Molecular responses of agroinfiltrated Nicotiana benthamiana leaves expressing suppressor of silencing P19 and influenza virus‐like particles

Summary The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial vector Agrobacterium tumefaciens. HA proteins are then produced and matured through the secretory pathway of plant cells, before being tr...

Full description

Saved in:
Bibliographic Details
Published inPlant biotechnology journal Vol. 22; no. 5; pp. 1078 - 1100
Main Authors Hamel, Louis‐Philippe, Tardif, Rachel, Poirier‐Gravel, Francis, Rasoolizadeh, Asieh, Brosseau, Chantal, Giroux, Geneviève, Lucier, Jean‐François, Goulet, Marie‐Claire, Barrada, Adam, Paré, Marie‐Ève, Roussel, Élise, Comeau, Marc‐André, Lavoie, Pierre‐Olivier, Moffett, Peter, Michaud, Dominique, D'Aoust, Marc‐André
Format Journal Article
LanguageEnglish
Published England John Wiley and Sons Inc 01.05.2024
Subjects
Agrobacterium radiobacter
Agrobacterium tumefaciens - genetics
ascorbic acid
biotechnology
cell walls
chloroplast genes
gene expression
hemagglutinins
Humans
influenza
Influenza hemagglutinin
Influenza Vaccines
Influenza, Human
leaves
lignification
lipid metabolism
Nicotiana - genetics
Nicotiana benthamiana
Orthomyxoviridae - genetics
oxidative stress
oxylipins
Oxylipins - metabolism
phytomass
Plant immunity
Plant Leaves - genetics
Plant molecular farming
Plants, Genetically Modified - genetics
plasma membrane
protein synthesis
recombinant proteins
RNA
salicylic acid
Transient Agrobacterium‐mediated expression
Virus‐like particles
Virus‐like particles
Nicotiana benthamiana
Plant molecular farming
Transient Agrobacterium‐mediated expression
Influenza hemagglutinin
Plant immunity
Online AccessGet full text
ISSN1467-7644
1467-7652
1467-7652
DOI10.1111/pbi.14247

Cover

Abstract Summary The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial vector Agrobacterium tumefaciens. HA proteins are then produced and matured through the secretory pathway of plant cells, before being trafficked to the plasma membrane where they induce formation of virus‐like particles (VLPs). Production of VLPs unavoidably impacts plant cells, as do viral suppressors of RNA silencing (VSRs) that are co‐expressed to increase recombinant protein yields. However, little information is available on host molecular responses to foreign protein expression. This work provides a comprehensive overview of molecular changes occurring in Nicotiana benthamiana leaf cells transiently expressing the VSR P19, or co‐expressing P19 and an influenza HA. Our data identifies general responses to Agrobacterium‐mediated expression of foreign proteins, including shutdown of chloroplast gene expression, activation of oxidative stress responses and reinforcement of the plant cell wall through lignification. Our results also indicate that P19 expression promotes salicylic acid (SA) signalling, a process dampened by co‐expression of the HA protein. While reducing P19 level, HA expression also induces specific signatures, with effects on lipid metabolism, lipid distribution within membranes and oxylipin‐related signalling. When producing VLPs, dampening of P19 responses thus likely results from lower expression of the VSR, crosstalk between SA and oxylipin pathways, or a combination of both outcomes. Consistent with the upregulation of oxidative stress responses, we finally show that reduction of oxidative stress damage through exogenous application of ascorbic acid improves plant biomass quality during production of VLPs.
AbstractList The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial vector Agrobacterium tumefaciens. HA proteins are then produced and matured through the secretory pathway of plant cells, before being trafficked to the plasma membrane where they induce formation of virus-like particles (VLPs). Production of VLPs unavoidably impacts plant cells, as do viral suppressors of RNA silencing (VSRs) that are co-expressed to increase recombinant protein yields. However, little information is available on host molecular responses to foreign protein expression. This work provides a comprehensive overview of molecular changes occurring in Nicotiana benthamiana leaf cells transiently expressing the VSR P19, or co-expressing P19 and an influenza HA. Our data identifies general responses to Agrobacterium-mediated expression of foreign proteins, including shutdown of chloroplast gene expression, activation of oxidative stress responses and reinforcement of the plant cell wall through lignification. Our results also indicate that P19 expression promotes salicylic acid (SA) signalling, a process dampened by co-expression of the HA protein. While reducing P19 level, HA expression also induces specific signatures, with effects on lipid metabolism, lipid distribution within membranes and oxylipin-related signalling. When producing VLPs, dampening of P19 responses thus likely results from lower expression of the VSR, crosstalk between SA and oxylipin pathways, or a combination of both outcomes. Consistent with the upregulation of oxidative stress responses, we finally show that reduction of oxidative stress damage through exogenous application of ascorbic acid improves plant biomass quality during production of VLPs.The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial vector Agrobacterium tumefaciens. HA proteins are then produced and matured through the secretory pathway of plant cells, before being trafficked to the plasma membrane where they induce formation of virus-like particles (VLPs). Production of VLPs unavoidably impacts plant cells, as do viral suppressors of RNA silencing (VSRs) that are co-expressed to increase recombinant protein yields. However, little information is available on host molecular responses to foreign protein expression. This work provides a comprehensive overview of molecular changes occurring in Nicotiana benthamiana leaf cells transiently expressing the VSR P19, or co-expressing P19 and an influenza HA. Our data identifies general responses to Agrobacterium-mediated expression of foreign proteins, including shutdown of chloroplast gene expression, activation of oxidative stress responses and reinforcement of the plant cell wall through lignification. Our results also indicate that P19 expression promotes salicylic acid (SA) signalling, a process dampened by co-expression of the HA protein. While reducing P19 level, HA expression also induces specific signatures, with effects on lipid metabolism, lipid distribution within membranes and oxylipin-related signalling. When producing VLPs, dampening of P19 responses thus likely results from lower expression of the VSR, crosstalk between SA and oxylipin pathways, or a combination of both outcomes. Consistent with the upregulation of oxidative stress responses, we finally show that reduction of oxidative stress damage through exogenous application of ascorbic acid improves plant biomass quality during production of VLPs.
The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial vector Agrobacterium tumefaciens . HA proteins are then produced and matured through the secretory pathway of plant cells, before being trafficked to the plasma membrane where they induce formation of virus‐like particles (VLPs). Production of VLPs unavoidably impacts plant cells, as do viral suppressors of RNA silencing (VSRs) that are co‐expressed to increase recombinant protein yields. However, little information is available on host molecular responses to foreign protein expression. This work provides a comprehensive overview of molecular changes occurring in Nicotiana benthamiana leaf cells transiently expressing the VSR P19, or co‐expressing P19 and an influenza HA. Our data identifies general responses to Agrobacterium ‐mediated expression of foreign proteins, including shutdown of chloroplast gene expression, activation of oxidative stress responses and reinforcement of the plant cell wall through lignification. Our results also indicate that P19 expression promotes salicylic acid (SA) signalling, a process dampened by co‐expression of the HA protein. While reducing P19 level, HA expression also induces specific signatures, with effects on lipid metabolism, lipid distribution within membranes and oxylipin‐related signalling. When producing VLPs, dampening of P19 responses thus likely results from lower expression of the VSR, crosstalk between SA and oxylipin pathways, or a combination of both outcomes. Consistent with the upregulation of oxidative stress responses, we finally show that reduction of oxidative stress damage through exogenous application of ascorbic acid improves plant biomass quality during production of VLPs.
