Orchestration of hydrogen peroxide and nitric oxide in brassinosteroid‐mediated systemic virus resistance in Nicotiana benthamiana

Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accomp...

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Published inThe Plant journal : for cell and molecular biology Vol. 85; no. 4; pp. 478 - 493
Main Authors Deng, Xing‐Guang, Zhu, Tong, Zou, Li‐Juan, Han, Xue‐Ying, Zhou, Xue, Xi, De‐Hui, Zhang, Da‐Wei, Lin, Hong‐Hui
Format Journal Article
LanguageEnglish
Published England Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology 01.02.2016
Blackwell Publishing Ltd
Subjects
brassinosteroids
Brassinosteroids - metabolism
Disease Resistance
Gene Expression Regulation, Plant
genes
Genes, Reporter
Hydrogen peroxide
Hydrogen Peroxide - metabolism
Kinases
Leaves
Models, Biological
NAD(P)H oxidase (H2O2-forming)
NADP (coenzyme)
NADPH Oxidases - genetics
NADPH Oxidases - metabolism
Nicotiana - cytology
Nicotiana - genetics
Nicotiana - immunology
Nicotiana benthamiana
nitrate reductase
Nitric oxide
Nitric Oxide - metabolism
nitroprusside
Plant Diseases - immunology
Plant growth
Plant Leaves - cytology
Plant Leaves - genetics
Plant Leaves - immunology
Plant Proteins - genetics
Plant Proteins - metabolism
Reactive Oxygen Species - metabolism
Signal Transduction
stress response
systemic virus resistance
Tobacco Mosaic Virus - pathogenicity
viruses
virus‐induced gene silencing
Nicotiana benthamiana
nitric oxide
brassinosteroids
virus-induced gene silencing
hydrogen peroxide
systemic virus resistance
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Abstract Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H₂O₂ and NO. Scavenging of H₂O₂ or NO in upper leaves blocked BR‐induced systemic virus resistance. BR‐induced systemic H₂O₂ accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite‐dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR‐triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR‐activated H₂O₂ is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H₂O₂ generation blocked BR‐induced systemic NO production, but BR‐induced H₂O₂ production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR‐induced systemic virus defense in NbRBOHB‐silenced plants, but H₂O₂ did not reverse the effect of NbNR silencing on BR‐induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR‐mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR‐induced H₂O₂ and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR‐mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)‐dependent H₂O₂ production and subsequent systemic NR‐dependent NO generation.
AbstractList Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H2O2 and NO. Scavenging of H2O2 or NO in upper leaves blocked BR-induced systemic virus resistance. BR-induced systemic H2O2 accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite-dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR-triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR-activated H2O2 is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H2O2 generation blocked BR-induced systemic NO production, but BR-induced H2O2 production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR-induced systemic virus defense in NbRBOHB-silenced plants, but H2O2 did not reverse the effect of NbNR silencing on BR-induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR-mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR-induced H2O2 and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR-mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)-dependent H2O2 production and subsequent systemic NR-dependent NO generation.
Brassinosteroids ( BR s) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BR s in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BR s induced virus resistance in upper untreated leaves, accompanied by accumulations of H 2 O 2 and NO . Scavenging of H 2 O 2 or NO in upper leaves blocked BR ‐induced systemic virus resistance. BR ‐induced systemic H 2 O 2 accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene Nb RBOHB , but not by systemic NADPH oxidase inhibition or Nb RBOHA silencing. Silencing of the nitrite‐dependent nitrate reductase gene Nb NR or systemic pharmacological inhibition of NR compromised BR ‐triggered systemic NO accumulation, while local inhibition of NR , silencing of Nb NOA 1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR ‐activated H 2 O 2 is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H 2 O 2 generation blocked BR ‐induced systemic NO production, but BR ‐induced H 2 O 2 production was not sensitive to NO scavengers or silencing of Nb NR . Systemically applied sodium nitroprusside rescued BR ‐induced systemic virus defense in Nb RBOHB ‐silenced plants, but H 2 O 2 did not reverse the effect of Nb NR silencing on BR ‐induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI 1(BR insensitive 1) is an upstream component in BR ‐mediated systemic defense signaling, as silencing of Nb BRI 1 compromised the BR ‐induced H 2 O 2 and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR ‐mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)‐dependent H 2 O 2 production and subsequent systemic NR ‐dependent NO generation. Through pharmacological and genetic approaches in combination with infection experiments, we established a signaling pathway leading to BR‐mediated systemic defense response that involved local RBOHB‐dependent H 2 O 2 production and subsequent systemic NR‐dependent NO generation.
Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H2O2 and NO. Scavenging of H2O2 or NO in upper leaves blocked BR-induced systemic virus resistance. BR-induced systemic H2O2 accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite-dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR-triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR-activated H2O2 is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H2O2 generation blocked BR-induced systemic NO production, but BR-induced H2O2 production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR-induced systemic virus defense in NbRBOHB-silenced plants, but H2O2 did not reverse the effect of NbNR silencing on BR-induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR-mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR-induced H2O2 and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR-mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)-dependent H2O2 production and subsequent systemic NR-dependent NO generation.Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H2O2 and NO. Scavenging of H2O2 or NO in upper leaves blocked BR-induced systemic virus resistance. BR-induced systemic H2O2 accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite-dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR-triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR-activated H2O2 is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H2O2 generation blocked BR-induced systemic NO production, but BR-induced H2O2 production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR-induced systemic virus defense in NbRBOHB-silenced plants, but H2O2 did not reverse the effect of NbNR silencing on BR-induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR-mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR-induced H2O2 and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR-mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)-dependent H2O2 production and subsequent systemic NR-dependent NO generation.
