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Unusual embryo structure in viviparous Utricularia nelumbifolia, with remarks on embryo evolution in genus Utricularia

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Abstract

In most species of the Genlisea–Utricularia sister lineage, the organs arising directly after germination comprise a single leaf-like structure, followed by a bladder-trap/stolon, with the lack of an embryonic primary root considered a synapomorphic character. Previous anatomical work suggests that the most common recent ancestor of Utricularia possessed an embryo comprising storage tissue and a meristematic apical region minus lateral organs. Studies of embryogenesis across the Utricularia lineage suggest that multiple primary organs have only evolved in the viviparous Utricularia nelumbifolia, Utricularia reniformis, and Utricularia humboldtii within the derived Iperua/Orchidioides clade. All three of these species are specialized for growth as “aquatic epiphytes” in the tanks of bromeliads, with recent phylogenetic evidence suggesting the possibility that multiple primary organs may have evolved twice independently within this clade. The primary organs of viviparous Utricularia also possess epidermal surface glands, and our study suggests that these may function as root hairs for uptake of solutes from the external environment—a possible adaptation for the “aquatic–epiphytic” habitat.

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References

  • Arditti J (1992) Fundamentals of orchid biology. Wiley, New York

    Google Scholar 

  • Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  CAS  PubMed  Google Scholar 

  • Brugger J, Rutishauser R (1989) Bau und Entwicklung landbewohnender Utricularia-Arten. Bot Helv 99:91–146

    Google Scholar 

  • Chandler JW (2008) Cotyledon organogenesis. J Exp Bot 59:2917–2931

    Article  CAS  PubMed  Google Scholar 

  • Compton RH (1909) The morphology and anatomy of Utricularia brachiata, Oliver. New Phytol 8:117–130

    Article  Google Scholar 

  • Czapik R, Izmaiłow R (2001) Zygotic embryogenesis. In: Bhojwani SS, Soh WY (eds) Current Trends in the Embryology of Angiosperms. Kluwer Academic Publishers, Dordrecht, the Netherlands, pp. 197–222

  • Degtjareva G, Casper J, Hellwig F, Sokoloff D (2004) Seed morphology in the genus Pinguicula (Lentibulariaceae) and its relation to taxonomy and phylogeny. Bot Jahrb Syst 125:431–452

    Article  Google Scholar 

  • Degtjareva GV, Casper SJ, Hellwig FH, Schmidt AR, Steiger J, Sokoloff DD (2006) Morphology and nrITS phylogeny of the genus Pinguicula L. (Lentibulariaceae), with special attention to embryo evolution. Plant Biol 8:778–790

    Article  CAS  PubMed  Google Scholar 

  • Farooq M (1965) Studies in the Lentibulariaceae III. The embryology of Utricularia uliginosa Vahl. Phytomorphology 15:123–131

    Google Scholar 

  • Farooq M, Siddiqui SA (1964) The embryology of Utricularia stellaris Linn. f. Sci Cult 30:394–395

    Google Scholar 

  • Farooq M, Bilquis S (1966) Studies in the Lentibulariaceae 7. The embryogeny in U. scandens Benj. Beitr Biol Pflanz 42:127–131

    Google Scholar 

  • Fineran BA (1980) Ontogeny of external glands in the bladderwort Utricularia monanthos. Protoplasma105: 9–25

  • Goebel K (1891) Morphologische und biologische Studien, V. Utricularia. Ann Jard Bot Buitenzorg 9:41–119

    Google Scholar 

  • Goebel K (1893a) Pflanzenbiologische Schilderungen, vol 2. N.G. Elwert’sche Velagsbuchhandlung, Marburg, Germany

    Google Scholar 

  • Goebel K (1893b) Zur Biologie von Genlisea. Flora 77:208–212

    Google Scholar 

  • Hadfi K, Speth V, Neuhaus G (1998) Auxin-induced developmental patterns in Brassica juncea embryos. Development 125:879–887

    CAS  PubMed  Google Scholar 

  • Jobson RW, Albert VA (2002) Molecular rates parallel diversification contrasts between carnivorous plant sister lineages. Cladistics 18:127–136

    Google Scholar 

  • 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

    Google Scholar 

  • Kamieński F (1876) Porównawcze badania nad wzrostem pływaczów (Utricularia) Rozprawy i Sprawozdania z Posiedzeń Wydziału Matematyczno-Przyrodniczego Akademii Umiejętności 3: 210-240

  • Kaplan DR, Cooke TJ (1997) Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9:1903–1919

