even-skipped acts as a pair-rule gene in germ band stages of Tribolium development

The pair-rule gene even-skipped (eve) is essential for insect segmentation, yet its function varies among insect clades. While loss of eve results in typical pair-rule phenotypes in Drosophila, knock-down of eve orthologs shows segmental, gap-like, or asegmental phenotypes in non-Drosophila insects....

Full description

Saved in:
Bibliographic Details
Published inDevelopmental biology Vol. 462; no. 1; pp. 1 - 6
Main Authors O, Jiyun, Choe, Chong Pyo
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.06.2020
Subjects
Online AccessGet full text

Cover

Loading…
Abstract The pair-rule gene even-skipped (eve) is essential for insect segmentation, yet its function varies among insect clades. While loss of eve results in typical pair-rule phenotypes in Drosophila, knock-down of eve orthologs shows segmental, gap-like, or asegmental phenotypes in non-Drosophila insects. In Tribolium, knock-down of the eve ortholog (Tc-eve) resulted in a graded phenotypic series ranging from strong to weak, the most informative of which was intermediate phenotypes. The strong knock-down embryos displayed asegmental phenotypes and severely disorganized germ bands which have prevented determination of Tc-eve function in later stages. In order to understand the segmentation function of Tc-eve during later germ band elongation stages, we analyzed intermediate Tc-eveRNAi embryos in which germ band elongation was less affected. Most intermediate Tc-eveRNAi germ bands displayed segmentation defects with a double segmental periodicity in the abdomen. In these intermediate embryos, Tc-engrailed (Tc-en) stripes were ectopically expanded into large bands with a double segmental periodicity, while the remaining Tc-en stripes between the expanded Tc-en stripes were absent or barely formed. The expanded Tc-en stripes seemed to be activated by primary Tc-eve stripes and Tc-paired, both of which failed to resolve into secondary segmental stripes. The absence of Tc-en stripes appeared to be a consequence of the absence of the secondary stripes of Tc-runt that were required for the activation of Tc-en stripes. These results suggest that Tc-eve functions as a pair-rule gene at least in the germ band stages of Tribolium development. •Injection of eve dsRNA causes pair-rule-like defects in Tribolium germ bands.•Primary eve stripes form in knockdown embryos but fail to resolve into segmental stripes.•Abnormal eve stripes lead to an expansion of en stripes with a double segmental periodicity.•Secondary stripes of the pair rule gene run are not maintained in the germ bands of knockdown embryos.•Absence of run stripes leads to a reduced number of en stripes.
AbstractList The pair-rule gene even-skipped (eve) is essential for insect segmentation, yet its function varies among insect clades. While loss of eve results in typical pair-rule phenotypes in Drosophila, knock-down of eve orthologs shows segmental, gap-like, or asegmental phenotypes in non-Drosophila insects. In Tribolium, knock-down of the eve ortholog (Tc-eve) resulted in a graded phenotypic series ranging from strong to weak, the most informative of which was intermediate phenotypes. The strong knock-down embryos displayed asegmental phenotypes and severely disorganized germ bands which have prevented determination of Tc-eve function in later stages. In order to understand the segmentation function of Tc-eve during later germ band elongation stages, we analyzed intermediate Tc-eveRNAi embryos in which germ band elongation was less affected. Most intermediate Tc-eveRNAi germ bands displayed segmentation defects with a double segmental periodicity in the abdomen. In these intermediate embryos, Tc-engrailed (Tc-en) stripes were ectopically expanded into large bands with a double segmental periodicity, while the remaining Tc-en stripes between the expanded Tc-en stripes were absent or barely formed. The expanded Tc-en stripes seemed to be activated by primary Tc-eve stripes and Tc-paired, both of which failed to resolve into secondary segmental stripes. The absence of Tc-en stripes appeared to be a consequence of the absence of the secondary stripes of Tc-runt that were required for the activation of Tc-en stripes. These results suggest that Tc-eve functions as a pair-rule gene at least in the germ band stages of Tribolium development. •Injection of eve dsRNA causes pair-rule-like defects in Tribolium germ bands.•Primary eve stripes form in knockdown embryos but fail to resolve into segmental stripes.•Abnormal eve stripes lead to an expansion of en stripes with a double segmental periodicity.•Secondary stripes of the pair rule gene run are not maintained in the germ bands of knockdown embryos.•Absence of run stripes leads to a reduced number of en stripes.
