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 1[W][OPEN] Frederikke Gro Malinovsky 2 , Martine Batoux 3 , Benjamin Schwessinger 4 , Ji Hyun Youn, Lena Stransfeld, Joe Win, Seong-Ki Kim, and Cyril Zipfel* Sainsbury Laboratory, Norwich NR4 7UH, United Kingdom (F.G.M., M.B., B.S., L.S., J.W., C.Z.); and Department of Life Science, Chung-Ang University, Seoul 156–756, Korea (J.H.Y., S.-K.K.) Plants need to finely balance resources allocated to growth and immunity to achieve optimal fitness. A tradeoff between pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and brassinosteroid (BR)-mediated growth was recently reported, but more information about the underlying mechanisms is needed. Here, we identify the basic helix-loop- helix (bHLH) transcription factor HOMOLOG OF BRASSINOSTEROID ENHANCED EXPRESSION2 INTERACTING WITH IBH1 (HBI1) as a negative regulator of PTI signaling in Arabidopsis (Arabidopsis thaliana). HBI1 expression is down-regulated in response to different PAMPs. HBI1 overexpression leads to reduced PAMP-triggered responses. This inhibition correlates with reduced steady-state expression of immune marker genes, leading to increased susceptibility to the bacterium Pseudomonas syringae. Overexpression of the HBI1-related bHLHs BRASSINOSTEROID ENHANCED EXPRESSION2 (BEE2) and CRYPTOCHROME- INTERACTING bHLH (CIB1) partially inhibits immunity, indicating that BEE2 and CIB1 may act redundantly with HBI1. In contrast to its expression pattern upon PAMP treatment, HBI1 expression is enhanced by BR treatment. Also, HBI1-overexpressing plants are hyperresponsive to BR and more resistant to the BR biosynthetic inhibitor brassinazole. HBI1 is nucleus localized, and a mutation in a conserved leucine residue within the first helix of the protein interaction domain impairs its function in BR signaling. Interestingly, HBI1 interacts with several inhibitory atypical bHLHs, which likely keep HBI1 under negative control. Hence, HBI1 is a positive regulator of BR-triggered responses, and the negative effect of PTI is likely due to the antagonism between BR and PTI signaling. This study identifies a novel component involved in the complex tradeoff between innate immunity and BR-regulated growth. The first layer of plant innate immunity is con- stituted by the recognition of pathogen-associated molecular patterns (PAMPs) or microbe-associated mo- lecular patterns that act as distinctive microbial features betraying the presence of potentially infectious nonself (Dodds and Rathjen, 2010). Recognition of PAMPs by corresponding surface-localized plant pattern rec- ognition receptors (PRRs) leads to PAMP-triggered immunity (PTI), which is sufficient to provide broad- spectrum disease resistance to most microbes. In the plant model Arabidopsis (Arabidopsis thaliana), the best- studied PRRs are the leucine-rich repeat receptor kinases (LRR-RKs) FLAGELLIN-SENSING2 (FLS2) and ELONGATION FACTOR TU RECEPTOR (EFR) that recognize the bacterial PAMPs flagellin (or its peptide surrogate flg22) and elongation factor Tu (or its peptide surrogates elf18 or elf26, respectively; Monaghan and Zipfel, 2012). Immediately after binding to their respective ligands, FLS2 and EFR heteromerize with the regulatory LRR-RK BRI1- ASSOCIATED KINASE1/SOMATIC-EMBRYOGENESIS RECEPTOR KINASE3 (BAK1/SERK3) as well as addi- tional members of the SERK subfamily of LRR-RKs (Chinchilla et al., 2007; Heese et al., 2007; Roux et al., 2011; Sun et al., 2013). The receptor-like cytoplasmic kinase BOTRYTIS-INDUCED KINASE1 (BIK1) is a direct sub- strate of FLS2, EFR, and BAK1 that is required for a 1 This work was supported by the Gatsby Charitable Foundation (to C.Z.), by the United Kingdom Biotechnology and Biological Sci- ences Research Council (grant no. BB/E024874/1 ERA-PG [RLPRLKs] and grant no. BB/G024944/1 ERA-PG [Pathonet] to C.Z.), by the National Research Foundation of Korea (grant no. NRF.–2011–220–C00059 to S.-K.K.), and by the John Innes Centre and the Sainsbury Laboratory rotation program (to B.S.). 2 Present address: Danish National Research Foundation Center DynaMo, Department of Plant and Environmental Sciences, Univer- sity of Copenhagen, 1871 Frederiksberg, Denmark. 3 Present address: Agence National de la Recherche, 75012 Paris, France. 4 Present address: Department of Plant Pathology, College of Agricultural and Environmental Sciences, University of California, Davis, CA 95616. * Address correspondence to cyril.zipfel@tsl.ac.uk. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy de- scribed in the Instructions for Authors (www.plantphysiol.org) is: Cyril Zipfel (cyril.zipfel@tsl.ac.uk). [W] The online version of this article contains Web-only data. [OPEN] Articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.113.234625 Plant Physiology Ò , March 2014, Vol. 164, pp. 1443–1455, www.plantphysiol.org Ó 2014 American Society of Plant Biologists. All Rights Reserved. 1443 www.plant.org on July 1, 2014 - Published by www.plantphysiol.org Downloaded from Copyright © 2014 American Society of Plant Biologists. All rights reserved.