Plant Molecular Biology

, Volume 96, Issue 4–5, pp 375–392 | Cite as

The calmodulin-like protein, CML39, is involved in regulating seed development, germination, and fruit development in Arabidopsis

  • Ubaid Midhat
  • Michael K. Y. Ting
  • Howard J. Teresinski
  • Wayne A. Snedden


Key message

We show that the calcium sensor, CML39, is important in various developmental processes from seeds to mature plants. This study bridges previous work on CML39 as a stress-induced gene and highlights the importance of calcium signalling in plant development.


In addition to the evolutionarily-conserved Ca2+ sensor, calmodulin (CaM), plants possess a large family of CaM-related proteins (CMLs). Using a cml39 loss-of-function mutant, we investigated the roles of CML39 in Arabidopsis and discovered a range of phenotypes across developmental stages and in different tissues. In mature plants, loss of CML39 results in shorter siliques, reduced seed number per silique, and reduced number of ovules per pistil. We also observed changes in seed development, germination, and seed coat properties in cml39 mutants in comparison to wild-type plants. Using radicle emergence as a measure of germination, cml39 mutants showed more rapid germination than wild-type plants. In marked contrast to wild-type seeds, the germination of developing, immature cml39 seeds was not sensitive to cold-stratification. In addition, germination of cml39 seeds was less sensitive than wild-type to inhibition by ABA or by treatments that impaired gibberellic acid biosynthesis. Tetrazolium red staining indicated that the seed-coat permeability of cml39 seeds is greater than that of wild-type seeds. RNA sequencing analysis of cml39 seedlings suggests that changes in chromatin modification may underlie some of the phenotypes associated with cml39 mutants, consistent with previous reports that orthologs of CML39 participate in gene silencing. Aberrant ectopic expression of transcripts for seed storage proteins in 7-day old cml39 seedlings was observed, suggesting mis-regulation of early developmental programs. Collectively, our data support a model where CML39 serves as an important Ca2+ sensor during ovule and seed development, as well as during germination and seedling establishment.


Calcium Signal transduction Calmodulin CML Arabidopsis Development 



We are grateful to Profs. Sharon Regan and Jacqueline Monaghan (Queen’s Univ) for helpful discussions. This research was financially supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery, and Research Tool and Infrastructure grants to WAS.

Author contributions

WAS designed and supervised this study. UM and HJT designed and performed the experiments. MKYT contributed to bioinformatic data analysis. All authors contributed to writing, editing, and approval of the article.

Supplementary material

11103_2018_703_MOESM1_ESM.pdf (22.6 mb)
Supplementary material 1 (PDF 23152 KB)
11103_2018_703_MOESM2_ESM.xlsx (225 kb)
Supplementary material 2 (XLSX 225 KB)
11103_2018_703_MOESM3_ESM.pdf (61 kb)
Supplementary material 3 (PDF 60 KB)