The pair-rule gene even-skipped (eve) is essential for insect segmentation, yet its function varies among insect clades. While loss of eve results in typical pair-rule phenotypes in Drosophila, knock-down of eve orthologs shows segmental, gap-like, or asegmental phenotypes in non-Drosophila insects. In Tribolium, knock-down of the eve ortholog (Tc-eve) resulted in a graded phenotypic series ranging from strong to weak, the most informative of which was intermediate phenotypes. The strong knock-down embryos displayed asegmental phenotypes and severely disorganized germ bands which have prevented determination of Tc-eve function in later stages. In order to understand the segmentation function of Tc-eve during later germ band elongation stages, we analyzed intermediate Tc-eve embryos in which germ band elongation was less affected. Most intermediate Tc-eve germ bands displayed segmentation defects with a double segmental periodicity in the abdomen. In these intermediate embryos, Tc-engrailed (Tc-en) stripes were ectopically expanded into large bands with a double segmental periodicity, while the remaining Tc-en stripes between the expanded Tc-en stripes were absent or barely formed. The expanded Tc-en stripes seemed to be activated by primary Tc-eve stripes and Tc-paired, both of which failed to resolve into secondary segmental stripes. The absence of Tc-en stripes appeared to be a consequence of the absence of the secondary stripes of Tc-runt that were required for the activation of Tc-en stripes. These results suggest that Tc-eve functions as a pair-rule gene at least in the germ band stages of Tribolium development.
Author Choe, Chong Pyo
O, Jiyun
Author_xml – sequence: 1
  givenname: Jiyun
  surname: O
  fullname: O, Jiyun
  organization: Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, South Korea
– sequence: 2
  givenname: Chong Pyo
  surname: Choe
  fullname: Choe, Chong Pyo
  email: cpchoe@gnu.ac.kr
  organization: Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, South Korea
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32179089$$D View this record in MEDLINE/PubMed
BookMark eNp9kEtLHUEQhRsxxKvmFwjSy2xmUv2481hkEcQ8QBDEgLumHzXS15nusXvmgv8-ba5mGSg4m1PnVH2n5DjEgIRcMKgZsObLrn5xxseaA4caRA0MjsiGQb-tto18OCYbAMYr1kBzQk5z3gGA6DrxkZwIztoeun5D7nCPocpPfp7RUW2XTHUZOmufqrSOSB8xIPWhaJqo0cHRvOhHzDQO9D55E0e_TtSVnDHOE4blnHwY9Jjx05uekd_fr--vflY3tz9-XX27qawEuVQNk9yg6YCZAbgVWsjWDdu-7RCca60wgoNwzgxu4K7fIsqu7crhspGsBy7OyOdD7pzi84p5UZPPFsdRB4xrVly0HQCXghWrOFhtijknHNSc_KTTi2KgXmGqnfoLU73CVCBUgVm2Lt8KVjOh-7fzTq8Yvh4MWN7ce0wqW4_BovMJ7aJc9P8t-APku4ei
CitedBy_id crossref_primary_10_1016_j_ydbio_2020_07_002
Cites_doi 10.1038/nrg1724
10.1126/science.1218256
10.1007/s00427-008-0207-2
10.7554/eLife.01440
10.1016/j.ydbio.2004.03.001
10.1002/jez.b.21328
10.1016/j.ydbio.2015.06.012
10.1038/367429a0
10.1016/S0925-4773(96)00642-9
10.1073/pnas.0510440103
10.1016/j.ydbio.2006.11.003
10.1016/0092-8674(86)90515-5
10.1016/j.jinsphys.2013.08.014
10.1242/dev.01807
10.1016/j.ydbio.2006.09.037
10.1016/j.ydbio.2008.10.037
10.1016/S0960-9822(02)00666-8
10.1146/annurev.ento.47.091201.145251
10.1016/0092-8674(92)90466-P
10.1242/dev.085126
10.1038/367460a0
10.1002/dvg.1020150103
ContentType Journal Article
Copyright 2020 Elsevier Inc.
Copyright © 2020 Elsevier Inc. All rights reserved.
Copyright_xml – notice: 2020 Elsevier Inc.
– notice: Copyright © 2020 Elsevier Inc. All rights reserved.
