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Generation of Transgenic Spores of the Fern Ceratopteris richardii to Analyze Ca2+ Transport Dynamics During Gravity-Directed Polarization

  • Ashley E. Cannon
  • Mari L. Salmi
  • Araceli Cantero
  • Stanley J. Roux
Chapter

Abstract

Spores from the fern, Ceratopteris richardii, have been used to study gravity-directed cell polarization for over three decades. This system is ideal for these studies because it has a highly predictable growth and developmental pattern and primarily responds to the mechanical force of gravity during polarization. Early studies on the development in this system showed that during the first 24 h of germination, Ceratopteris spores establish a Ca2+ concentration differential along the outer periphery of the cell that is defined by the uptake of Ca2+ through channels at the bottom of the spore and an efflux of Ca2+ through pumps at the top. This 100-fold [Ca2+] differential is sensitive to the direction and magnitude of the gravitational force. In a low-gravity environment or when the uptake of Ca2+ is blocked, spore polarization becomes random. These results support the hypothesis that the uptake of Ca2+ is necessary for gravity-directed polarization in Ceratopteris spores. For many years, studies of Ceratopteris were limited by the inability to produce stable transformants. However, recent protocols have led to the first stably transformed lines in Ceratopteris richardii. This work reviews and discusses the latest studies of gravity-induced changes in Ca2+ transport dynamics in Ceratopteris spores, the use of transformation protocols to overexpress or knock out genes relevant to the transport of Ca2+ in Ceratopteris, and the potential value of mutants to more thoroughly understand the role of Ca2+ transport dynamics in gravity-directed polarization of spores.

Keywords

Annexin Apyrase Calcium channels Extracellular ATP Mechanosensitive channels Yellow Cameleon 3.60 

Notes

Acknowledgments

We acknowledge the critically valuable assistance of Dr. Benjamin Smith at the University of Oklahoma who did the FLIM imaging and video assembly and Dr. Greg Clark at the University of Texas at Austin in facilitating all the research described here, which was supported by grants NNX13AM54G and NNX15AB85A from NASA awarded to S. Roux and G. Clark.

