Skip to main content

The Gametophyte of Fern: Born to Reproduce

  • Chapter
  • First Online:

Abstract

The gametophyte of ferns is a cellular monolayer structure, whose more important function is to form the gametes, responsible of sexual fusion that will lead to sporophyte generation. In most cases, as sporophyte develops, the gametophyte is about to disappear, reflecting to have a role purely involved on reproduction. Omics technologies based on comprehensive biochemical and molecular characterizations of an organism, tissue, or cell type and next-generation omics approaches facilitate the analyses of non-model organisms owing to the rapid generation of large amounts of de novo systems biology data, making them attractive options for studying plant development and evolution.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aya K, Kobayashi M, Tanaka J, Ohyanagi H, Suzuki T, Yano K, Takano T, Yano K, Matsuoka M (2015) De novo transcriptome assembly of a fern, Lygodium japonicum, and a web resource database, Ljtrans DB. Plant Cell Physiol 56:e5

    Article  PubMed  Google Scholar 

  • Barcaccia G, Albertini E (2013) Apomixis in plant reproduction: a novel perspective on an old dilemma. Plant Reprod 26:159–179

    Article  PubMed  PubMed Central  Google Scholar 

  • Barker MS, Wolf PG (2010) Unfurling fern biology in the genomics age. Bioscience 60:177–185

    Article  Google Scholar 

  • Bateman RM, Dimichele WA (1994) Heterospory: the most iterative key innovation in the evolutionary history of the plant kingdom. Biol Rev 69:345–417

    Article  Google Scholar 

  • Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103:999–1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16(Suppl):S228–S245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braithwaite AF (1964) A new type of apogamy in ferns. New Phytol 63:293–305

    Article  Google Scholar 

  • Bui LT, Pandzic D, Youngstrom CE, Wallace S, Irish EE, Szövényi P, Cheng C-L (2017) A fern AINTEGUMENTA gene mirrors BABY BOOM in promoting apogamy in Ceratopteris richardii. Plant J 90:122–132

    Article  CAS  PubMed  Google Scholar 

  • 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 100:161–174

    Article  CAS  PubMed  Google Scholar 

  • Chaturvedi P, Ghatak A, Weckwerth W (2016a) Pollen proteomics: from stress physiology to developmental priming. Plant Reprod 29:119–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaturvedi P, Selymesi M, Ghatak A, Mesihovic A, Scharf K-D, Weckwerth W, Simm S, Schleiff E (2016b) The membrane proteome of male gametophyte in Solanum lycopersicum. J Proteome 131:48–60

    Article  Google Scholar 

  • Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, Peacock WJ (1997) Fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 94(8):4223–4228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordle AR, Irish EE, Cheng CL (2007) Apogamy induction in Ceratopteris richardii. Int J Plant Sci 168:361–369

    Article  Google Scholar 

  • Cordle AR, Bui LT, Irish EE, Cheng CL (2010) Laboratory-induced apogamy and apospory in Ceratopteris richardii. In: Fernández H, Kumar A, Revilla MA (eds) Working with Ferns. Issues and applications, New York, Springer, pp 25–36

    Google Scholar 

  • Cordle AR, Irish EE, Cheng CL (2012) Gene expression associated with apogamy commitment in Ceratopteris richardii. Sex Plant Reprod 25:293–304

    Article  CAS  PubMed  Google Scholar 

  • Cousens MI (1979) Gametophytic ontogeny, sex expression, and genetic load as measures of population divergence in Blechnum spicant. Am J Bot 66:116–132

    Google Scholar 

  • d’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R (2009) Turning meiosis into mitosis (GP Copenhaver, Ed.) PLoS Biol 7:e1000124

    Article  PubMed  PubMed Central  Google Scholar 

  • Dai S, Wang T, Yan X, Chen S (2007) Proteomics of pollen development and germination. J Proteome Res 6:4556–4563

    Article  CAS  PubMed  Google Scholar 

  • De Vries J, Fischer AM, Roettger M, Rommel S, Schluepmann H (2016) Cytokinin-induced promotion of root meristem size in the fern Azolla supports a shoot-like origin of euphyllophyte roots. New Phytologist, 209:705–720

