{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T08:09:07Z","timestamp":1791619747729,"version":"4.3.4"},"reference-count":110,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2021,1,20]],"date-time":"2021-01-20T00:00:00Z","timestamp":1611100800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004442","name":"Narodowym Centrum Nauki","doi-asserted-by":"publisher","award":["Opus15 project (2018\/29\/B\/NZ3\/01198)"],"award-info":[{"award-number":["Opus15 project (2018\/29\/B\/NZ3\/01198)"]}],"id":[{"id":"10.13039\/501100004442","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003130","name":"FWO","doi-asserted-by":"publisher","award":["grant 3G006916"],"award-info":[{"award-number":["grant 3G006916"]}],"id":[{"id":"10.13039\/501100003130","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Phototropins are plasma membrane-associated photoreceptors of blue light and UV-A\/B radiation. The Arabidopsis thaliana genome encodes two phototropins, PHOT1 and PHOT2, that mediate phototropism, chloroplast positioning, and stomatal opening. They are well characterized in terms of photomorphogenetic processes, but so far, little was known about their involvement in photosynthesis, oxidative stress responses, and cell death. By analyzing phot1, phot2 single, and phot1phot2 double mutants, we demonstrated that both phototropins influence the photochemical and non-photochemical reactions, photosynthetic pigments composition, stomata conductance, and water-use efficiency. After oxidative stress caused by UV-C treatment, phot1 and phot2 single and double mutants showed a significantly reduced accumulation of H2O2 and more efficient photosynthetic electron transport compared to the wild type. However, all phot mutants exhibited higher levels of cell death four days after UV-C treatment, as well as deregulated gene expression. Taken together, our results reveal that on the one hand, both phot1 and phot2 contribute to the inhibition of UV-C-induced foliar cell death, but on the other hand, they also contribute to the maintenance of foliar H2O2 levels and optimal intensity of photochemical reactions and non-photochemical quenching after an exposure to UV-C stress. Our data indicate a novel role for phototropins in the condition-dependent optimization of photosynthesis, growth, and water-use efficiency as well as oxidative stress and cell death response after UV-C exposure.<\/jats:p>","DOI":"10.3390\/cells10020200","type":"journal-article","created":{"date-parts":[[2021,1,20]],"date-time":"2021-01-20T12:16:18Z","timestamp":1611144978000},"page":"200","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":30,"title":["Phototropin 1 and 2 Influence Photosynthesis, UV-C Induced Photooxidative Stress Responses, and Cell Death"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9677-4614","authenticated-orcid":false,"given":"Anna","family":"Rusaczonek","sequence":"first","affiliation":[{"name":"Department of Botany, Institute of Biology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland"},{"name":"Department of Plant Genetics, Breeding and Biotechnology, Institute of Biology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4062-0370","authenticated-orcid":false,"given":"Weronika","family":"Czarnocka","sequence":"additional","affiliation":[{"name":"Department of Botany, Institute of Biology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland"},{"name":"Department of Plant Genetics, Breeding and Biotechnology, Institute of Biology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4667-2294","authenticated-orcid":false,"given":"Patrick","family":"Willems","sequence":"additional","affiliation":[{"name":"Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium"},{"name":"VIB Center of Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5234-2008","authenticated-orcid":false,"given":"Marzena","family":"Sujkowska-Rybkowska","sequence":"additional","affiliation":[{"name":"Department of Botany, Institute of Biology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3147-0860","authenticated-orcid":false,"given":"Frank","family":"Van Breusegem","sequence":"additional","affiliation":[{"name":"Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium"},{"name":"VIB Center of Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4328-1207","authenticated-orcid":false,"given":"Stanis\u0142aw","family":"Karpi\u0144ski","sequence":"additional","affiliation":[{"name":"Department