References

  1. Aranda PS, LaJoie DM, Jorcyk CL (2012) Bleach gel: a simple agarose gel for analyzing RNA quality. Electrophoresis 33(2):366–369.  https://doi.org/10.1002/elps.201100335 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Battraw MJ, Hall TC (1990) Histochemical analysis of CaMV 35S promoter-beta-glucuronidase gene expression in transgenic rice plants. Plant Mol Biol 15(4):527–538CrossRefPubMedGoogle Scholar
  3. Behera S, Wang N, Zhang C, Schmitz-Thom I, Strohkamp S, Schultke S, Hashimoto K, Xiong L, Kudla J (2015) Analyses of Ca2+ dynamics using a ubiquitin-10 promoter-driven Yellow Cameleon 3.6 indicator reveal reliable transgene expression and differences in cytoplasmic Ca2+ responses in Arabidopsis and rice (Oryza sativa) roots. New Phytol 206(2):751–760.  https://doi.org/10.1111/nph.13250 CrossRefPubMedGoogle Scholar
  4. Belanger KD, Quatrano RS (2000) Polarity: the role of localized secretion. Curr Opin Plant Biol 3(1):67–72.  https://doi.org/10.1016/s1369-5266(99)00043-6 CrossRefPubMedGoogle Scholar
  5. Benfey PN, Chua NH (1989) Regulated genes in transgenic plants. Science (New York, NY) 244(4901):174–181.  https://doi.org/10.1126/science.244.4901.174 CrossRefGoogle Scholar
  6. Benfey PN, Ren L, Chua NH (1990) Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J 9(6):1677–1684PubMedPubMedCentralGoogle Scholar
  7. Bui LT, Cordle AR, Irish EE, Cheng CL (2015) Transient and stable transformation of Ceratopteris richardii gametophytes. BMC Res Notes 8:214.  https://doi.org/10.1186/s13104-015-1193-x CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bushart TJ, Cannon AE, Ul Haque A, San Miguel P, Mostajeran K, Clark GB, Porterfield DM, Roux SJ (2013) RNA-seq analysis identifies potential modulators of gravity response in spores of Ceratopteris (Parkeriaceae): evidence for modulation by calcium pumps and apyrase activity. Am J Bot 100(1):161–174.  https://doi.org/10.3732/ajb.1200292 CrossRefPubMedGoogle Scholar
  9. Cannon AE (2016) Investigation of the role of extracellular nucleotide gradients in plant gravity responses. Dissertation, University of Texas, AustinGoogle Scholar
  10. Chatterjee A, Porterfield DM, Smith PS, Roux SJ (2000) Gravity-directed calcium current in germinating spores of Ceratopteris richardii. Planta 210:607–610CrossRefPubMedGoogle Scholar
  11. Chatterjee A, Roux S (2000) Ceratopteris richardii: a productive model for revealing secrets of signaling and development. J Plant Growth Regul 19:284–289.  https://doi.org/10.1007/s003440000032 CrossRefPubMedGoogle Scholar
  12. Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014) Identification of a plant receptor for extracellular ATP. Science (New York, NY) 343(6168):290–294.  https://doi.org/10.1126/science.343.6168.290 CrossRefGoogle Scholar
  13. Clark G, Roux SJ (2011) Apyrases, extracellular ATP and the regulation of growth. Curr Opin Plant Biol 14(6):700–706.  https://doi.org/10.1016/j.pbi.2011.07.013 CrossRefPubMedGoogle Scholar
  14. Clark GB, Morgan RO, Fernandez MP, Roux SJ (2012) Evolutionary adaptation of plant annexins has diversified their molecular structures, interactions and functional roles. New Phytol 196(3):695–712.  https://doi.org/10.1111/j.1469-8137.2012.04308.x CrossRefPubMedGoogle Scholar
  15. Clark GB, Rafati DS, Bolton RJ, Dauwalder M, Roux SJ (2000) Redistribution of annexin in gravistimulated pea plumules. Plant Physiol Biochem 38(12):937–947.  https://doi.org/10.1016/s0981-9428(00)01206-7 CrossRefPubMedGoogle Scholar
