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Arabinogalactan proteins and arabinan pectins abound in the specialized matrices surrounding female gametes of the fern Ceratopteris richardii

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Abstract

Main conclusion

Both male and female gametes of archegoniates are highly specialized cells surrounded by an extraprotoplasmic matrix rich in AGPs, which are speculated to facilitate development and gamete fusion through Ca 2+ oscillations. An additional layer, the egg envelope, forms around the egg periphery, except at the fertilization pore, and contains arabinose-rich polymers that presumably impart flexibility for the rapidly growing zygote and embryo. The abundant AGPs and arabinan pectins associated with the eggs of C. richardii not only are integral to development, fertilization, and early embryogenesis, but also may be involved in desiccation tolerance important to the survival of the reproductive gametophyte.

A defining feature of gametogenesis in archegoniates is the deposition of a special matrix outside of the plasmalemma of both egg and sperm cells that displaces the primary cell wall away from the protoplasm. It is within this matrix that gamete differentiation occurs. In leptosporangiate ferns, maturation of the egg cell involves the deposition of a second specialized wall, the so-called egg envelope that surrounds the cell except at the fertilization pore, a narrow site where gamete fusion takes place. We provide the first conclusive evidence of the macromolecular constituents in the unique structures surrounding fern egg cells before and after fertilization. To test the hypotheses that the egg extracellular matrix contains arabinogalactan proteins (AGPs) as does the sperm cell matrix, and that cell wall polysaccharides, especially pectins, are components of the egg envelope, we examined the expression patterns of AGPs and cell wall constituents during oogenesis in Ceratopteris richardii. Utilizing histochemical stains for callose, cellulose and AGPs coupled with immunogold localizations employing a suite of monoclonal antibodies to cell wall components (JIM13, JIM8, LM2, LM5, LM6, LM19, LM20 and anticallose), we demonstrate that AGPs, but not pectins, are abundant in the matrix around egg cells and degrading neck canal and ventral canal cells during archegonial development. A striking finding is that both AGPs and (1,5)-α-l-arabinan pectin epitopes are principle components of the egg envelope before and after fertilization, suggesting that they are important in both egg maturation and gamete fusion.

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Abbreviations

AGP:

Arabinogalactan protein

MAb:

Monoclonal antibody

References

  • Acosta-García G, Vielle-Calzada JP (2004) A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16:2614–2628

    Article  PubMed  PubMed Central  Google Scholar 

  • Antoine AF, Faure JE, Cordeiro S, Dumas C, Rougier M, Feijo JA (2000) A calcium influx is triggered and propagates in the zygote as a wave front during in vitro fertilization of flowering plants. Proc Natl Acad Sci 97:10643–10648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao WM, Qun HE, Wang QX, Tian GW, Cao JG (2005) Ultrastructure of oogenesis in Dryopteris crassirhizoma Nakai. J Integr Plant Biol 47:201–213

    Article  Google Scholar 

  • Bell PR, Duckett JG (1976) Gametogenesis and fertilization in Pteridium. Bot J Linn Soc 73:47–78

    Article  Google Scholar 

  • Bush MS, Marry M, Huxham MI, Jarvis MC, McCann MC (2001) Developmental regulation of pectic epitopes during potato tuberisation. Planta 213:869–880

    Article  CAS  PubMed  Google Scholar 

  • Cao JG, Wang QX, Bao WM (2010a) Formation of the fertilization pore during oogenesis of the fern Ceratopteris thalictroides. J Integr Plant Biol 52:518–527

    Article  PubMed  Google Scholar 

  • Cao JG, Wang QX, Dai XL (2010b) Ultrastructural observations of oogenesis in the fern Adiantum flabellulatum L. (Adiantaceae). Am Fern J 100:93–102

    Article  Google Scholar 

  • Cao JG, Dai XL, Wang QX (2012a) Cytological features of oogenesis and their evolutionary significance in the fern Osmunda japonica. Sex Plant Reprod 25:147–156

    Article  CAS  PubMed  Google Scholar 

  • Cao JG, Dai XL, Wang QX (2012b) Ultrastructural and chemical studies on oogenesis of the fern Pteridium aquilinum. Sex Plant Reprod 25:61–69

    Article  PubMed  Google Scholar 

  • Cave CF, Bell PR (1974) The nature of the membrane around the egg of Pteridium aquilinum (L.) Kuhn. Ann Bot 38:17–21

    Google Scholar 

  • Chudzik B, Zarzyka B, Śniezko R (2005) Immunodetection of arabinogalactan proteins in different types of plant ovules. Acta Biol Cracov Ser Bot 47:139–146

    Google Scholar 

  • Coimbra S, Duarte C (2003) Arabinogalactan proteins may facilitate the movement of pollen tubes from the stigma to the ovules in Actinidia deliciosa and Amaranthus hypochondriacus. Euphytica 133:171–178

