Like all organisms, plants must perform a careful balancing act with their resources. Investing in the growth of new roots or leaves can allow a plant to better exploit its environment—but it must not be at the expense of leaving the plant vulnerable to attack by pests and pathogens. As such, there is an obvious trade-off between allocating resources to growth or defense against disease. This trade-off must be finely balanced, and must also be responsive to different cues in the environment that would favor either growth or defense.

The plant’s immune system is able to detect invading microbes, and trigger a defensive response against them. At the surface of plant cells, proteins called pattern recognition receptors are able to recognize specific molecules that are the tell-tale signs of microbes and pathogens—such as the proteins in the molecular tails that bacteria use to move around.

For many pattern recognition receptors, signaling that they have recognized a potential invading microbe requires the actions of a co-receptor called BAK1. Interestingly, BAK1 also interacts with the receptor that identifies brassinosteroids—hormones that stimulate plant growth. Since growth and a functioning immune system are both reliant on BAK1, it was hypothesized that competition for this co-receptor could have a role in the trade-off between the two processes in plants. However, this explanation was controversial and the mechanisms underlying the trade-off still required clarification.

Now, Lozano-Durán et al. have debunked the idea that competition for BAK1 is directly responsible for the trade-off between growth and immunity. By examining how BAK1 interacts with immune receptors in the plant model species Arabidopsis thaliana, the trade-off was actually shown to be independent of BAK1. Instead, it was discovered that activation of a protein, called BZR1, reprogramed gene expression to ‘switch off’ immune signaling in response to brassinosteroids.

Lozano-Durán et al. also show that BZR1 allows the balance of the trade-off between growth and immunity to be shifted in response to cues from the environment. The suppression of the immune system by BZR1 was particularly pronounced when the conditions required fast plant growth—for example, when they mimicked the conditions experienced by seedlings before they emerge from the soil, and must grow swiftly to reach the light before they starve.

The trade-off between plant growth and immunity needs to be finely regulated to ensure proper allocation of resources in an efficient and timely manner upon effective integration of environmental cues (Pieterse et al., 2012). A key aspect of plant immunity is the perception of pathogen-associated molecular patterns (PAMPs) by surface-localized pattern-recognition receptors (PRRs), leading to PAMP-triggered immunity (PTI) (Dodds and Rathjen, 2010). PRRs of the leucine-rich repeat receptor kinases (LRR-RKs) class rely on the regulatory LRR-RK BAK1 (BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1) for signaling (Monaghan and Zipfel, 2012); that is the case of FLS2 (FLAGELLIN SENSITIVE 2) and EFR (EF-TU RECEPTOR), which perceive bacterial flagellin (or the active peptide flg22) and EF-Tu (or the active peptide elf18) respectively. BAK1 also interacts with the LRR-RK BRI1 (BRASSINOSTEROID INSENSITIVE 1), the main receptor for the growth-promoting steroid hormones brassinosteroids (BR), and is a positive regulator of BR-mediated growth (Kim and Wang, 2010). Hence, a crosstalk between the BR- and PAMP-triggered signaling pathways resulting from competition for BAK1 was hypothesized. While a unidirectional antagonism between BR and PTI signaling has been recently described in Arabidopsis (Albrecht et al., 2012; Belkhadir et al., 2012), the exact underlying mechanisms are still controversial. Activation of the BR signaling pathway via either transgenic overexpression of BRI1 or the BR biosynthetic gene DWF4 or expression of the activated BRI1 allele BRI1^sud suppresses PTI outputs (Belkhadir et al., 2012). One such output, the PAMP-triggered callose deposition, could be restored by over-expression of BAK1-HA, suggesting that BAK1 is a limiting factor (Belkhadir et al., 2012). However, exogenous BR treatment of wild-type plants does not affect the FLS2-BAK1 complex formation upon FLS2 activation, while it results in decreased PTI responses (Albrecht et al., 2012).

