Abstract
Key message
Analyses of the function of Arabidopsis Calmodulin7 (CAM7) in concert with multiple regulatory proteins involved in various signal transduction processes.
Abstract
Calmodulin (CaM) plays various regulatory roles in multiple signaling pathways in eukaryotes. Arabidopsis CALMODULIN 7 (CAM7) is a unique member of the CAM family that works as a transcription factor in light signaling pathways. CAM7 works in concert with CONSTITUTIVE PHOTOMORPHOGENIC 1 and ELONGATED HYPOCOTYL 5, and plays an important role in seedling development. Further, it is involved in the regulation of the activity of various Ca2+-gated channels such as cyclic nucleotide gated channel 6 (CNGC6), CNGC14 and auto-inhibited Ca2+ ATPase 8. Recent studies further indicate that CAM7 is also an integral part of multiple signaling pathways including hormone, immunity and stress. Here, we review the recent advances in understanding the multifaceted role of CAM7. We highlight the open-ended questions, and also discuss the diverse aspects of CAM7 characterization that need to be addressed for comprehensive understanding of its cellular functions.
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References
Abbas N, Chattopadhyay S (2014) CAM7 and HY5 genetically interact to regulate root growth and abscisic acid responses. Plant Signal Behav 9:e29763
Abbas N, Maurya JP, Senapati D, Gangappa SN, Chattopadhyay S (2014) Arabidopsis CAM7 and HY5 physically interact and directly bind to the HY5 promoter to regulate its expression and thereby promote photomorphogenesis. Plant Cell 26:1036–1052
Ang LH, Deng XW (1994) Regulatory hierarchy of photomorphogenic loci: allele-specific and light-dependent interaction between the HY5 and COP1 loci. Plant Cell 6:613–628
Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Dend XW (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1:213–222
Anil VS, Rao KS (2001) Calcium-mediated signal transduction in plants: a perspective on the role of Ca2+ and CDPKs during early plant development. J Plant Physiol 158:1237–1256
Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101
Bachs O, Agell N, Carafoli E (1994) Calmodulin and calmodulin-binding proteins in the nucleus. Cell Calcium 16:289–296
Baek D, Nam J, Koo YD, Kim DH, Lee J, Jeong JC, Kwak SS, Chung WS, Lim CO, Bahk JD, Hong JC, Lee SY, Kawai-Yamada M, Uchimiya H, Yun DJ (2004) Bax-induced cell death of Arabidopsis is meditated through reactive oxygen-dependent and -independent processes. Plant Mol Biol 56:15–27
Banerjee J, Magnani R, Nair M, Dirk LM, DeBolt S, Maiti IB, Houtz R (2013) Calmodulin-mediated signal transduction pathways in Arabidopsis are fine-tuned by methylation. Plant Cell 25:4493–4511
Barbato G, Ikura M, Kay LE, Pastor RW, Bax A (1992) Backbone dynamics of calmodulin studied by 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry 31:5269–5278
Benaim G, Villalobo A (2002) Phosphorylation of calmodulin. Functional Implications. Eur J Biochem 269:3619–3631
Bergink S, Jentsch S (2009) Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458:461–467
Binkert M, Kozma-Bognár L, Terecskei K, De Veylder L, Nagy F, Ulm R (2014) UV-B-responsive association of the Arabidopsis bZIP transcription factor ELONGATED HYPOCOTYL5 with target genes, including its own promoter. Plant Cell 26:4200–4213
Biro RL, Daye S, Serlin BS, Terry ME, Datta N, Sopory SK, Roux SJ (1984) Characterization of oat calmodulin and radioimmunoassay of its subcellular distribution. Plant Physiol 75:382–386
Blom N, Sicheritz-Ponten T, Gupta R, Gammeltoft S, Brunak S (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4:1633–1649
Bouche N, Scharlat A, Snedden W, Bouchez D, Fromm H (2002) A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 277:21851–21861
Bouché N, Yellin A, Snedden WA, Fromm H (2005) Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–466
Bourbousse C, Ahmed I, Roudier F, Zabulon G, Blondet E, Balzergue S, Colot V, Boler C, Barneche C (2012) Histone H2B monoubiquitination facilitates the rapid modulation of gene expression during Arabidopsis photomorphogenesis. PLoS Genet 8:100
Braam J, Davis RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60:357–364
Brost C, Studtrucker T, Reimann R, Denninger P, Czekalla J, Krebs M, Fabry B, Schumacher K, Grossmann G, Dietrich P (2019) Multiple cyclic nucleotide-gated channels coordinate calcium oscillations and polar growth of root hairs. Plant J 99:910–923
Brown BA, Jenkins GI (2008) UV-B signaling pathways with different fluence-rate response profiles are distinguished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH. Plant Physiol 146:576–588