of Plant Genetics, Breeding and Biotechnology, Institute of Biology, Warsaw University of Life Sciences, Nowoursynowska 159, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"8494","DOI":"10.1021\/bi047518q","article-title":"Two-Step Mechanism of Photodamage to Photosystem II: Step 1 Occurs at the Oxygen-Evolving Complex and Step 2 Occurs at the Photochemical Reaction Center","volume":"44","author":"Ohnishi","year":"2005","journal-title":"Biochemistry"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1111\/pce.12288","article-title":"Lesion Simulating Disease 1 and Enhanced Disease Susceptibility 1 Differentially Regulate UV-C-Induced Photooxidative Stress Signalling and Programmed Cell Death in Arabidopsis thaliana","volume":"38","author":"Sobczak","year":"2015","journal-title":"Plant Cell Environ."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1124","DOI":"10.3389\/fpls.2020.01124","article-title":"Novel Role of JAC1 in Influencing Photosynthesis, Stomatal Conductance, and Photooxidative Stress Signalling Pathway in Arabidopsis thaliana","volume":"11","author":"Czarnocka","year":"2020","journal-title":"Front. Plant Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1111\/pce.12018","article-title":"Light Acclimation, Retrograde Signalling, Cell Death and Immune Defences in Plants","volume":"36","author":"Burdiak","year":"2013","journal-title":"Plant Cell Environ."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/j.freeradbiomed.2018.01.011","article-title":"Friend or Foe? Reactive Oxygen Species Production, Scavenging and Signaling in Plant Response to Environmental Stresses","volume":"122","author":"Czarnocka","year":"2018","journal-title":"Free Radic. Biol. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.tplants.2017.11.007","article-title":"Coping with \u201cDark Sides of the Sun\u201d through Photoreceptor Signaling","volume":"23","author":"Demarsy","year":"2018","journal-title":"Trends Plant Sci."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Czarnocka, W., Fichman, Y., Bernacki, M., R\u00f3\u017ca\u0144ska, E., Sa\u0144ko-Sawczenko, I., Mittler, R., and Karpi\u0144ski, S. (2020). FMO1 Is Involved in Excess Light Stress-Induced Signal Transduction and Cell Death Signaling. Cells, 9.","DOI":"10.3390\/cells9102163"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1606","DOI":"10.1104\/pp.16.00434","article-title":"ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants","volume":"171","author":"Gilroy","year":"2016","journal-title":"Plant Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Wituszy\u0144ska, W., and Karpi\u0144ski, S. (2013). Programmed Cell Death as a Response to High Light, UV and Drought Stress in Plants. Abiotic Stress Plant Responses Appl. Agric.","DOI":"10.5772\/53127"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/s11120-018-0482-3","article-title":"Linking Chloroplast Relocation to Different Responses of Photosynthesis to Blue and Red Radiation in Low and High Light-Acclimated Leaves of Arabidopsis thaliana (L.)","volume":"137","author":"Latouche","year":"2018","journal-title":"Photosynth. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1515\/BC.2007.118","article-title":"Chloroplast Photorelocation Movement Mediated by Phototropin Family Proteins in Green Plants","volume":"388","author":"Suetsugu","year":"2007","journal-title":"Biol. Chem."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/s10265-016-0783-6","article-title":"Molecular Mechanism of Phototropin Light Signaling","volume":"129","author":"Okajima","year":"2016","journal-title":"J. Plant Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1007\/s11120-020-00736-9","article-title":"Chloroplast Avoidance Movement: A Novel Paradigm of ROS Signalling","volume":"144","author":"Majumdar","year":"2020","journal-title":"Photosynth. Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"6969","DOI":"10.1073\/pnas.101137598","article-title":"Arabidopsis Nph1 and Npl1: Blue Light Receptors That Mediate Both Phototropism and Chloroplast Relocation","volume":"98","author":"Sakai","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1038\/414656a","article-title":"Phot1 and Phot2 Mediate Blue Light Regulation of Stomatal Opening","volume":"414","author":"Kinoshita","year":"2001","journal-title":"Nature"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1071\/FP19053","article-title":"Contributions of Cryptochromes and Phototropins to Stomatal Opening through the Day","volume":"47","author":"Wang","year":"2020","journal-title":"Funct. Plant Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1723","DOI":"10.1105\/tpc.003293","article-title":"Cellular and Subcellular Localization of Phototropin 1","volume":"14","author":"Sakamoto","year":"2002","journal-title":"Plant Cell"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/mp\/ssm001","article-title":"Leaf Positioning of Arabidopsis in Response to Blue Light","volume":"1","author":"Inoue","year":"2008","journal-title":"Mol. Plant"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1105\/tpc.12.2.225","article-title":"RPT2. A Signal Transducer of the Phototropic Response in Arabidopsis","volume":"12","author":"Sakai","year":"2000","journal-title":"Plant Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1464","DOI":"10.1104\/pp.103.024372","article-title":"Primary Inhibition of Hypocotyl Growth and Phototropism Depend Differently on Phototropin-Mediated Increases in Cytoplasmic Calcium Induced by Blue Light","volume":"133","author":"Folta","year":"2003","journal-title":"Plant Physiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1111\/plb.12187","article-title":"The Blue Light Receptor Phototropin 1 Suppresses Lateral Root Growth by Controlling Cell Elongation","volume":"17","author":"Moni","year":"2015","journal-title":"Plant Biol. Stuttg. Ger."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2138","DOI":"10.1126\/science.291.5511.2138","article-title":"Arabidopsis NPL1: A Phototropin Homolog Controlling the Chloroplast High-Light Avoidance Response","volume":"291","author":"Kagawa","year":"2001","journal-title":"Science"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1291","DOI":"10.1093\/pcp\/pcm095","article-title":"Blue Light-Dependent Nuclear Positioning in Arabidopsis thaliana Leaf Cells","volume":"48","author":"Iwabuchi","year":"2007","journal-title":"Plant Cell Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1104\/pp.002410","article-title":"Photochemical Properties of the Flavin Mononucleotide-Binding Domains of the Phototropins from Arabidopsis, Rice, and Chlamydomonas reinhardtii","volume":"129","author":"Kasahara","year":"2002","journal-title":"Plant Physiol."},{"key":"ref_25","first-page":"215","article-title":"Repressor of Ultraviolet-B Photomorphogenesis Function Allows Efficient Phototropin Mediated Ultraviolet-B Phototropism in Etiolated Seedlings","volume":"252","author":"Vanhaelewyn","year":"2016","journal-title":"Plant Sci. Int. J. Exp. Plant Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3226","DOI":"10.1105\/tpc.109.067876","article-title":"Domain Swapping to Assess the Mechanistic Basis of Arabidopsis Phototropin 1 Receptor Kinase Activation and Endocytosis by Blue Light","volume":"21","author":"Kaiserli","year":"2009","journal-title":"Plant Cell"},{"key":"ref_27","first-page":"1158","article-title":"Signaling Mechanisms of LOV Domains: New Insights from Molecular Dynamics Studies","volume":"12","author":"Freddolino","year":"2013","journal-title":"Photochem. Photobiol. Sci. Off. J. Eur. Photochem. Assoc. Eur. Soc. Photobiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.bbapap.2007.09.010","article-title":"Molecular Structure and Regulation of Phototropin Kinase by Blue Light","volume":"1784","author":"Tokutomi","year":"2008","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"14881","DOI":"10.1021\/bi0485530","article-title":"Light-Induced Structural Changes of LOV Domain-Containing Polypeptides from Arabidopsis Phototropin 1 and 2 Studied by Small-Angle X-ray Scattering","volume":"43","author":"Nakasako","year":"2004","journal-title":"Biochemistry"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5626","DOI":"10.1073\/pnas.0709189105","article-title":"Blue Light-Induced Autophosphorylation of Phototropin Is a Primary Step for Signaling","volume":"105","author":"Inoue","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1104\/pp.111.175943","article-title":"Functional Analyses of the Activation Loop of Phototropin2 in Arabidopsis","volume":"156","author":"Inoue","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1093\/pcp\/pci104","article-title":"Biochemical Characterization of Plasma Membrane H+-ATPase Activation in Guard Cell Protoplasts of Arabidopsis thaliana in Response