Exposure of plants to low temperature in the light may induce photoinhibitory stress symptoms, including oxidative damage. However, it is also known that light is a critical factor for the development of frost hardiness in cold tolerant plants. In the present work the effects of light during the cold acclimation period were studied in chilling-sensitive maize plants. Before exposure to chilling temperature at 5°C, plants were cold acclimated at non-lethal temperature (15°C) under different light conditions. Although exposure to relatively high light intensities during cold acclimation caused various stress symptoms, it also enhanced the effectiveness of acclimation processes to a subsequent severe cold stress. It seems that the photoinhibition induced by low temperature is a necessary evil for cold acclimation processes in plants. Greater accumulations of soluble sugars were also detected during hardening at relatively high light intensity. Certain stress responses were light-dependent not only in the leaves, but also in the roots. The comparison of the gene expression profiles based on a microarray study demonstrated that the light intensity is at least as important a factor as the temperature during the cold acclimation period. Differentially expressed genes were mainly involved in most of assimilation and metabolic pathways, namely photosynthetic light capture via the modification of chlorophyll biosynthesis and the dark reactions, carboxylic acid metabolism, cellular amino acid, porphyrin or glutathione metabolic processes, ribosome biogenesis and translation. Results revealed complex regulation mechanisms and interactions between cold and light signalling processes.

Centre for Agricultural Research Plant Physiology Department Agricultural Institute MTA Martonvásár Hungary

Department of Plant Physiology and Plant Molecular Biology Eötvös Loránd University Budapest Hungary

Laboratory of Hormonal Regulations in Plants Institute of Experimental Botany Czech Academy of Sciences Prague Czechia

Zobrazit více v PubMed

Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., et al. . (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25, 3389–3402. 10.1093/nar/25.17.3389 PubMed DOI PMC

Anderson M. D., Prasad T. K., Martin B. A., Stewart C. R. (1994). Differential gene expression in chilling-acclimated maize seedlings and evidence for the involvement of abscisic acid in chilling tolerance. Plant Physiol. 105, 331–339. 10.1104/pp.105.1.331 PubMed DOI PMC

Apostol S., Szalai G., Sujbert L., Popova L. P., Janda T. (2006). Non-invasive monitoring of the light-induced cyclic photosynthetic electron flow during cold hardening in wheat leaves. Z. Nat. C. 61, 734–740. 10.1515/znc-2006-9-1021 PubMed DOI

Benjamini Y., Yekutieli D. (2001). The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188. 10.1214/aos/1013699998 DOI

Boldizsár Á., Carrera D. Á., Gulyás Z., Vashegyi I., Novák A., Kalapos B., et al. . (2016a). Comparison of redox and gene expression changes during the vegetative/generative transition in crowns and leaves of wheat chromosome 5A substitution lines at low temperature. J. Appl. Gen. 57, 1–13. 10.1007/s13353-015-0297-2 PubMed DOI

Boldizsár Á., Vankova R., Novák A., Kalapos B., Gulyás Z., Pál M., et al. . (2016b). The mvp2 mutation affects the generative transition through the modification of transcriptome pattern, salicylic acid and cytokinin metabolism in Triticum monococcum. J. Plant Physiol. 202, 21–33. 10.1016/j.jplph.2016.07.005 PubMed DOI

Bredenkamp G. J., Baker N. R. (1994). Temperature-sensitivity of D1 protein metabolism in isolated Zea mays chloroplasts. Plant Cell Environ. 17, 205–210. 10.1111/j.1365-3040.1994.tb00284.x DOI

Catalá R., Medina J., Salinas J. (2011). Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 16475–16480. 10.1073/pnas.1107161108 PubMed DOI PMC

Chrost B., Kolukisaoglu U., Schulz B., Krupinska K. (2007). An alpha-galactosidase with an essential function during leaf development. Planta 225, 311–320. 10.1007/s00425-006-0350-9 PubMed DOI

Foyer C. H., Ruban A. V., Noctor G. (2017). Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem. J. 474, 877–883. 10.1042/BCJ20160814 PubMed DOI PMC

Fracheboud Y., Jompuk C., Ribaut J.-M., Stamp P., Leipner J. (2004). Genetic analysis of cold-tolerance of photosynthesis in maize. Plant Mol. Biol. 56, 241–253. 10.1007/s11103-004-3353-6 PubMed DOI

Gill S. S., Tuteja N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909–930. 10.1016/j.plaphy.2010.08.016 PubMed DOI

Gómez M., González A., Sáez C. A., Morales B., Moenne A. (2015). Copper-induced activation of TRP channels promotes extracellular calcium entry, activation of CaMs and CDPKs, copper entry and membrane depolarization in Ulva compressa. Front. Plant Sci. 6:182. 10.3389/fpls.2015.00182 PubMed DOI PMC

Gondor O. K., Janda T., Soós V., Pál M., Majláth I., Adak M. K., et al. . (2016a). Salicylic acid induction of flavonoid biosynthesis pathways in wheat varies by treatment. Front. Plant Sci. 7:1447. 10.3389/fpls.2016.01447 PubMed DOI PMC