The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial vector Agrobacterium tumefaciens. HA proteins are then produced and matured through the secretory pathway of plant cells, before being trafficked to the plasma membrane where they induce formation of virus-like particles (VLPs). Production of VLPs unavoidably impacts plant cells, as do viral suppressors of RNA silencing (VSRs) that are co-expressed to increase recombinant protein yields. However, little information is available on host molecular responses to foreign protein expression. This work provides a comprehensive overview of molecular changes occurring in Nicotiana benthamiana leaf cells transiently expressing the VSR P19, or co-expressing P19 and an influenza HA. Our data identifies general responses to Agrobacterium-mediated expression of foreign proteins, including shutdown of chloroplast gene expression, activation of oxidative stress responses and reinforcement of the plant cell wall through lignification. Our results also indicate that P19 expression promotes salicylic acid (SA) signalling, a process dampened by co-expression of the HA protein. While reducing P19 level, HA expression also induces specific signatures, with effects on lipid metabolism, lipid distribution within membranes and oxylipin-related signalling. When producing VLPs, dampening of P19 responses thus likely results from lower expression of the VSR, crosstalk between SA and oxylipin pathways, or a combination of both outcomes. Consistent with the upregulation of oxidative stress responses, we finally show that reduction of oxidative stress damage through exogenous application of ascorbic acid improves plant biomass quality during production of VLPs.
The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial vector Agrobacterium tumefaciens. HA proteins are then produced and matured through the secretory pathway of plant cells, before being trafficked to the plasma membrane where they induce formation of virus‐like particles (VLPs). Production of VLPs unavoidably impacts plant cells, as do viral suppressors of RNA silencing (VSRs) that are co‐expressed to increase recombinant protein yields. However, little information is available on host molecular responses to foreign protein expression. This work provides a comprehensive overview of molecular changes occurring in Nicotiana benthamiana leaf cells transiently expressing the VSR P19, or co‐expressing P19 and an influenza HA. Our data identifies general responses to Agrobacterium‐mediated expression of foreign proteins, including shutdown of chloroplast gene expression, activation of oxidative stress responses and reinforcement of the plant cell wall through lignification. Our results also indicate that P19 expression promotes salicylic acid (SA) signalling, a process dampened by co‐expression of the HA protein. While reducing P19 level, HA expression also induces specific signatures, with effects on lipid metabolism, lipid distribution within membranes and oxylipin‐related signalling. When producing VLPs, dampening of P19 responses thus likely results from lower expression of the VSR, crosstalk between SA and oxylipin pathways, or a combination of both outcomes. Consistent with the upregulation of oxidative stress responses, we finally show that reduction of oxidative stress damage through exogenous application of ascorbic acid improves plant biomass quality during production of VLPs.
Summary The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial vector Agrobacterium tumefaciens. HA proteins are then produced and matured through the secretory pathway of plant cells, before being trafficked to the plasma membrane where they induce formation of virus‐like particles (VLPs). Production of VLPs unavoidably impacts plant cells, as do viral suppressors of RNA silencing (VSRs) that are co‐expressed to increase recombinant protein yields. However, little information is available on host molecular responses to foreign protein expression. This work provides a comprehensive overview of molecular changes occurring in Nicotiana benthamiana leaf cells transiently expressing the VSR P19, or co‐expressing P19 and an influenza HA. Our data identifies general responses to Agrobacterium‐mediated expression of foreign proteins, including shutdown of chloroplast gene expression, activation of oxidative stress responses and reinforcement of the plant cell wall through lignification. Our results also indicate that P19 expression promotes salicylic acid (SA) signalling, a process dampened by co‐expression of the HA protein. While reducing P19 level, HA expression also induces specific signatures, with effects on lipid metabolism, lipid distribution within membranes and oxylipin‐related signalling. When producing VLPs, dampening of P19 responses thus likely results from lower expression of the VSR, crosstalk between SA and oxylipin pathways, or a combination of both outcomes. Consistent with the upregulation of oxidative stress responses, we finally show that reduction of oxidative stress damage through exogenous application of ascorbic acid improves plant biomass quality during production of VLPs.
Author Hamel, Louis‐Philippe
Moffett, Peter
Brosseau, Chantal
D'Aoust, Marc‐André
Tardif, Rachel
Giroux, Geneviève
Comeau, Marc‐André
Rasoolizadeh, Asieh
Lucier, Jean‐François
Roussel, Élise
Poirier‐Gravel, Francis
Michaud, Dominique
Goulet, Marie‐Claire
Barrada, Adam
Paré, Marie‐Ève
Lavoie, Pierre‐Olivier
AuthorAffiliation 3 Centre de Recherche et d'innovation sur les Végétaux, Département de Phytologie Université Laval Québec Québec Canada
1 Medicago Inc. Québec Québec Canada
2 Centre SÈVE, Faculté des Sciences, Département de Biologie Université de Sherbrooke Sherbrooke Québec Canada
AuthorAffiliation_xml – name: 1 Medicago Inc. Québec Québec Canada
– name: 2 Centre SÈVE, Faculté des Sciences, Département de Biologie Université de Sherbrooke Sherbrooke Québec Canada
– name: 3 Centre de Recherche et d'innovation sur les Végétaux, Département de Phytologie Université Laval Québec Québec Canada
Author_xml – sequence: 1
  givenname: Louis‐Philippe
  orcidid: 0000-0001-8289-4498
  surname: Hamel
  fullname: Hamel, Louis‐Philippe
  email: louis-philippe.hamel@usherbrooke.ca
  organization: Medicago Inc
– sequence: 2
