Skip to main content
Log in

Gravity-controlled asymmetrical transport of auxin regulates a gravitropic response in the early growth stage of etiolated pea (Pisum sativum) epicotyls: studies using simulated microgravity conditions on a three-dimensional clinostat and using an agravitropic mutant, ageotropum

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Increased expression of the auxin-inducible gene PsIAA4/5 was observed in the elongated side of epicotyls in early growth stages of etiolated pea (Pisum sativum L. cv. Alaska) seedlings grown in a horizontal or an inclined position under 1 g conditions. Under simulated microgravity conditions on a 3D clinostat, accumulation of PsIAA4/5 mRNA was found throughout epicotyls showing automorphosis. Polar auxin transport in the proximal side of epicotyls changed when the seedlings were grown in a horizontal or an inclined position under 1 g conditions, but that under clinorotation did not, regardless of the direction of seed setting. Accumulation of PsPIN1 and PsPIN2 mRNAs in epicotyls was affected by gravistimulation, but not by clinorotation. Under 1 g conditions, auxin-transport inhibitors made epicotyls of seedlings grown in a horizontal or inclined position grow toward the proximal direction to cotyledons. These inhibitors led to epicotyl bending toward the cotyledons in seedlings grown in an inclined position under clinorotation. Polar auxin transport, as well as growth direction, of epicotyls of the agravitropic mutant ageotropum did not respond to various gravistimulation. These results suggest that alteration of polar auxin transport in the proximal side of epicotyls regulates the graviresponse of pea epicotyls.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1a–f
Fig. 2
Fig. 3
Fig. 4
Fig. 5a–c
Fig. 6a–d

Similar content being viewed by others

References

  • Bai F, DeMason DA (2006) Hormone interactions and regulation of Unifoliata, PsPK2, PsPIN1 and LE gene expression in pea (Pisum sativum) shoot tips. Plant Cell Physiol 47:935–948

    Article  PubMed  CAS  Google Scholar 

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  Google Scholar 

  • Blakeslee JJ, Peer WA, Murphy AS (2005) Auxin transport. Curr Opin Plant Biol 8:494–500

    Article  PubMed  CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  PubMed  CAS  Google Scholar 

  • Blixt S, Ehrenberg L, Gelin O (1958) Quantitative studies of induced mutations in peas. I. Methodological investigation Agri Hortic Genet 16:238–250

    Google Scholar 

  • Brown AH, Chapman DK, Lewis RF, Venditti AL (1990) Circumnutations of sunflower hypocotyls in satellite orbit. Plant Physiol 94:233–238

    PubMed  CAS  Google Scholar 

  • Chawla R, DeMason DA (2004) Molecular expression of PsPIN1, a putative auxin efflux carrier gene from pea (Pisum sativum L.). Plant Growth Regul 44:1–14

    Article  CAS  Google Scholar 

  • Friml J (2003) Auxin transport—shaping the plant. Curr Opin Plant Biol 6:7–12

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Palme K (2002) Polar auxin transport—old questions and new concepts? Plant Mol Biol 49:273–284

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  PubMed  CAS  Google Scholar 

  • Halstead TW, Dutcher FR (1987) Plants in space. Annu Rev Plant Physiol 38:317–345

    Article  PubMed  CAS  Google Scholar 

  • Hoshino T, Hitotsubashi R, Miyamoto K, Tanimoto E, Ueda J (2005) Isolation of PsPIN2 and PsAUX1 from etiolated pea epicotyls and their expression on a three-dimensional clinostat. Adv Space Res 36:1284–1291

    Article  CAS  Google Scholar 

  • Hoshino T, Miyamoto K, Ueda J (2006) Requirement for the gravity-controlled transport of auxin for a negative gravitropic response of epicotyls in the early growth stage of etiolated pea seedlings. Plant Cell Physiol 47:1496–1508

    Article  PubMed  CAS  Google Scholar 

  • Hoson T, Kamisaka S, Masuda Y, Yamashita M (1992) Changes in plant growth processes under microgravity conditions simulated by a three-dimensional clinostat. Bot Mag Tokyo 105:53–70

    Article  Google Scholar 

  • Hoson T, Kamisaka S, Masuda Y, Yamashita M, Buchen B (1997) Evaluation of the three-dimensional clinostat as a simulator of weightlessness. Planta 203:S187–S197

