Stromule extension along microtubules coordinated with actin-mediated anchoring guides perinuclear chloroplast movement during innate immunity

Dynamic tubular extensions from chloroplasts called stromules have recently been shown to connect with nuclei and function during innate immunity. We demonstrate that stromules extend along microtubules (MTs) and MT organization directly affects stromule dynamics since stabilization of MTs chemicall...

Full description

Saved in:
Bibliographic Details
Published ineLife Vol. 7
Main Authors Kumar, Amutha Sampath, Park, Eunsook, Nedo, Alexander, Alqarni, Ali, Ren, Li, Hoban, Kyle, Modla, Shannon, McDonald, John H, Kambhamettu, Chandra, Dinesh-Kumar, Savithramma P, Caplan, Jeffrey Lewis
Format Journal Article
LanguageEnglish
Published England eLife Science Publications, Ltd 17.01.2018
eLife Sciences Publications Ltd
eLife Sciences Publications, Ltd
Subjects
Actin
Actins - metabolism
Analysis
Cell Biology
Chloroplasts
Chloroplasts - metabolism
cytoskeleton
Epidermal Cells - metabolism
Filaments
Immune response
Immunity, Innate
Innate immunity
Medical research
Microtubules
Microtubules - metabolism
Morphology
Motility
Movement
Muscle proteins
Nicotiana
Nicotiana benthamiana
Nuclei
organelle movement
Parks
Photosynthesis
Plant biochemistry
Plant Biology
Plant Epidermis - cytology
Plant Epidermis - immunology
plant innate immunity
Proteins
Scientists
Soil sciences
Statistical analysis
stromules
Transmission electron microscopy
Viral proteins
United States > US
California
organelle movement
Nicotiana benthamiana
cell biology
cytoskeleton
plant innate immunity
chloroplasts
plant biology
stromules
Online AccessGet full text

Cover

Abstract Dynamic tubular extensions from chloroplasts called stromules have recently been shown to connect with nuclei and function during innate immunity. We demonstrate that stromules extend along microtubules (MTs) and MT organization directly affects stromule dynamics since stabilization of MTs chemically or genetically increases stromule numbers and length. Although actin filaments (AFs) are not required for stromule extension, they provide anchor points for stromules. Interestingly, there is a strong correlation between the direction of stromules from chloroplasts and the direction of chloroplast movement. Stromule-directed chloroplast movement was observed in steady-state conditions without immune induction, suggesting it is a general function of stromules in epidermal cells. Our results show that MTs and AFs may facilitate perinuclear clustering of chloroplasts during an innate immune response. We propose a model in which stromules extend along MTs and connect to AF anchor points surrounding nuclei, facilitating stromule-directed movement of chloroplasts to nuclei during innate immunity.
AbstractList Dynamic tubular extensions from chloroplasts called stromules have recently been shown to connect with nuclei and function during innate immunity. We demonstrate that stromules extend along microtubules (MTs) and MT organization directly affects stromule dynamics since stabilization of MTs chemically or genetically increases stromule numbers and length. Although actin filaments (AFs) are not required for stromule extension, they provide anchor points for stromules. Interestingly, there is a strong correlation between the direction of stromules from chloroplasts and the direction of chloroplast movement. Stromule-directed chloroplast movement was observed in steady-state conditions without immune induction, suggesting it is a general function of stromules in epidermal cells. Our results show that MTs and AFs may facilitate perinuclear clustering of chloroplasts during an innate immune response. We propose a model in which stromules extend along MTs and connect to AF anchor points surrounding nuclei, facilitating stromule-directed movement of chloroplasts to nuclei during innate immunity.
Dynamic tubular extensions from chloroplasts called stromules have recently been shown to connect with nuclei and function during innate immunity. We demonstrate that stromules extend along microtubules (MTs) and MT organization directly affects stromule dynamics since stabilization of MTs chemically or genetically increases stromule numbers and length. Although actin filaments (AFs) are not required for stromule extension, they provide anchor points for stromules. Interestingly, there is a strong correlation between the direction of stromules from chloroplasts and the direction of chloroplast movement. Stromule-directed chloroplast movement was observed in steady-state conditions without immune induction, suggesting it is a general function of stromules in epidermal cells. Our results show that MTs and AFs may facilitate perinuclear clustering of chloroplasts during an innate immune response. We propose a model in which stromules extend along MTs and connect to AF anchor points surrounding nuclei, facilitating stromule-directed movement of chloroplasts to nuclei during innate immunity. Within a plant’s cells, compartments called chloroplasts harvest energy from sunlight. This process, termed photosynthesis, keeps the plant alive and growing. Yet this is not all that chloroplasts do. For example, if a harmful microbe infects the plant, its chloroplasts rapidly change shape and move toward the cell’s nucleus – the compartment of the cell that contains the bulk of the plant’s genetic material. The chloroplasts then send warning signals to the nucleus that boost the plant’s defenses. In 2015, researchers showed that, during an infection, tiny tubes called stromules extend out from chloroplasts and make contact with the nucleus. Stromules are flexible structures that can extend and retract. However, it is not yet understood what exactly the stromules do, or how they establish connections with the nucleus. Some scientists had suggested the internal skeleton of the cell – a complex network of protein filaments called actin and microtubules – might regulate the movements of the stromules. Now, Kumar, Park et al. – including several researchers from the 2015 study – have monitored the interaction between stromules and this internal “cytoskeleton” in leaf cells from a plant called Nicotiana benthamiana . Stromules, microtubules and actin were marked with fluorescent tags, which allowed them to be tracked under a microscope. This showed that the stromules actively extend along microtubules and anchor to a network of actin filaments. Further work showed that chloroplasts move in the direction of the stromules. This suggests that chloroplast movement may actually be directed by these structures. This movement was seen in healthy plants growing under normal conditions, suggesting that it may be a more general occurrence in plants. Next, Kumar, Park et al. used a viral protein to provoke an immune response in the plants, and saw that a larger number of chloroplasts moved and clustered around the nucleus. This chloroplast clustering was also guided by stromules anchored to the actin filaments that surround the nucleus. These findings shed new light on how chloroplasts communicate with the nucleus. Future work is needed to determine if stromules just guide chloroplast movement or if they provide a physical force that drives this process.
