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.

1. 1. Albrecht C
   2. Boutrot F
   3. Segonzac C
   4. Schwessinger B
   5. Gimenez-Ibanez S
   6. Chinchilla D
   7. Rathjen JP
   8. de Vries SC
   9. Zipfel C

   (2012) Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1

   Proceedings of the National Academy of Sciences of the United States of America 109:303–308.

   https://doi.org/10.1073/pnas.1109921108

   • Google Scholar
2. 1. Alonso JM
   2. Stepanova AN
   3. Leisse TJ
   4. Kim CJ
   5. Chen H
   6. Shinn P
   7. Stevenson DK
   8. Zimmerman J
   9. Barajas P
   10. Cheuk R
   11. Gadrinab C
   12. Heller C
   13. Jeske A
   14. Koesema E
   15. Meyers CC
   16. Parker H
   17. Prednis L
   18. Ansari Y
   19. Choy N
   20. Deen H
   21. Geralt M
   22. Hazari N
   23. Hom E
   24. Karnes M
   25. Mulholland C
   26. Ndubaku R
   27. Schmidt I
   28. Guzman P
   29. Aguilar-Henonin L
   30. Schmid M
   31. Weigel D
   32. Carter DE
   33. Marchand T
   34. Risseeuw E
   35. Brogden D
   36. Zeko A
   37. Crosby WL
   38. Berry CC
   39. Ecker JR

   (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana

   Science 301:653–657.

   https://doi.org/10.1126/science.1086391

   • Google Scholar
3. 1. Bai MY
   2. Fan M
   3. Oh E
   4. Wang ZY

   (2012a) A triple helix-loop-helix/basic helix-loop-helix cascade controls cell elongation downstream of multiple hormonal and environmental signaling pathways in Arabidopsis

   Plant Cell 24:4917–4929.

   https://doi.org/10.1105/tpc.112.105163

   • Google Scholar
4. 1. Bai MY
   2. Shang JX
   3. Oh E
   4. Fan M
   5. Bai Y
   6. Zentella R
   7. Sun TP
   8. Wang ZY

   (2012b) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis

   Nature Cell Biology 14:810–817.

   https://doi.org/10.1038/ncb2546

   • Google Scholar
5. 1. Belkhadir Y
   2. Jaillais Y
   3. Epple P
   4. Balsemao-Pires E
   5. Dangl JL
   6. Chory J

   (2012) Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns

   Proceedings of the National Academy of Sciences of the United States of America 109:297–302.

   https://doi.org/10.1073/pnas.1112840108

   • Google Scholar
6. 1. Boudsocq M
   2. Willmann MR
   3. McCormack M
   4. Lee H
   5. Shan L
   6. He P
   7. Bush J
   8. Cheng SH
   9. Sheen J

   (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases

   Nature 464:418–422.

   https://doi.org/10.1038/nature08794

   • Google Scholar
7. 1. Brotman Y
   2. Landau U
   3. Cuadros-Inostroza A
   4. Tohge T
   5. Fernie AR
   6. Chet I
   7. Viterbo A
   8. Willmitzer L

   (2013) Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance

   PLOS Pathogens 9:e1003221.

   https://doi.org/10.1371/journal.ppat.1003221

   • Google Scholar
8. 1. Casal JJ

   (2013) Photoreceptor signaling networks in plant responses to shade

   Annual Review of Plant Biology 64:403–427.

   https://doi.org/10.1146/annurev-arplant-050312-120221

   • Google Scholar
9. 1. Choudhary SP
   2. Yu JQ
   3. Yamaguchi-Shinozaki K
   4. Shinozaki K
   5. Tran LS

   (2012) Benefits of brassinosteroid crosstalk

   Trends in Plant Science 17:594–605.

