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First published online May 18, 2007; 10.1105/tpc.106.047795 The Plant Cell 19:1709-1717 (2007) © 2007 American Society of Plant Biologists Tomato BRASSINOSTEROID INSENSITIVE1 Is Required for Systemin-Induced Root Elongation in Solanum pimpinellifolium but Is Not Essential for Wound Signaling[W]
a Division of Biology, Imperial College London, Ashford, Kent TN25 5AN, United Kingdom 2 To whom correspondence should be addressed. E-mail g.bishop{at}imperial.ac.uk; fax 44-207-584-2056.
The tomato Leu-rich repeat receptor kinase BRASSINOSTEROID INSENSITIVE1 (BRI1) has been implicated in both peptide (systemin) and steroid (brassinosteroid [BR]) hormone perception. In an attempt to dissect these signaling pathways, we show that transgenic expression of BRI1 can restore the dwarf phenotype of the tomato curl3 (cu3) mutation. Confirmation that BRI1 is involved in BR signaling is highlighted by the lack of BR binding to microsomal fractions made from cu3 mutants and the restoration of BR responsiveness following transformation with BRI1. In addition, wound and systemin responses in the cu3 mutants are functional, as assayed by proteinase inhibitor gene induction and rapid alkalinization of culture medium. However, we observed BRI1-dependent root elongation in response to systemin in Solanum pimpinellifolium. In addition, ethylene perception is required for normal systemin responses in roots. These data taken together suggest that cu3 is not defective in systemin-induced wound signaling and that systemin perception can occur via a non-BRI1 mechanism.
Brassinosteroids (BRs) are plant steroid hormones required for normal growth and development. Mutants in BR biosynthesis or signaling have a characteristic dramatic dwarf phenotype, indicating the importance of these hormones in plant growth and development (for reviews on BRs and BR signaling, see Bishop, 2003  ; Vert et al., 2005; Szekeres and Bishop, 2006). The major BR receptor in Arabidopsis thaliana is encoded by the BRASSINOSTEROID INSENSITIVE1 (BRI1) gene, which when mutated, results in a dwarf plant, similar in stature to BR biosynthesis mutants (Clouse et al., 1996). BRI1 encodes a receptor Ser/Thr kinase with a predicted extracellular domain of  24 Leu-rich repeats (LRRs) that is interrupted by an island domain between repeat 20 and 21 (Li and Chory, 1997; Vert et al., 2005). This is followed by a transmembrane domain and a C-terminal kinase (Li and Chory, 1997; Vert et al., 2005). BRI1 binds BRs via a novel steroid binding domain of 100 amino acids that encompasses LRR21 and the island domain (Kinoshita et al., 2005; Vert et al., 2005). BRI1 orthologs are known in several plant species. In tomato (Solanum lycopersicum), the curl3 (cu3) mutant has been characterized as a BR-insensitive dwarf (Koka et al., 2000), and a candidate gene approach showed that this mutant was defective in a homolog of BRI1 (Montoya et al., 2002).
Tomato BRI1 also has been purified as a systemin binding protein (Scheer and Ryan, 2002 Here, we provide further proof that Sl BRI1 is a functional BR receptor. In addition, we demonstrate that both cu3 and the BR synthesis mutant extreme dwarf (dx) are capable of producing systemin and wound responses. Intriguingly, we found that Solanum pimpinellifolium roots elongate in response to systemin, in a BRI1-dependent fashion. However, systemin-induced root elongation was not observed in closely related species. In these species, root length was reduced, which in S. lycopersicum is both jasmonate and BR independent but is ethylene dependent. These results indicate that Sl BRI1 is not essential for systemin-induced wound response, although in certain species, it may promote root growth.
Genetic Complementation of the cu3 Phenotype Previous analysis of the cu3 dwarf mutant demonstrated that it is insensitive to BL and that Spi BRI1 (S. pimpinellifolium BRI1) is mutated (Montoya et al., 2002 ). To confirm that Spi BRI1 is responsible for the cu3 phenotype, complementation was performed by introduction of Sl BRI1 (L. esculentum BRI1) under the control of the cauliflower mosaic virus (CaMV) 35S promoter (35S:Sl BRI1). Introduction of this T-DNA construct into the cu3 background generated two lines that recovered the dwarf phenotype (Figure 1
). The 35S:Sl BRI1 plants exhibited additional phenotypes, including delayed germination by 1 to 2 d, compared with the wild type or cu3. Internodal distance and hypocotyl length were greater than wild-type plants, and lateral branching (side shoot length) was also reduced (see Supplemental Table 1 online). Although Arabidopsis plants overexpressing At BRI1 have elongated petioles, this was not observed in 35S:Sl BRI1 plants. The leaves were more ovoid, with reduced serration, than those of the wild type. Leaves also frequently developed necrotic patches, reminiscent of a hypersensitive response. However, no pathogen could be associated with this phenotype, and wild-type plants did not exhibit a similar phenotype, even following inoculation with 35S:Sl BRI1 leaf extracts. Complementation of cu3 with Sl BRI1 under the control of its native promoter restored plants to the wild type and did not exhibit the additional phenotypes observed with 35S:Sl BRI1 (Figure 1).
