Advertisement

Protoplasma

pp 1–14 | Cite as

Cytosolic calcium localization and dynamics during early endosperm development in the genus Agave (Asparagales, Asparagaceae)

  • Angel Martín Barranco-Guzmán
  • Alejandra G. González-Gutiérrez
  • Nutan Prasad Rout
  • Jorge Verdín
  • Benjamín Rodríguez-GarayEmail author
Original Article
  • 57 Downloads

Abstract

Calcium is a secondary messenger that regulates and coordinates the cellular responses to environmental cues. Despite calcium being a key player during fertilization in plants, little is known about its role during the development of the endosperm. For this reason, the distribution, abundance, and dynamics of cytosolic calcium during the first stages of endosperm development of Agave tequilana and Agave salmiana were analyzed. Cytosolic calcium and actin filaments detected in the embryo sacs of Agave tequilana and A. salmiana revealed that they play an important role during the division and nuclear migration of the endosperm. After fertilization, a relatively high concentration of cytosolic calcium was located in the primary nucleus of the endosperm, as well as around migrating nuclei during the development of the endosperm. Cytosolic calcium participates actively during the first mitosis of the endosperm mother cell and interacts with the actin filaments that generate the motor forces during the migration of the nuclei through the large cytoplasm of the central cell.

Keywords

Actin Embryo sac Endosperm mother cell Mitosis Nuclear movement 

Notes

Acknowledgements

The authors thank L.M. Sánchez-Noriega and L. Díaz-Godínez for their help at the CIATEJ Confocal Microscopy Laboratory. Also, the authors thank the five anonymous referees that allowed the improvement of the manuscript, as well as the advice of the editor in chief and the handling editor, and to B. Rodríguez-Julián for linguistic corrections.

Funding information

This research was carried out with the support of the Frontiers of Science Program of the National Council of Science and Technology (CONACyT-Mexico), Project 544, and Project PlanTECC CONACyT-Mexico No. 2018-293362.

Supplementary material

709_2019_1366_MOESM1_ESM.pdf (536 kb)
ESM 1 (PDF 536 kb)
709_2019_1366_MOESM2_ESM.pdf (250 kb)
ESM 2 (PDF 249 kb)