Dynamic tubular extensions from chloroplasts called stromules have recently been shown to connect with nuclei and function during innate immunity. We demonstrate that stromules extend along microtubules (MTs) and MT organization directly affects stromule dynamics since stabilization of MTs chemically or genetically increases stromule numbers and length. Although actin filaments (AFs) are not required for stromule extension, they provide anchor points for stromules. Interestingly, there is a strong correlation between the direction of stromules from chloroplasts and the direction of chloroplast movement. Stromule-directed chloroplast movement was observed in steady-state conditions without immune induction, suggesting it is a general function of stromules in epidermal cells. Our results show that MTs and AFs may facilitate perinuclear clustering of chloroplasts during an innate immune response. We propose a model in which stromules extend along MTs and connect to AF anchor points surrounding nuclei, facilitating stromule-directed movement of chloroplasts to nuclei during innate immunity. Within a plant’s cells, compartments called chloroplasts harvest energy from sunlight. This process, termed photosynthesis, keeps the plant alive and growing. Yet this is not all that chloroplasts do. For example, if a harmful microbe infects the plant, its chloroplasts rapidly change shape and move toward the cell’s nucleus – the compartment of the cell that contains the bulk of the plant’s genetic material. The chloroplasts then send warning signals to the nucleus that boost the plant’s defenses. In 2015, researchers showed that, during an infection, tiny tubes called stromules extend out from chloroplasts and make contact with the nucleus. Stromules are flexible structures that can extend and retract. However, it is not yet understood what exactly the stromules do, or how they establish connections with the nucleus. Some scientists had suggested the internal skeleton of the cell – a complex network of protein filaments called actin and microtubules – might regulate the movements of the stromules. Now, Kumar, Park et al. – including several researchers from the 2015 study – have monitored the interaction between stromules and this internal “cytoskeleton” in leaf cells from a plant called Nicotiana benthamiana. Stromules, microtubules and actin were marked with fluorescent tags, which allowed them to be tracked under a microscope. This showed that the stromules actively extend along microtubules and anchor to a network of actin filaments. Further work showed that chloroplasts move in the direction of the stromules. This suggests that chloroplast movement may actually be directed by these structures. This movement was seen in healthy plants growing under normal conditions, suggesting that it may be a more general occurrence in plants. Next, Kumar, Park et al. used a viral protein to provoke an immune response in the plants, and saw that a larger number of chloroplasts moved and clustered around the nucleus. This chloroplast clustering was also guided by stromules anchored to the actin filaments that surround the nucleus. These findings shed new light on how chloroplasts communicate with the nucleus. Future work is needed to determine if stromules just guide chloroplast movement or if they provide a physical force that drives this process.
Audience Academic
Author Nedo, Alexander
Dinesh-Kumar, Savithramma P
Kumar, Amutha Sampath
Alqarni, Ali
Kambhamettu, Chandra
Park, Eunsook
McDonald, John H
Caplan, Jeffrey Lewis
Ren, Li
Modla, Shannon
Hoban, Kyle
Author_xml – sequence: 1
  givenname: Amutha Sampath
  surname: Kumar
  fullname: Kumar, Amutha Sampath
  organization: Delaware Biotechnology Institute, University of Delaware, Newark, United States
– sequence: 2
  givenname: Eunsook
  orcidid: 0000-0003-2984-3039
  surname: Park
  fullname: Park, Eunsook
  organization: The Genome Center, College of Biological Sciences, University of California, Davis, Davis, United States
– sequence: 3
  givenname: Alexander
  surname: Nedo
  fullname: Nedo, Alexander
  organization: Department of Biological Sciences, College of Arts and Sciences, University of Delaware, Newark, United States
– sequence: 4
  givenname: Ali
  surname: Alqarni
  fullname: Alqarni, Ali
  organization: Department of Plant and Soil Sciences, College of Agriculture and Natural Resources, University of Delaware, Newark, United States
– sequence: 5
  givenname: Li
  surname: Ren
  fullname: Ren, Li
  organization: Department of Plant and Soil Sciences, College of Agriculture and Natural Resources, University of Delaware, Newark, United States
– sequence: 6
  givenname: Kyle
  surname: Hoban
  fullname: Hoban, Kyle
  organization: Department of Biological Sciences, College of Arts and Sciences, University of Delaware, Newark, United States
– sequence: 7
  givenname: Shannon
  surname: Modla
  fullname: Modla, Shannon
  organization: Delaware Biotechnology Institute, University of Delaware, Newark, United States
– sequence: 8
  givenname: John H
  surname: McDonald
  fullname: McDonald, John H
  organization: Department of Biological Sciences, College of Arts and Sciences, University of Delaware, Newark, United States
– sequence: 9
  givenname: Chandra
  surname: Kambhamettu
  fullname: Kambhamettu, Chandra
  organization: Department of Computer and Information Sciences, College of Engineering, University of Delaware, Newark, United States
– sequence: 10
  givenname: Savithramma P
  orcidid: 0000-0001-5738-316X
  surname: Dinesh-Kumar
  fullname: Dinesh-Kumar, Savithramma P
  organization: The Genome Center, College of Biological Sciences, University of California, Davis, Davis, United States
– sequence: 11
  givenname: Jeffrey Lewis
  orcidid: 0000-0002-3991-0912
  surname: Caplan
  fullname: Caplan, Jeffrey Lewis
  organization: Department of Plant and Soil Sciences, College of Agriculture and Natural Resources, University of Delaware, Newark, United States
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29338837$$D View this record in MEDLINE/PubMed
BookMark eNpdkltrFDEYhgep2Fp75b0MeKPI1pwncyOU4mFhQbAK3oUkk8ymzCRrDtX-CX-z2d1au-Ymp-d7k_fjfdoc-eBN0zyH4LyjlLw1K2fNOcIM0UfNCQIULAAn348erI-bs5SuQR0d4Rz2T5pj1GPMOe5Omt9XOYa5TKY1v7LxyQXfyin4sZ2djiEXVe9Sq0OIg_Mym6H96fK6lTo7v5jN4HZn0ut1iK6WjcUNtWBj6q7oycjY6vUUYthMMuV2DjdmNj63Q9nhzm9FWzfPxbt8-6x5bOWUzNndfNp8-_D-6-Wnxerzx-XlxWqhadfnBaOKKku7zmKrVad71EupENvaGwgniqKBWYIx0gNDgFgFNZPEWNJhzS3Ep81yrzsEeS020c0y3oogndgdhDgKGbOr_xeId8BQC0HHAZFaqb6nFEEzYAAJUapqvdtrbYqqDdHVXZTTgejhjXdrMYYbQTmknG4_8-pOIIYfxaQsZpe0mSbpTShJwJ73lDOGeEVf_odehxJ9bZVAAPSwmqX4HzXKasB5G-q7eisqLhjClAHWg0q9PqB08LmGYJQlJbG8-nLIvtmzNRMpRWPv7UEgtkEUuyCKXRAr_eJhR-7Zv7HDfwBU_t3f
CitedBy_id crossref_primary_10_1093_jxb_erac334
crossref_primary_10_3390_biom13040627
crossref_primary_10_1093_pcp_pcad098
crossref_primary_10_1111_nph_16650
crossref_primary_10_1111_mpp_12922