    Article  PubMed  CAS  Google Scholar 

  • Hoson T, Soga K, Mori R, Saiki M, Wakabayashi K, Kamisaka S, Kamigaichi S, Aizawa S, Yoshizaki I, Mukai C, Shimazu T, Fukui K, Yamashita M (1999) Morphogenesis of rice and Arabidopsis seedlings in space. J Plant Res 112:477–486

    Article  PubMed  CAS  Google Scholar 

  • Jaffe MJ, Takahashi H, Biro RL (1985) A pea mutant for the study of hydrotropism in roots. Science 230:445–447

    Article  PubMed  Google Scholar 

  • Kamada M, Yamasaki S, Fujii N, Higashitani A, Takahashi H (2003) Gravity-induced modification of auxin transport and distribution for peg formation in cucumber seedlings: possible roles for CS-AUX1 and CS-PIN1. Planta 218:15–26

    Article  PubMed  CAS  Google Scholar 

  • Katekar GF, Geissler AE (1980) Auxin transport inhibitors: IV. Evidence of a common mode of action for a proposed class of auxin transport inhibitors: the phytotropins. Plant Physiol 66:1190–1195

    Article  PubMed  CAS  Google Scholar 

  • Kiss JZ (2000) Mechanisms of the early phases of plant gravitropism. CRC Crit Rev Plant Sci 19:551–573

    Article  PubMed  CAS  Google Scholar 

  • Kiss JZ, Katembe WJ, Edelmann RE (1998) Gravitropism and development of wild-type and starch-deficient mutants of Arabidopsis during spaceflight. Physiol Plant 102:493–502

    Article  PubMed  CAS  Google Scholar 

  • Kraft TFB, van Loon JJWA, Kiss JZ (2000) Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta 211:415–422

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto K, Hoshino T, Yamashita M, Ueda J (2005) Automorphosis of etiolated pea seedlings in space is simulated by a three-dimensional clinostat and the application of inhibitors of auxin polar transport. Physiol Plant 123:467–474

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto K, Hoshino T, Takahashi Y, Ueda J (2006) Auxin polar transport of etiolated epicotyls of ageotropum pea seedlings is not affected by gravistimulation: relevance to automorphosis-like growth and development. 36th COPAR Scientific Assembly Abstracts, Beijing

  • Moore I (2002) Gravitropism: lateral thinking in auxin transport. Curr Biol 2002:R452–R454

    Article  Google Scholar 

  • Morita MT, Tasaka M (2004) Gravity sensing and signaling. Curr Opin Plant Biol 7:712–718

    Article  PubMed  CAS  Google Scholar 

  • Morris DA, Friml J, Zazímalová E (2004) The transport of auxins. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action! Kluwer, Dordrecht, pp 437–470

    Google Scholar 

  • Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends Plant Sci 6:535–542

    Article  PubMed  CAS  Google Scholar 

  • Muday GK, Murphy AS (2002) An emerging model of auxin transport regulation. Plant Cell 14:293–299

    Article  PubMed  CAS  Google Scholar 

  • Musgrave ME, Kuang A, Matthews SW (1997) Plant reproduction during spaceflight: importance of the gaseous environment. Planta 203:S177–S184

    Article  PubMed  CAS  Google Scholar 

  • Musgrave ME, Kuang A, Xiao Y, Stout SC, Bingham GE, Briarty LG, Levinskikh MA, Sychev VN, Podolski IG (2000) Gravity independence of seed-to-seed cycling in Brassica rapa. Planta 210:400–406

    Article  PubMed  CAS  Google Scholar 

  • Ni WN, Chen XY, Xu ZH, Xue HW (2002) Isolation and functional analysis of a Brassica juncea gene encoding a component of auxin efflux carrier. Cell Res 12:235–245

    Article  PubMed  Google Scholar 

  • Oka M, Ueda J, Miyamoto K, Yamamoto R, Hoson T, Kamisaka S. (1995) Effect of simulated microgravity on auxin polar transport in inflorescence axis of Arabidopsis thaliana. Biol Sci Space 9:331–336

    Article  PubMed  CAS  Google Scholar 

  • Rashotte AM, Brady SR, Reed RC, Ante SJ, Muday GK (2000) Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol 122:481–490