  1. Abbas N, Maurya JP, Senapati D, Gangappa SN, Chattopadhyay S (2014) Arabidopsis CAM7 and HY5 physically interact and directly bind to the HY 5 promoter to regulate its expression and thereby promote photomorphogenesis. Plant Cell 26:1036–1052.
  2. Anandalakshmi R, Marathe R, Ge X Jr, Herr J, Mau C, Mallory A, Pruss G, Bowman L, Vance VB (2000) REPORTS A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290:142–144. CrossRefPubMedGoogle Scholar
  3. Anil VS, Harmon AC, Rao KS (2000) Spatio-temporal accumulation and activity of calcium-dependent protein kinases during embryogenesis, seed development, and germination in sandalwood. Plant Physiol 122:1035–1044. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ariizumi T, Hauvermale AL, Nelson SK, Hanada A, Yamaguchi S, Steber CM (2013) Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling. Plant Physiol 162:2125–2139. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Beisson F, Li Y, Bonaventure G, Pollard M, Ohlrogge JB (2007) The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell 19:351–368. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bender KW, Snedden WA (2013) Calmodulin-related proteins step out from the shadow of their namesake. Plant Physiol 163:486–495. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bender KW, Rosenbaum DM, Vanderbeld B, Ubaid M, Snedden W (2013) The Arabidopsis calmodulin-like protein, CML39, functions during early seedling establishment. Plant J 76:634–647. CrossRefPubMedGoogle Scholar
  8. Bethke PC, Libourel IGL, Aoyama N, Chung Y-Y, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143:1173–1188. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chaiwongsar S, Strohm AK, Roe JR, Godiwalla RY, Chan CWM (2009) A cyclic nucleotide-gated channel is necessary for optimum fertility in high-calcium environments. New Phytol 183:76–87. CrossRefPubMedGoogle Scholar
  10. Chiasson D, Ekengren SK, Martin GB, Dobney SL, Snedden WA (2005) Calmodulin-like proteins from Arabidopsis and tomato are involved in host defense against Pseudomonas syringae pv. tomato. Plant Mol Biol 58:887–897. CrossRefPubMedGoogle Scholar
  11. Colville A, Alhattab R, Hu M, Labbé H, Xing T, Miki B (2011) Role of HD2 genes in seed germination and early seedling growth in Arabidopsis. Plant Cell Rep 30:1969–1979. CrossRefPubMedGoogle Scholar
  12. Corbineau F, Bianco J, Garello G, Come D (2002) Breakage of Pseudotsuga menziesii seed dormancy by cold treatment as related to changes in seed ABA sensitivity and ABA levels. Physiol Plant 114:313–319. CrossRefPubMedGoogle Scholar
  13. Cucinotta M, Colombo L, Roig-Villanova I (2014) Ovule development, a new model for lateral organ formation. Front Plant Sci 5:117. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Debeaujon I, Léon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122:403–414. CrossRefPubMedPubMedCentralGoogle Scholar
  15. DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem J 425:27–40. CrossRefGoogle Scholar
  16. Delk N, Johnson K, Chowdhury NI, Braam J (2005) CML24, regulated in expression by diverse stimuli, encodes a potential Ca2+ sensor that functions in responses to abscisic acid, daylength, and ion stress. Plant Physiol 139:240–253. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. CrossRefPubMedGoogle Scholar
  18. Dobney S, Chiasson D, Lam P, Smith SP, Snedden WA (2009) The calmodulin-related calcium sensor CML42 plays a role in trichome branching. J Biol Chem 284:31647–31657. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620. CrossRefPubMedGoogle Scholar
  20. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64-70. CrossRefPubMedGoogle Scholar
  21. Duval D, Renard M, Jaquinod M (2002) Differential expression and functional analysis of three calmodulin isoforms in germinating pea (Pisum sativum L.) seeds. 32:481–493Google Scholar
  22. Edel KH, Kudla J (2015) Increasing complexity and versatility: how the calcium signaling toolkit was shaped during plant land colonization. Cell Calcium 57:231–246. CrossRefPubMedGoogle Scholar
  23. Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415. CrossRefPubMedGoogle Scholar
  24. Gao M-J, Lydiate DJ, Li X, Lui H, Gjetvaj B, Hegedus DD, Rozwadowski K (2009) Repression of seed maturation genes by a trihelix transcriptional repressor in Arabidopsis seedlings. Plant Cell 21:54–71. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gilroy S (1996) Signal transduction in barley aleurone protoplasts is calcium dependent and independent. Plant Cell 8:2193–2209. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gomez MD, Ventimilla D, Sacristan R, Perez-Amador MA (2016) Gibberellins regulate ovule integument development by interfering with the transcription factor ATS. Plant Physiol 172:2403–2415. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Graeber K, Linkies A, Müller K, Wunchova A, Rott A, Leubner-Metzger G (2010) Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes. Plant Mol Biol 73:67–87. CrossRefPubMedGoogle Scholar