Summary Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H2O2 and NO. Scavenging of H2O2 or NO in upper leaves blocked BR‐induced systemic virus resistance. BR‐induced systemic H2O2 accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite‐dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR‐triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR‐activated H2O2 is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H2O2 generation blocked BR‐induced systemic NO production, but BR‐induced H2O2 production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR‐induced systemic virus defense in NbRBOHB‐silenced plants, but H2O2 did not reverse the effect of NbNR silencing on BR‐induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR‐mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR‐induced H2O2 and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR‐mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)‐dependent H2O2 production and subsequent systemic NR‐dependent NO generation. Significance Statement Through pharmacological and genetic approaches in combination with infection experiments, we established a signaling pathway leading to BR‐mediated systemic defense response that involved local RBOHB‐dependent H2O2 production and subsequent systemic NR‐dependent NO generation.
Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H₂O₂ and NO. Scavenging of H₂O₂ or NO in upper leaves blocked BR‐induced systemic virus resistance. BR‐induced systemic H₂O₂ accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite‐dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR‐triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR‐activated H₂O₂ is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H₂O₂ generation blocked BR‐induced systemic NO production, but BR‐induced H₂O₂ production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR‐induced systemic virus defense in NbRBOHB‐silenced plants, but H₂O₂ did not reverse the effect of NbNR silencing on BR‐induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR‐mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR‐induced H₂O₂ and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR‐mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)‐dependent H₂O₂ production and subsequent systemic NR‐dependent NO generation.
Summary Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H2O2 and NO. Scavenging of H2O2 or NO in upper leaves blocked BR-induced systemic virus resistance. BR-induced systemic H2O2 accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite-dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR-triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR-activated H2O2 is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H2O2 generation blocked BR-induced systemic NO production, but BR-induced H2O2 production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR-induced systemic virus defense in NbRBOHB-silenced plants, but H2O2 did not reverse the effect of NbNR silencing on BR-induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR-mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR-induced H2O2 and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR-mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)-dependent H2O2 production and subsequent systemic NR-dependent NO generation. Significance Statement Through pharmacological and genetic approaches in combination with infection experiments, we established a signaling pathway leading to BR-mediated systemic defense response that involved local RBOHB-dependent H2O2 production and subsequent systemic NR-dependent NO generation.
Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H sub(2)O sub(2) and NO. Scavenging of H sub(2)O sub(2) or NO in upper leaves blocked BR-induced systemic virus resistance. BR-induced systemic H sub(2)O sub(2) accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite-dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR-triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR-activated H sub(2)O sub(2) is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H sub(2)O sub(2) generation blocked BR-induced systemic NO production, but BR-induced H sub(2)O sub(2) production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR-induced systemic virus defense in NbRBOHB-silenced plants, but H sub(2)O sub(2) did not reverse the effect of NbNR silencing on BR-induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR-mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR-induced H sub(2)O sub(2) and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR-mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)-dependent H sub(2)O sub(2) production and subsequent systemic NR-dependent NO generation. Significance Statement Through pharmacological and genetic approaches in combination with infection experiments, we established a signaling pathway leading to BR-mediated systemic defense response that involved local RBOHB-dependent H sub(2)O sub(2) production and subsequent systemic NR-dependent NO generation.
Author Lin, Hong‐Hui
Zhang, Da‐Wei
Deng, Xing‐Guang
Zou, Li‐Juan
Xi, De‐Hui
Han, Xue‐Ying
Zhu, Tong
Zhou, Xue
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  fullname: Han, Xue‐Ying
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/26749255$$D View this record in MEDLINE/PubMed
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Issue 4
Keywords Nicotiana benthamiana
nitric oxide
brassinosteroids
virus-induced gene silencing
hydrogen peroxide
systemic virus resistance
Language English
License 2016 The Authors The Plant Journal © 2016 John Wiley & Sons Ltd.
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Snippet Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance...
Summary Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic...
Brassinosteroids ( BR s) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BR s in plant systemic...
Summary Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic...
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SubjectTerms brassinosteroids
Brassinosteroids - metabolism
Disease Resistance
Gene Expression Regulation, Plant
genes
Genes, Reporter
Hydrogen peroxide
Hydrogen Peroxide - metabolism
Kinases
Leaves
Models, Biological
NAD(P)H oxidase (H2O2-forming)
NADP (coenzyme)
NADPH Oxidases - genetics
NADPH Oxidases - metabolism
Nicotiana - cytology
Nicotiana - genetics
Nicotiana - immunology
Nicotiana benthamiana
nitrate reductase
Nitric oxide
Nitric Oxide - metabolism
nitroprusside
Plant Diseases - immunology
Plant growth
Plant Leaves - cytology
Plant Leaves - genetics
Plant Leaves - immunology
Plant Proteins - genetics
Plant Proteins - metabolism
Reactive Oxygen Species - metabolism
Signal Transduction
stress response
systemic virus resistance
Tobacco Mosaic Virus - pathogenicity
viruses
virus‐induced gene silencing
Title Orchestration of hydrogen peroxide and nitric oxide in brassinosteroid‐mediated systemic virus resistance in Nicotiana benthamiana
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Ftpj.13120
https://www.ncbi.nlm.nih.gov/pubmed/26749255
https://www.proquest.com/docview/1764686586
https://www.proquest.com/docview/1765117877
https://www.proquest.com/docview/1803088735
https://www.proquest.com/docview/1850769972
Volume 85
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