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Journal of Plant Research

, Volume 131, Issue 1, pp 165–178 | Cite as

Circumnutation and distribution of phytohormones in Vigna angularis epicotyls

  • Motoyuki Iida
  • Toshihiko Takano
  • Takakazu Matsuura
  • Izumi C. Mori
  • Shingo Takagi
Regular Paper
  • 241 Downloads

Abstract

Circumnutation is a plant growth movement in which the tips of axial organs draw a circular orbit. Although it has been studied since the nineteenth century, its mechanism and significance are still unclear. Greened adzuki bean (Vigna angularis) epicotyls exhibited a clockwise circumnutation in the top view with a constant period of 60 min under continuous white light. The bending zone of circumnutation on the epicotyls was always located in the region 1–3 cm below the tip, and its basal end was almost identical to the apical end of the region where the epicotyl had completely elongated. Therefore, epidermal cells that construct the bending zone are constantly turning over with their elongation growth. Since exogenously applied auxin transport inhibitors and indole-3-acetic acid (IAA) impaired circumnutation without any effect on the elongation rate of epicotyls, we attempted to identify the distribution pattern of endogenous auxin. Taking advantage of its large size, we separated the bending zone of epicotyls into two halves along the longitudinal axis, either convex/concave pairs in the plane of curvature of circumnutation or pre-convex/pre-concave pairs perpendicular to the plane. By liquid chromatography–mass spectrometry, we found, for the first time, that IAA and gibberellin A1 were asymmetrically distributed in the pre-convex part in the region 1–2 cm below the tip. This region of epicotyl sections exhibited the highest responsiveness to exogenously applied hormones, and the latent period between the hormone application and the detection of a significant enhancement in elongation was 15 min. Our results suggest that circumnutation in adzuki bean epicotyls with a 60 min period is maintained by differential growth in the bending zone, which reflects the hormonal status 15 min before and which is shifting sequentially in a circumferential direction. Cortical microtubules do not seem to be involved in this regulation.

Keywords

Adzuki bean Auxin Circumnutation Gibberellin LC–MS. 

Notes

Acknowledgements

This work was partly supported by Grant-in-Aid for Scientific Research No. 26440143 from the Japan Society for the Promotion of Science, and by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) as part of Joint Research Program implemented at the Institute of Plant Science and Resources, Okayama University in Japan.

Supplementary material

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Supplementary material 1 (MPG 1668 KB)
10265_2017_972_MOESM2_ESM.pdf (13.8 mb)
Supplementary material 2 (PDF 14160 KB)

