Phototropin2 3'UTR overlaps with the AT5G58150 gene encoding an inactive RLK kinase.
AT5G58150
Arabidopsis
Kinase
LRR RLK
Osmotic stress
Salt stress
phototropin2
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
18 Jan 2024
18 Jan 2024
Historique:
received:
09
03
2023
accepted:
05
01
2024
medline:
19
1
2024
pubmed:
19
1
2024
entrez:
18
1
2024
Statut:
epublish
Résumé
This study examines the biological implications of an overlap between two sequences in the Arabidopsis genome, the 3'UTR of the PHOT2 gene and a putative AT5G58150 gene, encoded on the complementary strand. AT5G58150 is a probably inactive protein kinase that belongs to the transmembrane, leucine-rich repeat receptor-like kinase family. Phot2 is a membrane-bound UV/blue light photoreceptor kinase. Thus, both proteins share their cellular localization, on top of the proximity of their loci. The extent of the overlap between 3'UTR regions of AT5G58150 and PHOT2 was found to be 66 bp, using RACE PCR. Both the at5g58150 T-DNA SALK_093781C (with insertion in the promoter region) and 35S::AT5G58150-GFP lines overexpress the AT5G58150 gene. A detailed analysis did not reveal any substantial impact of PHOT2 or AT5G58150 on their mutual expression levels in different light and osmotic stress conditions. AT5G58150 is a plasma membrane protein, with no apparent kinase activity, as tested on several potential substrates. It appears not to form homodimers and it does not interact with PHOT2. Lines that overexpress AT5G58150 exhibit a greater reduction in lateral root density due to salt and osmotic stress than wild-type plants, which suggests that AT5G58150 may participate in root elongation and formation of lateral roots. In line with this, mass spectrometry analysis identified proteins with ATPase activity, which are involved in proton transport and cell elongation, as putative interactors of AT5G58150. Membrane kinases, including other members of the LRR RLK family and BSK kinases (positive regulators of brassinosteroid signalling), can also act as partners for AT5G58150. AT5G58150 is a membrane protein that does not exhibit measurable kinase activity, but is involved in signalling through interactions with other proteins. Based on the interactome and root architecture analysis, AT5G58150 may be involved in plant response to salt and osmotic stress and the formation of roots in Arabidopsis.
Sections du résumé
BACKGROUND
BACKGROUND
This study examines the biological implications of an overlap between two sequences in the Arabidopsis genome, the 3'UTR of the PHOT2 gene and a putative AT5G58150 gene, encoded on the complementary strand. AT5G58150 is a probably inactive protein kinase that belongs to the transmembrane, leucine-rich repeat receptor-like kinase family. Phot2 is a membrane-bound UV/blue light photoreceptor kinase. Thus, both proteins share their cellular localization, on top of the proximity of their loci.
RESULTS
RESULTS
The extent of the overlap between 3'UTR regions of AT5G58150 and PHOT2 was found to be 66 bp, using RACE PCR. Both the at5g58150 T-DNA SALK_093781C (with insertion in the promoter region) and 35S::AT5G58150-GFP lines overexpress the AT5G58150 gene. A detailed analysis did not reveal any substantial impact of PHOT2 or AT5G58150 on their mutual expression levels in different light and osmotic stress conditions. AT5G58150 is a plasma membrane protein, with no apparent kinase activity, as tested on several potential substrates. It appears not to form homodimers and it does not interact with PHOT2. Lines that overexpress AT5G58150 exhibit a greater reduction in lateral root density due to salt and osmotic stress than wild-type plants, which suggests that AT5G58150 may participate in root elongation and formation of lateral roots. In line with this, mass spectrometry analysis identified proteins with ATPase activity, which are involved in proton transport and cell elongation, as putative interactors of AT5G58150. Membrane kinases, including other members of the LRR RLK family and BSK kinases (positive regulators of brassinosteroid signalling), can also act as partners for AT5G58150.
CONCLUSIONS
CONCLUSIONS
AT5G58150 is a membrane protein that does not exhibit measurable kinase activity, but is involved in signalling through interactions with other proteins. Based on the interactome and root architecture analysis, AT5G58150 may be involved in plant response to salt and osmotic stress and the formation of roots in Arabidopsis.