References

  1. Allen GJ, Sanders D (1997) Vacuolar ion channels of higher plants. Adv Bot Res 25:217–252.  https://doi.org/10.1016/S0065-2296(08)60154-8 CrossRefGoogle Scholar
  2. Al-Mohanna FA, Caddy KW, Bolsover SR (1994) The nucleus is insulated from large cytosolic calcium ion changes. Nature 367:745–750.  https://doi.org/10.1038/367745a0 CrossRefPubMedGoogle Scholar
  3. Bajer A, Molè-Bajer J (1969) Formation of spindle fibers, kinetochore orientation, and behavior of the nuclear envelope during mitosis in endosperm. Chromosoma 27:448–484.  https://doi.org/10.1007/BF00325682 CrossRefGoogle Scholar
  4. Barrell PJ, Grossniklaus U (2005) Confocal microscopy of whole ovules for analysis of reproductive development: the elongate1 mutant affects meiosis II. Plant J 43:309–320.  https://doi.org/10.1111/j.1365-313X.2005.02456.x CrossRefPubMedGoogle Scholar
  5. Bascom CS, Winship LJ, Bezanilla M (2018) Simultaneous imaging and functional studies reveal a tight correlation between calcium and actin networks. Proc Natl Acad Sci U S A 115:2869–2878.  https://doi.org/10.1073/pnas.1711037115 CrossRefGoogle Scholar
  6. Blatt MR (2000) Ca2+ signalling and control of guard-cell volume in stomatal movements. Curr Opin Plant Biol 3:196–204.  https://doi.org/10.1016/S1369-5266(00)80065-5 CrossRefPubMedGoogle Scholar
  7. Bloom K (2001) Nuclear migration: cortical anchors for cytoplasmic dynein. Curr Biol 11:326–329.  https://doi.org/10.1016/S0960-9822(01)00176-2 CrossRefGoogle Scholar
  8. Bootman M, Fearnley C, Smyrnias I, MacDonald F, Roderick H (2009) An update on nuclear calcium signaling. J Cell Sci 1(22):2337–2350.  https://doi.org/10.1242/jcs.028100 CrossRefGoogle Scholar
  9. Brauer M, Sanders D, Stitt M (1990) Regulation of photosynthetic sucrose synthesis: a role for calcium? Planta 182:236–243.  https://doi.org/10.1007/BF00197117 CrossRefPubMedGoogle Scholar
  10. Brown RC, Lemmon BE, Nguyen H, Olsen OA (1999) Development of endosperm in Arabidopsis thaliana. Sex Plant Reprod 12:32–42.  https://doi.org/10.1007/s004970050169 CrossRefGoogle Scholar
  11. Brown RC, Lemmon BE, Nguyen H (2003) Events during the first four rounds of mitosis establish three developmental domains in the syncytial endosperm of Arabidopsis thaliana. Protoplasma 222:167–174.  https://doi.org/10.1007/s00709-003-0010-x CrossRefPubMedGoogle Scholar
  12. Bush DS (1993) Regulation of cytosolic calcium in plants. Plant Physiol 103:7–13.  https://doi.org/10.1104/pp.103.1.7 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cai G, Moscatelli A, Cresti M (1997) Cytoskeletal organization and pollen tube growth. Trends Plant Sci 2:86–91.  https://doi.org/10.1016/S1360-1385(96)10057-1 CrossRefGoogle Scholar
  14. Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262:740–744 https://doi.org/10.1126%2Fscience.8235594 CrossRefPubMedGoogle Scholar
  15. Chudzik B, Sniezko R (2003) Calcium ion presence as a trait of receptivity in tenuinucellar ovules of Galanthus nivalis L. Acta Biol Cracov Ser Bot 45:133–141Google Scholar
  16. Chytilova E, Macas J, Sliwinska E, Rafelski SM, Lambert GM, Galbraith DW (2000) Nuclear dynamics in Arabidopsis thaliana. Mol Biol Cell 11:2733–2741.  https://doi.org/10.1091/mbc.11.8.2733 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Denecke J, Carlsson LE, Vidal S, Höglund AS, Ek B, van Zeijl MJ, Palva ET (1995) The tobacco homolog of mammalian calreticulin is present in protein complexes in vivo. Plant Cell 7:391–406.  https://doi.org/10.1105/tpc.7.4.391 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Denninger P, Bleckmann A, Lausser A, Vogler F, Ott T, Ehrhardt DW, Grossmann G (2014) Male–female communication triggers calcium signatures during fertilization in Arabidopsis. Nat Commun 5:4645.  https://doi.org/10.1038/ncomms5645 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Digonnet C, Aldon D, Leduc N, Dumas C, Rougier M (1997) First evidence of a calcium transient in flowering plants at fertilization. Development 124:2867–2874PubMedGoogle Scholar