    Article  CAS  PubMed  Google Scholar 

  • Kausik SD (1938) Pollen development and seed formation in Utricularia caerulea. Beih Bot Zbl 58A: 365–378

    Google Scholar 

  • Khan R (1954) A contribution to the embryology of Utricularia flexuosa Vahl. Phytomorphology 4:80–117

    Google Scholar 

  • Khan R (1992) Lentibulariaceae. In: Johri BM, Ambegaokar KB, Srivastava PS (eds) Comparative embryology of angiosperms II. Springer, Berlin, pp 755–762

    Google Scholar 

  • Kondo K (1971) Germination and developmental morphology of seeds inUtricularia cornuta Michx. and Utricularia juncea Vahl. Rhodora 73:541–547

    Google Scholar 

  • Kondo K, Segawa M, Nehira K (1978) Anatomical studies on seeds and seedlings of some Utricularia (Lentibulariaceae). Brittonia 30:89–95

    Article  Google Scholar 

  • Kumazawa M (1967) An experimental study on the seedling of Utricularia pilosa Makino. Phytomorphology 17:494–498

    Google Scholar 

  • Lang FX (1901) Untersuchungen über Morphologie, Anatomie und Samenentwicklung von Polypompholyx und Byblis gigantea. Flora 88:149–206

    Google Scholar 

  • Lloyd FE (1942) The carnivorous plants. Chronica Botanica, Waltham

    Google Scholar 

  • Lomax T, Muday G, Rubery P (1995) Auxin transport. In: Davies PJ (ed) Plant hormones: physiology, biochemistry, and molecular biology. Kluwer, Norwell, MA, pp 509–530

    Google Scholar 

  • Mantegazza R, Möller M, Harrison CJ, Fior S, De Luca C, Spada A (2007) Anisocotyly and meristem initiation in an unorthodox plant, Streptocarpus rexii (Gesneriaceae). Planta 225:653–63

    Article  CAS  PubMed  Google Scholar 

  • Möller M, Cronk QCB (2001) Evolution of morphological novelty: a phylogenetic analysis of growth patterns in Streptocarpus (Gesneriaceae). Evolution 55:918–929

    Article  PubMed  Google Scholar 

  • Merl EM (1915) Beiträge zur Kenntnis der Utricularien und Genlisen. Flora 108:127–200

    Google Scholar 

  • Merl EM (1925) Beiträge zur Kenntnis der brasilianischen Utricularien. Flora 118–119:386–392

    Google Scholar 

  • Merz M (1897) Untersuchungen über die Samenentwicklung der Utricularien. Flora 84:69–87

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Müller K, Borsch T, Legendre L, Porembski S, Barthlott W (2006) Recent progress in understanding the evolution of Lentibulariaceae. Plant Biol 8:748–757

    Article  PubMed  Google Scholar 

  • Natesh S, Rau MA (1984) The embryo. In: Johri BM (ed) Embryology of angiosperms. Springer-Verlag, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • Olson AR (1980) Seed morphology of Monotropa uniflora L. (Ericaceae). Am J Bot 67:968–974

    Article  Google Scholar 

  • Płachno B (2002) Embryology of section Calpidisca members: Utricularia livida E. Meyer and Utricularia sandersonii Oliver (Lentibulariaceae). MSc thesis. The Jagiellonian University, Cracow (in Polish)

  • Płachno BJ, Świątek P (2008) Cytoarchitecture of Utricularia nutritive tissue. Protoplasma 234:25–32

    Article  PubMed  Google Scholar 

  • Płachno BJ, Adamus K, Faber J, Kozłowski J (2005a) Feeding behaviour of carnivorous Genlisea plants in the laboratory. Acta Bot Gall 152:159–164

    Google Scholar 

  • Płachno BJ, Faber J, Jankun A (2005b) Cuticular discontinuities in glandular hairs of Genlisea St.-Hil. in relation to their functions. Acta Bot Gall 152:125–130

    Google Scholar 

  • Płachno BJ, Clivati D, Miranda VFO de and Świątek P (2009) Are there seed pedestals in Lentibulariaceae? Acta Biol Cracovi Bot, in press

  • Rajan SS, Kumar DJ (1974) Embryological studies in Lentibulariaceae I. Floral morphology and embryology of Utricularia smithiana, Wt. Ic. Proceedings. Plant Sci 80:18–25

    Google Scholar 

  • Rebernig CA, Weber A (2007) Diversity, development and systematic significance of seed pedestals in Scrophulariaceae (s.l.). Bot Jahrb Syst 127:133–150