to Blue Light","volume":"46","author":"Ueno","year":"2005","journal-title":"Plant Cell Physiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3684","DOI":"10.1105\/tpc.111.085852","article-title":"Tissue-Autonomous Promotion of Palisade Cell Development by Phototropin 2 in Arabidopsis","volume":"23","author":"Kozuka","year":"2011","journal-title":"Plant Cell"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1007\/s11120-010-9580-6","article-title":"Light, Genotype, and Abscisic Acid Affect Chloroplast Positioning in Guard Cells of Arabidopsis thaliana Leaves in Distinct Ways","volume":"105","author":"Jessen","year":"2010","journal-title":"Photosynth. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"994","DOI":"10.1111\/j.1365-313X.2006.02667.x","article-title":"Blue Light-Induced Association of Phototropin 2 with the Golgi Apparatus","volume":"45","author":"Kong","year":"2006","journal-title":"Plant J. Cell Mol. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1093\/pcp\/pcs151","article-title":"Both Phototropin 1 and 2 Localize on the Chloroplast Outer Membrane with Distinct Localization Activity","volume":"54","author":"Kong","year":"2013","journal-title":"Plant Cell Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1093\/mp\/ssm011","article-title":"The Subcellular Localization and Blue-Light-Induced Movement of Phototropin 1-GFP in Etiolated Seedlings of Arabidopsis thaliana","volume":"1","author":"Wan","year":"2008","journal-title":"Mol. Plant"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3627","DOI":"10.1105\/tpc.111.087999","article-title":"Modulation of Phototropic Responsiveness in Arabidopsis through Ubiquitination of Phototropin 1 by the CUL3-Ring E3 Ubiquitin Ligase CRL3(NPH3)","volume":"23","author":"Roberts","year":"2011","journal-title":"Plant Cell"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3263","DOI":"10.1093\/jxb\/eru172","article-title":"Blue-Light-Activated Phototropin2 Trafficking from the Cytoplasm to Golgi\/Post-Golgi Vesicles","volume":"65","author":"Aggarwal","year":"2014","journal-title":"J. Exp. Bot."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"13106","DOI":"10.1073\/pnas.0906250106","article-title":"Short Actin-Based Mechanism for Light-Directed Chloroplast Movement in Arabidopsis","volume":"106","author":"Kadota","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.1104\/pp.18.00484","article-title":"Chloroplast Accumulation Response Enhances Leaf Photosynthesis and Plant Biomass Production","volume":"178","author":"Gotoh","year":"2018","journal-title":"Plant Physiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1038\/nature01213","article-title":"Chloroplast Avoidance Movement Reduces Photodamage in Plants","volume":"420","author":"Kasahara","year":"2002","journal-title":"Nature"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1422","DOI":"10.1093\/pcp\/pcr087","article-title":"Red Light, Phot1 and JAC1 Modulate Phot2-Dependent Reorganization of Chloroplast Actin Filaments and Chloroplast Avoidance Movement","volume":"52","author":"Ichikawa","year":"2011","journal-title":"Plant Cell Physiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"387","DOI":"10.2183\/pjab.92.387","article-title":"Chloroplast and Nuclear Photorelocation Movements","volume":"92","author":"Wada","year":"2016","journal-title":"Proc. Jpn. Acad. Ser. B Phys. Biol. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e1041","DOI":"10.21769\/BioProtoc.1041","article-title":"Determination of Water Use Efficiency for Arabidopsis thaliana","volume":"4","author":"Wituszynska","year":"2014","journal-title":"Bio-Protoc"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/j.jplph.2012.11.016","article-title":"Multivariable Environmental Conditions Promote Photosynthetic Adaptation Potential in Arabidopsis thaliana","volume":"170","author":"Rusaczonek","year":"2013","journal-title":"J. Plant Physiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1146\/annurev.arplant.59.032607.092759","article-title":"Chlorophyll Fluorescence: A Probe of Photosynthesis in Vivo","volume":"59","author":"Baker","year":"2008","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"6679","DOI":"10.1093\/jxb\/erv375","article-title":"Role of Phytochromes A and B in the Regulation of Cell Death and Acclimatory Responses to UV Stress in Arabidopsis thaliana","volume":"66","author":"Rusaczonek","year":"2015","journal-title":"J. Exp. Bot."