  20. Dresselhaus T, Sprunck S, Wessel GM (2016) Fertilization mechanisms in flowering plants. Curr Biol 26:R125–R139.  https://doi.org/10.1016/j.cub.2015.12.032 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Edel KH, Marchadier E, Brownlee C, Kudla J, Hetherington AM (2017) The evolution of calcium-based signalling in plants. Curr Biol 27:R667–R679.  https://doi.org/10.1016/j.cub.2017.05.020 CrossRefPubMedGoogle Scholar
  22. Escobar-Guzmán R, Zamudio-Hernández F, Gil-Vega K, Simpson J (2008) Seed production and gametophyte formation in Agave tequilana and Agave americana. Botany 86:1343–1353.  https://doi.org/10.1139/B08-099 CrossRefGoogle Scholar
  23. Fan X, Hou J, Chen X, Chaudhry F, Staiger CJ, Ren H (2004) Identification and characterization of a Ca2+-dependent actin filament-severing protein from lily pollen. Plant Physiol 136:3979–3989.  https://doi.org/10.1104/pp.104.046326 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Faure JE, Digonnet C, Dumas C (1994) An in vitro system for adhesion and fusion of maize gametes. Science 263:1598–1600.  https://doi.org/10.1126/science.263.5153.1598 CrossRefPubMedGoogle Scholar
  25. Faure JE, Rotman N, Fortuné P, Dumas C (2002) Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 30:481–488.  https://doi.org/10.1046/j.1365-313X.2002.01305.x CrossRefPubMedGoogle Scholar
  26. Foe VE, Alberts BM (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61:31–70PubMedGoogle Scholar
  27. Franklin-Tong VE (1999) Signaling and the modulation of pollen tube growth. Plant Cell 11:727–738.  https://doi.org/10.1105/tpc.11.4.727 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ge LL, Tian HQ, Russell SD (2007) Calcium function and distribution during fertilization in angiosperms. Am J Bot 94:1046–1060.  https://doi.org/10.3732/ajb.94.6.1046 CrossRefPubMedGoogle Scholar
  29. Gentry HS (1982) Agaves of continental North America. The University of Arizona Press. Tucson, ArizonaGoogle Scholar
  30. Gimona M, Djinovic-Carugo K, Kranewitter WJ, Winder SJ (2002) Functional plasticity of CH domains. FEBS Lett 513:98–106.  https://doi.org/10.1016/S0014-5793(01)03240-9 CrossRefPubMedGoogle Scholar
  31. González-Gutiérrez AG, Rodríguez-Garay B (2016) Embryogenesis in Polianthes tuberosa L var. simple: from megasporogenesis to early embryo development. SpringerPlus 5:1804.  https://doi.org/10.1186/s40064-016-3528-z CrossRefPubMedPubMedCentralGoogle Scholar
  32. González-Gutiérrez AG, Gutiérrez-Mora A, Rodríguez-Garay B (2014) Embryo sac formation and early embryo development in Agave tequilana (Asparagaceae). SpringerPlus 3:575.  https://doi.org/10.1186/2193-1801-3-575 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Grossniklaus U, Schneitz K (1998) The molecular and genetic basis of ovule and megagametophyte development. Semin Cell Dev Biol 9:227–238.  https://doi.org/10.1006/scdb.1997.0214 CrossRefPubMedGoogle Scholar
  34. Hamamura Y, Nishimaki M, Takeuchi H, Geitmann A, Kurihara D, Higashiyama T (2014) Live imaging of calcium spikes during double fertilization in Arabidopsis. Nat Commun 5:4722.  https://doi.org/10.1038/ncomms5722 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Harada A, Shimazaki KI (2007) Phototropins and blue light-dependent calcium signaling in higher plants. Photochem Photobiol 83:102–111.  https://doi.org/10.1562/2006-03-08-IR-837 CrossRefPubMedGoogle Scholar
  36. Hepler PK (1994) The role of calcium in cell division. Cell Calcium 16:322–330.  https://doi.org/10.1016/0143-4160(94)90096-5 CrossRefPubMedGoogle Scholar
  37. Hepler PK (2016) The cytoskeleton and its regulation by calcium and protons. Plant Physiol 170:3–22.  https://doi.org/10.1104/pp.15.01506 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hetzer MW (2010) The nuclear envelope. CSH Perspect Biol 2:a000539.  https://doi.org/10.1101/cshperspect.a000539 CrossRefGoogle Scholar