Buetow L, Huang DT (2016) Structural insights into the catalysis and regulation of E3 ubiquitin ligases. Nat Rev Mol Cell Biol 17:626–642
Burko Y, Seluzicki A, Zander M, Pedmale UV, Ecker JR, Chory J (2020) Chimeric activators and repressors define HY5 activity and reveal a light-regulated feedback mechanism. Plant Cell 32:967–983
Bursch K, Toledo-Ortiz G, Pireyre M, Lohr M, Braatz C, Johansson H (2020) Identification of BBX proteins as rate-limiting cofactors of HY5. Nat Plants 6:921–928
Burstenbinder K, Moller B, Plotner R, Stamm G, Hause G, Mitra D, Abel S (2017) The IQD family of calmodulin-binding proteins links calcium signaling to microtubules, membrane subdomains, and the nucleus. Plant Physiol 173:1692–1708
Bush DS (1993) Regulation of cytosolic calcium in plants. Plant Physiol 103:7–13
Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46:95–122
Campe R, Langenbach C, Leissing F, Popescu G, Popescu S, Goellner K, Beckers G, Conrath U (2016) ABC transporter PEN3/PDR8/ABCG36 interacts with calmodulin that, like PEN3, is required for Arabidopsis nonhost resistance. New Phytol 209:294–306
Carrión AM, Link WA, Ledo F, Mellström B, Naranjo JR (1999) DREAM is a Ca2+-regulated transcriptional repressor. Nature 398:80–84
Cashmore AR, Jarillo JA, Wu YJ, Liu D (1999) Cryptochromes: blue light receptors for plants and animals. Science 284:760–765
Chattopadhyay S, Ang LH, Puente P, Deng XW, Wei N (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10:673–683
Chen M, Chory J (2011) Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21:664–671
Chen ZJ, Sun LJ (2009) Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell 33:275–286
Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105:4495–4500
Cheng FY, Blackburn K, Lin YM, Goshe MB, Williamson JD (2009) Absolute protein quantification by LC/MS(E) for global analysis of salicylic acid-induced plant protein secretion responses. J Proteome Res 8:82–93
Chin D, Means AR (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 2000(10):322–328
Crivici A, Ikura M (1995) Molecular and structural basis of target recognition by calmodulin. Annu Rev Biophys Biomol Struct 24:85–116
Dagher R, Peng S, Gioria S, Fève M, Zeniou M, Zimmermann M, Pigault C, Haiech J, Kilhoffer MC (2011) A general strategy to characterize calmodulin-calcium complexes involved in CaM-target recognition: DAPK and EGFR calmodulin binding domains interact with different calmodulin-calcium complexes. Biochim Biophys Acta 1813:1059–1067
Deng XW, Quail PH (1999) Signaling in light-controlled development. Semin Cell Dev Biol 10:121–129
Dindas J, Scherzer S, Roelfsema MRG, Meyer K, Müller HM, Al-Rasheid KAS, Palme K, Dietrich P, Becker D, Bennett MJ, Hedrich R (2018) AUX1-mediated root hair auxin influx governs SCFTIR1/AFB-type Ca2+ signaling. Nat Commun 9:1174
Ding Y, Wang J, Wang J, Stierhof YD, Robinson DG, Jiang L (2012) Unconventional protein secretion. Trends Plant Sci 17:606–615
Donald RG, Cashmore AR (1990) Mutation of either G box or I box sequences profoundly affects expression from the Arabidopsis rbcS-1A promoter. EMBO J 9:1717–1726
Drum CL, Yan SZ, Bard J, Shen YQ, Lu D, Soelaiman S, Grabarek Z, Bohm A, Tang WJ (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415:396–402
Duek PD, Elmer MV, van Oosten VR, Fankhauser C (2004) The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr Biol 14:2296–2301
Dutta S, Basu R, Pal A, Parvez SW, Chattopadhyay S (2020) The Z-box binding factors (ZBFs): emerging new facets in Arabidopsis seedling development. J Plant Biochem Biotechnol. https://doi.org/10.1007/s13562-020-00593-6
Edel KH, Marchadier E, Brownlee C, Kudla J, Hetherington AM (2017) The evolution of calcium-based signalling in plants. Curr Biol. 27(13):667–679. https://doi.org/10.1016/j.cub.2017.05.020
Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016
Fankhauser C, Chory J (1997) Light control of plant development. Annu Rev Cell Dev Biol 13:203–229
Fischer C, DeFalco TA, Karia P, Snedden WA, Moeder W, Yoshioka K, Dietrich P (2017) Calmodulin as a Ca2+-sensing subunit of Arabidopsis cyclic nucleotide-gated channel complexes. Plant Cell Physiol 58:1208–1221
Friedberg F, Rhoads AR (2001) Evolutionary aspects of calmodulin. IUBMB Life 51:215–221
Galon Y, Finkler A, Fromm H (2010) Calcium-regulated transcription in plants. Mol Plant 3(4):653–669. https://doi.org/10.1093/mp/ssq019
Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Mol Plant 9:1353–1365
