Plant Cell Reports

, Volume 36, Issue 8, pp 1225–1236 | Cite as

Water-Wisteria as an ideal plant to study heterophylly in higher aquatic plants

  • Gaojie Li
  • Shiqi Hu
  • Jingjing Yang
  • Elizabeth A. Schultz
  • Kurtis Clarke
  • Hongwei HouEmail author
Original Article


Key message

The semi-aquatic plant Water-Wisteria is suggested as a new model to study heterophylly due to its many advantages and typical leaf phenotypic plasticity in response to environmental factors and phytohormones.


Water-Wisteria, Hygrophila difformis (Acanthaceae), is a fast growing semi-aquatic plant that exhibits a variety of leaf shapes, from simple leaves to highly branched compound leaves, depending on the environment. The phenomenon by which leaves change their morphology in response to environmental conditions is called heterophylly. In order to investigate the characteristics of heterophylly, we assessed the morphology and anatomy of Hygrophila difformis in different conditions. Subsequently, we verified that phytohormones and environmental factors can induce heterophylly and found that Hygrophila difformis is easily propagated vegetatively through either leaf cuttings or callus induction, and the callus can be easily transformed by Agrobacterium tumefaciens. These results suggested that Hygrophila difformis is a good model plant to study heterophylly in higher aquatic plants.


Hygrophila difformis Aquatic plant Heterophylly Leaf Model plant Phytohormone 



We thank Dr. Seisuke Kimura from Kyoto Sangyo University for his generous help on H. difformis genome survey. We also offer our thanks to Dr. Lei Chen from the South China Botanical Garden, the Chinese Academy of Sciences for his helpful discussions. This work was supported by grants to Prof. Hongwei Hou from the Project of the State Key Laboratory of Freshwater Ecology and Biotechnology (2016FB04) and the project of the Natural Science Foundation of Hubei Province (2015CFB488).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

299_2017_2148_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)