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"6553","DOI":"10.1073\/pnas.96.11.6553","article-title":"Hydrogen Peroxide Is Generated Systemically in Plant Leaves by Wounding and Systemin via the Octadecanoid Pathway","volume":"96","author":"Ryan","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1104\/pp.124.2.609","article-title":"Ethylene Induces Epidermal Cell Death at the Site of Adventitious Root Emergence in Rice","volume":"124","author":"Mergemann","year":"2000","journal-title":"Plant Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"420747","DOI":"10.1155\/2008\/420747","article-title":"Genevestigator v3: A Reference Expression Database for the Meta-Analysis of Transcriptomes","volume":"2008","author":"Hruz","year":"2008","journal-title":"Adv. Bioinforma."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/S0304-3940(02)01423-4","article-title":"Assumption-Free Analysis of Quantitative Real-Time Polymerase Chain Reaction (PCR) Data","volume":"339","author":"Ramakers","year":"2003","journal-title":"Neurosci. Lett."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"e36","DOI":"10.1093\/nar\/30.9.e36","article-title":"Relative Expression Software Tool (REST) for Group-Wise Comparison and Statistical Analysis of Relative Expression Results in Real-Time PCR","volume":"30","author":"Pfaffl","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: Ultrafast Universal RNA-Seq Aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinforma. Oxf. Engl."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1111\/tpj.13415","article-title":"Araport11: A Complete Reannotation of the Arabidopsis thaliana Reference Genome","volume":"89","author":"Cheng","year":"2017","journal-title":"Plant J. Cell Mol. Biol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","article-title":"FeatureCounts: An Efficient General Purpose Program for Assigning Sequence Reads to Genomic Features","volume":"30","author":"Liao","year":"2014","journal-title":"Bioinforma. Oxf. Engl."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"EdgeR: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data","volume":"26","author":"Robinson","year":"2010","journal-title":"Bioinform. Oxf. Engl."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2010-11-3-r25","article-title":"A Scaling Normalization Method for Differential Expression Analysis of RNA-Seq Data","volume":"11","author":"Robinson","year":"2010","journal-title":"Genome Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"4288","DOI":"10.1093\/nar\/gks042","article-title":"Differential Expression Analysis of Multifactor RNA-Seq Experiments with Respect to Biological Variation","volume":"40","author":"McCarthy","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. Ser. B Methodol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"D1003","DOI":"10.1093\/nar\/gku1200","article-title":"Araport: The Arabidopsis Information Portal","volume":"43","author":"Krishnakumar","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1111\/j.1365-313X.2004.02016.x","article-title":"Mapman: A User-Driven Tool to Display Genomics Data Sets onto Diagrams of Metabolic Pathways and Other Biological Processes","volume":"37","author":"Thimm","year":"2004","journal-title":"Plant J. Cell Mol. Biol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1111\/pce.13686","article-title":"Photosystem II 22kDa Protein Level\u2014A Prerequisite for Excess Light-Inducible Memory, Cross-Tolerance to UV-C and Regulation of Electrical Signalling","volume":"43","author":"Lewandowska","year":"2020","journal-title":"Plant Cell Environ."},{"key":"ref_64","unstructured":"Lichtenthaler, H.K. (1988). The measurement of Rfd-values as plant vitality indices with the portable field chlorophyll fluorometer and the pam-fluorometer. Applications of Chlorophyll Fluorescence in Photosynthesis Research, Stress Physiology, Hydrobiology and Remote Sensing: An Introduction to the Various Fields of Applications of the In Vivo Chlorophyll Fluorescence also Including the Proceedings of the First International Chlorophyll Fluorescence Symposium Held in the Physikzentrum, Bad Honnef, F.R.G., 6\u20138 June 1998, Springer."