Skip to main content

The Ceratopteris (fern) developing motile gamete walls contain diverse polysaccharides, but not pectin

Abstract

Main conclusion

Unlike most plant cell walls, the five consecutive walls laid down during spermatogenesis in the model fern Ceratopteris contain sparse cellulose, lack pectin and are enriched with callose and hemicelluloses.

Seed-free plants like bryophytes and pteridophytes produce swimming male gametes for sexual reproduction. During spermatogenesis, unique walls are formed that are essential to the appropriate development and maturation of the motile gametes. Other than the detection of callose and general wall polysaccharides in scattered groups, little is known about the sequence of wall formation and the composition of these walls during sperm cell differentiation in plants that produce swimming sperm. Using histochemistry and immunogold localizations, we examined the distribution of callose, cellulose, mannan and xylan-containing hemicelluloses, and homogalacturonan (HG) pectins in the special walls deposited during spermatogenesis in Ceratopteris. Five walls are produced in sequence and each has a unique fate. The first wall (W1) contains callose and sparse xylan-containing hemicelluloses. Wall two (W2) is thin and composed of cellulose crosslinked by xylan-containing hemicelluloses. The third wall (W3) is thick and composed entirely of callose, and the fourth wall (W4) is built of cellulose heavily crosslinked by galactoxyloglucan hemicelluloses. Wall five (W5) is an arabinogalactan protein (AGP)-rich matrix in which the gamete changes shape and multiple flagella elongate. We detected no esterified or unesterified HG pectins in any of the walls laid down during spermatogenesis. To consider evolutionary modifications in cell walls associated with motile gametes, comparisons are presented with male gametophyte and spermatogenous cell walls across plant groups.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

AGP:

Arabinogalactan proteins

ßGlucY:

ß-d-glucosyl Yariv

HG:

Homogalacturonan

MAb:

Monoclonal antibodies

References

  • Bhalla PL, Slattery HD (1984) Callose deposits make clover seeds impermeable to water. Ann Bot-Lond 53:125–128

    CAS  Article  Google Scholar 

  • Blake AW, McCartney L, Flint JE, Bolam DN, Boraston AB, Gilbert HJ, Knox JP (2006) Understanding the biological rational for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. J Biol Chem 281:29321–29329

    CAS  Article  PubMed  Google Scholar 

  • Buchanan BB, Gruissem W, Jones RL (eds) (2000) Biochemistry and molecular biology of plants. Wiley, London

    Google Scholar 

  • Burgert I, Fratzl P (2009) Plants control the properties and actuation of their organs through the orientation of cellulose fibrils in their cell walls. Integr Comp Biol 49:69–79

    Article  PubMed  Google Scholar 

  • Cave CF, Bell PR (1973) The cytochemistry of the walls of the spermatocytes of Ceratopteris thalictroides. Planta 109:99–104

    CAS  Article  PubMed  Google Scholar 

  • Cornuault V, Buffetto F, Rydahl MG, Marcus SE, Torode TA, Xue J, Crépeau MJ, Faria-Blanc N, Willats WG, Dupree P, et al. (2015) Monoclonal antibodies indicate low-abundance links between heteroxylan and other glycans of plant cell walls. Planta 242:1321–1334

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Eggert D, Naumann M, Reimer R, Voigt CA (2014) Nanoscale glucan polymer network causes pathogen resistance. Sci Rep-UK 4:4159

    Article  Google Scholar 

  • El Hadrami A, Adam LR, El Hadrami I, Daayf F (2010) Chitosan in plant protection. Mar Drugs 8:968–987

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T, Manisseri C, Somerville SC, Voigt CA (2013) Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol 161:1433–1444

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Evert R (2006) Esau’s plant anatomy: meristems, cells and tissues—their structure, function, and development, 3rd edn. Wiley, New Jersey

    Book  Google Scholar 

  • Flors V, Ton J, Jakab G, Mauch-Mani B (2005) Abscisic acid and callose: team players in defence against pathogens? J Phytopathol 153:377–383

    CAS  Article  Google Scholar 

  • Gomez LD, Steele-King CG, Jones L, Foster JM, Vuttipongchaikij S, McQueen-Mason SJ (2009) Arabinan metabolism during seed development and germination in Arabidopsis. Mol Plant 2:966–976

    CAS  Article  PubMed  Google Scholar 

  • Gori P, Muccifora S, Woo SL, Bellani LM (1997) An ultrastructural study of the mature spermatozoid of the fern Asplenium trichomanes L. subsp. trichomanes. Sex Plant Reprod 10:142–148

    Article  Google Scholar 

  • Gorska-Brylass A (1968) Callose in the cell walls of the developing male gametophyte in Gymnospermae. Acta Soc Bot Pol 37:119–124

