Auxin-Induced WUSCHEL-RELATED HOMEOBOX13 Mediates Asymmetric Activity of Callus Formation upon Cutting

Abstract Plants have the regenerative ability to reconnect cut organs, which is physiologically important to survive severe tissue damage. The ability to reconnect organs is utilized as grafting to combine two different individuals. Callus formation at the graft junction facilitates organ attachment...

Full description

Saved in:
Bibliographic Details
Published inPlant and cell physiology Vol. 64; no. 3; pp. 305 - 316
Main Authors Tanaka, Hayato, Hashimoto, Naoki, Kawai, Satomi, Yumoto, Emi, Shibata, Kyomi, Tameshige, Toshiaki, Yamamoto, Yuma, Sugimoto, Keiko, Asahina, Masashi, Ikeuchi, Momoko
Format Journal Article
LanguageEnglish
Published UK Oxford University Press 15.03.2023
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Abstract Plants have the regenerative ability to reconnect cut organs, which is physiologically important to survive severe tissue damage. The ability to reconnect organs is utilized as grafting to combine two different individuals. Callus formation at the graft junction facilitates organ attachment and vascular reconnection. While it is well documented that local wounding signals provoke callus formation, how callus formation is differentially regulated at each cut end remains elusive. Here, we report that callus formation activity is asymmetrical between the top and bottom cut ends and is regulated by differential auxin accumulation. Gene expression analyses revealed that cellular auxin response is preferentially upregulated in the top part of the graft. Disruption of polar auxin transport inhibited callus formation from the top, while external application of auxin was sufficient to induce callus formation from the bottom, suggesting that asymmetric auxin accumulation is responsible for active callus formation from the top end. We further found that the expression of a key regulator of callus formation, WUSCHEL-RELATED HOMEOBOX 13 (WOX13), is induced by auxin. The ectopic callus formation from the bottom end, which is triggered by locally supplemented auxin, requires WOX13 function, demonstrating that WOX13 plays a pivotal role in auxin-dependent callus formation. The asymmetric WOX13 expression is observed both in grafted petioles and incised inflorescence stems, underscoring the generality of our findings. We propose that efficient organ reconnection is achieved by a combination of local wounding stimuli and disrupted long-distance signaling.
AbstractList Abstract Plants have the regenerative ability to reconnect cut organs, which is physiologically important to survive severe tissue damage. The ability to reconnect organs is utilized as grafting to combine two different individuals. Callus formation at the graft junction facilitates organ attachment and vascular reconnection. While it is well documented that local wounding signals provoke callus formation, how callus formation is differentially regulated at each cut end remains elusive. Here, we report that callus formation activity is asymmetrical between the top and bottom cut ends and is regulated by differential auxin accumulation. Gene expression analyses revealed that cellular auxin response is preferentially upregulated in the top part of the graft. Disruption of polar auxin transport inhibited callus formation from the top, while external application of auxin was sufficient to induce callus formation from the bottom, suggesting that asymmetric auxin accumulation is responsible for active callus formation from the top end. We further found that the expression of a key regulator of callus formation, WUSCHEL-RELATED HOMEOBOX 13 (WOX13), is induced by auxin. The ectopic callus formation from the bottom end, which is triggered by locally supplemented auxin, requires WOX13 function, demonstrating that WOX13 plays a pivotal role in auxin-dependent callus formation. The asymmetric WOX13 expression is observed both in grafted petioles and incised inflorescence stems, underscoring the generality of our findings. We propose that efficient organ reconnection is achieved by a combination of local wounding stimuli and disrupted long-distance signaling.
Plants have the regenerative ability to reconnect cut organs, which is physiologically important to survive severe tissue damage. The ability to reconnect organs is utilized as grafting to combine two different individuals. Callus formation at the graft junction facilitates organ attachment and vascular reconnection. While it is well documented that local wounding signals provoke callus formation, how callus formation is differentially regulated at each cut end remains elusive. Here, we report that callus formation activity is asymmetrical between the top and bottom cut ends and is regulated by differential auxin accumulation. Gene expression analyses revealed that cellular auxin response is preferentially upregulated in the top part of the graft. Disruption of polar auxin transport inhibited callus formation from the top, while external application of auxin was sufficient to induce callus formation from the bottom, suggesting that asymmetric auxin accumulation is responsible for active callus formation from the top end. We further found that the expression of a key regulator of callus formation, WUSCHEL-RELATED HOMEOBOX 13 (WOX13), is induced by auxin. The ectopic callus formation from the bottom end, which is triggered by locally supplemented auxin, requires WOX13 function, demonstrating that WOX13 plays a pivotal role in auxin-dependent callus formation. The asymmetric WOX13 expression is observed both in grafted petioles and incised inflorescence stems, underscoring the generality of our findings. We propose that efficient organ reconnection is achieved by a combination of local wounding stimuli and disrupted long-distance signaling.