Gangappa SN, Srivastava AK, Maurya JP, Ram H, Chattopadhyay S (2013) Z-box binding transcription factors (ZBFs): a new class of transcription factors in Arabidopsis seedling development. Mol Plant 6:1758–1768
Gao F, Han X, Wu J, Zheng S, Shang Z, Sun D, Zhou R, Li B (2012) A heat-activated calcium-permeable channel–Arabidopsis cyclic nucleotide-gated ion channel 6- is involved in heat shock responses. Plant J 70:1056–1069
Gilchrist CA, Holm CF, Hughes MA, Schaenman JM, Mann BJ, Petri WA (2001) Identification and characterization of an Entamoeba histolytica upstream regulatory element 3 sequence specific DNA-binding protein containing EF-hand motifs. J Biol Chem 276:11838–11843
Gilli R, Lafitte D, Lopez C, Kilhoffer M, Makarov A, Briand C, Haiech J (1998) Thermodynamic analysis of calcium and magnesium binding to calmodulin. Biochemistry 37:5450–5456
Gilmartin PM, Sarokin L, Memelink J, Chua NH (1990) Molecular light switches for plant genes. Plant Cell 2:369–378
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212:205–214
Ha SB, An G (1998) Identification of upstream regulatory elements involved in the developmental expression of the Arabidopsis thaliana cab1 gene. Proc Natl Acad Sci USA 85:8017–8021
Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, Dikic I (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 5:461–466
Haiech J, Klee CB, Demaille JG (1981) Effects of cations on affinity of calmodulin for calcium: ordered binding of calcium ions allows the specific activation of calmodulin-stimulated enzymes. Biochemistry 20:3890–3897
Hajdu A, Dobos O, Domijan M, Bälint B, Nagy F, Kozma-Bognár L (2018) Elongated hypocotyl 5 mediates blue light signalling to the Arabidopsis circadian clock. Plant J 96:1242–1254
Hardtke CS, Gohda K, Osterlund MT, Oyama T, Okada K, Deng XW (2000) HY5 stability and activity in arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19:4997–5006
Harter K, Kircher S, Frohnmeyer H, Krenz M, Nagy F, Schäfer E (1994) Light-regulated modification and nuclear translocation of cytosolic G-box binding factors in parsley. Plant Cell 6:545–559
Hashiguchi A, Komatsu S (2017) Posttranslational modifications and plant-environment interaction. Methods Enzymol 586:97–113
Hicke L (2001) Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2:195–201
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300
Hilleary R, Paez-Valencia J, Vens C, Toyota M, Palmgren M, Gilroy S (2020) Tonoplast-localized Ca2+ pumps regulate Ca2+ signals during pattern-triggered immunity in Arabidopsis thaliana. Proc Natl Acad Sci USA 117(31):18849–18857. https://doi.org/10.1073/pnas.2004183117
Hochstrasser M (1995) Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr Opin Cell Biol 7:215–223
Hoeflich KP, Ikura M (2002) Calmodulin in action. Cell 108:739–742
Hofmann NR (2013) Calmodulin methylation: another layer of regulation in calcium signaling. Plant Cell 25:4284
Holm M, Ma LG, Qu LJ, Deng XW (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev 16:1247–1259
Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 20:4207
Hsieh HL, Song CJ, Roux SJ (2000) Regulation of a recombinant pea nuclear apyrase by calmodulin and casein kinase II. Biochim Biophys Acta 1494:248–255
Huang F, Luo J, Ning T, Cao W, Jin X, Zhao H, Wang Y, Han S (2017) Cytosolic and nucleosolic calcium signaling in response to osmotic and salt stresses are independent of each other in roots of Arabidopsis seedlings. Front Plant Sci 21(8):1648
Huberts DH, van der Klei IJ (2010) Moonlighting proteins: an intriguing mode of multitasking. Biochim Biophys Acta 1803:520–525
Iglesias MJ, Sellaro R, Zurbriggen MD, Casal JJ (2018) Multiple links between shade avoidance and auxin networks. J Exp Bot 69:213–228
Ihara-Ohori Y, Nagano M, Muto S, Uchimiya H, Kawai-Yamada M (2007) Cell death suppressor Arabidopsis bax inhibitor-1 is associated with calmodulin binding and ion homeostasis. Plant Physiol 143:650–660
Ikura M, Osawa M, Ames JB (2002) The role of calcium-binding proteins in the control of transcription: structure to function. BioEssays 24:625–636
Jang IC, Yang JY, Seo HS, Chua NH (2005) HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev 19:593–602
Jang IC, Henriques R, Seo HS, Nagatani A, Chua NH (2010) Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. Plant Cell 22:2370–2383
Jeffery CJ (2017) Protein moonlighting: what is it, and why is it important? Phil Trans R Soc B 373:20160523
Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8:217–230
