Skip to main content
SpringerLink
Log in

AtSec20 is involved in osmotic stress tolerance and AtSec20 mutation unaffects the integrity of intracellular organelles and the anterograde biosynthetic trafficking

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) play essential roles in intracellular trafficking. However, few experimental data have clarified their roles in the stress responses and the early secretary pathway in Arabidopsis. The AtSec20 gene encodes a protein that is homologous to yeast Sec20p and mammalian BNIP1, which are involved in the Golgi-to-ER retrograde trafficking in yeast and mammalian cells. In this study, AtSec20 is found to be required for the responses to salt stress, osmotic stress and gibberellin (GA) during seed germination and early seedling establishment. Mutation of AtSec20 unaffects the morphology of intracellular organelles, such as endoplasmic reticulum (ER), trans-Golgi network, and peroxisome, and vacuolar protein trafficking is normal in sec20 mutants. Collectively, these results imply that the AtSec20 is involved in abiotic stress tolerance, potentially via roles in retrograde vesicle fusion process in Arabidopsis.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Andag U, Schmitt HD (2003) Dsl1p, an essential component of the Golgi–endoplasmic reticulum retrieval system in yeast, uses the same sequence motif to interact with different subunits of the COPI vesicle coat. J Biol Chem 278:51722–51734

    Article  PubMed  CAS  Google Scholar 

  • Andag U, Neumann T, Schmitt HD (2001) The coatomer-interacting protein Dsl1p is required for Golgi-to-endoplasmic reticulum retrieval in yeast. J Biol Chem 276:39150–39160

    Article  PubMed  CAS  Google Scholar 

  • Aoki T, Kojima M, Tani K, Tagaya M (2008) Sec22b-dependent assembly of endoplasmic reticulum Q-SNARE proteins. Biochem J 410:93–100

    Article  PubMed  CAS  Google Scholar 

  • Aoki T, Ichimura S, Itoh A, Kuramoto M, Shinkawa T, Isobe T, Tagaya M (2009) Identification of the neuroblastoma-amplified gene (NAG) product as a component of the syntaxin 18 complex implicated in Golgi-to-endoplasmic reticulum retrograde transport. Mol Biol Cell 20:2639–2649

    Article  PubMed  CAS  Google Scholar 

  • Arasaki K, Taniguchi M, Tani K, Tagaya M (2006) RINT-1 regulates the localization and entry of ZW10 to the syntaxin 18 complex. Mol Biol Cell 17:2780–2788

    Article  PubMed  CAS  Google Scholar 

  • Bassham DC, Blatt MR (2008) SNAREs: cogs and coordinators in signaling and development. Plant Physiol 147:1504–1515

    Article  PubMed  CAS  Google Scholar 

  • Bassham DC, Brandizzi F, Otegui M, Sanderfoot AA (2008) The secretory system of Arabidopsis. In: Somerville CR, Meyerowitz EM (eds) the Arabidopsis Book. vol 6. American Society of Plant Biologists, Rockville, MD, pp e0116

  • Bassham DC, Sanderfoot AA, Kovaleva V, Zheng H, Raikhel NV (2000) AtVPS45 complex formation at the trans-Golgi network. Mol Biol Cell 11:2251–2265

    PubMed  CAS  Google Scholar 

  • Batoko H, Zheng HQ, Hawes C, Moore I (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12:2201–2217

    PubMed  CAS  Google Scholar 

  • Bubeck J, Scheuring D, Hummel E, Langhans M, Viotti C, Foresti O, Denecke J, Banfield DK, Robinson DG (2008) The syntaxins SYP31 and SYP81 control ER–Golgi trafficking in the plant secretory pathway. Traffic 9:1629–1652

    Article  PubMed  CAS  Google Scholar 

  • Cai H, Reinisch K, Ferro-Novick S (2007) Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12:671–682

    Google Scholar 

  • Dilcher M, Veith B, Chidambaram S, Hartmann E, Schmitt HD, Fischer von Mollard G (2003) Use1p is a yeast SNARE protein required for retrograde traffic to the ER. EMBO J 22:3664–3674