DBID CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
DOI 10.1016/j.ydbio.2020.03.010
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
MEDLINE - Academic
DatabaseTitleList
MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Zoology
Biology
EISSN 1095-564X
EndPage 6
ExternalDocumentID 10_1016_j_ydbio_2020_03_010
32179089
S0012160620300920
Genre Research Support, Non-U.S. Gov't
Journal Article
GroupedDBID ---
--K
--M
-DZ
-~X
.~1
0R~
1B1
1RT
1~.
1~5
4.4
457
4G.
53G
5GY
5RE
5VS
7-5
71M
85S
8P~
9JM
AABNK
AACTN
AADPK
AAEDT
AAEDW
AAFTH
AAIAV
AAIKJ
AAKOC
AALRI
AAOAW
AAQFI
AAXLA
AAXUO
ABCQJ
ABFNM
ABFRF
ABGSF
ABJNI
ABMAC
ABUDA
ABVKL
ABYKQ
ACDAQ
ACGFO
ACGFS
ACNCT
ACRLP
ADBBV
ADEZE
ADUVX
AEBSH
AEFWE
AEHWI
AEKER
AENEX
AEXQZ
AFFNX
AFKWA
AFTJW
AFXIZ
AGHSJ
AGUBO
AGWIK
AGYEJ
AIEXJ
AIKHN
AITUG
AJOXV
ALMA_UNASSIGNED_HOLDINGS
AMFUW
AMRAJ
AXJTR
BAWUL
BKOJK
BLXMC
CS3
D0L
DIK
DM4
DOVZS
DU5
E3Z
EBS
EFBJH
EFLBG
EO8
EO9
EP2
EP3
F5P
FDB
FIRID
FNPLU
FYGXN
G-Q
GBLVA
HLW
IH2
IHE
IXB
J1W
K-O
KOM
LG5
LX2
M41
MO0
MOBAO
N9A
NCXOZ
O-L
O9-
OAUVE
OK1
OZT
P-8
P-9
P2P
PC.
Q38
ROL
RPZ
RSU
SCC
SDF
SDG
SES
SPCBC
SSN
SSU
SSZ
T5K
TAE
TN5
TR2
UPT
WH7
~G-
~KM
0SF
AAHBH
AAXKI
ADVLN
AKRWK
CGR
CUY
CVF
ECM
EIF
NPM
RIG
.55
.GJ
186
29F
3O-
4R4
6I.
9M8
AAQXK
AAYXX
ABXDB
ADFGL
ADIYS
ADMUD
AFJKZ
AGHFR
AHHHB
AI.
ASPBG
AVWKF
AZFZN
CAG
CITATION
COF
EJD
FA8
FEDTE
FGOYB
G-2
G8K
HVGLF
HZ~
H~9
MVM
R2-
SBG
SEW
UQL
VH1
WUQ
X7M
XJT
XOL
XPP
ZGI
ZKB
ZMT
7X8
ID FETCH-LOGICAL-c404t-6142beb801bf02c3a347df5978e0dd7c3b3203ddbfdf2d95ee487821746419023
IEDL.DBID ABVKL
ISSN 0012-1606
IngestDate Fri Oct 25 09:08:11 EDT 2024
Thu Sep 26 20:58:50 EDT 2024
Sat Sep 28 08:26:19 EDT 2024
Fri Feb 23 02:47:18 EST 2024
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 1
Keywords Tribolium castaneum
Segmentation
Even-skipped
Pair-rule patterning
Language English
License Copyright © 2020 Elsevier Inc. All rights reserved.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c404t-6142beb801bf02c3a347df5978e0dd7c3b3203ddbfdf2d95ee487821746419023
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
OpenAccessLink https://doi.org/10.1016/j.ydbio.2020.03.010
PMID 32179089
PQID 2378002431
PQPubID 23479
PageCount 6
ParticipantIDs proquest_miscellaneous_2378002431
crossref_primary_10_1016_j_ydbio_2020_03_010
pubmed_primary_32179089
elsevier_sciencedirect_doi_10_1016_j_ydbio_2020_03_010
PublicationCentury 2000
PublicationDate 2020-06-01
2020-06-00
20200601
PublicationDateYYYYMMDD 2020-06-01
PublicationDate_xml – month: 06
  year: 2020
  text: 2020-06-01
  day: 01
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Developmental biology
PublicationTitleAlternate Dev Biol
PublicationYear 2020
Publisher Elsevier Inc
Publisher_xml – name: Elsevier Inc
References Bucher, Scholten, Klingler (bib3) 2002; 12
Nagy, Carroll (bib15) 1994; 367
St Johnston, Nusslein-Volhard (bib23) 1992; 68
