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.13220S583596876Albert, 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

WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana

The plant-specific WRKY transcription factor (TF) family with 74 members in Arabidopsis thaliana appears to be involved in the regulation of various physiological processes including plant defence and senescence. WRKY53 and WRKY70 were previously implicated as positive and negative regulators of senescence, respectively. Here the putative function of other WRKY group III proteins in Arabidopsis leaf senescence has been explored and the results suggest the involvement of two additional WRKY TFs, WRKY 54 and WRKY30, in this process. The structurally related WRKY54 and WRKY70 exhibit a similar expression pattern during leaf development and appear to have co-operative and partly redundant functions in senescence, as revealed by single and double mutant studies. These two negative senescence regulators and the positive regulator WRKY53 were shown by yeast two-hydrid analysis to interact independently with WRKY30. WRKY30 was expressed during developmental leaf senescence and consequently it is hypothesized that the corresponding protein could participate in a senescence regulatory network with the other WRKYs. Expression in wild-type and salicylic acid-deficient mutants suggests a common but not exclusive role for SA in induction of WRKY30, 53, 54, and 70 during senescence. WRKY30 and WRKY53 but not WRKY54 and WRKY70 are also responsive to additional signals such as reactive oxygen species. The results suggest that WRKY53, WRKY54, and WRKY70 may participate in a regulatory network that integrates internal and environmental cues to modulate the onset and the progression of leaf senescence, possibly through an interaction with WRKY30

Consolidation of unsaturated seabed around an inserted pile foundation and its effects on the wave-induced momentary liquefaction

YesSeabed consolidation state is one of important factors for evaluating the foundation stability of the marine structures. Most previous studies focused on the seabed consolidation around breakwaters standing on the seabed surface. In this study, a numerical model, based on Biot’s poro-elasticity theory, is developed to investigate the unsaturated seabed consolidation around a nearshore pile foundation, in which the pile inserted depth leads to a different stress distribution. Seabed instabilities of shear failure by the pile self-weight and the potential liquefaction under the dynamic wave loading are also examined. Results indicate that (1) the presence of the inserted pile foundation increases the effective stresses below the foundation, while increases and decreases the effective stresses around the pile foundation for small (de/R3.3) inserted depths, respectively, after seabed consolidation, (2) the aforementioned effects are relatively more significant for small inserted depth, large external loading, and small Young’s modulus, (3) the shear failure mainly occurs around the inserted pile foundation, rather than below the foundation as previously found for the located marine structures, and (4) wave-induced momentary liquefaction near the inserted pile foundation significantly increases with the increase of inserted depth, due to the change of seabed consolidation state.National Natural Science Foundation for Distinguished Young Scholars (51425901), the National Natural Science Foundation of China (51209082, 51209083), the Natural Science Foundation of Jiangsu Province (BK20161509), the Fundamental Research Funds for the Central Universities (2015B15514), Jiangsu Graduate Research and Innovation Plan Grant (#CXLX11_0450) and the 111 project (B12032)

Supportive development of functional tissues for biomedical research using the MINUSHEET(R) perfusion system

Functional tissues generated under in vitro conditions are urgently needed in biomedical research. However, the engineering of tissues is rather difficult, since their development is influenced by numerous parameters. In consequence, a versatile culture system was developed to respond the unmet needs.Optimal adhesion for cells in this system is reached by the selection of individual biomaterials. To protect cells during handling and culture, the biomaterial is mounted onto a MINUSHEET(R) tissue carrier. While adherence of cells takes place in the static environment of a 24 well culture plate, generation of tissues is accomplished in one of several available perfusion culture containers. In the basic version a continuous flow of always fresh culture medium is provided to the developing tissue. In a gradient perfusion culture container epithelia are exposed to different fluids at the luminal and basal sides. Another special container with a transparent lid and base enables microscopic visualization of ongoing tissue development. A further container exhibits a flexible silicone lid to apply force onto the developing tissue thereby mimicking mechanical load that is required for developing connective and muscular tissue. Finally, stem/progenitor cells are kept at the interface of an artificial polyester interstitium within a perfusion culture container offering for example an optimal environment for the spatial development of renal tubules.The system presented here was evaluated by various research groups. As a result a variety of publications including most interesting applications were published. In the present paper these data were reviewed and analyzed. All of the results point out that the cell biological profile of engineered tissues can be strongly improved, when the introduced perfusion culture technique is applied in combination with specific biomaterials supporting primary adhesion of cells