Morphological analyses showed that the introduction of 35S:Sl BRI1 restored the BL responses abolished by the cu3 mutation. To confirm this, seedlings were treated with BL and root length was recorded (Figure 2 ). As had been previously demonstrated, cu3 roots were insensitive to BL treatment (Koka et al., 2000 ; Montoya et al., 2002). The introduction of 35S:Sl BRI1 restored a BL-responsive reduction in root elongation, with the sensitivity to BL being similar to wild-type plants.
Sl BRI1 Does Not Fully Complement Arabidopsis bri1-5 The results shown here and previously strongly indicated that Sl BRI1 is the functional ortholog of At BRI1. However, when Sl BRI1 was transformed into the At BRI1 mutant bri1-5, it failed to fully complement this mutation when placed under the control of either the Arabidopsis BRI1, S. lycopersicum BRI1, or CaMV 35S promoter (Table 1 ; see Supplemental Figure 1 online). Partially complementing lines had longer hypocotyls, increased rosette area, and longer inflorescence stems compared with bri1-5, although they were smaller than wild-type plants. To determine if the failure of Sl BRI1 to complement the Arabidopsis mutant was specific to Sl BRI1 or common to other solanaceous species, the tobacco and potato homologs Nb BRI1 (Nicotiana benthamiana BRI1) and St BRI1 (Solanum tuberosum BRI1), respectively, were transformed into bri1-5. Both of these genes failed to fully complement the bri1-5 mutant phenotype, although both morphologically recovered the cu3 phenotype. Interestingly, At BRI1 morphologically restores the cu3 phenotype to almost the wild type, indicating that a more stringent sequence requirement in Arabidopsis is required for genetic complementation.
To further investigate why Sl BRI1 failed to rescue bri1-5, chimeric constructs between At BRI1 and Sl BRI1 were produced. Complementation was achieved when the kinase domain of Sl BRI1 (amino acids 749 to 1207) was fused to the extracellular LRR region of At BRI1 (amino acids 1 to 739). However, the reciprocal construct failed to restore the bri1-5 mutant phenotype (Table 1).
BL Binding Is Not Detectable in cu3 Microsomes
Systemin-Induced PINII Expression Does Not Require BRI1 or BR PIN gene induction and rapid alkalization of cell suspension culture medium are key assays in determining the bioactivity of systemin (Meindl et al., 1998 ). Scheer et al. (2003) showed that cu3 had a reduced ability to induce the accumulation of PIN protein following treatment with either methyl jasmonate or systemin. Systemin treatments of 35S:Sl BRI1, cu3, and wild-type seedlings were performed to confirm the BRI1 dependence of systemin-induced PINII expression. During these studies, we noted that the rate of systemin solution uptake in cu3 was significantly lower than the wild type (Figure 4A
). This was presumably due to a lower transpiration rate in cu3 mutants because of the reduced leaf area. Systemin treatments were performed so that all seedlings were treated with the same amount of systemin, and no difference in the level of PINII transcripts or the sensitivity to systemin was observed between the wild type and mutants (Figure 4B). To confirm this result, systemin treatments were performed with another tomato BRI1 mutant, abs, and systemin-induced PINII transcript accumulation was also found to be similar to wild-type plants (Figure 4B). To test whether BRs are required for PINII transcript accumulation, the BR synthesis mutant dx, which lacks bioactive BRs in vegetative tissue (Bishop et al., 1999), was examined for its response to systemin. The dx mutants had wild-type levels of PINII expression, indicating that bioactive BRs are not required for systemin-mediated PIN gene induction.
cu3 Is Not Compromised in Wound-Induced PINII Expression Systemin induction is associated with mechanical wounding, and it may be expected that mutants in the systemin receptor would be defective in their wound response. cu3 mutants were mechanically wounded, and this treatment induced systemic PINII expression (Figure 5 ). In addition, systemic accumulation of PINII transcripts was found in the Sl BRI1 mutant abs and in the BR synthesis mutant dx. PINII transcripts were detectable between 2 and 4 h after wounding, and no significant difference was observed in the timing of the induction or the duration of response in any of the mutants. The level of PINII accumulation in all mutants was greater than the wild type, which may be a consequence of leaf morphology rather than alteration in wound responsiveness.
