The Power of Gametophyte Transformation

  • Linh Thuy Bui
  • Holly Long
  • Erin E. Irish
  • Angela R. Cordle
  • Chi-Lien Cheng
Chapter

Abstract

A simple, reliable, and efficient transgenesis method is essential for the establishment of any model organism. Mosses and liverworts, non-seed plants, have a dominant gametophyte generation. As the haploid generation is preferred for transgenesis, multiple methods have been developed to transform gametophytes of the model species Physcomitrella patens and Marchantia polymorpha, firmly establishing them as models of nonvascular, non-seed plants. Only recently, transgenesis has been made possible in vascular non-seed plants, the ferns. Reliable methods of transforming both the sporophyte and the gametophyte generations have been developed. Although the fern sporophyte generation, as in seed plants, is the dominant generation, the gametophytes are free-living, independent entities. This life cycle offers an opportunity for developing gametophyte transgenesis methods. Simple, reliable, and efficient methods for transient and stable Agrobacterium-mediated transformation of gametophytes have been developed for the diploid fern Ceratopteris richardii, long-promoted as a model fern. The ability to transform the gametophyte has greatly facilitated the study of candidate genes functioning in promoting apogamy—a form of asexual alternation of generations. It is our great hope that this method will stimulate further development of C. richardii into a model organism. It is also our hope that this method be adapted for transforming other fern species.

