Arabidopsis COGWHEEL1 links light perception and gibberellins with seed tolerance to deterioration

[ES] Significance Statement Seed tolerance to deterioration depends on anti-aging defenses only partially understood. COG1 encodes a transcription factor previously described to attenuate phytochrome responses to light and we found that it is a positive regulator of seed tolerance to deterioration while light perception by phytochromes is negative. The proposed mechanism is that COG1 increases gibberellins levels, leading to a seed coat containing more suberin and less permeable to oxygen. Light is known to inhibit gibberellins action.This work was supported by grant BIO2014-52621-R from the Spanish 'Ministerio de Economia y Competitividad', Madrid. We thank the 'Servicio de Cuantificacion de Hormonas Vegetales' of our institute for the determination of GA, ABA and auxin.Bueso Ródenas, E.; Muñoz Bertomeu, J.; Campos, F.; Martínez-Ortuño, CJ.; Tello Lacal, C.; Martínez-Almonacid, I.; Ballester Fuentes, P.... (2016). Arabidopsis COGWHEEL1 links light perception and gibberellins with seed tolerance to deterioration. The Plant Journal. 87(6):583-596. https://doi.org/10.1111/tpj.13220583596876Albert, S., Delseny, M., & Devic, M. (1997). BANYULS, a novel negative regulator of flavonoid biosynthesis in the Arabidopsis seed coat. The Plant Journal, 11(2), 289-299. doi:10.1046/j.1365-313x.1997.11020289.xAlejandro, S., Rodríguez, P. L., Bellés, J. M., Yenush, L., García-Sanchez, M. J., Fernández, J. A., & Serrano, R. (2007). An Arabidopsis quiescin-sulfhydryl oxidase regulates cation homeostasis at the root symplast–xylem interface. The EMBO Journal, 26(13), 3203-3215. doi:10.1038/sj.emboj.7601757Arsovski, A. A., Haughn, G. W., & Western, T. L. (2010). Seed coat mucilage cells ofArabidopsis thalianaas a model for plant cell wall research. Plant Signaling & Behavior, 5(7), 796-801. doi:10.4161/psb.5.7.11773Bailly, C. (2004). Active oxygen species and antioxidants in seed biology. Seed Science Research, 14(2), 93-107. doi:10.1079/ssr2004159Beisson, F., Li, Y., Bonaventure, G., Pollard, M., & Ohlrogge, J. B. (2007). The Acyltransferase GPAT5 Is Required for the Synthesis of Suberin in Seed Coat and Root of Arabidopsis. The Plant Cell, 19(1), 351-368. doi:10.1105/tpc.106.048033Bernard, V., Lecharny, A., & Brunaud, V. (2010). Improved detection of motifs with preferential location in promoters. Genome, 53(9), 739-752. doi:10.1139/g10-042Berridge, M. V., Herst, P. M., & Tan, A. S. (2005). Tetrazolium dyes as tools in cell biology: New insights into their cellular reduction. Biotechnology Annual Review, 127-152. doi:10.1016/s1387-2656(05)11004-7BRAYBROOK, S., & HARADA, J. (2008). LECs go crazy in embryo development. Trends in Plant Science, 13(12), 624-630. doi:10.1016/j.tplants.2008.09.008Brazma, A., Hingamp, P., Quackenbush, J., Sherlock, G., Spellman, P., Stoeckert, C., … Vingron, M. (2001). Minimum information about a microarray experiment (MIAME)—toward standards for microarray data. Nature Genetics, 29(4), 365-371. doi:10.1038/ng1201-365Brundrett, M. C., Kendrick, B., & Peterson, C. A. (1991). Efficient Lipid Staining in Plant Material with Sudan Red 7B or Fluoral Yellow 088 in Polyethylene Glycol-Glycerol. Biotechnic & Histochemistry, 66(3), 