Medium Alkalinization in Response to Systemin Is Not Altered in cu3 The alkalinization of cell suspension medium has been used to show the activity of systemin (Meindl et al., 1998 ). This response is not affected by BL, although overexpression of tomato BRI1 in tobacco suspension enables systemin-responsive alkalinization (Scheer et al., 2003). Suspension cultures of the wild type and cu3 were generated, and the pH of the medium was recorded after the addition of systemin (Figure 6
). Both mutant and wild-type cultures responded at similar times and with similar amplitudes (P > 0.1).
Tomato Roots Respond to Systemin To discern the possible involvement of systemin in the BR response, we used root elongation to monitor the bioactivity of various systemin and hormone treatments. Root elongation was used because it is known to be a sensitive method to measure BR bioactivity in tomato (Roddick, 1994 ) and because cu3 mutants are known to be defective in the inhibition of root elongation in response to BRs (Koka et al., 2000; Montoya et al., 2002). Wild-type and cu3 seedlings were grown on medium containing systemin, and root length was recorded (Figure 7
). When wild-type S. pimpinellifolium seedlings were grown on systemin, roots were longer than those of untreated seedlings (P < 0.001 for all systemin concentrations). In addition, lateral branching and root hair growth were inhibited. Interestingly, cu3 seedlings exhibited a dose-dependent inhibition of root elongation (P < 0.001 for systemin concentrations >0.1 nM). Root hair growth in these mutants was not suppressed by the addition of systemin. In addition, an anthocyanin-like coloration was observed in cu3 roots at systemin concentrations >10 nM. The involvement of BRI1 in this response was confirmed by systemin treatment of cu3 plants transformed with Sl BRI1 (Figure 8
). These plants showed a restoration of wild-type systemin response. As a control for these experiments, the biologically inactive Ala-17 systemin was used and did not exhibit any significant bioactivity in roots (P > 0.05; see Supplemental Figure 2 online).
The inhibition of root growth in cu3 indicates that BRI1 is required for a wild-type response to systemin in this assay. To further investigate the role of BR in this systemin response, treatments with systemin in the presence of BL were performed (Figure 8). Not surprisingly, the response to systemin in the BR-insensitive mutant cu3 was not altered by the addition of BL. In wild-type seedlings, systemin partially suppressed the BL-induced reduction in root length. This response was dose dependent and required >1 nM systemin to elongate roots in the presence of 1 nM BL. This indicated that BRI1 plays a role in root elongation and that its function impacts both the systemin and BL signaling pathways.
The interaction between systemin and BL responses was examined further by investigating the effect of BL on the root growth of seedlings expressing reduced levels of prosystemin. Roots of antisense prosystemin plants responded in a similar way as the wild type (see Supplemental Figure 3 online). This was not unexpected since systemin is not expressed in roots (McGurl et al., 1992 The antisense line used was in an S. lycopersicum cultivar, and this species exhibited reduced root length in response to systemin (P < 0.001 for systemin concentrations >0.1 nM) (Figure 7). This result was opposite to that observed in S. pimpinellifolium roots. However, similar to S. pimpinellifolium roots, those of S. lycopersicum had decreased root hair growth and lateral branching in the presence of systemin. Since BR mutants exhibit defective etiolation, we analyzed the root response to systemin in both light- and dark-grown seedlings. When systemin treatments of S. pimpinellifolium and cu3 were performed on etiolated seedlings, root length was decreased in the presence of systemin (Figure 7B). We also noticed that the root length of untreated etiolated S. pimpinellifolium seedlings was significantly longer than light-grown seedlings; however, this was not the case for cu3 (P < 0.001 and P > 0.1, respectively). These data indicated that the response to systemin was different between S. lycopersicum and S. pimpinellifolium species (i.e., S. lycopersicum seedlings lacked root elongation). However, when grown in the dark, S. pimpinellifolium seedlings responded in a similar manner to light-grown S. lycopersicum seedlings, in that both sets of seedlings have reduced root length in the presence of systemin. Further investigation of the role of BRI1 in the response to systemin was performed using the weak BRI1 mutant abs (S. lycopersicum). In this mutant, systemin induced a response similar to wild-type roots. In addition, the BL synthesis mutant dx produced a response equivalent to the wild type. These data suggested that the systemin-induced root inhibition of S. lycopersicum seedlings is not influenced by BR signaling, but it is in S. pimpinellifolium seedlings.
