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PreprintCited by 21Plant Stress Responses and TolerancePlant Molecular Biology ResearchPlant and Biological Electrophysiology Studies

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Arabidopsis calmodulin-like proteins CML13 and CML14 interact with proteins that have IQ domains

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Teresinski, Howard J., Hau, Bryan, Symonds, Kyle, Kilburn, Ryan, Munro, Kim A., Doner, Nathan M., Mullen, Robert, Li, Vivian H., Snedden, Wayne A.·2023·Plant Cell & Environment
DOI 10.1101/2023.03.09.531943

Preprint — published as 10.1111/pce.14616 · Paper page

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Abstract

SUMMARY: In response to Ca 2+ signals, the evolutionarily-conserved Ca 2+ sensor calmodulin (CaM) regulates protein targets via direct interaction. Plants possess many CaM-like (CML) proteins, but their binding partners and functions are mostly unknown. Here, using Arabidopsis CML13 as ‘bait’ in a yeast two-hybrid screen, we isolated putative targets from three, unrelated protein families, namely, IQD proteins, calmodulin-binding transcriptional activators (CAMTAs), and myosins, all of which possess tandem isoleucine-glutamine (IQ) structural domains. Using the split-luciferase complementation assay in planta and the yeast 2-hybrid system, CML13 and CML14 showed a preference for interaction with tandem over single IQ domains. Relative to CaM, CML13 and CML14 displayed weaker signals when tested with the non-IQ, CaM-binding domain of glutamate decarboxylase or the single IQ domains of CNGC20 (cyclic-nucleotide gated channel-20) or IQM1 (IQ motif protein1). We examined IQD14 as a representative tandem IQ-protein and found that only CaM, CML13, and CML14 interacted with IQD14 among 12 CaM/CMLs tested. CaM, CML13, and CML14 bound in vitro to IQD14 in the presence or absence of Ca 2+ . Binding affinities were in the nM range and were higher when two tandem IQ domains from IQD14 were present. Green fluorescent protein-tagged versions of CaM, CML13, and CML14 localized to both the cytosol and nucleus in plant cells but were partially relocalized to the microtubules when co-expressed with IQD14 tagged with mCherry. These and other data are discussed in the context of possible roles for these CMLs in gene regulation via CAMTAs and cytoskeletal activity via myosins and IQD proteins.