Keywords

Agrobacterium AIL5 Apogamy BBM Ceratopteris CrANT gametophyte transformation 

Abbreviations

dsRNA

Double-stranded RNA

gRNA

Guide RNA

GUS

β-Glucuronidase

HR

Homologous recombination

RNAi

RNA interference

siRNA

Small interfering RNA

T0

Primary transformant of gametophyte or sporophyte

T1

Generation produced by selfing T0

TALEN-mediated genome editing

Transcription activator-like effector nuclease-mediated genome editing

References

  1. Aoyama T, Hiwatashi Y, Shigyo M, Kofuji R, Kubo M, Ito M, Hasebe M (2012) AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development 139:3120–3129CrossRefPubMedGoogle Scholar
  2. Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C.R. Acad Sci Sér 3 Sci Vie 316:1194–1199Google Scholar
  3. Bechtold N, Jaudeau B, Jolivet S, Maba B, Vezon D, Voisin R, Pelletier G (2000) The maternal chromosome set is the target of the T-DNA in the in-planta transformation of Arabidopsis thaliana. Genetics 155:1875–1887PubMedPubMedCentralGoogle Scholar
  4. Bezanilla M, Pan A, Quatrano RS (2003) RNA interference in the moss Physcomitrella patens. Plant Physiol 133:470–474CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bezanilla M, Perroud PF, Pan A, Klueh P, Quatrano RS (2005) An RNAi system in Physcomitrella patens with an internal marker for silencing allows for rapid identification of loss of function phenotypes. Plant Biol 7:251–257CrossRefPubMedGoogle Scholar
  6. Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bui LT, Hurst A, Irish EE, Cheng CL (2012) The effects of sugars and ethylene on apospory and regeneration in Ceratopteris richardii. AJPS 3:953–961CrossRefGoogle Scholar
  8. Bui LT, Cordle AR, Irish EE, Cheng CL (2015) Transient and stable tranformation of Ceratopteris richardii gametophytes. BMC Res Notes 8:214–223CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bui LT, Pandzic D, Youngstrom CE, Wallace S, Irish EE, Szövényi P, Cheng CL (2017) A fern AINTEGUMENTA gene mirrors BABY BOOM in promoting apogamy in Ceratopteris richardii. Plant J 90:122–132CrossRefPubMedGoogle Scholar
  10. Burkart GM, Baskin TI, Bezanilla M (2015) A family of ROP proteins that suppresses actin dynamics, and is essential for polarized growth and cell adhesion. J Cell Sci 128:2553–2564CrossRefPubMedGoogle Scholar
  11. Chatterjee A, Roux SJ (2000) Ceratopteris richardii: a productive model for revealing secrets of signaling and development. J Plant Growth Regul 19:284–289CrossRefPubMedGoogle Scholar
  12. Chiyoda S, Ishizaki K, Kataoka H, Yamato KT, Kohchi T (2008) Direct transformation of the liverwort Marchantia polymorpha L. by particle bombardment using immature thalli developing from spores. Plant Cell Rep 27:1467–1473CrossRefPubMedGoogle Scholar
  13. Cho SH, Chung YS, Cho SK, Rim YW, Shin JS (1999) Particle bombardment mediated transformation and GFP expression in the moss Physcomitrella patens. Mol Cells 9:14–19PubMedGoogle Scholar
  14. Collonnier C, Epert A, Mara K, Maclot F, Guyon-Debast A, Charlot F, White C, Schaefer DG, Nogué F (2017) CRISPR-Cas9-mediated efficient directed mutagenesis and RAD51-dependent and RAD51-independent gene targeting in the moss Physcomitrella patens. Plant Biotechnol J 15:122–131CrossRefPubMedGoogle Scholar
  15. Conner JA, Mookkan M, Huo H, Chae K, Ozias-Akins P (2015) A parthenogenesis gene of apomictic origin elicits embryo formation from unfertilized eggs in a sexual plant. Proc Natl Acad Sci U S A 112:11205–11210CrossRefPubMedPubMedCentralGoogle Scholar
  16. Cordle AR, Irish EE, Cheng CL (2007) Apogamy induction in Ceratopteris richardii. Int J Plant Sci 168:361–369CrossRefGoogle Scholar
  17. Cordle AR, Bui LT, Irish EE, Cheng CL (2011) Laboratory-induced apogamy and apospory in Ceratopteris richardii. In: Kumar A, Fernández H, Revilla MA (eds) Working with ferns. Springer, New York, pp 25–36CrossRefGoogle Scholar
  18. Desfeux C, Clough SJ, Bent AF (2000) Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol 123:895–904CrossRefPubMedPubMedCentralGoogle Scholar
  19. El Ouakfaoui S, Schnell J, Abdeen A, Colville A, Labbé H, Han S, Baum B, Laberge S, Miki B (2010) Control of somatic embryogenesis and embryo development by AP2 transcription factors. Plant Mol Biol 74:313–326CrossRefPubMedPubMedCentralGoogle Scholar
  20. Floyd SK, Bowman JL (2007) The ancestral developmental tool kit of land plants. Int J Plant Sci 168:1–35CrossRefGoogle Scholar
  21. Heidmann I, de Lange B, Lambalk J, Angenent GC, Boutilier K (2011) Efficient sweet pepper transformation mediated by the BABY BOOM transcription factor. Plant Cell Rep 30:1107–1115CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hickok LG, Warne TR, Fribourg RS (1995) The biology of the fern Ceratopteris and its use as a model system. Int J Plant Sci 156:332–345CrossRefGoogle Scholar
  23. Hohe A, Egener T, Lucht JM, Holtorf H, Reinhard C, Schween G, Reski R (2004) An improved and highly standardised transformation procedure allows efficient production of single and multiple targeted gene-knockouts in a moss, Physcomitrella patens. Curr Genet 44:339–347CrossRefPubMedGoogle Scholar