Author Tameshige, Toshiaki
Sugimoto, Keiko
Ikeuchi, Momoko
Shibata, Kyomi
Kawai, Satomi
Yumoto, Emi
Tanaka, Hayato
Yamamoto, Yuma
Hashimoto, Naoki
Asahina, Masashi
Author_xml – sequence: 1
  givenname: Hayato
  orcidid: 0000-0002-1405-7716
  surname: Tanaka
  fullname: Tanaka, Hayato
– sequence: 2
  givenname: Naoki
  surname: Hashimoto
  fullname: Hashimoto, Naoki
– sequence: 3
  givenname: Satomi
  surname: Kawai
  fullname: Kawai, Satomi
– sequence: 4
  givenname: Emi
  surname: Yumoto
  fullname: Yumoto, Emi
– sequence: 5
  givenname: Kyomi
  surname: Shibata
  fullname: Shibata, Kyomi
– sequence: 6
  givenname: Toshiaki
  surname: Tameshige
  fullname: Tameshige, Toshiaki
– sequence: 7
  givenname: Yuma
  surname: Yamamoto
  fullname: Yamamoto, Yuma
– sequence: 8
  givenname: Keiko
  orcidid: 0000-0002-9209-8230
  surname: Sugimoto
  fullname: Sugimoto, Keiko
– sequence: 9
  givenname: Masashi
  orcidid: 0000-0002-1828-0966
  surname: Asahina
  fullname: Asahina, Masashi
– sequence: 10
  givenname: Momoko
  orcidid: 0000-0001-9474-5131
  surname: Ikeuchi
  fullname: Ikeuchi, Momoko
  email: momoko.ikeuchi@bs.naist.jp
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36263676$$D View this record in MEDLINE/PubMed
BookMark eNp9kMtLwzAcgINM3ENP3iUnEaSaR5u2x1o7J2wMdENvJU1SifRlk4j7761sevTwexw-vsM3BaOmbRQA5xjdYBTT2050w3CBfXYEJtgPsRejgI7ABCFKPBRGeAymxrwjNPwUnYAxZYRRFrIJKBP3pRvvsZFOKAlfts_pIlt6T9ky2WT3cLFeZeu79SumcKWk5lYZmJhdXSvbawETYfWntjvYljDlVeUMnLd9za1uG-i6YaXOWt28nYLjkldGnR3uDGzn2SZdeMv1w2OaLD1BI2a9EsUBVUFBUCgCHisp4khSXCAW-RzJkmJVCl74iErGSMlJKEVEmB_5YeGrOKQzcLX3dn374ZSxea2NUFXFG9U6k5OQsJhQjIMBvd6jom-N6VWZd72ueb_LMcp_wuZD2PwQdqAvDmJX1Er-sb8lB-ByD7Su-9f0DaFGgh4
CitedBy_id crossref_primary_10_3390_ijms242115832
crossref_primary_10_1093_pcp_pcad009
crossref_primary_10_1007_s10725_023_01052_7
crossref_primary_10_3390_ijms232416112
crossref_primary_10_1016_j_pbi_2023_102452
crossref_primary_10_1007_s11427_024_2581_2
crossref_primary_10_1126_sciadv_adg6983
Cites_doi 10.1016/j.cub.2013.04.048
10.1002/j.1537-2197.1952.tb14277.x
10.1093/plphys/kiab510
10.1007/BF00624737
10.1093/pcp/pcw177
10.1105/tpc.111.087874
10.1038/s42003-021-01895-8
10.1126/science.abc3710
10.1242/dev.134668
10.1111/tpj.12654
10.1016/j.cub.2011.02.020
10.1016/j.pbi.2020.06.007
10.1093/pcp/pcac004
10.1016/S0065-2296(08)60351-1
10.1016/j.cub.2020.09.037
10.1104/pp.17.01035
10.1242/dev.00596
10.1016/j.cub.2022.02.069
10.1073/pnas.1110443108
10.1038/s42003-020-01143-5
10.1105/tpc.113.109538
10.1146/annurev-arplant-050718-100434
10.1105/tpc.16.00623
10.1105/tpc.114.122887
10.1093/aob/mcf137
10.1038/s41477-021-01015-8
10.1007/s10265-015-0724-9