    CAS  Article  Google Scholar 

  • Gorska-Brylass A (1969) Callose in gametogenesis in liverworts. Bull Pol Acad Sci Biol Sci 17:549–554

    Google Scholar 

  • Górska-Brylass A (1970) The “callose stage” of the generative cells in pollen grains. Grana 10:21–30

    Article  Google Scholar 

  • Herburger K, Lewis LA, Holzinger A (2015) Photosynthetic efficiency, desiccation tolerance and ultrastructure in two phylogenetically distinct strains of alpine Zygnema sp. (Zygnematophyceae, Streptophyta): role of pre-akinete formation. Protoplasma 252:571–589

    CAS  Article  PubMed  Google Scholar 

  • Heslop-Harrison J (1968) Synchronous pollen mitosis and the formation of the generative cell in massulate orchids. J Cell Sci 3:457–466

    Google Scholar 

  • Huang L, Chen XY, Rim Y, Han X, Cho WK, Kim SW, Kim JY (2009) Arabidopsis glucan synthase-like 10 functions in male gametogenesis. J Plant Physiol 166:344–352

    CAS  Article  PubMed  Google Scholar 

  • Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15:250–313

    Article  Google Scholar 

  • Jones L, Milne JL, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci 100:11783–11788

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kartusch R (2003) On the mechanism of callose synthesis induction by metal ions in onion epidermal cells. Protoplasma 220:219–225

    CAS  Article  PubMed  Google Scholar 

  • Kaźmierczak A (2008) Cell number, cell growth, antheridiogenesis, and callose amount is reduced and atrophy induced by deoxyglucose in Anemia phyllitidis gametophytes. Plant Cell Rep 27:813–821

    Article  PubMed  Google Scholar 

  • Kim JY, Rim Y, Wang J, Jackson D (2005) A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Gene Dev 19:788–793

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Knox JP (2008) Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol 11:308–313

    CAS  Article  PubMed  Google Scholar 

  • Koh EJ, Zhou L, Williams DS, Park J, Ding N, Duan YP, Kang BH (2012) Callose deposition in the phloem plasmodesmata and inhibition of phloem transport in citrus leaves infected with Candidatus Liberibacter asiaticus. Protoplasma 249:687–697

    Article  PubMed  Google Scholar 

  • Kotenko JL (1990) Spermatogenesis in a homosporous fern, Onoclea sensibilis. Am J Bot 77:809–825

    Article  Google Scholar 

  • Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51

    Article  Google Scholar 

  • Kuhn SA, de Araujo-Mariath JE (2014) Reproductive biology of the “Brazilian pine” (Araucaria angustifolia–Araucariaceae): development of microspores and microgametophytes. Flora 209:290–298

    Article  Google Scholar 

  • Lamport DT, Várnai P (2013) Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol 197:58–64

    CAS  Article  PubMed  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

    CAS  Article  PubMed  Google Scholar 

  • Lopez RA, Renzaglia KS (2016) Arabinogalactan proteins and arabinan pectins abound in the specialized matrices surrounding female gametes of the fern Ceratopteris richardii. Planta 243:947–957

    CAS  Article  PubMed  Google Scholar 

  • Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant-Microbe In 24:183–193

    CAS  Article  Google Scholar 

  • Marcus SE, Blake AW, Benians TA, Lee KJ, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert HJ (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64:191–203

    CAS  Article  PubMed  Google Scholar 

  • Marcus SE, Verhertbruggen Y, Hervé C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WG, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60

    Article  PubMed  PubMed Central  Google Scholar 

  • McCabe PF, Levine A, Meijer PJ, Tapon NA, Pennell RI (1997) A programmed cell death pathway activated in carrot cells cultured at low cell density. Plant J 12:267–280

    CAS  Article  Google Scholar 

  • Meikle PJ, Bonig I, Hoogenraad NJ, Clarke AE, Stone BA (1991) The location of (1→ 3)-β-glucans in the walls of pollen tubes of Nicotiana alata using a (1→ 3)-β-glucan-specific monoclonal antibody. Planta 185:1–8

    CAS  Article  PubMed  Google Scholar 

  • Moore PJ, Staehelin LA (1988) Immunogold localization of the cell-wall-matrix polysaccharides rhamnogalacturonan I and xyloglucan during cell expansion and cytokinesis in Trifolium pratense L.; implication for secretory pathways. Planta 174:433–445

    CAS  Article  PubMed  Google Scholar 

  • Moore JP, Nguema-Ona EE, Vicré-Gibouin M, Sørensen I, Willats WG, Driouich A, Farrant JM (2013) Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 237:739–754

    CAS  Article  PubMed  Google Scholar 

  • Muccifora S, Bellani LM (2011) Antheridial dehiscence in ferns. Plant Syst Evol 297:51–56