  24. Honkanen S, Jones VA, Morieri G, Champion C, Hetherington AJ, Kelly S, Proust H, Saint-Marcoux D, Prescott H, Dolan L (2016) The mechanism forming the cell surface of tip-growing rooting cells is conserved among land plants. Curr Biol 26:3238–3244CrossRefPubMedPubMedCentralGoogle Scholar
  25. Horst NA, Katz A, Pereman I, Decker EL, Ohad N, Reski R (2016) A single homeobox gene triggers phase transition, embryogenesis and asexual reproduction. Nat Plants 2:15209.  https://doi.org/10.1038/nplants.2015.209 CrossRefPubMedGoogle Scholar
  26. Indriolo E, Na G, Ellis D, Salt DE, Banks JA (2010) A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 22:2045–2057CrossRefPubMedPubMedCentralGoogle Scholar
  27. Ishizaki K, Chiyoda S, Yamato KT, Kohchi T (2008) Agrobacterium-mediated transformation of the haploid liverwort Marchantia polymorpha L., an emerging model for plant biology. Plant Cell Physiol 49:1084–1091CrossRefPubMedGoogle Scholar
  28. Ishizaki K, Johzuka-Hisatomi Y, Ishida S, Iida S, Kohchi T (2013) Homologous recombination-mediated gene targeting in the liverwort Marchantia polymorpha L. Sci Rep 3:1532.  https://doi.org/10.1038/srep01532 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ishizaki K, Nishihama R, Yamato KT, Kohchi T (2016) Molecular genetic tools and techniques for Marchantia polymorpha research. Plant Cell Physiol 57:262–270CrossRefPubMedGoogle Scholar
  30. Kajikawa M, Matsui K, Ochiai M, Tanaka Y, Kita Y, Ishimoto M, Kohzu Y, Shoji S, Yamato KT, Ohyama K, Fukuzawa H, Kohchi T (2008) Production of arachidonic and eicosapentaenoic acids in plants using bryophyte fatty acid Δ6-desaturase, Δ6-elongase, and Δ5-desaturase genes. Biosci Biotechnol Biochem 72:435–444CrossRefPubMedGoogle Scholar
  31. Kamisugi Y, Schlink K, Rensing SA, Schween G, von Stackelberg M, Cuming AC, Reski R, Cove DJ (2006) The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration. Nucleic Acids Res 34:6205–6214CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kawai-Toyooka H, Kuramoto C, Orui K, Motoyama K, Kikuchi K, Kanegae T, Wada M (2004) DNA interference: a simple and efficient gene-silencing system for high-throughput functional analysis in the fern Adiantum. Plant Cell Physiol 45:1648–1657CrossRefPubMedGoogle Scholar
  33. Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39CrossRefGoogle Scholar
  34. Kim S, Soltis PS, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23:107–120CrossRefPubMedGoogle Scholar
  35. Klink VP, Wolniak SM (2001) Centrin is necessary for the formation of the motile apparatus in spermatids of Marsilea. Mol Biol Cell 12:761–776CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kopischke S, Schüßler E, Althoff F, Zachgo S (2017) TALEN-mediated genome-editing approaches in the liverwort Marchantia polymorpha yield high efficiencies for targeted mutagenesis. Plant Methods 13:20.  https://doi.org/10.1186/s13007-017-0167-5 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Leroux O, Eeckhout S, Viane RL, Popper ZA (2013) Ceratopteris richardii (C-Fern): a model for investigating adaptive modification of vascular plant cell walls. Front Plant Sci 4:367.  https://doi.org/10.3389/fpls.2013.00367 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Li C, Sako Y, Imai A, Nishiyama T, Thompson K, Kubo M, Hiwatashi Y, Kabeya Y, Karlson D, Wu SH, Ishikawa M, Murata T, Benfrey PN, Sato Y, Tamada Y, Hasebe M (2017) A Lin28 homologue reprograms differentiated cells to stem cells in the moss Physcomitrella patens. Nat Commun 8:14242.  https://doi.org/10.1038/ncomms14242 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lopez-Obando M, Conn CE, Hoffmann B, Bythell-Douglas R, Nelson DC, Rameau C, Bonhomme S (2016) Structural modelling and transcriptional responses highlight a clade of PpKAI2-LIKE genes as candidate receptors for strigolactones in Physcomitrella patens. Planta 243:1441–1453CrossRefPubMedGoogle Scholar
  40. Lowe K et al (2016) Morphogenic regulators baby boom and wuschel improve monocot transformation. Plant Cell 28:1998–2015CrossRefPubMedCentralGoogle Scholar
  41. Muthukumar B, Joyce BL, Elless MP, Stewart CN (2013) Stable transformation of ferns using spores as targets: Pteris vittata and Ceratopteris thalictroides. Plant Physiol 163:648–658CrossRefPubMedPubMedCentralGoogle Scholar
  42. Nakaoka Y, Miki T, Fujioka R, Uehara R, Tomioka A, Obuse C, Kubo M, Hiwatashi Y, Goshima G (2012) An inducible RNA interference system in Physcomitrella patens reveals a dominant role of augmin in phragmoplast microtubule generation. Plant Cell 24:1478–1493CrossRefPubMedPubMedCentralGoogle Scholar
  43. Nogler GA (1984) Gametophytic apomixis. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin/Heidelberg, pp 475–518CrossRefGoogle Scholar
  44. Osakabe Y, Watanabe T, Sugano SS, Ueta R, Ishihara R, Shinozaki K, Osakabe K (2016) Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci Rep 6:26685.  https://doi.org/10.1038/srep26685 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Ozias-Akins P (2006) Apomixis: developmental characteristics and genetics. CRC Crit Rev Plant Sci 25:199–214CrossRefGoogle Scholar
