Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

An essential role for Arabidopsis Trs33 in cell growth and organization in plant apical meristems

Abstract

Key message

Trafficking protein particle (TRAPP) complexes subunit gene AtTrs33 plays an important role in keeping apical meristematic activity and dominance in Arabidopsis.

Abstract

TRAPP complexes, composed of multimeric subunits, are guanine–nucleotide exchange factors for certain Rab GTPases and are believed to be involved in the regulation of membrane trafficking, but the cases in Arabidopsis are largely unknown. Trs33, recently proposed to be a component of TRAPP IV, is non-essential in yeast cells. A single copy of Trs33 gene, AtTrs33, was identified in Arabidopsis. GUS activity assay indicated that AtTrs33 was ubiquitously expressed. Based on a T-DNA insertion line, we found that loss-of-function of AtTrs33 is lethal for apical growth. Knock-down or knock-in of AtTrs33 affects apical meristematic growth and fertility, which indicates that AtTrs33 plays an important role in keeping apical meristematic activity and dominance in Arabidopsis. Analysis of auxin responses and PIN1/2 localization indicate that impaired apical meristematic activity and dominance were caused by altered auxin responses through non-polarized PIN1 localization. The present study reported that AtTrs33 plays an essential role in Arabidopsis cell growth and organization, which is different with its homologue in yeast. These findings provide new insights into the functional divergence of TRAPP subunits.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

DAG:

Days after germination

ER:

Endoplasmic reticulum

GEF:

Guanine–nucleotide exchange factor

GFP:

Green fluorescent protein

PI:

Propidium iodide

RNAi:

RNA interference

TRAPP:

Trafficking protein particle

YFP:

Yellow fluorescent proteins

References

  1. Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256

  2. Barrowman J, Bhandari D, Reinisch K, Ferro-Novick S (2010) TRAPP complexes in membrane traffic: convergence through a common Rab. Nat Rev 11:759–763

  3. Battraw MJ, Hall TC (1990) Histochemical analysis of CaMV 35S promoter-β-glucuronidase gene expression in transgenic rice plants. Plant Mol Biol 15:527–538

  4. Benjamins R, Malenica N, Luschnig C (2005) Regulating the regulator: the control of auxin transport. BioEssays 27:1246–1255

  5. Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447

  6. Cai Y, Chin HF, Lazarova D, Menon S, Fu C, Cai H, Sclafani A, Rodgers DW, De La Cruz EM, Ferro-Novick S, Reinisch KM (2008) The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell 133:1202–1213

  7. Choi C, Davey M, Schluter C, Pandher P, Fang Y, Foster LJ, Conibear E (2011) Organization and assembly of the TRAPPII complex. Traffic (Copenhagen, Denmark) 12:715–725

  8. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

  9. Cox R, Chen SH, Yoo E, Segev N (2007) Conservation of the TRAPPII-specific subunits of a Ypt/Rab exchanger complex. BMC Evol Biol 7:12

  10. Dhonukshe P, Tanaka H, Goh T, Ebine K, Mahonen AP, Prasad K, Blilou I, Geldner N, Xu J, Uemura T, Chory J, Ueda T, Nakano A, Scheres B, Friml J (2008) Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456:962–966

  11. Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci USA 107:12046–12051

  12. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science (New York, NY) 282:2226–2230

  13. Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013

  14. Gwynn B, Smith RS, Rowe LB, Taylor BA, Peters LL (2006) A mouse TRAPP-related protein is involved in pigmentation. Genomics 88:196–203

  15. Jaber E, Thiele K, Kindzierski V, Loderer C, Rybak K, Jurgens G, Mayer U, Sollner R, Wanner G, Assaad FF (2010) A putative TRAPPII tethering factor is required for cell plate assembly during cytokinesis in Arabidopsis. New Phytol 187:751–763

  16. Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miege C, Gaude T (2007) The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130:1057–1070

  17. Jiang K, Feldman LJ (2005) Regulation of root apical meristem development. Annu Rev Cell Dev Biol 21:485–509

  18. Kim JJ, Lipatova Z, Segev N (2016) TRAPP complexes in secretion and autophagy. Front Cell Dev Biol 4:20

  19. Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J (2006) Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell 18:3171–3181

  20. Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wisniewska J, Paciorek T, Benkova E, Friml J (2008) ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 18:526–531

  21. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazimalova E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249

  22. Latijnhouwers M, Hawes C, Carvalho C (2005) Holding it all together? Candidate proteins for the plant Golgi matrix. Curr Opin Plant Biol 8:632–639

  23. Lipatova Z, Majumdar U, Segev N (2016) Trs33-containing TRAPP IV: a novel autophagy-specific Ypt1 GEF. Genetics 204:1117–1128

  24. Liu ZB, Ulmasov T, Shi X, Hagen G, Guilfoyle TJ (1994) Soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell 6:645–657

  25. Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947

  26. Morozova N, Liang Y, Tokarev AA, Chen SH, Cox R, Andrejic J, Lipatova Z, Sciorra VA, Emr SD, Segev N (2006) TRAPPII subunits are required for the specificity switch of a Ypt-Rab GEF. Nat Cell Biol 8:1263–1269

  27. Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684

  28. Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659–1668

  29. Petrasek J, Friml J (2009) Auxin transport routes in plant development. Development (Cambridge, England) 136:2675–2688