Mito, Kobayashi, Sarashina, Zhang, Shinahara, Miyawaki, Shinmyo, Ohuchi, Noji (bib14) 2007; 303
Brown, Patel, Denell (bib2) 1994; 15
Stahi, Chipman (bib24) 2016; 283
Nakao (bib17) 2015; 405
Farzana, Brown (bib9) 2008; 218
Rosenberg, Brent, Payre, Desplan (bib20) 2014; 3
Davis, Patel (bib7) 2002; 47
Nakao (bib16) 2010; 314
Brown, Parrish, Beeman, Denell (bib1) 1997; 61
Macdonald, Ingham, Struhl (bib13) 1986; 47
Choe, Brown (bib5) 2009; 325
Choe, Miller, Brown (bib6) 2006; 103
Sarrazin, Peel, Averof (bib21) 2012; 336
Choe, Brown (bib4) 2007; 302
El-Sherif, Averof, Brown (bib8) 2012; 139
Scott, Michel, Bartholomay, Siegfried, Hunter, Smagghe, Zhu, Douglas (bib22) 2013; 59
Liu, Kaufman (bib12) 2005; 132
Jaynes, Fujioka (bib10) 2004; 269
Patel, Condron, Zinn (bib18) 1994; 367
Lawrence (bib11) 1992
Peel, Chipman, Akam (bib19) 2005; 6
Sarrazin (10.1016/j.ydbio.2020.03.010_bib21) 2012; 336
Brown (10.1016/j.ydbio.2020.03.010_bib2) 1994; 15
Rosenberg (10.1016/j.ydbio.2020.03.010_bib20) 2014; 3
Scott (10.1016/j.ydbio.2020.03.010_bib22) 2013; 59
Choe (10.1016/j.ydbio.2020.03.010_bib6) 2006; 103
Patel (10.1016/j.ydbio.2020.03.010_bib18) 1994; 367
Nakao (10.1016/j.ydbio.2020.03.010_bib16) 2010; 314
El-Sherif (10.1016/j.ydbio.2020.03.010_bib8) 2012; 139
Farzana (10.1016/j.ydbio.2020.03.010_bib9) 2008; 218
Bucher (10.1016/j.ydbio.2020.03.010_bib3) 2002; 12
Stahi (10.1016/j.ydbio.2020.03.010_bib24) 2016; 283
Davis (10.1016/j.ydbio.2020.03.010_bib7) 2002; 47
Macdonald (10.1016/j.ydbio.2020.03.010_bib13) 1986; 47
Mito (10.1016/j.ydbio.2020.03.010_bib14) 2007; 303
Brown (10.1016/j.ydbio.2020.03.010_bib1) 1997; 61
Liu (10.1016/j.ydbio.2020.03.010_bib12) 2005; 132
Choe (10.1016/j.ydbio.2020.03.010_bib4) 2007; 302
Lawrence (10.1016/j.ydbio.2020.03.010_bib11) 1992
Nagy (10.1016/j.ydbio.2020.03.010_bib15) 1994; 367
St Johnston (10.1016/j.ydbio.2020.03.010_bib23) 1992; 68
Jaynes (10.1016/j.ydbio.2020.03.010_bib10) 2004; 269
Peel (10.1016/j.ydbio.2020.03.010_bib19) 2005; 6
Choe (10.1016/j.ydbio.2020.03.010_bib5) 2009; 325
Nakao (10.1016/j.ydbio.2020.03.010_bib17) 2015; 405
References_xml – volume: 336
  start-page: 338
  year: 2012
  end-page: 341
  ident: bib21
  article-title: A segmentation clock with two-segment periodicity in insects
  publication-title: Science
  contributor:
    fullname: Averof
– volume: 139
  start-page: 4341
  year: 2012
  end-page: 4346
  ident: bib8
  article-title: A segmentation clock operating in blastoderm and germband stages of
  publication-title: Development
  contributor:
    fullname: Brown
– volume: 3
  year: 2014
  ident: bib20
  article-title: Dual mode of embryonic development is highlighted by expression and function of
  publication-title: Elife
  contributor:
    fullname: Desplan
– volume: 283
  year: 2016
  ident: bib24
  article-title: Blastoderm segmentation in
  publication-title: Proc. Biol. Sci.