Jing Y, Lin R (2020) Transcriptional regulatory network of the light signaling pathways. New Phytol 227:683–697
Josse EM, Halliday KJ (2008) Skotomorphogenesis: the dark side of light signalling. Curr Biol 18:R1144–R1146
Kawai M, Pan L, Reed JC, Uchimiya H (1999) Evolutionally conserved plant homologue of the Bax inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast(1). FEBS Lett 464:143–147
Kawai-Yamada M, Jin L, Yoshinaga K, Hirata A, Uchimiya H (2001) Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (AtBI-1). Proc Natl Acad Sci USA 98:12295–12300
Kawai-Yamada M, Ohori Y, Uchimiya H (2004) Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell 16:21–32
Kilhoffer MC, Kubina M, Travers F, Haiech J (1992) Use of engineered proteins with internal tryptophan reporter groups and pertubation techniques to probe the mechanism of ligand-protein interactions: investigation of the mechanism of calcium binding to calmodulin. Biochemistry 31:8098–8106
Kim YM, Woo JC, Song PS, Soh MS (2002) HFR1, a phytochrome A-signalling component, acts in a separate pathway from HY5, downstream of COP1 in Arabidopsis thaliana. Plant J 30:711–719
Kim MC, Chung WS, Yun DJ, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21
Klimczak LJ, Schindler U, Cashmore AR (1992) DNA binding activity of the Arabidopsis G-box binding factor GBF1 is stimulated by phosphorylation by casein kinase II from broccoli. Plant Cell 4:87–98
Klimczak LJ, Collinge MA, Farini D, Giuliano G, Walker JC, Cashmore AR (1995) Reconstitution of Arabidopsis casein kinase II from recombinant subunits and phosphorylation of transcription factor GBF1. Plant Cell 7:105–115
Knight H (2000) Calcium signaling during abiotic stress in plants. Int Rev Cytol 195:269–324
Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267
Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526
Koorneef M, Rolff E, Spruitt CJP (1980) Genetic control of light inhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z Pflanzenphysiol 100:147–160
Kretsinger RH, Nockolds CE (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J Biol Chem 248:3313–3326
Kumar S, Mazumder M, Gupta N, Chattopadhyay S, Gourinath S (2016) Crystal structure of Arabidopsis thaliana calmodulin7 and insight into its mode of DNA binding. FEBS Lett 590:3029–3039
Kursula P (2014) The many structural faces of calmodulin: a multitasking molecular jackknife. Amino Acids 46(10):2295–2304. https://doi.org/10.1007/s00726-014-1795-y
Kushwaha R, Singh A, Chattopadhyay S (2008) Calmodulin7 plays an important role as transcriptional regulator in Arabidopsis seedling development. Plant Cell 20:1747–1759
Landoni M, De Francesco A, Galbiati M, Tonelli C (2010) A loss-of-function mutation in Calmodulin2 gene affects pollen germination in Arabidopsis thaliana. Plant Mol Biol 74:235–247
Lau OS, Deng XW (2012) The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci 17:584–593
Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Deng XW (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749
Lee K, Song EH, Kim HS, Yoo JH, Han HJ, Jung MS, Lee SM, Kim KE, Kim MC, Cho MJ, Chung WS (2008) Regulation of MAPK phosphatase 1 (AtMKP1) by calmodulin in Arabidopsis. J Biol Chem. 283(35):23581–8. https://doi.org/10.1074/jbc.M801549200
Li J, Yang L, Jin D, Nezames CD, Terzaghi W, Deng XW (2013) UV-B-induced photomorphogenesis in Arabidopsis. Protein Cell 4:485–492
Li X, Liu C, Zhao Z, Ma D, Zhang J, Yang Y, Liu Y, Liu H (2020) COR27 and COR28 are novel regulators of the COP1-HY5 regulatory hub and photomorphogenesis in Arabidopsis. Plant Cell 32:3139–3154
Lin JR, Hu J (2013) SeqNLS: nuclear localization signal prediction based on frequent pattern mining and linear motif scoring. PLoS ONE 8:e76864
Lin F, Jiang Y, Li J, Yan T, Fan L, Liang J, Chen J, Xu D, Deng XW (2018) B-BOX DOMAIN PROTEIN28 negatively regulates photomorphogenesis by repressing the activity of transcription factor HY5 and undergoes COP1-mediated degradation. Plant Cell 30:2006–2019
Ling JJ, Li J, Zhu D, Deng XW (2017) Noncanonical role of Arabidopsis COP1/SPA complexinrepressingBIN2-mediated PIF3 phosphorylation and degradation in darkness. Proc Natl Acad Sci USA 114:3539–3544
Lockhart J (2014) How elongated HYPOCOTYL5 helps protect plants from UV-B rays. Plant Cell 26:3826
Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607
Mallappa C, Yadav V, Negi P, Chattopadhyay S (2006) A basic leucine zipper transcription factor, G-box-binding factor 1, regulates blue light-mediated photomorphogenic growth in Arabidopsis. J Biol Chem 281:22190–22199
