An allele of Arabidopsis COI1 with hypo- and hypermorphic phenotypes in plant growth, defence and fertility

Resistance to biotrophic pathogens is largely dependent on the hormone salicylic acid (SA) while jasmonic acid (JA) regulates resistance against necrotrophs. JA negatively regulates SA and is, in itself, negatively regulated by SA. A key component of the JA signal transduction pathway is its receptor, the COI1 gene. Mutations in this gene can affect all the JA phenotypes, whereas mutations in other genes, either in JA signal transduction or in JA biosynthesis, lack this general effect. To identify components of the part of the resistance against biotrophs independent of SA, a mutagenised population of NahG plants (severely depleted of SA) was screened for suppression of susceptibility. The screen resulted in the identification of intragenic and extragenic suppressors, and the results presented here correspond to the characterization of one extragenic suppressor, coi1-40. coi1-40 is quite different from previously described coi1 alleles, and it represents a strategy for enhancing resistance to biotrophs with low levels of SA, likely suppressing NahG by increasing the perception to the remaining SA. The phenotypes of coi1-40 lead us to speculate about a modular function for COI1, since we have recovered a mutation in COI1 which has a number of JA-related phenotypes reduced while others are equal to or above wild type levels.This work was supported by grant BIO201018896 from "Ministerio de Economia y Competitividad" (MINECO) of Spain and by grant ACOMP/2012/105 from "Generalitat Valenciana" to PT, a JAE-CSIC Fellowship to JVC, a FPI-MINECO to AD, and Fellowships from the European Molecular Biology Organization and the Human Frontier Science Program to BBHW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Dobón Alonso, A.; Wulff, BBH.; Canet Perez, JV.; Fort Rausell, P.; Tornero Feliciano, P. (2013). An allele of Arabidopsis COI1 with hypo- and hypermorphic phenotypes in plant growth, defence and fertility. PLoS ONE. 1(8):55115-55115. https://doi.org/10.1371/journal.pone.0055115551155511518Vlot, A. C., Dempsey, D. A., & Klessig, D. F. (2009). Salicylic Acid, a Multifaceted Hormone to Combat Disease. Annual Review of Phytopathology, 47(1), 177-206. doi:10.1146/annurev.phyto.050908.135202Mauch, F., Mauch-Mani, B., Gaille, C., Kull, B., Haas, D., & Reimmann, C. (2001). Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase. The Plant Journal, 25(1), 67-77. doi:10.1046/j.1365-313x.2001.00940.xGaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., … Ryals, J. (1993). Requirement of Salicylic Acid for the Induction of Systemic Acquired Resistance. Science, 261(5122), 754-756. doi:10.1126/science.261.5122.754Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., … Ryals, J. (1994). A Central Role of Salicylic Acid in Plant Disease Resistance. Science, 266(5188), 1247-1250. doi:10.1126/science.266.5188.1247Lawton, K. (1995). Systemic Acquired Resistance inArabidopsisRequires Salicylic Acid but Not Ethylene. Molecular Plant-Microbe Interactions, 8(6), 863. doi:10.1094/mpmi-8-0863Ross, A. F. (1961). Systemic acquired resistance induced by localized virus infections in plants. Virology, 14(3), 340-358. doi:10.1016/0042-6822(61)90319-1Pieterse, C. M. ., & van Loon, L. C. (1999). Salicylic acid-independent plant defence pathways. Trends in Plant Science, 4(2), 52-58. doi:10.1016/s1360-1385(98)01364-8Fonseca, S., Chico, J. M., & Solano, R. (2009). The jasmonate pathway: the ligand, the receptor and the core signalling module. Current Opinion in Plant Biology, 12(5), 539-547. doi:10.1016/j.pbi.2009.07.013Ton, J., De Vos, M., Robben, C., Buchala, A., Métraux, J.