10.1111/j.1469-8137.1983.tb02701.x
10.1111/j.1469-8137.1982.tb03350.x
10.1073/pnas.1718263115
10.1242/dev.185710
10.1105/tpc.12.4.507
10.1038/s41467-019-13074-9
10.1093/pcp/pcz202
10.1038/nature07597
10.1111/nph.17594
10.1111/tpj.12010
10.1007/s10265-021-01360-x
10.1016/j.cub.2015.01.029
10.1038/s42003-019-0646-5
10.1016/j.cell.2008.01.040
10.1016/j.cub.2015.03.032
10.1016/S0092-8674(03)00924-3
10.1016/j.cell.2016.04.038
10.1073/pnas.85.15.5536
ContentType Journal Article
Copyright The Author(s) 2023. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2023
The Author(s) 2023. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Copyright_xml – notice: The Author(s) 2023. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2023
– notice: The Author(s) 2023. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
DBID CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
DOI 10.1093/pcp/pcac146
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
CrossRef
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 Biology
Botany
EISSN 1471-9053
EndPage 316
ExternalDocumentID 10_1093_pcp_pcac146
36263676
10.1093/pcp/pcac146
Genre Journal Article
GrantInformation_xml – fundername: Japan Society for the Promotion of Science
  grantid: 20K06712, 20H04894, 19K06728
– fundername: The Naito Foundation
– fundername: The Promotion and Mutual Aid Corporation for Private School of Japan
– fundername: Takeda Science Foundation
– fundername: Shiseido Female Researcher Science Grant
GroupedDBID ---
-E4
-~X
.2P
.I3
0R~
123
1TH
29O
2WC
4.4
482
48X
53G
5VS
5WD
6.Y
6P2
7.U
70D
A8Z
AAHBH
AAIMJ
AAJKP
AAJQQ
AAKDD
AAMDB
AAMVS
AAOGV
AAPQZ
AAPXW
AARHZ
AASNB
AAUAY
AAUQX
AAVAP
AAVLN
AAWDT
ABDBF
ABEUO
ABIXL
ABJNI
ABMNT
ABNKS
ABPTD
ABQLI
ABQTQ
ABSAR
ABSMQ
ABWST
ABXVV
ABZBJ
ACFRR
ACGFS
ACIWK
ACKIV
ACMRT
ACNCT
ACPQN
ACPRK
ACUFI
ACUTJ
ACZBC
ADBBV
ADEYI
ADEZT
ADFTL
ADGKP
ADGZP
ADHKW
ADHZD
ADIPN
ADOCK
ADQBN
ADRIX
ADRTK
ADVEK
ADYVW
ADZTZ
ADZXQ
AEGPL
AEJOX
AEKPW
AEKSI
AELWJ
AEMDU
AENEX
AENZO
AEPUE
AETBJ
AEWNT
AFFNX
AFFZL
AFGWE
AFIYH
AFOFC
AFRAH
AFSHK
AFXEN
AFYAG
AGINJ
AGKEF
AGKRT
AGMDO
AGQXC
AGSYK
AHMBA
AHXPO
AIDBO
AIJHB
AJEEA
AKHUL
AKWXX
ALMA_UNASSIGNED_HOLDINGS
ALUQC
ANFBD
APIBT
APJGH
APWMN
AQDSO
ARIXL
ASAOO
ASPBG
ATDFG
ATGXG
ATTQO
AVWKF
AXUDD
AYOIW
AZFZN
BAWUL
BAYMD
BCRHZ
BEYMZ
BHONS
BQDIO
BSWAC
CAG
CDBKE
COF
CS3
CXTWN
CZ4
DAKXR
DFGAJ
DIK
DILTD
DU5
D~K
EBD
EBS
ECGQY
EDH
EE~
EJD
ELUNK
EMOBN
ESTFP
ESX
F20
F5P
F9B
FEDTE
FHSFR
FLUFQ
FOEOM
FQBLK
GAUVT
GJXCC
H13
H5~
HAR
HVGLF
HW0
HZ~
IOX
J21
JXSIZ
KAQDR
KBUDW
KC5
KOP
KQ8
KSI
KSN
M-Z
M49
MBTAY
N9A
NGC
NLBLG
NOMLY
NTWIH
NU-
NVLIB
O0~
O9-
OAWHX
OBOKY
ODMLO
OHT
OJQWA
OJZSN
OK1
OVD
OWPYF
O~Y
P2P
PAFKI
PB-
PEELM
PQQKQ
Q1.