In order to clarify the role of BAK1 in the BR-PTI crosstalk, we investigated FLS2-BAK1 complex formation in the transgenic Arabidopsis lines overexpressing BRI1 or DWF4 or expressing BRI1^sud (Belkhadir et al., 2012). Upon treatment with flg22, FLS2 associated normally with BAK1 in these transgenic plants, and neither FLS2 nor BAK1 accumulation was altered (Figure 1—figure supplement 1A). Moreover, these plants displayed a weaker reactive oxygen species (ROS) burst in response to chitin (Figure 1—figure supplement 1B), whose signaling pathway is BAK1-independent (Shan et al., 2008; Ranf et al., 2011). This result is consistent with the previous finding that exogenous BR treatment can also inhibit the chitin-induced ROS burst (Albrecht et al., 2012). BAK1-HA is not fully functional in BR signaling and exerts a dominant-negative effect on the endogenous BAK1 (Figure 1—figure supplement 1C), which may explain that introduction of the BAK1-HA transgene can override the suppression of immunity triggered by overexpression of BRI1 (Belkhadir et al., 2012); BAK1-HA does not exert such a dominant negative effect, however, on PTI signaling (Figure 1—figure supplement 1D). Taken together, these results indicate that the BR-mediated suppression of PTI is triggered independently of a competition between BRI1 and PRRs for BAK1.

We sought to determine at which level of the BR signaling pathway the antagonism initiates. After BR perception by BRI1 and activation of the BRI1-BAK1 complex, the BR signal transduction cascade includes inactivation of BIN2 (BR INSENSITIVE 2) and BIN2-like kinases, a family of GSK3-like kinases acting as negative regulators of the pathway (Vert and Chory, 2006). This leads to dephosphorylation of BZR1 (BRASSINAZOLE RESISTANT 1) and BES1/BZR2 (BRI1-EMS-SUPPRESSOR 1/BRASSINAZOLE RESISTANT 2), two bHLH transcription factors acting as major regulators of BR-induced transcriptional changes, which then become active (Wang et al., 2002; Yin et al., 2002). Treatment with the chemicals LiCl and bikinin, which inhibit GSK3-like kinases (De Rybel et al., 2009; Yan et al., 2009), resulted in impaired flg22-triggered ROS burst (Figure 1A,B), as observed upon genetic or ligand-induced activation of the BR pathway. Furthermore, a triple mutant in BIN2 and the two closest related GSK3-like kinases, BIL1 (BIN2-LIKE 1) and BIL2 (triple GSK3 mutant; Vert and Chory, 2006), shows a similar impairment in response to either flg22 or chitin (Figure 1C). Interestingly, in spite of regulating MAPKs involved in stomata development (Kim et al., 2012; Khan et al., 2013), neither BR treatment nor loss of function of BIN2 affect flg22-triggered MAPK activation (Figure 1—figure supplement 2), contrary to what has been recently suggested (Choudhary et al., 2012; Zhu et al., 2013). These results indicate that the BR-PTI crosstalk occurs downstream of BIN2.