  39. Higashiyama T (2002) The synergid cell: attractor and acceptor of the pollen tube for double fertilization. J Plant Res 115:149–160.  https://doi.org/10.1007/s102650200020 CrossRefPubMedGoogle Scholar
  40. Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T (1997) Kinetics of double fertilization in Torenia fournieri based on direct observations of the naked embryo sac. Planta 203:101–110.  https://doi.org/10.1007/s00050170 CrossRefGoogle Scholar
  41. Himschoot E, Beeckman T, Friml J, Vanneste S (2015) Calcium is an organizer of cell polarity in plants. BBA-Mol Cell Res 1853:2168–2172.  https://doi.org/10.1016/j.bbamcr.2015.02.017 CrossRefGoogle Scholar
  42. Huang BQ, Russell SD (1994) Fertilization in Nicotiana tabacum: cytoskeletal modifications in the embryo sac during synergid degeneration. Planta 194:200–214.  https://doi.org/10.1007/BF01101679 CrossRefGoogle Scholar
  43. Huang BQ, Sheridan WF (1998) Actin coronas in normal and indeterminate gametophyte1 embryo sacs of maize. Sex Plant Reprod 11:257–264.  https://doi.org/10.1007/s004970050151 CrossRefGoogle Scholar
  44. Huang BQ, Fu Y, Zee SY, Hepler PK (1999) Three-dimensional organization and dynamic changes of the actin cytoskeleton in embryo sacs of Zea mays and Torenia fournieri. Protoplasma 209:105–119.  https://doi.org/10.1007/BF01415706 CrossRefPubMedGoogle Scholar
  45. Iwano M, Ngo QA, Entani T, Shiba H, Nagai T, Miyawaki A, Takayama S (2012) Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells. Development 139:4202–4209.  https://doi.org/10.1242/dev.081208 CrossRefPubMedGoogle Scholar
  46. Janmey PA (1994) Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu Rev Physiol 56:169–191.  https://doi.org/10.1146/annurev.ph.56.030194.001125 CrossRefPubMedGoogle Scholar
  47. Jenkins GI (1998) Signal transduction networks and the integration of responses to environmental stimuli. Adv Bot Res 29:54–73.  https://doi.org/10.1016/S0065-2296(08)60308-0 CrossRefGoogle Scholar
  48. Jinsong Z, Hongyuan Y (1995) Ultracytochemical localization of calcium in the stigma, style and micropyle of sunflower. Acta Bot Sin 37:691–696Google Scholar
  49. Kaneuchi T, Sartain CV, Takeo S, Horner VL, Buehner NA, Aigaki T, Wolfner MF (2015) Calcium waves occur as Drosophila oocytes activate. Proc Natl Acad Sci U S A 112:791–796.  https://doi.org/10.1073/pnas.1420589112 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kite GL (1913) The relative permeability of the surface and interior portions of the cytoplasm of animal and plant cells. Biol Bull 25:1–7. http://www.jstor.org/stable/1536080. Accessed 16 Apr 2018CrossRefGoogle Scholar
  51. 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.  https://doi.org/10.1038/352524a0 CrossRefPubMedGoogle Scholar
  52. Krause KH, Michalak M (1997) Calreticulin. Cell 88:439–443.  https://doi.org/10.1016/S0092-8674(00)81884-X CrossRefPubMedGoogle Scholar
  53. Kristóf Z, Tímár O, Imre K (1999) Changes of calcium distribution in ovules of Torenia fournieri during pollination and fertilization. Protoplasma 208:149–155.  https://doi.org/10.1007/BF01279085 CrossRefGoogle Scholar
  54. Kutay U, Hetzer MW (2008) Reorganization of the nuclear envelope during open mitosis. Curr Opin Cell Biol 20:669–677.  https://doi.org/10.1016/j.ceb.2008.09.010 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Lenartowska M, Karaś K, Marshall J, Napier R, Bednarska E (2002) Immunocytochemical evidence of calreticulin-like protein in pollen tubes and styles of Petunia hybrida Hort. Protoplasma 219:23–30.  https://doi.org/10.1007/s007090200002 CrossRefPubMedGoogle Scholar
  56. Lenartowski R, Suwińska A, Lenartowska M (2015) Calreticulin expression in relation to exchangeable Ca2+ level that changes dynamically during anthesis, progamic phase, and double fertilization in Petunia. Planta 241:209–227.  https://doi.org/10.1007/s00709-017-1134-8 CrossRefPubMedGoogle Scholar
  57. Li L, Lin F, Qu Y, Zhang Q (2015) A protocol to measure the cytoplasmic calcium in Arabidopsis guard cells. Bio-protocol:e1462.  https://doi.org/10.21769/BioProtoc.1462
