Abstract
The syncytium formed by Utricularia is extremely unusual and perhaps unique among angiosperm syncytia. All typical plant syncytia (articulated laticifers, amoeboid tapetum, the nucellar plasmodium of river weeds) are formed only by fusion of sporophytic cells which possess the same genetic material, unlike Utricularia in which the syncytium possesses nuclei from two different sources: cells of maternal sporophytic nutritive tissue and endosperm haustorium (both maternal and paternal genetic material). How is this kind of syncytium formed and organized and is it similar to other plant syncytial structures? We used light and electron microscopy to reconstruct the step-by-step development of the Utricularia syncytia. The syncytia of Utricularia developed through heterotypic cell fusion involving the digestion of the cell wall, and finally, heterokaryotic multinucleate structures were formed, which possessed different-sized nuclei that were not regularly arranged in the cytoplasm. We showed that these syncytia were characterized by hypertrophy of nuclei, abundant endoplasmic reticulum and organelles, and the occurrence of wall ingrowths. All these characters testify to high activity and may confirm the nutritive and transport functions of the syncytium for the develo** embryo. In Utricularia, the formation of the syncytium provides an economical way to redistribute cell components and release nutrients from the digested cell walls, which can now be used for the embryo, and finally to create a large surface for the exchange of nutrients between the placenta and endosperm.
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References
Anger EM, Weber M (2006) Pollen-wall formation in Arum alpinum. Ann Bot (Lond) 97:239–244
Arekal GD, Nagendran CR (1975a) Is there a Podostemum type of embryo sac in the genus Farmeria? Caryologia 28:229–235
Arekal GD, Nagendran CR (1975b) Embryo sac of Hydrobryopsis sessilis (Podostemaceae)—origin, organization and significance. Bot Not 128:332–337
Baluška F, Volkmann D, Barlow PW (2004) Eukaryotic cells and their cell bodies: Cell Theory revised. Ann Bot (Lond) 94:9–32
Battaglia E (1987) Embryological questions: 11. Has the debated case of Podostemaceae been resolved? Ann Bot (Roma) 45:37–64
Brown RC, Lemmon BE (2001) The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 215:35–49
Brown RC, Lemmon BE, Nguyen H (2004) Comparative anatomy of the chalazal endosperm cyst in seeds of the Brassicaceae. Bot J Linn Soc 144:375–394
Esau K (1965) Plant Anatomy. Wiley, London
Farooq M (1964) Studies in the Lentibulariaceae I. The embryology of Utricularia stellaris L. var. inflexa Clarke. Part II. Microsporangium, male gametophyte, fertilization, endosperm, embryo, and seed. Proc Natl Inst Sci India 30:280–299
Gabara B (2001) Jądro. In: Woźny A, Michejda J, Ratajczak L (eds) Podstawy biologii komórki roślinnej. Uniwersytet im Adama Mickiewicza w Poznaniu, Poznań, pp 158–226
Ghogue J-P, Ameka GK, Grob V, Huber KA, Pfeifer E, Rutishauser R (2009) Enigmatic morphology of D**ga felicis (Podostemaceae–Podostemoideae), a badly known endemic from northwestern Cameroon. Bot J Linn Soc 160:64–81
Golinowski W, Magnusson C (1991) Tissue response induced by Heterodera schachtii (Nematoda) in susceptible and resistant white mustard cultivars. Can J Bot 69:53–62
Golinowski W, Grundler FMW, Sobczak M (1996) Changes in the structure of Arabidopsis thaliana during female development of the plant-parasitic nematode Heterodera schachtii. Protoplasma 194:103–116
