Nitric oxide deficiency decreases C-repeat binding factor-dependent and -independent induction of cold acclimation

[EN] Plant tolerance to freezing temperatures is governed by endogenous components and environmental factors. Exposure to low non-freezing temperatures is a key factor in the induction of freezing tolerance in the process called cold acclimation. The role of nitric oxide (NO) in cold acclimation was explored in Arabidopsis using triple nia1nia2noa1-2 mutants that are impaired in the nitrate-dependent and nitrate-independent pathways of NO production, and are thus NO deficient. Here, we demonstrate that cold-induced NO accumulation is required to promote the full cold acclimation response through C-repeat Binding Factor (CBF)-dependent gene expression, as well as the CBF-independent expression of other cold-responsive genes such as Oxidation-Related Zinc Finger 2 (ZF/OZF2). NO deficiency also altered abscisic acid perception and signaling and the cold-induced production of anthocyanins, which are additional factors involved in cold acclimation.We thank Isabel Lopez-Diaz and Esther Carrera for the hormone quantification carried out at the Plant Hormone Quantification Service, IBMCP, Valencia, Spain. This work was supported by grants from MINECO of Spain Government and FEDER EU funds [BIO2014-56067-P, BIO2017-82945-P to JL and BIO2016-79187-R to JS].Costa-Broseta, Á.; Perea-Resa, C.; Castillo, M.; Ruíz, MF.; Salinas, J.; Leon Ramos, J. (2019). Nitric oxide deficiency decreases C-repeat binding factor-dependent and -independent induction of cold acclimation. Journal of Experimental Botany. 70(12):3283-3296. https://doi.org/10.1093/jxb/erz115328332967012Adams, S., & Carré, I. A. (2011). Downstream of the plant circadian clock: output pathways for the control of physiology and development. Essays in Biochemistry, 49, 53-69. doi:10.1042/bse0490053Arakawa, T., & Timasheff, S. N. (1982). Stabilization of protein structure by sugars. Biochemistry, 21(25), 6536-6544. doi:10.1021/bi00268a033Astier, J., & Lindermayr, C. (2012). Nitric Oxide-Dependent Posttranslational Modification in Plants: An Update. International Journal of Molecular Sciences, 13(12), 15193-15208. doi:10.3390/ijms131115193Atamian, H. S., & Harmer, S. L. (2016). Circadian regulation of hormone signaling and plant physiology. Plant Molecular Biology, 91(6), 691-702. doi:10.1007/s11103-016-0477-4Barrero-Gil, J., & Salinas, J. (2013). Post-translational regulation of cold acclimation response. Plant Science, 205-206, 48-54. doi:10.1016/j.plantsci.2013.01.008Borevitz, 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.12.12.2383Cantrel, C., Vazquez, T., Puyaubert, J., Rezé, N., Lesch, M., Kaiser, W. M., … Baudouin, E. (2010). Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytologist, 189(2), 415-427. doi:10.1111/j.1469-8137.2010.03500.xCastillo, M. C., & León, J. (2008). Expression of the β-oxidation gene 3-ketoacyl-CoA thiolase 2 (KAT2) is required for the timely onset of natural and dark-induced leaf senescence in Arabidopsis. Journal of Experimental Botany, 59(8), 2171-2179. doi:10.1093/jxb/ern079Castillo, M.-C., Lozano-Juste, J., González-Guzmán, M., Rodriguez, L., Rodriguez, P. L., & León, J. (2015). Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Science Signaling, 8(392), ra89-ra89. doi:10.1126/scisignal.aaa7981Catala, R., Medina, J., & Salinas, J. (2011). Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proceedings of the National Academy of Sciences, 108(39), 16475-16480. doi:10.1073/pnas.1107161108Chen, M., & Thelen, J. J. (2016). Acyl-lipid desaturase 1primes cold acclimation response inArabidopsis. Physiologia Plantarum, 158(1), 11-22. doi:10.1111/ppl.12448Costa-Broseta, Á., Perea-Resa, C., Castillo, M.-C., Ruíz, M. F., Salinas, J., & León, J. (2018). Nitric Oxide Controls Constitutive Freezing Tolerance in Arabidopsis by Attenuating the Levels of Osmoprotectants, Stress-Related Hormones and Anthocyanins. Scientific Reports, 8(1). doi:10.1038/s41598-018-27668-8Cuevas, J. C., López-Cobollo, R., Alcázar, R., Zarza, X., Koncz, C., Altabella, T., … Ferrando, A. (2008). Putrescine Is Involved in Arabidopsis Freezing Tolerance and Cold Acclimation by Regulating Abscisic Acid Levels in Response to Low Temperature. Plant Physiology, 148(2), 1094-1105. doi:10.1104/pp.108.122945Diaz, C., Saliba-Colombani, V., Loudet, O., Belluomo, P., Moreau, L., Daniel-Vedele, F., … Masclaux-Daubresse, C. (2006). Leaf Yellowing and Anthocyanin Accumulation are Two Genetically Independent Strategies in Response to Nitrogen Limitation in Arabidopsis thaliana. Plant and Cell Physiology, 47(1), 74-83. doi:10.1093/pcp/pci225Eremina, M., Unterholzner, S. J., Rathnayake, A. I., Castellanos, M., Khan, M., Kugler, K. G., … Poppenberger, B. (2016). Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants. Proceedings of the National Academy of Sciences, 113(40), E5982-E5991. doi:10.1073/pnas.1611477113Fan, J., Chen, K., Amombo, E., Hu, Z., Chen, L., & Fu, J. (2015). Physiological and Molecular Mechanism of Nitric Oxide (NO) Involved in Bermudagrass Response to Cold Stress. PLOS ONE, 10(7), e0132991. doi:10.1371/journal.pone.0132991Guo, F.-Q. (2003). Identification of a Plant Nitric Oxide Synthase Gene Involved in Hormonal Signaling. Science, 302(5642), 100-103. doi:10.1126/science.1086770Hannah, M. A., Heyer, A. G., & Hincha, D. K. (2005). A Global Survey of Gene Regulation during Cold Acclimation in Arabidopsis thaliana. PLoS Genetics, 1(2), e26. doi:10.1371/journal.pgen.0010026Igamberdiev, A. U., Ratcliffe, R. G., & Gupta, K. J. (2014). Plant mitochondria: Source and target for nitric oxide. Mitochondrion, 19, 329-333. doi:10.1016/j.mito.2014.02.003Jensen, M. K., Lindemose, S., de Masi, F., Reimer, J. J., Nielsen, M., Perera, V., … Skriver, K. (2013). ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Bio, 3(1), 321-327. doi:10.1016/j.fob.2013.07.006Jeon, J., Kim, N. Y., Kim, S., Kang, N. Y., Novák, O., Ku, S.-J., … Kim, J. (2010). A Subset of Cytokinin Two-component Signaling System Plays a Role in Cold Temperature Stress Response in Arabidopsis. Journal of Biological Chemistry, 285(30), 23371-23386. doi:10.1074/jbc.m109.096644Kakei, Y., & Shimada, Y. (2014). AtCAST3.0 Update: A Web-Based Tool for Analysis of Transcriptome Data by Searching Similarities in Gene Expression Profiles. Plant and Cell Physiology, 56(1), e7-e7. doi:10.1093/pcp/pcu174Krol, M., Gray, G. R., Huner, N. P. A., Hurry, V. M., Öquist, G., & Malek, L. (1995). Low-temperature