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Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development

Nicolas Frei Dit Frey, Malick Mbengue, Mark Kwaaitaal, Lisette Nitsch, Denise Altenbach, Heidrun Häweker, Rosa Lozano-Duran, Maria Njo UGent, Tom Beeckman UGent, Bruno Huettel, et al. (2012) PLANT PHYSIOLOGY. 159(2). p.798-809
abstract
Plasma membrane-resident receptor kinases (RKs) initiate signaling pathways important for plant immunity and development. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating FLS2-mediated signaling remain largely unknown. We show that plasma membrane ARABIDOPSIS-AUTOINHIBITED Ca2+-ATPase (ACA8) forms a complex with FLS2 in planta. ACA8 and its closest homolog ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca2+ ions, which is crucial for many of the well-described downstream responses (e.g. generation of reactive oxygen species and the transcriptional activation of defense-associated genes). Mutant aca8 aca10 plants show decreased flg22-induced Ca2+ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas calcium-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca2+ fluxes across the plasma membrane is critical for the coordination of the downstream microbe-associated molecular pattern responses and suggest a mechanistic link between the FLS2 receptor complex and signaling kinases via the secondary messenger Ca2+. ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca2+ ATPases appear to represent general regulatory components of RK-mediated signaling pathways.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
INNATE IMMUNITY, PATTERN-RECOGNITION RECEPTORS, ARABIDOPSIS-THALIANA, MOLECULAR-PATTERNS, PROTEIN-KINASES, NADPH OXIDASE, CELL-DEATH, DEFENSE, BAK1, BRASSINOSTEROIDS
journal title
PLANT PHYSIOLOGY
Plant Physiol.
volume
159
issue
2
pages
798 - 809
Web of Science type
Article
Web of Science id
000304834800022
JCR category
PLANT SCIENCES
JCR impact factor
6.555 (2012)
JCR rank
8/193 (2012)
JCR quartile
1 (2012)
ISSN
0032-0889
DOI
10.1104/pp.111.192575
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
2964832
handle
http://hdl.handle.net/1854/LU-2964832
date created
2012-07-30 11:48:59
date last changed
2016-12-19 15:42:25
@article{2964832,
  abstract     = {Plasma membrane-resident receptor kinases (RKs) initiate signaling pathways important for plant immunity and development. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating FLS2-mediated signaling remain largely unknown. We show that plasma membrane ARABIDOPSIS-AUTOINHIBITED Ca2+-ATPase (ACA8) forms a complex with FLS2 in planta. ACA8 and its closest homolog ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca2+ ions, which is crucial for many of the well-described downstream responses (e.g. generation of reactive oxygen species and the transcriptional activation of defense-associated genes). Mutant aca8 aca10 plants show decreased flg22-induced Ca2+ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas calcium-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca2+ fluxes across the plasma membrane is critical for the coordination of the downstream microbe-associated molecular pattern responses and suggest a mechanistic link between the FLS2 receptor complex and signaling kinases via the secondary messenger Ca2+. ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca2+ ATPases appear to represent general regulatory components of RK-mediated signaling pathways.},
  author       = {Frey, Nicolas Frei Dit and Mbengue, Malick and Kwaaitaal, Mark and Nitsch, Lisette and Altenbach, Denise and H{\"a}weker, Heidrun and Lozano-Duran, Rosa and Njo, Maria and Beeckman, Tom and Huettel, Bruno and Borst, Jan Willem and Panstruga, Ralph and Robatzek, Silke},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  keyword      = {INNATE IMMUNITY,PATTERN-RECOGNITION RECEPTORS,ARABIDOPSIS-THALIANA,MOLECULAR-PATTERNS,PROTEIN-KINASES,NADPH OXIDASE,CELL-DEATH,DEFENSE,BAK1,BRASSINOSTEROIDS},
  language     = {eng},
  number       = {2},
  pages        = {798--809},
  title        = {Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development},
  url          = {http://dx.doi.org/10.1104/pp.111.192575},
  volume       = {159},
  year         = {2012},
}

Chicago
Frey, Nicolas Frei Dit, Malick Mbengue, Mark Kwaaitaal, Lisette Nitsch, Denise Altenbach, Heidrun Häweker, Rosa Lozano-Duran, et al. 2012. “Plasma Membrane Calcium ATPases Are Important Components of Receptor-mediated Signaling in Plant Immune Responses and Development.” Plant Physiology 159 (2): 798–809.
APA
Frey, N. F. D., Mbengue, M., Kwaaitaal, M., Nitsch, L., Altenbach, D., Häweker, H., Lozano-Duran, R., et al. (2012). Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. PLANT PHYSIOLOGY, 159(2), 798–809.
Vancouver
1.
Frey NFD, Mbengue M, Kwaaitaal M, Nitsch L, Altenbach D, Häweker H, et al. Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. PLANT PHYSIOLOGY. 2012;159(2):798–809.
MLA
Frey, Nicolas Frei Dit, Malick Mbengue, Mark Kwaaitaal, et al. “Plasma Membrane Calcium ATPases Are Important Components of Receptor-mediated Signaling in Plant Immune Responses and Development.” PLANT PHYSIOLOGY 159.2 (2012): 798–809. Print.