Gondor O. K., Szalai G., Kovács V., Janda T., Pál M. (2016b). Relationship between polyamines and other cold-induced response mechanisms in different cereal species. J. Agr. Crop Sci. 202, 217–230. 10.1111/jac.12144 DOI

Gray G. R., Chauvin L. P., Sarhan F., Huner N. (1997). Cold acclimation and freezing tolerance (a complex interaction of light and temperature). Plant Physiol. 114, 467–474. 10.1104/pp.114.2.467 PubMed DOI PMC

Greaves J. A. (1996). Improving suboptimal temperature tolerance in maize - the search for variation. J. Exp. Bot. 47, 307–323. 10.1093/jxb/47.3.307 DOI

Grimaud F., Renaut J., Dumont E., Sergeant K., Lucau-Danila A., Blervacq A. S., et al. . (2013). Exploring chloroplastic changes related to chilling and freezing tolerance during cold acclimation of pea (Pisum sativum L.). J. Prot. 80, 145–159. 10.1016/j.jprot.2012.12.030 PubMed DOI

Gururani M. A., Venkatesh J., Tran L. S. P. (2015). Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol. Plant 8, 1304–1320. 10.1016/j.molp.2015.05.005 PubMed DOI

Hammer R., Harper D. A. T., Ryan P. D. (2001). PAST: paleontological statistics software package for education and data analysis. Pal. Electr. 4, 1–9.

Heberle H., Meirelles G. V., da Silva F. R., Telles G. P., Minghim R. (2015). InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics 16:169. 10.1186/s12859-015-0611-3 PubMed DOI PMC

Janda T., Majláth I., Szalai G. (2014). Interaction of temperature and light in the development of freezing tolerance in plants. J. Plant Growth Regul. 33, 460–469. 10.1007/s00344-013-9381-1 DOI

Janda T., Szalai G., Ducruet J.-M., Páldi E. (1998). Changes in photosynthesis in inbred maize lines with different degrees of chilling tolerance grown at optimum and suboptimum temperatures. Photosynthetica 35, 205–212. 10.1023/A:1006954605631 DOI

Janda T., Szalai G., Kissimon J., Páldi E., Marton C., Szigeti Z. (1994). Role of irradiance in the chilling injury of young maize plants studied by chlorophyll fluorescence induction measurements. Photosynthetica 30, 293–299.

Khatri N., Mudgil Y. (2015). Hypothesis: NDL proteins function in stress responses by regulating microtubule organization. Front. Plant Sci. 6:947. 10.3389/fpls.2015.00947 PubMed DOI PMC

Klughammer C., Schreiber U. (2008). Saturation pulse method for assessment of energy conversion in PS I. PAM Appl. Notes 1, 11–14.

Kocsy G. (2015). Die or survive? Redox changes as seed viability markers. Plant Cell Environ. 38, 1008–1010. 10.1111/pce.12515 PubMed DOI

Lazár D. (2015). Parameters of photosynthetic energy partitioning. J. Plant Physiol. 175, 131–147. 10.1016/j.jplph.2014.10.021 PubMed DOI

Lee C. M., Thomashow M. F. (2012). Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 109, 15054–15059. 10.1073/pnas.1211295109 PubMed DOI PMC

Legris M., Klose C., Costigliolo C., Burgie E., Neme M., Hiltbrunner A., et al. . (2016). Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354, 897–900. 10.1126/science.aaf5656 PubMed DOI

Legris M., Nieto C., Sellaro R., Prat S., Casal J. J. (2017). Perception and signalling of light and temperature cues in plants. Plant J. 90, 683–697. 10.1111/tpj.13467 PubMed DOI

Li Z., Hu G., Liu X., Zhou Y., Li Y., Zhang X., et al. . (2016). Transcriptome sequencing identified genes and gene ontologies associated with early freezing tolerance in maize. Front. Plant Sci. 7:1477. 10.3389/fpls.2016.01477 PubMed DOI PMC

Liu Y., Ji X., Zheng L., Nie X., Wang Y. (2013). Microarray analysis of transcriptional responses to abscisic acid and salt stress in Arabidopsis thaliana. Int. J. Mol. Sci. 14, 9979–9998. 10.3390/ijms14059979 PubMed DOI PMC

Livak K. J., Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔCT) method. Methods 25, 402–408. 10.1006/meth.2001.1262 PubMed DOI

Long S. P., East T. M., Baker N. R. (1983). Chilling damage to photosynthesis in young Zea mays I. effects of light and temperature variation on photosynthetic CO2 assimilation. J. Exp. Bot. 34, 177–188. 10.1093/jxb/34.2.177 DOI

Marocco A., Lorenzoni C., Fracheboud Y. (2005). Chilling stress in maize. Maydica 50, 571–580.