    Article  PubMed  CAS  Google Scholar 

  • Ebine K, Okatani Y, Uemura T, Goh T, Shoda K, Niihama M, Morita MT, Spitzer C, Otegui MS, Nakano A, Ueda T (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell 20:3006–3021

    Article  PubMed  CAS  Google Scholar 

  • Hamaji K, Nagira M, Yoshida K, Ohnishi M, Oda Y, Uemura T, Goh T, Sato MH, Morita MT, Tasaka M, Hasezawa S, Nakano A, Hara-Nishimura I, Maeshima M, Fukaki H, Mimura T (2009) Dynamic aspects of ion accumulation by vesicle traffic under salt stress in Arabidopsis. Plant Cell Physiol 50:2023–2033

    Article  PubMed  CAS  Google Scholar 

  • Hwang I (2008) Sorting and anterograde trafficking at the Golgi apparatus. Plant Physiol 148:673–683

    Article  PubMed  CAS  Google Scholar 

  • Iinuma T, Aoki T, Arasaki K, Hirose H, Yamamoto A, Samata R, Hauri HP, Arimitsu N, Tagaya M, Tani K (2009) Role of syntaxin 18 in the organization of endoplasmic reticulum subdomains. J Cell Sci 122(Pt 10):1680–1690

    Article  PubMed  CAS  Google Scholar 

  • Jahn RC, Scheller RH (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7:631–643

    Article  PubMed  CAS  Google Scholar 

  • Kim SJ, Bassham DC (2011) TNO1 is involved in salt tolerance and vacuolar trafficking in Arabidopsis. Plant Physiol 156:514–526

    Article  PubMed  CAS  Google Scholar 

  • Kraynack BA, Chan A, Rosenthal E, Essid M, Umansky B, Waters MG, Schmitt HD (2005) Dsl1p, Tip20p, and the novel Dsl3(Sec39) protein are required for the stability of the Q/t–SNARE complex at the endoplasmic reticulum in yeast. Mol Biol Cell 16:3963–3677

    Article  PubMed  CAS  Google Scholar 

  • Lee CF, Pu HY, Wang LC, Sayler RJ, Yeh CH, Wu SJ (2006) Mutation in a homolog of yeast Vps53p accounts for the heat and osmotic hypersensitive phenotypes in Arabidopsis hit1-1 mutant. Planta 224:330–338

    Article  PubMed  CAS  Google Scholar 

  • Leshem Y, Melamed-Book N, Cagnac O, Ronen G, Nishri Y, Solomon M, Cohen G, Levine A (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Natl Acad Sci USA 103:18008–18013

    Article  PubMed  CAS  Google Scholar 

  • Lewis MJ, Pelham HR (1996) SNARE-mediated retrograde traffic from the Golgi complex to the endoplasmic reticulum. Cell 85:205–215

    Article  PubMed  CAS  Google Scholar 

  • Lewis MJ, Rayner JC, Pelham HR (1997) A novel SNARE complex implicated in vesicle fusion with the endoplasmic reticulum. EMBO J 16:3017–3024

    Article  PubMed  CAS  Google Scholar 

  • Leyman B, Geelen D, Quintero FJ, Blatt M (1999) A tobacco syntaxin with a role in hormonal control of guard cell ion channels. Science 283:537–540

    Google Scholar 

  • Li L, Shimada T, Takahashi H, Ueda H, Fukao Y, Kondo M, Nishimura M, Hara-Nishimura I (2006) MAIGO2 is involved in exit of seed storage proteins from the endoplasmic reticulum in Arabidopsis thaliana. Plant Cell 18:3535–3547

    Article  PubMed  CAS  Google Scholar 

  • Nakajima K, Hirose H, Taniguchi M, Kurashina H, Arasaki K, Nagahama M, Tani K, Yamamoto A, Tagaya M (2004) Involvement of BNIP1 in apoptosis and endoplasmic reticulum membrane fusion. EMBO J 23:3216–3226