Q5Y
QBD
R44
RD5
RHF
RNI
ROL
ROX
ROZ
RUSNO
RW1
RXO
RZF
RZO
SV3
TCN
TEORI
TLC
TN5
TUS
TWZ
W8F
WHG
X7H
Y6R
YAYTL
YKOAZ
YNT
YSK
YXANX
ZCG
ZJWQK
ZKX
~91
~KM
CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
ID FETCH-LOGICAL-c386t-f0953e5b207c5a9edc98d31b0684a0df31efcab403d662fa27dc8264847b4e973
ISSN 0032-0781
IngestDate Fri Oct 25 11:58:46 EDT 2024
Thu Sep 12 17:20:24 EDT 2024
Wed Oct 16 00:39:30 EDT 2024
Wed Aug 28 03:17:54 EDT 2024
IsPeerReviewed true
IsScholarly true
Issue 3
Keywords Callus formation
WOX
Auxin
Organ asymmetry
Grafting
Arabidopsis thaliana
Language English
License This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/pages/standard-publication-reuse-rights)
The Author(s) 2023. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c386t-f0953e5b207c5a9edc98d31b0684a0df31efcab403d662fa27dc8264847b4e973
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0002-9209-8230
0000-0001-9474-5131
0000-0002-1405-7716
0000-0002-1828-0966
PMID 36263676
PQID 2726923115
PQPubID 23479
PageCount 12
ParticipantIDs proquest_miscellaneous_2726923115
crossref_primary_10_1093_pcp_pcac146
pubmed_primary_36263676
oup_primary_10_1093_pcp_pcac146
PublicationCentury 2000
PublicationDate 2023-03-15
PublicationDateYYYYMMDD 2023-03-15
PublicationDate_xml – month: 03
  year: 2023
  text: 2023-03-15
  day: 15
PublicationDecade 2020
PublicationPlace UK
PublicationPlace_xml – name: UK
– name: Japan
PublicationTitle Plant and cell physiology
PublicationTitleAlternate Plant Cell Physiol
PublicationYear 2023
Publisher Oxford University Press
Publisher_xml – name: Oxford University Press
References Iwase (2023031515261857700_) 2021; 232
Ikeuchi (2023031515261857700_) 2022; 188
Stobbe (2023031515261857700_) 2002; 89
Sachs (2023031515261857700_) 1981; 9
Sena (2023031515261857700_) 2009; 457
Reinhardt (2023031515261857700_) 2000; 12
Liu (2023031515261857700_) 2014; 26
Iwase (2023031515261857700_) 2011; 21
Asahina (2023031515261857700_) 2011; 108
Iwase (2023031515261857700_) 2017; 29
Matsuoka (2023031515261857700_) 2016; 57
Yamada (2023031515261857700_) 2022; 135
Reinhardt (2023031515261857700_) 2003; 130
Amano (2023031515261857700_) 2020; 61
Kurotani (2023031515261857700_) 2020; 30
Zhang (2023031515261857700_) 2020; 30
Valvekens (2023031515261857700_) 1988; 85
Jacobs (2023031515261857700_) 1952; 39
Ikeuchi (2023031515261857700_) 2020; 57
Melnyk (2023031515261857700_) 2018; 115
Ikeuchi (2023031515261857700_) 2016; 143
Suer (2023031515261857700_) 2011; 23
Zhang (2023031515261857700_) 2022; 32
Birnbaum (2023031515261857700_) 2008; 132
Ikeuchi (2023031515261857700_) 2019; 70
Nishihama (2023031515261857700_) 2015; 128
O’Malley (2023031515261857700_) 2016; 165
Pitaksaringkarn (2023031515261857700_) 2014; 80
Chupeau (2023031515261857700_) 2013; 25
Rymen (2023031515261857700_) 2019; 2
Ikeuchi (2023031515261857700_) 2017; 175
Radhakrishnan (2023031515261857700_) 2020; 30: 147
Benková (2023031515261857700_) 2003; 115
Matsuoka (2023031515261857700_) 2021; 4
Zhai (2023031515261857700_) 2021; 7
Jeffree (2023031515261857700_) 1983; 93
Parkinson (2023031515261857700_) 1982; 91
Hofhuis (2023031515261857700_) 2013; 23
Notaguchi (2023031515261857700_) 2020; 369
Takebe (2023031515261857700_) 1971; 58
Romera-Branchat (2023031515261857700_) 2012; 73
Ma (2023031515261857700_) 2019; 10
Melnyk (2023031515261857700_) 2015; 25
Ishida (2023031515261857700_) 2022; 63
References_xml – volume: 23
  start-page: 956
  year: 2013
  ident: 2023031515261857700_
  article-title: Phyllotaxis and rhizotaxis in Arabidopsis are modified by three PLETHORA transcription factors
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2013.04.048
  contributor:
    fullname: Hofhuis
– volume: 39
  start-page: 301
  year: 1952
  ident: 2023031515261857700_
  article-title: The role of auxin in differentiation of xylem around a wound
  publication-title: Am. J. Bot.
