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Floral development of petaloid Alismatales as an insight into the origin of the trimerous Bauplan in monocot flowers

Journal of Plant Research volume 131, pages 395–407 (2018)Cite this article

Abstract

Monocots are remarkably homogeneous in sharing a common trimerous pentacyclic floral Bauplan. A major factor affecting monocot evolution is the unique origin of the clade from basal angiosperms. The origin of the floral Bauplan of monocots remains controversial, as no immediate sister groups with similar structure can be identified among basal angiosperms, and there are several possibilities for an ancestral floral structure, including more complex flowers with higher stamen and carpel numbers, or strongly reduced flowers. Additionally, a stable Bauplan is only established beyond the divergence of Alismatales. Here, we observed the floral development of five members of the three ‘petaloid’ Alismatales families Butomaceae, Hydrocharitaceae, and Alismataceae. Outer stamen pairs can be recognized in mature flowers of Alismataceae and Butomaceae. Paired stamens always arise independently, and are either shifted opposite the sepals or close to the petals. The position of stamen pairs is related to the early development of the petals. In Butomaceae, the perianth is not differentiated and the development of the inner tepals is not delayed; the larger inner tepals (petals) only permit the initiation of stamens in antesepalous pairs. Alismataceae has delayed petals and the stamens are shifted close to the petals, leading to an association of stamen pairs with petals in so-called stamen–petal complexes. In the studied Hydrocharitaceae species, which have the monocot floral Bauplan, paired stamens are replaced by larger single stamens and the petals are not delayed. These results indicate that the origin of the floral Bauplan, at least in petaloid Alismatales, is closely linked to the position of stamen pairs and the rate of petal development. Although the petaloid Alismatales are not immediately at the base of monocot divergence, the floral evolution inferred from the results should be a key to elucidate the origin of the floral Bauplan of monocots.

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References

  • APG (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Article  Google Scholar 

  • Burger WC (1977) The Piperales and the monocots. Alternate hypotheses for the origin of monocotyledonous flowers. Bot Rev 43:345–393

    Article  Google Scholar 

  • Buzgo M, Endress P (2000) Floral structure and development of Acoraceae and its systematic relationships with basal angiosperms. Int J Plant Sci 161:23–41

    CAS  Article  Google Scholar 

  • Buzgo M, Soltis PS, Soltis DE (2004) Floral developmental morphology of Amborella trichopoda (Amborellaceae). Int J Plant Sci 165:925–947

    Article  Google Scholar 

  • Buzgo M, Soltis DE, Soltis PS et al (2006) Perianth development in the basal monoco Triglochin maritima (Juncaginaceae). Aliso J Syst Evol Bot 22:107–125

    Google Scholar 

  • Charlton W (1991) Studies in the Alismataceae. IX. Development of the flower in Ranalisma humile. Can J Bot 69:2790–2796

    Article  Google Scholar 

  • Charlton W (1999a) Studies in the Alismataceae. X. Floral organogenesis in Luronium natans (L.) Raf. Can J Bot 77:1560–1568

    Article  Google Scholar 

  • Charlton W (1999b) Studies in the Alismataceae. XI. Development of the inflorescence and flowers of Wiesneria triandra (Dalzell) Micheli. Can J Bot 77:1569–1579

    Article  Google Scholar 

  • Charlton W (2004) Studies in the Alismataceae. XII. Floral organogenesis in Damasonium alisma and Baldellia ranunculoides, and comparisons with Butomus umbellatus. Can J Bot 82:528–539

    Article  Google Scholar 

  • Chase MW, Fay MF, Devey DS et al (2006) Multigene analyses of monocot relationships. Aliso J Syst Evol Bot 22:63–75

    Google Scholar 

  • Chen D, Chen J, Wang Y, Wang Q (2002) Floral organogenesis of Caldesia grandis Samuel. (Alismataceae). Acta Phytotaxon Sin 41:229–234

    Google Scholar 

  • Dahlgren RMT, Clifford HT, Yeo PF (1985) The families of the monocotyledons. Structure, evolution, and taxonomy. Springer, Berlin

    Book  Google Scholar 

  • Eichler AW (1875) Blüthendiagramme I. Wilhelm Engelmann, Leipzig

    Google Scholar 

  • Endress PK (1987) Floral phyllotaxis and floral evolution. Bot Jahrb Syst 108:417–438

    Google Scholar 

  • Endress PK (1995) Major evolutionary traits of monocot flowers. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ (eds) Monocotyledons: systematics and evolution. Royal Botanic Gardens, Kew, pp 43–79

    Google Scholar 

  • Endress PK (1996) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge

    Google Scholar 

  • Erbar C, Leins P (1981) Zur Spirale in Magnolien-Bluten. Beitrage Zur Biol Pflanz