Mohanty S., Grimm B., Tripathy B. C. (2006). Light and dark modulation of chlorophyll biosynthetic genes in response to temperature. Planta 224, 692–699. 10.1007/s00425-006-0248-6 PubMed DOI

Mudunuri U., Che A., Yi M., Stephens R. M. (2009). bioDBnet: the biological database network. Bioinformatics 25, 555–556. 10.1093/bioinformatics/btn654 PubMed DOI PMC

Pál M., Horváth E., Janda T., Páldi E., Szalai G. (2005). Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays L.) plants. Physiol. Plant. 125, 356–364. 10.1111/j.1399-3054.2005.00545.x DOI

Pál M., Janda T., Szalai G. (2011). Abscisic acid may alter the salicylic acid-related abiotic stress response in maize. J. Agr. Crop Sci. 197, 368–377. 10.1111/j.1439-037X.2011.00474.x DOI

Pospíšil P. (2016). Production of reactive oxygen species by Photosystem II as a response to light and temperature stress. Front. Plant Sci. 7:1950. 10.3389/fpls.2016.01950 PubMed DOI PMC

Prasad T. K. (1996). Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activity. Plant J. 10, 1017–1026. 10.1046/j.1365-313X.1996.10061017.x DOI

Sobkowiak A., Jónczyk M., Adamczyk J., Solecka D., Kuciara I., Hetmanczyk K., et al. . (2016). Molecular foundations of chilling-tolerance of modern maize. BMC Genomics 17:125. 10.1186/s12864-016-2453-4 PubMed DOI PMC

Sobkowiak A., Jonczyk M., Jarochowska E., Biecek P., Trzcinska-Danielewicz J., Leipner J., et al. . (2014). Genome-wide transcriptomic analysis of response to low temperature reveals candidate genes determining divergent cold-sensitivity of maize inbred lines. Plant Mol. Biol. 85, 317–331. 10.1007/s11103-014-0187-8 PubMed DOI PMC

Song Y., Diao Q., Qi H. (2015). Polyamine metabolism and biosynthetic genes expression in tomato (Lycopersicon esculentum Mill.) seedlings during cold acclimation. Plant Growth Regul. 75, 21–32. 10.1007/s10725-014-9928-6 DOI

Szalai G., Janda T., Bartók T., Páldi E. (1997). Role of light in changes in free amino acid and polyamine contents at chilling temperature in maize (Zea mays L.). Physiol. Plant. 101, 434–438.

Szalai G., Janda T., Páldi E., Szigeti Z. (1996). Role of light in the development of post-chilling symptoms in maize. J. Plant Physiol. 148, 378–383. 10.1016/S0176-1617(96)80269-0 DOI

Thimm O., Blasing O., Gibon Y., Nagel A., Meyer S., Kruger P., et al. . (2004). MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914–939. 10.1111/j.1365-313X.2004.02016.x PubMed DOI

Thomashow M. F. (1999). Plant cold acclimation. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50, 571–599. 10.1146/annurev.arplant.50.1.571 PubMed DOI

Tian Y.-H., Yuan H.-F., Xie J., Deng J.-W., Dao X.-S., Zheng Y.-L. (2016). Effect of diurnal irradiance on night-chilling tolerance of six rubber cultivars. Photosynthetica 54, 374–380. 10.1007/s11099-016-0192-z DOI

Tian T., Liu Y., Yan H., You Q., Yi X., Du Z., et al. . (2017). agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 45, W122–W129. 10.1093/nar/gkx382 PubMed DOI PMC

Trzcinska-Danielewicz J., Bilska A., Fronk J., Zielenkiewicz P., Jarochowska E., Roszczyk M., et al. (2009). Global analysis of gene expression in maize leaves treated with low temperature I. moderate chilling (14 °C). Plant Sci. 177, 648–658. 10.1016/j.plantsci.2009.09.001 DOI

Van Buskirk H. A., Thomashow M. F. (2006). Arabidopsis transcription factors regulating cold acclimation. Physiol. Plant. 126, 72–80. 10.1111/j.1399-3054.2006.00625.x DOI

Wallsgrove R. M., Keys A. J., Lea P. J., Miflin B. J. (1983). Photosynthesis, photorespiration and nitrogen metabolism. Plant Cell Environ. 6, 310–309.

Wanner L. A., Junttila O. (1999). Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 120, 391–400. 10.1104/pp.120.2.391 PubMed DOI PMC

Winfield M. O., Lu C., Wilson I. D., Coghill J. A., Edwards K. J. (2010). Plant responses to cold: transcriptome analysis of wheat. Plant Biotech. J. 8, 749–771. 10.1111/j.1467-7652.2010.00536.x PubMed DOI

Zhang L., Xiao S., Chen Y. J., Xu H., Li Y. G., Zhang Y. W., et al. (2017). Ozone sensitivity of four Pakchoi cultivars with different leaf colors: physiological and biochemical mechanisms. Photosynthetica 55, 478–490. 10.1007/s11099-016-0661-4 DOI

Crosstalk between Light- and Temperature-Mediated Processes under Cold and Heat Stress Conditions in Plants

Temperature and Light-Quality-Dependent Regulation of Freezing Tolerance in Barley