Mallappa C, Singh A, Ram H, Chattopadhyay S (2008) GBF1, a transcription factor of blue light signaling in Arabidopsis, is degraded in the dark by a proteasome-mediated pathway independent of COP1 and SPA1. J Biol Chem 283:35772–35782
Maréchal E, Hiratsuka K, Delgado J, Nairn A, Qin J, Chait BT, Chua NH (1999) Modulation of GT-1 DNA-binding activity by calcium-dependent phosphorylation. Plant Mol Biol 40:373–386
Maurya JP, Sethi V, Gangappa SN, Gupta N, Chattopadhyay S (2015) Interaction of MYC2 and GBF1 results in functional antagonism in blue light-mediated Arabidopsis seedling development. Plant J 83:439–450
McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159:585–598
McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389
Meador WE, Means AR, Quiocho FA (1992) Target enzyme recognition by calmodulin: 2.4 a structure of a calmodulin-peptide complex. Science 257:1251–1255
Meador WE, Means AR, Quiocho FA (1993) Modulation of calmodulin plasticity in molecular recognition on the basis of X-ray structures. Science 262:1718–1721
Millar AJ, Kay SA (1996) Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis. Proc Natl Acad Sci USA 93:15491–15496
Miller A, Sanders D (1987) Depletion of cytosolic free calcium induced by photosynthesis. Nature 326:397–400
Mohanta TK, Yadav D, Khan AL, Hashem A, Abd Allah EF, Al-Harrasi A (2019) Molecular players of EF-hand containing calcium signaling event in plants. Int J Mol Sci 20(6):1476
Moore B (2004) Bifunctional and moonlighting enzymes: lighting the way to regulatory control. Trends Plant Sci 9:221–228
Ni W, Xu SL, Chalkley RJ, Pham TND, Guan S, Maltby DA, Burlingame AL, Wang ZY, Quail PH (2013) Multisite light-induced phosphorylation of the transcription factor PIF3 is necessary for both its rapid degradation and concomitant negative feedback modulation of photoreceptor phyB levels in Arabidopsis. Plant Cell 25:2679–2698
Ni L, Fu X, Zhang H, Li X, Cai X, Zhang P, Liu L, Wang Q, Sun M, Wang QW, Zhang A, Zhang Z, Jiang M (2019) Abscisic acid inhibits rice protein phosphatase PP45 via H2O2 and relieves repression of the Ca2+/CaM-dependent protein kinase DMI3. Plant Cell 31:128–152. https://doi.org/10.1105/tpc.18.00506
Nitsche J, Josts I, Heidemann J, Mertens HD, Maric S, Moulin M, Haertlein M, Busch S, Forsyth VT, Svergun DI, Uetrecht C, Todow H (2018) Structural basis for activation of plasma-membrane Ca2+-ATPase by calmodulin. Commun Biol 1:206
Niu WT, Han XW, Wei SS, Shang ZL, Wang J, Yang DW, Fan X, Gao F, Zheng SZ, Bai JT, Zhang B, Wang ZX, Li B (2020) Arabidopsis cyclic nucleotide-gated channel 6 is negatively modulated by multiple calmodulin isoforms during heat shock. J Exp Bot 71:90–104
Noman M, Aysha J, Ketehouli T, Yang J, Du L, Wang F, Li H (2021) Calmodulin binding transcription activators: an interplay between calcium signalling and plant stress tolerance. J Plant Physiol 256:153327
Oravecz A, Baumann A, Máté Z, Brzezinska A, Molinier J, Oakeley EJ, Adam E, Schafer E, Nagy F, Ulm R (2006) Constitutively photomorphogenic1 is required for the UV-B response in Arabidopsis. Plant Cell 18:1975–1990
Osawa M, Dace A, Tong KI, Valiveti A, Ikura M, Ames JB (2005) Mg2+ and Ca2+ differentially regulate DNA binding and dimerization of DREAM. J Biol Chem 280:18008–18014
Osterlund MT, Hardtke CS, Wei N, Deng XW (2000a) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–466
Osterlund MT, Wei N, Deng XW (2000b) The roles of photoreceptor systems and the COP1-targeted destabilization of HY5 in light control of Arabidopsis seedling development. Plant Physiol 124:1520–1524
Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11:2983–2995
Pan Y, Shi H (2017) Stabilizing the transcription factors by E3 ligase COP1. Trends in Plant Sci 22:999–1001
Pan MR, Peng G, Hung WC, Lin SY (2011) Monoubiquitination of H2AX protein regulates DNA damage response signaling. J Biol Chem 286:28599–28607
Pan Y, Chai X, Gao Q, Zhou L, Zhang S, Li L, Luan S (2019) Dynamic interactions of plant CNGC subunits and calmodulins drive oscillatory Ca2+ channel activities. Dev Cell 48:710-725.e5. https://doi.org/10.1016/j.devcel.2018.12.025
Pandey S, Tiwari SB, Tyagi W, Reddy MK, Upadhyaya KC, Sopory SK (2002) A Ca2+/CaM-dependent kinase from pea is stress regulated and in vitro phosphorylates a protein that binds to AtCaM5 promoter. Eur J Biochem 269(13):3193–3204. https://doi.org/10.1046/j.1432-1033.2002.02994.x (PMID: 12084059)