   https://doi.org/10.1016/j.tplants.2012.05.012

   • Google Scholar
10. 1. De Rybel B
    2. Audenaert D
    3. Vert G
    4. Rozhon W
    5. Mayerhofer J
    6. Peelman F
    7. Coutuer S
    8. Denayer T
    9. Jansen L
    10. Nguyen L
    11. Vanhoutte I
    12. Beemster GT
    13. Vleminckx K
    14. Jonak C
    15. Chory J
    16. Inzé D
    17. Russinova E
    18. Beeckman T

    (2009) Chemical inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates brassinosteroid signaling

    Chemical Biology 16:594–604.

    https://doi.org/10.1016/j.chembiol.2009.04.008

    • Google Scholar
11. 1. Dodds PN
    2. Rathjen JP

    (2010) Plant immunity: towards an integrated view of plant-pathogen interactions

    Nature Reviews Genetics 11:539–548.

    https://doi.org/10.1038/nrg2812

    • Google Scholar
12. 1. Gallego-Bartolome J
    2. Minguet EG
    3. Grau-Enguix F
    4. Abbas M
    5. Locascio A
    6. Thomas SG
    7. Alabadi D
    8. Blazquez MA

    (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis

    Proceedings of the National Academy of Sciences of the United States of America 109:13446–13451.

    https://doi.org/10.1073/pnas.1119992109

    • Google Scholar
13. 1. Gampala SS
    2. Kim TW
    3. He JX
    4. Tang W
    5. Deng Z
    6. Bai MY
    7. Guan S
    8. Lalonde S
    9. Sun Y
    10. Gendron JM
    11. Chen H
    12. Shibagaki N
    13. Ferl RJ
    14. Ehrhardt D
    15. Chong K
    16. Burlingame AL
    17. Wang ZY

    (2007) An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis

    Developmental Cell 13:177–189.

    https://doi.org/10.1016/j.devcel.2007.06.009

    • Google Scholar
14. 1. Grefen C
    2. Donald N
    3. Hashimoto K
    4. Kudla J
    5. Schumacher K
    6. Blatt MR

    (2010) A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies

    Plant Journal 64:355–365.

    https://doi.org/10.1111/j.1365-313X.2010.04322.x

    • Google Scholar
15. 1. Jaillais Y
    2. Vert G

    (2012) Brassinosteroids, gibberellins and light-mediated signalling are the three-way controls of plant sprouting

    Nature Cell Biology 14:788–790.

    https://doi.org/10.1038/ncb2551

    • Google Scholar
16. 1. Journot-Catalino N
    2. Somssich IE
    3. Roby D
    4. Kroj T

    (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana

    Plant Cell 18:3289–3302.

    https://doi.org/10.1105/tpc.106.044149

    • Google Scholar
17. 1. Katari MS
    2. Nowicki SD
    3. Aceituno FF
    4. Nero D
    5. Kelfer J
    6. Thompson LP
    7. Cabello JM
    8. Davidson RS
    9. Goldberg AP
    10. Shasha DE
    11. Coruzzi GM
    12. Gutiérrez RA

    (2010) VirtualPlant: a software platform to support systems biology research

    Plant Physiology 152:500–515.

    https://doi.org/10.1104/pp.109.147025

    • Google Scholar
18. 1. Khan M
    2. Rozhon W
    3. Bigeard J
    4. Pflieger D
    5. Husar S
    6. Pitzschke A
    7. Teige M
    8. Jonak C
    9. Hirt H
    10. Poppenberger B

    (2013) Brassinosteroid-regulated GSK3/Shaggy-like kinases phosphorylate mitogen-activated protein (MAP) kinase kinases, which control stomata development in Arabidopsis thaliana

    The Journal of Biological Chemistry 288:7519–7527.

    https://doi.org/10.1074/jbc.M112.384453

    • Google Scholar
19. 1. Kim TW
    2. Michniewicz M
    3. Bergmann DC
    4. Wang ZY

    (2012) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway

    Nature 482:419–422.

    https://doi.org/10.1038/nature10794

    • Google Scholar
20. 1. Kim TW
    2. Wang ZY

    (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors

    Annual Review of Plant Biology 61:681–704.

