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First published online April 9, 2004; 10.1105/tpc.020370 © 2004 American Society of Plant Biologists COS1: An Arabidopsis coronatine insensitive1 Suppressor Essential for Regulation of Jasmonate-Mediated Plant Defense and Senescence
a Laboratory of Plant Signal Transduction, Institute of Molecular and Cell Biology, National University of Singapore, 117604 Republic of Singapore 1 To whom correspondence should be addressed. Email daoxin{at}imcb.a-star.edu.sg; fax 65-68727517.
The Arabidopsis thaliana CORONATINE INSENSITIVE1 (COI1) gene encodes an F-box protein to assemble SCFCOI1 complexes essential for response to jasmonates (JAs), which are a family of plant signaling molecules required for many essential functions, including plant defense and reproduction. To better understand the molecular basis of JA action, we screened for suppressors of coi1 and isolated a coi1 suppressor1 (cos1) mutant. The cos1 mutation restores the coi1-related phenotypes, including defects in JA sensitivity, senescence, and plant defense responses. The COS1 gene was cloned through a map-based approach and found to encode lumazine synthase, a key component in the riboflavin pathway that is essential for diverse yet critical cellular processes. We demonstrated a novel function for the riboflavin pathway that acts downstream of COI1 in the JA signaling pathway and is required for suppression of the COI1-mediated root growth, senescence, and plant defense.
Jasmonates (JAs), which include jasmonic acid and its cyclopentane derivatives as well as cyclopentenones (Reymond and Farmer, 1998  ), are synthesized from the octadecanoid/hexadecanoid pathways and widely distributed throughout the plant kingdom. JAs modulate the expression of numerous genes (Reymond et al., 2000; Schenk et al., 2000; Sasaki et al., 2001; Feng et al., 2003) and mediate responses to stress, wounding, insect attack, pathogen infection, and UV damage (Staswick, 1992; McConn et al., 1997; Wasternack and Parthier, 1997; Reymond and Farmer, 1998; Farmer, 2001). They also play pivotal roles in reproduction (Feys et al., 1994; McConn and Browse, 1996; Xie et al., 1998) and regulate many other plant developmental processes (Creelman and Mullet, 1997). Without JA, Arabidopsis thaliana plants, such as the JA biosynthetic mutants fad (McConn and Browse, 1996), opr3/dd1 (Sanders et al., 2000; Stintzi and Browse, 2000; Stintzi et al., 2001), and aos (Park et al., 2002), are unable to generate viable pollen and therefore fail to complete their life cycle. Without JA signaling or JA adenylation, Arabidopsis plants, including jar1 (Staswick et al., 1992, 1998), coronatine insensitive1 (coi1) (Feys et al., 1994), and jin (Berger et al., 1996), are unresponsive to JA-inhibitory root growth, unable to accumulate JA-inducible genes, and susceptible to pest attack and pathogen infection.
The coi1 mutation defined a key regulator in the JA signaling pathway. The recessive coi1 mutants fail to respond to JA and coronatine, a phytotoxin structurally similar to jasmonic acid (Feys et al., 1994
Genetic screens for suppressors have been used to further investigate gene functions and to dissect signaling transduction pathways. In Arabidopsis, suppressor screens have been used to identify genes/mutants functional in many pathways, including the auxin (Cernac et al., 1997 To better understand the molecular mechanism via which COI1 regulates JA responses, we conducted a screen for suppressors of the coi1 mutant. A coi1 suppressor1 (cos1) recessive mutant was identified and found to regain wild-type–like phenotypes of JA-sensitive root elongation, gene expression, senescence, and defense response in the coi1 background. The COS1 gene was cloned using a map-based approach and found to encode lumazine synthase, a key component in the riboflavin pathway that is essential for diverse yet critical cellular processes. The riboflavin pathway appears to act downstream of COI1 and to be required for suppression of the COI1-mediated root growth, senescence, and plant defense.