-P., Van Loon, L. C., & Pieterse, C. M. J. (2002). Characterization ofArabidopsisenhanced disease susceptibility mutants that are affected in systemically induced resistance. The Plant Journal, 29(1), 11-21. doi:10.1046/j.1365-313x.2002.01190.xCui, J., Bahrami, A. K., Pringle, E. G., Hernandez-Guzman, G., Bender, C. L., Pierce, N. E., & Ausubel, F. M. (2005). Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proceedings of the National Academy of Sciences, 102(5), 1791-1796. doi:10.1073/pnas.0409450102Robert-Seilaniantz, A., Navarro, L., Bari, R., & Jones, J. D. (2007). Pathological hormone imbalances. Current Opinion in Plant Biology, 10(4), 372-379. doi:10.1016/j.pbi.2007.06.003Garcion, C., Lohmann, A., Lamodière, E., Catinot, J., Buchala, A., Doermann, P., & Métraux, J.-P. (2008). Characterization and Biological Function of the ISOCHORISMATE SYNTHASE2 Gene of Arabidopsis. Plant Physiology, 147(3), 1279-1287. doi:10.1104/pp.108.119420Tornero, P., Chao, R. A., Luthin, W. N., Goff, S. A., & Dangl, J. L. (2002). Large-Scale Structure –Function Analysis of the Arabidopsis RPM1 Disease Resistance Protein. The Plant Cell, 14(2), 435-450. doi:10.1105/tpc.010393Bowling, S. A., Guo, A., Cao, H., Gordon, A. S., Klessig, D. F., & Dong, X. (1994). A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. The Plant Cell, 6(12), 1845-1857. doi:10.1105/tpc.6.12.1845Bowling, S. A., Clarke, J. D., Liu, Y., Klessig, D. F., & Dong, X. (1997). The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. The Plant Cell, 9(9), 1573-1584. doi:10.1105/tpc.9.9.1573Yu, I. -c., Parker, J., & Bent, A. F. (1998). Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proceedings of the National Academy of Sciences, 95(13), 7819-7824. doi:10.1073/pnas.95.13.7819Dietrich, R. A., Delaney, T. P., Uknes, S. J., Ward, E. R., Ryals, J. A., & Dangl, J. L. (1994). Arabidopsis mutants simulating disease resistance response. Cell, 77(4), 565-577. doi:10.1016/0092-8674(94)90218-6Rivas-San Vicente, M., & Plasencia, J. (2011). Salicylic acid beyond defence: its role in plant growth and development. Journal of Experimental Botany, 62(10), 3321-3338. doi:10.1093/jxb/err031Wang, D. (2005). Induction of Protein Secretory Pathway Is Required for Systemic Acquired Resistance. Science, 308(5724), 1036-1040. doi:10.1126/science.1108791Ritter, C. (1995). TheavrRpm1Gene ofPseudomonas syringaepv.maculicolaIs Required for Virulence on Arabidopsis. Molecular Plant-Microbe Interactions, 8(3), 444. doi:10.1094/mpmi-8-0444Debener, T., Lehnackers, H., Arnold, M., & Dangl, J. L. (1991). Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. The Plant Journal, 1(3), 289-302. doi:10.1046/j.1365-313x.1991.t01-7-00999.xGrant, M., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A., … Dangl, J. (1995). Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science, 269(5225), 843-846. doi:10.1126/science.7638602Mindrinos, M., Katagiri, F., Yu, G.