    Article  Google Scholar 

  • Coimbra S, Pereira G (2012) Arabinogalactan proteins in Arabidopsis thaliana pollen development. In: Ciftci YO (ed) Transgenic plants—advances and limitations, pp 329–352, InTech. http://www.intechopen.com/books/transgenic-plants-advances-and-limitations/arabinogalactan-proteins-in-arabidopsis-thaliana-pollen-development

  • Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG (2007) Arabinogalactin proteins as a molecular markers in Arabidopsis thaliana sexual reproduction. J Exp Bot 58:4027–4035

    Article  CAS  PubMed  Google Scholar 

  • Coimbra S, Jones B, Pereira LG (2008) Arabinogalactan proteins (AGPs) related to pollen tube guidance into the embryo sac in Arabidopsis. Plant Signal Behav 3:455–456

    Article  PubMed  PubMed Central  Google Scholar 

  • Costa M, Pereira AM, Rudall PJ, Coimbra S (2013) Immunolocalization of arabinogalactan proteins (AGPs) in reproductive structures of an early-divergent angiosperm, Trithuria (Hydatellaceae). Ann Bot Lond 111:183–190

    Article  CAS  Google Scholar 

  • Denninger P, Bleckmann A, Lausser A, Vogler F, Ott T, Ehrhardt DW, Frommer WB, Sprunck S, Dresselhaus T, Grossman G (2014) Male–female communication triggers calcium signatures during fertilization in Arabidopsis. Nat Commun 5:1–12

    Article  Google Scholar 

  • Ducibella T, Huneau D, Angelichio E, Xu Z, Schultz RM, Kopf GS, Fissore R, Madoux S, Ozil J-P (2002) Egg-to-embryo transition is driven by differential responses to Ca2+ oscillation number. Dev Biol 250:280–291

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fangel JU, Ulvskov P, Knox JP, Mikkelsen MD, Harholt J, Popper ZA, Willats WGT (2012) Cell wall evolution and diversity. Front Plant Sci 3:1–8

    Article  Google Scholar 

  • Fasciati R, Schneller J, Jenni V, Roos UP (1994) Fertilization in the fern Athyrium felix-femina (Pterophyta) II. Ultrastructure. Crypt Bot 4:356–367

    Google Scholar 

  • Faure JE, Digonnet C, Dumas C (1994) An in vitro system for adhesion and fusion of maize gametes. Science 263:1598–1600

    Article  CAS  PubMed  Google Scholar 

  • Ge LL, Tian HQ, Russell SD (2007) Calcium function and distribution during fertilization in angiosperms. Am J Bot 94:1046–1060

    Article  CAS  PubMed  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

  • Ha MA, Viëtor RJ, Jardine GD, Apperley DC, Jarvis MC (2005) Conformation and mobility of the arabinan and galactan side chains of pectin. Phytochemistry 66:1817–1824

    Article  CAS  PubMed  Google Scholar 

  • Jaffe LF (1990) The roles of intramembrane calcium in polarizing and activating eggs. In: Dale B (ed) Mechanism of fertilization: plants to humans. Springer, Berlin, pp 389–417

    Chapter  Google Scholar 

  • Jauh GY, Lord FM (1996) Localization of pectins and arabinogalactan-proteins in lily (Lilium longiflorum L.) pollen tube and style and their possible roles in pollination. Planta 199:251–261

    Article  CAS  Google Scholar 

  • Johnson GP, Renzaglia KS (2008) Embryology of Ceratopteris richardii (Pteridaceae, tribe Ceratopterideae), with emphasis on placental development. J Plant Res 12:581–592

    Article  Google Scholar 

  • Johnson GP, Renzaglia KS (2009) Evaluating the diversity of pteridophyte embryology in the light of recent phylogenetic analyses leads to new inferences on character evolution. Plant Syst Evol 283:149–164

    Article  Google Scholar 

  • Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1–4)-β-d-galactan. Plant Physiol 113:1405–1412

    CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Lloyd RM (1974) Systematics of the genus Ceratopteris Brongn.(Parkeriaceae) II. Taxonomy. Brittonia 26:139–160

  • 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 

  • Lopez-Smith RA, Renzaglia KS (2008) Sperm cell architecture, insemination, and fertilization in the model fern, Ceratopteris richardii. Sex Plant Reprod 21:153–167

    Article  Google Scholar 

  • Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122:3–10

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Mogami N, Nakamura S, Nakamura N (1999) Immunolocalization of the cell wall components in Pinus densiflora pollen. Protoplasma 206:1–10

    Article  CAS  Google Scholar 

  • Moore JP, Vicré-Gibouin M, Farrant JM, Driouich A (2008) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plantarum 134:237–245