Identifiants
pubmed: 38238701
doi: 10.1186/s12870-024-04732-2
pii: 10.1186/s12870-024-04732-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
55Subventions
Organisme : Polish National Science Centre
ID : UMO-2014/15/D/NZ2/02306
Organisme : Polish National Science Centre
ID : UMO-2014/15/D/NZ2/02306
Organisme : Polish National Science Centre
ID : UMO-2014/15/D/NZ2/02306
Organisme : Polish National Science Centre
ID : UMO-2014/15/D/NZ2/02306
Organisme : Polish National Science Centre
ID : UMO-2014/15/D/NZ2/02306
Informations de copyright
© 2024. The Author(s).
Références
Christie JM. Phototropin Blue-Light Receptors. Annu Rev Plant Biol. 2007;58(1):21–45.
pubmed: 17067285
doi: 10.1146/annurev.arplant.58.032806.103951
Huala E, Oeller P, Liscum, Emmanuel, In-Seob H, Larsen E, Briggs WR. Arabidopsis NPH1: A Protein Kinase with a Putative Redox-Sensing Domain. Sci (1979). 1997;278(5346):2120–3.
Christie JM, Blackwood L, Petersen J, Sullivan S. Plant flavoprotein photoreceptors. Plant Cell Physiol. 2015;56(3):401–13.
pubmed: 25516569
doi: 10.1093/pcp/pcu196
Kong SG, Suzuki T, Tamura K, Mochizuki N, Hara-Nishimura I, Nagatani A. Blue light-induced association of phototropin 2 with the Golgi apparatus. Plant J. 2006;45(6):994–1005.
pubmed: 16507089
doi: 10.1111/j.1365-313X.2006.02667.x
Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, et al. Arabidopsis nph1 and npl1: Blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci. 2001;98(12):6969–74.
pubmed: 11371609
pmcid: 34462
doi: 10.1073/pnas.101137598
Kinoshita T, Doi M, Suetsugu N. phot1 and phot2 mediate blue light stomatal opening. Nature. 2001;414(December):656–60.
pubmed: 11740564
doi: 10.1038/414656a
Sakamoto K, Briggs WR. Cellular and subcellular localization of phototropin 1. Plant Cell. 2002;14(8):1723–35.
pubmed: 12172018
pmcid: 151461
doi: 10.1105/tpc.003293
Inoue SI, Kinoshita T, Takemiya A, Doi M, Shimazaki KI. Leaf positioning of Arabidopsis in response to blue light. Mol Plant. 2008;1(1):15–26.
pubmed: 20031912
doi: 10.1093/mp/ssm001
Iwabuchi K, Sakai T, Takagi S. Blue Light-Dependent Nuclear Positioning in Arabidopsis thaliana Leaf Cells. Plant Cell Physiol. 2007;48(9):1291–8.
pubmed: 17652112
doi: 10.1093/pcp/pcm095
Iwabuchi K, Hidema J, Tamura K, Takagi S, Hara-Nishimura I. Plant Nuclei Move to Escape Ultraviolet-Induced DNA Damage and Cell Death. Plant Physiol. 2016;170(2):678–85.
pubmed: 26681797
doi: 10.1104/pp.15.01400
Suetsugu N, Kagawa T, Wada M. An Auxilin-Like J-Domain Protein, JAC1, Regulates Phototropin-Mediated Chloroplast Movement. Plant Physiol. 2005;139(September):151–62.
pubmed: 16113208
pmcid: 1203365
doi: 10.1104/pp.105.067371
Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: Computational tools for comparative genomics. Nucleic Acids Res. 2004;32(WEB SERVER ISS):273–9.
doi: 10.1093/nar/gkh458
Zhan S, Lukens L. Protein-Coding cis-Natural Antisense Transcripts Have High and Broad Expression in Arabidopsis. Plant Physiol. 2013;161(4):2171–80.
pubmed: 23457227
pmcid: 3613485
doi: 10.1104/pp.112.212100
Diévart A, Clark SE. Using mutant alleles to determine the structure and function of leucine-rich repeat receptor-like kinases. Curr Opin Plant Biol. 2003;6(5):507–16.
pubmed: 12972053
doi: 10.1016/S1369-5266(03)00089-X
Gish LA, Clark SE. The RLK/Pelle family of kinases. Plant J. 2011;66(1):117–27.
pubmed: 21443627
pmcid: 4657737
doi: 10.1111/j.1365-313X.2011.04518.x
Castells E, Casacuberta JM. Signalling through kinase-defective domains: The prevalence of atypical receptor-like kinases in plants. J Exp Bot. 2007;58(13):3503–11.