  givenname: Rachel
  surname: Tardif
  fullname: Tardif, Rachel
  organization: Medicago Inc
– sequence: 3
  givenname: Francis
  surname: Poirier‐Gravel
  fullname: Poirier‐Gravel, Francis
  organization: Medicago Inc
– sequence: 4
  givenname: Asieh
  surname: Rasoolizadeh
  fullname: Rasoolizadeh, Asieh
  organization: Université de Sherbrooke
– sequence: 5
  givenname: Chantal
  surname: Brosseau
  fullname: Brosseau, Chantal
  organization: Université de Sherbrooke
– sequence: 6
  givenname: Geneviève
  surname: Giroux
  fullname: Giroux, Geneviève
  organization: Université de Sherbrooke
– sequence: 7
  givenname: Jean‐François
  surname: Lucier
  fullname: Lucier, Jean‐François
  organization: Université de Sherbrooke
– sequence: 8
  givenname: Marie‐Claire
  surname: Goulet
  fullname: Goulet, Marie‐Claire
  organization: Université Laval
– sequence: 9
  givenname: Adam
  surname: Barrada
  fullname: Barrada, Adam
  organization: Université Laval
– sequence: 10
  givenname: Marie‐Ève
  surname: Paré
  fullname: Paré, Marie‐Ève
  organization: Medicago Inc
– sequence: 11
  givenname: Élise
  surname: Roussel
  fullname: Roussel, Élise
  organization: Medicago Inc
– sequence: 12
  givenname: Marc‐André
  surname: Comeau
  fullname: Comeau, Marc‐André
  organization: Medicago Inc
– sequence: 13
  givenname: Pierre‐Olivier
  surname: Lavoie
  fullname: Lavoie, Pierre‐Olivier
  organization: Medicago Inc
– sequence: 14
  givenname: Peter
  surname: Moffett
  fullname: Moffett, Peter
  email: peter.moffett@usherbrooke.ca
  organization: Université de Sherbrooke
– sequence: 15
  givenname: Dominique
  orcidid: 0000-0002-5177-1142
  surname: Michaud
  fullname: Michaud, Dominique
  email: dominique.michaud@fsaa.ulaval.ca
  organization: Université Laval
– sequence: 16
  givenname: Marc‐André
  surname: D'Aoust
  fullname: D'Aoust, Marc‐André
  email: daoustma@hotmail.com
  organization: Medicago Inc
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38041470$$D View this record in MEDLINE/PubMed
BookMark eNqFkktuFDEQhi0URB6w4ALIS1hMYrvdD68QiXhECpAFrK1qd_XE4LEbu3sgrLgBnJGT4J4JI0ACvPEv-6u_qlR1SPZ88EjIfc6OeT4nQ2uPuRSyvkUOuKzqRV2VYm-npdwnhym9Y0zwqqzukP2iYZLLmh2Qry-DQzM5iDRiGoJPmGjoKSxjsL63bowwYkdfWRNGCx5oi368gtVGO4R15vHTkIOT9UuapmGjQ5xdknXozfx-yRUF39Hs6Sb0n4GubZzS9y_fnH2PdIA4WuMw3SW3e3AJ793cR-Tts6dvzl4sLl4_Pz97crEwUqp6UaFRpmRlD23RNk1bt6IVnZIMTGOw7CtV1NCxqua8AwG85pg167hSAqATxRF5vPUdpnaFnclNRXB6iHYF8VoHsPr3H2-v9DKsNedMiIbNDg9vHGL4MGEa9comg86BxzAlXfCyyHmFVP9FRaOqhhWNYhl98Gtdu4J-TiwDj7aAiSGliP0O4UzP26DzNujNNmT25A_W2BFGG-aWrPtXxMc8ueu_W-vL0_NtxA-v-csP
CitedBy_id crossref_primary_10_1111_nph_19894
crossref_primary_10_1093_hr_uhae197
crossref_primary_10_3389_fpls_2024_1453930
crossref_primary_10_1038_s41477_024_01898_3
crossref_primary_10_1016_j_plaphy_2024_109278
crossref_primary_10_1016_j_fitote_2024_106338
crossref_primary_10_1093_jxb_erae458
crossref_primary_10_1111_pbi_14252
crossref_primary_10_1007_s11033_024_10164_w
Cites_doi 10.3389/fpls.2016.01899
10.1046/j.1365-313X.2002.01465.x
10.1002/biot.201500056
10.1093/bioinformatics/btn595
10.1146/annurev-arplant-042817-040440
10.1186/1471-2164-13-395
10.1006/meth.2001.1262
10.1104/pp.17.00173
10.1111/j.1467-7652.2011.00643.x
10.1038/embor.2013.24
10.1105/tpc.104.023549
10.1104/pp.113.232462
10.1016/j.abb.2017.06.023
10.1093/mp/ssr105
10.1094/MPMI-19-0665
10.14348/molcells.2015.0039
10.1111/pce.12771
10.1111/j.1365-313X.2004.02117.x
10.1016/j.chemphyslip.2006.02.007
10.1093/plphys/kiab102
10.1007/s11103-014-0198-5
10.3732/ajb.1400305
10.1016/j.pbi.2014.02.003
10.3389/fpls.2013.00220
10.1016/j.jprot.2013.04.023
10.1111/pbi.12916
10.1104/pp.114.237388
10.1146/annurev.arplant.58.032806.103946
10.1016/S1369-5266(03)00069-4
10.4161/psb.4.6.8392
10.1111/j.1600-0854.2008.00742.x
10.1007/s00424-013-1363-4
10.1074/jbc.REV120.010854
10.1104/pp.107.109264
10.1073/pnas.012452499
10.1046/j.1364-3703.2003.00163.x
10.1104/pp.105.067058
10.1105/tpc.18.00250
10.1074/jbc.M114.558817
10.1111/j.1399-3054.2007.01041.x
10.1146/annurev.phyto.42.040803.140421
10.1111/j.1365-313X.2004.02200.x
10.1007/s11101-017-9530-4
10.1016/j.tplants.2015.08.002
10.1373/clinchem.2008.112797
10.1073/pnas.211311098
10.3390/vaccines6030058
10.1105/tpc.107.054767
10.1093/jxb/ern075
10.1038/s41578-021-00399-5
10.1104/pp.107.111302
10.3390/vaccines9111255
10.1111/j.1467-7652.2010.00508.x
10.1105/tpc.114.131185
10.1111/j.1365-313X.2008.03486.x
10.1104/pp.106.087304
10.1016/j.febslet.2007.12.039
10.1371/journal.pone.0015559
10.1105/tpc.108.065250
10.4161/psb.6.1.14037
10.1371/journal.pone.0033042
10.1111/j.1467-7652.2008.00384.x
10.1038/ncomms8658
10.1104/pp.106.078469
10.1105/tpc.16.00898
10.1186/gb-2002-3-7-research0034
10.3390/plants8110492
10.1105/tpc.106.041103
10.1177/2515135520908121
10.1104/pp.108.3.1277
10.1038/ncomms8649
10.1104/pp.108.119321
10.31083/j.fbl2711310
10.1111/j.1365-3040.2005.01369.x
10.1016/j.chom.2012.04.014
10.1016/j.biochi.2012.06.011
10.1021/acs.jproteome.9b00409
10.1111/nph.12256
10.1093/emboj/cdf312
10.1146/annurev-phyto-080516-035406
10.1038/nrm2330
10.1023/B:PLAN.0000038276.95539.39
ContentType Journal Article
Copyright 2023 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
Copyright_xml – notice: 2023 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
– notice: 2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
DBID 24P
AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7X8
7S9
L.6
5PM
DOI 10.1111/pbi.14247
DatabaseName Wiley Online Library Open Access
CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
AGRICOLA
AGRICOLA - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
AGRICOLA
AGRICOLA - Academic
DatabaseTitleList MEDLINE - Academic
CrossRef
MEDLINE
AGRICOLA
Database_xml – sequence: 1
  dbid: 24P
  name: Wiley Online Library Open Access
  url: https://authorservices.wiley.com/open-science/open-access/browse-journals.html
  sourceTypes: Publisher
– 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
DeliveryMethod fulltext_linktorsrc
Discipline Agriculture
DocumentTitleAlternate Molecular signature of influenza vaccine production in plants
EISSN 1467-7652
EndPage 1100
ExternalDocumentID PMC11022802
38041470
10_1111_pbi_14247
PBI14247
Genre researchArticle
Journal Article
Review
GrantInformation_xml – fundername: Medicago Inc.