  16. Demidchik V, Shang Z, Shin R, Colaco R, Laohavisit A, Shabala S, Davies JM (2011) Receptor-like activity evoked by extracellular ADP in Arabidopsis root epidermal plasma membrane. Plant Physiol 156(3):1375–1385.  https://doi.org/10.1104/pp.111.174722 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Demidchik V, Shang Z, Shin R, Thompson E, Rubio L, Laohavisit A, Mortimer JC, Chivasa S, Slabas AR, Glover BJ, Schachtman DP, Shabala SN, Davies JM (2009) Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. Plant J 58(6):903–913.  https://doi.org/10.1111/j.1365-313X.2009.03830.x CrossRefPubMedGoogle Scholar
  18. Deng S, Sun J, Zhao R, Ding M, Zhang Y, Sun Y, Wang W, Tan Y, Liu D, Ma X, Hou P, Wang M, Lu C, Shen X, Chen S (2015) Populus Euphratica APYRASE2 enhances cold tolerance by modulating vesicular trafficking and extracellular ATP in Arabidopsis plants. Plant Physiol 169(1):530-+.  https://doi.org/10.1104/pp.15.00581 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Edwards E, Roux S (1998) Influence of gravity and light on the developmental polarity of Ceratopteris Richardii fern spores. Planta 205(4):553–560CrossRefPubMedGoogle Scholar
  20. Edwards ES, Roux SJ (1994) Limited period of graviresponsiveness in germinating spores of Ceratopteris Richardii. Planta 195(1):150–152.  https://doi.org/10.1007/bf00206304 CrossRefPubMedGoogle Scholar
  21. Grefen C, Donald N, Hashimoto K, Kudla J, Schumacher K, Blatt MR (2010) A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. The Plant J cell Mol Biol 64(2):355–365.  https://doi.org/10.1111/j.1365-313X.2010.04322.x CrossRefGoogle Scholar
  22. Hickok L, Warne T, Fribourg R (1995) The biology of the fern Ceratopteris and its use as a model system. Int J Plant Sci 156:332–345CrossRefGoogle Scholar
  23. Hickok LG, Warne TR, Slocum MK (1987) Ceratopteris richardii: applications for experimental plant biology. Am J Bot 74:1304–1316CrossRefGoogle Scholar
  24. Hoover EE, Squier JA (2013) Advances in multiphoton microscopy technology. Nat Photon 7(2):93–101CrossRefGoogle Scholar
  25. Keinath NF, Waadt R, Brugman R, Schroeder JI, Grossmann G, Schumacher K, Krebs M (2015) Live cell imaging with R-GECO1 sheds light on flg22- and chitin-induced transient [Ca2+]cyt patterns in Arabidopsis. Mol Plant 8(8):1188–1200.  https://doi.org/10.1016/j.molp.2015.05.006 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Konopka-Postupolska D, Clark G, Hofmann A (2011) Structure, function and membrane interactions of plant annexins: an update. Plant Sci 181(3):230–241.  https://doi.org/10.1016/j.plantsci.2011.05.013 CrossRefPubMedGoogle Scholar
  27. Krebs M, Held K, Binder A, Hashimoto K, Den Herder G, Parniske M, Kudla J, Schumacher K (2012) FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca2+ dynamics. The Plant J cell Mol Biol 69(1):181–192.  https://doi.org/10.1111/j.1365-313X.2011.04780.x CrossRefGoogle Scholar
  28. Laohavisit A, Davies JM (2009) Multifunctional annexins. Plant Sci 177(6):532–539.  https://doi.org/10.1016/j.plantsci.2009.09.008 CrossRefGoogle Scholar
  29. Laohavisit A, Davies JM (2011) Annexins. New Phytol 189(1):40–53.  https://doi.org/10.1111/j.1469-8137.2010.03533.x CrossRefPubMedGoogle Scholar
  30. Laohavisit A, Shang Z, Rubio L, Cuin TA, Very AA, Wang A, Mortimer JC, Macpherson N, Coxon KM, Battey NH, Brownlee C, Park OK, Sentenac H, Shabala S, Webb AA, Davies JM (2012) Arabidopsis annexin1 mediates the radical-activated plasma membrane Ca2+- and K+-permeable conductance in root cells. Plant Cell 24(4):1522–1533.  https://doi.org/10.1105/tpc.112.097881 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lim MH, Wu J, Yao J, Gallardo IF, Dugger JW, Webb LJ, Huang J, Salmi ML, Song J, Clark G, Roux SJ (2014) Apyrase suppression raises extracellular ATP levels and induces gene expression and Cell Wall changes characteristic of stress responses. Plant Physiol 164(4):2054–2067.  