Park CY, Heo WD, Yoo JH, Lee JH, Kim MC, Chun HJ, Moon BC, Kim IH, Park HC, Choi MS, Ok HM, Cheong MS, Lee SM, Kim HS, Lee KH, Lim CO, Chung WS, Cho MJ (2004) Pathogenesis-related gene expression by specific calmodulin isoforms is dependent on NIM1, a key regulator of systemic acquired resistance. Mol Cells 18:207–213
Passmore LA, Barford D (2004) Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem J 379:513–525
Peng H, Yang T, Ii WM (2014) Calmodulin gene expression in response to mechanical wounding and Botrytis cinerea infection in tomato fruit. Plants (basel) 3:427–441
Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786
Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6:9–20
Pfeiffer A, Janocha D, Dong Y, Medzihradszky A, Schone S, Daum G, Suzaki T, Forner J, Langenecker T, Rempel E, Schmid M, Wirtz M, Hell R, Lohmann JU (2016) Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. Elife 5:e17023
Pickart CM, Eddins MJ (2004) Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta 1695:55–72
Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci U S A 104:4730–4735
Puente P, Wei N, Deng XW (1996) Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J 15:3732–3743
Qiu WR, Xiao X, Lin WZ, Chou KC (2014) iMethyl-PseAAC: identification of protein methylation sites via a pseudo amino acid composition approach. Biomed Res Int 2014:947416
Radivojac P, Vucetic S, O’Connor TR, Uversky VN, Obradovic Z, Dunker AK (2006) Calmodulin signaling: analysis and prediction of a disorder-dependent molecular recognition. Proteins 63:398–410
Ranjeva R, Boudet AM (1987) Phosphorylation of proteins in plants: regulatory effects and potential involvement in stimulus/response coupling. Annu Rev Plant Physiol 38:73–94
Ranty B, Aldon D, Galaud JP (2006) Plant calmodulins and calmodulin-related proteins: multifaceted relays to decode calcium signals. Plant Signal Behav 1:96–104
Rizzini L, Favory JJ, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schäfer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106
Roberts DM, Crea R, Malech AM, Alvarado-Urbina G, Chiarello RH, Watterson DM (1985) Chemical synthesis and expression of a calmodulin gene designed for site-specific mutagenesis. Biochemistry 24:5090–8
Roberts DM, Rowe PM, Siegel FL, Lukas TJ, Watterson DM (1986) Trimethyllysine and protein function. Effect of methylation and mutagenesis of lysine 115 of calmodulin on NAD kinase activation. J Biol Chem 261:1491–1494
Rodríguez-Concepción M, Yalovsky S, Zik M, Fromm H, Gruissem W (1999) The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein. EMBO J 18:1996–2200
Rudd JJ, Franklin-Tong VE (2001) Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytol 151:7–33
Sadowski M, Suryadinata R, Tan AR, Roesley SN, Sarcevic B (2012) Protein monoubiquitination and polyubiquitination generate structural diversity to control distinct biological processes. IUBMB Life 64:136–142
Sanchez P, de Torres Zabala M, Grant M (2000) AtBI-1, a plant homologue of Bax inhibitor-1, suppresses Bax-induced cell death in yeast and is rapidly upregulated during wounding and pathogen challenge. Plant J 21:393–399
Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706
Sarcevic B, Mawson A, Baker RT, Sutherland RL (2002) Regulation of the ubiquitin-conjugating enzyme hHR6A by CDK-mediated phosphorylation. EMBO J 21:2009–2018
Sarokin LP, Chua NH (1992) Binding sites for two novel phosphoproteins, 3AF5 and 3AF3, are required for rbcS-3A expression. Plant Cell 4:473–483
Schepens I, Duek P, Fankhauser C (2004) Phytochrome-mediated light signalling in Arabidopsis. Curr Opin Plant Biol 7:564–569
Schumacher MA, Rivard AF, Bächinger HP, Adelman JP (2001) Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin. Nature 410:1120–1124
Senapati D, Kushwaha R, Dutta S, Maurya JP, Biswas S, Gangappa S, Chattopadhyay S (2019) COP1 regulates the stability of CAM7 to promote photomorphogenic growth. Plant Direct 3:e00144
Seo HS, Yang JY, Ishikawa M, Bolle C, Ballesteros ML, Chua NH (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423:995–999
Seo HS, Watanabe E, Tokutomi S, Nagatani A, Chua NH (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev 18:617–622
Sethi V, Raghuram B, Sinha AK, Chattopadhyay S (2014) A mitogen-activated protein kinase cascade module, MKK3-MPK6 and MYC2, is involved in blue light-mediated seedling development in Arabidopsis. Plant Cell 26:3343–3357
Shi J, Du X (2020) Identification, characterization and expression analysis of calmodulin and calmodulin-like proteins in Solanum pennellii. Sci Rep 10:7474