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Transgenic expression of two different constitutively active versions of BZR1, BZR1Δ (Gampala et al., 2007) and BZR1^S173A (Ryu et al., 2007), results in impaired flg22- or chitin-triggered ROS burst (Figure 1D, Figure 1—figure supplement 3A). Consistent with previous results (Albrecht et al., 2012; Figure 1—figure supplements 1A and 2), plants expressing BZR1Δ or BZR1^S173A display normal FLS2-BAK1 complex formation and MAPK activation upon flg22 treatment (Figure 2A,B, Figure 2—figure supplement 1A,B), but are impaired in PAMP-triggered marker gene expression, seedling growth inhibition (SGI) (Figure 2C–E) and induced resistance to P. syringae pv. tomato (Pto) DC3000 (Figure 2F, Figure 2—figure supplement 1C), and are more susceptible to the non-host strain Pseudomonas syringae pv. cilantro (Pci) 0788-9 (Lewis et al., 2010) (Figure 2G). Notably, transgenic expression of a constitutively active form of BES1, BES1^S171A (Gampala et al., 2007), does not impact the flg22-triggered ROS burst (Figure 1—figure supplement 3B). We then tested if activation of BZR1 is sufficient to inhibit PTI signaling. Induction of BR signaling by bikinin treatment still represses elf18-induced ROS burst in the BRI1 mutant bri1-5 (we used elf18 in this experiment because bri1-5 is in the Ws-2 background, which is a natural fls2 mutant) (Figure 1—figure supplement 3C). bri1-5/BZR1Δ plants (Gampala et al., 2007) still exhibited reduced PAMP-triggered ROS burst (Figure 1E), and treatment with the BR biosynthetic inhibitor brassinazole (BRZ) did not affect the BZR1Δ effect (Figure 1—figure supplement 3D). Interestingly, BRZ treatment of wild-type Col-0 plants results in increased ROS production (Figure 1—figure supplement 3D), which is consistent with the fact that BR inhibits PTI responses and suggests that endogenous concentrations of the hormone exert this effect. These results demonstrate that activation of BZR1 affects PTI signaling independently of BR perception or synthesis.

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To understand how BZR1 mediates the BR-PTI crosstalk, we performed meta-analysis of microarray and ChIP-chip data containing BR-regulated and BZR1 or BES1 target genes (Sun et al., 2010; Yu et al., 2011). Functional enrichment of BR-regulated genes unveiled a statistically significant over-representation of defense-related GO terms of the Biological Process ontology (Table 1), indicating that BR signaling regulates the expression of defense-related genes. Independent analysis of BR-regulated BZR1 or BES1 targets confirmed BZR1 as the main transcription factor involved in the regulation of defense gene expression (Table 1). Two out of four over-represented GO terms of the Molecular Function ontology among the BR-regulated BZR1 targets are transcription factor and transcription repressor activity (Table 2). Interestingly, several defense-related GO terms are also over-represented in the subset of BR-regulated BZR1-targeted transcription factors (Table 3), pointing at a BZR1-mediated secondary transcriptional wave of defense-related genes.

To identify BZR1-regulated transcription factors with a prominent role in defense, we performed promoter enrichment analysis on the subset of defense-related BR-regulated genes, and found the W-box motif as the only significantly over-represented motif (Table 4). The W-box motif is the binding site for the WRKY family of transcription factors (Rushton et al., 2010), and several members of this family are BR-regulated BZR1-targets (Table 5). We hypothesized that WRKYs that are BR-induced and BZR1 targets may be involved in PTI signaling. Notably, wrky11, wrky15, wrky18 and wrky70 mutants displayed enhanced PAMP-triggered ROS (Figure 3A), suggesting that these transcription factors act as negative regulators of early PTI signaling. This is in accordance with their role as negative regulators of immunity (Figure 3—figure supplement 1A; Journot-Catalino et al., 2006). Therefore, the BZR1-mediated inhibition of PTI might be partially explained by the up-regulation of genes encoding WRKY transcription factors that negatively control the expression of genes involved in early PTI signaling.

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One of the WRKY genes targeted by BZR1 is WRKY40 (Sun et al., 2010). Interestingly, all described targets of WRKY40 (Pandey et al., 2010) are also targets of BZR1 (Sun et al., 2010) (Table 6). The over-representation of the W-box motif among BZR1 targets (Table 7) suggests that BZR1 may interact with WRKY transcription factors (such as WRKY40) to cooperatively regulate transcription. WRKY40 has been described as a negative regulator of defense against biotrophic pathogens and insects (Xu et al., 2006; Pandey et al., 2010; Brotman et al., 2013; Schon et al., 2013; Schweizer et al., 2013). In agreement with this, we found that a null wrky40 mutant is more resistant to Pto DC3000 (Figure 3—figure supplement 1B). Strikingly, wrky40 plants are partially impaired in the BR-mediated suppression of PAMP-triggered ROS (Figure 3B), suggesting that WRKY40 may act coordinately with BZR1 to suppress immunity. Indeed, we found that BZR1 associates with WRKY40, but not WRKY6, in co-immunoprecipitation experiments when transiently co-expressed in Nicotiana benthamiana leaves (Figure 3C) or Arabidopsis protoplasts (Figure 3D). Collectively, these results indicate that BZR1 and WRKY40 form a protein complex that may participate in the transcriptional inhibition of PTI signaling.