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  1. 10.1186/1471-2148-5-72 · DOI
  2. 10.1111/j.1365-313X.2006.02883.x · DOI
  3. Aldon, D. , Mbengue, M. , Mazars, C. & Galaud, J.-P . (2018) Calcium Signalling in Plant Biotic Interactions. Int. J. Mol. Sci., 19. · DOI
  4. 1988, Identification and characterization of the calmodulin-binding domain of neuromodulin, a neurospecific calmodulin-binding protein, J. Biol. Chem, 263, 7544, 10.1016/S0021-9258(18)68533-3 · DOI
  5. 10.1006/abio.2002.5661 · DOI
  6. 2020, Structural Aspects and Prediction of Calmodulin-Binding Proteins, International Journal of Molecular Sciences, 22, 308, 10.3390/ijms22010308 · DOI
  7. 10.1042/BSR20100123 · DOI
  8. 10.1016/S0014-5793(01)03239-2 · DOI
  9. 10.1104/pp.107.4.1201 · DOI
  10. 2011, pep2pro: a new tool for comprehensive proteome data analysis to reveal information about organ-specific proteomes in Arabidopsis thaliana, Integr. Biol, 3, 225, 10.1039/c0ib00078g · DOI
  11. 2015, Within leaf variation is the largest source of variation in agroinfiltration of Nicotiana benthamiana, Plant Methods, 11, 47, 10.1186/s13007-015-0091-5 · DOI
  12. 10.1042/BJ20131080 · DOI
  13. 10.1111/tpj.12323 · DOI
  14. 10.1104/pp.113.221069 · DOI
  15. 10.1016/j.ceca.2003.10.005 · DOI
  16. 10.1074/jbc.M200268200 · DOI
  17. 2000, Yeast myosin light chain, Mlc1p, interacts with both IQGAP and class II myosin to effect cytokinesis, J. Cell Sci., 113, 4533, 10.1242/jcs.113.24.4533 · DOI
  18. 10.1016/0003-2697(76)90527-3 · DOI · Paper page
  19. Brandizzi, F. , Irons, S. , Kearns, A. & Hawes, C . (2003) BY-2 cells: culture and transformation for live cell imaging. Curr. Protoc. Cell Biol., Chapter 1, Unit 1.7. · DOI
  20. 10.1038/nprot.2016.044 · DOI
  21. 10.1104/pp.16.01743 · DOI
  22. 10.1074/jbc.M112.396200 · DOI
  23. 10.1104/pp.107.111740 · DOI
  24. 10.1016/S0959-440X(99)80055-4 · DOI
  25. 2018, The contribution of organelles to plant intracellular Calcium signalling, J. Exp. Bot, 17, 4175
  26. 10.1021/bi2007178 · DOI
  27. 10.1074/jbc.M508670200 · DOI
  28. 10.1042/BJ20091147 · DOI
  29. 10.1105/tpc.15.00870 · DOI
  30. 10.1016/j.febslet.2010.10.059 · DOI
  31. 10.1042/bj20030656 · DOI
  32. 10.1371/journal.pone.0010098 · DOI
  33. 10.1074/jbc.M109.056770 · DOI
  34. 10.1146/annurev-arplant-070109-104628 · DOI
  35. 10.1002/prot.24215 · DOI
  36. 10.1093/pcp/pct021 · DOI
  37. 10.1042/BJ20070255 · DOI
  38. Golomb, L. , Abu-Abied, M. , Belausov, E. & Sadot, E . (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biology, 8. · DOI
  39. 10.1046/j.1462-2920.2002.00362.x · DOI
  40. 10.1093/pcp/pcy147 · DOI
  41. 10.1074/jbc.M113.521716 · DOI
  42. 10.1080/19490992.2015.1054092 · DOI
  43. 10.1074/jbc.M003132200 · DOI
  44. 10.1073/pnas.0609436103 · DOI
  45. 10.1073/pnas.0508640103 · DOI
  46. 2020, Ca2+/Calmodulin Complex Triggers CAMTA Transcriptional Machinery Under Stress in Plants: Signaling Cascade and Molecular Regulation, Front. Plant Sci, 11, 598327, 10.3389/fpls.2020.598327 · DOI
  47. 10.1152/physrev.1999.79.3.661 · DOI
  48. 10.1002/pro.3233 · DOI
  49. 10.1016/j.bbapap.2005.06.005 · DOI
  50. 10.1105/tpc.16.00669 · DOI
  51. 10.1105/tpc.16.00865 · DOI
  52. 2019, Calcium-and calmodulin-regulated microtubule-associated proteins as signal-integration hubs at the plasma membrane-cytoskeleton nexus, J. Exp. Bot, 70, 387, 10.1093/jxb/ery397 · DOI
  53. 2018, Advances and current challenges in calcium signaling, New Phytol, 218, 414, 10.1111/nph.14966 · DOI
  54. 2021, IQ67 DOMAIN proteins facilitate preprophase band formation and division-plane orientation, Nat Plants, 7, 739, 10.1038/s41477-021-00923-z · DOI
  55. 10.1074/jbc.M116.746313 · DOI
  56. La Verde, V. , Dominici, P. & Astegno, A. (2018) Towards Understanding Plant Calcium Signaling through Calmodulin-Like Proteins: A Biochemical and Structural Perspective. Int. J. Mol. Sci., 19. · DOI
  57. 10.1111/j.1365-313X.2012.05045.x · DOI
  58. 2021, Ca2+talyzing Initial Responses to Environmental Stresses, Trends in Plant Science, 26, 849, 10.1016/j.tplants.2021.02.007 · DOI
  59. 10.1016/j.str.2017.02.002 · DOI
  60. 2015, Combining modelling and experimental approaches to explain how calcium signatures are decoded by calmodulin-binding transcription activators (CAMTAs) to produce specific gene expression responses, New Phytol, 208, 174, 10.1111/nph.13428 · DOI
  61. 10.1074/jbc.M208579200 · DOI
  62. McAinsh, M.R. & Ng, C.K.-Y . (2013) Measurement of Cytosolic-Free Ca2+ in Plant Tissue. Methods in Molecular Biology, 327–341. · DOI
  63. 10.1046/j.1469-8137.2003.00845.x · DOI
  64. 10.1016/j.tplants.2005.07.001 · DOI
  65. 2015, Dynamic visualization of calcium-dependent signaling in cellular microdomains, Cell Calcium, 58, 333, 10.1016/j.ceca.2015.01.009 · DOI
  66. 10.1093/jxb/erl009 · DOI
  67. 10.1038/nprot.2007.360 · DOI
  68. 1962, A revised medium for rapid growth and bioassays with tobacco tissue cultures, Physiologia Pl, 15, 473, 10.1111/j.1399-3054.1962.tb08052.x · DOI
  69. 10.1093/jxb/ery395 · DOI
  70. Ogunrinde, A. , Munro, K. , Davidson, A. , Ubaid, M. & Snedden, W.A . (2017) Arabidopsis Calmodulin-Like Proteins, CML15 and CML16 Possess Biochemical Properties Distinct from Calmodulin and Show Non-overlapping Tissue Expression Patterns. Frontiers in Plant Science, 8. · DOI
  71. 10.1146/annurev.arplant.59.032607.092839 · DOI
  72. 10.1007/s11010-008-9855-9 · DOI
  73. 2020, SAC3B is a target of CML19, the centrin 2 of Arabidopsis thaliana, Biochem. J, 477, 173, 10.1042/BCJ20190674 · DOI
  74. 10.3389/fpls.2012.00184 · DOI
  75. 10.1074/jbc.274.11.6827 · DOI
  76. 10.1104/pp.113.220780 · DOI
  77. 10.1074/jbc.M117.809632 · DOI
  78. 10.1038/nmeth.2089 · DOI · Paper page
  79. 10.1093/mp/ssu102 · DOI
  80. 10.1073/pnas.1607702113 · DOI
  81. 10.1038/msb.2011.80 · DOI
  82. 10.1371/journal.pone.0061765 · DOI
  83. 2019, An RK/ST C-terminal motif is required for targeting of OEP7.2 and a subset of other arabidopsis tail-anchored proteins to the plastid outer envelope membrane, Plant and Cell Physiology, 60, 516, 10.1093/pcp/pcy234 · DOI
  84. 2020, Calcium spikes, waves and oscillations in plant development and biotic interactions, Nat Plants, 6, 750, 10.1038/s41477-020-0667-6 · DOI
  85. 10.1111/tpj.12043 · DOI
  86. 10.1104/pp.112.198150 · DOI
  87. 2016, Metal binding affinity and structural properties of calmodulin-like protein 14 from Arabidopsis thaliana, Protein Sci, 25, 1461, 10.1002/pro.2942 · DOI
  88. 10.1007/s11103-007-9189-0 · DOI
  89. 10.1002/pmic.201400441 · DOI
  90. Wendrich, J. R. , Yang, B.-J. , Mijnhout, P. , Xue, H.-W. , Rybel, B. De , & Weijers, D. (2018) IQD proteins integrate auxin and calcium signaling to regulate microtubule dynamics during Arabidopsis development. BioRxiv, 275560. https://doi.org/10.1101/275560 · DOI
  91. 10.3389/fpls.2016.01296 · DOI
  92. 2019, The Plant PTM Viewer, a central resource for exploring plant protein modifications, Plant J, 99, 752, 10.1111/tpj.14345 · DOI
  93. 10.1371/journal.pone.0000718 · DOI
  94. Wu, S.-Z. & Bezanilla, M . (2014) Myosin VIII associates with microtubule ends and together with actin plays a role in guiding plant cell division. eLife, 3. · DOI
  95. 10.1126/science.1203877 · DOI
  96. 10.1038/nsb0995-758 · DOI
  97. 10.1016/j.tplants.2015.05.010 · DOI
  98. 2022, Calmodulin-like protein CML24 interacts with CAMTA2 and WRKY46 to regulate ALMT1-dependent Al resistance in Arabidopsis thaliana, New Phytol, 233, 2471, 10.1111/nph.17812 · DOI