crossref_primary_10_1111_mpp_12840
crossref_primary_10_1038_s41467_021_22977_5
crossref_primary_10_1093_aob_mcae092
crossref_primary_10_3390_genes11060650
crossref_primary_10_3390_plants11040552
crossref_primary_10_1093_hr_uhad046
crossref_primary_10_1111_pce_14157
crossref_primary_10_3390_ijms23105568
crossref_primary_10_1080_15592324_2018_1500064
crossref_primary_10_1093_plphys_kiaa088
crossref_primary_10_1016_j_tplants_2022_11_001
crossref_primary_10_3389_fpls_2019_01665
crossref_primary_10_1111_mpp_13385
crossref_primary_10_3389_fpls_2021_637853
crossref_primary_10_1111_tpj_15287
crossref_primary_10_1094_MPMI_07_18_0195_FI
crossref_primary_10_1111_nph_18425
crossref_primary_10_1016_j_pbi_2020_10_005
crossref_primary_10_3389_fpls_2018_00754
crossref_primary_10_1002_pld3_124
crossref_primary_10_1016_j_pbi_2018_07_012
crossref_primary_10_1042_BST20221093
crossref_primary_10_1094_MPMI_05_18_0113_R
crossref_primary_10_3390_pathogens9010019
crossref_primary_10_1016_j_pbi_2022_102269
crossref_primary_10_1016_j_pbi_2019_08_002
crossref_primary_10_1093_plphys_kiac481
crossref_primary_10_1093_jxb_erad449
crossref_primary_10_1094_MPMI_09_23_0148_FI
crossref_primary_10_1016_j_pbi_2024_102529
crossref_primary_10_1111_nph_19149
crossref_primary_10_1111_tpj_15137
crossref_primary_10_1111_tpj_15416
crossref_primary_10_1093_jxb_erae177
crossref_primary_10_3390_ijms232415553
crossref_primary_10_1016_j_pbi_2018_07_003
crossref_primary_10_1111_nph_17929
crossref_primary_10_1140_epjst_e2020_000130_7
crossref_primary_10_1016_j_xplc_2023_100775
crossref_primary_10_1007_s12551_018_0470_z
crossref_primary_10_1093_plphys_kiab060
crossref_primary_10_3390_ijms23074043
crossref_primary_10_1111_nph_17076
crossref_primary_10_1016_j_freeradbiomed_2023_01_014
crossref_primary_10_1111_nph_16584
crossref_primary_10_1126_sciadv_adi7407
crossref_primary_10_1371_journal_pone_0245148
crossref_primary_10_1126_sciadv_abo0724
crossref_primary_10_1016_j_indcrop_2019_111781
crossref_primary_10_1093_pnasnexus_pgac225
crossref_primary_10_1146_annurev_virology_111821_122847
crossref_primary_10_1098_rstb_2019_0405
crossref_primary_10_1093_plphys_kiaa055
crossref_primary_10_1146_annurev_phyto_020620_115813
crossref_primary_10_1016_j_pmpp_2023_102000
crossref_primary_10_1186_s11658_021_00300_w
crossref_primary_10_3389_fpls_2023_1293906
Cites_doi 10.1093/mp/ssp094
10.1104/pp.108.123075
10.1038/nmeth.2019
10.1093/pcp/pcp055
10.1046/j.1365-313X.2003.01777.x
10.1105/tpc.109.071191
10.1007/BF01403955
10.1371/journal.pone.0076745
10.1002/(SICI)1097-0169(199910)44:2<110::AID-CM3>3.0.CO;2-O
10.1242/jcs.202275
10.1073/pnas.77.3.1561
10.1007/s004250050584
10.1385/1-59259-413-1:287
10.1111/j.1365-313X.2011.04800.x
10.1007/s00709-004-0073-3
10.1073/pnas.0906250106
10.1038/nsmb.2083
10.1111/jipb.12289
10.1104/pp.108.129346
10.1093/mp/ssp078
10.1111/tpj.13813
10.1038/srep09081
10.1055/s-2001-15204
10.1093/jxb/eri088
10.1093/jxb/ert414
10.1093/biomet/70.2.327
10.1186/1471-2229-7-6
10.1016/j.devcel.2015.05.011
10.3389/fpls.2016.00561
10.1104/pp.114.244335
10.1007/978-1-4939-1136-3_7
10.1104/pp.110.170480
10.1007/s00299-004-0824-9
10.1371/journal.pone.0146489
10.1007/s00709-006-0222-y
10.1091/mbc.02-01-0607
10.1073/pnas.1511570112
10.1111/j.1365-3040.2007.01768.x
10.3389/fpls.2015.00282
10.1016/j.cell.2007.12.031
10.1055/s-2006-924727
10.1038/nmeth.1220
10.1105/tpc.002303
10.1016/S0959-440X(00)00187-1
10.1111/j.0022-2720.2004.01317.x
10.1111/j.1365-3040.2007.01707.x
10.1111/pce.12483
10.1186/1471-2229-4-2
10.1083/jcb.19.1.239
10.1104/pp.107.113647
10.1038/ncb1057
10.1242/jcs.113.1.81
10.1186/1471-2229-11-115
10.1016/0092-8674(94)90283-6
10.1186/1471-2229-14-127
10.1111/j.1365-313X.2004.02164.x
10.3389/fpls.2017.01135
ContentType Journal Article
Copyright 2018, Kumar et al.
COPYRIGHT 2018 eLife Science Publications, Ltd.
2018, Kumar et al. This work is licensed under the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/3.0/ ) (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2018, Kumar et al 2018 Kumar et al
Copyright_xml – notice: 2018, Kumar et al.
– notice: COPYRIGHT 2018 eLife Science Publications, Ltd.
– notice: 2018, Kumar et al. This work is licensed under the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/3.0/ ) (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2018, Kumar et al 2018 Kumar et al
DBID CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
ISR
3V.
7X7
7XB
88E
88I
8FE
8FH
8FI
8FJ
8FK
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
FYUFA
GHDGH
GNUQQ
HCIFZ
K9.
LK8
M0S
M1P
M2P
M7P
PIMPY
PQEST
PQQKQ
PQUKI
PRINS
Q9U
7X8
5PM
DOA
DOI 10.7554/eLife.23625
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
Science in Context
ProQuest Central (Corporate)
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
Science Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central
ProQuest Central Essentials
Biological Science Collection
ProQuest Databases
Natural Science Collection
ProQuest One Community College
ProQuest Central Korea
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
Health & Medical Collection (Alumni Edition)
PML(ProQuest Medical Library)
Science Database (ProQuest)
Biological Science Database
Publicly Available Content Database
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
ProQuest Central Basic
MEDLINE - Academic
PubMed Central (Full Participant titles)
Directory of Open Access Journals
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
Publicly Available Content Database
ProQuest Central Student
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
ProQuest Central China
ProQuest Central
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Biological Science Collection
ProQuest Medical Library (Alumni)
ProQuest Science Journals (Alumni Edition)
ProQuest Biological Science Collection
ProQuest Central Basic
ProQuest Science Journals
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList Publicly Available Content Database


MEDLINE - Academic

CrossRef

MEDLINE
Database_xml – sequence: 1
  dbid: DOA
  name: Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  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: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 4
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
EISSN 2050-084X
ExternalDocumentID oai_doaj_org_article_2870e5f107804acbb995521ed30144bb
A623560690
10_7554_eLife_23625
29338837
Genre Journal Article
Research Support, N.I.H., Extramural
GeographicLocations United States--US
California
GeographicLocations_xml – name: United States--US
– name: California
GrantInformation_xml – fundername: NIGMS NIH HHS
  grantid: R01 GM097587
– fundername: NCRR NIH HHS
  grantid: S10 RR027273
– fundername: NIGMS NIH HHS
  grantid: P20 GM103446
– fundername: NIH HHS
  grantid: S10 OD016361
– fundername: ;
  grantid: S10 OD016361
– fundername: ;
  grantid: R01 GM097587
– fundername: ;
  grantid: S10 RR027273
– fundername: ;
  grantid: P20 GM103446
GroupedDBID 3V.