BZR1, together with DELLAs and PIF4, is part of a core transcription module that integrates hormonal (gibberellin [GA] and BR) and environmental (light) signals (Gallego-Bartolome et al., 2012; Li et al., 2012; Oh et al., 2012; Bai et al., 2012b). In the dark, BZR1 is activated by endogenous BR and GA to promote growth, partially through the synergistic interaction with PIF4 (Jaillais and Vert, 2012). Because etiolation requires rapid growth, we hypothesized that plants may prioritize growth over immunity in dark conditions. In fact, we found that PAMP-triggered SGI was partially impaired in dark-grown seedlings (Figure 4A–D). This impairment was abolished in the BR-insensitive mutants bri1-301 and bin2-1 (Figure 4A, Figure 4—figure supplement 2A), indicating that BR signaling is responsible for the dark-induced suppression of this PTI response. Activation of BZR1 in the BZR1Δ line mimicked the dark-induced suppression of SGI in both light and dark (Figure 4B). However, activation of BES1 in the BES1^S171A line did not impact SGI (Figure 4—figure supplement 3A). Consistent with the previous results, exogenous BR treatment suppressed SGI in both light and dark (Figure 4C, Figure 4—figure supplement 2B,C). While treatment with GA alone did not have a dramatic effect on SGI, co-treatment with BL and GA resulted in an enhancement of the BR-mediated suppression of SGI (Figure 4C, Figure 4—figure supplement 2B), indicating an additive effect of these two hormones when applied together. Moreover, treatment with the GA synthesis inhibitors paclobutrazol (PAC) or uniconazole (Uni) abolished the effect of BL on SGI (Figure 4—figure supplement 1A,B and Figure 4—figure supplement 2B,C), and this effect was reduced in the GA biosynthetic mutant ga1-3 (Figure 4—figure supplement 1C). Taken together, these results demonstrate that BR suppress at least one PTI output, SGI, in the dark in a GA-dependent manner, most likely through activation of BZR1. Notably, although the wrky40 mutant undergoes etiolation normally (Figure 4—figure supplement 2D), it shows a diminished suppression of SGI in the dark (Figure 4D, Figure 4—figure supplement 2D), supporting the idea that WRKY40 is required for the BZR1-mediated inhibition of PTI.

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Previously, a unidirectional negative crosstalk between the growth-promoting hormone BR and PTI had been described (Albrecht et al., 2012; Belkhadir et al., 2012). In this work, we show that activation of one of two major BR-activated transcription factors, BZR1, is sufficient to suppress PTI, measured as PAMP-triggered ROS production, PAMP-triggered gene expression, SGI or induced resistance (Figures 1 and 2, Figure 1—figure supplement 3, Figure 2—figure supplement 1). Of note, another PTI output, MAPK activation, is not affected by activation of the BR pathway (Figure 2B, Figure 1—figure supplement 2, Figure 2—figure supplement 1B). BR treatment results in BZR1-dependent changes in the expression of defense-related genes, among which several members of the WRKY family of transcription factors can be found. Because the promoters of BR-regulated defense-related genes are enriched in the W-box motif (Table 4), BZR1-targeted WRKY transcription factors could be responsible for a secondary wave of transcription, ultimately leading to the suppression of PTI. In agreement with this idea, a subset of WRKYs induced by BR (WRKY11, WRKY15 and WRKY18) (Figure 3A) act as negative regulators of PAMP-triggered ROS, potentially by controlling the steady-state expression of genes encoding components required for this response. The over-representation of the W-box motif among the BZR1 targets (Table 7) raises the possibility that, additionally, WRKY transcription factors could also act together with BZR1 to cooperatively regulate gene expression. We found that WRKY40 associates with BZR1 directly or indirectly in planta (Figure 3C,D); in the absence of WRKY40, the BR-mediated suppression of PAMP-triggered ROS burst is partially impaired (Figure 3B). Therefore, WRKYs may play a dual role in the BZR1-mediated suppression of defense, as both co- and secondary regulators of defense gene expression. Given that the loss of BR-mediated suppression of PAMP-triggered ROS burst in the wrky40 mutant is only partial, BZR1 may interact with other members of the WRKY family, such as WRKY18 or WRKY60, to repress immunity.