– fundername: Natural Sciences and Engineering Research Council of Canada
  funderid: CRDPJ 477619; CRDPJ 495852
– fundername: Natural Sciences and Engineering Research Council of Canada
  grantid: CRDPJ 495852
– fundername: Natural Sciences and Engineering Research Council of Canada
  grantid: CRDPJ 477619
GroupedDBID ---
.3N
.GA
.Y3
05W
0R~
10A
123
1OC
24P
29O
31~
33P
4.4
50Y
50Z
51W
51X
52M
52N
52O
52P
52S
52T
52W
52X
53G
5HH
5LA
5VS
66C
702
7PT
8-0
8-1
8-3
8-4
8-5
8FE
8FG
8FH
8UM
930
A03
A8Z
AAEVG
AAHBH
AAHHS
AANHP
AAONW
AAZKR
ABCQN
ABDBF
ABEML
ABIJN
ABJCF
ABPVW
ACBWZ
ACCFJ
ACCMX
ACIWK
ACPRK
ACRPL
ACSCC
ACUHS
ACXQS
ACYXJ
ADBBV
ADIZJ
ADKYN
ADNMO
ADZMN
AEEZP
AEIMD
AENEX
AEQDE
AEUQT
AEUYN
AFBPY
AFEBI
AFKRA
AFRAH
AFZJQ
AIWBW
AJBDE
ALAGY
ALMA_UNASSIGNED_HOLDINGS
ALUQN
AMBMR
ASPBG
ATUGU
AVUZU
AVWKF
AZBYB
AZFZN
BAFTC
BBNVY
BCNDV
BDRZF
BENPR
BFHJK
BGLVJ
BHPHI
BNHUX
BROTX
BRXPI
BY8
CAG
CCPQU
COF
CS3
D-E
D-F
DPXWK
DR2
DU5
EAD
EAP
EBD
EBS
ECGQY
EDH
EJD
EMK
EMOBN
EST
ESX
F00
F01
F04
F5P
FEDTE
G-S
G.N
GODZA
GROUPED_DOAJ
H.T
H.X
HCIFZ
HF~
HOLLA
HVGLF
HZ~
IAO
IEP
IGS
IHE
ITC
IX1
J0M
KQ8
L6V
LC2
LC3
LH4
LK8
LP6
LP7
LW6
M7P
M7S
MK4
ML0
N04
N05
N9A
NF~
O66
O9-
OIG
OK1
P2P
P2X
P4D
PIMPY
PROAC
PTHSS
Q.N
Q11
QB0
QM4
QO4
R.K
ROL
RPM
RX1
SUPJJ
SV3
TUS
UB1
W8V
W99
WIH
WIN
WQJ
WRC
XG1
~IA
~KM
~WT
AAYXX
AGQPQ
CITATION
PHGZM
PHGZT
CGR
CUY
CVF
ECM
EIF
NPM
7X8
AAMMB
AEFGJ
AGXDD
AIDQK
AIDYY
ESTFP
PQGLB
PUEGO
7S9
L.6
5PM
ID FETCH-LOGICAL-c4497-6ec9c505fab3b88b7b2b2d940ac8ce5f6937ad06711da2a171e6710d1992aad23
IEDL.DBID DR2
ISSN 1467-7644
1467-7652
IngestDate Thu Aug 21 18:34:07 EDT 2025
Fri Sep 05 17:30:40 EDT 2025
Mon Sep 08 10:27:37 EDT 2025
Thu Apr 03 07:06:01 EDT 2025
Tue Jul 01 02:34:51 EDT 2025
Thu Apr 24 23:06:19 EDT 2025
Wed Jan 22 17:21:16 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 5
Keywords Virus‐like particles
Nicotiana benthamiana
Plant molecular farming
Transient Agrobacterium‐mediated expression
Influenza hemagglutinin
Plant immunity
Language English
License Attribution
2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c4497-6ec9c505fab3b88b7b2b2d940ac8ce5f6937ad06711da2a171e6710d1992aad23
Notes ObjectType-Article-2
SourceType-Scholarly Journals-1
ObjectType-Feature-3
content type line 23
ObjectType-Review-1
ObjectType-Article-1
ObjectType-Feature-2
ORCID 0000-0002-5177-1142
0000-0001-8289-4498
OpenAccessLink https://proxy.k.utb.cz/login?url=https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.14247
PMID 38041470
PQID 2896803890
PQPubID 23479
PageCount 23
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_11022802
proquest_miscellaneous_3153171249
proquest_miscellaneous_2896803890
pubmed_primary_38041470
crossref_primary_10_1111_pbi_14247
crossref_citationtrail_10_1111_pbi_14247
wiley_primary_10_1111_pbi_14247_PBI14247
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate May 2024
PublicationDateYYYYMMDD 2024-05-01
PublicationDate_xml – month: 05
  year: 2024
  text: May 2024
PublicationDecade 2020
PublicationPlace England
PublicationPlace_xml – name: England
– name: Hoboken
PublicationTitle Plant biotechnology journal
PublicationTitleAlternate Plant Biotechnol J
PublicationYear 2024
Publisher John Wiley and Sons Inc
Publisher_xml – name: John Wiley and Sons Inc
References 2017; 40
2015; 38
2013; 4
2007; 143
2005; 139
2002; 99
2008; 9
2014; 26
2008; 6
2008; 147
2008; 146
2012; 13
2005; 28
2008; 582
2012; 11
2017; 632
2012; 10
2022; 27
2020; 19
2004; 134
2020; 8
2018; 6
2009; 55
2013; 14
2020; 295
2004; 39
2013; 95
2003; 6
2013; 199
2018; 30
2014; 19
2008; 20
2014; 166
2010; 5
2014; 164
2010; 8
2014; 289
2001; 98
2019; 8
2021; 9
2009; 25
2004; 42
2015; 6
2004; 40
2009; 21
2015; 367
2002; 32
2015; 10
2008; 59
2013; 93
2006; 18
2002; 3
2006; 19
2021; 186
2008; 55
2017; 29
2017; 175
2014; 85
2011; 6
2001; 25
2007; 58
2018; 69
2004; 54
2018; 17
2016; 7
2004; 16
2022; 7
2017; 55
2015; 20
1995; 108
2002; 21
2006; 141
2009; 4
2012; 7
2008; 132
2012; 5
2018; 16
2014; 466
2014; 101
e_1_2_10_23_1
e_1_2_10_46_1
e_1_2_10_69_1
e_1_2_10_21_1
e_1_2_10_42_1
e_1_2_10_40_1
e_1_2_10_70_1
e_1_2_10_2_1
e_1_2_10_72_1
e_1_2_10_4_1
e_1_2_10_18_1
e_1_2_10_74_1
e_1_2_10_53_1
e_1_2_10_6_1
e_1_2_10_16_1
e_1_2_10_39_1
e_1_2_10_76_1
e_1_2_10_55_1
e_1_2_10_8_1
e_1_2_10_14_1
e_1_2_10_37_1
e_1_2_10_57_1
e_1_2_10_78_1
e_1_2_10_58_1
e_1_2_10_13_1
e_1_2_10_34_1
Matrosovich M. (e_1_2_10_44_1) 2015; 367
e_1_2_10_11_1
e_1_2_10_32_1
e_1_2_10_30_1
e_1_2_10_51_1
e_1_2_10_80_1
e_1_2_10_82_1
e_1_2_10_61_1
e_1_2_10_84_1
e_1_2_10_29_1
e_1_2_10_63_1
e_1_2_10_27_1
e_1_2_10_65_1
e_1_2_10_25_1
e_1_2_10_48_1
e_1_2_10_67_1
e_1_2_10_24_1
e_1_2_10_45_1
e_1_2_10_22_1
e_1_2_10_43_1
e_1_2_10_20_1
e_1_2_10_41_1
e_1_2_10_71_1
e_1_2_10_73_1
e_1_2_10_52_1
e_1_2_10_3_1
e_1_2_10_19_1
e_1_2_10_75_1
e_1_2_10_54_1
e_1_2_10_5_1
e_1_2_10_17_1
e_1_2_10_38_1
e_1_2_10_77_1
e_1_2_10_56_1
e_1_2_10_79_1
e_1_2_10_7_1
e_1_2_10_15_1
e_1_2_10_36_1
e_1_2_10_12_1
e_1_2_10_35_1
e_1_2_10_9_1
e_1_2_10_59_1
e_1_2_10_10_1
e_1_2_10_33_1
e_1_2_10_31_1
e_1_2_10_50_1
e_1_2_10_60_1
e_1_2_10_81_1
e_1_2_10_62_1
e_1_2_10_83_1
e_1_2_10_64_1
e_1_2_10_28_1
e_1_2_10_49_1
e_1_2_10_66_1
e_1_2_10_26_1
e_1_2_10_47_1
e_1_2_10_68_1
References_xml – volume: 6
  start-page: 58
  year: 2018
  article-title: The future of influenza vaccines: a historical and clinical perspective
  publication-title: Vaccines (Basel)
– volume: 42
  start-page: 185
  year: 2004
  end-page: 209
  article-title: Systemic acquired resistance
  publication-title: Annu. Rev. Phytopathol.
– volume: 55
  start-page: 611
  year: 2009
  end-page: 622
  article-title: The MIQE guidelines: minimum information for publication of quantitative real‐time PCR experiments
  publication-title: Clin. Chem.