References

  1. Badescu GO, Napier RM (2006) Receptors for auxin: will it all end in TIRs? Trends Plant Sci 11:217–223CrossRefPubMedGoogle Scholar
  2. Badot P-M, Melin D, Garrec J-P (1990) Circumnutation in Phaseolus vulgaris. II. Potassium content in the free moving part of the shoot. Plant Physiol Biochem 28:123–130Google Scholar
  3. Barkley GM, Evans ML (1970) Timing of the auxin response in etiolated pea stem sections. Plant Physiol 45:143–147CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baskin TI (2007) Ultradian growth oscillations in organs: physiological signal or noise? In: Mancuso S, Shabala S (eds) Rhythms in plants: phenomenology, mechanisms and adaptative significance. Springer, Berlin, pp 63–76CrossRefGoogle Scholar
  5. Britz SJ, Galston AW (1982a) Physiology of movements in stems of seedling Pisum sativum L. cv. Alaska. I. Experimental separation of nutation from gravitropism. Plant Physiol 70:264–271CrossRefPubMedPubMedCentralGoogle Scholar
  6. Britz SJ, Galston AW (1982b) Physiology of movements in stems of seedling Pisum sativum L. cv. Alaska. II. The role of the apical hook and of auxin in nutation. Plant Physiol 70:1401–1404CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brown AH (1993) Circumnutations: from Darwin to space flights. Plant Physiol 101:345–348CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brown AH, Chapman DK (1984) Circumnutation observed without a significant gravitational force in spaceflight. Science 225:230–232CrossRefPubMedGoogle Scholar
  9. Caré AF, Nefed’ev L, Bonnet B, Millet B, Badot P-M (1998) Cell elongation and revolving movement in Phaseolus vulgaris L. twining shoots. Plant Cell Physiol 39:914–912CrossRefGoogle Scholar
  10. Chapman DK, Brown AH (1979) Residual nutational activity of the sunflower hypocotyl in simulated weightlessness. Plant Cell Physiol 20:473–478CrossRefGoogle Scholar
  11. Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285CrossRefPubMedGoogle Scholar
  12. Comparot S, Morillon R, Badot P-M (2000) Water permeability and revolving movement in Phaseolus vulgaris L. twining shoots. Plant Cell Physiol 41:114–118CrossRefPubMedGoogle Scholar
  13. Darwin C, Darwin F (1880) The power of movements in plants. John Murray, LondonCrossRefGoogle Scholar
  14. Ding Z, Galván-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R, Friml J (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 13:447–452CrossRefPubMedGoogle Scholar
  15. Evans ML (1974) Rapid responses to plant hormones. Annu Rev Plant Physiol 25:195–223CrossRefGoogle Scholar
  16. Fischer K, Schopfer P (1997) Interaction of auxin, light, and mechanical stress in orienting microtubules in relation to tropic curvature in the epidermis of maize coleoptiles. Protoplasma 196:108–116CrossRefGoogle Scholar
  17. Friml J, Wisniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809CrossRefPubMedGoogle Scholar
  18. Fukaki H, Wysocka-Diller J, Kato T, Fujisawa H, Benfey PN, Tasaka M (1998) Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J 14:425–430CrossRefPubMedGoogle Scholar
  19. Haga K, Iino M (2006) Asymmetric distribution of auxin correlated with gravitropism and phototropism but not with autostraightening (autotropism) in pea epicotyls. J Exp Bot 57:837–847CrossRefPubMedGoogle Scholar
  20. Haga K, Takano M, Neumann R, Iino M (2005) The rice COLEOPTILE PHOTOTROPISM1 gene encoding an ortholog of Arabidopsis NPH3 is required for phototropism of coleoptiles and lateral translocation of auxin. Plant Cell 17:103–115CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483–505CrossRefPubMedGoogle Scholar
  22. Hatakeda Y, Kamada Y, Goto N, Fukaki H, Tasaka M, Suge H, Takahashi H (2003) Gravitropic response plays an important role in the nutational movements of the shoots of Pharbitis nil and Arabidopsis thaliana. Physiol Plant 118:464–473CrossRefGoogle Scholar
  23. Iino M (1991) Mediation of tropisms by lateral translocation of endogenous indole-3-acetic acid in maize coleoptiles. Plant Cell Environ 14:279–286CrossRefGoogle Scholar
  24. Israelsson D, Johnsson A (1967) A theory for circumnutations in Helianthus annuus. Physiol Plant 20:957–976CrossRefGoogle Scholar
  25. Kim HJ, Kobayashi A, Fujii N, Miyazawa Y, Takahashi H (2016) Gravitropic response and circumnutation in pea (Pisum sativum) seedling roots. Physiol Plant 157:108–118CrossRefPubMedGoogle Scholar
  26. Kitazawa D, Hatakeda Y, Kamada M, Fujii N, Miyazawa Y, Hoshino A, Iida S, Fukaki H, Terao-Morita M, Tasaka M, Suge H, Takahashi H (2005) Shoot circumnutation and winding movements require gravisensing cells. Proc Natl Acad Sci USA 102:18742–18747CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kosuge K, Iida S, Katou K, Mimura T (2013) Circumnutation on the water surface: female flowers of Vallisneria. Sci Rep 3:1133CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kutschera U, Niklas KJ (2007) The epidermal-growth-control theory of stem elongation: an old and a new perspective. J Plant Physiol 164:1395–1409CrossRefPubMedGoogle Scholar
  29. Landrein B, Hamant O (2013) How mechanical stress controls microtubules behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J 75:324–338CrossRefPubMedGoogle Scholar
  30. Li Y, Hagen G, Guilfoyle TJ (1991) An auxin-responsive promoter is differentially induced by auxin gradients during tropisms. Plant Cell 3:1167–1175CrossRefPubMedPubMedCentralGoogle Scholar