  58. Macer DRJ, Koch GLE (1988) Identification of a set of calcium binding proteins in reticuloplasm, the luminal content of the endoplasmic reticulum. J Cell Sci 91:61–70PubMedGoogle Scholar
  59. Mauger JP (2012) Role of the nuclear envelope in calcium signaling. Biol Cell 104:70–83.  https://doi.org/10.1111/boc.201100103 CrossRefPubMedGoogle Scholar
  60. Meng, G., Pan, L., Li, C., Hu, F., Shi, X., Lee, I., and Xu, J. (2014). Temperature-induced labelling of Fluo-3 AM selectively yields brighter nucleus in adherent cells. Biochem Biophys Res Commun 443:888–893.  https://doi.org/10.1016/j.bbrc.2013.12.105
  61. Mery L, Mesaeli N, Michalak M, Opas M, Lew DP, Krause KH (1996) Overexpression of calreticulin increases intracellular Ca2+ storage and decreases store operated Ca2+ influx. J Biol Chem 271:9332–9339CrossRefPubMedGoogle Scholar
  62. Michalak M, Milner RE, Burns K, Opas M (1992) Calreticulin. Biochem J 258:681–692.  https://doi.org/10.1007/978-3-662-06203-6 CrossRefGoogle Scholar
  63. Mòl R, Matthys-Rochon E, Dumas C (1994) The kinetics of cytological events during double fertilization in Zea mays L. Plant J 5:197–206.  https://doi.org/10.1046/j.1365-313X.1994.05020197.x CrossRefGoogle Scholar
  64. Mühlhäusser P, Kutay U (2007) An in vitro nuclear disassembly system reveals a role for the RanGTPase system and microtubule-dependent steps in nuclear envelope breakdown. J Cell Biol 178:595–610.  https://doi.org/10.1083/jcb.200703002 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Nakamura M, Moriya M, Baba T, Michikawa Y, Yamanobe T, Arai K, Okinaga S, Kobayashi T (1993) An endoplasmic reticulum protein, calreticulin, is transported into the acrosome of rat sperm. Exp Cell Res 205:101–110.  https://doi.org/10.1006/excr.1993.1063 CrossRefPubMedGoogle Scholar
  66. Nelson DE, Glaunsinger B, Bohnert HJ (1997) Abundant accumulation of the calcium-binding molecular chaperone calreticulin in specific floral tissues of Arabidopsis thaliana. Plant Physiol 114:29–37.  https://doi.org/10.1104/pp.114.1.29 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Nguyen H, Brown R, Lemmon B (2002) Cytoskeletal organization of the micropylar endosperm in Coronopus didymus L. (Brassicaceae). Protoplasma 219:210–220.  https://doi.org/10.1007/s007090200022 CrossRefPubMedGoogle Scholar
  68. Nguyen H, Brown RC, Lemmon BE (2001) Patterns of cytoskeletal organization reflect distinct developmental domains in endosperm of Coronopus didymus (Brassicaceae). Int J Plant Sci 162:1–14.  https://doi.org/10.1086/317898 CrossRefGoogle Scholar
  69. Niedojadło K, Lenartowski R, Lenartowska M, Bednarska-Kozakiewicz E (2015) Late progamic phase and fertilization affect calreticulin expression in the Hyacinthus orientalisfemale gametophyte. Plant Cell Rep 34:2201–2215.  https://doi.org/10.1007/s00299-015-1863-0 CrossRefPubMedPubMedCentralGoogle Scholar
  70. O’Malley DM, Burbach BJ, Adams PR (1999) Fluorescent calcium indicators: subcellular behavior and use in confocal imaging. In: Paddock SW (ed) Confocal microscopy methods and protocols. Methods in molecular biology, Vol 122. Humana Press, New York CityGoogle Scholar
  71. Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Phys 52:233–267.  https://doi.org/10.1146/annurev.arplant.52.1.233 CrossRefGoogle Scholar
  72. Pidcock E, Moore GR (2001) Structural characteristics of protein binding sites for calcium and lanthanide ions. J Biol Inorg Chem 6:479–489.  https://doi.org/10.1007/s007750100214 CrossRefPubMedGoogle Scholar
  73. Piven NM, Barredo-Pool FA, Borges-Argáez IC, Herrera-Alamillo MA, Mayo-Mosqueda A, Herrera-Herrera JL, Robert ML (2001) Reproductive biology of henequen (Agave fourcroydes) and its wild ancestor Agave angustifolia (Agavaceae). I. Gametophyte development. Am J Bot 88:1966–1976.  https://doi.org/10.2307/3558424 CrossRefPubMedGoogle Scholar