  • Erbar C, Leins P (1983) Zur Sequenz von Blütenorganen bei einigen Magnoliiden. Bot Jahrb Syst Pflanzengesch Pflanzengeogr 103:433–449

    Google Scholar 

  • Erbar C, Leins P (1994) Flowers in Magnoliidae and the origin of flowers in other subclasses of the angiosperms. I. The relationships between flowers of Magnoliidae and Alismatidae. In: Endress PK, Friis EM (eds) Early evolution of flowers. Springer, Vienna, pp 193–208

    Chapter  Google Scholar 

  • Graham SW, Zgurski JM, McPherson MA et al (2006) Robust inference of monocot deep phylogeny using an expanded multigene plastid data set. Aliso J Syst Evol Bot 22:3–21

    Google Scholar 

  • Hertweck KL, Kinney MS, Stuart SA et al (2015) Phylogenetics, divergence times and diversification from three genomic partitions in monocots. Bot J Linn Soc 178:375–393

    Article  Google Scholar 

  • Iles WJ, Smith SY, Graham SW (2013) A well-supported phylogenetic framework for the monocot order Alismatales reveals multiple losses of the plastid NADH dehydrogenase complex and a strong long-branch effect. In: Wilkin P, Mayo SJ (eds) Early events in monocot evolution. Cambridge University Press, Cambridge, pp 1–28

    Google Scholar 

  • Kaul RB (1967a) Development and vasculature of the flowers of Lophotocarpus calycinus and Sagittaria latifolia (Alismaceae). Am J Bot 54:914–920

    Article  Google Scholar 

  • Kaul RB (1967b) Ontogeny and anatomy of the flower of Limnocharis flava (Butomaceae). Am J Bot 54:1223–1230

    Article  Google Scholar 

  • Kaul RB (1968a) Floral development and vasculature in Hydroceleis nymphoides (Butomaceae). Am J Bot 55:236–242

    Article  Google Scholar 

  • Kaul RB (1968b) Floral morphology and phylogeny in the Hydrocharitaceae. Phytomorphology 18:13–35

    Google Scholar 

  • Kaul RB (1969) Morphology and development of the flowers of Boottia cordata, Ottelia alismoides, and their synthetic hybrid (Hydrocharitaceae). Am J Bot 951–959

  • Leins P, Erbar C (1994) Flowers in Magnoliidae and the origin of flowers in other subclasses of the angiosperms. II. The relationships between flowers of Magnoliidae, Dilleniidae, and Caryophyllidae. In: Endress PK, Friis EM (eds) Early evolution of flowers. Springer, Wien, pp 209–218

    Chapter  Google Scholar 

  • Leins P, Stadler P (1973) Entwicklungsgeschichtliche Untersuchungen am Androeceum der Alismatales. Österr Bot Z 121:51–63

    Article  Google Scholar 

  • Liu K, Lei I, Hu G (2002) Developmental study on the inflorescence and flower of Caldesia grandis Samuel (Alismataceae). Bot J Linn Soc 140:39–47

    Article  Google Scholar 

  • Nunes ELP, de Lima MC, Moço MCC, Coan AI (2012) Floral development in Potamogeton (Potamogetonaceae, Alismatales) with emphasis on gynoecial features. Aquat Bot 100:56–61

    Article  Google Scholar 

  • Petersen G, Seberg O, Cuenca A, Stevenson DW, Thadeo M, Davis JI, Graham S, Ross TG (2016) Phylogeny of the Alismatales (Monocotyledons) and the relationship of Acorus (Acorales?) Cladistics 32:141–159

    Article  Google Scholar 

  • Posluszny U (1983) Reevaluation of certain key relationships in the Alismatidae: floral organogenesis of Scheuchzeria palustris (Scheuchzeriaceae). Am J Bot 70:925–933

    Article  Google Scholar 

  • Posluszny U, Charlton WA (1993) Evolution of the Helobial flower. Aquat Bot 44:303–324

    Article  Google Scholar 

  • Remizowa M, Sokoloff DD (2003) Inflorescence and floral morphology in Tofieldia (Tofieldiaceae) compared with Araceae, Acoraceae and Alismatales s.str. Bot Jahrb Syst 124:255–271

    Article  Google Scholar 

  • Remizowa MV, Sokoloff DD, Kondo K (2010) Early flower and inflorescence development in Dioscorea tokoro (Dioscoreales): shoot chirality, handedness of cincinni and common tepal–stamen primordia. Wulfenia 17:77–97

    Google Scholar 

  • Remizowa MV, Kuznetsov AN, Kuznetsova SP, Rudall PJ, Nuraliev MS, Sokoloff DD (2012) Flower development and vasculature in Xyris grandis (Xyridaceae, Poales); a case study for examining petal diversity in monocot flowers with a double perianth. Bot J Linn Soc 170:93–111

    Article  Google Scholar 

  • Richards JH, Barrett SCH (1984) The developmental basis of tristyly in Eichhornia paniculata (Pontederiaceae). Am J Bot 71:1347–1363