  contributor:
    fullname: Chipman
– volume: 59
  start-page: 1212
  year: 2013
  end-page: 1221
  ident: bib22
  article-title: Towards the elements of successful insect RNAi
  publication-title: J. Insect Physiol.
  contributor:
    fullname: Douglas
– volume: 47
  start-page: 721
  year: 1986
  end-page: 734
  ident: bib13
  article-title: Isolation, structure, and expression of
  publication-title: Cell
  contributor:
    fullname: Struhl
– volume: 15
  start-page: 7
  year: 1994
  end-page: 18
  ident: bib2
  article-title: Embryonic expression of the single
  publication-title: Dev. Genet.
  contributor:
    fullname: Denell
– volume: 6
  start-page: 905
  year: 2005
  end-page: 916
  ident: bib19
  article-title: Arthropod segmentation: beyond the
  publication-title: Nat. Rev. Genet.
  contributor:
    fullname: Akam
– volume: 325
  start-page: 482
  year: 2009
  end-page: 491
  ident: bib5
  article-title: Genetic regulation of
  publication-title: Dev. Biol.
  contributor:
    fullname: Brown
– volume: 103
  start-page: 6560
  year: 2006
  end-page: 6564
  ident: bib6
  article-title: A pair-rule gene circuit defines segments sequentially in the short-germ insect
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  contributor:
    fullname: Brown
– volume: 302
  start-page: 281
  year: 2007
  end-page: 294
  ident: bib4
  article-title: Evolutionary flexibility of pair-rule patterning revealed by functional analysis of secondary pair-rule genes,
  publication-title: Dev. Biol.
  contributor:
    fullname: Brown
– volume: 405
  start-page: 149
  year: 2015
  end-page: 157
  ident: bib17
  article-title: Analyses of interactions among pair-rule genes and the gap gene
  publication-title: Dev. Biol.
  contributor:
    fullname: Nakao
– volume: 314
  start-page: 224
  year: 2010
  end-page: 231
  ident: bib16
  article-title: Characterization of
  publication-title: J. Exp. Zool. B Mol. Dev. Evol.
  contributor:
    fullname: Nakao
– volume: 61
  start-page: 165
  year: 1997
  end-page: 173
  ident: bib1
  article-title: Molecular characterization and embryonic expression of the
  publication-title: Mech. Dev.
  contributor:
    fullname: Denell
– volume: 303
  start-page: 202
  year: 2007
  end-page: 213
  ident: bib14
  article-title: has gap-like, pair-rule-like, and segmental functions in the cricket
  publication-title: Dev. Biol.
  contributor:
    fullname: Noji
– volume: 68
  start-page: 201
  year: 1992
  end-page: 219
  ident: bib23
  article-title: The origin of pattern and polarity in the
  publication-title: Cell
  contributor:
    fullname: Nusslein-Volhard
– volume: 47
  start-page: 669
  year: 2002
  end-page: 699
  ident: bib7
  article-title: Short, long, and beyond: molecular and embryological approaches to insect segmentation
  publication-title: Annu. Rev. Entomol.
  contributor:
    fullname: Patel
– volume: 12
  start-page: R85
  year: 2002
  end-page: R86
  ident: bib3
  article-title: Parental RNAi in
  publication-title: Curr. Biol.
  contributor:
    fullname: Klingler
– volume: 218
  start-page: 181
  year: 2008
  end-page: 192
  ident: bib9
  article-title: Hedgehog signaling pathway function conserved in
  publication-title: Dev. Gene. Evol.
  contributor:
    fullname: Brown
– volume: 367
  start-page: 460
  year: 1994
  end-page: 463
  ident: bib15
  article-title: Conservation of
  publication-title: Nature
  contributor:
    fullname: Carroll
– volume: 367
  start-page: 429
  year: 1994
  end-page: 434
  ident: bib18
  article-title: Pair-rule expression patterns of
  publication-title: Nature
  contributor:
    fullname: Zinn
– volume: 269
  start-page: 609
  year: 2004
  end-page: 622
  ident: bib10
  article-title: Drawing lines in the sand:
  publication-title: Dev. Biol.