Goverse A, Overmars H, Engelbertink J, Schots A, Bakier J, Helder J (2000) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. MPMI 13:1121–1129
Grundler MW, Sobczak M, Golinowski W (1998) Formation of wall openings in root cells of Arabidopsis thaliana following infection by the plant-parasitic nematode Heterodera schachtii. Eur J Plant Pathol 104:545–551
Gunning BES, Pate JS (1969) “Transfer cells” plant cells with wall ingrowths, specialized in relation to short distance transport of solutes—their occurrence, structure, and development. Protoplasma 68:107–133
Gunning BES, Pate JS (1974) Transfer cells. In: Robards AW (ed) Dynamic aspects of plant ultrastructure. McGraw-Hill, London, pp 441–480
Holtmann B, Kleine M, Grundler FMW (2000) Ultrastructure and anatomy of nematode-induced syncytia in roots of susceptible and resistant sugar beet. Protoplasma 211:39–50
Jäger-Zürn I (1997) Embryological and floral studies in Weddellina squamulosa Tul. (Podostemaceae, Tristichoideae). Aquat Bot 57:151–182
Jankun A, Płachno B (2000) Embryology of Utricularia vulgaris L. Acta Biol Cracov Bot 42/1: 23. Abstracts of the XXIV Conference on Embryology Plants, Animals, Humans May 24–26, 2000, Podlesice, Poland
Jobson RW, Albert VA (2002) Molecular rates parallel diversification contrasts between carnivorous plant sister lineages. Cladistics 18:127–136
Jobson RW, Playford J, Cameron KM, Albert VA (2003) Molecular phylogenetics of Lentibulariaceae inferred from plastid rps16 intron and trnL-F DNA sequences: implications for character evolution and biogeography. Syst Bot 28:157–171
Kausik SD (1938) Pollen development and seed formation in Utricularia caerulea. Beih Bot Zbl 58A:365–378
Kausik SB, Raju MVS (1955) A contribution to the floral morphology and embryology of Utricularia retriculata. Proc Indian Acad Sci 41:155–166
Khan R (1954) A contribution to the embryology of Utricularia flexuosa Vahl. Phytomorphol 4:80–117
Kirchoff BK, Pfeifer E, Rutishauser R (2008) Plant structure ontology: how should we label plant structures with doubtful or mixed identities? Zootaxa 1950:103–122
Magnusson C, Golinowski W (1991) Ultrastructural relationships of the develo** syncytium induced by Heterodera schachtii (Nematoda) in root tissues of rape. Can J Bot 69:44–52
Maheshwari P (1950) An introduction to the embryology of angiosperms. New York, McGraw-Hill
Merz M (1897) Untersuchungen über die Samenentwicklung der Utricularien. Flora 84:69–87
Mepham R, Lane G (1969) Formation and development of the tapetal periplasmodium in Tradescantia bracteata. Protoplasma 68:175–192
Mukkada AJ (1962) Some observations on the embryology of Dicraeea stylosa Wight. In: Plant embryology—a symposium. CSIR, New Delhi, pp 139–145
Müller K, Borsch T, Legendre L, Porembski S, Theisen I, Barthlott W (2004) Evolution of carnivory in Lentibulariaceae and the Lamiales. Plant Biol 6:477–490
Müller K, Borsch T (2005) Phylogenetics of Utricularia (Lentibulariaceae) and molecular evolution of the trnK intron in a lineage with high substitutional rates. Plant Syst Evol 250:39–67. doi:10.1007/s00606-004-0224-1
Müller K, Borsch T, Legendre L, Porembski S, Theisen I, Barthlott W (2006) Recent progress in understanding the evolution of carnivorous Lentibulariaceae (Lamiales). Plant Biol 6:477–490. doi:10.1055/s-2004-817909
Murguía-Sánchez G, Alejandro Novelo R, Thomas Philbrick C, Márquez Guzmán GJ (2002) Embryo sac development in Vanroyenella plumosa, Podostemaceae. Aquat Bot 73:201–210
Nagendran CR, Arekal GD, Subramanyan K (1977) Embryo sac studies in three species of Polypleurum (Podostemaceae). Plant Syst Evol 128:215–226