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Pillitteri, L.J., and Dong, J. (2013). Stomatal Development in Arabidopsis. Arab. Book Am. Soc. Plant Biol., 11.","DOI":"10.1199\/tab.0162"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1365","DOI":"10.1093\/mp\/ssu072","article-title":"Salicylic Acid Signaling Controls the Maturation and Localization of the Arabidopsis Defense Protein Accelerated Cell Death6","volume":"7","author":"Zhang","year":"2014","journal-title":"Mol. Plant"},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Wrzaczek, M., Brosch\u00e9, M., Saloj\u00e4rvi, J., Kangasj\u00e4rvi, S., Id\u00e4nheimo, N., Mersmann, S., Robatzek, S., Karpi\u0144ski, S., Karpi\u0144ska, B., and Kangasj\u00e4rvi, J. (2010). Transcriptional Regulation of the CRK\/DUF26 Group of Receptor-like Protein Kinases by Ozone and Plant Hormones in Arabidopsis. BMC Plant Biol., 10.","DOI":"10.1186\/1471-2229-10-95"},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Bourdais, G., Burdiak, P., Gauthier, A., Nitsch, L., Saloj\u00e4rvi, J., Rayapuram, C., Id\u00e4nheimo, N., Hunter, K., Kimura, S., and Merilo, E. (2015). Large-Scale Phenomics Identifies Primary and Fine-Tuning Roles for CRKs in Responses Related to Oxidative Stress. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1005373"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1146\/annurev.phyto.44.070505.143425","article-title":"Significance of Inducible Defense-Related Proteins in Infected Plants","volume":"44","author":"Rep","year":"2006","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/j.tplants.2004.02.004","article-title":"Plant Actin-Related Proteins","volume":"9","author":"Kandasamy","year":"2004","journal-title":"Trends Plant Sci."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.plaphy.2013.04.009","article-title":"Overexpression of TsGOLS2, a Galactinol Synthase, in Arabidopsis thaliana Enhances Tolerance to High Salinity and Osmotic Stresses","volume":"69","author":"Sun","year":"2013","journal-title":"Plant Physiol. Biochem."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"477","DOI":"10.14348\/molcells.2016.0027","article-title":"Overexpression of Heat Shock Factor Gene HsfA3 Increases Galactinol Levels and Oxidative Stress Tolerance in Arabidopsis","volume":"39","author":"Song","year":"2016","journal-title":"Mol. Cells"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1465","DOI":"10.1111\/pbi.12731","article-title":"Overexpression of an Arabidopsis thaliana Galactinol Synthase Gene Improves Drought Tolerance in Transgenic Rice and Increased Grain Yield in the Field","volume":"15","author":"Selvaraj","year":"2017","journal-title":"Plant Biotechnol. J."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1111\/j.1365-313X.2006.02723.x","article-title":"AtNAP, a NAC Family Transcription Factor, Has an Important Role in Leaf Senescence","volume":"46","author":"Guo","year":"2006","journal-title":"Plant J. Cell Mol. Biol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1007\/s00425-016-2609-0","article-title":"Arabidopsis AtNAP Functions as a Negative Regulator via Repression of AREB1 in Salt Stress Response","volume":"245","author":"Seok","year":"2017","journal-title":"Planta"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s00299-019-02474-2","article-title":"NAP Is Involved in GA-Mediated Chlorophyll Degradation and Leaf Senescence by Interacting with DELLAs in Arabidopsis","volume":"39","author":"Lei","year":"2020","journal-title":"Plant Cell Rep."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"2584","DOI":"10.1016\/j.febslet.2013.06.038","article-title":"Suppression of Arabidopsis RING E3 Ubiquitin Ligase AtATL78 Increases Tolerance to Cold Stress and Decreases Tolerance to Drought Stress","volume":"587","author":"Kim","year":"2013","journal-title":"FEBS Lett."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.bbrc.2015.11.061","article-title":"Arabidopsis T\u00f3xicos En Levadura 78 (AtATL78) Mediates ABA-Dependent ROS Signaling in Response to Drought Stress","volume":"469","author":"Suh","year":"2016","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1438-8677.2010.00377.x","article-title":"Transitions of Gene Expression Induced by Short-Term Blue Light","volume":"13","author":"Lehmann","year":"2011","journal-title":"Plant Biol. Stuttg. Ger."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., and van Wijk, K.J. (2008). Sorting Signals, N-Terminal Modifications and Abundance of the Chloroplast Proteome. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0001994"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1007\/s00299-016-1991-1","article-title":"The Role of ANAC072 in the Regulation of Chlorophyll Degradation during Age- and Dark-Induced Leaf Senescence","volume":"35","author":"Li","year":"2016","journal-title":"Plant Cell Rep."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1543","DOI":"10.1111\/nph.15127","article-title":"Transcription Factor RD26 Is a Key Regulator of Metabolic Reprogramming during Dark-Induced Senescence","volume":"218","author":"Kamranfar","year":"2018","journal-title":"New Phytol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1198","DOI":"10.1074\/mcp.M600429-MCP200","article-title":"Quantitative Phosphoproteomics of Early Elicitor Signaling in Arabidopsis","volume":"6","author":"Benschop","year":"2007","journal-title":"Mol. Cell. Proteomics"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1104\/pp.108.124875","article-title":"Enhanced Tolerance to Oxidative Stress in Transgenic Arabidopsis Plants Expressing Proteins of Unknown Function","volume":"148","author":"Luhua","year":"2008","journal-title":"Plant Physiol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1093\/jxb\/erm289","article-title":"Impact of Chloroplastic- and Extracellular-Sourced ROS on High Light-Responsive Gene Expression in Arabidopsis","volume":"59","author":"Bechtold","year":"2008","journal-title":"J. Exp. Bot."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1120","DOI":"10.1105\/tpc.104.030049","article-title":"Phototropins Promote Plant Growth in Response to Blue Light in Low Light Environments","volume":"17","author":"Takemiya","year":"2005","journal-title":"Plant Cell"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1007\/s00425-007-0599-7","article-title":"Distinct Leaf Developmental and Gene Expression Responses to Light Quantity Depend on Blue-Photoreceptor or Plastid-Derived Signals, and Can Occur in the Absence of Phototropins","volume":"227","author":"Bowyer","year":"2007","journal-title":"Planta"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1093\/mp\/ssm017","article-title":"In Vivo Phosphorylation Site Mapping and Functional Characterization of Arabidopsis Phototropin 1","volume":"1","author":"Sullivan","year":"2008","journal-title":"Mol. Plant"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1093\/pcp\/pcs094","article-title":"Role of RPT2 in Leaf Positioning and Flattening and a Possible Inhibition of Phot2 Signaling by Phot1","volume":"54","author":"Harada","year":"2013","journal-title":"Plant Cell Physiol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"12550","DOI":"10.1073\/pnas.1902915116","article-title":"Engineering the Phototropin Photocycle Improves Photoreceptor Performance and Plant Biomass Production","volume":"116","author":"Hart","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1146\/annurev.arplant.57.032905.105434","article-title":"Light Regulation of Stomatal Movement","volume":"58","author":"Shimazaki","year":"2007","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1093\/pcp\/pcv180","article-title":"Reconstitution of an Initial Step of Phototropin Signaling in Stomatal Guard Cells","volume":"57","author":"Takemiya","year":"2016","journal-title":"Plant Cell Physiol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1475","DOI":"10.1104\/pp.111.187237","article-title":"Phototropins but Not Cryptochromes Mediate the Blue Light-Specific Promotion of Stomatal Conductance, While Both Enhance Photosynthesis and Transpiration under Full Sunlight","volume":"158","author":"Boccalandro","year":"2012","journal-title":"Plant Physiol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1104\/pp.19.01528","article-title":"Guard Cells Integrate Light and Temperature Signals to Control Stomatal Aperture","volume":"182","author":"Kostaki","year":"2020","journal-title":"Plant Physiol."},{"key":"ref_95","unstructured":"Bacon, M.A. (2004). Molecular approaches to unravel the genetic basis of water use efficiency. Water Use Efficiency in Plant Biology, Blackwell Publishing."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1016\/j.jplph.2009.12.015","article-title":"Photoprotective Function of Chloroplast Avoidance Movement: In Vivo Chlorophyll Fluorescence Study","volume":"167","author":"Sztatelman","year":"2010","journal-title":"J. Plant Physiol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s11120-012-9755-4","article-title":"Chloroplast Movement Provides Photoprotection to Plants by Redistributing PSII Damage within Leaves","volume":"112","author":"Davis","year":"2012","journal-title":"Photosynth. Res."