53G
5VS
7X7
88E
88I
8FE
8FH
8FI
8FJ
AAFWJ
AAKDD
ABUWG
ACGFO
ACGOD
ACPRK
ADBBV
ADRAZ
AENEX
AFKRA
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AOIJS
AZQEC
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
CCPQU
CGR
CUY
CVF
DIK
DWQXO
ECM
EIF
EMOBN
FRP
FYUFA
GNUQQ
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IEA
IHR
INH
INR
ISR
ITC
KQ8
LK8
M1P
M2P
M48
M7P
M~E
NPM
NQS
OK1
PGMZT
PIMPY
PQQKQ
PROAC
PSQYO
RHF
RHI
RNS
RPM
UKHRP
AAYXX
CITATION
AFPKN
7XB
8FK
K9.
PQEST
PQUKI
PRINS
Q9U
7X8
5PM
ID FETCH-LOGICAL-c579t-65b5bf577f3fcb7c929aab268819d484b52d6f4332cd6204fb1c6a4ef473c8f13
IEDL.DBID RPM
ISSN 2050-084X
IngestDate Tue Oct 22 15:12:53 EDT 2024
Tue Sep 17 21:04:25 EDT 2024
Fri Oct 25 09:27:04 EDT 2024
Wed Nov 27 16:53:55 EST 2024
Tue Nov 19 20:54:49 EST 2024
Thu Aug 01 20:15:21 EDT 2024
Fri Dec 06 02:18:52 EST 2024
Sat Nov 02 12:31:16 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Keywords organelle movement
Nicotiana benthamiana
cell biology
cytoskeleton
plant innate immunity
chloroplasts
plant biology
stromules
Language English
License 2018, Kumar et al.
http://creativecommons.org/licenses/by/4.0
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c579t-65b5bf577f3fcb7c929aab268819d484b52d6f4332cd6204fb1c6a4ef473c8f13
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
These authors contributed equally to this work.
Department of Plant Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul, Korea.
ORCID 0000-0003-2984-3039
0000-0002-3991-0912
0000-0001-5738-316X
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5815851/
PMID 29338837
PQID 2009162053
PQPubID 2045579
ParticipantIDs doaj_primary_oai_doaj_org_article_2870e5f107804acbb995521ed30144bb
pubmedcentral_primary_oai_pubmedcentral_nih_gov_5815851
proquest_miscellaneous_1989586628
proquest_journals_2009162053
gale_infotracmisc_A623560690
gale_incontextgauss_ISR_A623560690
crossref_primary_10_7554_eLife_23625
pubmed_primary_29338837
PublicationCentury 2000
PublicationDate 2018-01-17
PublicationDateYYYYMMDD 2018-01-17
PublicationDate_xml – month: 01
  year: 2018
  text: 2018-01-17
  day: 17
PublicationDecade 2010
PublicationPlace England
PublicationPlace_xml – name: England
– name: Cambridge
PublicationTitle eLife
PublicationTitleAlternate Elife
PublicationYear 2018
Publisher eLife Science Publications, Ltd
eLife Sciences Publications Ltd
eLife Sciences Publications, Ltd
Publisher_xml – name: eLife Science Publications, Ltd
– name: eLife Sciences Publications Ltd
– name: eLife Sciences Publications, Ltd
References Holzinger (bib25) 2007; 230
Moritz (bib41) 2001; 11
Natesan (bib43) 2005; 56
Lawrence (bib36) 1984; 52
Brunkard (bib5) 2015; 112
Buchner (bib6) 2007; 30
Higa (bib24) 2014; 65
Avisar (bib1) 2008; 146
Kandasamy (bib28) 1999; 44
Ho (bib57) 2016; 11
Kwok (bib32) 2003; 35
Gray (bib20) 2001; 3
Kumar (bib31) 2014
Riedl (bib48) 2008; 5
Caplan (bib10) 2008; 132
Erickson (bib14) 2017
Guillet (bib21) 2011; 18
Whitham (bib60) 1994; 78
Dinesh-Kumar (bib12) 2003; 236
Reisen (bib47) 2007; 7
Gunning (bib22) 2005; 225
Holzinger (bib26) 2007; 9
Ben-Nissan (bib3) 2008; 148
Erickson (bib16) 2014; 14
Kadota (bib27) 2009; 106
Schattat (bib50) 2011; 155
Bourett (bib4) 1999; 208
Caplan (bib9) 2015; 34
Gillespie (bib18) 2002; 14
Gray (bib19) 2012; 69
Barton (bib2) 2017
Takeuchi (bib56) 2017
Waters (bib59) 2004; 39
Chan (bib11) 2003; 5
Kwok (bib33) 2004; 4
Lu (bib39) 2017
Kwok (bib35) 2004; 214
Sokal (bib54) 1995
Suetsugu (bib55) 2016; 7
Köhler (bib30) 2000; 113
Hanson (bib23) 2008; 31
Era (bib13) 2009; 50
Park (bib46) 2013; 8
Vinh (bib58) 2002; 13
Fisher (bib17) 1983; 70
Menzel (bib40) 1994; 179
Moser (bib42) 2015; 38
Xu (bib61) 2015; 5
Sattarzadeh (bib49) 2009; 2
Cai (bib8) 2015; 57
Schindelin (bib53) 2012; 9
Kong (bib29) 2010; 22
Ledbetter (bib37) 1963; 19
Li (bib38) 2015; 6
Kwok (bib34) 2004; 23
Erickson (bib15) 2017; 8
Cai (bib7) 2014; 166
Oikawa (bib45) 2008; 148
Schattat (bib51) 2011; 11
Natesan (bib44) 2009; 2
Schiff (bib52) 1980; 77
References_xml – volume: 2
  start-page: 1351
  year: 2009
  ident: bib49
  article-title: A myosin XI tail domain homologous to the yeast myosin vacuole-binding domain interacts with plastids and stromules in Nicotiana benthamiana
  publication-title: Molecular Plant
  doi: 10.1093/mp/ssp094
  contributor:
    fullname: Sattarzadeh
– volume: 148
  start-page: 829
  year: 2008
  ident: bib45
  article-title: Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement
  publication-title: Plant Physiology
  doi: 10.1104/pp.108.123075
  contributor:
    fullname: Oikawa
– volume: 9
  start-page: 676
  year: 2012
  ident: bib53
  article-title: Fiji: an open-source platform for biological-image analysis
  publication-title: Nature Methods
  doi: 10.1038/nmeth.2019
  contributor:
    fullname: Schindelin
– volume: 50
  start-page: 1041
  year: 2009
  ident: bib13
  article-title: Application of Lifeact reveals F-actin dynamics in Arabidopsis thaliana and the liverwort, Marchantia polymorpha
  publication-title: Plant and Cell Physiology
  doi: 10.1093/pcp/pcp055
  contributor:
    fullname: Era
– volume: 35
  start-page: 16
  year: 2003
  ident: bib32
  article-title: Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum
  publication-title: The Plant Journal
  doi: 10.1046/j.1365-313X.2003.01777.x
  contributor:
    fullname: Kwok
– volume: 22
  start-page: 191
  year: 2010
  ident: bib29
  article-title: The {gamma}-tubulin complex protein GCP4 is required for organizing functional microtubule arrays in Arabidopsis thaliana
  publication-title: The Plant Cell
  doi: 10.1105/tpc.109.071191
  contributor:
    fullname: Kong
– volume: 179
  start-page: 166
  year: 1994
  ident: bib40
  article-title: An interconnected plastidom inAcetabularia: Implications for the mechanism of chloroplast motility
  publication-title: Protoplasma
  doi: 10.1007/BF01403955
  contributor:
    fullname: Menzel
– volume: 8
  start-page: e76745
  year: 2013
  ident: bib46
  article-title: Myosin XIK of Arabidopsis thaliana accumulates at the root hair tip and is required for fast root hair growth
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0076745
  contributor:
    fullname: Park
– volume: 44
  start-page: 110
  year: 1999
  ident: bib28
  article-title: Actin-organelle interaction: association with chloroplast in arabidopsis leaf mesophyll cells
  publication-title: Cell Motility and the Cytoskeleton
  doi: 10.1002/(SICI)1097-0169(199910)44:2<110::AID-CM3>3.0.CO;2-O
  contributor:
    fullname: Kandasamy
– start-page: jcs.202275
  year: 2017
  ident: bib2
  article-title: Chloroplast behaviour and interactions with other organelles in Arabidopsis thaliana pavement cells