https://doi.org/10.1104/pp.113.233429 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Liu X, Wu J, Clark G, Lundy S, Lim M, Arnold D, Chan J, Tang W, Muday GK, Gardner G, Roux SJ (2012) Role for apyrases in polar auxin transport in Arabidopsis. Plant Physiol 160(4):1985–1995.  https://doi.org/10.1104/pp.112.202887 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Muthukumar B, Joyce BL, Elless MP, Stewart CN (2013) Stable transformation of ferns using spores as targets: Pteris vittata and Ceratopteris thalictroides. Plant Physiol 163(2):648–658.  https://doi.org/10.1104/pp.113.224675 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Nakazato T, Jung M-K, Housworth EA, Rieseberg LH, Gastony GJ (2006) Genetic map-based analysis of genome structure in the homosporous fern Ceratopteris richardii. Genetics 173(3):1585–1597CrossRefPubMedPubMedCentralGoogle Scholar
  35. Norris SR, Meyer SE, Callis J (1993) The intron of Arabidopsis thaliana polyubiquitin genes is conserved in location and is a quantitative determinant of chimeric gene-expression. Plant Mol Biol 21:895–906CrossRefPubMedGoogle Scholar
  36. Odell JT, Nagy F, Chua NH (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313(6005):810–812CrossRefPubMedGoogle Scholar
  37. Park J, Salmi ML, Wan Salim WW, Rademacher A, Wickizer B, Schooley A, Benton J, Cantero A, Argote PF, Ren M, Zhang M, Porterfield DM, Ricco AJ, Roux SJ, Rickus JL (2017) An autonomous lab on a chip for space flight calibration of gravity-induced transcellular calcium polarization in single-cell fern spores. Lab Chip 17(6):1095–1103.  https://doi.org/10.1039/c6lc01370h CrossRefPubMedGoogle Scholar
  38. Plackett ARG, Huang LD, Sanders HL, Langdale JA (2014) High-efficiency stable transformation of the model Fern species Ceratopteris richardii via microparticle bombardment. Plant Physiol 165(1):3–14.  https://doi.org/10.1104/pp.113.231357 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Plackett ARG, Rabbinowitsch EH, Langdale JA (2015) Protocol: genetic transformation of the fern Ceratopteris richardii through microparticle bombardment. Plant Methods 11.  https://doi.org/10.1186/s13007-015-0080-8
  40. Roux SJ, Chatterjee A, Hillier S, Cannon T (2003) Early development of fern gametophytes in microgravity. Adv Space Res Off J Committee Space Res (COSPAR) 31(1):215–220CrossRefGoogle Scholar
  41. Roux SJ, Steinebrunner I (2007) Extracellular ATP: an unexpected role as a signaler in plants. Trends Plant Sci 12(11):522–527.  https://doi.org/10.1016/j.tplants.2007.09.003 CrossRefPubMedGoogle Scholar
  42. Salmi ML, Bushart TJ, Stout SC, Roux SJ (2005) Profile and analysis of gene expression changes during early development in germinating spores of Ceratopteris richardii. Plant Physiol 138(3):1734–1745.  https://doi.org/10.1104/pp.105.062851 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Salmi ML, ul Haque A, Bushart TJ, Stout SC, Roux SJ, Porterfield DM (2011) Changes in gravity rapidly alter the magnitude and direction of a cellular calcium current. Planta 233(5):911–920.  https://doi.org/10.1007/s00425-010-1343-2 CrossRefPubMedGoogle Scholar
  44. Stout SC, Clark GB, Archer-Evans S, Roux SJ (2003) Rapid and efficient suppression of gene expression in a single-cell model system, Ceratopteris richardii. Plant Physiol 131(3):1165–1168.  https://doi.org/10.1104/pp.016949 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sunilkumar G, Mohr L, Lopata-Finch E, Emani C, Rathore KS (2002) Developmental and tissue-specific expression of CaMV 35S promoter in cotton as revealed by GFP. Plant Mol Biol 50(3):463–474CrossRefPubMedGoogle Scholar
  46. Talamond P, Verdeil JL, Conejero G (2015) Secondary metabolite localization by autofluorescence in living plant cells. Molecules (Basel, Switzerland) 20(3):5024–5037.  https://doi.org/10.3390/molecules20035024 CrossRefGoogle Scholar