  contributor:
    fullname: Fujioka
– volume: 132
  start-page: 2081
  year: 2005
  end-page: 2092
  ident: bib12
  article-title: is not a pair-rule gene but has segmental and gap-like functions in
  publication-title: Development
  contributor:
    fullname: Kaufman
– year: 1992
  ident: bib11
  article-title: The Making of a Fly: The Genetics of Animal Design
  contributor:
    fullname: Lawrence
– volume: 6
  start-page: 905
  year: 2005
  ident: 10.1016/j.ydbio.2020.03.010_bib19
  article-title: Arthropod segmentation: beyond the Drosophila paradigm
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg1724
  contributor:
    fullname: Peel
– volume: 336
  start-page: 338
  year: 2012
  ident: 10.1016/j.ydbio.2020.03.010_bib21
  article-title: A segmentation clock with two-segment periodicity in insects
  publication-title: Science
  doi: 10.1126/science.1218256
  contributor:
    fullname: Sarrazin
– volume: 218
  start-page: 181
  year: 2008
  ident: 10.1016/j.ydbio.2020.03.010_bib9
  article-title: Hedgehog signaling pathway function conserved in Tribolium segmentation
  publication-title: Dev. Gene. Evol.
  doi: 10.1007/s00427-008-0207-2
  contributor:
    fullname: Farzana
– volume: 3
  year: 2014
  ident: 10.1016/j.ydbio.2020.03.010_bib20
  article-title: Dual mode of embryonic development is highlighted by expression and function of Nasonia pair-rule genes
  publication-title: Elife
  doi: 10.7554/eLife.01440
  contributor:
    fullname: Rosenberg
– volume: 283
  year: 2016
  ident: 10.1016/j.ydbio.2020.03.010_bib24
  article-title: Blastoderm segmentation in Oncopeltus fasciatus and the evolution of insect segmentation mechanisms
  publication-title: Proc. Biol. Sci.
  contributor:
    fullname: Stahi
– volume: 269
  start-page: 609
  year: 2004
  ident: 10.1016/j.ydbio.2020.03.010_bib10
  article-title: Drawing lines in the sand: even skipped et al. and parasegment boundaries
  publication-title: Dev. Biol.
  doi: 10.1016/j.ydbio.2004.03.001
  contributor:
    fullname: Jaynes
– volume: 314
  start-page: 224
  year: 2010
  ident: 10.1016/j.ydbio.2020.03.010_bib16
  article-title: Characterization of Bombyx embryo segmentation process: expression profiles of engrailed, even-skipped, caudal, and wnt1/wingless homologues
  publication-title: J. Exp. Zool. B Mol. Dev. Evol.
  doi: 10.1002/jez.b.21328
  contributor:
    fullname: Nakao
– volume: 405
  start-page: 149
  year: 2015
  ident: 10.1016/j.ydbio.2020.03.010_bib17
  article-title: Analyses of interactions among pair-rule genes and the gap gene Kruppel in Bombyx segmentation
  publication-title: Dev. Biol.
  doi: 10.1016/j.ydbio.2015.06.012
  contributor:
    fullname: Nakao
– volume: 367
  start-page: 429
  year: 1994
  ident: 10.1016/j.ydbio.2020.03.010_bib18
  article-title: Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles
  publication-title: Nature
  doi: 10.1038/367429a0
  contributor:
    fullname: Patel
– volume: 61
  start-page: 165
  year: 1997
  ident: 10.1016/j.ydbio.2020.03.010_bib1
  article-title: Molecular characterization and embryonic expression of the even-skipped ortholog of Tribolium castaneum
  publication-title: Mech. Dev.
  doi: 10.1016/S0925-4773(96)00642-9
  contributor:
    fullname: Brown
– volume: 103
  start-page: 6560
  year: 2006
  ident: 10.1016/j.ydbio.2020.03.010_bib6
  article-title: A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.0510440103
  contributor:
    fullname: Choe
– volume: 303
  start-page: 202
  year: 2007
  ident: 10.1016/j.ydbio.2020.03.010_bib14
  article-title: even-skipped has gap-like, pair-rule-like, and segmental functions in the cricket Gryllus bimaculatus, a basal, intermediate germ insect (Orthoptera)
  publication-title: Dev. Biol.