    Article  PubMed  CAS  Google Scholar 

  • Perry RJ, Mast FD, Rachubinski RA (2009) Endoplasmic reticulum-associated secretory proteins Sec20p, Sec39p, and Dsl1p are involved in peroxisome biogenesis. Eukaryot Cell 8:830–843

    Article  PubMed  CAS  Google Scholar 

  • Reilly BA, Kraynack BA, VanRheenen SM, Waters MG (2001) Golgi-to-endoplasmic reticulum (ER) retrograde traffic in yeast requires Dsl1p, a component of the ER target site that interacts with a COPI coat subunit. Mol Biol Cell 12:3783–3796

    PubMed  CAS  Google Scholar 

  • Ren Y, Yip CK, Tripathi A, Huie D, Jeffrey PD, Walz T, Hughson FM (2009) A structure-based mechanism for vesicle capture by the multisubunit tethering complex Dsl1. Cell 139:1119–1129

    Article  PubMed  CAS  Google Scholar 

  • Sanderfoot AA, Assaad FF, Raikhel NV (2000) The Arabidopsis genome. An abundance of soluble N-ethylmaleimide sensitive factor adaptor protein receptors. Plant Physiol 124:1558–1569

    Article  PubMed  CAS  Google Scholar 

  • Schmitt HD (2010) Dsl1p/Zw10: common mechanisms behind tethering vesicles and microtubules. Trends Cell Biol 20:257–268

    Article  PubMed  CAS  Google Scholar 

  • Surpin M, Raikhel NV (2004) Traffic jams affect plant development and signal transduction. Nat Rev Mol Cell Biol 5:100–109

    Article  PubMed  CAS  Google Scholar 

  • Sweet DJ, Pelham HR (1992) The Saccharomyces cerevisiae SEC20 gene encodes a membrane glycoprotein which is sorted by the HDEL retrieval system. EMBO J 11:423–432

    PubMed  CAS  Google Scholar 

  • Sweet DJ, Pelham HR (1993) The TIP1 gene of Saccharomyces cerevisiae encodes an 80 kDa cytoplasmic protein that interacts with the cytoplasmic domain of Sec20p. EMBO J 12:2831–2840

    Google Scholar 

  • Sztul E, Lupashin V (2006) Role of tethering factors in secretory membrane traffic. Am J Physiol Cell Physiol 290:C11–C26

    Google Scholar 

  • Tamura K, Shimada T, Ono E, Tanaka Y, Nagatani A, Higashi SI, Watanabe M, Nishimura M, Hara-Nishimura I (2003) Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants. Plant J 35:545–555

    Article  PubMed  CAS  Google Scholar 

  • Tripathi A, Ren Y, Jeffrey PD, Hughson FM (2009) Structural characterization of Tip20p and Dsl1p, subunits of the Dsl1p vesicle tethering complex. Nat Struct Mol Biol 16:114–123

    Article  PubMed  CAS  Google Scholar 

  • Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 29:49–65

    Article  PubMed  CAS  Google Scholar 

  • Uemura T, Sato T, Aoki T, Yamamoto A, Okada T, Hirai R, Harada R, Mori K, Tagaya M, Harada A (2009) p31 deficiency influences endoplasmic reticulum tubular morphology and cell survival. Mol Cell Biol 29:1869–1881

    Article  PubMed  CAS  Google Scholar 

  • Vicient CM, Delseny M (1999) Isolation of total RNA from Arabidopsis thaliana seeds. Anal Biochem 268:412–413

    Article  PubMed  CAS  Google Scholar 

  • Wang LC, Tsai MC, Chang KY, Fan YS, Yeh CH, Wu SJ (2011) Involvement of the Arabidopsis HIT1/AtVPS53 tethering protein homologue in the acclimation of the plasma membrane to heat stress. J Exp Bot 62:3609–3620

    Article  PubMed  CAS  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  PubMed  CAS  Google Scholar 

  • Zhao P, Liu F, Ma M, Gong J, Wang Q, Jia P, Zheng GC, Liu H (2011) Overexpression of AtLEA3-3 confers resistance to cold stress to Escherichia coli and provides enhanced osmotic stress tolerance and ABA sensitivity in Arabidopsis thaliana. Mol Biol (Mosk) 45:851–862

