The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana

Jessica L. Erickson; Norman Adlung; Christina Lampe; Ulla Bonas; Martin H. Schattat

doi:10.1111/tpj.13813

The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana

Jessica L. Erickson
, Norman Adlung
, Christina Lampe
, Ulla Bonas^*
, Martin H. Schattat

^*Corresponding author for this work

Not published at VTT

Martin Luther University Halle-Wittenberg

Research output: Contribution to journal › Article › Scientific › peer-review

52 Citations (Scopus)

Abstract

Xanthomonas campestris pv. vesicatoria type III-secreted effectors were screened for candidates influencing plant cell processes relevant to the formation and maintenance of stromules in Nicotiana benthamiana lower leaf epidermis. Transient expression of XopL, a unique type of E3 ubiquitin ligase, led to a nearly complete elimination of stromules and the relocation of plastids to the nucleus. Further characterization of XopL revealed that the E3 ligase activity is essential for the two plastid phenotypes. In contrast to the XopL wild type, a mutant XopL lacking E3 ligase activity specifically localized to microtubules. Interestingly, mutant XopL-labeled filaments frequently aligned with stromules, suggesting an important, yet unexplored, microtubule–stromule relationship. High time-resolution movies confirmed that microtubules provide a scaffold for stromule movement and contribute to stromule shape. Taken together, this study has defined two populations of stromules: microtubule-dependent stromules, which were found to move slower and persist longer, and microtubule-independent stromules, which move faster and are transient. Our results provide the basis for a new model of stromule dynamics including interactions with both actin and microtubules.

Original language	English
Pages (from-to)	856-870
Journal	Plant Journal
Volume	93
Issue number	5
DOIs	https://doi.org/10.1111/tpj.13813
Publication status	Published - Mar 2018
MoE publication type	A1 Journal article-refereed

Funding

We would like to acknowledge Ralf Klo€sgen, Katharina Bu€rsten-binder and Jaideep Mathur for providing constructs, and Peter John, who cloned pGGA11. This work was funded by grants from the Deutsche Forschungsgemeinschaft (CRC 648 “Molecular mechanisms of information processing in plants” and the Gottfried Wilhelm Leibniz-Prize) to UB. Additional funding was provided by Martin Luther University, Halle-Wittenberg, Halle, Germany.

Keywords

actin
E3 ubiquitin ligase
microtubules
Nicotiana benthamiana
stromule dynamics
stromule morphology
stromule velocity
Xanthomonas campestris pv. vesicatoria
XopL
Tobacco/cytology
Actin Cytoskeleton/metabolism
Thiazolidines/pharmacology
Dinitrobenzenes/pharmacology
Plant Cells
Microtubules/metabolism
Bridged Bicyclo Compounds, Heterocyclic/pharmacology
Sulfanilamides/pharmacology
Bacterial Proteins/genetics
Plants, Genetically Modified
Green Fluorescent Proteins/genetics
Xanthomonas campestris/metabolism
Mutation
Plastids/metabolism
Ubiquitin-Protein Ligases/genetics

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10.1111/tpj.13813

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@article{84d5c8b8b1bf41b4afd58ab628c56eb8,

title = "The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana",

abstract = "Xanthomonas campestris pv. vesicatoria type III-secreted effectors were screened for candidates influencing plant cell processes relevant to the formation and maintenance of stromules in Nicotiana benthamiana lower leaf epidermis. Transient expression of XopL, a unique type of E3 ubiquitin ligase, led to a nearly complete elimination of stromules and the relocation of plastids to the nucleus. Further characterization of XopL revealed that the E3 ligase activity is essential for the two plastid phenotypes. In contrast to the XopL wild type, a mutant XopL lacking E3 ligase activity specifically localized to microtubules. Interestingly, mutant XopL-labeled filaments frequently aligned with stromules, suggesting an important, yet unexplored, microtubule–stromule relationship. High time-resolution movies confirmed that microtubules provide a scaffold for stromule movement and contribute to stromule shape. Taken together, this study has defined two populations of stromules: microtubule-dependent stromules, which were found to move slower and persist longer, and microtubule-independent stromules, which move faster and are transient. Our results provide the basis for a new model of stromule dynamics including interactions with both actin and microtubules.",

keywords = "actin, E3 ubiquitin ligase, microtubules, Nicotiana benthamiana, stromule dynamics, stromule morphology, stromule velocity, Xanthomonas campestris pv. vesicatoria, XopL, Tobacco/cytology, Actin Cytoskeleton/metabolism, Thiazolidines/pharmacology, Dinitrobenzenes/pharmacology, Plant Cells, Microtubules/metabolism, Bridged Bicyclo Compounds, Heterocyclic/pharmacology, Sulfanilamides/pharmacology, Bacterial Proteins/genetics, Plants, Genetically Modified, Green Fluorescent Proteins/genetics, Xanthomonas campestris/metabolism, Mutation, Plastids/metabolism, Ubiquitin-Protein Ligases/genetics",

author = "Erickson, \{Jessica L.\} and Norman Adlung and Christina Lampe and Ulla Bonas and Schattat, \{Martin H.\}",