Overexpression of prosystemin results in jasmonate-dependent increased hypocotyl elongation (Howe and Ryan, 1999
The role of BRI1 in BR perception in Arabidopsis is well established. As such, the purification of tomato BRI1 by binding to systemin has been an enigma (Yin et al., 2002 ; Bishop, 2003; Szekeres, 2003; Boller, 2005). It was therefore important to show that Sl BRI1 was a functional BR receptor using both genetic and biochemical approaches. Genetic restoration of the cu3 mutant phenotype using the CaMV 35S promoter to express the tomato BRI1 generated nondwarf plants that had elongated stems, indicating a role for tomato BRI1 in growth. The rescued lines also exhibited less serration of the leaf margins, indicating a role for BRs in leaf margin development. This is not surprising since Arabidopsis mutants in BR biosynthesis and signaling have been identified in screens for leaf phenotypes (Kim et al., 1998; Pérez-Pérez et al., 2002). Transformation experiments using the endogenous Sl BRI1 promoter to express the Sl BRI1 gene resulted in plants that have phenotypes very similar to those of the wild type, providing further proof that the cu3 mutant is defective in the LRR receptor kinase Sl BRI1. Sl BRI1, Nb BRI1, and St BRI1 are able to phenotypically rescue the cu3 phenotype to the wild type. However, these genes fail to fully complement the Arabidopsis BRI1 mutant bri1-5 when expressed under the control of the Arabidopsis BRI1 promoter. When the extracellular domain of the Arabidopsis gene is fused to the tomato kinase domain, complementation is achieved; this suggests that the extracellular LRR region from Arabidopsis is required for full function in Arabidopsis.
The extracellular region of BRI1 is poorly conserved between species when compared with the kinase domain. However, several amino acids are conserved in this region in all known BRI1 homologs. Of particular interest is the NGSM motif located in the region that has recently been shown to bind BRs (Kinoshita et al., 2005
To study the putative interaction of BR and systemin signaling, we sought confirmation that cu3 mutants were defective in systemin signaling. In previous studies, the cu3 mutant was shown to have only
These results are consistent with the observation that dx, cu3, and abs mutants exhibit a wound response. This response is greater than in wild-type plants, and this is most likely the consequence of altered plant morphology. However, the possibility exists that BRI1 and BRs are involved in the regulation of wound-induced PINII induction. Taken together, these data suggested that a functional BRI1 receptor is not essential for the systemin-induced wound response. Furthermore, systemin treatments of suspension cultures from cu3 mutants and the wild type confirmed that medium alkalinization in response to systemin was normal. Thus, Sl BRI1 is not essential for the systemin-induced alkalinization response. However, Scheer et al. (2003)
BRs cause cell elongation, and although the overexpression of prosystemin results in plants with jasmonate-dependent elongated hypocotyls (Howe and Ryan, 1999
When etiolated S. pimpinellifolium or light-grown S. lycopersicum roots were investigated, root length was reduced in response to systemin, suggesting that both environmental and species-specific factors influence the way in which roots respond to systemin. The reduction in root length observed in S. lycopersicum was not altered in jasmonate synthesis mutants, unlike the response observed in hypocotyls of plants overexpressing prosystemin (Howe and Ryan, 1999
The interaction between ethylene and BR signaling is not well understood; however, an interaction has been observed. BRs can stimulate ethylene biosynthesis, and ethylene induces expression of BR synthesis genes (Schlagnhaufer and Arteca, 1985
Systemin is a member of the growing number of peptides that have been shown to have biological activity in plants that include tobacco systemins, CLAVATA3, S-locus protein 11, phytosulfokine, and RALFs (Matsubayashi and Sakagami, 2006
