Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

PNAS 109 (1): 297-302

Copyright © 2012 by the National Academy of Sciences.


BIOLOGICAL SCIENCES / PLANT BIOLOGY

Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns

Youssef Belkhadira,b,1, Yvon Jaillaisa,b,1, Petra Epplec, Emilia Balsemão-Piresa,b,2, Jeffery L. Danglc,d,3, and Joanne Chorya,b,3

aPlant Biology Laboratory and bHoward Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, CA 92037; and cHoward Hughes Medical Institute, Department of Biology, and dDepartment of Microbiology and Immunology, Curriculum in Genetics, Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, NC 27599

Contributed by Joanne Chory, August 6, 2011 (sent for review June 16, 2011)

Abstract: Metazoans and plants use pattern recognition receptors (PRRs) to sense conserved microbial-associated molecular patterns (MAMPs) in the extracellular environment. In plants, the bacterial MAMPs flagellin and elongation factor Tu (EF-Tu) activate distinct, phylogenetically related cell surface pattern recognition receptors of the leucine-rich repeat receptor kinase (LRR-RK) family called FLS2 and EF-Tu receptor, respectively. BAK1 is an LRR-RK coreceptor for both FLS2 and EF-Tu receptor. BAK1 is also a coreceptor for the plant brassinosteroid (BR) receptor, the LRR-RK BRI1. Binding of BR to BRI1 primarily promotes cell elongation. Here, we tune the BR pathway response to establish how plant cells can generate functionally different cellular outputs in response to MAMPs and pathogens. We demonstrate that BR can act antagonistically or synergistically with responses to MAMPs. We further show that the synergistic activities of BRs on MAMP responses require BAK1. Our results highlight the importance of plant steroid homeostasis as a critical step in the establishment of plant immunity. We propose that tradeoffs associated with plasticity in the face of infection are layered atop plant steroid developmental programs.

Key Words: brassinosteroid signaling • plant immune system signaling • signaling crosstalk


Author contributions: Y.B., Y.J., P.E., E.B.-P., J.L.D., and J.C. designed research; Y.B., Y.J., P.E., and E.B.-P. performed research; Y.B., Y.J., P.E., E.B.-P., J.L.D., and J.C. analyzed data; and Y.B., Y.J., P.E., J.L.D., and J.C. wrote the paper.

1Y.B. and Y.J. contributed equally to this work.

2Present address: Department of Genetics, Laboratório de Genômica Funcional e Transdução de Sinal, Universidade Federal do Rio de Janeiro, 21944-970, Rio de Janeiro, Brazil.

The authors declare no conflict of interest.

See Commentary on page 7.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1112840108/-/DCSupplemental.