note = "Funding Information: We would like to acknowledge Ralf Klo€sgen, Katharina Bu€rsten-binder and Jaideep Mathur for providing constructs, and Peter John, who cloned pGGA11. This work was funded by grants from the Deutsche Forschungsgemeinschaft (CRC 648 “Molecular mechanisms of information processing in plants” and the Gottfried Wilhelm Leibniz-Prize) to UB. Additional funding was provided by Martin Luther University, Halle-Wittenberg, Halle, Germany. Publisher Copyright: {\textcopyright} 2017 The Authors The Plant Journal {\textcopyright} 2017 John Wiley \& Sons Ltd",

year = "2018",

month = mar,

doi = "10.1111/tpj.13813",

language = "English",

volume = "93",

pages = "856--870",

journal = "Plant Journal",

issn = "0960-7412",

publisher = "Wiley",

number = "5",

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TY - JOUR

T1 - The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana

AU - Erickson, Jessica L.

AU - Adlung, Norman

AU - Lampe, Christina

AU - Bonas, Ulla

AU - Schattat, Martin H.

N1 - Funding Information: We would like to acknowledge Ralf Klo€sgen, Katharina Bu€rsten-binder and Jaideep Mathur for providing constructs, and Peter John, who cloned pGGA11. This work was funded by grants from the Deutsche Forschungsgemeinschaft (CRC 648 “Molecular mechanisms of information processing in plants” and the Gottfried Wilhelm Leibniz-Prize) to UB. Additional funding was provided by Martin Luther University, Halle-Wittenberg, Halle, Germany. Publisher Copyright: © 2017 The Authors The Plant Journal © 2017 John Wiley & Sons Ltd

PY - 2018/3

Y1 - 2018/3

N2 - Xanthomonas campestris pv. vesicatoria type III-secreted effectors were screened for candidates influencing plant cell processes relevant to the formation and maintenance of stromules in Nicotiana benthamiana lower leaf epidermis. Transient expression of XopL, a unique type of E3 ubiquitin ligase, led to a nearly complete elimination of stromules and the relocation of plastids to the nucleus. Further characterization of XopL revealed that the E3 ligase activity is essential for the two plastid phenotypes. In contrast to the XopL wild type, a mutant XopL lacking E3 ligase activity specifically localized to microtubules. Interestingly, mutant XopL-labeled filaments frequently aligned with stromules, suggesting an important, yet unexplored, microtubule–stromule relationship. High time-resolution movies confirmed that microtubules provide a scaffold for stromule movement and contribute to stromule shape. Taken together, this study has defined two populations of stromules: microtubule-dependent stromules, which were found to move slower and persist longer, and microtubule-independent stromules, which move faster and are transient. Our results provide the basis for a new model of stromule dynamics including interactions with both actin and microtubules.

AB - Xanthomonas campestris pv. vesicatoria type III-secreted effectors were screened for candidates influencing plant cell processes relevant to the formation and maintenance of stromules in Nicotiana benthamiana lower leaf epidermis. Transient expression of XopL, a unique type of E3 ubiquitin ligase, led to a nearly complete elimination of stromules and the relocation of plastids to the nucleus. Further characterization of XopL revealed that the E3 ligase activity is essential for the two plastid phenotypes. In contrast to the XopL wild type, a mutant XopL lacking E3 ligase activity specifically localized to microtubules. Interestingly, mutant XopL-labeled filaments frequently aligned with stromules, suggesting an important, yet unexplored, microtubule–stromule relationship. High time-resolution movies confirmed that microtubules provide a scaffold for stromule movement and contribute to stromule shape. Taken together, this study has defined two populations of stromules: microtubule-dependent stromules, which were found to move slower and persist longer, and microtubule-independent stromules, which move faster and are transient. Our results provide the basis for a new model of stromule dynamics including interactions with both actin and microtubules.

KW - actin

KW - E3 ubiquitin ligase

KW - microtubules

KW - Nicotiana benthamiana

KW - stromule dynamics

KW - stromule morphology

KW - stromule velocity

KW - Xanthomonas campestris pv. vesicatoria

KW - XopL

KW - Tobacco/cytology

KW - Actin Cytoskeleton/metabolism

KW - Thiazolidines/pharmacology

KW - Dinitrobenzenes/pharmacology

KW - Plant Cells

KW - Microtubules/metabolism

KW - Bridged Bicyclo Compounds, Heterocyclic/pharmacology

KW - Sulfanilamides/pharmacology

KW - Bacterial Proteins/genetics

KW - Plants, Genetically Modified

KW - Green Fluorescent Proteins/genetics

KW - Xanthomonas campestris/metabolism

KW - Mutation

KW - Plastids/metabolism

KW - Ubiquitin-Protein Ligases/genetics

UR - https://www.scopus.com/pages/publications/85041185160

U2 - 10.1111/tpj.13813

DO - 10.1111/tpj.13813

M3 - Article

C2 - 29285819

AN - SCOPUS:85041185160

SN - 0960-7412

VL - 93

SP - 856

EP - 870

JO - Plant Journal

JF - Plant Journal

IS - 5

ER -

The Xanthomonas effector XopL uncovers the role of microtubules in stromule extension and dynamics in Nicotiana benthamiana

Abstract

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Keywords

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