T-DNA Construction and Generation of Complemented Lines Sl BRI1 was PCR amplified from Solanum lycopersicum cv Moneymaker using primers 5'-CATCAAGAGCTCAAGCTATAGATTCAAG-3' to introduce an SstI site in the 5' untranslated leader of Sl BRI1 and 5'-TGGATGGGAACTAGTGGTACATAC-3' that introduced an SpeI site in the 3' untranslated tail. The PCR product was cloned and sequenced. The resulting plasmid was digested with SstI and SpeI, and Sl BRI1 was cloned into T-DNA vector GB1421 (Bishop et al., 1999 ) cut with SstI and XbaI to generate 35S:Sl BRI1. To produce BRI1 constructs under the control of the S. lycopersicum promoter, a 2-kb promoter region was amplified from the tomato BAC LeHBa28J23 (Clemson University Genomics Institute) using the primers 5'-GAATTCTAGAGAGGGAAACATCGT-3' and 5'-GGTACCGAAACTTTATAGCTTAAATGGTG-3'. The promoter region was then cloned into the EcoRI/KpnI sites of pCA2302 (pCAMBIA2300 containing the EcoRI/BstUI green fluorescent protein fragment from pCAMBIA1302 cloned into the EcoRI/PmeI sites). A 1.8-kb Arabidopsis thaliana promoter was amplified using PCR primers (5'-CAATTGGAGCGCGTGTAGACCACG-3' and 5'-GGTACCTTGTGAGAGAGAAAAGTGTG-3') and cloned as an MfeI/KpnI fragment into EcoRI/KpnI of pCA2302. BRI1 gene regions were then cloned into either vector as KpnI/SpeI fragments following amplification with the following PCR primers: Sl BRI1, 5'-GGTACCTTTGAAGATGAAAGC-3' and 5'-ACTAGTACCTCCAAGGTGTTTGCTCAG-3'; At BRI1, 5'-GGTACCTTGAGAAATGAAGAC-3' and 5'-ACTAGTTCCACCTAATTTTCCTTCAGG-3'. The Sl BRI1/At BRI1 fusion constructs were produced by amplifying both the LRR and kinase regions and introducing an internal Kpn2I restriction site. This was performed using terminal primers described above and the following internal primers: Sl BRI1, 5'-TCATTCCGGAGAGATTATTGTTTGACAGGTCAATC-3' and 5'-AATCTCTCCGGAATGATTCCTGAATCTGCACC-3'; At BRI1, 5'-TTGTCCGGACCGATTCCTGAGATGGGTC-3' and 5'-TCGGTCCGGACAAATTATTATTCG-3'. These fragments were then sequentially ligated into the binary vectors containing either promoter. The Nicotiana benthamiana and Solanum tuberosum cv Maris Peer BRI1 genes were amplified by PCR (5'-TCGGTACCTTTGAAGATGAAACCTCACAAGAG-3' and 5'-TCACTAGTACCTCCTAGGTGTTTGCTCAGCTCATTA-3'; 5'-GGTACCTTTGAAGATGAAAGC-3' and 5'-ACTAGTACCTCCAAGGTGTTTGCTTAGCTCATTGCC-3', respectively) and cloned as KpnI/SpeI fragments under the control of the Arabidopsis promoter. All constructs were sequenced to ensure no mutations were introduced during PCR.
All constructs were transformed into cu3 as described previously (Bishop et al., 1999
3H-BL Binding to Microsomal Fractions
Systemin Application and Wounding Mechanical wounding was performed on 4- to 5-week-old seedlings by crushing terminal leaflets with forceps three times. Samples were taken from the leaf immediately above that which had been wounded. At least six seedlings were used for each sample. RNA was extracted from systemin- and wound-treated samples, and RNA gel blotting was performed using either PINII or tomato 18S rRNA derived probes. Wounding and systemin treatments were performed at least three times with similar results.
Alkalinization Experiments
Root Elongation Assay
Accession Numbers
Supplemental Data
We thank the glasshouse staff at both the Institute of Biological Sciences, Aberystwyth, and the Division of Biology, Wye, for plant care. This work has been generously supported by the Biotechnology and Biosciences Research Council (Grant P19961 to G.J.B.), by the Human Frontier Research Program (G.J.B. and J.C.), and by the USDA (J.C.). A.C.-D. was a long-term fellow of the Human Frontier Research Program. We also thank C. Ryan and G. Howe for seeds of the tomato antisense systemin line and jasmonate mutants, respectively, and J. Giovannoni for the tomato BAC clone.
1 Current address: Genética Molecular, CONSORCIO Consejo Superior de Investigaciones Cientificas–Institut de Recerca i Tecnologia Agroalimentàries, C/Jordi Girona 18-26, Barcelona 08034, Spain.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Gerard J. Bishop (g.bishop{at}imperial.ac.uk).
[W] Online version contains Web-only data. www.plantcell.org/cgi/doi/10.1105/tpc.106.047795 Received September 29, 2006; Revision received March 29, 2007. accepted April 27, 2007.
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