-L., & Ausubel, F. M. (1994). The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell, 78(6), 1089-1099. doi:10.1016/0092-8674(94)90282-8Coego, A., Ramirez, V., Gil, M. J., Flors, V., Mauch-Mani, B., & Vera, P. (2005). An Arabidopsis Homeodomain Transcription Factor, OVEREXPRESSOR OF CATIONIC PEROXIDASE 3, Mediates Resistance to Infection by Necrotrophic Pathogens. The Plant Cell, 17(7), 2123-2137. doi:10.1105/tpc.105.032375Pieterse, C. M. J., van Wees, S. C. M., van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., … van Loon, L. C. (1998). A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis. The Plant Cell, 10(9), 1571-1580. doi:10.1105/tpc.10.9.1571Berger, S., Bell, E., & Mullet, J. E. (1996). Two Methyl Jasmonate-Insensitive Mutants Show Altered Expression of AtVsp in Response to Methyl Jasmonate and Wounding. Plant Physiology, 111(2), 525-531. doi:10.1104/pp.111.2.525Attaran, E., Zeier, T. E., Griebel, T., & Zeier, J. (2009). Methyl Salicylate Production and Jasmonate Signaling Are Not Essential for Systemic Acquired Resistance in Arabidopsis. The Plant Cell, 21(3), 954-971. doi:10.1105/tpc.108.063164Yan, J., Zhang, C., Gu, M., Bai, Z., Zhang, W., Qi, T., … Xie, D. (2009). The Arabidopsis CORONATINE INSENSITIVE1 Protein Is a Jasmonate Receptor. The Plant Cell, 21(8), 2220-2236. doi:10.1105/tpc.109.065730Mittal, S. (1995). Role of the Phytotoxin Coronatine in the Infection ofAmbidopsis thalianabyPseudomonas syringaepv.tomato. Molecular Plant-Microbe Interactions, 8(1), 165. doi:10.1094/mpmi-8-0165Genoud, T., & Métraux, J.-P. (1999). Crosstalk in plant cell signaling: structure and function of the genetic network. Trends in Plant Science, 4(12), 503-507. doi:10.1016/s1360-1385(99)01498-3Lawton, K. A., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., … Ryals, J. (1996). Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. The Plant Journal, 10(1), 71-82. doi:10.1046/j.1365-313x.1996.10010071.xFeys, B., Benedetti, C. E., Penfold, C. N., & Turner, J. G. (1994). Arabidopsis Mutants Selected for Resistance to the Phytotoxin Coronatine Are Male Sterile, Insensitive to Methyl Jasmonate, and Resistant to a Bacterial Pathogen. The Plant Cell, 751-759. doi:10.1105/tpc.6.5.751Sun, J., Xu, Y., Ye, S., Jiang, H., Chen, Q., Liu, F., … Li, C. (2009). Arabidopsis ASA1 Is Important for Jasmonate-Mediated Regulation of Auxin Biosynthesis and Transport during Lateral Root Formation. The Plant Cell, 21(5), 1495-1511. doi:10.1105/tpc.108.064303He, Y., Fukushige, H., Hildebrand, D. F., & Gan, S. (2002). Evidence Supporting a Role of Jasmonic Acid in Arabidopsis Leaf Senescence. Plant Physiology, 128(3), 876-884. doi:10.1104/pp.010843Shan, X., Zhang, Y., Peng, W., Wang, Z., & Xie, D. (2009). Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. Journal of Experimental Botany, 60(13), 3849-3860. doi:10.1093/jxb/erp223Yoshida, Y., Sano, R., Wada, T., Takabayashi, J., & Okada, K. (2009). Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development, 136(6), 1039-1048. doi:10.1242/dev.030585Borevitz, J. O., Xia, Y., Blount, J., Dixon, R. A., & Lamb, C. (2000). Activation Tagging Identifies a Conserved MYB Regulator of Phenylpropanoid Biosynthesis. The Plant Cell, 12(12), 2383-2393. doi:10.1105/tpc.12.12.2383Berger, S., Bell, E., Sadka, A., & Mullet, J. E. (1995). Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Molecular Biology, 27(5), 933-942. doi:10.1007/bf00037021Feng, S., Ma, L., Wang, X., Xie, D., Dinesh-Kumar, S. P., Wei, N., & Deng, X. W. (2003). The COP9 Signalosome Interacts Physically with SCFCOI1 and Modulates Jasmonate Responses. The Plant Cell, 15(5), 1083-1094. doi:10.1105/tpc.010207Nawrath C, Métraux JP, Genoud T (2005) Chemical signals in plant resistance: salicylic acid. . In: Tuzun S, Bent E, editors. Multigenic and Induced Systemic Resistance in Plants. Dordrecht, Netherlands.: Springer US. pp. pp. 143–165.Kunkel, B. N., & Brooks, D. M. (2002). Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology, 5(4), 325-331. doi:10.1016/s1369-5266(02)00275-3Truman, W., Bennett, M. H., Kubigsteltig, I., Turnbull, C., & Grant, M. (2007). Arabidopsissystemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proceedings of the National Academy of Sciences, 104(3), 1075-1080. doi:10.1073/pnas.0605423104Canet, J. V., Dobón, A., Ibáñez, F., Perales, L., & Tornero, P. (2010). Resistance and biomass in Arabidopsis: a new model for Salicylic Acid perception. Plant Biotechnology Journal, 8(2), 126-141. doi:10.1111/j.1467-7652.2009.00468.xCasimiro, I., Marchant, A., Bhalerao, R. P., Beeckman, T., Dhooge, S., Swarup, R., … Bennett, M. (2001). Auxin Transport Promotes Arabidopsis Lateral Root Initiation. The Plant Cell, 13(4), 843-852. doi:10.1105/tpc.13.4.843Celenza, J. L., Grisafi, P. L., & Fink, G. R. (1995). A pathway for lateral root formation in Arabidopsis thaliana. Genes & Development, 9(17), 2131-2142. doi:10.1101/gad.9.17.2131Traw, M. B., & Bergelson, J. (2003). Interactive Effects of Jasmonic Acid, Salicylic Acid, and Gibberellin on Induction of Trichomes in Arabidopsis. Plant Physiology, 133(3), 1367-1375. doi:10.1104/pp.103.027086Kloek, A. P., Verbsky, M. L., Sharma, S. B., Schoelz, J. E., Vogel, J., Klessig, D. F., & Kunkel, B. N. (2001). Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. The Plant Journal, 26(5), 509-522. doi:10.1046/j.1365-313x.2001.01050.xXie, D. (1998). COI1: An Arabidopsis Gene Required for Jasmonate-Regulated Defense and Fertility. Science, 280(5366), 1091-1094. doi:10.1126/science.280.5366.1091Ellis, C., & Turner, J. (2002). A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta, 215(4), 549-556. doi:10.1007/s00425-002-0787-4Fernández-Arbaizar, A., Regalado, J. J., & Lorenzo, O. (2011). Isolation and Characterization of Novel Mutant Loci Suppressing the ABA Hypersensitivity of the Arabidopsis coronatine insensitive 1-16 (coi1-16) Mutant During Germination and Seedling Growth. Plant and Cell Physiology, 53(1), 53-63. doi:10.1093/pcp/pcr174He, Y., Chung, E.-H., Hubert, D. A., Tornero, P., & Dangl, J. L. (2012). Specific Missense Alleles of the Arabidopsis Jasmonic Acid Co-Receptor COI1 Regulate Innate Immune Receptor Accumulation and Function. PLoS Genetics, 8(10), e1003018. doi:10.1371/journal.pgen.1003018Xu, L., Liu, F., Lechner, E., Genschik, P., Crosby, W. L., Ma, H., … Xie, D. (2002). The SCFCOI1 Ubiquitin-Ligase Complexes Are Required for Jasmonate Response in Arabidopsis. The Plant Cell, 14(8), 1919-1935. doi:10.1105/tpc.003368Chini, A., Fonseca, S., Fernández, G., Adie, B., Chico, J. M., Lorenzo, O., … Solano, R. (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 448(7154), 666-671. doi:10.1038/nature06006Grunewald, W., Vanholme, B., Pauwels, L., Plovie, E., Inzé, D., Gheysen, G., & Goossens, A. (2009). Expression of the Arabidopsis jasmonate signalling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO reports, 10(8), 923-928. doi:10.1038/embor.2009.103Cao, H., Glazebrook, J., Clarke, J. D., Volko, S., & Dong, X. (1997). The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats. Cell, 88(1), 57-63. doi:10.1016/s0092-8674(00)81858-9Century, K. S., Holub, E. B., & Staskawicz, B. J. (1995). NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proceedings of the National Academy of Sciences, 92(14), 6597-6601. doi:10.1073/pnas.92.14.6597Wildermuth, M. C., Dewdney, J., Wu, G., & Ausubel, F. M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414(6863), 562-565. doi:10.1038/35107108Lu, M., Tang, X., & Zhou, J.