111-116. doi:10.3109/10520299109110562Bueso, E., Muñoz-Bertomeu, J., Campos, F., Brunaud, V., Martínez, L., Sayas, E., … Serrano, R. (2013). ARABIDOPSIS THALIANA HOMEOBOX25 Uncovers a Role for Gibberellins in Seed Longevity. Plant Physiology, 164(2), 999-1010. doi:10.1104/pp.113.232223Bueso, E., Ibañez, C., Sayas, E., Muñoz-Bertomeu, J., Gonzalez-Guzmán, M., Rodriguez, P. L., & Serrano, R. (2014). A forward genetic approach in Arabidopsis thaliana identifies a RING-type ubiquitin ligase as a novel determinant of seed longevity. Plant Science, 215-216, 110-116. doi:10.1016/j.plantsci.2013.11.004Chandler, J. W., Abrams, S. R., & Bartels, D. (1997). The effect of ABA analogs on callus viability and gene expression in Craterostigma plantagineum. Physiologia Plantarum, 99(3), 465-469. doi:10.1034/j.1399-3054.1997.990315.xChâtelain, E., Satour, P., Laugier, E., Ly Vu, B., Payet, N., Rey, P., & Montrichard, F. (2013). Evidence for participation of the methionine sulfoxide reductase repair system in plant seed longevity. Proceedings of the National Academy of Sciences, 110(9), 3633-3638. doi:10.1073/pnas.1220589110Chen, H., Chu, P., Zhou, Y., Li, Y., Liu, J., Ding, Y., … Huang, S. (2012). Overexpression of AtOGG1, a DNA glycosylase/AP lyase, enhances seed longevity and abiotic stress tolerance in Arabidopsis. Journal of Experimental Botany, 63(11), 4107-4121. doi:10.1093/jxb/ers093Clerkx, E. J. M., Blankestijn-De Vries, H., Ruys, G. J., Groot, S. P. C., & Koornneef, M. (2004). Genetic differences in seed longevity of various Arabidopsis mutants. Physiologia Plantarum, 121(3), 448-461. doi:10.1111/j.0031-9317.2004.00339.xCurtis, M. D., & Grossniklaus, U. (2003). A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta. Plant Physiology, 133(2), 462-469. doi:10.1104/pp.103.027979De Simone, O., Haase, K., Müller, E., Junk, W. J., Hartmann, K., Schreiber, L., & Schmidt, W. (2003). Apoplasmic Barriers and Oxygen Transport Properties of Hypodermal Cell Walls in Roots from Four Amazonian Tree Species. Plant Physiology, 132(1), 206-217. doi:10.1104/pp.102.014902Debeaujon, I., Léon-Kloosterziel, K. M., & Koornneef, M. (2000). Influence of the Testa on Seed Dormancy, Germination, and Longevity in Arabidopsis. Plant Physiology, 122(2), 403-414. doi:10.1104/pp.122.2.403Domergue, F., Vishwanath, S. J., Joubès, J., Ono, J., Lee, J. A., Bourdon, M., … Rowland, O. (2010). Three Arabidopsis Fatty Acyl-Coenzyme A Reductases, FAR1, FAR4, and FAR5, Generate Primary Fatty Alcohols Associated with Suberin Deposition. Plant Physiology, 153(4), 1539-1554. doi:10.1104/pp.110.158238Espley, R. V., Brendolise, C., Chagné, D., Kutty-Amma, S., Green, S., Volz, R., … Allan, A. C. (2009). Multiple Repeats of a Promoter Segment Causes Transcription Factor Autoregulation in Red Apples. The Plant Cell, 21(1), 168-183. doi:10.1105/tpc.108.059329Farrant, J. M., & Moore, J. P. (2011). Programming desiccation-tolerance: from plants to seeds to resurrection plants. Current Opinion in Plant Biology, 14(3), 340-345. doi:10.1016/j.pbi.2011.03.018Fornara, F., Panigrahi, K. C. S., Gissot, L., Sauerbrunn, N., Rühl, M., Jarillo, J. A., & Coupland, G. (2009). Arabidopsis DOF Transcription Factors Act Redundantly to Reduce CONSTANS Expression and Are Essential for a Photoperiodic Flowering