    https://doi.org/10.1146/annurev.arplant.043008.092057

    • Google Scholar
21. 1. Lewis JD
    2. Wu R
    3. Guttman DS
    4. Desveaux D

    (2010) Allele-specific virulence attenuation of the Pseudomonas syringae HopZ1a type III effector via the Arabidopsis ZAR1 resistance protein

    PLOS Genetics 6:e1000894.

    https://doi.org/10.1371/journal.pgen.1000894

    • Google Scholar
22. 1. Li QF
    2. Wang C
    3. Jiang L
    4. Li S
    5. Sun SS
    6. He JX

    (2012) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis

    Science Signaling 5:ra72.

    https://doi.org/10.1126/scisignal.2002908

    • Google Scholar
23. 1. Monaghan J
    2. Zipfel C

    (2012) Plant pattern recognition receptor complexes at the plasma membrane

    Current Opinion in Plant Biology 15:349–357.

    https://doi.org/10.1016/j.pbi.2012.05.006

    • Google Scholar
24. 1. Mukhtar MS
    2. Deslandes L
    3. Auriac MC
    4. Marco Y
    5. Somssich IE

    (2008) The Arabidopsis transcription factor WRKY27 influences wilt disease symptom development caused by Ralstonia solanacearum

    Plant Journal 56:935–947.

    https://doi.org/10.1111/j.1365-313X.2008.03651.x

    • Google Scholar
25. 1. Nakagawa T
    2. Suzuki T
    3. Murata S
    4. Nakamura S
    5. Hino T
    6. Maeo K
    7. Tabata R
    8. Kawai T
    9. Tanaka K
    10. Niwa Y
    11. Watanabe Y
    12. Nakamura K
    13. Kimura T
    14. Ishiguro S

    (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants

    Bioscience Biotechnology and Biochemistry 71:2095–2100.

    https://doi.org/10.1271/bbb.70216

    • Google Scholar
26. 1. Navarro L
    2. Bari R
    3. Achard P
    4. Lison P
    5. Nemri A
    6. Harberd NP
    7. Jones JD

    (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling

    Current Biology 18:650–655.

    https://doi.org/10.1016/j.cub.2008.03.060

    • Google Scholar
27. 1. Nekrasov V
    2. Li J
    3. Batoux M
    4. Roux M
    5. Chu ZH
    6. Lacombe S
    7. Rougon A
    8. Bittel P
    9. Kiss-Papp M
    10. Chinchilla D
    11. van Esse HP
    12. Jorda L
    13. Schwessinger B
    14. Nicaise V
    15. Thomma BP
    16. Molina A
    17. Jones JD
    18. Zipfel C

    (2009) Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity

    The EMBO Journal 28:3428–3438.

    https://doi.org/10.1038/emboj.2009.262

    • Google Scholar
28. 1. Noguchi T
    2. Fujioka S
    3. Choe S
    4. Takatsuto S
    5. Yoshida S
    6. Yuan H
    7. Feldmann KA
    8. Tax FE

    (1999) Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids

    Plant Physiology 121:743–752.

    https://doi.org/10.1104/pp.121.3.743

    • Google Scholar
29. 1. O’Connor TR
    2. Dyreson C
    3. Wyrick JJ

    (2005) Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences

    Bioinformatics 21:4411–4413.

    https://doi.org/10.1093/bioinformatics/bti714

    • Google Scholar
30. 1. Oh E
    2. Zhu JY
    3. Wang ZY

    (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses

    Nature Cell Biology 14:802–809.

    https://doi.org/10.1038/ncb2545

    • Google Scholar
31. 1. Onate-Sanchez L
    2. Vicente-Carbajosa J

    (2008) DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques

    BMC Research Notes 1:93.

    https://doi.org/10.1186/1756-0500-1-93

    • Google Scholar
32. 1. Pandey SP
    2. Roccaro M
    3. Schon M
    4. Logemann E
    5. Somssich IE