    Google Scholar 

  • Der JP, Barker MS, Wickett NJ, dePamphilis CW, Wolf PG (2011) De novo characterization of the gametophyte transcriptome in bracken fern, Pteridium aquilinum. BMC Genomics 12:99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeSmet I, Lau S, Mayer U, Jürgens G (2010) Embryogenesis – the humble beginnings of plant life. Plant J 61:959–970

    Article  CAS  Google Scholar 

  • Domżalska L, Kędracka-Krok S, Jankowska U, Grzyb M, Sobczak M, Rybczyński JJ, Mikuła A (2017) Proteomic analysis of stipe explants reveals differentially expressed proteins involved in early direct somatic embryogenesis of the tree fern Cyathea delgadii Sternb. Plant Sci 258:61–76

    Article  PubMed  Google Scholar 

  • Döpp W (1939) Cytologische und genetische Untersuchungen innerhalb der Gattung Dryopteris. Planta 29:481

    Google Scholar 

  • Eeckhout S, Leroux O, Willats WGT, Popper ZA, Viane RLL (2014) Comparative glycan profiling of Ceratopteris richardii C-Fern` gametophytes and sporophytes links cell-wall composition to functional specialization. Ann Bot 114:1295–1307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ehrhardt DW, Frommer WB (2012) New technologies for 21st century plant science. Plant Cell 24:374–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ekrt L, Koutecký P (2016) Between sexual and apomictic: unexpectedly variable sporogenesis and production of viable polyhaploids in the pentaploid fern of the Dryopteris affinis agg. (Dryopteridaceae). Ann Bot 117:97–106

    Article  PubMed  Google Scholar 

  • Fernández H, Revilla MA (2003) In vitro culture of ornamental ferns. Plant Cell Tissue Organ Cult 73:1–13

    Article  Google Scholar 

  • Fernández H, Bertrand AM, Sánchez-Tamés R (1996) Influence of tissue culture conditions on apogamy in Dryopteris affinis sp. affinis. Plant Cell Tissue Organ Cult 45:93–97

    Article  Google Scholar 

  • Fernández H, Bertrand AM, Feito I, Sánchez-Tamés R (1997) Gametophyte culture in vitro and antheridiogen activity in Blechnum spicant. Plant Cell Tissue Organ Cult 50:71–77

    Article  Google Scholar 

  • Fernández H, Bertrand AM, Sierra MI, Sánchez-Tamés R (1999) An apolar GA-like compound responsible for the antheridiogen activity in Blechnum spicant. Plant Growth Regul 28:143–144

    Article  Google Scholar 

  • Germanà MA (2011) Gametic embryogenesis and haploid technology as valuable support to plant breeding. Plant Cell Rep 30:839–857

    Article  PubMed  Google Scholar 

  • Grossmann J, Fernández H, Chaubey PM, Valdés AE, Gagliardini V, Cañal MJ, Russo G, Grossniklaus U (2017) Proteogenomic analysis greatly expands the identification of proteins related to reproduction in the apogamous fern Dryopteris affinis ssp. affinis. Front Plant Sci 8

    Google Scholar 

  • Grossniklaus U, Koltunow A, van Lookeren Campagne M (1998) A bright future for apomixis. Trends Plant Sci 3:415–416

    Article  Google Scholar 

  • Grossniklaus U, Nogler GA, van Dijk PJ (2001) How to avoid sex: the genetic control of developmental aspects. Plant Cell 13:1491–1497

    Google Scholar 

  • Haufler CH, Pryer KM, Schuettpelz E, Sessa EB, Farrar DR, Moran R, Schneller JJ, Watkins JE, Windham MD (2016) Sex and the single gametophyte: revising the homosporous vascular plant life cycle in light of contemporary research. Bioscience 66:928–937

    Article  Google Scholar 

  • Hendrix SD (1980) An evolutionary and ecological perspective of the insect fauna of ferns The American Society of Naturalists An Evolutionary and Ecological Perspective of the Insect Fauna of Ferns. Am Nat Source Am Nat 115:171–196

    Article  Google Scholar 

  • Ischebeck T, Valledor L, Lyon D, Gingl S, Nagler M, Meijón M, Egelhofer V, Weckwerth W (2014) Comprehensive cell-specific protein analysis in early and late pollen development from diploid microsporocytes to pollen tube growth. Mol Cell Proteomics 14(:295–310

