, Volume 228, Issue 1, pp 27–36 | Cite as

Temperature-dependent changes of cell shape during heterophyllous leaf formation in Ludwigia arcuata (Onagraceae)

  • Masashi Sato
  • Maki Tsutsumi
  • Akane Ohtsubo
  • Kanae Nishii
  • Asuka Kuwabara
  • Toshiyuki Nagata
Original Article


Although elongation of epidermal cells in submerged leaves is thought to be a common feature of heterophyllous aquatic plants, such elongation has not been observed in Ludwigia arcuata Walt. (Onagraceae). In this study we found that reduced culture temperature induced the elongation of epidermal cells of submerged leaves in L. arcuata. Since such submerged leaves also showed a reduction in the number of epidermal cells aligned across the leaf transverse axis, these data indicate that heterophyllous leaf formation in L. arcuata is partially temperature sensitive, i.e., the elongation of epidermal cells was temperature sensitive while the reduction in the number of epidermal cells did not show such temperature sensitivity. To clarify the mechanisms that cause such temperature sensitivity, we examined the effects of ethylene, which induced the formation of submerged-type leaves on aerial shoots at the relatively high culture-temperature of 28°C. At 23°C, ethylene induced both cell elongation and reduction in the number of epidermal cells across the leaf transverse axis, while cell elongation was not observed at 28°C. Moreover, both submergence and ethylene treatment induced a change in the arrangement of cortical microtubules (MTs) in epidermal cells of developing leaves at 23°C. Such changes in the arrangement of MTs was not induced at 28°C. Factors involved in the temperature-sensitive response to ethylene would be critical for temperature-sensitive heterophyllous leaf formation in L. arcuata.


Cell elongation Heterophylly Leaf shape Ludwigia Submergence Temperature sensitivity 



Analysis of variance





We thank Professor Andrew Fleming (University of Sheffield, UK) for his critical reading of this manuscript and helpful comments. Thanks are also due to Dr. Arata Yoneda (The University of Tokyo, Japan) for his technical support. This study was partly supported by the Wada Kunkokai Foundation, Japan.


  1. Akashi T, Izumi K, Nagano E, Enomoto M, Mizuno K, Shibaoka H (1988) Effects of propyzamide on tobacco cell microtubules in vivo and in vitro. Plant Cell Physiol 29:1053–1062Google Scholar
  2. Anderson LWJ (1978) Abscisic acid induces formation of floating leaves in the heterophyllous aquatic angiosperm Potamogeton nodosus. Science 201:1135–1138PubMedCrossRefGoogle Scholar
  3. Bruni NC, Young JP, Dengler NG (1996) Leaf developmental plasticity of Ranunculus flabellaris in response to terrestrial and submerged environments. Can J Bot 74:823–837CrossRefGoogle Scholar
  4. Cleary AL, Smith LG (1998) The tangled1 gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10:1875–1888 PubMedCrossRefGoogle Scholar
  5. Deschamp PA, Cooke TJ (1983) Leaf dimorphism in aquatic angiosperms: significance of turgor pressure and cell expansion. Science 219:505–507PubMedCrossRefGoogle Scholar
  6. Giddings TH, Staehelin LA (1988) Spatial relationship between microtubules and plasma-membrane rosettes during the deposition of primary wall microfibrils in Closterium sp. Planta 173:22–30CrossRefGoogle Scholar
  7. Goliber TE, Feldman LJ (1990) Developmental analysis of leaf plasticity in the heterophyllous aquatic plant Hippuris vulgaris. Am J Bot 77:399–412CrossRefGoogle Scholar
  8. Johnson MP (1967) Temperature dependent leaf morphogenesis in Ranunculus flabellaris. Nature 214:1354–1355CrossRefGoogle Scholar
  9. Kane ME, Albert LS (1982) Environmental and growth regulator effects on heterophylly and growth of Proserpinaca intermedia. Aquat Bot 13:73–85CrossRefGoogle Scholar
  10. Kuwabara A, Nagata T (2002) Views on developmental plasticity of plants through heterophylly. Recent Res Dev Plant Physiol 3:45–59Google Scholar
  11. Kuwabara A, Nagata T (2006) Cellular basis of developmental plasticity observed in heterophyllous leaf formation of Ludwigia arcuata (Onagraceae). Planta 224:761–770PubMedCrossRefGoogle Scholar
  12. Kuwabara A, Tsukaya H, Nagata T (2001) Identification of factors that cause heterophylly in Ludwigia arcuata Walt. (Onagraceae). Plant Biol 3:98–105CrossRefGoogle Scholar
  13. Kuwabara A, Ikegami K, Koshiba T, Nagata T (2003) Effects of ethylene and abscisic acid upon heterophylly in Ludwigia arcuata Walt. (Onagraceae). Planta 217:880–887PubMedCrossRefGoogle Scholar
  14. Lin BL, Wang HJ, Wang JS, Zaharia LI, Abrams SR (2005) Abscisic acid regulation of heterophylly in Marsilea quadrifolia L.: effects of R-(−) and S-(+) isomers. J Exp Bot 56:2935–2948PubMedCrossRefGoogle Scholar
  15. McCully ME, Dale HM (1961) Heterophylly in Hippuris, a problem in identification. Can J Bot 39:1099–1116Google Scholar
  16. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  17. Raskin I, Kende H (1984) Role of gibberellin in the growth response of submerged deepwater rice. Plant Physiol 76:947–950 PubMedCrossRefGoogle Scholar
  18. Wallenstein A, Albert LS (1963) Plant morphology: its control in Proserpinaca by photoperiod, temperature, and gibberellic acid. Science 140:998–1000PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Masashi Sato
    • 1
    • 2
  • Maki Tsutsumi
    • 1
  • Akane Ohtsubo
    • 1
  • Kanae Nishii
    • 1
    • 3
  • Asuka Kuwabara
    • 1
    • 4
  • Toshiyuki Nagata
    • 1
    • 5
  1. 1.Department of Biological SciencesGraduate School of Science, The University of TokyoTokyoJapan
  2. 2.Takii Plant Breeding and Experiment StationKonanJapan
  3. 3.Department of Life ScienceNational Taiwan UniversityTaipeiTaiwan, ROC
  4. 4.Department of Animal and Plant ScienceThe University of SheffieldSheffieldUK
  5. 5.IT Research Centre, Hosei UniversityTokyoJapan

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