pubmed: 17951602
doi: 10.1093/jxb/erm226
Kajava AV. Structural diversity of leucine-rich repeat proteins. J Mol Biol. 1998;277(3):519–27.
pubmed: 9533877
doi: 10.1006/jmbi.1998.1643
Chen T. Identification and characterization of the LRR repeats in plant LRR-RLKs. BMC Mol Cell Biol. 2021;22(1):1–16.
doi: 10.1186/s12860-021-00344-y
Zhang Z, Thomma BPHJ. Structure-function aspects of extracellular leucine-rich repeat-containing cell surface receptors in plants. J Integr Plant Biol. 2013;55(12):1212–23.
pubmed: 23718712
doi: 10.1111/jipb.12080
Hong SW, Jon JH, Kwak JM, Nam HG. Identification of a receptor-like protein kinase gene rapidly induced by abscisic acid, dehydration, high salt, and cold treatments in Arabidopsis thaliana. Plant Physiol. 1997;113(4):1203–12.
pubmed: 9112773
pmcid: 158243
doi: 10.1104/pp.113.4.1203
de Lorenzo L, Merchan F, Laporte P, Thompson R, Clarke J, Sousa C, et al. A novel plant leucine-rich repeat receptor kinase regulates the response of medicago truncatula roots to salt stress. Plant Cell. 2009;21(2):668–80.
pubmed: 19244136
pmcid: 2660638
doi: 10.1105/tpc.108.059576
Park SJ, Moon JC, Park YC, Kim JH, Kim DS, Jang CS. Molecular dissection of the response of a rice leucine-rich repeat receptor-like kinase (LRR-RLK) gene to abiotic stresses. J Plant Physiol. 2014;171(17):1645–53.
pubmed: 25173451
doi: 10.1016/j.jplph.2014.08.002
Li J, Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell. 1997;90(5):929–38.
pubmed: 9298904
doi: 10.1016/S0092-8674(00)80357-8
Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K. Leucine-rich repeat receptor-like kinasel is a key membrane-bound regulator of abscisic acid early signaling in arabidopsis. Plant Cell. 2005;17(4):1105–19.
pubmed: 15772289
pmcid: 1087989
doi: 10.1105/tpc.104.027474
Xu ZS, Xiong TF, Ni ZY, Chen XP, Chen M, Li LC, et al. Isolation and identification of two genes encoding leucine-rich repeat (LRR) proteins differentially responsive to pathogen attack and salt stress in tobacco. Plant Sci. 2009;176(1):38–45.
doi: 10.1016/j.plantsci.2008.09.004
Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Hoisten T, et al. A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21. Sci. 1995;270(December):2–4.
Clark SE, Williams RW, Meyerowitz EM. The CLAVATA1 Gene Encodes a Putative Receptor Kinase That Controls Shoot and Floral Meristem Size in Arabidopsis. Cell. 1997;89:575–85.
pubmed: 9160749
doi: 10.1016/S0092-8674(00)80239-1
Wang J, Kucukoglu M, Zhang L, Chen P, Decker D, Nilsson O, et al. The Arabidopsis LRR-RLK, PXC1, is a regulator of secondary wall formation correlated with the TDIF-PXY/TDR-WOX4 signaling pathway. BMC Plant Biol. 2013;13(1):1–11.
doi: 10.1186/1471-2229-13-94
Deeken R, Kaldenhoff R. Light-repressible receptor protein kinase: A novel photo-regulated gene from Arabidopsis thaliana. Planta. 1997;202(4):479–86.
pubmed: 9265789
doi: 10.1007/s004250050152
Li C, Chen J, Li X, Zhang X, Liu Y, Zhu S, Wang L, Zheng H, Luan S, Li J, Yu F. FERONIA is involved in phototropin 1-mediated blue light phototropic growth in Arabidopsis. J Integr Plant Biol. 2022;64:1901–15.
pubmed: 35924740
doi: 10.1111/jipb.13336
Consortium TU. UniProt: the Universal Protein Knowledgebase in 2023. Nucleic Acids Res. 2023;51(D1):D523–31.
doi: 10.1093/nar/gkac1052
Carter C. The Vegetative Vacuole Proteome of Arabidopsis thaliana Reveals Predicted and Unexpected Proteins. Plant Cell. 2004;16(12):3285–303.
pubmed: 15539469
pmcid: 535874
doi: 10.1105/tpc.104.027078
Hove CA, Bochdanovits Z, Jansweijer VMA, Koning FG, Berke L, Sanchez-Perez GF, et al. Probing the roles of LRR RLK genes in Arabidopsis thaliana roots using a custom T-DNA insertion set. Plant Mol Biol. 2011;76(1–2):69–83.