Genetic Screening for the coi1 Suppressors Because null mutant alleles of COI1 are male sterile (Feys et al., 1994 ; Xie et al., 1998) and unsuitable for suppressor screening, we isolated the leaky allele coi1-2 (Xu et al., 2002), which is resistant to JA but partially fertile and able to produce a small quantity of seeds. The coi1-2 seeds were mutagenized with ethyl methanesulfonate (EMS), and the M2 seeds harvested from  20,000 M1 EMS-mutagenized coi1-2 plants were then used in a screen for coi1 suppressors based on the suppression of JA resistance in the elongating root of coi1-2. Approximately 100,000 M2 seeds were germinated on plant growth medium containing 25 µM methyl JA (MeJA) that inhibits root growth in wild-type seedlings but not in coi1-2 seedlings. Fourteen seedlings were isolated from the mutagenized coi1-2 M2 population because they regained the JA-sensitive phenotype displaying short roots and stunted growth when grown on medium containing MeJA. These fourteen plants were therefore selected as suppressor candidates of coi1. Each suppressor candidate was backcrossed to the coi1-2 plant, and all the F1 plants were found to be resistant to MeJA, demonstrating that they are all recessive mutations. Among the fourteen F2 populations, four F2 progeny clearly showed 3:1 segregation of JA resistance/sensitivity, indicating that the restoration of JA inhibitory root growth in each of these four mutants results from a single recessive mutant locus. Genetic crosses between these four lines demonstrate that they are mutated at different loci because all the F1 progeny show resistance to MeJA. One locus, which is named cos1, was chosen for further studies because of the strong suppression phenotypes (Figure 1A). This cos1 coi1-2 mutant (homozygous for both cos1 and coi1-2 mutations) was backcrossed to coi1-2 four times to segregate away other potential mutations.
Suppression of cos1 on coi1-Mediated JA Insensitivity The basis for the initial screen for coi1 suppressors was the suppression of JA insensitivity in the elongating coi1-2 root. To further confirm the effect of the cos1 mutation, we measured the root length of seedlings grown on MS medium supplemented with various concentrations of MeJA (0, 1, 5, and 25 µM). As expected, the coi1-2 is resistant to JA (Figures 1A and 1B). However, root growth of the cos1 coi1-2 seedlings was inhibited by MeJA (Figures 1A and 1B), demonstrating that the cos1 mutation fully suppresses coi1-mediated JA insensitivity. In contrast with JA-sensitive root growth rescued by cos1 in coi1-2, the cos1 mutation was unable to restore the male fertility defect of coi1-2 plants (data not shown).
Restoration of JA-Inducible Gene Expression in the coi1 Mutant by cos1
Mutations in COI1 were found to cause a defect in JA-inducible expression of senescence-associated genes (Y. He et al., 2002
Restoration of JA-Dependent Senescence in the coi1 Mutant by cos1
Senescence also was assessed by measuring chlorophyll content, a typical senescence-associated physiological marker, which is known to decline with the progression of age-dependent senescence (Yoshida et al., 2002 ). The rosette leaves of 20-d-old plants grown in soil were harvested and used in the chlorophyll content measurement. As shown in Figure 2B, the relative chlorophyll content of the coi1-2 mutant (100%) is higher than that of the wild type (90%). The chlorophyll content in cos1 coi1-2 is severely reduced (60%), suggesting that cos1 severely suppresses the defect of leaf senescence in coi1-2.