  publication-title: Journal of Cell Science
  doi: 10.1242/jcs.202275
  contributor:
    fullname: Barton
– volume: 77
  start-page: 1561
  year: 1980
  ident: bib52
  article-title: Taxol stabilizes microtubules in mouse fibroblast cells
  publication-title: PNAS
  doi: 10.1073/pnas.77.3.1561
  contributor:
    fullname: Schiff
– volume: 208
  start-page: 472
  year: 1999
  ident: bib4
  article-title: Ultrastructure of chloroplast protuberances in rice leaves preserved by high-pressure freezing
  publication-title: Planta
  doi: 10.1007/s004250050584
  contributor:
    fullname: Bourett
– volume: 236
  start-page: 287
  year: 2003
  ident: bib12
  article-title: Virus-induced gene silencing
  publication-title: Methods in molecular biology
  doi: 10.1385/1-59259-413-1:287
  contributor:
    fullname: Dinesh-Kumar
– volume: 69
  start-page: 387
  year: 2012
  ident: bib19
  article-title: Plastid stromules are induced by stress treatments acting through abscisic acid
  publication-title: The Plant Journal
  doi: 10.1111/j.1365-313X.2011.04800.x
  contributor:
    fullname: Gray
– volume: 225
  start-page: 33
  year: 2005
  ident: bib22
  article-title: Plastid stromules: video microscopy of their outgrowth, retraction, tensioning, anchoring, branching, bridging, and tip-shedding
  publication-title: Protoplasma
  doi: 10.1007/s00709-004-0073-3
  contributor:
    fullname: Gunning
– volume: 106
  start-page: 13106
  year: 2009
  ident: bib27
  article-title: Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis
  publication-title: PNAS
  doi: 10.1073/pnas.0906250106
  contributor:
    fullname: Kadota
– volume: 18
  start-page: 915
  year: 2011
  ident: bib21
  article-title: Crystal structure of γ-tubulin complex protein GCP4 provides insight into microtubule nucleation
  publication-title: Nature Structural & Molecular Biology
  doi: 10.1038/nsmb.2083
  contributor:
    fullname: Guillet
– volume: 57
  start-page: 63
  year: 2015
  ident: bib8
  article-title: Organelle trafficking, the cytoskeleton, and pollen tube growth
  publication-title: Journal of Integrative Plant Biology
  doi: 10.1111/jipb.12289
  contributor:
    fullname: Cai
– volume: 148
  start-page: 1897
  year: 2008
  ident: bib3
  article-title: Arabidopsis casein kinase 1-like 6 contains a microtubule-binding domain and affects the organization of cortical microtubules,
  publication-title: Plant Physiology
  doi: 10.1104/pp.108.129346
  contributor:
    fullname: Ben-Nissan
– volume: 2
  start-page: 1262
  year: 2009
  ident: bib44
  article-title: Myosin XI is required for actin-associated movement of plastid stromules
  publication-title: Molecular Plant
  doi: 10.1093/mp/ssp078
  contributor:
    fullname: Natesan
– year: 2017
  ident: bib14
  article-title: The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana
  publication-title: The Plant Journal
  doi: 10.1111/tpj.13813
  contributor:
    fullname: Erickson
– volume: 5
  start-page: 9081
  year: 2015
  ident: bib61
  article-title: SOAX: a software for quantification of 3D biopolymer networks
  publication-title: Scientific Reports
  doi: 10.1038/srep09081
  contributor:
    fullname: Xu
– volume: 3
  start-page: 223
  year: 2001
  ident: bib20
  article-title: Stromules: mobile protrusions and interconnections between plastids
  publication-title: Plant Biology
  doi: 10.1055/s-2001-15204
  contributor:
    fullname: Gray
– volume: 56
  start-page: 787
  year: 2005
  ident: bib43
  article-title: Stromules: a characteristic cell-specific feature of plastid morphology
  publication-title: Journal of Experimental Botany
  doi: 10.1093/jxb/eri088
  contributor:
    fullname: Natesan
– volume: 65
  start-page: 2873
  year: 2014
  ident: bib24
  article-title: Plant nuclear photorelocation movement
  publication-title: Journal of Experimental Botany
  doi: 10.1093/jxb/ert414
  contributor:
    fullname: Higa
– volume: 70
  start-page: 327
  year: 1983
  ident: bib17
  article-title: A correlation coefficient for circular data
  publication-title: Biometrika
  doi: 10.1093/biomet/70.2.327
  contributor:
    fullname: Fisher
– volume: 7
  start-page: 6
  year: 2007
  ident: bib47
  article-title: Association of six YFP-myosin XI-tail fusions with mobile plant cell organelles
  publication-title: BMC Plant Biology
  doi: 10.1186/1471-2229-7-6
  contributor:
    fullname: Reisen
– volume: 52
  start-page: 77
  year: 1984
  ident: bib36
  article-title: Observations of microtubule-like structures within spinach plastids
  publication-title: Biology of the Cell
  contributor:
    fullname: Lawrence
– volume: 34
  start-page: 45
  year: 2015
  ident: bib9
  article-title: Chloroplast stromules function during innate immunity
  publication-title: Developmental Cell
  doi: 10.1016/j.devcel.2015.05.011
  contributor:
    fullname: Caplan
– volume-title: IEEE SigPort
  year: 2017
  ident: bib39
  article-title: Stromule branch tip detection based on accurate cell image segmentation
  contributor:
    fullname: Lu
– volume: 7
  start-page: 561
  year: 2016
  ident: bib55
  article-title: Evolution of the Cp-actin-based motility system of chloroplasts in green plants
  publication-title: Frontiers in Plant Science
  doi: 10.3389/fpls.2016.00561
  contributor:
    fullname: Suetsugu
– volume: 166
  start-page: 1359
  year: 2014
  ident: bib7
  article-title: Arabidopsis myosin XI: a motor rules the tracks
  publication-title: Plant Physiology
  doi: 10.1104/pp.114.244335
  contributor:
    fullname: Cai
– start-page: 189
  volume-title: Plastid Biology
  year: 2014
  ident: bib31
  doi: 10.1007/978-1-4939-1136-3_7
  contributor:
    fullname: Kumar
– volume: 155
  start-page: 1667
  year: 2011
  ident: bib50
  article-title: Plastid stromule branching coincides with contiguous endoplasmic reticulum dynamics
  publication-title: Plant Physiology
  doi: 10.1104/pp.110.170480
  contributor:
    fullname: Schattat
– volume: 23
  start-page: 188
  year: 2004
  ident: bib34
  article-title: Plastids and stromules interact with the nucleus and cell membrane in vascular plants
  publication-title: Plant Cell Reports
  doi: 10.1007/s00299-004-0824-9
  contributor:
    fullname: Kwok
– volume: 11
  start-page: e0146489
  year: 2016
  ident: bib57
  article-title: The formation of stromules in vitro from chloroplasts isolated from nicotiana benthamiana
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0146489
  contributor:
    fullname: Ho
– volume: 230
  start-page: 23
  year: 2007
  ident: bib25
  article-title: Temperature-sensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana
  publication-title: Protoplasma
  doi: 10.1007/s00709-006-0222-y
  contributor:
    fullname: Holzinger
– volume: 13
  start-page: 1144
  year: 2002
  ident: bib58
  article-title: Reconstitution and characterization of budding yeast gamma-tubulin complex
  publication-title: Molecular Biology of the Cell
  doi: 10.1091/mbc.02-01-0607
  contributor:
    fullname: Vinh
– volume: 112
  start-page: 10044
  year: 2015
  ident: bib5
  article-title: Chloroplasts extend stromules independently and in response to internal redox signals
  publication-title: PNAS
  doi: 10.1073/pnas.1511570112
  contributor:
    fullname: Brunkard
– volume: 31
  start-page: 646
  year: 2008
  ident: bib23
  article-title: Dynamic morphology of plastids and stromules in angiosperm plants
  publication-title: Plant, Cell & Environment
  doi: 10.1111/j.1365-3040.2007.01768.x
  contributor:
    fullname: Hanson
– volume: 6
  start-page: 282
  year: 2015
  ident: bib38
  article-title: The functions of the cytoskeleton and associated proteins during mitosis and cytokinesis in plant cells
  publication-title: Frontiers in Plant Science
  doi: 10.3389/fpls.2015.00282
  contributor:
    fullname: Li
– volume: 132
  start-page: 449
  year: 2008
  ident: bib10
  article-title: Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector
  publication-title: Cell
  doi: 10.1016/j.cell.2007.12.031
  contributor:
    fullname: Caplan
– volume: 9
  start-page: 400
  year: 2007
  ident: bib26
  article-title: Investigating cytoskeletal function in chloroplast protrusion formation in the arctic-alpine plant Oxyria digyna
  publication-title: Plant Biology
  doi: 10.1055/s-2006-924727
  contributor:
    fullname: Holzinger
– volume: 5
  start-page: 605
  year: 2008
  ident: bib48
  article-title: Lifeact: a versatile marker to visualize F-actin
  publication-title: Nature Methods
  doi: 10.1038/nmeth.1220
  contributor:
    fullname: Riedl
– volume: 14
  start-page: 1207
  year: 2002
  ident: bib18
  article-title: Functional analysis of a DNA-shuffled movement protein reveals that microtubules are dispensable for the cell-to-cell movement of tobacco mosaic virus
  publication-title: The Plant Cell Online
  doi: 10.1105/tpc.002303
  contributor:
    fullname: Gillespie
– volume: 11
  start-page: 174
  year: 2001
  ident: bib41
  article-title: Gamma-tubulin complexes and microtubule nucleation
  publication-title: Current Opinion in Structural Biology
  doi: 10.1016/S0959-440X(00)00187-1
  contributor:
    fullname: Moritz
– volume-title: Biometry: The Principles and Practice of Statistics in Biological Research
  year: 1995
  ident: bib54
  contributor:
    fullname: Sokal
– volume: 214
  start-page: 124
  year: 2004
  ident: bib35
  article-title: Stromules and the dynamic nature of plastid morphology
  publication-title: Journal of Microscopy
  doi: 10.1111/j.0022-2720.2004.01317.x
  contributor:
    fullname: Kwok
– volume: 30
  start-page: 1347
  year: 2007
  ident: bib6
  article-title: Effects of temperature and light on the formation of chloroplast protrusions in leaf mesophyll cells of high alpine plants
  publication-title: Plant, Cell & Environment
  doi: 10.1111/j.1365-3040.2007.01707.x
  contributor:
    fullname: Buchner
– volume: 38
  start-page: 1347
  year: 2015
  ident: bib42
  article-title: Chloroplast protrusions in leaves of Ranunculus glacialis L. respond significantly to different ambient conditions, but are not related to temperature stress
  publication-title: Plant, Cell & Environment
  doi: 10.1111/pce.12483
  contributor:
    fullname: Moser
– volume: 4
  start-page: 2
  year: 2004
  ident: bib33
  article-title: In vivo analysis of interactions between GFP-labeled microfilaments and plastid stromules
  publication-title: BMC Plant Biology
  doi: 10.1186/1471-2229-4-2
  contributor:
    fullname: Kwok
– volume: 19
  start-page: 239
  year: 1963
  ident: bib37
  article-title: A "microtubule" in plant cell fine structure
  publication-title: The Journal of Cell Biology
  doi: 10.1083/jcb.19.1.239
  contributor:
    fullname: Ledbetter
– volume: 146
  start-page: 1098
  year: 2008
  ident: bib1
  article-title: Myosin XI-K Is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana
  publication-title: Plant Physiology
  doi: 10.1104/pp.107.113647
  contributor:
    fullname: Avisar
– volume: 5
  start-page: 967
  year: 2003
  ident: bib11
  article-title: EB1 reveals mobile microtubule nucleation sites in Arabidopsis
  publication-title: Nature Cell Biology
  doi: 10.1038/ncb1057
  contributor:
    fullname: Chan
– volume: 113
  start-page: 81
  year: 2000
  ident: bib30
  article-title: Plastid tubules of higher plants are tissue-specific and developmentally regulated
  publication-title: Journal of Cell Science
  doi: 10.1242/jcs.113.1.81
  contributor:
    fullname: Köhler
– volume: 11
  start-page: 115
  year: 2011
  ident: bib51
  article-title: Induction of stromule formation by extracellular sucrose and glucose in epidermal leaf tissue of Arabidopsis thaliana
  publication-title: BMC Plant Biology
  doi: 10.1186/1471-2229-11-115
  contributor:
    fullname: Schattat
– volume: 78
  start-page: 1101
  year: 1994
  ident: bib60
  article-title: The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor
  publication-title: Cell
  doi: 10.1016/0092-8674(94)90283-6
  contributor:
    fullname: Whitham
– volume: 14
  start-page: 127
  year: 2014
  ident: bib16
  article-title: Agrobacterium-derived cytokinin influences plastid morphology and starch accumulation in Nicotiana benthamiana during transient assays
  publication-title: BMC Plant Biology
  doi: 10.1186/1471-2229-14-127
  contributor:
    fullname: Erickson
– start-page: 33
  volume-title: Cytoskeleton - Structure, Dynamics, Function and Disease
  year: 2017
  ident: bib56
  contributor:
    fullname: Takeuchi
– volume: 39
  start-page: 655
  year: 2004
  ident: bib59
  article-title: Stromule formation is dependent upon plastid size, plastid differentiation status and the density of plastids within the cell
  publication-title: The Plant Journal
  doi: 10.1111/j.1365-313X.2004.02164.x
  contributor:
    fullname: Waters
– volume: 8
  start-page: 1135
  year: 2017
  ident: bib15
  article-title: Plastid-nucleus distance alters the behavior of stromules
  publication-title: Frontiers in Plant Science
  doi: 10.3389/fpls.2017.01135
  contributor:
    fullname: Erickson
SSID ssj0000748819
Score 2.4806702
Snippet Dynamic tubular extensions from chloroplasts called stromules have recently been shown to connect with nuclei and function during innate immunity. We...