  1. Amano R, Nakayama H, Morohoshi Y, Kawakatsu Y, Ferjani A, Kimura S (2015) A decrease in ambient temperature induces post-mitotic enlargement of palisade cells in North American lake cress. PLoS One 10:340–351Google Scholar
  2. Anderson LW (1978) Abscisic acid induces formation of floating leaves in the heterophyllous aquatic angiosperm Potamogeton nodosus. Science 201:1135–1138CrossRefPubMedGoogle Scholar
  3. Bodkin PC, Spence DHN, Weeks DC (1980) Photoreversible control of heterophylly in Hippuris vulgaris. New Phytol 84:533–542CrossRefGoogle Scholar
  4. Cook CDK (1969) On the determination of leaf form in Ranunculus aquatilis. New Phytol 68:469–480CrossRefGoogle Scholar
  5. Deschamp PA, Cooke TJ (1984) Causal mechanisms of leaf dimorphism in the aquatic angiosperm Callitriche heterophylla. Am J Bot 71:319–329CrossRefGoogle Scholar
  6. Deschamp PA, Cooke TJ (1985) Leaf dimorphism in the aquatic angiosperm Callitriche heterophylla. Am J Bot 72:1377–1387CrossRefGoogle Scholar
  7. Gaudet JJ (1963) Marsilea vestita: conversion of the water form to the land form by darkness and by far-red light. Science 140:975–976CrossRefPubMedGoogle Scholar
  8. Goliber TE, Feldman LJ (1989) Osmotic stress, endogenous abscisic acid and the control of leaf morphology in Hippuris vulgaris. Plant Cell Environ 12:163–171CrossRefPubMedGoogle Scholar
  9. Hay A, Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38:942–947CrossRefPubMedGoogle Scholar
  10. Jackson MB (2008) Ethylene-promoted elongation: an adaptation to submergence stress. Ann Bot 101:229–248CrossRefPubMedGoogle Scholar
  11. Jo IS, Dong UH, Yong JC, Lee EJ (2010) Effects of light, temperature, and water depth on growth of a rare aquatic plant, Ranunculus kadzusensis. J Plant Biol 53:88–93CrossRefGoogle Scholar
  12. Johnson MP (1967) Temperature dependent leaf morphogenesis in Ranunculus flabellaris. Nature 214:1354–1355CrossRefGoogle Scholar
  13. Kane ME, Albert LS (1989) Abscisic-acid induction of aerial leaf development in Myriophyllum and Proserpinaca species cultured in vitro. J Aquat Plant Manage 27:102–111Google Scholar
  14. Keener CS, Gifford EM, Foster AS (1990) Morphology and evolution of vascular plants. Syst Bot 15:348CrossRefGoogle Scholar
  15. Kimura S, Koenig D, Kang J, Fei YY, Sinha N (2008) Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr Biol 18:672–677CrossRefPubMedGoogle Scholar
  16. Kuwabara A, Tsukaya H, Nagata T (2001) Identification of factors that cause heterophylly in Ludwigia arcuata Walt. (Onagraceae). Plant Biol 3:98–105CrossRefGoogle Scholar
  17. Kuwabara A, Ikegami K, Koshiba T, Nagata T (2003) Effects of ethylene and abscisic acid upon heterophylly in Ludwigia arcuata (Onagraceae). Planta 217:880–887CrossRefPubMedGoogle Scholar
  18. Lin BL, Abrams SR (2005) Abscisic acid regulation of heterophylly in marsilea quadrifolia: effects of r-(−) and s-(+) isomers. J Exp Bot 56:2935–2948CrossRefPubMedGoogle Scholar
  19. Lin BL, Yang WJ (1999) Blue light and abscisic acid independently induce heterophyllous switch in Marsilea quadrifolia. Plant Physiol 119:429–434CrossRefPubMedPubMedCentralGoogle Scholar
  20. McCully ME, Dale HM (1961) Heterophylly in Hippuris, a problem in identification. Can J Bot 39:1099–1116CrossRefGoogle Scholar
  21. Müller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094–1097CrossRefPubMedPubMedCentralGoogle Scholar
  22. Nakayama H, Nakayama N, Nakamasu A, Sinha N, Kimura S (2012) Toward elucidating the mechanisms that regulate heterophylly. Plant Morphol 24:57–63CrossRefGoogle Scholar
  23. Nakayama H, Nakayama N, Seiki S, Kojima M, Sakakibara H, Sinha N, Kimura S (2014) Regulation of the KNOX-GA gene module induces heterophyllic alteration in North American lake cress. Plant Cell 26:4733–4748CrossRefPubMedPubMedCentralGoogle Scholar
  24. Pal D, Samanta K (2011) CNS activities of ethanol extract of aerial parts of Hygrophila difformis in mice. Acta Pol Pharm 68:75–81PubMedGoogle Scholar
  25. Rascio N, Cuccato F, Vecchia FD, Rocca NL, Larcher W (1999) Structural and functional features of the leaves of Ranunculus trichophyllus, Chaix., a freshwater submerged macrophophyte. Plant Cell Environ 22:205–212CrossRefGoogle Scholar
  26. Sato M, Tsutsumi M, Ohtsubo A, Nishii K, Kuwabara A, Nagata T (2008) Temperature-dependent changes of cell shape during heterophyllous leaf formation in Ludwigia arcuata (onagraceae). Planta 228:27–36CrossRefPubMedGoogle Scholar
  27. Schiller P, Heilmeier H, Hartung W (1997) Abscisic acid (ABA) relations in the aquatic resurrection plant Chamaegigas intrepidus under naturally fluctuating environmental conditions. New Phytol 136:603–611CrossRefGoogle Scholar
  28. Schmidt BL, Millington WF (1968) Regulation of leaf shape in Proserpinaca palustris. Bull Torrey Bot Club 95:264–286CrossRefGoogle Scholar
  29. Sculthorpe CD (1967) The biology of aquatic vascular plants. Edward Arnold, LondonGoogle Scholar
  30. Shani E, Yanai O, Ori N (2006) The role of hormones in shoot apical meristem function. Curr Opin Plant Biol 9:484–489CrossRefPubMedGoogle Scholar
  31. Titus JE, Sullivan PG (2001) Heterophylly in the yellow waterlily, nuphar variegata (Nymphaeaceae): effects of [CO2], natural sediment type, and water depth. Am J Bot 88:1469CrossRefPubMedGoogle Scholar
  32. Wanke D (2011) The ABA-mediated switch between submersed and emersed life-styles in aquatic macrophytes. J Plant Res 124:467–475CrossRefPubMedGoogle Scholar
  33. Wissler L, Codoñer FM, Gu J, Reusch TB, Olsen JL, Procaccini G, Bornberg BE (2011) Back to the sea twice: identifying candidate plant genes for molecular evolution to marine life. BMC Evol Biol 11:76–92CrossRefGoogle Scholar
  34. Zotz G, Wilhelm K, Becker A (2011) Heteroblasty—a review. Bot Rev 77:109–151CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Gaojie Li
    • 1
  • Shiqi Hu
    • 1
  • Jingjing Yang
    • 1
  • Elizabeth A. Schultz
    • 2
  • Kurtis Clarke
    • 2
  • Hongwei Hou
    • 1
    Email author
  1. 1.The State Key Laboratory of Freshwater Ecology and Biotechnology, The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of HydrobiologyChinese Academy of Sciences, University of Chinese Academy of SciencesWuhanPeople’s Republic of China
  2. 2.Department of Biological SciencesUniversity of LethbridgeLethbridgeCanada

Personalised recommendations