The leaves of Arabidopsis wild-type seedlings treated with JA displayed visible yellowing, which is one of the striking precocious symptoms associated with leaf senescence (Y. He et al., 2002
Restoration of the JA-Regulated Defense Response in the coi1 Mutant by cos1
The Effect of cos1 on transport inhibitor response1 In addition to COI1, the JAR1 gene was the only cloned gene in the signaling pathway defined by the JA-insensitive mutants (Staswick et al., 2002 ). To examine the effects of the cos1 mutation in the JA-insensitive mutant jar1 (Staswick, 1992; Staswick et al., 1998), we attempted to generate the cos1 jar1 double mutant through sequence verification of the jar1-1 allele among cos1 homozygous plants, which were identified from F2 progeny of a cross between jar1-1 and cos1 coi1-2 based on cos1-conferred lesion-like yellow spots (Figures 2C and 2D). Surprisingly, we were unable to identify the cos1 jar1-1 mutants because none of the cos1 homozygous F2 plants contained the jar1-1 allele, though >100 plants were sequence verified. These data indicate that the cos1 locus has tight genetic linkage with the JAR1 locus, which makes it difficult to generate the cos1 jar1-1 double mutants. Similarly, we also failed to generate cos1 in the wild-type COI1 or coi1-1 null mutant background through genetic crossing (data not shown), suggesting a tight linkage of cos1 with COI1 that is physically close to the JAR1 gene (Arabidopsis genome sequencing project).
We then attempted to investigate the role for the cos1 mutation in transport inhibitor response1 (tir1), an auxin-insensitive mutant, which defines the F-box protein TIR1 that is most closely related to COI1 (Ruegger et al., 1998
Map-Based Cloning of COS1 To genetically map the COS1 locus, we identified a Landsberg erecta JA-insensitive mutant allele coi1-12, which contains a single amino acid replacement from Phe 359 to Lys in COI1 (D. Xie, unpublished data) and has a polymorphic genetic background from the Columbia cos1 coi1-2 mutant. We made the genetic crossing between the coi1-12 and cos1 coi1-2 plants and subsequently screened for their F2 progeny (homozygous for both cos1 and coi1) those that are sensitive to JA. Based on the linkage analysis among molecular markers and the cos1-conferred JA-sensitive phenotype using these JA-sensitive F2 progeny, we localized the COS1 locus on chromosome II between two amplified fragment length polymorphism (AFLP) markers, A18000 and A18300. As shown in Figure 5A, the COS1 locus was mapped between the JAR1 and COI1 loci, consistent with our previous observation that cos1 has tight genetic linkage with JAR1 and COI1. Further mapping using a cleaved amplified polymorphic sequence marker, C18150 (one recombinant), and AFLP marker A18250 (four recombinants) placed COS1 on a BAC, F6E13, which contains a 110-kb Arabidopsis genomic insert (Figure 5B).
The COS1 gene was finally localized onto an 4-kb BamHI fragment (B4) by functional complementation with the subcloned F6E13 fragments (Figure 5C). The B4 fragment identifies a single 684-bp full-length cDNA (Figure 5C). Thus, the 684-bp cDNA is the COS1 gene. Further analysis of the cos1 coi1-2 plants transgenic for either the B4 fragment or the COS1 cDNA that was 5' myc-tagged under the control of the 35S promoter of Cauliflower mosaic virus (CaMV 35S) (referred to as tCOS1) demonstrates that both the B4 fragment and the COS1 cDNA can complement the cos1-conferred senescence (Figure 5D; data not shown), JA sensitivity (Figure 5E), and defense response (Figure 5F). The corresponding sequence from the cos1 mutation deviated from that of the wild type by a single nucleotide change (G238A), G to A, at position + 238 relative to the translation start codon of the COS1 genomic DNA (Figure 6). This single nucleotide, G238, is the first nucleotide of the second exon and therefore is crucial for RNA splicing. The G238A point mutation abolished the splicing recognition sequence (from TA/GG to TA/AG), and the TA/GC sequence located 18 bp downstream of G238A mutation serves as a new RNA splicing recognition site resulting in an 18-nucleotide deletion in the mutant cos1 cDNA (Figure 6), which was confirmed by sequence verification of the RT-PCR–amplified cos1 mutant cDNA.
To investigate whether the 18-bp deletion in the mutant cos1 mRNA affects the protein expression of the mutant cos1, we made transgenic plants expressing the mutant cos1 cDNA that was 5' myc-tagged under the control of the CaMV 35S constitutive promoter (referred to as tcos1). Protein gel blotting with  -Myc antibody shows that the tcos1-encoded mutant protein was accumulated at a level similar to the tCOS1-encoded protein in the transgenic lines (data not shown); however, tCOS1 is able to fully complement the cos1 mutation, whereas tcos1 could not (Figures 5D to 5F; data not shown). The result indicates that the 18-bp deletion in cos1 does not disrupt COS1 protein stability; however, the six amino acids encoded by the deleted 18 nucleotides are crucial for COS1 function.