    Article  Google Scholar 

  • Jorrín-Novo JV, Pascual J, Sánchez-Lucas R, Romero-Rodríguez MC, Rodríguez-Ortega MJ, Lenz C, Valledor L (2015) Fourteen years of plant proteomics reflected in Proteomics: moving from model species and 2DE-based approaches to orphan species and gel-free platforms. Proteomics 15:1089–1112

    Article  PubMed  Google Scholar 

  • Kandemi̇r N, Saygili İ (2015) Turkish Journal of Agriculture and Forestry Apomixis: new horizons in plant breeding

    Google Scholar 

  • Kazmierczak A (2010) Gibberellic acid and ethylene control male sex determination and development of Anemia phyllitidis gametophytes. In: Fernández H, Kumar A, Revilla MA (eds) Working with ferns. Issues and applications. Springer, New York, pp 49–65

    Google Scholar 

  • Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39

    Article  CAS  Google Scholar 

  • Kerim T, Imin N, Weinman JJ, Rolfe BG (2003) Proteome analysis of male gametophyte development in rice anthers. Proteomics 3:738–751

    Article  CAS  PubMed  Google Scholar 

  • Klekowski EJ (1969) Reproductive biology of the Pteridophyta. III. A study of the Blechnaceae. Bot J Linn Soc 62:361–377

    Article  Google Scholar 

  • Klekowski EJ, Baker HG (1966) Evolutionary significance of polyploidy in the pteridophyta. Science 153:305–307

    Article  PubMed  Google Scholar 

  • Koltunow AM, Grossniklaus U (2003) Apomixis: a developmental perspective. Annu Rev Plant Biol 54:547–574

    Article  CAS  PubMed  Google Scholar 

  • Koltunow AM, Bicknell RA, Chaudhury AM (1995) Apomixis: molecular strategies for the generation of genetically identical seeds without fertilization. Plant Physiol 108:1345–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotani Y, Henderson ST, Suzuki G, et al (2014) The LOSS OF APOMEIOSIS (LOA) locus in Hieracium praealtum can function independently of the associated large-scale repetitive chromosomal structure. New Phytologist 201:973–981

    Google Scholar 

  • Li JJ, Liu L, Ouyang YD, Yao JL (2011) Sexual reproduction development in apomictic Eulaliopsis binata (Poaceae). Genet Mol Res 10:2326–2339. https://doi.org/10.4238/2011.October.5.3

    Article  CAS  PubMed  Google Scholar 

  • Liu H-M, Dyer RJ, Guo Z-Y, Meng Z, Li J-H, Schneider H (2012) The evolutionary dynamics of apomixis in ferns: a case study from polystichoid ferns. J Bot 2012:1–11

    Article  Google Scholar 

  • Lopez RA, Renzaglia KS (2014) Multiflagellated sperm cells of Ceratopteris richardii are bathed in arabinogalactan proteins throughout development. Am J Bot 101:2052–2061

    Article  CAS  PubMed  Google Scholar 

  • Manton I (1950) Problems o cytology and evolution in the pteridophyta. Cambridge University Press

    Google Scholar 

  • Marimuthu MPA, Jolivet S, Ravi M et al (2011) Synthetic clonal reproduction through seeds. Science 331:876–876

    Article  CAS  PubMed  Google Scholar 

  • Markham K, Chalk T, Stewart CN Jr (2006) Evaluation of fern and moss protein-based defenses against phytophagous insects. Int J Plant Sci 167:111–117

    Article  CAS  Google Scholar 

  • Matasci N, Hung L-H, Yan Z et al (2014) Data access for the 1,000 Plants (1KP) project. 3:17

    Google Scholar 

  • Mayank P, Grossman J, Wuest S, Boisson-Dernier A, Roschitzki B, Nanni P, Nühse T, Grossniklaus U (2012) Characterization of the phosphoproteome of mature Arabidopsis pollen. Plant J 72:89–101

    Article  CAS  PubMed  Google Scholar 

  • Menéndez V, Revilla MA, Bernard P, Gotor V, Fernández H (2006a) Gibberellins and antheridiogen on sex in Blechnum spicant L. Plant Cell Rep 25:1104–1110