    Article  Google Scholar 

  • Nickle TC, Meinke DW (1998) A cytokinesis-defective mutant of Arabidopsis (cyt1) characterized by embryonic lethality, incomplete cell walls, and excessive callose accumulation. Plant J 15:321–332

    CAS  Article  PubMed  Google Scholar 

  • Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972

    CAS  Article  PubMed  Google Scholar 

  • Otegui M, Staehelin LA (2000) Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Plant Biol 3:493–502

    CAS  Article  PubMed  Google Scholar 

  • Otegui MS, Staehelin LA (2004) Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta 218:501–515

    CAS  Article  PubMed  Google Scholar 

  • Pedersen HL, Fangel JU, McCleary B, Ruzanski C, Rydahl MG, Ralet MC, Farkas V, von Schantz L, Marcus SE, Andersen MC, Field R (2012) Versatile high resolution oligosaccharide microarrays for plant glycobiology and cell wall research. J Biol Chem 287:39429–39438

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Piršelová B, Matušíková I (2013) Callose: the plant cell wall polysaccharide with multiple biological functions. Acta Physiol Plant 35:635–644

    Article  Google Scholar 

  • Renzaglia KS, Garbary DJ (2001) Motile male gametes of land plants: diversity, development, and evolution. Crit Rev Plant Sci 20:107–213

    Article  Google Scholar 

  • Rudall PJ, Bateman RM (2007) Developmental bases for key innovations in the seed-plant microgametophyte. Trends Plant Sci 12:317–326

    CAS  Article  PubMed  Google Scholar 

  • Samuels AL, Giddings TH, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357

    CAS  Article  PubMed  Google Scholar 

  • Staehelin LA, Hepler PK (1996) Cytokinesis in higher plants. Cell 84:821–824

    CAS  Article  PubMed  Google Scholar 

  • Töller A, Brownfield L, Neu C, Twell D, Schulze-Lefert P (2008) Dual function of Arabidopsis glucan synthase-like genes GSL8 and GSL10 in male gametophyte development and plant growth. Plant J 54:911–923

    Article  PubMed  Google Scholar 

  • Ton J, Mauch-Mani B (2004) β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38:119–130

    CAS  Article  PubMed  Google Scholar 

  • Ulvskov P, Wium H, Bruce D, Jørgensen B, Qvist KB, Skjøt M, Hepworth D, Borkhardt B, Sørensen SO (2005) Biophysical consequences of remodeling the neutral side chains of rhamnogalaturonan I in tubers of transgenic potatoes. Planta 220:609–620

    CAS  Article  PubMed  Google Scholar 

  • Verhertbruggen Y, Knox JP (2007) Pectic polysaccharides and expanding cell walls. In: Verbelen J-P, Vissenberg K (eds) Plant cell monographs: the expanding cell, vol 5. Springer, Berlin Heidelberg, pp 139–158

    Google Scholar 

  • Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohyd Res 344:1858–1862

    CAS  Article  Google Scholar 

  • Verma DP (2001) Cytokinesis and building of the cell plate in plants. Ann Rev Plant Biol 52:751–784

    CAS  Article  Google Scholar 

  • Vian B (1970) Observations sur l’evolution des substances intercellulaires pendant la spermatogénèse chez une hepatique, Fossombronia angulosa. Comptes Rendus de I’Académie des Sciences—Series D 270:1240–1243

  • Warne TR, Walker GL, Hickok LG (1986) A novel method for surface-sterilizing and sowing fern spores. Am Fern J 76:187–188

    Article  Google Scholar 

  • Wolf S, Hématy K, Höfte H (2012) Growth control and cell wall signaling in plants. Ann Rev Plant Biol 63:381–407

    CAS  Article  Google Scholar 

  • Yariv J, Lis H, Katchalski E (1967) Precipitation of Arabic acid and some seed polysaccharides by glycosyl phenylazo dyes. Biochem J 105:1c–2c

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Zimmerli L, Stein M, Lipka V, Schulze-Lefert P, Somerville S (2004) Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J 40:633–646

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Grants from the National Science Foundation (DEB-0521177, DEB-06387622, DUE-1136414) and the National Institutes of Health (4R25GM107760-04). We also thank Dr. Les Hickok for graciously supplying the Ceratopteris spores used in this investigation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Renee A. Lopez.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lopez, R.A., Renzaglia, K.S. The Ceratopteris (fern) developing motile gamete walls contain diverse polysaccharides, but not pectin. Planta 247, 393–404 (2018). https://doi.org/10.1007/s00425-017-2793-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2793-6

Keywords

  • Callose
  • Cell walls
  • Galactoxyloglucans
  • Hemicelluloses
  • Pectins
  • Spermatogenesis
  • Xyloglucans