pubmed: 21431781
pmcid: 3097349
doi: 10.1007/s11103-011-9769-x
Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR. Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature. 2001;410(6831):952–4.
pubmed: 11309623
doi: 10.1038/35073622
Łabuz J, Sztatelman O, Banaś AK, Gabryś H. The expression of phototropins in Arabidopsis leaves: Developmental and light regulation. J Exp Bot. 2012;63(4):1763–71.
pubmed: 22371325
doi: 10.1093/jxb/ers061
Whippo CW, Khurana P, Davis PA, Deblasio SL, Desloover D, Staiger CJ, et al. THRUMIN1 is a light-regulated actin-bundling protein involved in chloroplast motility. Curr Biol. 2011;21(1):59–64.
pubmed: 21185188
doi: 10.1016/j.cub.2010.11.059
Boex-Fontvieille E, Jossier M, Davanture M, Zivy M, Hodges M, Tcherkez G. Differential Protein Phosphorylation Regulates Chloroplast Movement in Response to Strong Light and Darkness in Arabidopsis thaliana. Plant Mol Biol Report. 2014;32(5):987–1001.
doi: 10.1007/s11105-014-0707-3
Waese J, Fan J, Pasha A, Yu H, Fucile G, Shi R, et al. ePlant: Visualizing and exploring multiple levels of data for hypothesis generation in plant biology. Plant Cell. 2017;29(8):1806–21.
pubmed: 28808136
pmcid: 5590499
doi: 10.1105/tpc.17.00073
Nelson BK, Cai X, Nebenfuhr A. A multicolored set of in vivo organelle markers for co-localization studies inArabidopsis and other plants. Plant J. 2007;51:1126–36.
pubmed: 17666025
doi: 10.1111/j.1365-313X.2007.03212.x
Inoue S, Takemiya A, Shimazaki K. Phototropin signaling and stomatal opening as a model case. Curr Opin Plant Biol. 2010;13(5):587–93.
pubmed: 20920881
doi: 10.1016/j.pbi.2010.09.002
Suetsugu N, Takemiya A, Kong SG, Higa T, Komatsu A, Shimazaki KI, et al. RPT2/NCH1 subfamily of NPH3-like proteins is essential for the chloroplast accumulation response in land plants. Proc Natl Acad Sci. 2016;113(37):10424–9.
pubmed: 27578868
pmcid: 5027436
doi: 10.1073/pnas.1602151113
Sztatelman O, Łabuz J, Hermanowicz P, Banaś AK, Bażant A, Zgłobicki P, et al. Fine tuning chloroplast movements through physical interactions between phototropins. J Exp Bot. 2016;67(17):4963–78.
pubmed: 27406783
pmcid: 5014152
doi: 10.1093/jxb/erw265
Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, et al. Arabidopsis NPL1: A Phototropin Homolog Controlling the Chloroplast High-Light Avoidance Response. Sci (1979). 2001;291(5511):2138–41.
Dievart A, Perin C, Hirsch J, Bettembourg M, Lanau N, Artus F, et al. The phenome analysis of mutant alleles in Leucine-Rich Repeat Receptor-Like Kinase genes in rice reveals new potential targets for stress tolerant cereals. Plant Sci. 2015;242:240–9.
pubmed: 26566841
doi: 10.1016/j.plantsci.2015.06.019
Wu Y, Xun Q, Guo Y, Zhang J, Cheng K, Shi T, et al. Genome-Wide Expression Pattern Analyses of the Arabidopsis Leucine-Rich Repeat Receptor-Like Kinases. Mol Plant. 2016;9(2):289–300.
pubmed: 26712505
doi: 10.1016/j.molp.2015.12.011
Haruta M, Sussman MR. The effect of a genetically reduced plasma membrane protonmotive force on vegetative growth of arabidopsiss. Plant Physiol. 2012;158(3):1158–71.
pubmed: 22214817
pmcid: 3291248
doi: 10.1104/pp.111.189167
Garciá I, Castellano JM, Vioque B, Solano R, Gotor C, Romero LC. Mitochondrial β-cyanoalanine synthase is essential for root hair formation in Arabidopsis thaliana. Plant Cell. 2010;22(10):3268–79.
pubmed: 20935247
pmcid: 2990132
doi: 10.1105/tpc.110.076828
Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, et al. The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 2021;49(18):D605–12.