– volume: 20
  start-page: 658
  year: 2008
  end-page: 676
  article-title: The P4‐ATPase ALA3 localizes to the Golgi and requires a β‐subunit to function in lipid translocation and secretory vesicle formation
  publication-title: Plant Cell
– volume: 3
  year: 2002
  article-title: Accurate normalization of real‐time quantitative RT‐PCR data by geometric averaging of multiple internal control genes
  publication-title: Genome Biol.
– volume: 21
  start-page: 3070
  year: 2002
  end-page: 3080
  article-title: A viral protein suppresses RNA silencing and binds silencing‐generated, 21‐ to 25‐nucleotide double‐stranded RNAs
  publication-title: EMBO J.
– volume: 99
  start-page: 517
  year: 2002
  end-page: 522
  article-title: gp91 homologues and are required for accumulation of reactive oxygen intermediates in the plant defense response
  publication-title: Proc. Natl. Acad. Sci. USA
– volume: 39
  start-page: 147
  year: 2004
  end-page: 160
  article-title: Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence
  publication-title: Plant J.
– volume: 175
  start-page: 970
  year: 2017
  end-page: 981
  article-title: Phospholipase C2 affects MAMP‐triggered immunity by modulating ROS production
  publication-title: Plant Physiol.
– volume: 19
  start-page: 1
  year: 2014
  end-page: 7
  article-title: Transient expressions of synthetic biology in plants
  publication-title: Curr. Opin. Plant Biol.
– volume: 40
  start-page: 200
  year: 2004
  end-page: 212
  article-title: A key role for in activation of local and systemic defenses in
  publication-title: Plant J.
– volume: 108
  start-page: 1277
  year: 1995
  end-page: 1287
  article-title: Elicitor‐induced spruce stress lignin: structural similarity to early developmental lignins
  publication-title: Plant Physiol.
– volume: 25
  start-page: 159
  year: 2009
  end-page: 162
  article-title: Phospholipid scramblases and Tubby‐like proteins belong to a new superfamily of membrane tethered transcription factors
  publication-title: Bioinformatics
– volume: 54
  start-page: 613
  year: 2004
  end-page: 622
  article-title: Identification of tobacco and two closely related genes as spermine‐responsive genes and their differential expression during the ‐induced hypersensitive response and during leaf‐ and flower‐senescence
  publication-title: Plant Mol. Biol.
– volume: 20
  start-page: 754
  year: 2015
  end-page: 766
  article-title: Licensed to kill: mitochondria, chloroplasts, and cell death
  publication-title: Trends Plant Sci.
– volume: 7
  year: 2012
  article-title: A putative plant aminophospholipid flippase, the P4 ATPase ALA1, localizes to the plasma membrane following association with a β‐subunit
  publication-title: PloS One
– volume: 132
  start-page: 417
  year: 2008
  end-page: 425
  article-title: Metabolism of salicylic acid in wild‐type, and glucosyltransferase mutants of
  publication-title: Physiol. Plant.
– volume: 141
  start-page: 119
  year: 2006
  end-page: 132
  article-title: Proteins involved in lipid translocation in eukaryotic cells
  publication-title: Chem. Phys. Lipids
– volume: 146
  start-page: 904
  year: 2008
  end-page: 915
  article-title: Comparisons of LIPOXYGENASE3‐ and JASMONATE‐RESISTANT4/6‐silenced plants reveal that jasmonic acid and jasmonic acid‐amino acid conjugates play different roles in herbivore resistance of
  publication-title: Plant Physiol.
– volume: 55
  start-page: 505
  year: 2017
  end-page: 536
  article-title: Fatty acid‐ and lipid‐mediated signaling in plant defense
  publication-title: Annu. Rev. Phytopathol.
– volume: 27
  start-page: 310
  year: 2022
  article-title: Role of salicylic acid in combating heat stress in plants: insights into modulation of vital processes
  publication-title: Front. Biosci. (Landmark Ed)
– volume: 7
  start-page: 1899
  year: 2016
  article-title: Targeting the gene to explore the role of invertases in sucrose transport in roots and during infection
  publication-title: Front. Plant Sci.
– volume: 38
  start-page: 390
  year: 2015
  end-page: 395
  article-title: The divergent roles of STAYGREEN (SGR) homologs in chlorophyll degradation
  publication-title: Mol. Cells
– volume: 55
  start-page: 53
  year: 2008
  end-page: 64
  article-title: The oomycete response gene is required for defense against in
  publication-title: Plant J.
– volume: 6
  start-page: 379
  year: 2003
  end-page: 389
  article-title: Apoplastic ascorbate metabolism and its role in the regulation of cell signalling
  publication-title: Curr. Opin. Plant Biol.
– volume: 146
  start-page: 703
  year: 2008
  end-page: 715
  article-title: Salicylic acid and systemic acquired resistance play a role in attenuating crown gall disease caused by
  publication-title: Plant Physiol.
– volume: 367
  start-page: 1
  year: 2015
  end-page: 28
  article-title: Sialic acid receptors of viruses
  publication-title: Top. Curr. Chem.
– volume: 32
  start-page: 749
  year: 2002
  end-page: 762
  article-title: Spatio‐temporal expression of patatin‐like lipid acyl hydrolases and accumulation of jasmonates in elicitor‐treated tobacco leaves are not affected by endogenous levels of salicylic acid
  publication-title: Plant J.
– volume: 4
  start-page: 220
  year: 2013
  article-title: Plant cell wall lignification and monolignol metabolism
  publication-title: Front. Plant Sci.
– volume: 59
  start-page: 2125
  year: 2008
  end-page: 2132
  article-title: Modulation of heat shock factors accompanies salicylic acid‐mediated potentiation of Hsp70 in tomato seedlings
  publication-title: J. Exp. Bot.
– volume: 85
  start-page: 473
  year: 2014
  end-page: 484
  article-title: Expression of sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to
  publication-title: Plant Mol. Biol.
– volume: 164
  start-page: 92
  year: 2014
  end-page: 104
  article-title: Deciphering the role of aspartate and prephenate aminotransferase activities in plastid nitrogen metabolism
  publication-title: Plant Physiol.
– volume: 466
  start-page: 1227
  year: 2014
  end-page: 1240
  article-title: P4‐ATPases: lipid flippases in cell membranes
  publication-title: Pflügers Arch.
– volume: 17
  start-page: 81
  year: 2018
  end-page: 111
  article-title: P450s controlling metabolic bifurcations in plant terpene specialized metabolism
  publication-title: Phytochem. Rev.
– volume: 14
  start-page: 382
  year: 2013
  end-page: 388
  article-title: ORE1 balances leaf senescence against maintenance by antagonizing G2‐like‐mediated transcription
  publication-title: EMBO Rep.
– volume: 6
  start-page: 7658
  year: 2015
  article-title: AZI1 family proteins mediate signal mobilization for systemic defence priming
  publication-title: Nat. Commun.
– volume: 18
  start-page: 3303
  year: 2006
  end-page: 3320
  article-title: Silencing and in impairs jasmonic acid‐isoleucine‐mediated defenses against
  publication-title: Plant Cell
– volume: 199
  start-page: 228
  year: 2013
  end-page: 240
  article-title: phospholipase Dβ1 modulates defense responses to bacterial and fungal pathogens
  publication-title: New Phytol.
– volume: 295
  start-page: 7710
  year: 2020
  end-page: 7725
  article-title: Ethylene signaling in plants
  publication-title: J. Biol. Chem.
– volume: 141
  start-page: 423
  year: 2006
  end-page: 435
  article-title: Ascorbate oxidase‐dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco
  publication-title: Plant Physiol.
