Advertisement

Protoplasma

, Volume 250, Issue 1, pp 407–414 | Cite as

Inducible growth mode switches influence Valonia rhizoid differentiation

  • Paul Rommel ElviraEmail author
  • Satoko Sekida
  • Kazuo Okuda
Short Communication

Abstract

Cell differentiation and cell type commitment are an integral part of plant growth and development. Investigations on how environmental conditions affect the formation of shoots, roots, and rhizoids can help illustrate how plants determine cell fate and overall morphology. In this study, we evaluated the role of substratum and light on rhizoid differentiation in the coenocytic green alga, Valonia aegagropila. Elongating rhizoids displayed varying growth modes and cell shape upon exposure to different substrata and light conditions. It was found that soft substrata and dark incubation promoted rhizoid elongation via tip growth while subsequent exposure to light prevented tip growth and instead induced swelling in the apical region of rhizoids. Swelling was accompanied by the accumulation of protoplasm in the rhizoid tip through expansion of the cell wall and uninhibited cytoplasmic streaming. Subsequent diffuse growth led to the transformation from slender, rod-shaped rhizoids into spherical thallus-like structures that required photosynthesis. Further manipulation of light regimes caused vacillating cell growth redirections. An elongating V. aegagropila rhizoid cell thus appears capable of growth mode switching that is regulated by immediate environmental conditions thereby influencing ultimate cell shape and function. This is the first description of inducible, multiple growth mode shifts in a single intact plant cell that directly impact its differentiation.

Keywords

Cytoplasmic streaming Growth mode Light Rhizoid Thallus Valonia aegagropila 

Notes

Acknowledgments

We thank Dr. Ichiro Mine of Kochi University, Japan, for technical suggestions. This study was supported by the “Monbukagakusho,” Ministry of Education, Science, Sports, and Culture, Japanese Government, as part of doctoral research of P.R.E.

Conflicts of interest

The authors declare that they have no conflict of interest.

Supplementary material

Online resource 1

Formation of a bulb-tipped rhizoid from a rod-shaped V. aegagropila rhizoid and subsequent resumption of tip growth. A cell was incubated in darkness for 14 days at 22°C then exposed to 96 h continuous light at 40 μmol photons m−2 s−1 and then 24 h of continuous light at 10 μmol photons m−2 s−1. Photomicrographs were taken at 10-min intervals (MPG 2980 kb)