  doi: 10.1002/j.1537-2197.1952.tb14277.x
  contributor:
    fullname: Jacobs
– volume: 188
  start-page: 425
  year: 2022
  ident: 2023031515261857700_
  article-title: Wound-inducible WUSCHEL RELATED HOMEOBOX 13 is required for callus growth and organ reconnection
  publication-title: Plant Physiol.
  doi: 10.1093/plphys/kiab510
  contributor:
    fullname: Ikeuchi
– volume: 58
  start-page: 318
  year: 1971
  ident: 2023031515261857700_
  article-title: Regeneration of whole plants from isolated mesophyll protoplasts of tobacco
  publication-title: Naturwissenschaften
  doi: 10.1007/BF00624737
  contributor:
    fullname: Takebe
– volume: 57
  start-page: 2620
  year: 2016
  ident: 2023031515261857700_
  article-title: Differential cellular control by cotyledon-derived phytohormones involved in graft reunion of Arabidopsis hypocotyls
  publication-title: Plant Cell Physiol.
  doi: 10.1093/pcp/pcw177
  contributor:
    fullname: Matsuoka
– volume: 23
  start-page: 3247
  year: 2011
  ident: 2023031515261857700_
  article-title: WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis
  publication-title: Plant Cell
  doi: 10.1105/tpc.111.087874
  contributor:
    fullname: Suer
– volume: 4
  year: 2021
  ident: 2023031515261857700_
  article-title: Wound-inducible ANAC071 and ANAC096 transcription factors promote cambial cell formation in incised Arabidopsis inflorescence stems
  publication-title: Commun. Biol.
  doi: 10.1038/s42003-021-01895-8
  contributor:
    fullname: Matsuoka
– volume: 369
  start-page: 698
  year: 2020
  ident: 2023031515261857700_
  article-title: Cell-cell adhesion in plant grafting is facilitated by β-1,4-glucanases
  publication-title: Science
  doi: 10.1126/science.abc3710
  contributor:
    fullname: Notaguchi
– volume: 143
  start-page: 1442
  year: 2016
  ident: 2023031515261857700_
  article-title: Plant regeneration: cellular origins and molecular mechanisms
  publication-title: Development
  doi: 10.1242/dev.134668
  contributor:
    fullname: Ikeuchi
– volume: 80
  start-page: 604
  year: 2014
  ident: 2023031515261857700_
  article-title: XTH 20 and XTH 19 regulated by ANAC 071 under auxin flow are involved in cell proliferation in incised Arabidopsis inflorescence stems
  publication-title: Plant J.
  doi: 10.1111/tpj.12654
  contributor:
    fullname: Pitaksaringkarn
– volume: 21
  start-page: 508
  year: 2011
  ident: 2023031515261857700_
  article-title: The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2011.02.020
  contributor:
    fullname: Iwase
– volume: 57
  start-page: 72
  year: 2020
  ident: 2023031515261857700_
  article-title: How do plants transduce wound signals to induce tissue repair and organ regeneration?
  publication-title: Curr. Opin Plant Biol.