– volume: 5
  start-page: 914
  year: 2012
  end-page: 928
  article-title: Role of 9‐lipoxygenase and α‐dioxygenase oxylipin pathways as modulators of local and systemic defense
  publication-title: Mol. Plant
– volume: 21
  start-page: 1109
  year: 2009
  end-page: 1128
  article-title: GLK transcription factors coordinate expression of the photosynthetic apparatus in
  publication-title: Plant Cell
– volume: 58
  start-page: 459
  year: 2007
  end-page: 481
  article-title: Oxidative modifications to cellular components in plants
  publication-title: Annu. Rev. Plant Biol.
– volume: 147
  start-page: 696
  year: 2008
  end-page: 706
  article-title: Induction of the gene by 12‐oxo‐phytodienoic acid but not jasmonic acid via a CORONATINE INSENSITIVE1‐dependent pathway
  publication-title: Plant Physiol.
– volume: 8
  year: 2020
  article-title: Influenza vaccines: the potential benefits of cell‐culture isolation and manufacturing
  publication-title: Ther. Adv. Vaccines Immunother.
– volume: 10
  start-page: 83
  year: 2012
  end-page: 94
  article-title: A protease activity‐depleted environment for heterologous proteins migrating towards the leaf cell apoplast
  publication-title: Plant Biotechnol. J.
– volume: 134
  start-page: 460
  year: 2004
  end-page: 469
  article-title: Tobacco nectarin V is a flavin‐containing berberine bridge enzyme‐like protein with glucose oxidase activity
  publication-title: Plant Physiol.
– volume: 632
  start-page: 88
  year: 2017
  end-page: 103
  article-title: The family of berberine bridge enzyme‐like enzymes: A treasure‐trove of oxidative reactions
  publication-title: Arch. Biochem. Biophys.
– volume: 143
  start-page: 378
  year: 2007
  end-page: 388
  article-title: Characterization of a divinyl ether biosynthetic pathway specifically associated with pathogenesis in tobacco
  publication-title: Plant Physiol.
– volume: 16
  start-page: 1797
  year: 2018
  end-page: 1810
  article-title: Three unrelated protease inhibitors enhance accumulation of pharmaceutical recombinant proteins in
  publication-title: Plant Biotechnol. J.
– volume: 7
  start-page: 372
  year: 2022
  end-page: 388
  article-title: Integrating plant molecular farming and materials research for next‐generation vaccines
  publication-title: Nat. Rev. Mater.
– volume: 19
  start-page: 106
  year: 2020
  end-page: 118
  article-title: pH gradient mitigation in the leaf cell secretory pathway attenuates the defense response of to agroinfiltration
  publication-title: J. Proteome Res.
– volume: 9
  start-page: 112
  year: 2008
  end-page: 124
  article-title: Membrane lipids: where they are and how they behave
  publication-title: Nat. Rev. Mol. Cell Biol.
– volume: 30
  start-page: 1006
  year: 2018
  end-page: 1022
  article-title: Two abscisic acid‐responsive plastid lipase genes involved in jasmonic acid biosynthesis in
  publication-title: Plant Cell
– volume: 25
  start-page: 402
  year: 2001
  end-page: 408
  article-title: Analysis of relative gene expression data using real‐time quantitative PCR and the 2 Method
  publication-title: Methods
– volume: 40
  start-page: 585
  year: 2017
  end-page: 598
  article-title: Diacylglycerol kinases activate tobacco NADPH oxidase‐dependent oxidative burst in response to cryptogein
  publication-title: Plant Cell Environ.
– volume: 19
  start-page: 665
  year: 2006
  end-page: 681
  article-title: The transcriptome in response to
  publication-title: Mol. Plant Microbe Interact.
– volume: 95
  start-page: 91
  year: 2013
  end-page: 95
  article-title: Role of epoxide hydrolases in lipid metabolism
  publication-title: Biochimie
– volume: 16
  start-page: 2117
  year: 2004
  end-page: 2127
  article-title: The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in
  publication-title: Plant Cell
– volume: 5
  year: 2010
  article-title: Preclinical and clinical development of plant‐made virus‐like particle vaccine against avian H5N1 influenza
  publication-title: PloS One
– volume: 29
  start-page: 1440
  year: 2017
  end-page: 1459
  article-title: Monoterpenes support systemic acquired resistance within and between Plants
  publication-title: Plant Cell
– volume: 101
  start-page: 1821
  year: 2014
  end-page: 1835
  article-title: The plastochron index: still useful after nearly six decades
  publication-title: Am. J. Bot.
– volume: 26
  start-page: 4135
  year: 2014
  end-page: 4148
  article-title: Quantitative peptidomics study reveals that a wound‐induced peptide from PR‐1 regulates immune signaling in tomato
  publication-title: Plant Cell
– volume: 69
  start-page: 363
  year: 2018
  end-page: 386
  article-title: The oxylipin pathways: biochemistry and function
  publication-title: Annu. Rev. Plant Biol.
– volume: 28
  start-page: 1367
  year: 2005
  end-page: 1378
  article-title: The combined action of 9 lipoxygenase and galactolipase is sufficient to bring about programmed cell death during tobacco hypersensitive response
  publication-title: Plant Cell Environ.
– volume: 582
  start-page: 473
  year: 2008
  end-page: 478
  article-title: Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in
  publication-title: FEBS Lett.
– volume: 93
  start-page: 356
  year: 2013
  end-page: 368
  article-title: The unfolded protein response in plants: a fundamental adaptive cellular response to internal and external stresses
  publication-title: J. Proteomics
– volume: 6
  start-page: 7649
  year: 2015
  article-title: A phospholipid uptake system in the model plant
  publication-title: Nat. Commun.
– volume: 9
  start-page: 1233
  year: 2008
  end-page: 1239
  article-title: Molecular mechanisms of PLD function in membrane traffic
  publication-title: Traffic
– volume: 98
  start-page: 12837
  year: 2001
  end-page: 12842
  article-title: Plant defense in the absence of jasmonic acid: the role of cyclopentenones
  publication-title: Proc. Natl. Acad. Sci. USA
– volume: 11
  start-page: 587
  year: 2012
  end-page: 596
  article-title: Coronatine promotes virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation
  publication-title: Cell Host Microbe
– volume: 6
  start-page: 13
  year: 2011
  end-page: 18
  article-title: Phospholipases in action during plant defense signaling
  publication-title: Plant Signal. Behav.
– volume: 6
  start-page: 930
  year: 2008
  end-page: 940
  article-title: Influenza virus‐like particles produced by transient expression in induce a protective immune response against a lethal viral challenge in mice
  publication-title: Plant Biotechnol. J.
– volume: 8
  start-page: 492
  year: 2019
  article-title: Asparagine synthesis during tobacco leaf curing
  publication-title: Plants (Basel)
– volume: 4
  start-page: 493
  year: 2009
  end-page: 496
  article-title: Biosynthesis of salicylic acid in plants
  publication-title: Plant Signal. Behav.
– volume: 186
  start-page: 832
  year: 2021
  end-page: 835
  article-title: Prevention of necrosis caused by transient expression in by application of ascorbic acid
  publication-title: Plant Physiol.
– volume: 9
  start-page: 1255
  year: 2021
  article-title: Estimation of reduction in influenza vaccine effectiveness due to egg‐adaptation changes‐systematic literature review and expert consensus
  publication-title: Vaccines (Basel)
– volume: 139
  start-page: 1268
  year: 2005
  end-page: 1283
  article-title: 12‐oxo‐phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound‐induced gene expression in
  publication-title: Plant Physiol.
– volume: 166
  start-page: 396
  year: 2014
  end-page: 410
  article-title: Jasmonic acid and its precursor 12‐oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in tomato
  publication-title: Plant Physiol.
– volume: 8
  start-page: 783
  year: 2010
  end-page: 795
  article-title: Overexpression of gene in using a viral vector system
  publication-title: Plant Biotechnol. J.
– volume: 10
  start-page: 1478
  year: 2015
  end-page: 1486
  article-title: Modulating secretory pathway pH by proton channel co‐expression can increase recombinant protein stability in plants
  publication-title: Biotechnol. J.