stress and photoperiod affect an increased tolerance to photoinhibition in Pinus banksiana seedlings. Canadian Journal of Botany, 73(8), 1119-1127. doi:10.1139/b95-122Lee, H. G., & Seo, P. J. (2015). The MYB 96– HHP module integrates cold and abscisic acid signaling to activate the CBF – COR pathway in Arabidopsis. The Plant Journal, 82(6), 962-977. doi:10.1111/tpj.12866León, J., Castillo, M. C., Coego, A., Lozano-Juste, J., & Mir, R. (2013). Diverse functional interactions between nitric oxide and abscisic acid in plant development and responses to stress. Journal of Experimental Botany, 65(4), 907-921. doi:10.1093/jxb/ert454Li, D., Li, Y., Zhang, L., Wang, X., Zhao, Z., Tao, Z., … Yang, Y. (2014). Arabidopsis ABA Receptor RCAR1/PYL9 Interacts with an R2R3-Type MYB Transcription Factor, AtMYB44. International Journal of Molecular Sciences, 15(5), 8473-8490. doi:10.3390/ijms15058473Lozano-Juste, J., Colom-Moreno, R., & León, J. (2011). In vivo protein tyrosine nitration in Arabidopsis thaliana. Journal of Experimental Botany, 62(10), 3501-3517. doi:10.1093/jxb/err042Lozano-Juste, J., & León, J. (2009). Enhanced Abscisic Acid-Mediated Responses in nia1nia2noa1-2 Triple Mutant Impaired in NIA/NR- and AtNOA1-Dependent Nitric Oxide Biosynthesis in Arabidopsis. Plant Physiology, 152(2), 891-903. doi:10.1104/pp.109.148023Morishita, T., Kojima, Y., Maruta, T., Nishizawa-Yokoi, A., Yabuta, Y., & Shigeoka, S. (2009). Arabidopsis NAC Transcription Factor, ANAC078, Regulates Flavonoid Biosynthesis under High-light. Plant and Cell Physiology, 50(12), 2210-2222. doi:10.1093/pcp/pcp159Nakashima, K., Yamaguchi-Shinozaki, K., & Shinozaki, K. (2014). The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Frontiers in Plant Science, 5. doi:10.3389/fpls.2014.00170Park, S., Lee, C.-M., Doherty, C. J., Gilmour, S. J., Kim, Y., & Thomashow, M. F. (2015). Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network. The Plant Journal, 82(2), 193-207. doi:10.1111/tpj.12796Perea-Resa, C., Rodríguez-Milla, M. A., Iniesto, E., Rubio, V., & Salinas, J. (2017). Prefoldins Negatively Regulate Cold Acclimation in Arabidopsis thaliana by Promoting Nuclear Proteasome-Mediated HY5 Degradation. Molecular Plant, 10(6), 791-804. doi:10.1016/j.molp.2017.03.012Persak, H., & Pitzschke, A. (2014). Dominant Repression by Arabidopsis Transcription Factor MYB44 Causes Oxidative Damage and Hypersensitivity to Abiotic Stress. International Journal of Molecular Sciences, 15(2), 2517-2537. doi:10.3390/ijms15022517Petroni, K., & Tonelli, C. (2011). Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Science, 181(3), 219-229. doi:10.1016/j.plantsci.2011.05.009PUYAUBERT, J., & BAUDOUIN, E. (2014). New clues for a cold case: nitric oxide response to low temperature. Plant, Cell & Environment, 37(12), 2623-2630. doi:10.1111/pce.12329Rahman, A. (2012). Auxin: a regulator of cold stress response. Physiologia Plantarum, 147(1), 28-35. doi:10.1111/j.1399-3054.2012.01617.xResponses of Poplar to Chilling Temperatures: Proteomic and Physiological Aspects. (2004). Plant Biology, 6(1), 81-90. doi:10.1055/s-2004-815733Reyes-Diaz, M., Ulloa, N., Zuniga-Feest, A., Gutierrez, A., Gidekel, M., Alberdi, M., … Bravo, L. A. (2006). Arabidopsis thaliana avoids freezing by supercooling. Journal of Experimental Botany, 57(14), 3687-3696. doi:10.1093/jxb/erl125Richter, R., Bastakis, E., & Schwechheimer, C. (2013). Cross-Repressive Interactions between SOC1 and the GATAs GNC and GNL/CGA1 in the Control of Greening, Cold Tolerance, and Flowering Time in Arabidopsis. Plant Physiology, 162(4), 1992-2004. doi:10.1104/pp.113.219238Rubin, G., Tohge, T., Matsuda, F., Saito, K., & Scheible, W.