  doi: 10.1016/j.pbi.2020.06.007
  contributor:
    fullname: Ikeuchi
– volume: 63
  start-page: 384
  year: 2022
  ident: 2023031515261857700_
  article-title: Diminished auxin signaling triggers cellular reprogramming by inducing a regeneration factor in the liverwort Marchantia polymorpha
  publication-title: Plant Cell Physiol.
  doi: 10.1093/pcp/pcac004
  contributor:
    fullname: Ishida
– volume: 9
  start-page: 151
  year: 1981
  ident: 2023031515261857700_
  article-title: The control of the patterned differentiation of vascular tissues
  publication-title: Adv. Bot. Res.
  doi: 10.1016/S0065-2296(08)60351-1
  contributor:
    fullname: Sachs
– volume: 30
  start-page: 4857
  year: 2020
  ident: 2023031515261857700_
  article-title: A WOX/auxin biosynthesis module controls growth to shape leaf form
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2020.09.037
  contributor:
    fullname: Zhang
– volume: 175
  start-page: 1158
  year: 2017
  ident: 2023031515261857700_
  article-title: Wounding triggers callus formation via dynamic hormonal and transcriptional changes
  publication-title: Plant Physiol.
  doi: 10.1104/pp.17.01035
  contributor:
    fullname: Ikeuchi
– volume: 130
  start-page: 4073
  year: 2003
  ident: 2023031515261857700_
  article-title: Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem
  publication-title: Development
  doi: 10.1242/dev.00596
  contributor:
    fullname: Reinhardt
– volume: 32
  start-page: 1883
  year: 2022
  ident: 2023031515261857700_
  article-title: Cell-wall damage activates DOF transcription factors to promote wound healing and tissue regeneration in Arabidopsis thaliana
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2022.02.069
  contributor:
    fullname: Zhang
– volume: 108
  start-page: 16128
  year: 2011
  ident: 2023031515261857700_
  article-title: Spatially selective hormonal control of RAP2.6L and ANAC071 transcription factors involved in tissue reunion in Arabidopsis
  publication-title: Proc. Natl Acad. Sci.
  doi: 10.1073/pnas.1110443108
  contributor:
    fullname: Asahina
– volume: 30
  year: 2020
  ident: 2023031515261857700_
  article-title: Host-parasite tissue adhesion by a secreted type of β-1,4-glucanase in the parasitic plant Phtheirospermum japonicum
  publication-title: Commun. Biol.
  doi: 10.1038/s42003-020-01143-5
  contributor:
    fullname: Kurotani
– volume: 25
  start-page: 2444
  year: 2013
  ident: 2023031515261857700_
  article-title: Characterization of the early events leading to totipotency in an Arabidopsis protoplast liquid culture by temporal transcript profiling
  publication-title: Plant Cell
  doi: 10.1105/tpc.113.109538
  contributor:
    fullname: Chupeau
– volume: 70
  start-page: 377
  year: 2019
  ident: 2023031515261857700_
  article-title: Molecular mechanisms of plant regeneration
  publication-title: Annu. Rev. Plant Biol.
  doi: 10.1146/annurev-arplant-050718-100434
  contributor:
    fullname: Ikeuchi
– volume: 29
  start-page: 54
  year: 2017
  ident: 2023031515261857700_
  article-title: WIND1 promotes shoot regeneration through transcriptional activation of ENHANCER OF SHOOT REGENERATION1 in Arabidopsis
  publication-title: Plant Cell
  doi: 10.1105/tpc.16.00623
  contributor:
    fullname: Iwase
– volume: 26
  start-page: 1081
  year: 2014
  ident: 2023031515261857700_
  article-title: WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis
  publication-title: Plant Cell
  doi: 10.1105/tpc.114.122887
  contributor:
    fullname: Liu
– volume: 89
  start-page: 773
  year: 2002
  ident: 2023031515261857700_
  article-title: Developmental stages and fine structure of surface callus formed after debarking of living lime trees (Tilia sp.)
  publication-title: Ann. Bot.
  doi: 10.1093/aob/mcf137
  contributor:
    fullname: Stobbe
– volume: 7
  start-page: 1453
  year: 2021
  ident: 2023031515261857700_
  article-title: Pluripotency acquisition in the middle cell layer of callus is required for organ regeneration
  publication-title: Nat. Plants
  doi: 10.1038/s41477-021-01015-8
  contributor:
    fullname: Zhai
– volume: 128
  start-page: 407
  year: 2015
  ident: 2023031515261857700_
  article-title: Phytochrome-mediated regulation of cell division and growth during regeneration and sporeling development in the liverwort Marchantia polymorpha
  publication-title: J. Plant Res.