3To whom correspondence may be addressed. E-mail: chory{at}salk.edu or dangl{at}e-mail.unc.edu.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
An XA21-Associated Kinase (OsSERK2) Regulates Immunity Mediated by the XA21 and XA3 Immune Receptors.
X. Chen, S. Zuo, B. Schwessinger, M. Chern, P. E. Canlas, D. Ruan, X. Zhou, J. Wang, A. Daudi, C. J. Petzold, et al. (2014)
Mol Plant
   Abstract »    Full Text »    PDF »
Antagonistic Regulation of Growth and Immunity by the Arabidopsis Basic Helix-Loop-Helix Transcription Factor HOMOLOG OF BRASSINOSTEROID ENHANCED EXPRESSION2 INTERACTING WITH INCREASED LEAF INCLINATION1 BINDING bHLH1.
F. G. Malinovsky, M. Batoux, B. Schwessinger, J. H. Youn, L. Stransfeld, J. Win, S.-K. Kim, and C. Zipfel (2014)
Plant Physiology 164, 1443-1455
   Abstract »    Full Text »    PDF »
The bHLH Transcription Factor HBI1 Mediates the Trade-Off between Growth and Pathogen-Associated Molecular Pattern-Triggered Immunity in Arabidopsis.
M. Fan, M.-Y. Bai, J.-G. Kim, T. Wang, E. Oh, L. Chen, C. H. Park, S.-H. Son, S.-K. Kim, M. B. Mudgett, et al. (2014)
PLANT CELL 26, 828-841
   Abstract »    Full Text »    PDF »
The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth.
R. Lozano-Duran, A. P. Macho, F. Boutrot, C. Segonzac, I. E. Somssich, and C. Zipfel (2013)
eLife Sci 2, e00983
   Abstract »    Full Text »    PDF »
A Mathematical Model for the Coreceptors SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 and SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE3 in BRASSINOSTEROID INSENSITIVE1-Mediated Signaling.
W. van Esse, S. van Mourik, C. Albrecht, J. van Leeuwen, and S. de Vries (2013)
Plant Physiology 163, 1472-1481
   Abstract »    Full Text »    PDF »
Molecular Mechanism for Plant Steroid Receptor Activation by Somatic Embryogenesis Co-Receptor Kinases.
J. Santiago, C. Henzler, and M. Hothorn (2013)
Science 341, 889-892
   Abstract »    Full Text »    PDF »
Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1.
W. Lin, D. Lu, X. Gao, S. Jiang, X. Ma, Z. Wang, T. Mengiste, P. He, and L. Shan (2013)
PNAS 110, 12114-12119
   Abstract »    Full Text »    PDF »
The Pseudomonas syringae Type III Effector AvrRpt2 Promotes Pathogen Virulence via Stimulating Arabidopsis Auxin/Indole Acetic Acid Protein Turnover.
F. Cui, S. Wu, W. Sun, G. Coaker, B. Kunkel, P. He, and L. Shan (2013)
Plant Physiology 162, 1018-1029
   Abstract »    Full Text »    PDF »
Recent Progress in Understanding PAMP- and Effector-Triggered Immunity against the Rice Blast Fungus Magnaporthe oryzae.
W. Liu, J. Liu, Y. Ning, B. Ding, X. Wang, Z. Wang, and G.-L. Wang (2013)
Mol Plant 6, 605-620
   Abstract »    Full Text »    PDF »
Transcriptomic Analysis of the Role of Carboxylic Acids in Metabolite Signaling in Arabidopsis Leaves.
I. Finkemeier, A.-C. Konig, W. Heard, A. Nunes-Nesi, P. A. Pham, D. Leister, A. R. Fernie, and L. J. Sweetlove (2013)
Plant Physiology 162, 239-253
   Abstract »    Full Text »    PDF »
Brassinosteroid signalling.
J.-Y. Zhu, J. Sae-Seaw, and Z.-Y. Wang (2013)
Development 140, 1615-1620
   Abstract »    Full Text »    PDF »
Brassinosteroid-regulated GSK3/Shaggy-like Kinases Phosphorylate Mitogen-activated Protein (MAP) Kinase Kinases, Which Control Stomata Development in Arabidopsis thaliana.
M. Khan, W. Rozhon, J. Bigeard, D. Pflieger, S. Husar, A. Pitzschke, M. Teige, C. Jonak, H. Hirt, and B. Poppenberger (2013)
J. Biol. Chem. 288, 7519-7527
   Abstract »    Full Text »    PDF »
BR-SIGNALING KINASE1 Physically Associates with FLAGELLIN SENSING2 and Regulates Plant Innate Immunity in Arabidopsis.
H. Shi, Q. Shen, Y. Qi, H. Yan, H. Nie, Y. Chen, T. Zhao, F. Katagiri, and D. Tang (2013)
PLANT CELL 25, 1143-1157
   Abstract »    Full Text »    PDF »
Ethylene promotes hyponastic growth through interaction with ROTUNDIFOLIA3/CYP90C1 in Arabidopsis.
J. K. Polko, R. Pierik, M. van Zanten, D. Tarkowska, M. Strnad, L. A. C. J. Voesenek, and A. J. M. Peeters (2013)
J. Exp. Bot. 64, 613-624
   Abstract »    Full Text »    PDF »
Recent Insights into Brassinosteroid Signaling in Plants: Its Dual Control of Plant Immunity and Stomatal Development.
X. Kong, J. Pan, G. Cai, and D. Li (2012)
Mol Plant 5, 1179-1181
   Abstract »    Full Text »    PDF »
Canopy Light and Plant Health.
C. L. Ballare, C. A. Mazza, A. T. Austin, and R. Pierik (2012)
Plant Physiology 160, 145-155
   Full Text »    PDF »
Plasma Membrane Calcium ATPases Are Important Components of Receptor-Mediated Signaling in Plant Immune Responses and Development.
N. Frei dit Frey, M. Mbengue, M. Kwaaitaal, L. Nitsch, D. Altenbach, H. Haweker, R. Lozano-Duran, M. F. Njo, T. Beeckman, B. Huettel, et al. (2012)
Plant Physiology 159, 798-809
   Abstract »    Full Text »    PDF »
Structural and Functional Analysis of VQ Motif-Containing Proteins in Arabidopsis as Interacting Proteins of WRKY Transcription Factors.
Y. Cheng, Y. Zhou, Y. Yang, Y.-J. Chi, J. Zhou, J.-Y. Chen, F. Wang, B. Fan, K. Shi, Y.-H. Zhou, et al. (2012)
Plant Physiology 159, 810-825
   Abstract »    Full Text »    PDF »
Brassinosteroids Antagonize Gibberellin- and Salicylate-Mediated Root Immunity in Rice.
D. De Vleesschauwer, E. Van Buyten, K. Satoh, J. Balidion, R. Mauleon, I.-R. Choi, C. Vera-Cruz, S. Kikuchi, and M. Hofte (2012)
Plant Physiology 158, 1833-1846
   Abstract »    Full Text »    PDF »
Boosting Crop Yields with Plant Steroids.
C. Vriet, E. Russinova, and C. Reuzeau (2012)
PLANT CELL 24, 842-857
   Abstract »    Full Text »    PDF »
Brassinosteroids modulate plant immunity at multiple levels.
Z.-Y. Wang (2012)
PNAS 109, 7-8
   Full Text »    PDF »
Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1.
C. Albrecht, F. Boutrot, C. Segonzac, B. Schwessinger, S. Gimenez-Ibanez, D. Chinchilla, J. P. Rathjen, S. C. de Vries, and C. Zipfel (2012)
PNAS 109, 303-308
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882