  74. Puhka M, Vihinen H, Joensuu M, Jokitalo E (2007) Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells. J Cell Biol 179:895–909.  https://doi.org/10.1083/jcb.200705112 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rodríguez-Garay B, López-Díaz S, Rodríguez-Domínguez JM, Gutiérrez-Mora A, Tapia-Campos E (2018) Application of in casa pollination and embryo rescue techniques for breeding of Agave species. In press: Víctor M Loyola-Vargas, Neftalí Ochoa-Alejo (eds.), Plant Cell Culture Protocols, Methods in Molecular Biology, vol. 1815.  https://doi.org/10.1007/978-1-4939-8594-4_20
  76. Rudd JJ, Franklin-Tong VE (1999) Calcium signaling in plants. Cell Mol Life Sci 55:214–232.  https://doi.org/10.1007/s000180050286 CrossRefPubMedGoogle Scholar
  77. Russell SD (1992) Double fertilization. Int Rev Cytol 140:357–388CrossRefGoogle Scholar
  78. Salmon ED (1982) Calcium, spindle microtubule dynamics and chromosome movement. Cell Differ 11:353–355.  https://doi.org/10.1016/0045-6039(82)90057-4 CrossRefGoogle Scholar
  79. Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706.  https://doi.org/10.1105/tpc.11.4.691 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Schel JHN, Kieft H (1986) An ultrastructural study of embryo and endosperm development during in vitro culture of maize ovaries (Zea mays). Can J Botany 64:2227–2238.  https://doi.org/10.1139/b86-297 CrossRefGoogle Scholar
  81. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675.  https://doi.org/10.1038/nmeth.2089 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Shacklock PS, Read ND, Trewavas AJ (1992) Cytosolic free calcium mediates red light induced photomorphogenesis. Nature 358:53–155  https://doi.org/10.1038/358753a0 CrossRefGoogle Scholar
  83. Sinclair W, Trewavas AJ (1997) Calcium in gravitropism: re-examination. Planta 203:585–590.  https://doi.org/10.1007/PL00008120 CrossRefGoogle Scholar
  84. Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T (2012) Egg cell–secreted EC1 triggers sperm cell activation during double fertilization. Science 338:1093–1097.  https://doi.org/10.1126/science.1223944 CrossRefPubMedGoogle Scholar
  85. Starr DA, Han M (2003) ANChors away: an actin based mechanism of nuclear positioning. J Cell Sci 116:211–216 http://jcs.biologists.org/content/116/2/211 CrossRefPubMedGoogle Scholar
  86. Steinhorst L, Kudla J (2013) Calcium-a central regulator of pollen germination and tube growth. BBA-Mol Cell Res 1833:1573–1581.  https://doi.org/10.1016/j.bbamcr.2012.10.009 CrossRefGoogle Scholar
  87. Subramanian K, Meyer T (1997) Calcium-induced restructuring of nuclear envelope and endoplasmic reticulum calcium stores. Cell 89:963–971.  https://doi.org/10.1016/S0092-8674(00)80281-0 CrossRefPubMedGoogle Scholar
  88. Suwińska A, Lenartowski R, Smoliński DJ, Lenartowska M (2015) Molecular evidence that rough endoplasmic reticulin is the site of calreticulin translation in Petunia pollen tubes growing in vitro. Plant Cell Rep 34:1189–1899.  https://doi.org/10.1007/s00299-015-1777-x CrossRefPubMedPubMedCentralGoogle Scholar
  89. Suwińska A, Wasąg P, Zakrzewski P, Lenartowska M, Lenartowski R (2017) Calreticulin is required for calcium homeostasis and proper pollen tube tip growth in Petunia. Planta 245:909–926.  https://doi.org/10.1007/s00425-017-2649-0 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Świerczyńska J, Kozieradzka-Kiszkurno M, Bohdanowicz J (2013) Rhinanthus serotinus (Schönheit) Oborny (Scrophulariaceae): immunohistochemical and ultrastructural studies of endosperm chalazal haustorium development. Protoplasma 250:1369–1380.  https://doi.org/10.1007/s00709-013-0520-0 CrossRefPubMedGoogle Scholar
  91. Tang TS, Dong JB, Huang XY, Sun FZ (2000) Ca2+ oscillations induced by a cytosolic sperm protein factor are mediated by a maternal machinery that functions only once in mammalian eggs. Development 127:1141–1150PubMedGoogle Scholar
  92. Taylor LP, Hepler PK (1997) Pollen germination and tube growth. Annu Rev Plant Phys 48:461–491.  https://doi.org/10.1146/annurev.arplant.48.1.461 CrossRefGoogle Scholar