    Google Scholar 

  • Zhao P, Liu F, Zhang B, Liu X, Wang B, Gong J, Yu G, Ma M, Lu Y, Sun J, Wang Z, Jia P, Liu H (2012) MAIGO2 is involved in abscisic acid-mediated response to abiotic stresses and Golgi-to-ER retrograde transport. Physiol Plant. doi:10.1111/j.1399-3054.2012.01704.x

    Google Scholar 

  • Zhou ZY, Zhang CG, Wu L, Zhang CG, Chai J, Wang M, Jha A, Jia PF, Cui SJ, Yang M, Chen R, Guo GQ (2011) Functional characterization of the CKRC1/TAA1 gene and dissection of hormonal actions in the Arabidopsis root. Plant J 66:516–527

    Article  PubMed  CAS  Google Scholar 

  • Zhu JH, Gong ZZ, Zhang CQ, Song CP, Damsz B, Inan G, Koiwa H, Zhu JK, Hasegawa PM, Bressan RA (2002) OSM1/SYP61: a syntaxin protein in Arabidopsis controls abscisic acid-mediated and non-abscisic acid-mediated responses to abiotic stress. Plant Cell 14:3009–3028

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Ian Moore (University of Oxford) for providing plasmid pVKHEn6-GFP-HDEL; Dr. Ikuko Hara-Nishimura (Kyoto University) for providing sp-GFP-2SC/pBI221, sp-GFP-CTPP/pBI221, sp-NTPP-GFP/pBI221 plasmids and transgenic seeds sp-GFP-2SC/pBI121, and Dr. Zhaoyang Zhou and Qianqian Qin for providing ethylene (Zhou et al. 2011) and GA signal homozygous mutants. This work was supported by National Natural Science Foundation of China (No. 30771091, 30970234, and 41201048) and the Program for New Century Excellent Talents in University (NCET-11-0212) by the Ministry of Education to H. L. (2011), by Grant 29Y127E71 from the “One Hundred Talents” Project of the Chinese Academy of Sciences, and by the Foundation for Excellent Youth Scholars of CAREERI, CAS (51Y251A11).

Author information

Authors and Affiliations

  1. Key Laboratory of Stress Physiology and Ecology in Cold and Arid Regions, Gansu Province, Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences, Donggang West Road 320, Lanzhou, 730000, People’s Republic of China

    Pengshan Zhao

  2. Institute of Cell Biology, Life Sciences School, Lanzhou University, 222# Tianshui Nan Lu, Lanzhou, 730000, People’s Republic of China

    Pengshan Zhao, Fei Liu, Bing Wang, Guanzhong Yu, Pengfei Jia & Heng Liu

Authors
  1. Pengshan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guanzhong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pengfei Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Pengshan Zhao or Heng Liu.

Additional information

Communicated by J.-H. Liu.

P. Zhao and F. Liu contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1 Phenotypes of the wt and sec20 plants with or without treatments at 7 day after stratification. Photographs were taken at the end of treatments.

Fig. S2 Expression patterns of AtSec20 in the ABA, GA, and ethylene signal mutants. RNA was isolate from 7 d-old plants. Transcript levels were measured by real-time RT-PCR, and actin2 was used as an internal control. The expression levels in Col 0 and Ler were designated as a value 1. Data represent the mean ± SD. Bars with different letters were significantly different at the 0.01 level.

Supplementary material 1 (JPEG 1.47 mb)

Supplementary material 2 (JPEG 283 kb)

Supplementary material 3 (DOC 35 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, P., Liu, F., Wang, B. et al. AtSec20 is involved in osmotic stress tolerance and AtSec20 mutation unaffects the integrity of intracellular organelles and the anterograde biosynthetic trafficking. Acta Physiol Plant 35, 1625–1632 (2013). https://doi.org/10.1007/s11738-012-1205-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-012-1205-6

Keywords

Search

Navigation