    Article  PubMed  Google Scholar 

  • Menéndez V, Villacorta NF, Revilla MA, Gotor V, Bernard P, Fernández H (2006b) Exogenous and endogenous growth regulators on apogamy in Dryopteris affinis (Lowe) Fraser-Jenkins sp. affinis. Plant Cell Rep 25:85–91

    Article  PubMed  Google Scholar 

  • Mikuła A, Pożoga M, Tomiczak K, Rybczyński JJ (2015) Somatic embryogenesis in ferns: a new experimental system. Plant Cell Rep 34:783–794

    Article  PubMed  PubMed Central  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:73–497

    Google Scholar 

  • Neiman M, Sharbel TF, Schwander T (2014) Genetic causes of transitions from sexual reproduction to asexuality in plants and animals. J Evol Biol 27:1346–1359

    Article  CAS  PubMed  Google Scholar 

  • Nogler GA (1984) Embryology of angioesperms. In: Johri B (ed) Embryology of angiosperms. Springer, Berlín, pp 475–518

    Chapter  Google Scholar 

  • Okada S, Sone T, Fujisawa M et al (2001) The Y chromosome in the liverwort Marchantia polymorpha has accumulated unique repeat sequences harboring a male-specific gene. Proc Natl Acad Sci U S A 98:9454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okano Y, Aono N, Hiwatashi Y, Murata T, Nishiyama T, Ishikawa T (2009) A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proc Natl Acad Sci U S A 106:16321–16326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozias-Akins P (2006) Apomixis: Developmental characteristics and genetics. Crit Rev Plant Sci 25:199–214

    Article  Google Scholar 

  • Pannell JR (2017) Plant sex determination. Curr Biol 27:R191–R197

    Article  CAS  PubMed  Google Scholar 

  • Peredo EL, Méndez-Couz M, Revilla MA, Fernández H (2013) Mating system in Blechnum spicant and Dryopteris affinis ssp. affinis correlates with genetic variability. Am Fern J 103:27

    Article  Google Scholar 

  • Pires ND, Dolan L (2012) Morphological evolution in land plants: new designs with old genes. Philos Trans R Soc Biol Sci 367:508

    Article  CAS  Google Scholar 

  • Radoeva T, Weijers D (2014) A roadmap to embryo identity in plants. Trends Plant Sci 19:709–716

    Article  CAS  PubMed  Google Scholar 

  • Rathinasabapathi B (2006) Ferns represent an untapped biodiversity for improving crops for environmental stress tolerance. New Phytol 172:385–390

    Article  PubMed  Google Scholar 

  • Ravi M, Marimuthu MPA, Siddiqi I (2008) Gamete formation without meiosis in Arabidopsis. Nature 451:1121–1124

    Article  CAS  PubMed  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science (New York, NY) 319:64–69

    Article  CAS  Google Scholar 

  • Rodriguez-Leal D, Vielle-Calzada J-P (2012) Regulation of apomixis: learning from sexual experience. Curr Opin Plant Biol 15:549–555

    Article  PubMed  Google Scholar 

  • Romero-Rodríguez MC, Pascual J, Valledor L, Jorrín-Novo J (2014) Improving the quality of protein identification in non-model species. Characterization of Quercus ilex seed and Pinus radiata needle proteomes by using SEQUEST and custom databases. J Proteome 105:85–91

    Article  Google Scholar 

  • Sakamaki Y, Ino Y (2007) Gametophyte contribution to sporophyte growth on the basis of carbon gain in the fern Thelypteris palustris: effect of gametophyte organic-matter production on sporophytes. J Plant Res 120:301–308

    Article  PubMed  Google Scholar 

  • Salmi ML, Bushart TJRS (2010) Cellular, molecular, and genetic changes during the development of Ceratopteris richardii gametophytes. In: Fernández AK H, Revilla MA (eds) Working with ferns. Issues and applications. Springer, New York, pp 11–24

    Google Scholar 

  • 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 138:1734–1745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salmi ML, Morris KE, Roux SJ, Porterfield DM (2007) Nitric oxide and cGMP signaling in calcium-dependent development of cell polarity in Ceratopteris richardii. Plant Physiol 144:94–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salvo E (1990) Guía de helechos de la Península Ibérica y Baleares. Ediciones Pirámide S.A.