References

  1. Basu S, Sun H, Brian L, Quatrano RL, Muday GK (2002) Early embryo development in Fucus distichus is auxin sensitive. Plant Physiol 130:292–302PubMedCrossRefGoogle Scholar
  2. Berger F, Taylor A, Brownlee C (1994) Cell fate determination by the cell wall in early Fucus development. Science 263:1421–1423PubMedCrossRefGoogle Scholar
  3. Bold H, Wynne MJ (1985) Introduction to the algae. Prentice-Hall Inc, Englewood CliffsGoogle Scholar
  4. Bouget F, Berger F, Brownlee C (1998) Position dependent control of cell fate in the Fucus embryo: role of intercellular communication. Development 125:1999–2008PubMedGoogle Scholar
  5. Chihara M (1959) Studies on the life history of the green algae in the warm seas around Japan (9). Supplementary note on the life history of Valonia macrophysa Kutz. J Jpn Bot 34:257–268Google Scholar
  6. Cooke TJ, Poli DB, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338PubMedCrossRefGoogle Scholar
  7. Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol Biochem 38:109–124PubMedCrossRefGoogle Scholar
  8. Dazy AC, Puiseux-Dao S, Borghi H (1989) The effects of blue and red light on Acetabularia mediterranea after long exposure to darkness. Biol Cell 67:227–234Google Scholar
  9. Elvira PR, Sekida S, Okuda K (2012) Rhizoid formation in Valonia (Siphonocladales, Chlorophyceae). PhycologiaGoogle Scholar
  10. Flores HE, Dai Y, Cuello JL, Maldonado-Mendoza IE, Loyola-Vargas VM (1993) Green roots: photosynthesis and photoautotrophy in an underground plant organ. Plant Physiol 101:363–371PubMedGoogle Scholar
  11. Fritsch FE (1935) The structure and reproduction of the alga. Cambridge Univ Press, LondonGoogle Scholar
  12. Grafi G, Chalifa-Caspi V, Nagar T, Plaschkes I, Barak S, Ransbotyn V (2011) Plant response to stress meets dedifferentiation. Planta 233:433–438PubMedCrossRefGoogle Scholar
  13. Gull K, Trinci APJ (1974) Detection of areas of wall differentiation in fungi using fluorescent staining. Arch Microbiol 96:53–57CrossRefGoogle Scholar
  14. Harold FM (2002) Force and compliance: rethinking morphogenesis in walled cells. Fungal Gen Biol 37:271–282CrossRefGoogle Scholar
  15. Hughes J, McCully ME (1975) The use of an optical brightener in the study of plant structure. Stain Technol 50:319–329PubMedGoogle Scholar
  16. Inoue N, Yamada S, Nagata Y, Shimmen T (2002) Rhizoid differentiation in Spirogyra: position sensing by terminal cells. Plant Cell Physiol 43:479–483PubMedCrossRefGoogle Scholar
  17. Jacobs WP (1951) Studies on cell differentiation: the role of auxin in algae, with particular reference to rhizoid-formation in Bryopsis. Biol Bull 101:300–306CrossRefGoogle Scholar
  18. Jacobs WP, Falkenstein K, Hamilton RH (1985) Nature and amount of auxin in algae. IAA from extracts of Caulerpa paspaloides (Siphonales). Plant Physiol 78:844–848PubMedCrossRefGoogle Scholar
  19. Jang G, Yi K, Pires ND, Menand B, Dolan L (2011) RSL genes are sufficient for rhizoid system development in early diverging land plants. Development 138(11):2273–2281PubMedCrossRefGoogle Scholar
  20. Johri MM (2008) Hormonal regulation in green plant lineage families. Physiol Mol Biol Plants 14(1–2):23–38CrossRefGoogle Scholar
  21. Kamiya N (1986) Cytoplasmic streaming in giant algal cells: a historical survey of experimental approaches. Bot Mag Tokyo 99:441–467CrossRefGoogle Scholar
  22. Kanda T (1940) Studies on the genus Valonia from Palao. Kagaku Nanyo 3:23–32Google Scholar
  23. Kawai H, Motomura T, Okuda K (2005) Isolation and purification techniques for macroalgae. In: Andersen A (ed) Algal culture techniques. Elsevier, Amsterdam, pp 133–143Google Scholar
  24. Klambt D, Knauth B, Dittmann I (1992) Auxin dependent growth of rhizoids of Chara globularis. Physiol Planta 85:537–540CrossRefGoogle Scholar
  25. Kropf DL, Bisgrove SR, Hable WE (1998) Cytoskeletal control of polar growth in plant cells. Curr Opin Plant Biol 10:117–122CrossRefGoogle Scholar
  26. Maclean N, Hall BK (1987) Cell commitment and differentiation. Cambridge University Press, LondonGoogle Scholar
  27. Martin C, Bhatt K, Baumann K (2001) Shaping in plant cells. Curr Opin Plant Biol 4:540–549PubMedCrossRefGoogle Scholar
  28. Mathur J (2006) Local interactions shape plant cells. Curr Opin Cell Biol 18:40–46PubMedCrossRefGoogle Scholar
  29. Metz JG, Pakrasi HB, Seibert M, Arntzen CJ (1986) Evidence for a dual function of the herbicide-binding D1 protein in photosystem II. FEBS 205:269–274CrossRefGoogle Scholar
  30. Mine I, Menzel D, Okuda K (2008) Morphogenesis in giant-celled algae. Intl Rev Cell Mol Biol 266:37–83CrossRefGoogle Scholar
  31. Okuda K, Ueno S, Mine I (1997) Cytomorphogenesis in coenocytic green algae. IV. The construction of cortical microtubules during lenticular cell formation in Valonia utricularis. Mem Fac Sci Kochi Univ Ser D 18:17–25Google Scholar
  32. Olsen JL, West JA (1988) Ventricaria (Siphonocladales-Cladophorales complex, Chlorophyta), a new genus for Valonia ventricosa. Phycologia 27:103–108CrossRefGoogle Scholar
  33. Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Proceedings of the US-Japan Conference, Hakone, September 1966. Japanese Society of Plant Physiologists, Japan, pp 63–75Google Scholar
  34. Saavedra L, Balbi V, Lerche J, Mikami K, Heilmann I, Sommarin M (2011) PIPKs are essential for rhizoid elongation and caulonemal cell development in the moss Physcomitrella patens. Plant J 67:635–647PubMedCrossRefGoogle Scholar
  35. Sakakibara K, Nishiyama T, Sumikawa N, Kofuji R, Murata T, Hasebe M (2003) Involvement of auxin and a homeodomain-leucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development 130:4835–4846PubMedCrossRefGoogle Scholar
  36. Smith LG, Oppenheimer DG (2005) Spatial control of cell expansion by the plant cytoskeleton. Ann Rev Cell Dev Biol 21:271–295CrossRefGoogle Scholar
  37. Steer MW, Steer JM (1989) Pollen tube growth. New Phytol 111:323–358CrossRefGoogle Scholar
  38. Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471PubMedCrossRefGoogle Scholar
  39. Sugimoto K, Gordon SP, Meyerowitz EM (2011) Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol 21:212–218PubMedCrossRefGoogle Scholar
  40. Waaland SD, Watson BA (1980) Isolation of a cell-fusion hormone from Griffithsia pacifica Kylin, a red alga. Planta 149:493–497CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Paul Rommel Elvira
    • 1
    Email author
  • Satoko Sekida
    • 1
  • Kazuo Okuda
    • 1
  1. 1.Cell Biology Laboratory, Graduate School of Kuroshio ScienceKochi UniversityKochiJapan

Personalised recommendations