  doi: 10.1016/j.ydbio.2006.11.003
  contributor:
    fullname: Mito
– year: 1992
  ident: 10.1016/j.ydbio.2020.03.010_bib11
  contributor:
    fullname: Lawrence
– volume: 47
  start-page: 721
  year: 1986
  ident: 10.1016/j.ydbio.2020.03.010_bib13
  article-title: Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box
  publication-title: Cell
  doi: 10.1016/0092-8674(86)90515-5
  contributor:
    fullname: Macdonald
– volume: 59
  start-page: 1212
  year: 2013
  ident: 10.1016/j.ydbio.2020.03.010_bib22
  article-title: Towards the elements of successful insect RNAi
  publication-title: J. Insect Physiol.
  doi: 10.1016/j.jinsphys.2013.08.014
  contributor:
    fullname: Scott
– volume: 132
  start-page: 2081
  year: 2005
  ident: 10.1016/j.ydbio.2020.03.010_bib12
  article-title: even-skipped is not a pair-rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect
  publication-title: Development
  doi: 10.1242/dev.01807
  contributor:
    fullname: Liu
– volume: 302
  start-page: 281
  year: 2007
  ident: 10.1016/j.ydbio.2020.03.010_bib4
  article-title: Evolutionary flexibility of pair-rule patterning revealed by functional analysis of secondary pair-rule genes, paired and sloppy-paired in the short-germ insect, Tribolium castaneum
  publication-title: Dev. Biol.
  doi: 10.1016/j.ydbio.2006.09.037
  contributor:
    fullname: Choe
– volume: 325
  start-page: 482
  year: 2009
  ident: 10.1016/j.ydbio.2020.03.010_bib5
  article-title: Genetic regulation of engrailed and wingless in Tribolium segmentation and the evolution of pair-rule segmentation
  publication-title: Dev. Biol.
  doi: 10.1016/j.ydbio.2008.10.037
  contributor:
    fullname: Choe
– volume: 12
  start-page: R85
  year: 2002
  ident: 10.1016/j.ydbio.2020.03.010_bib3
  article-title: Parental RNAi in Tribolium (Coleoptera)
  publication-title: Curr. Biol.
  doi: 10.1016/S0960-9822(02)00666-8
  contributor:
    fullname: Bucher
– volume: 47
  start-page: 669
  year: 2002
  ident: 10.1016/j.ydbio.2020.03.010_bib7
  article-title: Short, long, and beyond: molecular and embryological approaches to insect segmentation
  publication-title: Annu. Rev. Entomol.
  doi: 10.1146/annurev.ento.47.091201.145251
  contributor:
    fullname: Davis
– volume: 68
  start-page: 201
  year: 1992
  ident: 10.1016/j.ydbio.2020.03.010_bib23
  article-title: The origin of pattern and polarity in the Drosophila embryo
  publication-title: Cell
  doi: 10.1016/0092-8674(92)90466-P
  contributor:
    fullname: St Johnston
– volume: 139
  start-page: 4341
  year: 2012
  ident: 10.1016/j.ydbio.2020.03.010_bib8
  article-title: A segmentation clock operating in blastoderm and germband stages of Tribolium development
  publication-title: Development
  doi: 10.1242/dev.085126
  contributor:
    fullname: El-Sherif
– volume: 367
  start-page: 460
  year: 1994
  ident: 10.1016/j.ydbio.2020.03.010_bib15
  article-title: Conservation of wingless patterning functions in the short-germ embryos of Tribolium castaneum
  publication-title: Nature
  doi: 10.1038/367460a0
  contributor:
    fullname: Nagy
– volume: 15
  start-page: 7
  year: 1994
  ident: 10.1016/j.ydbio.2020.03.010_bib2
  article-title: Embryonic expression of the single Tribolium engrailed homolog
  publication-title: Dev. Genet.
  doi: 10.1002/dvg.1020150103
  contributor:
    fullname: Brown
SSID ssj0003883
Score 2.3807514
Snippet The pair-rule gene even-skipped (eve) is essential for insect segmentation, yet its function varies among insect clades. While loss of eve results in typical...