-M. (2001). Arabidopsis NHO1 Is Required for General Resistance against Pseudomonas Bacteria. The Plant Cell, 13(2), 437-447. doi:10.1105/tpc.13.2.437Ritter, C., & Dangl, J. L. (1996). Interference between Two Specific Pathogen Recognition Events Mediated by Distinct Plant Disease Resistance Genes. The Plant Cell, 251-257. doi:10.1105/tpc.8.2.251Tornero, P., & Dangl, J. L. (2002). A high-throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana. The Plant Journal, 28(4), 475-481. doi:10.1046/j.1365-313x.2001.01136.xMacho, A. P., Guevara, C. M., Tornero, P., Ruiz-Albert, J., & Beuzón, C. R. (2010). The Pseudomonas syringae effector protein HopZ1a suppresses effector-triggered immunity. New Phytologist, 187(4), 1018-1033. doi:10.1111/j.1469-8137.2010.03381.xTon, J., & Mauch-Mani, B. (2004). β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. The Plant Journal, 38(1), 119-130. doi:10.1111/j.1365-313x.2004.02028.xCANET, J. V., DOBÓN, A., ROIG, A., & TORNERO, P. (2010). Structure-function analysis of npr1 alleles in Arabidopsis reveals a role for its paralogs in the perception of salicylic acid. Plant, Cell & Environment, 33(11), 1911-1922. doi:10.1111/j.1365-3040.2010.02194.xJohnson, C. M., Stout, P. R., Broyer, T. C., & Carlton, A. B. (1957). Comparative chlorine requirements of different plant species. Plant and Soil, 8(4), 337-353. doi:10.1007/bf01666323Dobón, A., Canet, J. V., Perales, L., & Tornero, P. (2011). Quantitative genetic analysis of salicylic acid perception in Arabidopsis. Planta, 234(4), 671-684. doi:10.1007/s00425-011-1436-6Mehrtens, F., Kranz, H., Bednarek, P., & Weisshaar, B. (2005). The Arabidopsis Transcription Factor MYB12 Is a Flavonol-Specific Regulator of Phenylpropanoid Biosynthesis. Plant Physiology, 138(2), 1083-1096. doi:10.1104/pp.104.058032Konieczny, A., & Ausubel, F. M. (1993). A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. The Plant Journal, 4(2), 403-410. doi:10.1046/j.1365-313x.1993.04020403.xBell, C. J., & Ecker, J. R. (1994). Assignment of 30 Microsatellite Loci to the Linkage Map of Arabidopsis. Genomics, 19(1), 137-144. doi:10.1006/geno.1994.1023Swarbreck, D., Wilks, C., Lamesch, P., Berardini, T. Z., Garcia-Hernandez, M., Foerster, H., … Huala, E. (2007). The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Research, 36(Database), D1009-D1014. doi:10.1093/nar/gkm965Jürgens G, Mayer U, Torres Ruiz RA, Berleth T, Mísera S (1991) Genetic analysis of pattern formation in the Arabidopsis embryo. Development (Supplement 1) : 27–38.Huang, W. E., Wang, H., Zheng, H., Huang, L., Singer, A. C., Thompson, I., & Whiteley, A. S. (2005). Chromosomally located gene fusions constructed in Acinetobacter sp. ADP1 for the detection of salicylate. Environmental Microbiology, 7(9), 1339-1348. doi:10.1111/j.1462-5822.2005.00821.xDeFraia, C. T., Schmelz, E. A., & Mou, Z. (2008). A rapid biosensor-based method for quantification of free and glucose-conjugated salicylic acid. Plant Methods, 4(1), 28. doi:10.1186/1746-4811-4-28Chenna, R. (2003). Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research, 31(13), 3497-3500. doi:10.1093/nar/gkg50