  47. Tang W, Brady SR, Sun Y, Muday GK, Roux SJ (2003) Extracellular ATP inhibits root gravitropism at concentrations that inhibit polar auxin transport. Plant Physiol 131(1):147CrossRefPubMedPubMedCentralGoogle Scholar
  48. Tang WX, He YH, Tu LL, Wang MJ, Li Y, Ruan YL, Zhang XL (2014) Down-regulating annexin gene GhAnn2 inhibits cotton fiber elongation and decreases Ca2+ influx at the cell apex. Plant Mol Biol 85(6):613–625.  https://doi.org/10.1007/s11103-014-0208-7 CrossRefPubMedGoogle Scholar
  49. Thomas C, Sun Y, Naus K, Lloyd A, Roux S (1999) Apyrase functions in plant phosphate nutrition and mobilizes phosphate from extracellular ATP. Plant Physiol 119(2):543–552CrossRefPubMedPubMedCentralGoogle Scholar
  50. ul Haque A, Rokkam M, De Carlo AR, Wereley ST, Roux SJ, Irazoqui PP, Porterfield DM (2007) A MEMS fabricated cell electrophysiology biochip for in silico calcium measurements. Sens Actuators B Chem 123(1):391–399.  https://doi.org/10.1016/j.snb.2006.08.043 CrossRefGoogle Scholar
  51. Wang LK, Niu XW, Lv YH, Zhang TZ, Guo WZ (2010) Molecular cloning and localization of a novel cotton annexin gene expressed preferentially during fiber development. Mol Biol Rep 37(7):3327–3334.  https://doi.org/10.1007/s11033-009-9919-2 CrossRefPubMedGoogle Scholar
  52. Watson JM, Fusaro AF, Wang MB, Waterhouse PM (2005) RNA silencing platforms in plants. FEBS Lett 579(26):5982–5987.  https://doi.org/10.1016/j.febslet.2005.08.014 CrossRefPubMedGoogle Scholar
  53. Wen CK, Smith R, Banks JA (1999) ANI1. A sex pheromone-induced gene in Ceratopteris gametophytes and its possible role in sex determination. Plant Cell 11(7):1307–1318PubMedPubMedCentralGoogle Scholar
  54. Wilkinson JE, Twell D, Lindsey K (1997) Activities of CaMV 35S and nos promoters in pollen: implications for field release of transgenic plants. J Exp Bot 48(2):265–275.  https://doi.org/10.1093/jxb/48.2.265 CrossRefGoogle Scholar
  55. Wu J, Steinebrunner I, Sun Y, Butterfield T, Torres J, Arnold D, Gonzalez A, Jacob F, Reichler S, Roux SJ (2007) Apyrases (nucleoside triphosphate-diphosphohydrolases) play a key role in growth control in Arabidopsis. Plant Physiol 144(2):961–975.  https://doi.org/10.1104/pp.107.097568 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Xiong TC, Ronzier E, Sanchez F, Corratge-Faillie C, Mazars C, Thibaud JB (2014) Imaging long distance propagating calcium signals in intact plant leaves with the BRET-based GFP-aequorin reporter. Front Plant Sci 5:43.  https://doi.org/10.3389/fpls.2014.00043 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Yang N-S, Christou P (1990) Cell type specific expression of a CaMV 35S-GUS gene in transgenic soybean plants. Dev Genet 11(4):289–293.  https://doi.org/10.1002/dvg.1020110407 CrossRefGoogle Scholar
  58. Yang XY, Wang BC, Farris B, Clark G, Roux SJ (2015) Modulation of root skewing in Arabidopsis by apyrases and extracellular ATP. Plant Cell Physiol 56(11):2197–2206.  https://doi.org/10.1093/pcp/pcv134 PubMedGoogle Scholar
  59. Zhu JE, Wu XR, Yuan SJ, Qian D, Nan Q, An LZ, Xiang Y (2014) Annexin5 plays a vital role in Arabidopsis pollen development via Ca2+-dependent membrane trafficking. PLoS One 9(7):15.  https://doi.org/10.1371/journal.pone.0102407 Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ashley E. Cannon
    • 1
  • Mari L. Salmi
    • 2
  • Araceli Cantero
    • 2
  • Stanley J. Roux
    • 2
  1. 1.BioDiscovery Institute, Department of BiologyThe University of North TexasDentonUSA
  2. 2.Department of Molecular BiosciencesThe University of TexasAustinUSA

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