Shi H, Liu R, Xue C, Shen X, Wei N, Deng XW, Zhong S (2016) Seedlings transduce the depth and mechanical pressure of covering soil using COP1and ethylene to regulateEBF1/EBF2 for soil emergence. Curr Biol 26:139–149
Shih HW, DePew CL, Miller ND, Monshausen GB (2015) The cyclic nucleotide-gated channel CNGC14 regulates root gravitropism in Arabidopsis thaliana. Curr Biol 25:3119–3125
Singh A, Ram H, Abbas N, Chattopadhyay S (2012) Molecular interactions of GBF1 with HY5 and HYH proteins during light-mediated seedling development in Arabidopsis thaliana. J Biol Chem 287:25995–26009
Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151:35–66
Song Z, Yan T, Liu J, Bian Y, Heng Y, Lin F, Jiang Y, Deng XW, Xu D (2020) BBX28/BBX29, HY5 and BBX30/31 form a feedback loop to fine-tune photomorphogenic development. Plant J 104:377–390
Strehler EE, Caride AJ, Filoteo AG, Xiong Y, Penniston JT, Enyedi A (2007) Plasma membrane Ca2+ ATPases as dynamic regulators of cellular calcium handling. Ann N Y Acad Sci 1099:226–236
Sullivan JA, Shirasu K, Deng XW (2003) The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nat Rev Genet 4:948–958
Sun L, Tobin EM (1990) Phytochrome-regulated expression of genes encoding light-harvesting chlorophyll a/b-protein in two long hypocotyl mutants and wild type plants of Arabidopsis thaliana. Photochem Photobiol 52:51–56
Takahashi F, Mizoguchi T, Yoshida R, Ichimura K, Shinozaki K (2011) Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol Cell 41:649–660
Tarcsa E, Szymanska G, Lecker S, O’Connor CM, Goldberg AL (2000) Ca2+-free calmodulin and calmodulin damaged by in vitro aging are selectively degraded by 26S proteasomes without ubiquitination. J Biol Chem 275:20295–20301
Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH (2001) Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc Natl Acad Sci U S A 98:9437–9442
Terzaghi WB, Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Physiol Plant Mol Biol 46:445–474
Thorogate R, Torok K (2004) Ca2+-dependent and -independent mechanisms of calmodulin nuclear translocation. J Cell Sci 117:5923–5936
Tidow H, Nissen P (2013) Structural diversity of calmodulin binding to its target sites. FEBS J 280:5551–5565
Tidow H, Poulsen LR, Andreeva A, Knudsen M, Hein KL, Wiuf C, Palmgren MG, Nissen P (2012) A bimodular mechanism of calcium control in eukaryotes. Nature 2012(491):468–472
Tilman D, Lehman C (2001) Human-caused environmental change: impacts on plant diversity and evolution. Proc Natl Acad Sci U S A 98:5433–5440
Tobin EM, Kehoe DM (1994) Phytochrome regulated gene expression. Semin Cell Biol 5:335–346
Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signal Behav 2:79–85
Ulrich HD, Walden H (2010) Ubiquitin signalling in DNA replication and repair. Nat Rev Mol Cell Biol 11:479–489
van der Horst A, de Vries-Smits AM, Brenkman AB, van Triest MH, van den Broek N, Colland F, Maurice MM, Burgering BM (2006) FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat Cell Biol 8:1064–73
Vetter SW, Leclerc E (2003) Novel aspects of calmodulin target recognition and activation. Eur J Biochem 270:404–414
Vierstra RD (1996) Proteolysis in plants: mechanisms and functions. Plant Mol Biol 32:275–302
Villalobo A (2018) The multifunctional role of phospho-calmodulin in pathophysiological processes. Biochem J 475:4011–4023
Virdi AS, Singh S, Singh P (2015) Abiotic stress responses in plants: roles of calmodulin-regulated proteins. Front Plant Sci 6:809
Von Arnim A, Deng XW (1996) Light control of seedling development. Annu Rev Plant Physiol Plant Mol Biol 47:215–243
Wall ME, Clarage JB, Phillips GN (1997) Motions of calmodulin characterized using both Bragg and diffuse X-ray scattering. Structure 5:1599–1612
Wang ZY, Kenigsbuch D, Sun L, Harel E, Ong MS, Tobin EM (1997) A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9:491–507
Wang X, Wang Q, Nguyen P, Lin C (2014) Cryptochrome-mediated light responses in plants. Enzymes 35:167–189
Wu JF, Tsai HL, Joanito I, Wu YC, Chang CW, Li YH, Wang Y, Hong JC, Chu JW, Hsu CP, Wu SH (2016) LWD-TCP complex activates the morning gene CCA1 in Arabidopsis. Nat Commun 7:13181
Xu D, Jiang Y, Li J, Lin F, Holm M, Deng XW (2016) BBX21, an Arabidopsis B-box protein, directly activates HY5 and is targeted by COP1 for 26S proteasome-mediated degradation. Proc Natl Acad Sci U S A 113:7655–7660
Yadav V, Kundu S, Chattopadhyay D, Negi P, Wei N, Deng XW, Chattopadhyay S (2002) Light regulated modulation of Z-box containing promoters by photoreceptors and downstream regulatory components, COP1 and HY5, in Arabidopsis. Plant J 31:741–753