Response. Developmental Cell, 17(1), 75-86. doi:10.1016/j.devcel.2009.06.015Gutierrez, L., Van Wuytswinkel, O., Castelain, M., & Bellini, C. (2007). Combined networks regulating seed maturation. Trends in Plant Science, 12(7), 294-300. doi:10.1016/j.tplants.2007.06.003Hajdu, A., Ádám, É., Sheerin, D. J., Dobos, O., Bernula, P., Hiltbrunner, A., … Nagy, F. (2015). High-level expression and phosphorylation of phytochrome B modulates flowering time in Arabidopsis. The Plant Journal, 83(5), 794-805. doi:10.1111/tpj.12926Haughn, G., & Chaudhury, A. (2005). Genetic analysis of seed coat development in Arabidopsis. Trends in Plant Science, 10(10), 472-477. doi:10.1016/j.tplants.2005.08.005He, H., de Souza Vidigal, D., Snoek, L. B., Schnabel, S., Nijveen, H., Hilhorst, H., & Bentsink, L. (2014). Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis. Journal of Experimental Botany, 65(22), 6603-6615. doi:10.1093/jxb/eru378Hedden, P., & Thomas, S. G. (2012). Gibberellin biosynthesis and its regulation. Biochemical Journal, 444(1), 11-25. doi:10.1042/bj20120245Hellens, R., Allan, A., Friel, E., Bolitho, K., Grafton, K., Templeton, M., … Laing, W. (2005). Plant Methods, 1(1), 13. doi:10.1186/1746-4811-1-13Hoekstra, F. A., Golovina, E. A., & Buitink, J. (2001). Mechanisms of plant desiccation tolerance. Trends in Plant Science, 6(9), 431-438. doi:10.1016/s1360-1385(01)02052-0Holdsworth, M., Kurup, S., & MKibbin, R. (1999). Molecular and genetic mechanisms regulating the transition from embryo development to germination. Trends in Plant Science, 4(7), 275-280. doi:10.1016/s1360-1385(99)01429-6Hu, J., Mitchum, M. G., Barnaby, N., Ayele, B. T., Ogawa, M., Nam, E., … Sun, T. (2008). Potential Sites of Bioactive Gibberellin Production during Reproductive Growth in Arabidopsis. The Plant Cell, 20(2), 320-336. doi:10.1105/tpc.107.057752Hudson, M. E., & Quail, P. H. (2003). Identification of Promoter Motifs Involved in the Network of Phytochrome A-Regulated Gene Expression by Combined Analysis of Genomic Sequence and Microarray Data. Plant Physiology, 133(4), 1605-1616. doi:10.1104/pp.103.030437Jofuku, K. D., den Boer, B. G., Van Montagu, M., & Okamuro, J. K. (1994). Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. The Plant Cell, 6(9), 1211-1225. doi:10.1105/tpc.6.9.1211Kim, Y.-C., Nakajima, M., Nakayama, A., & Yamaguchi, I. (2005). Contribution of Gibberellins to the Formation of Arabidopsis Seed Coat Through Starch Degradation. Plant and Cell Physiology, 46(8), 1317-1325. doi:10.1093/pcp/pci141Kotak, S., Vierling, E., Bäumlein, H., & Koskull-Döring, P. von. (2007). A Novel Transcriptional Cascade Regulating Expression of Heat Stress Proteins during Seed Development of Arabidopsis. The Plant Cell, 19(1), 182-195. doi:10.1105/tpc.106.048165Le, B. H., Cheng, C., Bui, A. Q., Wagmaister, J. A., Henry, K. F., Pelletier, J., … Goldberg, R. B. (2010). Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proceedings of the National Academy of Sciences, 107(18), 8063-8070. doi:10.1073/pnas.1003530107Leivar, P., & Quail, P. H. (2011). PIFs: pivotal components in a cellular signaling hub. Trends in Plant Science, 16(1), 19-28. doi:10.1016/j.tplants.2010.08.003Liu, L.-J., Zhang, Y.-C., Li, Q.-H., Sang, Y., Mao, J., Lian, H.-L., … Yang, H.