Sequence analysis reveals that the COS1 gene encodes lumazine synthase, which was previously shown to functionally complement the bacterial lumazine synthase–deficient mutant (Jordan et al., 1999
Null mutations in COI1 abolish all the JA responses exhibiting resistance to JA inhibition of plant growth, defect in pollen fertility, reduction in senescence, and susceptibility to pathogen infection and insect attack. The COI1 protein previously was found to assemble into SCFCOI1 complexes that were speculated to recruit substrate proteins, which may function as suppressors to negatively regulate the expression of appropriate downstream genes essential for JA responses (Xie et al., 1998 ; Xu et al., 2002). To further dissect COI1-mediated JA responses and to gain insight into the mechanism of COI1 function, we have isolated a coi1 suppressor mutant, here referred as to cos1. The cos1 mutation can restore the coi1-related phenotypes, including defects in JA sensitivity, senescence, and plant defense responses in the coi1 background. However, the cos1 mutation failed to restore the male fertility defect of the coi1-2 plants, which further dissects the JA signal transduction pathway and indicates that JA-mediated pollen development is regulated by other component(s) independent of COS1. The cos1 mutation also failed to restore the auxin insensitivity in the tir1-1 mutant, demonstrating that cos1 is not a suppressor of tir1.
The COS1 gene was cloned via a map-based approach and found to encode lumazine synthase. Lumazine synthase catalyzes the penultimate step in biosynthesis of riboflavin (vitamin B2) in plants, fungi, and microorganisms (Persson et al., 1999 Because the riboflavin pathway is essential for diverse yet critical cellular processes, a complete abolishment of the riboflavin pathway would cause pleiotrophic phenotypes and probably affect the survival of plants. It is likely that the cos1 mutant identified in this work is a leaky allele and that the cos1 mutant protein is partially functional. In the cos1 coi1-2 mutant plants, the 6–amino acid deletion in the cos1 mutant protein appears to attenuate the riboflavin pathway but not to completely disrupt this pathway. Therefore, the cos1 mutation does not affect the plant survival but suppresses the defects in the JA sensitivity, senescence, and plant defense responses in the coi1-2 mutant background via attenuation of the unidentified negative regulator(s) that require the riboflavin pathway to exert their suppression action. Here, we propose a working model for the function of the riboflavin pathway in the JA signaling transduction chain. As shown in Figure 7, different SCFCOI1 substrates (indicated as groups S1 and S2), which will be degraded through SCFCOI1-26S proteasome in responsive to JA signaling, may negatively regulate different transcription factors and/or appropriate downstream genes (indicated as two sets of genes, G1 and G2) that mediate their corresponding JA responses (indicated as response I and response II). The first group of substrates (S1) may require the riboflavin pathway (indicated as RIB) to exert their suppression action on the downstream G1 target genes, whereas the action of the second group of substrates (S2) may not require the riboflavin pathway. In wild-type plants (Figure 7, left panel), the endogenous JA, and developmental and environmental cues (such as flowering and insect attack) that activate JA signaling, promote the ubiquitylation and degradation of substrate proteins. As a result, the downstream genes are expressed to maintain JA responses. In the coi1 null mutant plants (Figure 7, middle panel), mutation of COI1 disrupts SCFCOI1, resulting in a high level of accumulation of the SCFCOI1 substrates, which constantly exert suppression on the downstream genes, leading to loss of all the JA responses. In the cos1 coi1 double mutants (Figure 7, right panel), the cos1 mutation attenuates the riboflavin pathway and therefore decreases the suppression action exerted by the S1 substrates and finally activates the expression of their downstream genes (G1), leading to restoration of their corresponding JA responses, including JA sensitivity, senescence, and defense (response I). However, cos1 is unable to restore fertility in coi1 because the riboflavin pathway is not required for the suppression exerted by the S2 substrate that suppresses the G2 downstream genes, leading to defect in pollen fertility (response II).