  46. Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, den Boer B, van der Geest L, Boutilier K (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol Biol 68:225–237CrossRefPubMedGoogle Scholar
  47. Plackett A, Huang L, Sanders HL, Langdale JA (2014) High-efficiency stable transformation of the model fern species Ceratopteris richardii via microparticle bombardment. Plant Physiol 165:3–14CrossRefPubMedPubMedCentralGoogle Scholar
  48. Plackett AR, Rabbinowitsch EH, Langdale JA (2015) Protocol: genetic transformation of the fern Ceratopteris richardii through microparticle bombardment. Plant Methods 11:37.  https://doi.org/10.1186/s13007-015-0080-8 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618–622CrossRefPubMedGoogle Scholar
  50. Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:1697–1699CrossRefPubMedGoogle Scholar
  51. Rutherford G, Tanurdzic M, Hasebe M, Banks JA (2004) A systemic gene silencing method suitable for high throughput, reverse genetic analyses of gene function in fern gametophytes. BMC Plant Biol 4:6.  https://doi.org/10.1186/1471-2229-4-6 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Schaefer D, Zryd JP, Knight CD, Cove DJ (1991) Stable transformation of the moss Physcomitrella patens. Mol Gen Genet 226:418–424CrossRefPubMedGoogle Scholar
  53. Schaefer DG, Zrÿd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206CrossRefPubMedGoogle Scholar
  54. Schmidt A, Schmid MW, Grossniklaus U (2015) Plant germline formation: common concepts and developmental flexibility in sexual and asexual reproduction. Development 142:229–241CrossRefPubMedGoogle Scholar
  55. Shimakawa G, Ishizaki K, Tsukamoto S, Tanaka M, Sejima T, Miyake C (2017) The liverwort, Marchantia, drives alternative electron flow using a flavodiiron protein to protect PSI. Plant Physiol 173:1636–1647CrossRefPubMedPubMedCentralGoogle Scholar
  56. Šmídková M, Hola M, Angelis KJ (2010) Efficient biolistic transformation of the moss Physcomitrella patens. Biol Plant 54:777–780CrossRefGoogle Scholar
  57. Srinivasan C, Liu Z, Heidmann I, Supena ED, Fukuoka H, Joosen R, Lambalk J, Angenent G, Scorza R, Custers JB, Boutilier K (2007) Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.) Planta 225:341–351CrossRefPubMedGoogle Scholar
  58. Stevenson DW, Loconte H (1996) Ordinal and familial relationships of pteridophyte genera. In: Camus JM, Gibby M, Johns RJ (eds) Pteridology in perspective. Royal Botanic Gardens, Kew, pp 435–467Google Scholar
  59. 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 131:1165–1168CrossRefPubMedPubMedCentralGoogle Scholar
  60. Strepp R, Scholz S, Kruse S, Speth V, Reski R (1998) Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc Natl Acad Sci U S A 95:4368–4373CrossRefPubMedPubMedCentralGoogle Scholar
  61. Sugano SS, Shirakawa M, Takagi J, Matsuda Y, Shimada T, Hara-Nishimura I, Kohchi T (2014) CRISPR/Cas9 mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant Cell Physiol 55:475–481CrossRefPubMedGoogle Scholar
  62. Takenaka M, Yamaoka S, Hanajiri T, Shimizu-Ueda Y, Yamato KT, Fukuzawa H, Ohyama K (2000) Direct transformation and plant regeneration of the haploid liverwort Marchantia polymorpha L. Transgenic Res 9:179–185CrossRefPubMedGoogle Scholar
  63. Trouiller B, Charlot F, Choinard S, Schaefer DG, Nogué F (2007) Comparison of gene targeting efficiencies in two mosses suggests that it is a conserved feature of Bryophyte transformation. Biotechnol Lett 29:1591–1598CrossRefPubMedGoogle Scholar
  64. Tsuwamoto R, Yokoi S, Takahata Y (2010) Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol Biol 73:481–492CrossRefPubMedGoogle Scholar
  65. Tucker MR, Koltunow AM (2009) Sexual and asexual (apomictic) seed development in flowering plants: molecular, morphological and evolutionary relationships. Funct Plant Biol 36:490–504CrossRefGoogle Scholar
  66. Vidali L, van Gisbergen PA, Guérin C, Franco P, Li M, Burkart GM, Augustine RC, Blanchoin L, Bezanilla M (2009) Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proc Natl Acad Sci 106:13341–13346CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wendeler E, Zobell O, Chrost B, Reiss B (2015) Recombination products suggest the frequent occurrence of aberrant gene replacement in the moss Physcomitrella patens. Plant J 81:548–558CrossRefPubMedGoogle Scholar
  68. Willmann MR, Endres MW, Cook RT, Gregory BD (2011) The functions of RNA-dependent RNA polymerases in Arabidopsis. Arabidopsis Book 9:e0146.  https://doi.org/10.1199/tab.0146 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Ye GN, Stone D, Pang SZ, Creely W, Gonzalez K, Hinchee M (1999) Arabidopsis ovule is the target for Agrobacterium in planta vacuum infiltration transformation. Plant J 19:249–257CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Linh Thuy Bui
    • 1
    • 2
  • Holly Long
    • 1
  • Erin E. Irish
    • 1
  • Angela R. Cordle
    • 1
  • Chi-Lien Cheng
    • 1
  1. 1.Department of BiologyThe University of IowaIowa CityUSA
  2. 2.Department of BiologyIndiana UniversityBloomingtonUSA

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