    Article  PubMed  CAS  Google Scholar 

  • Schnabel EL, Frugoli J (2004) The PIN and LAX families of auxin transport genes in Medicago truncatula. Mol Genet Genomics 272:420–432

    Article  PubMed  CAS  Google Scholar 

  • Schöldéen C, Burström H (1960) Physiological studies of an ageotropic pea mutant. Physiol Plant 13:831–838

    Article  Google Scholar 

  • Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100:10096–10101

    Article  PubMed  CAS  Google Scholar 

  • Shimazu T, Miyamoto K, Hoson T, Kamisaka S, Ueda J (2000) Suitable experimental design for determination of auxin polar transport in space using a spacecraft. Biol Sci Space 14:9–13

    Article  PubMed  CAS  Google Scholar 

  • Shimazu T, Yuda T, Miyamoto K, Yamashita M, Ueda J (2001) Growth and development in higher plants under simulated microgravity conditions on a 3-dimensional clinostat. Adv Space Res 27:995–1000

    Article  PubMed  CAS  Google Scholar 

  • Stankovic B, Volkmann D, Sack FD (1998a) Autotropism, automorphogenesis, and gravity. Physiol Plant 102:328–335

    Article  PubMed  CAS  Google Scholar 

  • Stankovic B, Volkmann D, Sack FD (1998b) Autonomic straightening after gravitropic curvature of cress roots. Plant Physiol 117:893–900

    Article  PubMed  CAS  Google Scholar 

  • Stinemets C, Takahashi H, Suge H (1996) Characterization of hydrotropism: the timing of perception and signal movement from the root cap in the agravitropic pea mutant ageotropum. Plant Cell Physiol 37:800–805

    Google Scholar 

  • Takahashi H, Suge H (1991) Root hydrotropism of an agravitropic pea mutant, ageotropum. Physiol Plant 82:24–31

    Article  Google Scholar 

  • Takahashi H, Suge H, Jaffe MJ (1991) Agravitropic growth and its relation to the formation of the plumular hook in etiolated shoots of the pea mutant, ageotropum. J Plant Physiol 138:216–212

    Google Scholar 

  • Takahashi H, Mizuno H, Kamada M, Fujii N, Higashitani A, Kamigaichi S, Aizawa S, Mukai C, Shimazu T, Fukui K, Yamashita M (1999) A spaceflight experiment for the study of gravimorphogenesis and hydrotropism in cucumber seedlings. J Plant Res 112:497–505

    Article  PubMed  CAS  Google Scholar 

  • Takano M, Takahashi H, Hirasawa T, Suge H (1995) Hydrotropism in roots: sensing of a gradient in water potential by the root cap. Planta 197:410–413

    Article  CAS  Google Scholar 

  • Ueda J, Miyamoto K, Yuda T, Hoshino T, Fujii S, Mukai C, Kamigaichi S, Aizawa S, Yoshizaki I, Shimazu T, Fukui K (1999) Growth and development, and auxin polar transport in higher plants under microgravity conditions in space: BRIC-AUX on STS-95 space experiment. J Plant Res 112:487–492

    Article  PubMed  CAS  Google Scholar 

  • Ueda J, Miyamoto K, Yuda T, Hoshino T, Sato K, Fujii S, Kamigaichi S, Izumi R, Ishioka N, Aizawa S, Yoshizaki I, Shimazu T, Fukui K (2000) STS-95 space experiment for plant growth and development, and auxin polar transport. Biol Sci Space 14:47–57

    Article  PubMed  CAS  Google Scholar 

  • Went FW (1974) Reflections and speculations. Annu Rev Plant Physiol 25:1–26

    Article  CAS  Google Scholar 

  • Xu M, Zhu L, Shou H, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46:1674–1681

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Professors Hideyuki Takahashi and Nobuharu Fujii (Tohoku University, Sendai, Japan) for their invaluable suggestions and discussions, and kind gift of ageotropum seeds.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Junichi Ueda.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoshino, T., Miyamoto, K. & Ueda, J. Gravity-controlled asymmetrical transport of auxin regulates a gravitropic response in the early growth stage of etiolated pea (Pisum sativum) epicotyls: studies using simulated microgravity conditions on a three-dimensional clinostat and using an agravitropic mutant, ageotropum . J Plant Res 120, 619–628 (2007). https://doi.org/10.1007/s10265-007-0103-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-007-0103-2

Keywords

Navigation