Furthermore, we recently described that the bHLH transcription factor HBI1, which is a BRZ1 target (Sun et al., 2010; Bai et al., 2012a), negatively regulates PTI (Malinovsky et al., under revision). All together, these results illustrate that BZR1 controls the expression of transcription factors (e.g. WRKY11, WRKY15, WRKY18 and HBI1), which themselves might control the expression of PTI components (see model in Figure 4E) whose identities remain to be identified.

Plants need to finely regulate allocation of resources upon integration of environmental cues, both biotic and abiotic, in order to rapidly and readily adapt to changing conditions and ensure survival in a cost-efficient manner. Dark conditions impose an energetic limitation due to lack of photo-assimilates; in this situation, the restoration of normal photosynthesis by reaching light is an essential requirement to guarantee perpetuation, and as such must be given priority (Casal, 2013). We hypothesize that when plants face conditions that require rapid growth, such as when germinating in soil or when under a canopy, limited resources are invested in this developmental process at the expense of immunity in what must be a quantitative choice. Indeed, we show that etiolated seedlings do not arrest their growth in response to PAMPs as light-grown seedlings do, as measured by total fresh weight (Figure 4A–D). In addition, BR signaling, acting cooperatively with GA signaling, is required for the dark-induced suppression of this PTI response (Figure 4C, Figure 4—figure supplement 1), and activation of BZR1 is sufficient to exert this effect regardless of light conditions (Figure 4B). Although seedlings were used in these experiments due to technical reasons, BR also regulate growth at later developmental stages, so this phenomenon may be more general. Based on these findings, we propose a model in which BZR1 regulates the expression of defense genes, assisted by WRKY40 (and potentially other WRKYs), ultimately resulting in a quantitative suppression of immunity (Figure 4E). Because the activation status of BZR1 depends on BR, GA and light signaling, BZR1 would act as a molecular integrator of these inputs to effectively regulate the trade-off between growth and immunity.

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Author details

1. Rosa Lozano-Durán

   The Sainsbury Laboratory, Norwich, United Kingdom

   Contribution

   RL-D, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

2. Alberto P Macho

   The Sainsbury Laboratory, Norwich, United Kingdom

   Contribution

   APM, Conception and design, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

3. Freddy Boutrot

   The Sainsbury Laboratory, Norwich, United Kingdom

   Contribution

   FB, Conception and design, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

4. Cécile Segonzac

   The Sainsbury Laboratory, Norwich, United Kingdom

   Present address

   Institute of Agriculture and Environment, Massey University Manawatu, Palmerston North, New Zealand

   Contribution

   CS, Conception and design, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

5. Imre E Somssich

   Max Planck Institute for Plant Breeding Research, Köln, Germany

   Contribution

   IES, Conception and design, Drafting or revising the article, Contributed unpublished essential data or reagents

   Competing interests

   The authors declare that no competing interests exist.

6. Cyril Zipfel

   The Sainsbury Laboratory, Norwich, United Kingdom

   Contribution

   CZ, Conception and design, Analysis and interpretation of data, Drafting or revising the article

   For correspondence

   cyril.zipfel@tsl.ac.uk

   Competing interests

   The authors declare that no competing interests exist.

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