SourceID proquest
crossref
pubmed
elsevier
SourceType Aggregation Database
Index Database
Publisher
StartPage 1
SubjectTerms Amino Acid Sequence - genetics
Animals
Body Patterning - genetics
Embryo, Nonmammalian - metabolism
Even-skipped
Gene Expression Regulation, Developmental - genetics
Genes, Insect - genetics
Insect Proteins - genetics
Pair-rule patterning
Segmentation
Transcription Factors - metabolism
Tribolium - embryology
Tribolium - genetics
Tribolium castaneum
Title even-skipped acts as a pair-rule gene in germ band stages of Tribolium development
URI https://dx.doi.org/10.1016/j.ydbio.2020.03.010
https://www.ncbi.nlm.nih.gov/pubmed/32179089
https://search.proquest.com/docview/2378002431
Volume 462
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1JS8QwFA4uCF7E3XEjgkejaZLpclRRxvUgKoOXkK1Sl7bMcvDib_eliyKoB6GQNDQ0fElevte-fEFo139VSA2lxCuBEBGlCdExF0QHQaiUYUJVYtVX12HvTpz3u_0JdNzuhfFhlY3tr216Za2bkoMGzYMyy_we34AFwL8ZjFOaMPDbp1nUTWB2Th8e3V9cfhpkHtdqnPA88RVa8aEqzOvN6sxvAmS0Ejv1O2l_XqB-I6DVQnQ6j-YaBokP60YuoAmXL6KZ-kzJN8g9FFVuCd14cSYyfM7K0lmszGiIFVy4VNmADMYvDsPgcTjLIR28Yq1yi4ErProhLlLsJUWKl2z8iu1XXNEyujs9uT3ukeYIBWIEFSNwDAXTTsMypFPKDFdcRDYFJyJ21NrIcM0BPmt1alNmk65z4MDE3k0JBVAFxlfQVF7kbg1hZoFpKQr-h-oKZUJAPLFAOHRgUhNx00F7LW6yrJUyZBtC9iQrmKWHWVIuAeYOClts5bcOl2DL_6640_aEhKng_2-o3BXjoWQ8iiuFxaCDVusu-mwJZ16KLE7W__vaDTTr7-oosU00NRqM3RbwkZHeRpP778F2M-p8enbRu4bSs_7RB5Xi3ps
link.rule.ids 315,786,790,3520,4516,24137,27591,27946,27947,45609,45687,45703,45898
linkProvider Elsevier
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1La9wwEBYhIbSX0KSPbJs0KuQYdWVJ68cxhCybx-4hJLD0IvRycLtrm30ccslv70i2sxTSHgoGG1vG4tN49I098wmhU_9VITeUEq8EQkSSZ0SnXBAdRbFShgkVxKrHk3j0IK6ng-kWuuhqYXxaZev7G58evHV7pt-i2a-Lwtf4RiwC_s3ATmnGIG7fATZAvWl_f97kefC00eKE1sQ376SHQpLXk9WFLwFkNEid-jra16env9HPMA0N36G9lj_i86aL-2jLlQdot1lR8gmOflTh6D2689JMZPmrqGtnsTKrJVaw4VoVC7JYzxwG03G4KGG_mGOtSouBKT66Ja5y7AVFqlmxnmO7ySr6gB6Gl_cXI9IuoECMoGIFYaFg2mmYhHROmeGKi8TmEEKkjlqbGK45gGetzm3ObDZwDsKX1AcpsQCiwPhHtF1WpTtEmFngWYpC9KEGQpkY8M4s0A0dmdwk3PTQWYebrBudDNklkP2UAWbpYZaUS4C5h-IOW_nHcEvw5P--8Vs3EhJeBP93Q5WuWi8l40ka9BWjHvrUDNFLTzjzQmRp9vl_H3uC3ozux7fy9mpy8wW99VeafLEjtL1arN0xMJOV_hos7zdGu9zL
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=even-skipped+acts+as+a+pair-rule+gene+in+germ+band+stages+of+Tribolium+development&rft.jtitle=Developmental+biology&rft.au=O%2C+Jiyun&rft.au=Choe%2C+Chong+Pyo&rft.date=2020-06-01&rft.pub=Elsevier+Inc&rft.issn=0012-1606&rft.eissn=1095-564X&rft.volume=462&rft.issue=1&rft.spage=1&rft.epage=6&rft_id=info:doi/10.1016%2Fj.ydbio.2020.03.010&rft.externalDocID=S0012160620300920
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0012-1606&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0012-1606&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0012-1606&client=summon