-R. (2009). Members of the LBD Family of Transcription Factors Repress Anthocyanin Synthesis and Affect Additional Nitrogen Responses in Arabidopsis. The Plant Cell, 21(11), 3567-3584. doi:10.1105/tpc.109.067041Schulz, E., Tohge, T., Zuther, E., Fernie, A. R., & Hincha, D. K. (2016). Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana. Scientific Reports, 6(1). doi:10.1038/srep34027Seo, 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_7Shi, Y., Ding, Y., & Yang, S. (2018). Molecular Regulation of CBF Signaling in Cold Acclimation. Trends in Plant Science, 23(7), 623-637. doi:10.1016/j.tplants.2018.04.002Solfanelli, C., Poggi, A., Loreti, E., Alpi, A., & Perata, P. (2005). Sucrose-Specific Induction of the Anthocyanin Biosynthetic Pathway in Arabidopsis. Plant Physiology, 140(2), 637-646. doi:10.1104/pp.105.072579Soubeyrand, E., Basteau, C., Hilbert, G., van Leeuwen, C., Delrot, S., & Gomès, E. (2014). Nitrogen supply affects anthocyanin biosynthetic and regulatory genes in grapevine cv. Cabernet-Sauvignon berries. Phytochemistry, 103, 38-49. doi:10.1016/j.phytochem.2014.03.024Takahashi, D., Kawamura, Y., & Uemura, M. (2016). Cold acclimation is accompanied by complex responses of glycosylphosphatidylinositol (GPI)-anchored proteins in Arabidopsis. Journal of Experimental Botany, 67(17), 5203-5215. doi:10.1093/jxb/erw279Thomashow, M. F. (1999). PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology, 50(1), 571-599. doi:10.1146/annurev.arplant.50.1.571Wang, X., Bian, Y., Cheng, K., Zou, H., Sun, S. S.-M., & He, J.-X. (2012). A Comprehensive Differential Proteomic Study of Nitrate Deprivation inArabidopsisReveals Complex Regulatory Networks of Plant Nitrogen Responses. Journal of Proteome Research, 11(4), 2301-2315. doi:10.1021/pr2010764Weiser, C. J. (1970). Cold Resistance and Injury in Woody Plants: Knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science, 169(3952), 1269-1278. doi:10.1126/science.169.3952.1269Zhai, H., Bai, X., Zhu, Y., Li, Y., Cai, H., Ji, W., … Li, J. (2010). A single-repeat R3-MYB transcription factor MYBC1 negatively regulates freezing tolerance in Arabidopsis. Biochemical and Biophysical Research Communications, 394(4), 1018-1023. doi:10.1016/j.bbrc.2010.03.114Zhao, M.-G., Chen, L., Zhang, L.-L., & Zhang, W.-H. (2009). Nitric Reductase-Dependent Nitric Oxide Production Is Involved in Cold Acclimation and Freezing Tolerance in Arabidopsis. Plant Physiology, 151(2), 755-767. doi:10.1104/pp.109.140996Zhao, R., Sheng, J., Lv, S., Zheng, Y., Zhang, J., Yu, M., & Shen, L. (2011). Nitric oxide participates in the regulation of LeCBF1 gene expression and improves cold tolerance in harvested tomato fruit. Postharvest Biology and Technology, 62(2), 121-126. doi:10.1016/j.postharvbio.2011.05.01