– volume: 289
  start-page: 25405
  year: 2014
  end-page: 25417
  article-title: Phospholipase D facilitates efficient entry of influenza virus, allowing escape from innate immune inhibition
  publication-title: J. Biol. Chem.
– volume: 13
  start-page: 395
  year: 2012
  article-title: The polyphenol oxidase gene family in land plants: lineage‐specific duplication and expansion
  publication-title: BMC Genomics
– ident: e_1_2_10_76_1
  doi: 10.3389/fpls.2016.01899
– ident: e_1_2_10_25_1
  doi: 10.1046/j.1365-313X.2002.01465.x
– ident: e_1_2_10_33_1
  doi: 10.1002/biot.201500056
– ident: e_1_2_10_4_1
  doi: 10.1093/bioinformatics/btn595
– ident: e_1_2_10_81_1
  doi: 10.1146/annurev-arplant-042817-040440
– ident: e_1_2_10_73_1
  doi: 10.1186/1471-2164-13-395
– ident: e_1_2_10_41_1
  doi: 10.1006/meth.2001.1262
– ident: e_1_2_10_20_1
  doi: 10.1104/pp.17.00173
– ident: e_1_2_10_30_1
  doi: 10.1111/j.1467-7652.2011.00643.x
– ident: e_1_2_10_57_1
  doi: 10.1038/embor.2013.24
– ident: e_1_2_10_67_1
  doi: 10.1105/tpc.104.023549
– ident: e_1_2_10_71_1
  doi: 10.1104/pp.113.232462
– ident: e_1_2_10_21_1
  doi: 10.1016/j.abb.2017.06.023
– ident: e_1_2_10_77_1
  doi: 10.1093/mp/ssr105
– ident: e_1_2_10_26_1
  doi: 10.1094/MPMI-19-0665
– ident: e_1_2_10_62_1
  doi: 10.14348/molcells.2015.0039
– ident: e_1_2_10_11_1
  doi: 10.1111/pce.12771
– ident: e_1_2_10_19_1
  doi: 10.1111/j.1365-313X.2004.02117.x
– ident: e_1_2_10_24_1
  doi: 10.1016/j.chemphyslip.2006.02.007
– ident: e_1_2_10_49_1
  doi: 10.1093/plphys/kiab102
– ident: e_1_2_10_39_1
  doi: 10.1007/s11103-014-0198-5
– ident: e_1_2_10_46_1
  doi: 10.3732/ajb.1400305
– ident: e_1_2_10_61_1
  doi: 10.1016/j.pbi.2014.02.003
– ident: e_1_2_10_79_1
  doi: 10.3389/fpls.2013.00220
– ident: e_1_2_10_28_1
  doi: 10.1016/j.jprot.2013.04.023
– volume: 367
  start-page: 1
  year: 2015
  ident: e_1_2_10_44_1
  article-title: Sialic acid receptors of viruses
  publication-title: Top. Curr. Chem.
– ident: e_1_2_10_31_1
  doi: 10.1111/pbi.12916
– ident: e_1_2_10_6_1
  doi: 10.1104/pp.114.237388
– ident: e_1_2_10_47_1
  doi: 10.1146/annurev.arplant.58.032806.103946
– ident: e_1_2_10_52_1
  doi: 10.1016/S1369-5266(03)00069-4
– ident: e_1_2_10_16_1
  doi: 10.4161/psb.4.6.8392
– ident: e_1_2_10_60_1
  doi: 10.1111/j.1600-0854.2008.00742.x
– ident: e_1_2_10_43_1
  doi: 10.1007/s00424-013-1363-4
– ident: e_1_2_10_5_1
  doi: 10.1074/jbc.REV120.010854
– ident: e_1_2_10_78_1
  doi: 10.1104/pp.107.109264
– ident: e_1_2_10_72_1
  doi: 10.1073/pnas.012452499
– ident: e_1_2_10_13_1
  doi: 10.1046/j.1364-3703.2003.00163.x
– ident: e_1_2_10_70_1
  doi: 10.1104/pp.105.067058
– ident: e_1_2_10_80_1
  doi: 10.1105/tpc.18.00250
– ident: e_1_2_10_50_1
  doi: 10.1074/jbc.M114.558817
– ident: e_1_2_10_23_1
  doi: 10.1111/j.1399-3054.2007.01041.x
– ident: e_1_2_10_27_1
  doi: 10.1146/annurev.phyto.42.040803.140421
– ident: e_1_2_10_66_1
  doi: 10.1111/j.1365-313X.2004.02200.x
– ident: e_1_2_10_3_1
  doi: 10.1007/s11101-017-9530-4
– ident: e_1_2_10_74_1
  doi: 10.1016/j.tplants.2015.08.002
– ident: e_1_2_10_9_1
  doi: 10.1373/clinchem.2008.112797
– ident: e_1_2_10_68_1
  doi: 10.1073/pnas.211311098
– ident: e_1_2_10_7_1
  doi: 10.3390/vaccines6030058
– ident: e_1_2_10_54_1
  doi: 10.1105/tpc.107.054767
– ident: e_1_2_10_65_1
  doi: 10.1093/jxb/ern075
– ident: e_1_2_10_18_1
  doi: 10.1038/s41578-021-00399-5
– ident: e_1_2_10_2_1
  doi: 10.1104/pp.107.111302
– ident: e_1_2_10_51_1
  doi: 10.3390/vaccines9111255
– ident: e_1_2_10_32_1
  doi: 10.1111/j.1467-7652.2010.00508.x
– ident: e_1_2_10_17_1
  doi: 10.1105/tpc.114.131185
– ident: e_1_2_10_36_1
  doi: 10.1111/j.1365-313X.2008.03486.x
– ident: e_1_2_10_29_1
  doi: 10.1104/pp.106.087304
– ident: e_1_2_10_14_1
  doi: 10.1016/j.febslet.2007.12.039
– ident: e_1_2_10_37_1
  doi: 10.1371/journal.pone.0015559
– ident: e_1_2_10_82_1
  doi: 10.1105/tpc.108.065250
– ident: e_1_2_10_12_1
  doi: 10.4161/psb.6.1.14037
– ident: e_1_2_10_42_1
  doi: 10.1371/journal.pone.0033042
– ident: e_1_2_10_22_1
  doi: 10.1111/j.1467-7652.2008.00384.x
– ident: e_1_2_10_15_1
  doi: 10.1038/ncomms8658
– ident: e_1_2_10_53_1
  doi: 10.1104/pp.106.078469
– ident: e_1_2_10_59_1
  doi: 10.1105/tpc.16.00898
– ident: e_1_2_10_75_1
  doi: 10.1186/gb-2002-3-7-research0034
– ident: e_1_2_10_8_1
  doi: 10.3390/plants8110492
– ident: e_1_2_10_35_1
  doi: 10.1105/tpc.106.041103
– ident: e_1_2_10_56_1
  doi: 10.1177/2515135520908121
– ident: e_1_2_10_38_1
  doi: 10.1104/pp.108.3.1277
– ident: e_1_2_10_55_1
  doi: 10.1038/ncomms8649
– ident: e_1_2_10_58_1
  doi: 10.1104/pp.108.119321
– ident: e_1_2_10_63_1
  doi: 10.31083/j.fbl2711310
– ident: e_1_2_10_10_1
  doi: 10.1111/j.1365-3040.2005.01369.x
– ident: e_1_2_10_84_1
  doi: 10.1016/j.chom.2012.04.014
– ident: e_1_2_10_48_1
  doi: 10.1016/j.biochi.2012.06.011
– ident: e_1_2_10_34_1
  doi: 10.1021/acs.jproteome.9b00409
– ident: e_1_2_10_83_1
  doi: 10.1111/nph.12256
– ident: e_1_2_10_64_1
  doi: 10.1093/emboj/cdf312
– ident: e_1_2_10_40_1
  doi: 10.1146/annurev-phyto-080516-035406
– ident: e_1_2_10_45_1
  doi: 10.1038/nrm2330
– ident: e_1_2_10_69_1
  doi: 10.1023/B:PLAN.0000038276.95539.39
SSID ssj0021656
Score 2.4720044
SecondaryResourceType review_article
Snippet Summary The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the...