    Article  Google Scholar 

  • Ronse De Craene LP (2003) The evolutionary significance of homeosis in flowers: a morphological perspective. Int J Plant Sci 164:225–235

    Article  Google Scholar 

  • Ronse De Craene LP (2010) Floral diagrams: an aid to understanding flower morphology and evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Ronse De Craene LP (2018) Understanding the role of floral development in the evolution of angiosperm flowers: clarifications from a historical and physico-dynamic perspective. J Plant Res. https://doi.org/10.1007/s10265-018-1021-1

    Article  Google Scholar 

  • Ronse De Craene LP, Smets EF (1993) Dédoublement revisited: towards a renewed interpretation of the androecium of the Magnoliophytina. Bot J Linn Soc 113:103–124

    Article  Google Scholar 

  • Ronse De Craene LP, Smets E (1994) Merosity in flowers: definition, origin, and taxonomic significance. Plant Syst Evol 191:83–104

    Article  Google Scholar 

  • Ronse De Craene LP, Smets EF (1995) The androecium of monocotyledons. Monocotyledons Syst Evol 1:243–254

    Google Scholar 

  • Ronse De Craene LP, Smets E (1996) The morphological variation and systematic value of stamen pairs in the Magnoliatae. Feddes Repert 107:1–17

    Google Scholar 

  • Ross TG, Barrett CF, Gomez MS, Lam VKY, Henriquez CL, Les DH, Davis JI, Cuenca A, Petersen G, Seberg O, Thadeo M, Givnish TJ, Conran J, Stevenson DW, Graham SW (2016) Plastid phylogenomics and molecular evolution of Alismatales. Cladistics 32:160–178

    Article  Google Scholar 

  • Salisbury EJ (1926) The geographical distribution of plants in relation to climatic factors. Geogr J 67:312–335

    Article  Google Scholar 

  • Sattler R, Singh V (1973) Floral development of Hydrocleis nymphoides. Can J Bot 51:2455–2458

    Article  Google Scholar 

  • Sattler R, Singh V (1977) Floral organogenesis of Limnocharis flava. Can J Bot 55:1076–1086

    Article  Google Scholar 

  • Sattler R, Singh V (1978) Floral organogenesis of Echinodorus amazonicus Rataj and floral construction of the Alismatales. Bot J Linn Soc 77:141–156

    Article  Google Scholar 

  • Sauquet H, von Balthazar M, Magallón S, Doyle JA, Endress PK et al (2017) The ancestral flower of angiosperms and its early diversification. Nat Commun 8:16047. https://doi.org/10.1038/ncomms16047

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Scribailo RW, Posluszny U (1985) Floral development of Hydrocharis morsus-ranae (Hydrocharitaceae). Am J Bot 72:1578–1589

    Article  Google Scholar 

  • Singh V, Sattler R (1972) Floral development of Alisma triviale. Can J Bot 50:619–627

    Article  Google Scholar 

  • Singh V, Sattler R (1973) Nonspiral androecium and gynoecium of Sagittaria latifolia. Can J Bot 51:1093–1095

    Article  Google Scholar 

  • Singh V, Sattler R (1974) Floral development of Butomus umbellatus. Can J Bot 52:223–230

    Article  Google Scholar 

  • Singh V, Sattler R (1977) Development of the inflorescence and flower of Sagittaria cuneata. Can J Bot 55:1087–1105

    Article  Google Scholar 

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Acknowledgements

This work was partly supported by JSPS KAKENHI Grant number 16K18576 to AI. The authors thank Dr. Paula Rudall, Royal Botanic gardens, Kew, Mr. Ueda, Mizunomori Water Botanical Garden, and the Royal Botanic Garden Edinburgh for support in collecting materials. Thanks of the authors also go to Robbie Lewis, MSc, from Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

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  1. Department of Biology, Tokyo Gakugei University, 4-1-1 Nukui Kita-machi, Koganei-shi, Tokyo, 184-8501, Japan

    Akitoshi Iwamoto, Ayaka Nakamura, Shinichi Kurihara & Ayumi Otani

  2. Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK

    Louis P. Ronse De Craene

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  1. Akitoshi Iwamoto
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  2. Ayaka Nakamura
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  3. Shinichi Kurihara
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  4. Ayumi Otani
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  5. Louis P. Ronse De Craene
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Correspondence to Akitoshi Iwamoto.

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Iwamoto, A., Nakamura, A., Kurihara, S. et al. Floral development of petaloid Alismatales as an insight into the origin of the trimerous Bauplan in monocot flowers. J Plant Res 131, 395–407 (2018). https://doi.org/10.1007/s10265-018-1022-0

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Keywords

  • Petaloid Alismatales
  • Floral development
  • Stamen pairs
  • Monocot flower
  • Trimerous Bauplan