  93. Tian HQ, Russell SD (1997) Calcium distribution in fertilized and unfertilized ovules and embryo sacs of Nicotiana tabacum L. Planta 202:93–105.  https://doi.org/10.1007/s004250050107 CrossRefGoogle Scholar
  94. Tian HQ, Zhu H, Russell SD (2000) Calcium changes in ovules and embryo sacs of Plumbago zeylanica L. Sex Plant Reprod 13:11–20.  https://doi.org/10.1007/PL00009837 CrossRefGoogle Scholar
  95. Tianl GW, You RL, Guo FL, Wang XC (1998) Microtubular cytoskeleton of free endosperm nuclei during division in wheat. Cytologia 63:427–433.  https://doi.org/10.1508/cytologia.63.427 CrossRefGoogle Scholar
  96. Tiwari SC (1983) The hypostase in Torenia fournieri Lind.: a histochemical study of the cell walls. Ann Bot 51:17–26.  https://doi.org/10.1093/oxfordjournals.aob.a086446 CrossRefGoogle Scholar
  97. Van Lammeren AAM, Kieft H, Ma F, Van Veenendaal WLH (1996) Light microscopical study of endosperm formation in Brassica napus L. Acta Soc Bot Pol 65:267–272.  https://doi.org/10.5586/asbp.1996.040 CrossRefGoogle Scholar
  98. Vollbrecht E, Hake S (1995) Deficiency analysis of female gametogenesis in maize. Genesis. 16:44–63.  https://doi.org/10.1002/dvg.1020160109 CrossRefGoogle Scholar
  99. Wang C, Xu W, Jin H, Zhang T, Lai J, Zhou X, Zhang S, Liu S, Duan X, Wang H, Peng C, Yang C (2016) A putative chloroplast-localized Ca2+/ H+ antiporter CCHA1 is involved in calcium and pH homeostasis and required for PSII function in Arabidopsis. Mol Plant 9:1183–1196.  https://doi.org/10.1016/j.molp.2016.05.015 CrossRefPubMedGoogle Scholar
  100. Wasąg P, Suwińska A, Zakrzewski P, Walczewski J, Lenartowski R, Lenartowska M (2018) Calreticulin localizes to plant intra/extracellular peripheries of highly specialized cells involved in pollen-pistil interactions. Protoplasma 255:57–67.  https://doi.org/10.1007/s00709-017-1134-8 CrossRefPubMedGoogle Scholar
  101. Weisenberg RC (1972) Microtubule formation in vitro in solutions containing low calcium concentrations. Science 177:1104–1105.  https://doi.org/10.1126/science.177.4054.1104 CrossRefPubMedGoogle Scholar
  102. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot-London 92:487–511.  https://doi.org/10.1093/aob/mcg164 CrossRefGoogle Scholar
  103. Wolniak SM, Hepler PK, Jackson WT (1980) Detection of the membrane-calcium distribution during mitosis in Haemanthus endosperm with chlorotetracycline. J Cell Biol 87:23–32.  https://doi.org/10.1083/jcb.87.1.23 CrossRefPubMedGoogle Scholar
  104. XuHan X, Lammeren AV (1994) Microtubular configurations during endosperm development in Phaseolus vulgaris. Can J Botany 72:1489–1495.  https://doi.org/10.1139/b94-183 CrossRefGoogle Scholar
  105. Yang J, Zhao J, Liang SP, Yang HY (2002) Ultracytochemical localization of calcium in rice central cell before and after fertilization. Acta Biol Cracov Ser Bot 44:223–230Google Scholar
  106. Yuan M, Fu Y, Wang F, Huang B, Sze-Yong Z, Hepler PK (2002) Fertilization in Torenia fournieri: actin organization and nuclear behavior in the central cell and primary endosperm. Sci China Ser C 45:211–224.  https://doi.org/10.1360/02yc9024 CrossRefGoogle Scholar
  107. Zhang G, Cass DD (1997) Calcium signaling in sexual reproduction of flowering plants. Rec Res Dev Plant Physiol 1:75–83Google Scholar
  108. Zhang DH, Wadsworth P, Hepler PK (1992) Modulation of anaphase spindle microtubule structure in stamen hair cells of Tradescantia by calcium and related agents. J Cell Sci 102:79–89Google Scholar
  109. Zhang WH, Rengel Z, Kuo J (1998) Determination of intracellular Ca2+ in cells of intact wheat roots: loading of acetoxymethyl ester of Fluo-3 under low temperature. Plant J 15:147–151.  https://doi.org/10.1046/j.1365-313X.1998.00188.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Unidad de Biotecnología Vegetal, Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco, A.C.ZapopanMexico
  2. 2.Unidad de Biotecnología Industrial, Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco, A.C.ZapopanMexico

Personalised recommendations