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1007\/s004250000392","article-title":"Light Quantity Controls Leaf-Cell and Chloroplast Development in Arabidopsis thaliana Wild Type and Blue-Light-Perception Mutants","volume":"211","author":"Weston","year":"2000","journal-title":"Planta"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1111","DOI":"10.1111\/j.1365-3040.1995.tb00623.x","article-title":"Comparative Ecophysiology of Leaf and Canopy Photosynthesis","volume":"18","author":"Terashima","year":"1995","journal-title":"Plant Cell Environ."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1046\/j.1365-3040.2003.01017.x","article-title":"Increases of Chlorophyll a\/b Ratios during Acclimation of Tropical Woody Seedlings to Nitrogen Limitation and High Light","volume":"26","author":"Kitajima","year":"2003","journal-title":"Plant Cell Environ."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1444","DOI":"10.1002\/ajb2.1378","article-title":"The Importance of Chloroplast Movement, Nonphotochemical Quenching, and Electron Transport Rates in Light Acclimation and Tolerance to High Light in Arabidopsis thaliana","volume":"106","author":"Howard","year":"2019","journal-title":"Am. J. Bot."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"69","DOI":"10.3389\/fpls.2015.00069","article-title":"ROS-Mediated Abiotic Stress-Induced Programmed Cell Death in Plants","volume":"6","author":"Petrov","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1016\/j.envexpbot.2018.05.003","article-title":"Reactive Oxygen Species, Oxidative Signaling and the Regulation of Photosynthesis","volume":"154","author":"Foyer","year":"2018","journal-title":"Environ. Exp. Bot."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"1795","DOI":"10.1104\/pp.112.208116","article-title":"Lesion Simulating Disease1, Enhanced Disease Susceptibility1, and Phytoalexin Deficient4 Conditionally Regulate Cellular Signaling Homeostasis, Photosynthesis, Water Use Efficiency, and Seed Yield in Arabidopsis","volume":"161","author":"Wituszynska","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"2644","DOI":"10.1111\/pce.12994","article-title":"The Dual Role of Lesion Simulating Disease 1 as a Condition-Dependent Scaffold Protein and Transcription Regulator","volume":"40","author":"Czarnocka","year":"2017","journal-title":"Plant Cell Environ."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1763","DOI":"10.1093\/jxb\/ers061","article-title":"The Expression of Phototropins in Arabidopsis Leaves: Developmental and Light Regulation","volume":"63","author":"Sztatelman","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1111\/j.1469-8137.2006.01893.x","article-title":"Functional Ecology of a Blue Light Photoreceptor: Effects of Phototropin-1 on Root Growth Enhance Drought Tolerance in Arabidopsis thaliana","volume":"173","author":"Galen","year":"2007","journal-title":"New Phytol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"2285","DOI":"10.1093\/jxb\/ern099","article-title":"Arabidopsis thaliana Leaves with Altered Chloroplast Numbers and Chloroplast Movement Exhibit Impaired Adjustments to Both Low and High Light","volume":"59","author":"Delamaide","year":"2008","journal-title":"J. Exp. Bot."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"1038","DOI":"10.1111\/nph.13299","article-title":"Lipid Anchoring of Arabidopsis Phototropin 1 to Assess the Functional Significance of Receptor Internalization: Should I Stay or Should I Go?","volume":"206","author":"Preuten","year":"2015","journal-title":"New Phytol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"R384","DOI":"10.1016\/j.cub.2015.03.020","article-title":"Plant Phototropic Growth","volume":"25","author":"Fankhauser","year":"2015","journal-title":"Curr. Biol."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/10\/2\/200\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:12:57Z","timestamp":1760159577000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/10\/2\/200"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,20]]},"references-count":110,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["cells10020200"],"URL":"https:\/\/doi.org\/10.3390\/cells10020200","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,20]]}}}