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Myles DG (1978) The fine structure of fertilization in the fern Marsilea vestita. J Cell Sci 30:265–281

    CAS  PubMed  Google Scholar 

  • Pennell RI, Janniche L, Kjellbom P, Scofield GN, Peart JM, Roberts K (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3:1317–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popper ZA, Michel G, Hervé C, Domozych DS, Willats WGT, Tuohy MG, Kloareg B, Stengel DB (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Ann Rev Plant Biol 62:567–590

    Article  CAS  Google Scholar 

  • Qin Y, Zhao J (2006) Localization of arabinogalactan proteins in egg cells, zygotes, and two-celled proembryos and effects of β-d-glucosyl Yariv reagent on egg cell fertilization and zygote division in Nicotiana tabacum L. J Exp Bot 57:2061–2074

    Article  CAS  PubMed  Google Scholar 

  • Rafińska K, Bednarska E (2011) Localisation pattern of homogalacturonan and arabinogalactan proteins in developing ovules of the gymnosperm plant Larix decidua Mill. Sex Plant Reprod 24:75–87

    Article  PubMed  Google Scholar 

  • Renzaglia KS, Lopez RA, Johnson EE (2014) Callose is integral to the development of permanent tetrads in the liverwort Sphaerocarpos. Planta 241:615–627

    Article  PubMed  Google Scholar 

  • Roberts S, Brownlee C (1995) Calcium influx, fertilisation potential and egg activation in Fucus serratus. Zygote 3:191–197

    Article  CAS  PubMed  Google Scholar 

  • Runft LL, Jaffe LA, Mehlmann LM (2002) Egg activation at fertilization: where it all begins. Dev Biol 245:237–254

    Article  CAS  PubMed  Google Scholar 

  • Smallwood M, Yates EA, Willats WG, Martin H, Knox JP (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459

    Article  CAS  Google Scholar 

  • Sørensen I, Domozych D, Willats WG (2010) How have plant cell walls evolved? Plant Physiol 153:366–372

    Article  PubMed  PubMed Central  Google Scholar 

  • Southworth D, Kwiatkowski S (1996) Arabinogalactan proteins at the cell surface of Brassica sperm and Lilium sperm and generative cells. Sex Plant Reprod 9:269–272

    Article  CAS  Google Scholar 

  • 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 127:1141–1150

    CAS  PubMed  Google Scholar 

  • Tian HQ, Russell SD (1997) Calcium distribution in fertilized and unfertilized ovules and embryo sacs of Nicotiana tabacum L. Planta 202:93–105

    Article  CAS  Google Scholar 

  • Tian HQ, Zhu H, Russell SD (2000) Calcium changes in ovules and embryo sacs of Plumbago zeylanica L. Sex Plant Reprod 13:11–20

    Article  CAS  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 rhamnogalacturonan I in tubers of transgenic potatoes. Planta 220:609–620

    Article  CAS  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, pp 139–158

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Verhertbruggen YS, Marcus SE, Haeger A, Verhoef R, Schols HA, McCleary BV, McKee L, Gilbert HG, Knox JP (2009b) Developmental complexity of arabinan polysaccharides and their processing in plant cell walls. Plant J 59:413–425

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Watkins JE, Mack MC, Sinclair TR, Mulkey SS (2007) Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes. New Phytol 176:708–717

    Article  PubMed  Google Scholar 

  • Willats WG, Marcus SE, Knox JP (1998) Generation of a monoclonal antibody specific to (1,5)-α-l-arabinan. Carbohyd Res 308:149–152

    Article  CAS  Google Scholar 

  • Willats WG, Steele-King CG, Marcus SE, Knox JP (1999) Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J 20:619–628

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yates EA, Valdor J-F, Haslam SM, Morris HR, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6:131–139

    Article  CAS  PubMed  Google Scholar 

  • Yu F, Zhao J, Liang S, Yang H (1998) Ultracytochemical localization of calcium in the gynoecium and embryo sac of rice. Acta Bot Sin 41:125–129

    Google Scholar 

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Acknowledgments

We thank Les Hickok for the Ceratopteris spores used in this study. We also thank Bryan Piatkowski, Amelia Merced, Nicholas Flowers and Jason Henry for technical support and comments on the manuscript. This work was supported by the National Science Foundation (Grants DEB-0423625, DEB-0521177, DEB-0638722).

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  1. Department of Plant Biology, MC: 6509, Southern Illinois University Carbondale, Carbondale, IL, 62901, USA

    Renee A. Lopez & Karen S. Renzaglia

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Correspondence to Renee A. Lopez.

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Lopez, R.A., Renzaglia, K.S. Arabinogalactan proteins and arabinan pectins abound in the specialized matrices surrounding female gametes of the fern Ceratopteris richardii . Planta 243, 947–957 (2016). https://doi.org/10.1007/s00425-015-2448-4

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