  doi: 10.1007/s10265-015-0724-9
  contributor:
    fullname: Nishihama
– volume: 93
  start-page: 491
  year: 1983
  ident: 2023031515261857700_
  article-title: Development of intercellular connections between opposing cells in a graft union
  publication-title: New Phytol.
  doi: 10.1111/j.1469-8137.1983.tb02701.x
  contributor:
    fullname: Jeffree
– volume: 91
  start-page: 711
  year: 1982
  ident: 2023031515261857700_
  article-title: Graft formation in cultured, explanted internodes
  publication-title: New Phytol.
  doi: 10.1111/j.1469-8137.1982.tb03350.x
  contributor:
    fullname: Parkinson
– volume: 115
  start-page: E2447
  year: 2018
  ident: 2023031515261857700_
  article-title: Transcriptome dynamics at Arabidopsis graft junctions reveal an intertissue recognition mechanism that activates vascular regeneration
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.1718263115
  contributor:
    fullname: Melnyk
– volume: 30: 147
  year: 2020
  ident: 2023031515261857700_
  article-title: A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context
  publication-title: Development
  doi: 10.1242/dev.185710
  contributor:
    fullname: Radhakrishnan
– volume: 12
  start-page: 507
  year: 2000
  ident: 2023031515261857700_
  article-title: Auxin regulates the initiation and radial position of plant lateral organs
  publication-title: Plant Cell
  doi: 10.1105/tpc.12.4.507
  contributor:
    fullname: Reinhardt
– volume: 10
  year: 2019
  ident: 2023031515261857700_
  article-title: WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-019-13074-9
  contributor:
    fullname: Ma
– volume: 61
  start-page: 353
  year: 2020
  ident: 2023031515261857700_
  article-title: Molecular basis for natural vegetative propagation via regeneration in North American lake cress, Rorippa aquatica (Brassicaceae)
  publication-title: Plant Cell Physiol.
  doi: 10.1093/pcp/pcz202
  contributor:
    fullname: Amano
– volume: 457
  start-page: 1150
  year: 2009
  ident: 2023031515261857700_
  article-title: Organ regeneration does not require a functional stem cell niche in plants
  publication-title: Nature
  doi: 10.1038/nature07597
  contributor:
    fullname: Sena
– volume: 232
  start-page: 734
  year: 2021
  ident: 2023031515261857700_
  article-title: WIND transcription factors orchestrate wound-induced callus formation, vascular reconnection and defense response in Arabidopsis
  publication-title: New Phytol.
  doi: 10.1111/nph.17594
  contributor:
    fullname: Iwase
– volume: 73
  start-page: 37
  year: 2012
  ident: 2023031515261857700_
  article-title: The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit
  publication-title: Plant J.
  doi: 10.1111/tpj.12010
  contributor:
    fullname: Romera-Branchat
– volume: 135
  start-page: 377
  year: 2022
  ident: 2023031515261857700_
  article-title: Spatiotemporal plant hormone analysis from cyosections using laser microdissection-liquid chromatography-mass spectrometry
  publication-title: J. Plant Res.
  doi: 10.1007/s10265-021-01360-x
  contributor:
    fullname: Yamada
– volume: 25
  start-page: R183
  year: 2015
  ident: 2023031515261857700_
  article-title: Plant grafting
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2015.01.029
  contributor:
    fullname: Melnyk
– volume: 2
  year: 2019
  ident: 2023031515261857700_
  article-title: Histone acetylation orchestrates wound-induced transcriptional activation and cellular reprogramming in Arabidopsis
  publication-title: Commun. Biol.