Metadata

Authors
Teresinski, H. J., Hau, B., Symonds, K., Kilburn, R., Munro, K. A., Doner, N. M., Mullen, R., Li, V. H., & Snedden, W. A.
Affiliations
  • Queen's University (CA)
  • McGill University (CA)
  • University of Guelph (CA)
Corresponding author
Snedden, Wayne A.
ORCID
Venue
Plant Cell & Environment
Publisher
openRxiv
Published
2023-03-12
Volume
46
Issue
8
Pages
2470-2491
ISSN
0140-7791 (ISSN-L)
DOI
10.1101/2023.03.09.531943
OpenAlex
W4377940205
Cited by
21
References
1
Citations by year
2026: 4 · 2025: 2 · 2024: 12 · 2023: 3
FWCI
3.31
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • Plant Cell & Environment (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
  • Queen's University
  • Natural Sciences and Engineering Research Council of Canada
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant and Biological Electrophysiology Studies
Keywords
calmodulin-like proteins, calmodulin, IQ domain, protein-protein interaction, calcium signaling, myosin, subcellular localization, microtubules, gene expression regulation, Arabidopsis thaliana
MeSH terms
Calcium, Calmodulin, Protein Binding, Saccharomyces cerevisiae, Arabidopsis, Calcium Signaling, Arabidopsis Proteins

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