SourceID doaj
pubmedcentral
proquest
gale
crossref
pubmed
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
SubjectTerms Actin
Actins - metabolism
Analysis
Cell Biology
Chloroplasts
Chloroplasts - metabolism
cytoskeleton
Epidermal Cells - metabolism
Filaments
Immune response
Immunity, Innate
Innate immunity
Medical research
Microtubules
Microtubules - metabolism
Morphology
Motility
Movement
Muscle proteins
Nicotiana
Nicotiana benthamiana
Nuclei
organelle movement
Parks
Photosynthesis
Plant biochemistry
Plant Biology
Plant Epidermis - cytology
Plant Epidermis - immunology
plant innate immunity
Proteins
Scientists
Soil sciences
Statistical analysis
stromules
Transmission electron microscopy
Viral proteins
SummonAdditionalLinks – databaseName: Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Nb9QwELVQT70gEC0ECjJVr6H5sGPnWBBVQcCBUqk3y3bs3Uhdp9okh_4JfjMzTrraiAMXLjnEdpR4xjNvnJlnQs4Ko1muLU91ZnjKhGvSWjYCLpmsG14bEY8D-v6jurphX2_57d5RX5gTNtEDTxN3jj_iHPcQpciMaWtMXXNwOa6JsYAx0fpmxV4wFW2wAMXM66kgT4DLPHffWu8-FGCv-cIFRab-v-3xnkNaJkvueZ_LZ-TpDBvpxfS6z8kTF16Q39fDttuMd47GrWzc96L6rgsrusE0u2E00NZT20GA2QYAlQ3FbVeKtQwhjTUjeA_kvo5peHQ1tg0MQPLjgDzHekvtGgL67h4w9kA3XSQXH-hU20jbgA-lbSwxGR6OyM3l51-frtL5fIXUclEPacUNN54L4UtvjbCAlLQ2RYUz1zDJDC-ayiPBmW2Qtt6b3FaaOc9EaaXPy2NyELrgXhGaFQ7iGMMAbki41JKxrGQmK6XOXVHyhJw9Trm6n2g0FIQfKBkVJaOiZBLyEcWx64Lc1_EGaISaNUL9SyMScorCVMhuETB9ZqXHvldfrn-qCwB7APGqOkvIydzJdyBWC4vKLpsfNUHNi7rHEzsBTBdgthLyfteMIzFRLbhu7BWmoHFZVYVMyMtJcXZfA8iqlLIUCRELlVp87rIltOtI-c1ljv9vX_-P-XlDDgH1YQpjmosTcjBsR_cWkNVg3sVF9AcHKiRi
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Health & Medical Collection
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwELagXLggEK-UggzqNTQPO3ZOqCCqgoADpdLeLL-yG6nrLJvkwJ_gNzPjzS6NkLjkkEmiJDP2fDOe-UzIaWE0y7Xlqc4MT5nwLq2lE3DIZO14bUTcDujrt-rymn1e8MWUcOunssr9nBgnatdZzJGfYRY_rwqwmXebnynuGoWrq9MWGnfJvRxEaOFiIQ45FnCPEjzeri1PgOM881_axr8tYNbmM0cU-fr_nZVvuaV5yeQtH3TxkDyYwCM932n7Ebnjw2Py-2rYduvxxtOY0MbsF9U3XVjSNRbbDaMBWU9tB2FmGwBaOorJV4odDSGNnSN4DrS_isV4dDm2Dm5ACuSAbMd6S-0KwvpuA0h7oOsuUowPdNfhSNuAD6VtbDQZfj0h1xcff3y4TKddFlLLRT2kFTfcNFyIpmysERbwktamqPDPOSaZ4YWrGqQ5sw7J6xuT20oz3zBRWtnk5VNyFLrgnxOaFR6iGcMAdEg41JKxrGQmK6XOfVHyhJzuf7na7Mg0FAQhqBkVNaOiZhLyHtVxuAQZsOOJbrtU04BSuEDreQPRq8yYtsbUNQco4l2MEY1JyBtUpkKOi4BFNEs99r36dPVdnQPkA6BX1VlCTqaLmg7UamFo2bl4bwlqGtq9-muICXl9EOOdWK4WfDf2CgvRuKyqQibk2c5wDl8D-KqUshQJETOTmn3uXBLaVST-5jLHVdzj_7_WC3IfUB2WKKa5OCFHw3b0LwE5DeZVHB5_AC6uHIg
  priority: 102
  providerName: ProQuest
– databaseName: Scholars Portal Open Access Journals
  dbid: M48
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwELZKuXBBIF6BggzqNUseduycUEFUBVEOlJV6s2zH2Y2065RsIrV_or-ZGW921QDikkMcR7Fn7PnGmfmGkOPMaJZqy2OdGB4z4aq4lJWASyLLipdGhHJA59-Lszn7eskvD8iuGOc4gZt_unZYT2rerWbXv24-wIIH_DoTYA3fu29N7WYZbMX8HrmfgUnE2K7zEeeHLVmAnqblNj_vzz4TixSI-__enu_Yp2ns5B1jdPqIPBxRJD3Ziv0xOXD-Cbm96Lt2PawcDSfbeAxG9ar1C7rGqLt-MNC2obYFf7PxgDEriqewFFMbfBxSSPAeqMEyROXRxdBU0AG5kD3SHuuO2iX49-0VQO6ertvANd7TbaojbTy-lDYh46S_eUrmp59_fjqLx3ILseWi7OOCG25qLkSd19YIC8BJa5MVOHMVk8zwrCpq5DuzFbLY1ya1hWauZiK3sk7zZ-TQt969IDTJHLg1hgH6kHApJWNJzkySS526LOcROd5Nubrasmoo8EZQMipIRgXJROQjimP_CFJhhxttt1DjylL4p9bxGtxYmTBtjSlLDpjEVcFZNCYi71CYCskuPEbTLPSw2agvFz_UCWA_QHxFmUTkaHyobkGsFtaYnTbvNEHtVBQLeAK2zmAXi8jbfTP2xLg179phozAijcuiyGREnm8VZz8aAFq5lLmIiJio1GS40xbfLAMDOJcp_s59-f_PekUeALzDWMU4FUfksO8G9xogVG_ehOXxG-zhHxY
  priority: 102
  providerName: Scholars Portal
Title Stromule extension along microtubules coordinated with actin-mediated anchoring guides perinuclear chloroplast movement during innate immunity
URI https://www.ncbi.nlm.nih.gov/pubmed/29338837
