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A role for the endoplasmic reticulum in the cell-to-cell movement of SHORT-ROOT

Abstract

Plasmodesmata enable the trafficking of various signaling molecules, as well as viruses that exploit these channels for their intercellular movement. Viral movement relies on the endoplasmic reticulum (ER), which serves as a stable platform for the assembly of viral replication complexes and their subsequent shuttling toward plasmodesmata. The role of the ER in the intercellular movement of endogenous proteins is less clear. In the root meristem, the mobile transcription factor SHORT-ROOT (SHR) traffics between cell layers to regulate root radial patterning and differentiation. Movement of SHR is a regulated process that requires several cellular factors including the endomembrane system, intact microtubules and an endosome-associated protein named SHR-interacting-embryonic-lethal (SIEL). Recently, we found that KINESIN G (KinG) interacts with both SIEL and microtubules to support the cell-to-cell movement of SHR. Here, we provide evidence that both SHR-associated endosomes and KinG localize to the endoplasmic reticulum (ER) and that movement of SHR-associated endosomes occurs on the ER. Moreover, we show that compromised ER structure leads to a reduction in the cell-to-cell movement of SHR. Collectively, these results support the hypothesis that the ER plays a role in SHR movement.

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References

  • Boyko V, Hu Q, Seemanpillai M, Ashby J, Heinlein M (2007) Validation of microtubule-associated tobacco mosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 51:589–603

    Article  CAS  PubMed  Google Scholar 

  • Brunkard JO, Runkel AM, Zambryski PC (2015) The cytosol must flow: intercellular transport through plasmodesmata. Curr Opin Cell Biol 35:3–20

    Article  CAS  Google Scholar 

  • Gallagher KL, Paquette AJ, Nakajima K, Benfey PN (2004) Mechanisms regulating SHORT-ROOT intercellular movement. Curr Biol 14:1847–1851

    Article  CAS  PubMed  Google Scholar 

  • Goodin MM, Dietzgen RG, Schichnes D, Ruzin S, Jackson AO (2002) pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J 31:375–383

    Article  CAS  PubMed  Google Scholar 

  • Hamada T, Tominaga M, Fukaya T, Nakamura M, Nakano A, Watanabe Y, Hashimoto T, Baskin TI (2012) RNA processing bodies, peroxisomes, Golgi bodies, mitochondria, and endoplasmic reticulum tubule junctions frequently pause at cortical microtubules. Plant Cell Physiol 53:699–708

    Article  CAS  PubMed  Google Scholar 

  • Heinlein M (2015) Plant virus replication and movement. Virology 479:657–671

    Article  CAS  PubMed  Google Scholar 

  • Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci U S A 101:6291–6296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koizumi K, Wu S, MacRae-Crerar A, Gallagher KL (2011) An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr Biol 21:1559–1564

    Article  CAS  PubMed  Google Scholar 

  • Kragler F (2013) Plasmodesmata: intercellular tunnels facilitating transport of macromolecules in plants. Cell Tissue Res 352:49–58

    Article  CAS  PubMed  Google Scholar 

  • Levy A, Zheng JY, Lazarowitz SG (2015) Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr Biol 25(15):2018–2025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis JD, Lazarowitz SG (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. PNAS 107(6):2491–2496

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu C, Nelson RS (2013) The cell biology of tobacco mosaic virus replication and movement. Front Plant Sci 4:12

    PubMed  PubMed Central  Google Scholar 

  • Mittelbrunn M, Sánchez-Madrid F (2012) Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 13:328–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311

    Article  CAS  PubMed  Google Scholar 

  • Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136

    Article  CAS  PubMed  Google Scholar 

  • Oparka KJ (2004) Getting the message across: how do plant cells exchange macromolecular complexes? Trends Plant Sci 9:33–41

    Article  CAS  PubMed  Google Scholar 

  • Pitzalis N, Heinlein M (2017) The roles of membranes and associated cytoskeleton in plant virus replication and cell-to-cell movement. J Exp Bot 69:117–132

    Article  CAS  PubMed  Google Scholar 

  • Sambade A, Brandner K, Hofmann C, Seemanpillai M, Mutterer J, Heinlein M (2008) Transport of TMV movement protein particles associated with the targeting of RNA to plasmodesmata. Traffic 9:2073–2088

    Article  PubMed  Google Scholar 

  • Spiegelman Z, Lee CM, Gallagher KL (2018) KinG is a plant-specific kinesin that regulates both intra-and intercellular movement of SHORT-ROOT. Plant Physiol 176:392–405

    Article  CAS  PubMed  Google Scholar 

  • Stefano G, Renna L, Moss T, McNew JA, Brandizzi F (2012) In Arabidopsis, the spatial and dynamic organization of the endoplasmic reticulum and Golgi apparatus is influenced by the integrity of the C-terminal domain of RHD3, a non-essential GTPase. Plant J 69:957–966

    Article  CAS  PubMed  Google Scholar 

  • Stefano G, Renna L, Lai Y, Slabaugh E, Mannino N, Buono RA, Otegui MS, Brandizzi F (2015) ER network homeostasis is critical for plant endosome streaming and endocytosis. Cell Discov 1:15033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Norman JM, Breakfield NW, Benfey PN (2011) Intercellular communication during plant development. Plant Cell 23:855–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu S, Gallagher KL (2012) Transcription factors on the move. Current Opin Plant Biol 15:645–651

    Article  CAS  Google Scholar 

  • Wu S, Gallagher KL (2013) Intact microtubules are required for the intercellular movement of the SHORT-ROOT transcription factor. Plant J 74:148–159

    Article  CAS  PubMed  Google Scholar 

  • Wu S, Gallagher KL (2014) The movement of the non-cell-autonomous transcription factor, SHORT-ROOT relies on the endomembrane system. Plant J 80:396–409

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Sondra G. Lazarowitz and Dr. Federica Brandizzi for sharing material used in this manuscript.

Funding

Z.S. was partially supported by the National Science Foundation Grant 1243945 awarded to K.L.G. Z.S. was partially supported by BARD, the United States–Israel Binational Agricultural Research and Development Fund, Vaadia-BARD Postdoctoral Fellowship Award FI-525-2015.

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Correspondence to Ziv Spiegelman or Kimberly L. Gallagher.

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The authors declare no conflict of interest.

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Spiegelman, Z., Wu, S. & Gallagher, K.L. A role for the endoplasmic reticulum in the cell-to-cell movement of SHORT-ROOT. Protoplasma 256, 1455–1459 (2019). https://doi.org/10.1007/s00709-019-01369-z

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  • DOI: https://doi.org/10.1007/s00709-019-01369-z

Keywords

  • Plasmodesmata
  • Intercellular trafficking
  • Synaptotagmin a
  • Golgi movement 8
  • Kinesin G
  • SHORT-ROOT
  • Endoplasmic reticulum
  • Cell-to-cell movement