Yadav V, Mallappa C, Gangappa SN, Bhatia S, Chattopadhyay S (2005) A basic helix-loop-helix transcription factor in Arabidopsis, MYC2, acts as a repressor of blue light-mediated photomorphogenic growth. Plant Cell 17:1953–1966
Yadukrishnan P, Rahul PV, Datta S (2020) HY5 suppresses, rather than promotes, ABA-mediated inhibition of post-germination seedling development. Plant Physiol 184:547–578
Yamakawa H, Katou S, Seo S, Mitsuhara I, Kamada H, Ohashi Y (2004) Plant MAPK phosphatase interacts with calmodulins. J Biol Chem 279:928–936
Yang C, Li L (2017) Hormonal regulation in shade avoidance. Front Plant Sci 8:1527
Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277:45049–45058
Yang J, Lin R, Hoecker U, Liu B, Xu L, Wang H (2005) Repression of light signaling by Arabidopsis SPA1 involves post-translational regulation of HFR1 protein accumulation. Plant J 43:131–141
Yang T, Peng H, Bauchan GR (2014) Functional analysis of tomato calmodulin gene family during fruit development and ripening. Hortic Res 1:14057
Yang C, Shen W, Yang L, Sun Y, Li X, Lai M, Wei J, Wang C, Xu Y, Li F, Liang S, Yang C, Zhong S, Luo M, Gao C (2020) HY5-HDA9 module transcriptionally regulates plant autophagy in response to light-to-dark conversion and nitrogen starvation. Mol Plant 13:515–531
Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, Menaker M, Takahasi JS (2004) PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A 101:5339–5346
Yoshinaga K, Arimura S, Niwa Y, Tsutsumi N, Uchimiya H, Kawai-Yamada M (2005) Mitochondrial behaviour in the early stages of ROS stress leading to cell death in Arabidopsis thaliana. Ann Bot 96:337–342
Yun CH, Bai J, Sun DY, Cui DF, Chang WR, Liang DC (2004) Structure of potato calmodulin PCM6: the first report of the three-dimensional structure of a plant calmodulin. Acta Crystallogr D Biol Crystallogr 60:1214–1219
Zeb Q, Wang X, Hou C, Zhang X, Dong M, Zhang S, Zhang Q, Ren Z, Tian W, Zhu H, Li L, Liu L (2020) The interaction of CaM7 and CNGC14 regulates root hair growth in Arabidopsis. J Integr Plant Biol 62:887–896
Zeng H, Xu L, Singh A, Wang H, Du L, Poovaiah BW (2015) Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses. Front Plant Sci 6:600
Zhai Q, Yan L, Tan D, Chen R, Sun J, Gao L, Dong MQ, Wang Y, Li C (2013) Phosphorylation-coupled proteolysis of the transcription factor MYC2 is important for jasmonate-signaled plant immunity. PLoS Genet. 9:e1003422
Zhang M, Jang H, Gaponenko V, Nussinov R (2017a) Phosphorylated calmodulin promotes PI3K activation by binding to the SH2 domains. Biophys J 113:1956–1967
Zhang S, Pan Y, Tian W, Zhu H, Luan S, Li L (2017b) Arabidopsis CNGC14 mediates calcium influx required for tip growth in root hairs. Mol Plant 10:1004–1006
Zhang K, Yue D, Wei W, Hu Y, Feng J, Zou Z (2016) Characterization and functional analysis of calmodulin and calmodulin-like genes in Fragaria vesca. Front Plant Sci 7:1820
Zhao Y, Liu W, Xu YP, Cao JY, Braam J, Cai XZ (2013) Genome-wide identification and functional analyses of calmodulin genes in Solanaceous species. BMC Plant Biol 13:70
Zhu X, Caplan J, Mamillapalli P, Czymmek K, Dinesh-Kumar SP (2010) Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death. EMBO J 29:1007–1018
Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 49:697–725
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This work is supported by J.C. Bose National Fellowship Award Grant of SERB, Government of India to S.C. R.B. and A.P. are recipients of CSIR-JRF from Council of Scientific and Industrial Research (CSIR), Government of India.
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RB, SD, and SC conceived and designed the review. SD extracted and analyzed the GO enrichment, KEGG pathway and Genevestigator expression data. RB, SD, AP, MS, and SC wrote the manuscript.
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11103_2021_1177_MOESM2_ESM.xlsx
Supplemental Data 2. List of CAM7 interacting proteins (CAM7-IPs) and overviews of GO and KEGG pathways analysis. Supplementary file2 (XLSX 24 kb)
11103_2021_1177_MOESM3_ESM.xlsx
Supplemental Data 3. List of Cis-acting regulatory elements (CREs) retrieved from PLACE database analysis of CAM7 promoter sequence. Supplementary file3 (XLSX 15 kb)
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Basu, R., Dutta, S., Pal, A. et al. Calmodulin7: recent insights into emerging roles in plant development and stress. Plant Mol Biol 107, 1–20 (2021). https://doi.org/10.1007/s11103-021-01177-1
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DOI: https://doi.org/10.1007/s11103-021-01177-1