Trafficking protein particle (TRAPP) complexes subunit gene AtTrs33 plays an important role in keeping apical meristematic activity and dominance in Arabidopsis.
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.
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Days after germination
Guanine–nucleotide exchange factor
Green fluorescent protein
Trafficking protein particle
Yellow fluorescent proteins
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
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
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
Benjamins R, Malenica N, Luschnig C (2005) Regulating the regulator: the control of auxin transport. BioEssays 27:1246–1255
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
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
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
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
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
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
Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci USA 107:12046–12051
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
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
Gwynn B, Smith RS, Rowe LB, Taylor BA, Peters LL (2006) A mouse TRAPP-related protein is involved in pigmentation. Genomics 88:196–203
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
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
Jiang K, Feldman LJ (2005) Regulation of root apical meristem development. Annu Rev Cell Dev Biol 21:485–509
Kim JJ, Lipatova Z, Segev N (2016) TRAPP complexes in secretion and autophagy. Front Cell Dev Biol 4:20
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
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
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
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
Lipatova Z, Majumdar U, Segev N (2016) Trs33-containing TRAPP IV: a novel autophagy-specific Ypt1 GEF. Genetics 204:1117–1128
Liu ZB, Ulmasov T, Shi X, Hagen G, Guilfoyle TJ (1994) Soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell 6:645–657
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
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
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
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
Petrasek J, Friml J (2009) Auxin transport routes in plant development. Development (Cambridge, England) 136:2675–2688
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
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
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
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
Ravikumar R, Steiner A, Assaad FF (2017) Multisubunit tethering complexes in higher plants. Curr Opin Plant Biol 40:97–105
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
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
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
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
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
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
Teh OK, Moore I (2007) An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448:493–496
Thellmann M, Rybak K, Thiele K, Wanner G, Assaad FF (2010) Tethering factors required for cytokinesis in Arabidopsis. Plant Physiol 154:720–732
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
Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623
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
Vernoux T, Besnard F, Traas J (2010) Auxin at the shoot apical meristem. Cold Spring Harb Perspect Biol 2:a001487
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
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
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
Zhuang X, Chung KP, Luo M, Jiang L (2018) Autophagosome biogenesis and the endoplasmic reticulum: a plant perspective. Trends Plant Sci 23:677–692
We would like to thank the reviewers and editors for their careful reading and helpful comments on this manuscript.
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.
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Communicated by Xian Sheng Zhang.
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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
- Apical meristem
- Subcellular localization