Wuren T,Simonson TS,Watkins WS,Witherspoon DJ,Wu W,Qin G,Huff CD,Jorde LB,Ge RL

    更新日期:2013-01-01 00:00:00

  • Tempo and mode in evolution of transcriptional regulation.

    abstract::Perennial questions of evolutionary biology can be applied to gene regulatory systems using the abundance of experimental data addressing gene regulation in a comparative context. What is the tempo (frequency, rate) and mode (way, mechanism) of transcriptional regulatory evolution? Here we synthesize the results of 23...

    journal_title:PLoS genetics

    pub_type: 杂志文章,评审

    doi:10.1371/journal.pgen.1002432

    authors: Gordon KL,Ruvinsky I

    更新日期:2012-01-01 00:00:00

  • Allele-specific virulence attenuation of the Pseudomonas syringae HopZ1a type III effector via the Arabidopsis ZAR1 resistance protein.

    abstract::Plant resistance (R) proteins provide a robust surveillance system to defend against potential pathogens. Despite their importance in plant innate immunity, relatively few of the approximately 170 R proteins in Arabidopsis have well-characterized resistance specificity. In order to identify the R protein responsible f...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1000894

    authors: Lewis JD,Wu R,Guttman DS,Desveaux D

    更新日期:2010-04-01 00:00:00

  • PCNA ubiquitylation ensures timely completion of unperturbed DNA replication in fission yeast.

    abstract::PCNA ubiquitylation on lysine 164 is required for DNA damage tolerance. In many organisms PCNA is also ubiquitylated in unchallenged S phase but the significance of this has not been established. Using Schizosaccharomyces pombe, we demonstrate that lysine 164 ubiquitylation of PCNA contributes to efficient DNA replica...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1006789

    authors: Daigaku Y,Etheridge TJ,Nakazawa Y,Nakayama M,Watson AT,Miyabe I,Ogi T,Osborne MA,Carr AM

    更新日期:2017-05-08 00:00:00

  • A yeast GSK-3 kinase Mck1 promotes Cdc6 degradation to inhibit DNA re-replication.

    abstract::Cdc6p is an essential component of the pre-replicative complex (pre-RC), which binds to DNA replication origins to promote initiation of DNA replication. Only once per cell cycle does DNA replication take place. After initiation, the pre-RC components are disassembled in order to prevent re-replication. It has been sh...

    journal_title:PLoS genetics

    pub_type: 杂志文章

    doi:10.1371/journal.pgen.1003099

    authors: Ikui AE,Rossio V,Schroeder L,Yoshida S

    更新日期:2012-01-01 00:00:00