In the cos1 coi1-2 double mutants, application of exogenous JA was found to cause enhanced inhibition of root growth (response I) and induction of gene expression (Figure 1). This induction of JA response by exogenous JA in the cos1 coi1-2 double mutants may result from activation of substrate (S1) degradation because coi1-2 is a leaky mutant allele. Alternatively, JA-responsive G1 genes may be repressed by substrate S1 but also activated by some unknown JA-regulated positive components, probably including dephosphorylated regulator(s) previously proposed (Rojo et al., 1998 ); the exogenous JA was therefore able to activate the unknown JA-regulated positive components that modulate the expression of JA-responsive G1 genes in the cos1 coi1-2 double mutants. More experiments will be required to test our working model and explanation. Identification and functional analysis of the SCFCOI1 substrates will be useful to understanding the novel role for the riboflavin pathway in JA signaling and will be essential for illustrating the molecular mechanism via which JA regulates plant defense and development.
Plant Growth Conditions Seeds were surface sterilized, plated on plant growth medium (MS; Sigma, St. Louis, MO), chilled at 4°C for 3 d, and then transferred to a growth chamber under a 16-h-light (22 to 24°C)/8-h-dark (16 to 19°C) photoperiod. For root length measurement experiments, the seedlings were grown on MS medium supplemented with various concentrations of MeJA (Aldrich, Milwaukee, WI) for 9 d before measurement.
Mutant Screening M2 Seeds were routinely plated on MS medium containing 25 µM MeJA to screen for mutants sensitive to MeJA exhibiting phenotypes of short root and stunted growth.
Generation of the tir1-1 cos1 coi1-2 Mutant
RNA Gel Blot and RT-PCR Analysis RT-PCR analysis was performed following routine procedures. The senescence marker gene SAG12 was amplified with primers 5'-CAGCTGCGGATGTTGTTG-3' and 5'-CCACTTTCTCCCCATTTTG-3', and the ACTIN gene was amplified with primers 5'-CACCGCTTAACCCGAA-3' and 5'-GTGAGGTCACGACCAG-3'. Total RNA used in Figure 1 was extracted from 20-d-old plants that were untreated (CK) or treated with 100 µM MeJA in daytime for 3, 6, and 9 h (Figure 1C) or for 48 h (Figures 1D and 1E).
Molecular Markers
Complementation Test
The cos1 coi1-2 plants transgenic for the mutant cos1 cDNA, the wild-type COS1 cDNA, and an
Pathogen Infection
Measurement of Chlorophyll and Transmission Electron Microscopy Samples examined by transmission electron microscopy were fixed in 2% paraformaldehyde and 4% glutaraldehyde in 100 mM cacodylate buffer for 3 h and then postfixed with 2% osmium tetroxide in 100 mM sodium cacodylate buffer for 1 h at 4°C. Samples were then dehydrated through a series of 30, 50, 70, 90, and 100% ethanol and finally in propylene oxide. Samples were embedded in 100% Spurr's resin (Electron Microscopy Sciences, Fort Washington, PA) and polymerized at 65°C overnight. Ultrathin sections were cut on a Jung Reichert ultramicrotome and examined with a transmission electron microscope (JEM1010; JEOL, Tokyo, Japan) at 100 kV. Sequence data from this article have been deposited with the GenBank data library under accession number NM_129967.
We thank Nottingham Arabidopsis Stock Centre and the ABRC for seeds and BAC clones and Paul Staswick and Mark Estelle for jar1 and tir1 mutants. L.D. was supported by the Science and Technology Department of Hunan Province, China. This work was supported by a grant to D.X. from Singapore Agency of Science, Technology, and Research.
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: Daoxin Xie (daoxin{at}imcb.a-star.edu.sg). Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.020370. Received December 21, 2003; accepted February 13, 2004.
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