  28. Graeber K, Linkies A, Steinbrecher T, Mummenhoff K, Tarkowská D, Turečková V, Ignatz M, Sperber K, Voegele A, de Jong H, Urbanová T, Strnad M, Leubner-Metzger G (2014) DELAY OF GERMINATION 1 mediates a conserved coat-dormancy mechanism for the temperature- and gibberellin-dependent control of seed germination. Proc Natl Acad Sci USA. Google Scholar
  29. Guo Y, Xiong L, Song C-P, Gong D, Halfter U, Zhu J-K (2002) A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev Cell 3:233–244. CrossRefPubMedGoogle Scholar
  30. Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, Twell D (1998) Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149:621–631PubMedPubMedCentralGoogle Scholar
  31. Huang H-Y, Jiang W-B, Hu Y-W, Wu P, Zhu J-Y, Liang W-Q, Wang Z-Y, Lin W-H (2013) BR signal influences Arabidopsis ovule and seed number through regulating related genes expression by BZR1. Mol Plant 6:456–469. CrossRefPubMedGoogle Scholar
  32. Jiang W-B, Lin W-H (2013) Brassinosteroid functions in Arabidopsis seed development. Plant Signal Behav. Google Scholar
  33. Kong D, Ju C, Parihar A, Kim S, Cho D, Kwak JM (2015) Arabidopsis glutamate receptor homolog3.5 modulates cytosolic Ca2+ level to counteract effect of abscisic acid in seed germination. Plant Physiol 167:1630–1642. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Koornneef M, Jorna ML, Brinkhorst-van der Swan DLC, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) heynh. Theor Appl Genet 61:385–393. PubMedGoogle Scholar
  35. Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61:377–383. CrossRefGoogle Scholar
  36. Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Leba LJ, Cheval C, Ortiz-Martín I, Ranty B, Beuzón CR, Galaud JP, Aldon D (2012) CML9, an Arabidopsis calmodulin-like protein, contributes to plant innate immunity through a flagellin-dependent signalling pathway. Plant J 71:976–989. CrossRefPubMedGoogle Scholar
  38. Lee KP, Piskurewicz U, Turecková V, Strnad M, Lopez-Molina L (2010) A seed coat bedding assay shows that RGL2-dependent release of abscisic acid by the endosperm controls embryo growth in Arabidopsis dormant seeds. Proc Natl Acad Sci USA 107:19108–19113. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45:309–319. CrossRefPubMedGoogle Scholar
  40. Leon-Kloosterziel KM, Keijzer CJ, Koornneef M (1994) A seed shape mutant of Arabidopsis that is affected in integument development. Plant Cell 6:385–392. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Léon-Kloosterziel KM, van de Bunt G, Zeevaart J, Koornneef M (1996) Arabidopsis mutants with a reduced seed dormancy. Plant Physiol 110:233–240. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Leubner-Metzger G (2003) Functions and regulation of β-1,3-glucanases during seed germination, dormancy release and after-ripening. Seed Sci Res 13:17–34. CrossRefGoogle Scholar
  43. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup 1000 Genome Project Data Processing (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Linkies A, Leubner-Metzger G (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep 31:253–270. CrossRefPubMedGoogle Scholar
  45. Lokdarshi A, Conner WC, McClintock C, Li T, Roberts D (2015) Arabidopsis CML38, a calcium sensor that localizes to ribonucleoprotein complexes under hypoxia stress. Plant Physiol. PubMedPubMedCentralGoogle Scholar
  46. Losa A, Colombo M, Brambilla V, Colombo L (2010) Genetic interaction between AINTEGUMENTA (ANT) and the ovule identity genes SEEDSTICK (STK), SHATTERPROOF1 (SHP1) and SHATTERPROOF2 (SHP2). Sex Plant Reprod 23:115–121. CrossRefPubMedGoogle Scholar
  47. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Luo M, Wang Y-Y, Liu X, Yang S, Wu K (2012) HD2 proteins interact with RPD3-type histone deacetylases. Plant Signal Behav 7:608–610. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud JP, Aldon D (2008) Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J 56:575–589. CrossRefPubMedGoogle Scholar
  50. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408. CrossRefPubMedGoogle Scholar
  51. McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389. CrossRefPubMedGoogle Scholar
  52. Molina I, Ohlrogge JB, Pollard M (2007) Deposition and localization of lipid polyester in developing seeds of Brassica napus and Arabidopsis thaliana. Plant J 53:437–449. CrossRefGoogle Scholar
  53. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497.
  54. Nakahara KS, Masuta C, Yamada S, Shimura H, Kashihara Y, Wada TS, Meguro A, Goto K, Tadamura K, Sueda K, Sekiguchi T, Shao J, Itchoda N, Matsumura T, Igarashi M, Ito K, Carthew RW, Uyeda I (2012) Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. Proc Natl Acad Sci USA 109:10113–10118. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Nambara E, Naito S, McCourt P (1992) A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele. Plant J 2:435–441. CrossRefGoogle Scholar
  56. Okonechnikov K, Conesa A, García-Alcalde F (2016) Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 32:292–294. PubMedGoogle Scholar
  57. Pandey GK, Grant JJ, Cheong YH, Kim BG, Li LG, Luan S (2008) Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. Mol Plant 1:238–248. CrossRefPubMedGoogle Scholar