    (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis

    Plant Journal 64:912–923.

    https://doi.org/10.1111/j.1365-313X.2010.04387.x

    • Google Scholar
33. 1. Peng P
    2. Yan Z
    3. Zhu Y
    4. Li J

    (2008) Regulation of the Arabidopsis GSK3-like kinase BRASSINOSTEROID-INSENSITIVE 2 through proteasome-mediated protein degradation

    Molecular Plant 1:338–346.

    https://doi.org/10.1093/mp/ssn001

    • Google Scholar
34. 1. Pieterse CM
    2. Van der Does D
    3. Zamioudis C
    4. Leon-Reyes A
    5. Van Wees SC

    (2012) Hormonal modulation of plant immunity

    Annu Review of Cell and Developmental Biology 28:489–521.

    https://doi.org/10.1146/annurev-cellbio-092910-154055

    • Google Scholar
35. 1. Ranf S
    2. Eschen-Lippold L
    3. Pecher P
    4. Lee J
    5. Scheel D

    (2011) Interplay between calcium signalling and early signalling elements during defense responses to microbe- or damage-associated molecular patterns

    Plant Journal 68:100–113.

    https://doi.org/10.1111/j.1365-313X.2011.04671.x

    • Google Scholar
36. 1. Rushton PJ
    2. Somssich IE
    3. Ringler P
    4. Shen QJ

    (2010) WRKY transcription factors

    Trends in Plant Science 15:247–258.

    https://doi.org/10.1016/j.tplants.2010.02.006

    • Google Scholar
37. 1. Ryu H
    2. Kim K
    3. Cho H
    4. Park J
    5. Choe S
    6. Hwang I

    (2007) Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling

    Plant Cell 19:2749–2762.

    https://doi.org/10.1105/tpc.107.053728

    • Google Scholar
38. 1. Schon M
    2. Toller A
    3. Diezel C
    4. Roth C
    5. Westphal L
    6. Wiermer M
    7. Somssich IE

    (2013) Analyses of wrky18 wrky40 plants reveal critical roles of SA/EDS1 signaling and indole-glucosinolate biosynthesis for Golovinomyces orontii resistance and a loss-of resistance towards Pseudomonas syringae pv. tomato AvrRPS4

    Molecular Plant-Microbe Interactions 26:758–767.

    https://doi.org/10.1094/MPMI-11-12-0265-R

    • Google Scholar
39. 1. Schweizer F
    2. Bodenhausen N
    3. Lassueur S
    4. Masclaux FG
    5. Reymond P

    (2013) Differential contribution of transcription factors to Arabidopsis thaliana defense against Spodoptera littoralis

    Frontiers of Plant Science 4:13.

    https://doi.org/10.3389/fpls.2013.00013

    • Google Scholar
40. 1. Schwessinger B
    2. Roux M
    3. Kadota Y
    4. Ntoukakis V
    5. Sklenar J
    6. Jones A
    7. Zipfel C

    (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1

    PLOS Genetics 7:e1002046.

    https://doi.org/10.1371/journal.pgen.1002046

    • Google Scholar
41. 1. Shan L
    2. He P
    3. Li J
    4. Heese A
    5. Peck SC
    6. Nurnberger T
    7. Martin GB
    8. Sheen J

    (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity

    Cell Host & Microbe 4:17–27.

    https://doi.org/10.1016/j.chom.2008.05.017

    • Google Scholar
42. 1. Sun Y
    2. Fan XY
    3. Cao DM
    4. Tang W
    5. He K
    6. Zhu JY
    7. He JX
    8. Bai MY
    9. Zhu S
    10. Oh E
    11. Patil S
    12. Kim TW
    13. Ji H
    14. Wong WH
    15. Rhee SY
    16. Wang ZY

    (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis

    Developmental Cell 19:765–777.

    https://doi.org/10.1016/j.devcel.2010.10.010

    • Google Scholar
43. 1. Toufighi K
    2. Brady SM
    3. Austin R
    4. Ly E
    5. Provart NJ