https://www.proquest.com/docview/2009162053
https://search.proquest.com/docview/1989586628
https://pubmed.ncbi.nlm.nih.gov/PMC5815851
https://doaj.org/article/2870e5f107804acbb995521ed30144bb
Volume 7
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9swDBba7rLLsGEvb12gDb068UOy5GNbtOiGpSjaFcjNkGQ5MRDLQWIf9if2m0cqTpBgt110sKwgNknxo_yRJOQi0YrFyvBQRZqHTNgyzGUpYIhkXvJcC98OaHqf3T2zHzM-OyF8lwvjSftG12O3bMauXnhu5aoxkx1PbPIwveYyxq9Zk1NyCu73IET3268AnYzzbS6eAG85sT_ryo4T2KqxTw34t1RK7Ht-4Ih8vf5_d-UDt3RMmTzwQbevyasBPNLL7Z98Q06se0v-PHXrtumXlvoDbTz9omrZujltkGzX9RrmNtS0EGbWDqBlSfHwlWJGgwt95gheA-kvPBmPzvu6hAVYAtlhtWO1pmYBYX27AqTd0ab1JcY7us1wpLXDH6W1TzTpfr8jz7c3v67vwqHLQmi4yLsw45rrigtRpZXRwgBeUkonGb7EkkmmeVJmFZY5MyUWr690bDLFbMVEamQVp-_JmWud_UholFiIZjQD0CFhyCVjUcp0lEoV2yTlAbnYvfJitS2mUUAQgkIqvJAKL6SAXKE49rdgBWx_oV3Pi0EPCvxAa3kF0auMmDJa5zkHKGJLHyNqHZBvKMwCa1w4JNHMVb_ZFN-fHotLgHwA9LI8Csj5cFPVglgNmJY5nt5pQjGY9gb7dgKkTmDzCsjX_TSuRLqas22_KZCIxmWWJTIgH7aKs3-anf4FRByp1NHjHs-AHfjC34Pef_rvlZ_JSwB8yF4MY3FOzrp1b78AqOr0CExpJkbkxdXN_cPjyB9NwDhlcuTN6y8KAin_
link.rule.ids 230,314,727,780,784,864,885,2102,12056,21388,24318,27924,27925,31719,31720,33744,33745,43310,43805,53791,53793,73745,74302
linkProvider National Library of Medicine
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwELZge4ALAvEKFDCo19A87Ng5oRa1amG7Qn1IvVm24-xG6ibLJjnwJ_jNzHizSyMkLj7YSZRkxp5vxjOfCTlIjGaxtjzUkeEhE64Ic1kIaCKZFzw3wh8HdDHLzm7Yt1t-OwTc2iGtcrsm-oW6aCzGyA8xih9nCejMl9XPEE-Nwt3V4QiNh2QPmdP5hOwdn8x-XO6iLGAgJdi8TWGeANN56KZV6T4nsG7zkSnyjP3_rsv3DNM4afKeFTp9Sp4M8JEebeT9jDxw9XPy-6pbN8v-zlEf0sb4F9V3TT2nS0y363oDYy21DTiaVQ3gsqAYfqVY01CHvnYE-0D-C5-OR-d9VcANSIJcI9-xXlO7AMe-WQHW7uiy8STjHd3UONKqxofSypeadL9ekJvTk-uvZ-FwzkJouci7MOOGm5ILUaalNcICYtLaJBn-uYJJZnhSZCUSndkC6etLE9tMM1cykVpZxulLMqmb2r0mNEoc-DOGAeyQ0OSSsShlJkqljl2S8oAcbH-5Wm3oNBS4ISgZ5SWjvGQCcozi2F2CHNi-o1nP1TClFG7ROl6C_yojpq0xec4BjLjCe4nGBOQTClMhy0WNaTRz3betOr-6VEcA-gDqZXkUkP3horIBsVqYXHY8vNUENUzuVv1VxYB83A3jnZiwVrumbxWmonGZZYkMyKuN4uy-BhBWKmUqAiJGKjX63PFIXS089TeXMe7jvvn_a30gj86uL6Zqej77_pY8BoyHCYthLPbJpFv37h3gqM68HybLH30zIN4
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwELZgKyEuCMQrUMCgXkPzsGPnhFroqoWyqloq9WbFjr0bqZssm-TAn-A3M-PNLo2QuOQQJ1GSmfF8M575TMhBogsWF4aHRaR5yIQtw1yWAg6RzEuea-G3A_o-y06v2dcbfjPUP7VDWeV2TvQTddkYzJEfYhY_zhLQmUM3lEVcfJl-Wv0McQcpXGkdttO4T_bAK0bJhOwdn8wuLncZF3CWEvzfpklPgBs9tOeVsx8TmMP5yC159v5_5-g7TmpcQHnHI00fk0cDlKRHG9k_Ifds_ZT8vurWzbK_tdSntzEXRovbpp7TJZbedb2GsZaaBoLOqgagWVJMxVLsb6hD30eC50AXFr40j877qoQbkBC5Ru7jYk3NAoL8ZgW4u6PLxhOOd3TT70irGh9KK9920v16Rq6nJz8-n4bDnguh4SLvwoxrrh0XwqXOaGEAPRWFTjL8cyWTTPOkzBySnpkSqeydjk1WMOuYSI10cfqcTOqmti8JjRILsY1mAEEkHHLJWJQyHaWyiG2S8oAcbH-5Wm2oNRSEJCgZ5SWjvGQCcozi2F2CfNj-RLOeq8G8FC7XWu4glpURK4zWec4BmNjSR4xaB-QDClMh40WNujMv-rZVZ1eX6ggAIMC-LI8Csj9c5BoQqwFDM-PhrSaowdBb9VctA_J-N4x3YvFabZu-VViWxmWWJTIgLzaKs_saQFuplKkIiBip1OhzxyN1tfA04FzGuKb76v-v9Y48ADtR52ezb6_JQ4B7WLsYxmKfTLp1b98ApOr028FW_gDALyUL
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=Stromule+extension+along+microtubules+coordinated+with+actin-mediated+anchoring+guides+perinuclear+chloroplast+movement+during+innate+immunity&rft.jtitle=eLife&rft.au=Kumar%2C+Amutha+Sampath&rft.au=Park%2C+Eunsook&rft.au=Nedo+Alexander&rft.au=Alqarni+Ali&rft.date=2018-01-17&rft.pub=eLife+Sciences+Publications+Ltd&rft.eissn=2050-084X&rft.volume=7&rft_id=info:doi/10.7554%2FeLife.23625&rft.externalDBID=HAS_PDF_LINK
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2050-084X&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2050-084X&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2050-084X&client=summon