    Article  Google Scholar 

  • Rice B, Studnička M (2004) Utricularia reniformis “Enfant Terrible”. Carniv Plant Newslett 33:53–55

    Google Scholar 

  • Rice B (2005) The carnivorous plant FAQ v. 11.5, http://www.sarracenia.com/faq.html

  • Rivadavia F (2001) Utricularia nelumbifolia Gardn. At last! Carniv Pl Newslett 30:5–10

    Google Scholar 

  • Rutishauser R, Sattler R (1989) Complementarity and heuristic value of contrasting models in structural botany. III. Case study on shootlike “leaves” and leaf-like “shoots” in Utricularia macrorhiza and U. purpurea (Lentibulariaceae). Bot Jahrb Syst 111:121–137

    Google Scholar 

  • Rutishauser R, Isler B (2001) Developmental genetics and morphological evolution of flowering plants, especially bladderworts (Utricularia): Fuzzy Arberian Morphology complements classical morphology. Ann Bot 88:1173–1202

    Article  Google Scholar 

  • Siddiqui SA (1978) Studies in the Lentibulariaceae 9. Pollination, fertilization, endosperm, embryo and seed in Utricularia dichotoma Labill. Bot Jahrb Syst Pflanzen Pflanzengeographie 100:237–245

    Google Scholar 

  • Siddiqui SA (1979) Lentibulariaceae 11. The development of endosperm and embryo in Utricularia cornuta Mixch. Proc Indian Acad Sci 88:213–217

    Google Scholar 

  • Shivaramiah G (1967) Observations on the floral morphology and embryology of Utricularia stricticaulis Stapf. Proc Plant Sci 65:56–62

    Google Scholar 

  • Swamy RD, Mohan Ram HY (1969) Studies on growth and flowering in axenic cultures of insectivorous plants. I. Seed germination and establishment of cultures of Utricularia inflexa. Phytomorphology 19:363–371

    Google Scholar 

  • Studnička M (2003) Observations on life strategies of Genlisea, Heliamphora, and Utricularia in natural habitats. Carniv Plant Newslett 32:57–61

    Google Scholar 

  • Studnička M (2004) Observations on two different forms of Utricularia reniformis. Carniv Plant Newslett 33:47–51

    Google Scholar 

  • Studnička M (2005) Podivne klíčíí bublinatky z Jižní Ameriky. Trifid 4:8–9

    Google Scholar 

  • Studnička M (2006) Masožravé rostliny-objekt badatelů, dobrodruhů a snílků. Academia, Praha

    Google Scholar 

  • Taylor P (1989) The genus Utricularia—a taxonomic monograph. Kew B 14:1–735

    Google Scholar 

  • Teryokhin ES and Nikiticheva ZI (1981) The family Orobanchaceae ontogeny and phylogeny. Leningrad “Nauka,” Leningrad

  • Treml BS, Winderl S, Radykewicz R, Herz M, Schweizer G, Hutzler P, Glawischnig E, Ruiz RAT (2005) The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development 132:4063–4074

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This paper is dedicated to Charles Darwin to mark 200 years since his birth and 150 years since the publication of his “On the Origin of Species”. 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 colleagues Kamil Pásek (Czech Republic, http://www.bestcarnivorousplants.com) and Dr. Lubomir Adamec for kindly providing seeds and seedlings for this study. We thank the rector of the Jagiellonian University, Professor Szczepan Biliński, for generously supporting our projects, and Dr. Miroslav Studnička (Director of the Botanical Garden in Liberec, Czech Republic) for kindly providing U. reniformis “Enfant Terrible” for our study. We particularly thank reviewers for very helpful suggestions to make our manuscripts more clear.

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The authors declare that they have no conflict of interest.

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  1. Department of Plant Cytology and Embryology, Jagiellonian University, ul. Grodzka 52, 31-044, Krakow, Poland

    Bartosz J. Płachno

  2. Department of Animal Histology and Embryology, University of Silesia, ul. Bankowa 9, 40-007, Katowice, Poland

    Piotr Świątek

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  1. Bartosz J. Płachno
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Correspondence to Bartosz J. Płachno.

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Płachno, B.J., Świątek, P. Unusual embryo structure in viviparous Utricularia nelumbifolia, with remarks on embryo evolution in genus Utricularia . Protoplasma 239, 69–80 (2010). https://doi.org/10.1007/s00709-009-0084-1

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