  30. Pinheiro H, Samalova M, Geldner N, Chory J, Martinez A, Moore I (2009) Genetic evidence that the higher plant Rab-D1 and Rab-D2 GTPases exhibit distinct but overlapping interactions in the early secretory pathway. J Cell Sci 122:3749–3758

  31. Qi X, Zheng H (2011) Arabidopsis TRAPPII is functionally linked to Rab-A, but not Rab-D in polar protein trafficking in trans-Golgi network. Plant Signal Behav 6:1679–1683

  32. Qi X, Kaneda M, Chen J, Geitmann A, Zheng H (2011) A specific role for Arabidopsis TRAPPII in post-Golgi trafficking that is crucial for cytokinesis and cell polarity. Plant J 68:234–248

  33. Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB, Baskin TI (2007) Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J 50:514–528

  34. Ravikumar R, Steiner A, Assaad FF (2017) Multisubunit tethering complexes in higher plants. Curr Opin Plant Biol 40:97–105

  35. Robert S, Chary SN, Drakakaki G, Li S, Yang Z, Raikhel NV, Hicks GR (2008) Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc Natl Acad Sci USA 105:8464–8469

  36. Sacher M, Barrowman J, Wang W, Horecka J, Zhang Y, Pypaert M, Ferro-Novick S (2001) TRAPP I implicated in the specificity of tethering in ER-to-Golgi transport. Mol Cell 7:433–442

  37. Somerville CR, Ogren WL (1982) Isolation of photorespiratory mutants of Arabidopsis. In: Hallick RB, Chua NH (eds) Methods in chloroplast molecular biology. Elsevier, New York, pp 129–139

  38. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science (New York, NY) 286:316–318

  39. Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JD, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954

  40. Tan D, Cai Y, Wang J, Zhang J, Menon S, Chou HT, Ferro-Novick S, Reinisch KM, Walz T (2013) The EM structure of the TRAPPIII complex leads to the identification of a requirement for COPII vesicles on the macroautophagy pathway. Proc Natl Acad Sci USA 110:19432–19437

  41. Teh OK, Moore I (2007) An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448:493–496

  42. Thellmann M, Rybak K, Thiele K, Wanner G, Assaad FF (2010) Tethering factors required for cytokinesis in Arabidopsis. Plant Physiol 154:720–732

  43. Tokarev AA, Taussig D, Sundaram G, Lipatova Z, Liang Y, Mulholland JW, Segev N (2009) TRAPP II complex assembly requires Trs33 or Trs65. Traffic (Copenhagen, Denmark) 10:1831–1844

  44. Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623

  45. Vandenbussche F, Petrasek J, Zadnikova P, Hoyerova K, Pesek B, Raz V, Swarup R, Bennett M, Zazimalova E, Benkova E, Van Der Straeten D (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development (Cambridge, England) 137:597–606

  46. Vernoux T, Besnard F, Traas J (2010) Auxin at the shoot apical meristem. Cold Spring Harb Perspect Biol 2:a001487

  47. Yamasaki A, Menon S, Yu S, Barrowman J, Meerloo T, Oorschot V, Klumperman J, Satoh A, Ferro-Novick S (2009) mTrs130 is a component of a mammalian TRAPPII complex, a Rab1 GEF that binds to COPI-coated vesicles. Mol Biol Cell 20:4205–4215

  48. Zhang J, Li J, Liu B, Zhang L, Chen J, Lu M (2013) Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses. BMC Genom 14:532

  49. Zhang J, Chen J, Wang LJ, Zhao ST, Li JB, Liu BB, Li HY, Qi XY, Zheng HQ, Lu MZ (2018) AtBET5 is essential for exine pattern formation and apical meristem organization in Arabidopsis. Plant Sci 274:231–241

  50. Zhuang X, Chung KP, Luo M, Jiang L (2018) Autophagosome biogenesis and the endoplasmic reticulum: a plant perspective. Trends Plant Sci 23:677–692

Download references

Acknowledgements

We would like to thank the reviewers and editors for their careful reading and helpful comments on this manuscript.

Funding

This work was supported by the Special Fund on Essential Research for National Non-profit Institutions to the Chinese Academy of Forestry (CAFYBB2011001) to ML, and a Grant from The National Science and Engineering Research Council of Canada and a startup grant from McGill University (Montreal, Canada) to HZ.

Author information

HZ and ML designed the study. JZ, JC and WW performed the experiments, JZ and JC analyzed the data and wrote the manuscript. LW, SZ, JL, BL and XQ contributed to the data collection and data analysis. JZ, JC, HZ and ML revised the manuscript. All authors read and approved the final manuscript.

Correspondence to Huanquan Zheng or Mengzhu Lu.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Publisher's Note

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

Communicated by Xian Sheng Zhang.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Chen, J., Wang, L. et al. An essential role for Arabidopsis Trs33 in cell growth and organization in plant apical meristems. Plant Cell Rep 39, 381–391 (2020). https://doi.org/10.1007/s00299-019-02497-9

Download citation

Keywords

  • Arabidopsis
  • Trs33
  • TRAPP
  • Apical meristem
  • Auxin
  • PIN1/2
  • Subcellular localization