Nagl W (1992) The polytenic endosperm haustorium of Rhinanthus minor (Scrophulariaceae) functional ultrastructure. Can J Bot 70:1997–2004
Nguyen H, Brown RC, Lemmon BE (2002) Cytoskeletal organization of the micropylar endosperm in Coronopus didymus L. (Brassicaceae). Protoplasma 219:210–220
Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54:431–454
Pacini E, Juniper BE (1983) The ultrastructure of the formation and development of the amoeboid tapetum in Arum italicum Miller. Protoplasma 117:116–129
Pastey MK, Gower TL, Spearman PW, Crowe JE Jr, Graham BS (2000) A RhoA-derived peptide inhibits syncytium formation induced by respiratory syncytial virus and parainfluenza virus type 3. Nat Med 6:35–40
Płachno BJ, Świątek P (2008) Cytoarchitecture of Utricularia nutritive tissue. Protoplasma 234:25–32
Płachno BJ, Świątek P (2010) Unusual embryo structure in viviparous Utricularia nelumbifolia, with remarks on embryo evolution in genus Utricularia. Protoplasma 239:69–80
Rutishauser R, Novelo RA, Philbrick CT (1999) Developmental morphology of New World Podostemaceae: Marathrum and Vanroyenella. Int J Plant Sci 160:29–45
Rutishauser R, Moline P (2005) Evo-devo and the search for homology (“sameness”) in biological systems. Theory Biosci 124:213–241
Shemer G, Podbilewicz B (2000) Fusomorphogenesis: cell fusion in organ formation. Dev Dyn 218:30–51
Sobczak M, Golinowski W (2009) Structure of cyst nematode feeding sites. In: Berg RH, Taylor CG (ed) Cell Biology of Plant Nematode Parasitism. Plant Cell Monographs 15
Sobczak M, Grymaszewska G, Kurek W, Golinowski W (1995) Biotechnologiczne metody wprowadzania odporności u roślin na nicienie. Kosmos 44:719–735
Sobczak M, Golinowski W, Grundler FMW (1997) Changes in the structure of Arabidopsis thaliana roots induced during development of males of the plant parasitic nematode Heterodera schachtii. Eur J Plant Pathol 103:113–124
Swamy BGL, Ganapathy PM (1957) A new type of endosperm haustorium in Nothapodytes foetida. Phytomorphol 7:331–336
Taylor P (1989) The genus Utricularia—a taxonomic monograph. Kew B 14:1–735
Tiwari SC, Gunning BES (1986) Colchicine inhibits plasmodium formation and disrupts pathways of sporopollenin secretion in the anther tapetum of Tradescantia virginiana L. Protoplasma 133:115–128
Vijayaraghavan MR, Prabhakar K (1984) The Endosperm. In: Johri BM (ed) Embryology of Angiosperms. Springer-Verlag, Berlin, pp 319–376
Weng J, Krementsov DN, Khurana S, Roy NH, Thali M (2009) Formation of syncytia is repressed by tetraspanins in human immunodeficiency virus type 1-producing cells. J Virol 83:7467–7474
Wylie R, Yocom AE (1923) The endosperm of Utricularia. U Iowa Stud Nat History 10(3–18):32
Acknowledgments
This study was funded by grant N N304 002536 from the Polish Ministry of Science and Higher Education. The first author gratefully acknowledges the support of an award from the Foundation for Polish Sciences (Start Programme). We thank our colleague Dr. Lubomir Adamec for kindly providing part of the material for this study and for hosting BJP in Třeboň. We particularly thank the reviewers for their very helpful suggestions for making our manuscript clearer.
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Płachno, B.J., Świątek, P. Syncytia in plants: cell fusion in endosperm—placental syncytium formation in Utricularia (Lentibulariaceae). Protoplasma 248, 425–435 (2011). https://doi.org/10.1007/s00709-010-0173-1
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DOI: https://doi.org/10.1007/s00709-010-0173-1