The production of influenza vaccines in plants is achieved through transient expression of viral hemagglutinins (HAs), a process mediated by the bacterial...
SourceID pubmedcentral
proquest
pubmed
crossref
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 1078
SubjectTerms Agrobacterium radiobacter
Agrobacterium tumefaciens - genetics
ascorbic acid
biotechnology
cell walls
chloroplast genes
gene expression
hemagglutinins
Humans
influenza
Influenza hemagglutinin
Influenza Vaccines
Influenza, Human
leaves
lignification
lipid metabolism
Nicotiana - genetics
Nicotiana benthamiana
Orthomyxoviridae - genetics
oxidative stress
oxylipins
Oxylipins - metabolism
phytomass
Plant immunity
Plant Leaves - genetics
Plant molecular farming
Plants, Genetically Modified - genetics
plasma membrane
protein synthesis
recombinant proteins
RNA
salicylic acid
Transient Agrobacterium‐mediated expression
Virus‐like particles
Title Molecular responses of agroinfiltrated Nicotiana benthamiana leaves expressing suppressor of silencing P19 and influenza virus‐like particles
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.14247
https://www.ncbi.nlm.nih.gov/pubmed/38041470
https://www.proquest.com/docview/2896803890
https://www.proquest.com/docview/3153171249
https://pubmed.ncbi.nlm.nih.gov/PMC11022802
Volume 22
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwELZKucCBN2ULrAziwCWrOHFe4tRCl4LUalVRqQekyI6dbdRtsko2FeqJfwC_kV_CjJ1EXUolxCWyknHix4xn7Mx8Q8ibMHR1ECvp6FALhzMZOYkQ0nETpVymlNQmx9LBYbh_zD-fBCcb5F0fC2PxIYYDN5QMs16jgAvZXBHypSwmGKaFkeTMDxE3_8PRAB3lIaqMjSyKnAiUfocqhF48Q811XXTNwLzuJ3nVfjUKaHqffO2bbv1OzibtSk6yyz9QHf-zbw_Ivc4wpTuWkx6SDV0-Ind35nUHzqEfkx8HfS5dWlvXWt3QKqdiXlfAqMXCIN0qityFC4egErp0Ks5NeaHFBdDrb9b1tpzTpl2aclXjW5oC45_w_owlVJSKFjaByqWgF0XdNr--_1wUZ5oue2e-J-R4uvfl_b7TJXRwMs6TyAl1lmRgcuVC-jKOZSQ96amEuyKLMx3kIdhKQoH-ZEwJT7CIaSi7Cl1khVCe_5RsllWpnxGqWKZgYmSYBSHPmUiCHC09zhFRzPX0iLztpzbNOrRzTLqxSPtdD4xxasZ4RF4PpEsL8fE3olc9f6QggPhXRZS6apsUdqxhjDCF7s00PugV6A1sdUdky_LU8CkfEaB4BLXjNW4bCBAAfP1JWZwaIHDGDJqRB5013HRz89PZ7idT2P530ufkjgcWnPXufEE2V3WrX4IFtpJjcsvjM7jG049jcnt373B2NDanGWMjhL8BSQg3ug
linkProvider Wiley-Blackwell
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV1Lb9QwELZKOUAPiDdbXgZx4BIUZx0nkbgURLWFbrWHVuotGsfONmJJVkm3Qj31H9Df2F_CjPNQV6USNysZJ7HHY3_jjL9h7INSvg1joz2rLHhS6MhLALTnJ8b4whhtXY6l6YGaHMnvx-HxBvvcn4Vp-SGGDTeyDDdfk4HThvQ1K1_q4hOd04rusLsScTkF9AVyNrhbxCvTni2KvAiX_Y5XiOJ4hqrrq9ENiHkzUvI6gnVL0O5D9qDDjnynVfYjtmHLx2xrZ153_Bn2Cfsz7dPd8rqNfrUNr3IO87rCsVQsHBmt4TQAyLaBa3znCfxy5YWFM5S3v9vo2HLOm9XSlauantIUdESJrs9EwqE0vGhznJwDPyvqVXN1cbkoflq-7OPtnrKj3W-HXydel3PBy6RMIk_ZLMkQFeWgxzqOdaQDHZhE-pDFmQ1zhXAGDC5xQhgIQETCYtk3FMUKYILxM7ZZVqV9wbgRmcGe0yoLlcwFJGFOYExKIv3yAztiH_u-T7OOkJzyYizS3jFBNaVOTSP2fhBdtiwc_xJ61yswRRuhHx9Q2mrVpOhUqpiYBP3bZcY49WNr0Bsdseet0odXjYmkSUZYO14bDoMAcXSv3ymLE8fVLYQjHAqwsW7k3P756ezLnits_7_oW3ZvcjjdT_f3Dn68ZPcDBFxtMOYrtnlar-xrBEyn-o2zi793vRbb
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV1Lb9QwELZKKyF6qHiz5WUQBy5BcdZxEnFaHqsWaLUHFlVcIjt2tlG3SZR0q4oT_wB-I7-EGTuJuiqVuFnJOI49M_ZMMvMNIa-E8E0Ya-UZYaTHmYq8RErl-YnWPtNaGVtj6eBQ7M35p6PwaIO87XNhHD7E8MENNcPu16jgtc4vKXmtijeYphXdIFuIkgdCvjX5Nv8-H_wtBJZxyUWRF8G53wELYSDP0Hn9OLpiY14NlbxswtozaHqb7HTGI504bt8hG6a8S7Yni6YD0DD3yK-Dvt4tbVz4q2lplVO5aCoQpmJp0Wg1RQlA5ZZUwZjH8tS2l0aeA725cOGx5YK2q9q2qwaf0haYo4TXZyyhstS0cEVOfkh6XjSr9s_P38vixNC6D7i7T-bTj1_f73ld0QUv4zyJPGGyJAOzKJdqrOJYRSpQgU64L7M4M2EuwJ6RGs44xrQMJIuYgbavMYxVSh2MH5DNsirNI0I1yzSsnBJZKHjOZBLmaI1xjqhffmBG5HW_9mnWIZJjYYxl2nsmwKbUsmlEXg6ktYPh-BfRi56BKSgJ_vmQpalWbQpepYgRStC_nmYMez_MBtzREXnomD4MNUaUJh5B73hNHAYCBOlev1MWxxasmzGLOBTAZK3kXP_66ezdvm3s_j_pc3Jz9mGaftk__PyY3ArA4HLBmE_I5lmzMk_BYDpTzzrF-AvZuBfK
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=Molecular+responses+of+agroinfiltrated+Nicotiana+benthamiana+leaves+expressing+suppressor+of+silencing+P19+and+influenza+virus-like+particles&rft.jtitle=Plant+biotechnology+journal&rft.au=Hamel%2C+Louis-Philippe&rft.au=Tardif%2C+Rachel&rft.au=Poirier-Gravel%2C+Francis&rft.au=Rasoolizadeh%2C+Asieh&rft.date=2024-05-01&rft.eissn=1467-7652&rft.volume=22&rft.issue=5&rft.spage=1078&rft_id=info:doi/10.1111%2Fpbi.14247&rft_id=info%3Apmid%2F38041470&rft.externalDocID=38041470
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1467-7644&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1467-7644&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1467-7644&client=summon