pubmed: 33237311
doi: 10.1093/nar/gkaa1074
Lichtenberg J, Yilmaz A, Welch JD, Kurz K, Liang X, Drews F, et al. The word landscape of the non-coding segments of the Arabidopsis thaliana genome. BMC Genomics. 2009;10:463.
pubmed: 19814816
pmcid: 2770528
doi: 10.1186/1471-2164-10-463
Shi H, Lee B ha, Wu SJ, Zhu JK. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol. 2003;21(1):81–5.
pubmed: 12469134
doi: 10.1038/nbt766
Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell. 2002;110(2):213–22.
pubmed: 12150929
doi: 10.1016/S0092-8674(02)00812-7
Zhao Y, Wang T, Zhang W, Li X. SOS3 mediates lateral root development under low salt stress through regulation of auxin redistribution and maxima in Arabidopsis. New Phytol. 2011;189(4):1122–34.
pubmed: 21087263
doi: 10.1111/j.1469-8137.2010.03545.x
McLoughlin F, Galvan-Ampudia CS, Julkowska MM, Caarls L, van der Does D, Laurière C, et al. The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant J. 2012;72(3):436–49.
pubmed: 22738204
pmcid: 3533798
doi: 10.1111/j.1365-313X.2012.05089.x
Xun Q, Wu Y, Li H, Chang J, Ou Y, He K, et al. Two receptor-like protein kinases, MUSTACHES and MUSTACHES-LIKE, regulate lateral root development in Arabidopsis thaliana. New Phytol. 2020;227:1157–73.
pubmed: 32278327
pmcid: 7383864
doi: 10.1111/nph.16599
Sreeramulu S, Mostizky Y, Sunitha S, Shani E, Nahum H, Salomon D, et al. BSKs are partially redundant positive regulators of brassinosteroid signaling in Arabidopsis. Plant J. 2013;74(6):905–19.
pubmed: 23496207
doi: 10.1111/tpj.12175
Tang W, Kim TW, Oses-Prieto JA, Sun Y, Deng Z, et al. Brassinosteroid-Signaling Kinases (BSKs) mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Sci (1979). 2008;321(5888):557–60.
Haruta M, Burch HL, Nelson RB, Barrett-Wilt G, Kline KG, Mohsin SB, et al. Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity. J Biol Chem. 2010;285(23):17918–29.
pubmed: 20348108
pmcid: 2878554
doi: 10.1074/jbc.M110.101733
Ladwig F, Dahlke RI, Stührwohldt N, Hartmann J, Harter K, Sauter M. Phytosulfokine regulates growth in arabidopsis through a response module at the plasma membrane that includes cyclic nucleotide-gated channel17, H+-ATPase, and BAK1. Plant Cell. 2015;27(6):1718–29.
pubmed: 26071421
pmcid: 4498212
doi: 10.1105/tpc.15.00306
Caesar K, Elgass K, Chen Z, Huppenberger P, Witthoft J, Schleifenbaum F, et al. A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana. Plant J. 2011;66:528–40.
pubmed: 21255166
doi: 10.1111/j.1365-313X.2011.04510.x
Morsomme P, Boutry M. The plant plasma membrane H+-ATPase: Structure, function and regulation. Biochim Biophys Acta Biomembr. 2000;1465(1–2):1–16.
doi: 10.1016/S0005-2736(00)00128-0
Vukašinović N, Wang Y, Vanhoutte I, Fendrych M, Guo B, Kvasnica M, et al. Local brassinosteroid biosynthesis enables optimal root growth. Nat Plants. 2021;7(5):619–32.
pubmed: 34007032
doi: 10.1038/s41477-021-00917-x
Pearson WR. An Introduction to Sequence Similarity (“Homology”) Searching. Curr Protoc Bioinformatics. 2013;3:3.1.1–3.: https://doi.org/10.1002/0471250953.bi0301s42 .