    Google Scholar 

  • Sanchez-Lucas R, Mehta A, Valledor L et al (2016) A year (2014-2015) of plants in Proteomics journal. Progress in wet and dry methodologies, moving from protein catalogs, and the view of classic plant biochemists. Proteomics 16:866–876

    Article  CAS  PubMed  Google Scholar 

  • Schwartz W (2007) Lynn Margulis, Origin of eukaryotic cells. Evidence and research implications for a theory of the origin and evolution of microbial, plant, and animal cells on the precambrian earth. XXII u. 349 S., 89 Abb., 49 Tab. New Haven-London 1970: Yale University. Z Allg Mikrobiol 13:186–186

    Article  Google Scholar 

  • Seguí-Simarro JM (2010) Androgenesis revisited. Bot Rev 76:377–404

    Article  Google Scholar 

  • Sheoran IS, Ross ARS, Olson DJH, Sawhney VK (2007) Proteomic analysis of tomato (Lycopersicon esculentum) pollen. J Exp Bot 58:3525–3535

    Article  CAS  PubMed  Google Scholar 

  • Shukla AK, Upadhyay SK, Mishra M et al (2016) Expression of an insecticidal fern protein in cotton protects against whitefly. Nat Biotechnol 34:1046–1051

    Article  CAS  PubMed  Google Scholar 

  • Spillane C, Curtis MD, Grossniklaus U (2004) Apomixis technology development—virgin births in farmers’ fields? Nat Biotechnol 22:687–691

    Article  CAS  PubMed  Google Scholar 

  • Suo J, Zhao Q, Zhang Z, Chen S, Cao J, Liu G, Wei X, Wang T, Yang C, Dai S (2015) Cytological and proteomic analyses of Osmunda cinnamomea germinating spores reveal characteristics of fern spore germination and rhizoid tip growth. Mol Cell Proteomics 14:2510–2534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taiz L, Zeiger E (2015) Plant physiology and development. Sinauers Associates, Inc., Sunderland

    Google Scholar 

  • Tucker MR, Araujo A-CG, Paech NA, Hecht V, Schmidt EDL, Rossell J-B, De Vries SC, Koltunow AMG (2003) Sexual and apomictic reproduction in Hieracium subgenus pilosella are closely interrelated developmental pathways. Plant Cell 15:1524–1537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valledor L, Jorrín JV, Rodríguez JL, Lenz C, Meijón M, Rodríguez R, Cañal MJ (2010) Combined proteomic and transcriptomic analysis identifies differentially expressed pathways associated to Pinus radiata needle maturation. J Proteome Res 9:3954–3979

    Article  CAS  PubMed  Google Scholar 

  • Valledor L, Menéndez V, Canal MJ, Revilla A, Fernández H (2014) Proteomic approaches to sexual development mediated by antheridiogen in the fern Blechnum spicant L. Proteomics 14:1–11

    Google Scholar 

  • von Aderkas P (1984) Promotion of apogamy in Matteuccia struthiopteris, the Ostrich Fern. Am Fern J 74(1):1–6

    Google Scholar 

  • Wada M (2007) The fern as a model system to study photomorphogenesis. J Plant Res 120:3–16

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S (2010) Desiccation tolerance mechanism in resurrection Fern-Ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res. 9:6561–6577

    Google Scholar 

  • Ward JA, Ponnala L, Weber CA (2012) Strategies for transcriptome analysis in nonmodel plants. Am J Bot 99:267–276

    Article  CAS  PubMed  Google Scholar 

  • 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 11:1307–1318

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whittier DP, Steeves T (1960) The induction of apogamy in the bracken fern. Can J Bot 38:925–930

    Article  CAS  Google Scholar 

  • Whittier D, Steeves T (1962) Further studies on induced apogamy in ferns. Can J Bot 40:1525–1531

    Article  CAS  Google Scholar 

  • Yang HY, Zhou C (1992) Experimental plant reproductive biology and reproductive cell manipulation in higher plants: now and the future. Am J Bot 79:354–363

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Helena Fernández .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Rivera, A., Cañal, M.J., Grossniklaus, U., Fernández, H. (2018). The Gametophyte of Fern: Born to Reproduce. In: Fernández, H. (eds) Current Advances in Fern Research. Springer, Cham. https://doi.org/10.1007/978-3-319-75103-0_1

Download citation

Publish with us

Policies and ethics