  58. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6:1567–1582. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Penfield S, Josse E-M, Kannangara R, Gilday AD, Halliday KJ, Graham IA (2005) Cold and light control seed germination through the bHLH Transcription Factor SPATULA. Curr Biol 15:1998–2006. CrossRefPubMedGoogle Scholar
  60. Pérez-España VH, Sánchez-León N, Vielle-Calzada J-P (2011) CYP85A1 is required for the initiation of female gametogenesis in Arabidopsis thaliana. Plant Signal Behav 6:321–326CrossRefPubMedPubMedCentralGoogle Scholar
  61. Piskurewicz U, Turečková V, Lacombe E, Lopez-Molina L (2009) Far-red light inhibits germination through DELLA-dependent stimulation of ABA synthesis and ABI3 activity. EMBO J 28:2259–2271. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Pitorre D, Llauro C, Jobet E, Guilleminot J, Brizard JP, Delseny M, Lasserre E (2010) RLK7, a leucine-rich repeat receptor-like kinase, is required for proper germination speed and tolerance to oxidative stress in Arabidopsis thaliana. Planta 232:1339–1353. CrossRefPubMedGoogle Scholar
  63. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Ris CH, Op T, Pl H (2005) Calcium: just another regulator in the machinery of life?
  65. Ritchie S, Swanson SJ, Gilroy S (2000) Physiology of the aleurone layer and starchy endosperm during grain development and early seedling growth: new insights from cell and molecular biology. Seed Sci Res 10:193–212. CrossRefGoogle Scholar
  66. Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54:608–620. CrossRefPubMedGoogle Scholar
  67. Schiott M, Romanowsky SM, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101:9502–9507CrossRefPubMedPubMedCentralGoogle Scholar
  68. Schneider K, Breuer C, Kawamura A, Jikumaru Y, Hanada A, Fujioka S, Ichikawa T, Kondou Y, Matsui M, Kamiya Y, Yamaguchi S, Sugimoto K (2012) Arabidopsis PIZZA has the capacity to acylate brassinosteroids. PLoS ONE 7:e46805. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Schneitz K, Hulskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7:731–749. CrossRefGoogle Scholar
  70. Scholz SS, Vadassery J, Heyer M, Reichelt M, Bender KW, Snedden WA, Boland W, Mithöfer A (2014) Mutation of the Arabidopsis calmodulin-like protein CML37 deregulates the jasmonate pathway and enhances susceptibility to herbivory. Mol Plant 7:1712–1726. CrossRefPubMedGoogle Scholar
  71. Scrase-Field SAMG, Knight MR (2003) Calcium: just a chemical switch? Curr Opin Plant Biol 6:500–506. CrossRefPubMedGoogle Scholar
  72. Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light and hormone signals in germinating seeds. Plant Mol Biol 69:463–472. CrossRefPubMedGoogle Scholar
  73. To A, Valon C, Savino G, Guilleminot J, Devic M (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18:1642–1651. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR (2004) DELLA proteins and gibberellin-regulated seed germination and floral development. Plant Physiol 135:1008–1019. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithofer A (2012) CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. Plant Physiol 159:1159–1175. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Vanderbeld B, Snedden WA (2007) Developmental and stimulus-induced expression patterns of Arabidopsis calmodulin-like genes CML37, CML38 and CML39. Plant Mol Biol 64:683–697. CrossRefPubMedGoogle Scholar
  77. Voegele A, Linkies A, Müller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot 62:5131–5147. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Witte CP, Noel LD, Gielbert J, Parker JE, Romeis T (2004) Rapid one-step protein purification from plant material using the eight-amino acid StrepII epitope. Plant Mol Biol 55:135–147. CrossRefPubMedGoogle Scholar
  79. Wu K, Tian L, Malik K, Brown D, Miki B (2000) Functional analysis of HD2 histone deacetylase homologues in Arabidopsis thaliana. Plant J 22:19–27. CrossRefPubMedGoogle Scholar
  80. Zentella R, Zhang Z-L, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun T-P (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057. CrossRefPubMedPubMedCentralGoogle Scholar
  81. Zhang L, Du L, Poovaiah BW (2014) Calcium signaling and biotic defense responses in plants. Plant Signal Behav 9:e973818. CrossRefPubMedPubMedCentralGoogle Scholar
  82. Zhou C, Labbe H, Sridha S, Wang L, Tian L, Latoszek-Green M, Yang Z, Brown D, Miki B, Wu K (2004) Expression and function of HD2-type histone deacetylases in Arabidopsis development. Plant J 38:715–724. CrossRefPubMedGoogle Scholar
  83. Zhou L, Lan W, Chen B, Fang W, Luan S (2015) A calcium sensor-regulated protein kinase, CALCINEURIN B-LIKE PROTEIN-INTERACTING PROTEIN KINASE19, is required for pollen tube growth and polarity. Plant Physiol. Google Scholar
  84. Zhu X, Dunand C, Snedden W, Galaud J-P (2015) CaM and CML emergence in the green lineage. Trends Plant Sci 20:483–489. CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of BiologyQueen’s UniversityKingstonCanada

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