  31. Liscum E, Askinosie SK, Leuchtman DL, Morrow J, Willenburg KT, Coats DR (2014) Phototropism: growing towards an understanding of plant movement. Plant Cell 26:38–55CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 50:309–332CrossRefGoogle Scholar
  33. Lloyd C (2011) Dynamic microtubules and the texture of plant cell walls. Int Rev. Cell Mol Biol 287:287–329CrossRefPubMedGoogle Scholar
  34. Mayumi K, Shibaoka H (1996) The cyclic reorientation of cortical microtubules on walls with a crossed polylamellate structure: effects of plant hormones and an inhibitor of protein kinases on the progression of the cycle. Protoplasma 195:112–122CrossRefGoogle Scholar
  35. Michniewicz M, Brewer PB, Friml J (2007) Polar auxin transport and asymmetric auxin distribution. Arabidopsis Book 5:e0108PubMedPubMedCentralGoogle Scholar
  36. Millet B, Melin D, Bonnet B, Ibrahim CA, Mercier J (1984) Rhythmic circumnutation movement of the shoots in Phaseolus vulgaris L. Chronobiol Int 1:11–19CrossRefPubMedGoogle Scholar
  37. Millet B, Melin D, Badot P-M (1988) Circumnutation in Phaseolus vulgaris. I. Growth, osmotic potential and cell ultrastructure in the free-moving part of the shoot. Physiol Plant 72:133–138CrossRefGoogle Scholar
  38. Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720CrossRefPubMedGoogle Scholar
  39. Murphy AS, Hoogner KR, Peer WA, Taiz L (2002) Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol 128:935–950CrossRefPubMedPubMedCentralGoogle Scholar
  40. Niinuma K, Someya N, Kimura M, Yamaguchi I, Hamamoto H (2005) Circadian rhythm of circumnutation in inflorescence stems of Arabidopsis. Plant Cell Physiol 46:1423–1427CrossRefPubMedGoogle Scholar
  41. O’neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982CrossRefPubMedPubMedCentralGoogle Scholar
  42. Parker KE, Briggs WR (1990) Transport of indole-3-acetic acid during gravitropism in intact maize coleoptiles. Plant Physiol 94:1763–1769CrossRefPubMedPubMedCentralGoogle Scholar
  43. Rakusová H, Gallego-Bartolomé J, Vanstraelen M, Robert HS, Alabadí D, Blázquez MA, Benková E, Friml J (2011) Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J 67:817–826CrossRefPubMedGoogle Scholar
  44. Ross JJ, O’neill DP, Smith JJ, Kerckhoffs LHJ, Elliott RC (2000) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21:547–552CrossRefPubMedGoogle Scholar
  45. Sakiyama M, Shibaoka H (1990) Effects of abscisic acid on the orientation and cold stability of cortical microtubules in epicotyl cells of the dwarf pea. Protoplasma 157:165–171CrossRefGoogle Scholar
  46. Sakiyama-Sogo M, Shibaoka H (1993) Gibberellin A3 and abscisic acid cause the reorientation of cortical microtubules in epicotyl cells of the decapitated dwarf pea. Plant Cell Physiol 34:431–437Google Scholar
  47. Schuster J, Engelmann W (1997) Circumnutation of Arabidopsis thaliana seedlings. Biol Rhythm Res 28:422–440CrossRefGoogle Scholar
  48. Shibaoka H (1972) Gibberellin–olchicine interaction in elongation of azuki bean epicotyl sections. Plant Cell Physiol 13:461–469Google Scholar
  49. Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annu Rev Plant Physiol Plant Mol Biol 45:527–544CrossRefGoogle Scholar
  50. Smyth DR (2016) Helical growth in plant organs: mechanisms and significance. Development 143:3272–3282CrossRefPubMedGoogle Scholar
  51. Someya N, Niinuma K, Kimura M, Yamaguchi I, Hamamoto H (2006) Circumnutation of Arabidopsis thaliana inflorescence stems. Biol Plant 50:287–290CrossRefGoogle Scholar
  52. Stolarz M (2009) Circumnutation as a visible plant action and reaction. Plant Signal Behav 4:380–387CrossRefPubMedPubMedCentralGoogle Scholar
  53. Takahashi K, Hayashi K, Kinoshita T (2012) Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol 159:632–641CrossRefPubMedPubMedCentralGoogle Scholar
  54. Takesue K, Shibaoka H (1998) The cyclic reorientation of cortical microtubules in epidermal cells of azuki bean epicotyls: the role of actin filaments in the progression of the cycle. Planta 205:539–546CrossRefPubMedGoogle Scholar
  55. Tsukahara K, Sawada H, Kohno Y, Matsuura T, Izumi MC, Terao T, Ioki M, Tamaoki M (2015) Ozone-induced rice grain yield loss is triggered via a change in panicle morphology that is controlled by ABERRANT PANICLE ORGANIZATION 1 gene. PLoS One 10:e0123308CrossRefPubMedPubMedCentralGoogle Scholar
  56. Velasquez SM, Balbez E, Kleine-Vehn J, Estevez JM (2016) Auxin and cellular elongation. Plant Physiol 170:1206–1215PubMedPubMedCentralGoogle Scholar
  57. Went FW, Thimann KV (1937) Phytohormones. Macmillan, New YorkGoogle Scholar
  58. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251CrossRefPubMedGoogle Scholar
  59. Yoshihara T, Iino M (2005) Circumnutation of rice coleoptiles: its occurrence, regulation by phytochrome, and relationship with gravitropism. Plant Cell Environ 28:134–146CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK 2017

Authors and Affiliations

  • Motoyuki Iida
    • 1
  • Toshihiko Takano
    • 1
  • Takakazu Matsuura
    • 2
  • Izumi C. Mori
    • 2
  • Shingo Takagi
    • 1
  1. 1.Department of Biological Sciences, Graduate School of ScienceOsaka UniversityToyonakaJapan
  2. 2.Institute of Plant Science and ResourcesOkayama UniversityKurashikiJapan

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