    (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses

    Plant Journal 43:153–163.

    https://doi.org/10.1111/j.1365-313X.2005.02437.x

    • Google Scholar
44. 1. Vert G
    2. Chory J

    (2006) Downstream nuclear events in brassinosteroid signalling

    Nature 441:96–100.

    https://doi.org/10.1038/nature04681

    • Google Scholar
45. 1. Wang D
    2. Amornsiripanitch N
    3. Dong X

    (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants

    PLOS Pathogens 2:e123.

    https://doi.org/10.1371/journal.ppat.0020123

    • Google Scholar
46. 1. Wang ZY
    2. Nakano T
    3. Gendron J
    4. He J
    5. Chen M
    6. Vafeados D
    7. Yang Y
    8. Fujioka S
    9. Yoshida S
    10. Asami T
    11. Chory J

    (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis

    Developmental Cell 2:505–513.

    https://doi.org/10.1016/S1534-5807(02)00153-3

    • Google Scholar
47. 1. Wisman E
    2. Cardon GH
    3. Fransz P
    4. Saedler H

    (1998a) The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis

    Plant Molecular Biology 37:989–999.

    https://doi.org/10.1023/A:1006082009151

    • Google Scholar
48. 1. Wisman E
    2. Hartmann U
    3. Sagasser M
    4. Baumann E
    5. Palme K
    6. Hahlbrock K
    7. Saedler H
    8. Weisshaar B

    (1998b) Knock-out mutants from an En-1 mutagenized Arabidopsis thaliana population generate phenylpropanoid biosynthesis phenotypes

    Proceedings of the National Academy of Sciences of the United States of America 95:12432–12437.

    https://doi.org/10.1073/pnas.95.21.12432

    • Google Scholar
49. 1. Xu W
    2. Huang J
    3. Li B
    4. Li J
    5. Wang Y

    (2008) Is kinase activity essential for biological functions of BRI1?

    Cell research 18:472–478.

    https://doi.org/10.1038/cr.2008.36

    • Google Scholar
50. 1. Xu X
    2. Chen C
    3. Fan B
    4. Chen Z

    (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors

    Plant Cell 18:1310–1326.

    https://doi.org/10.1105/tpc.105.037523

    • Google Scholar
51. 1. Yan Z
    2. Zhao J
    3. Peng P
    4. Chihara RK
    5. Li J

    (2009) BIN2 functions redundantly with other Arabidopsis GSK3-like kinases to regulate brassinosteroid signaling

    Plant Physiology 150:710–721.

    https://doi.org/10.1104/pp.109.138099

    • Google Scholar
52. 1. Yin Y
    2. Wang ZY
    3. Mora-Garcia S
    4. Li J
    5. Yoshida S
    6. Asami T
    7. Chory J

    (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation

    Cell 109:181–191.

    https://doi.org/10.1016/S0092-8674(02)00721-3

    • Google Scholar
53. 1. Yu X
    2. Li L
    3. Zola J
    4. Aluru M
    5. Ye H
    6. Foudree A
    7. Guo H
    8. Anderson S
    9. Aluru S
    10. Liu P
    11. Rodermel S
    12. Yin Y

    (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana

    Plant Journal 65:634–646.

    https://doi.org/10.1111/j.1365-313X.2010.04449.x

    • Google Scholar
54. 1. Zhu JY
    2. Sae-Seaw J
    3. Wang ZY

    (2013) Brassinosteroid signalling

    Development 140:1615–1620.

    https://doi.org/10.1242/dev.060590

    • Google Scholar
55. 1. Zipfel C
    2. Robatzek S
    3. Navarro L
    4. Oakeley EJ
    5. Jones JD
    6. Felix G
    7. Boller T

    (2004) Bacterial disease resistance in Arabidopsis through flagellin perception

    Nature 428:764–767.

    https://doi.org/10.1038/nature02485

    • Google Scholar

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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