Skip to main content
Log in

Long-distance regulation of shoot gravitropism by Cyclophilin 1 in tomato (Solanum lycopersicum) plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The phloem-mobile protein SlCyp1 traffics to distant parts of the shoot to regulate its gravitropic response. In addition, SlCyp1 targets specific cells in the root to promote lateral root development.

Abstract

The tomato (Solanum lycopersicum) Cyclophilin 1 (SlCyp1) gene encodes a peptidyl-prolyl isomerase required for auxin response, lateral root development and gravitropic growth. The SlCyp1 protein is a phloem-mobile signal that moves from shoot to root to regulate lateral root development (Spiegelman et al., Plant J 83:853–863, 2015; J Exp Bot 68:953–964, 2017a). Here, we explored the mechanism of SlCyp1 movement by fusing it to the fluorescent protein mCherry. We found that, once trafficked to the root, SlCyp1 is unloaded from the phloem to the surrounding tissues, including the pericycle and lateral root primordia. Interestingly, SlCyp1 not only moves to the root system, but also to distant parts of the shoot. Grafting of the SlCyp1 mutant diageotropica (dgt) scions on VFN8 control rootstocks resulted in recovery of dgt shoot gravitropism, which was associated with the restoration of auxin-response capacity. Application of the cyclophilin inhibitor cyclosporine A suppressed gravitropic recovery, indicating that SlCyp1 must be active in the target tissue to affect the gravitropic response. These results provide new insights on the mechanism of SlCyp1 transport and functioning as a long-distance signal regulating shoot gravitropism.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

CysA:

Cyclosporine A

dgt :

diageotropica.

SlCyp1:

Solanum lycopersicum Cyclophilin 1

pSuc2 :

Suc2 Promoter from Arabidopsis thaliana

References

  • Balbi V, Lomax TL (2003) Regulation of early tomato fruit development by the diageotropica gene. Plant Physiol 131:186–197

    CAS  PubMed  PubMed Central  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

    PubMed  Google Scholar 

  • Daniel SG, Rayle DL, Cleland RE (1989) Auxin physiology of the tomato mutant diageotropica. Plant Physiol 91:804–807

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Smet I, Tetsumura T, De Rybel B, dit Frey NF, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inzé D, Bennett MJ, Beeckman T, (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690

    PubMed  Google Scholar 

  • Dubrovsky JG, Rost TL, Colón-Carmona A, Doerner P (2001) Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214:30–36

    CAS  PubMed  Google Scholar 

  • Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105:8790–8794

    CAS  PubMed  Google Scholar 

  • Esmon CA, Tinsley AG, Ljung K, Sandberg G, Hearne LB, Liscum E (2006) A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc Natl Acad Sci USA 103:236–241

    CAS  PubMed  Google Scholar 

  • Estelle M (1996) Plant tropisms: the ins and outs of auxin. Curr Biol 6:1589–1591

    CAS  PubMed  Google Scholar 

  • Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809

    PubMed  Google Scholar 

  • Fujino DW, Nissen SJ, Jones AD, Burger DW, Bradford KJ (1988) Quantification of indole-3-acetic acid in dark-grown seedlings of the diageotropica and epinastic mutants of tomato (Lycopersicon esculentum Mill.). Plant Physiol 88:780–784

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168

    CAS  PubMed  Google Scholar 

  • Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 256:111–137

    CAS  PubMed  Google Scholar 

  • Gleave AP (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20:1203–1207

    CAS  PubMed  Google Scholar 

  • Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12:757–770

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanchenko MG, Zhu J, Wang B, Medvecká E, Du Y, Azzarello E, Mancuso S, Megraw M, Filichkin S, Dubrovsky JG, Friml J, Geisler M (2015) The cyclophilin A DIAGEOTROPICA gene affects auxin transport in both root and shoot to control lateral root formation. Development 142:712–721

    CAS  PubMed  Google Scholar 

  • Jing H, Yang X, Zhang J, Liu X, Zheng H, Dong G, Nian J, Feng J, Xia B, Qian Q, Li J, Zuo J (2015) Peptidyl-prolyl isomerization targets rice Aux/IAAs for proteasomal degradation during auxin signalling. Nat Commun 6:1–10

    Google Scholar 

  • Kang B, Zhang Z, Wang L, Zheng L, Mao W, Li M, Wu Y, Wu P, Mo X (2013) OsCYP 2, a chaperone involved in degradation of auxin-responsive proteins, plays crucial roles in rice lateral root initiation. Plant J 74:86–97

    CAS  PubMed  Google Scholar 

  • Kelly MO, Bradford KJ (1986) Insensitivity of the diageotropica tomato mutant to auxin. Plant Physiol 82:713–717