-Q. (2008). COP1-Mediated Ubiquitination of CONSTANS Is Implicated in Cryptochrome Regulation of Flowering in Arabidopsis. The Plant Cell, 20(2), 292-306. doi:10.1105/tpc.107.057281De Lucas, M., & Prat, S. (2014). PIFs get BRright: PHYTOCHROME INTERACTING FACTORs as integrators of light and hormonal signals. New Phytologist, 202(4), 1126-1141. doi:10.1111/nph.12725Molina, I., Ohlrogge, J. B., & Pollard, M. (2007). Deposition and localization of lipid polyester in developing seeds of Brassica napus and Arabidopsis thaliana. The Plant Journal, 53(3), 437-449. doi:10.1111/j.1365-313x.2007.03348.xNesi, N., Debeaujon, I., Jond, C., Stewart, A. J., Jenkins, G. I., Caboche, M., & Lepiniec, L. (2002). The TRANSPARENT TESTA16 Locus Encodes the ARABIDOPSIS BSISTER MADS Domain Protein and Is Required for Proper Development and Pigmentation of the Seed Coat. The Plant Cell, 14(10), 2463-2479. doi:10.1105/tpc.004127Ogé, L., Bourdais, G., Bove, J., Collet, B., Godin, B., Granier, F., … Grappin, P. (2008). Protein Repair l-Isoaspartyl Methyltransferase1 Is Involved in Both Seed Longevity and Germination Vigor in Arabidopsis. The Plant Cell, 20(11), 3022-3037. doi:10.1105/tpc.108.058479Ó’Maoiléidigh, D. S., Graciet, E., & Wellmer, F. (2013). Gene networks controllingArabidopsis thalianaflower development. New Phytologist, 201(1), 16-30. doi:10.1111/nph.12444Parcy, F., Valon, C., Kohara, A., Miséra, S., & Giraudat, J. (1997). The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. The Plant Cell, 9(8), 1265-1277. doi:10.1105/tpc.9.8.1265Park, D. H., Lim, P. O., Kim, J. S., Cho, D. S., Hong, S. H., & Nam, H. G. (2003). The Arabidopsis COG1 gene encodes a Dof domain transcription factor and negatively regulates phytochrome signaling. The Plant Journal, 34(2), 161-171. doi:10.1046/j.1365-313x.2003.01710.xPi, L., Aichinger, E., van der Graaff, E., Llavata-Peris, C. I., Weijers, D., Hennig, L., … Laux, T. (2015). Organizer-Derived WOX5 Signal Maintains Root Columella Stem Cells through Chromatin-Mediated Repression of CDF4 Expression. Developmental Cell, 33(5), 576-588. doi:10.1016/j.devcel.2015.04.024Pollard, M., Beisson, F., Li, Y., & Ohlrogge, J. B. (2008). Building lipid barriers: biosynthesis of cutin and suberin. Trends in Plant Science, 13(5), 236-246. doi:10.1016/j.tplants.2008.03.003Puig, J., Pauluzzi, G., Guiderdoni, E., & Gantet, P. (2012). Regulation of Shoot and Root Development through Mutual Signaling. Molecular Plant, 5(5), 974-983. doi:10.1093/mp/sss047Rajjou, L., & Debeaujon, I. (2008). Seed longevity: Survival and maintenance of high germination ability of dry seeds. Comptes Rendus Biologies, 331(10), 796-805. doi:10.1016/j.crvi.2008.07.021Riechmann, J. L., Heard, J., Martin, G., Reuber, L., -Z., C., Jiang, … -L. Yu, G. (2000). Arabidopsis Transcription Factors: Genome-Wide Comparative Analysis Among Eukaryotes. Science, 290(5499), 2105-2110. doi:10.1126/science.290.5499.2105Sano, N., Rajjou, L., North, H. M., Debeaujon, I., Marion-Poll, A., & Seo, M. (2015). Staying Alive: Molecular Aspects of Seed Longevity. Plant and Cell Physiology, 57(4), 660-674. doi:10.1093/pcp/pcv186Santos-Mendoza, M., Dubreucq, B., Baud, S., Parcy, F., Caboche, M., & Lepiniec, L. (2008). Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. The Plant Journal, 54(4), 608-620. doi:10.1111/j.1365-313x.2008.03461.xSattler, S. E., Gilliland, L. U., Magallanes-Lundback, M., Pollard, M., & DellaPenna, D. (2004). Vitamin E Is Essential for Seed Longevity and for Preventing Lipid Peroxidation during Germination. The Plant Cell, 16(6), 1419-1432. doi:10.1105/tpc.021360Schwab, R., Ossowski, S., Riester, M., Warthmann, N., & Weigel, D. (2006). Highly Specific Gene Silencing by Artificial MicroRNAs in Arabidopsis. The Plant Cell, 18(5), 1121-1133. doi:10.1105/tpc.105.039834Seo, M., Jikumaru, Y., & Kamiya, Y. (2011). Profiling of Hormones and Related Metabolites in Seed Dormancy and Germination Studies. Methods in Molecular Biology, 99-111. doi:10.1007/978-1-61779-231-1_7Shigeto, J., Kiyonaga, Y., Fujita, K., Kondo, R., & Tsutsumi, Y. (2013). Putative Cationic Cell-Wall-Bound Peroxidase Homologues in Arabidopsis, AtPrx2, AtPrx25, and AtPrx71, Are Involved in Lignification. Journal of Agricultural and Food Chemistry, 61(16), 3781-3788. doi:10.1021/jf400426gSparks, E., Wachsman, G., & Benfey, P. N. (2013). Spatiotemporal signalling in plant development. Nature Reviews Genetics, 14(9), 631-644. doi:10.1038/nrg3541Suzuki, M., & McCarty, D. R. (2008). Functional symmetry of the B3 network controlling seed development. Current Opinion in Plant Biology, 11(5), 548-553. doi:10.1016/j.pbi.2008.06.015Tan, Q. K.-G., & Irish, V. F. (2006). The Arabidopsis Zinc Finger-Homeodomain Genes Encode Proteins with Unique Biochemical Properties That Are Coordinately Expressed during Floral Development. Plant Physiology, 140(3), 1095-1108. doi:10.1104/pp.105.070565Ülker, B., & Somssich, I. E. (2004). WRKY transcription factors: from DNA binding towards biological function. Current Opinion in Plant Biology, 7(5), 491-498. doi:10.1016/j.pbi.2004.07.012Wachsman, G., Sparks, E. E., & Benfey, P. N. (2015). Genes and networks regulating root anatomy and architecture. New Phytologist, 208(1), 26-38. doi:10.1111/nph.13469Weigel, D., Ahn, J. H., Blázquez, M. A., Borevitz, J. O., Christensen, S. K., Fankhauser, C., … Chory, J. (2000). Activation Tagging in Arabidopsis. Plant Physiology, 122(4), 1003-1014. doi:10.1104/pp.122.4.1003Western, T. L., Young, D. S., Dean, G. H., Tan, W. L., Samuels, A. L., & Haughn, G. W. (2003). MUCILAGE-MODIFIED4 Encodes a Putative Pectin Biosynthetic Enzyme Developmentally Regulated by APETALA2, TRANSPARENT TESTA GLABRA1, and GLABRA2 in the Arabidopsis Seed Coat. Plant Physiology, 134(1), 296-306. doi:10.1104/pp.103.035519Xu, H., Wei, Y., Zhu, Y., Lian, L., Xie, H., Cai, Q., … Zhang, J. (2014). Antisense suppression ofLOX3gene expression in rice endosperm enhances seed longevity. Plant Biotechnology Journal, 13(4), 526-539. doi:10.1111/pbi.12277Yamaguchi-Shinozaki, K., & Shinozaki, K. (2005). Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends in Plant Science, 10(2), 88-94. doi:10.1016/j.tplants.2004.12.012Yanagisawa, S. (2002). The Dof family of plant transcription factors. Trends in Plant Science, 7(12), 555-560. doi:10.1016/s1360-1385(02)02362-2Zhang, C., Mallery, E. L., Schlueter, J., Huang, S., Fan, Y., Brankle, S., … Szymanski, D. B. (2008). Arabidopsis SCARs Function Interchangeably to Meet Actin-Related Protein 2/3 Activation Thresholds during Morphogenesis. The Plant Cell, 20(4), 995-1011. doi:10.1105/tpc.107.05535