  doi: 10.1038/s42003-019-0646-5
  contributor:
    fullname: Rymen
– volume: 132
  start-page: 697
  year: 2008
  ident: 2023031515261857700_
  article-title: Slicing across kingdoms: regeneration in plants and animals
  publication-title: Cell
  doi: 10.1016/j.cell.2008.01.040
  contributor:
    fullname: Birnbaum
– volume: 25
  start-page: 1306
  year: 2015
  ident: 2023031515261857700_
  article-title: A developmental framework for graft formation and vascular reconnection in Arabidopsis thaliana
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2015.03.032
  contributor:
    fullname: Melnyk
– volume: 115
  start-page: 591
  year: 2003
  ident: 2023031515261857700_
  article-title: Local, efflux-dependent auxin gradients as a common module for plant organ formation
  publication-title: Cell
  doi: 10.1016/S0092-8674(03)00924-3
  contributor:
    fullname: Benková
– volume: 165
  start-page: 1280
  year: 2016
  ident: 2023031515261857700_
  article-title: Cistrome and epicistrome features shape the regulatory DNA landscape
  publication-title: Cell
  doi: 10.1016/j.cell.2016.04.038
  contributor:
    fullname: O’Malley
– volume: 85
  start-page: 5536
  year: 1988
  ident: 2023031515261857700_
  article-title: Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.85.15.5536
  contributor:
    fullname: Valvekens
SSID ssj0007830
Score 2.4957204
Snippet Abstract Plants have the regenerative ability to reconnect cut organs, which is physiologically important to survive severe tissue damage. The ability to...
Plants have the regenerative ability to reconnect cut organs, which is physiologically important to survive severe tissue damage. The ability to reconnect...
SourceID proquest
crossref
pubmed
oup
SourceType Aggregation Database
Index Database
Publisher
StartPage 305
SubjectTerms Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Biological Transport
Gene Expression Regulation, Plant
Homeodomain Proteins - genetics
Homeodomain Proteins - metabolism
Indoleacetic Acids - metabolism
Plants - metabolism
Title Auxin-Induced WUSCHEL-RELATED HOMEOBOX13 Mediates Asymmetric Activity of Callus Formation upon Cutting
URI https://www.ncbi.nlm.nih.gov/pubmed/36263676
https://search.proquest.com/docview/2726923115
Volume 64
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lj9MwELZgAYkLguVVnkbaW5XdOM7z2K1SBehuD9uKcooc2xGrpUlFG0H59YxjJ2lYhBYuo8hy5uD5NJ4ZzwOhI5eJiORCWi4hQERALfCzmMUysJVpkMMtqGqHz879ZOF-WHrLLk-3ri7ZZsf85x_rSv5HqrAGclVVsv8g2ZYpLMA3yBcoSBjojWQ8qn5cFpaavqFe8T8tLsZJPLXUFAzQR8NkdhbPTmdLQuvnGGVUgjR2q5UaosWHI24GR-gKra_VZjhpKhmH1RrIuKqTovftVzXjSOekq4i_jov0AvNzVrCr2iBN2A4c-k7Dbb4oWJRapZdXl62qZ9_1SOwL2L5qlz9Xze7YLJrYhENVcpauzjyWWp_C3WdFtu4H3Chc3bbcAIvuaU9qe3sXMdVFmNd0vO5_tebrmjLexDB7vbTPZ-lkMZ2m83g5v43uOKCG6kf89x_bezoIqW0qNoHlCTA8Mex6Nkqv7vGa-1GbIfOH6IHxH_BIg-ERuiWLQ3RPTxTdHaK7pyVY-7vHKO9hA_-GDdxhAzfYwB02cIMNXOZYYwO32MAKG9hg4wlaTOL5OLHMTA2L09DfWrnqLyi9zLED7rFICh6FgpLM9kOX2SKnROacZa5Nhe87OXMCwUOVBekGmSujgD5FB0VZyOcIe6oRFFisYENSV_qSEcchapwBEZmAHwfoqDnFdK1bp6Q65YGmcNipOewBegsn_Pcd75rTT0H5KXyzQpbVJnUCx1ceCvEG6JkWS8uo7rPkB_6LG_z9Et3v4PsKHWy_VfI1GJvb7E2NmV-uNoEm
link.rule.ids 315,783,787,27936,27937
linkProvider Flying Publisher
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=Auxin-Induced+WUSCHEL-RELATED+HOMEOBOX13+Mediates+Asymmetric+Activity+of+Callus+Formation+upon+Cutting&rft.jtitle=Plant+and+cell+physiology&rft.au=Tanaka%2C+Hayato&rft.au=Hashimoto%2C+Naoki&rft.au=Kawai%2C+Satomi&rft.au=Yumoto%2C+Emi&rft.date=2023-03-15&rft.eissn=1471-9053&rft.volume=64&rft.issue=3&rft.spage=305&rft.epage=316&rft_id=info:doi/10.1093%2Fpcp%2Fpcac146&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0032-0781&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0032-0781&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0032-0781&client=summon