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18:450–458

    CAS  PubMed  Google Scholar 

  • Masson PH, Tasaka M, Morita MT, Guan C, Chen R, Boonsirichai K (2002) Arabidopsis thaliana: a model for the study of root and shoot gravitropism. Arabidopsis Book 1:e0043

    PubMed  PubMed Central  Google Scholar 

  • McCormick S (1991) Transformation of tomato with Agrobacterium tumefaciens. In: Lindsey K (ed) Plant tissue culture manual. Springer, Dordrecht, pp 311–319

    Google Scholar 

  • Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720

    CAS  PubMed  Google Scholar 

  • Muday GK, Lomax TL, Rayle DL (1995) Characterization of the growth and auxin physiology of roots of the tomato mutant, diageotropica. Planta 195:548–553

    CAS  PubMed  Google Scholar 

  • Nebenführ A, White TJ, Lomax TL (2000) The diageotropica mutation alters auxin induction of a subset of the Aux/IAA gene family in tomato. Plant Mol Biol 44(1):73–84

    PubMed  Google Scholar 

  • Oh K, Ivanchenko MG, White TJ, Lomax TL (2006) The diageotropica gene of tomato encodes a cyclophilin: a novel player in auxin signaling. Planta 224:133–144

    CAS  PubMed  Google Scholar 

  • Okushima Y, Mitina I, Quach HL, Theologis A (2005) Auxin Response Factor 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46

    CAS  PubMed  Google Scholar 

  • Paultre DSG, Gustin MP, Molnar A, Oparka KJ (2016) Lost in transit: long-distance trafficking and phloem unloading of protein signals in Arabidopsis homografts. Plant Cell 28:2016–2025

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petrásek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wisniewska J, Tadele Z, Kubes M, Covanová M, Dhonukshe P, Skupa P, Benková E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazímalová E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918

    PubMed  Google Scholar 

  • 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 67:817–826

    PubMed  Google Scholar 

  • Rice MS, Lomax TL (2000) The auxin-resistant diageotropica mutant of tomato responds to gravity via an auxin-mediated pathway. Planta 210:906–913

    CAS  PubMed  Google Scholar 

  • Spiegelman Z, Ham BK, Zhang Z, Toal TW, Brady SM, Zheng Y, Fei Z, Lucas WJ, Wolf S (2015) A tomato phloem-mobile protein regulates the shoot-to-root ratio by mediating the auxin response in distant organs. Plant J 83:853–863

    CAS  PubMed  Google Scholar 

  • Spiegelman Z, Omer S, Mansfeld BN, Wolf S (2017a) Function of Cyclophilin1 as a long-distance signal molecule in the phloem of tomato plants. J Exp Bot 68:953–964

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spiegelman Z, Shahar A, Wolf S (2017b) Down-regulation of SlCyp1 in the phloem reduces auxin response and photosynthetic rate in tomato (Solanum lycopersicum) plants. Plant Signal Behav 12:e1338224

    PubMed  PubMed Central  Google Scholar 

  • Swarup R, Péret B (2012) AUX/LAX family of auxin influx carriers—an overview. Front Plant Sci 3:225

    PubMed  PubMed Central  Google Scholar 

  • Tasaka M, Kato T, Fukaki H (1999) The endodermis and shoot gravitropism. Trends Plant Sci 4:103–107

    CAS  PubMed  Google Scholar 

  • Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Liscum E, Yamamoto KT (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell 16:379–393

    CAS  PubMed  PubMed Central  Google Scholar 

  • Truernit E, Sauer N (1995) The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta 196:564–570

    CAS  PubMed  Google Scholar 

  • Wang P, Heitman J (2005) The cyclophilins. Genome Biol 6:226

    PubMed  PubMed Central  Google Scholar 

  • Went FW, Thimann KV (1937) Phytohormones. Macmillan, New York

    Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zobel RW (1973) Some physiological characteristics of the ethylene-requiring tomato mutant diageotropica. Plant Physiol 52:385–389

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zobel RW (1974) Control of morphogenesis in the ethylene-requiring tomato mutant, diageotropica. Can J Bot 52:735–741

    Google Scholar 

Download references

Acknowledgements

This paper is a contribution from the Uri Kinamon Laboratory, and OB and AS were supported by a scholarship from the Kinamon Foundation. SO was supported by a scholarship from the PBC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ziv Spiegelman.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Additional information

Communicated by Dorothea Bartels.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 210 kb)

Supplementary file2 (MP4 6507 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Spiegelman, Z., Broshi, O., Shahar, A. et al. Long-distance regulation of shoot gravitropism by Cyclophilin 1 in tomato (Solanum lycopersicum) plants. Planta 252, 50 (2020). https://doi.org/10.1007/s00425-020-03448-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-020-03448-5

Keywords

Navigation