Salazar-Henao JE, Lehner R, Betegón-Putze I, Vilarrasa-Blasi J, Caño-Delgado AI. BES1 regulates the localization of the brassinosteroid receptor BRL3 within the provascular tissue of the Arabidopsis primary root. J Exp Bot. 2016;67(17):4951–61.
pubmed: 27511026
pmcid: 5014150
doi: 10.1093/jxb/erw258
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ. An ‘electronic fluorescent pictograph’ Browser for exploring and analyzing large-scale biological data sets. PLoS ONE. 2007;2(8):1–12.
doi: 10.1371/journal.pone.0000718
Fàbregas N, Li N, Boeren S, Nash TE, Goshe MB, Clouse SD, et al. The BRASSINOSTEROID INSENSITIVE1 – LIKE3 Signalosome Complex Regulates Arabidopsis Root Development. Plant Cell. 2013;25(September):3377–88.
pubmed: 24064770
pmcid: 3809538
doi: 10.1105/tpc.113.114462
Zogopoulos VL, Saxami G, Malatras A, Angelopoulou A, Jen CH, Duddy WJ, et al. Arabidopsis Coexpression Tool: a tool for gene coexpression analysis in Arabidopsis thaliana. iScience. 2021;24(8):102848.
pubmed: 34381973
pmcid: 8334378
doi: 10.1016/j.isci.2021.102848
Zogopoulos VL, Malatras A, Michalopoulos I. Gene coexpression analysis in Arabidopsis thaliana based on public microarray data. STAR Protoc. 2022;3(1):101208. https://doi.org/10.1016/j.xpro.2022.101208 .
Niwa Y, Hirano T, Yoshimoto K, Shimizu M, Kobayashi H. Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. Plant J. 1999;18(4):455–63.
pubmed: 10406127
doi: 10.1046/j.1365-313X.1999.00464.x
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5.
pubmed: 22930834
pmcid: 5554542
doi: 10.1038/nmeth.2089
Gabryś H, Banaś AK, Hermanowicz P, Krzeszowiec W, Leśniewski S, Łabuz J, et al. Photometric Assays for Chloroplast Movement Responses to Blue Light. Bio Protoc. 2017;7(11):1–11.
doi: 10.21769/BioProtoc.2310
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis. Plant Physiol. 2005;139(1):5–17.
pubmed: 16166256
pmcid: 1203353
doi: 10.1104/pp.105.063743
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):RESEARCH0034.1. https://doi.org/10.1186/gb-2002-3-7-research0034 .
Łabuz J, Hermanowicz P, Gabryś H. The impact of temperature on blue light induced chloroplast movements in Arabidopsis thaliana. Plant Sci. 2015;239:238–49.
pubmed: 26398808
doi: 10.1016/j.plantsci.2015.07.013
Aggarwal C, Banaś AK, Kasprowicz-Maluśki A, Borghetti C, Łabuz J, Dobrucki J, et al. Blue-light-activated phototropin2 trafficking from the cytoplasm to Golgi/post-Golgi vesicles. J Exp Bot. 2014;65(12):3263–76.
pubmed: 24821953
pmcid: 4071840
doi: 10.1093/jxb/eru172
Chakrabarty R, Banerjee R, Chung SM, Farman M, Citovsky V, Hogenhout SA, et al. pSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: Probing Nicotiana benthamiana-virus interactions. Mol Plant Microbe Interact. 2007;20(7):740–50.
pubmed: 17601162
doi: 10.1094/MPMI-20-7-0740
Strzalka WK, Aggarwal C, Krzeszowiec W, Jakubowska A, Sztatelman O, Banas AK. Arabidopsis PCNAs form complexes with selected D-type cyclins. Front Plant Sci. 2015;6(July):1–11.
Hubner NC, Bird AW, Cox J, Splettstoesser B, Bandilla P, Poser I, et al. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol. 2010;189(4):739–54.
pubmed: 20479470
pmcid: 2872919
doi: 10.1083/jcb.200911091
Hughes CS, Foehr S, Garfield DA, Furlong EE, Steinmetz LM, Krijgsveld J. Ultrasensitive proteome analysis using paramagnetic bead technology. Mol Syst Biol. 2014;10(10):757.
pubmed: 25358341
doi: 10.15252/msb.20145625
R Core Team. R: A language and environment for statistical computing. Vienna, Austria.: R Foundation for Statistical Computing; 2019. https://www.r-project.org/ .
Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J. 2008;50(3):346–63.
pubmed: 18481363
doi: 10.1002/bimj.200810425
Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67(1):1–48. https://doi.org/10.18637/jss.v067.i01 .
Wasson AP, Chiu GS, Zwart AB, Binns TR. Differentiating wheat genotypes by bayesian hierarchical nonlinear mixed modeling of wheat root density. Front Plant Sci. 2017;8(March):1–16.
Vizcaíno JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Ríos D, et al. ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination. Nat Biotechnol. 2013;32(3):223–6.
doi: 10.1038/nbt.2839