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Non-cell Autonomous RNA Trafficking and Long-Distance Signaling

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Abstract

A wide range of proteins and RNA molecules in plants have been recently identified as non-cell autonomous, phloem-mobile molecules and suggested to play important roles in physiological and developmental processes. Systemic movement of both protein-coding mRNAs and non-coding small RNAs is shown to correlate with the epigenetic changes brought about across grafting junctions, supporting their potential roles as long-distance signaling molecules. Plants appear to have evolved this unique RNA-based signaling mechanism to control systemic regulation of various responses to environmental stimuli and challenges such as photoperiods, nutrient availabilities, and pathogen attacks. This mechanism may have been exploited by viroids, non-coding RNA pathogens, to spread infection cell to cell and through phloem. A model describing potential molecular mechanisms by which the systemic RNA trafficking occurs will be presented.

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References

  1. Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151

    Article  PubMed  CAS  Google Scholar 

  2. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    Article  PubMed  CAS  Google Scholar 

  3. Banerjee AK, Chatterjee M, Yu Y, Suh SG, Miller WA, Hannapel DJ (2006) Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18:3443–3457

    Article  PubMed  CAS  Google Scholar 

  4. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  PubMed  CAS  Google Scholar 

  5. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  PubMed  CAS  Google Scholar 

  6. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  PubMed  CAS  Google Scholar 

  7. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280

    Article  PubMed  CAS  Google Scholar 

  8. Brosnan CA, Mitter N, Christie M, Smith NA, Waterhouse PM, Carroll BJ (2007) Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proc Natl Acad Sci U S A 104:14741–14746

    Article  PubMed  CAS  Google Scholar 

  9. Daros JA, Elena SF, Flores R (2006) Viroids: an Ariadne’s thread into the RNA labyrinth. EMBO Rep 7:593–598

    Article  PubMed  CAS  Google Scholar 

  10. Deeken R, Ache P, Kajahn I, Klinkenberg J, Bringmann G, Hedrich R (2008) Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. Plant J 55:746–759

    Article  PubMed  CAS  Google Scholar 

  11. Ding B, Itaya A, Qi YJ (2003) Symplasmic protein and RNA traffic: regulatory points and regulatory factors. Curr Opin Plant Biol 6:596–602

    Article  PubMed  CAS  Google Scholar 

  12. Doering-Saad C, Newbury HJ, Bale JS, Pritchard J (2002) Use of aphid stylectomy and RT-PCR for the detection of transporter mRNAs in sieve elements. J Exp Bot 53:631–637

    Article  PubMed  CAS  Google Scholar 

  13. Dunoyer P, Himber C, Ruiz-Ferrer V, Alioua A, Voinnet O (2007) Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat Genet 39:848–856

    Article  PubMed  CAS  Google Scholar 

  14. Dunoyer P, Himber C, Voinnet O (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 37:1356–1360

    Article  PubMed  CAS  Google Scholar 

  15. Dunoyer P, Voinnet O (2008) Mixing and matching: the essence of plant systemic silencing. Trends Genet 24:151–154

    Article  PubMed  CAS  Google Scholar 

  16. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight. Nat Rev Genet 9:102–114

    Article  PubMed  CAS  Google Scholar 

  17. Foster TM, Lough TJ, Emerson SJ, Lee RH, Bowman JL, Forster RLS, Lucas WJ (2002) A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14:1497–1508

    Article  PubMed  CAS  Google Scholar 

  18. Gaupels F, Buhtz A, Knauer T, Deshmukh S, Waller F, van Bel AJ, Kogel KH, Kehr J (2008) Adaptation of aphid stylectomy for analyses of proteins and mRNAs in barley phloem sap. J Exp Bot 59:3297–3306

    Article  PubMed  CAS  Google Scholar 

  19. Hammond RW (1994) Agrobacterium-mediated inoculation of PSTVd cDNAs onto tomato reveals the biological effect of apparently lethal mutations. Virology 201:36–45

    Article  PubMed  CAS  Google Scholar 

  20. Haywood V, Yu TS, Huang NC, Lucas WJ (2005) Phloem long-distance trafficking of Gibberellic acid-insensitive RNA regulates leaf development. Plant J 42:49–68

    Article  PubMed  CAS  Google Scholar 

  21. Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. Embo J 22:4523–4533

    Article  PubMed  CAS  Google Scholar 

  22. Jackson D (2001) The long and the short of it: Signaling development through plasmodesmata. Plant Cell 13:2569–2572

    Article  PubMed  CAS  Google Scholar 

  23. Kehr J, Buhtz A (2008) Long distance transport and movement of RNA through the phloem. J Exp Bot 59:85–92

    Article  PubMed  CAS  Google Scholar 

  24. Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293:287–289

    Article  PubMed  CAS  Google Scholar 

  25. Kuhn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997) Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275:1298–1300

    Article  PubMed  CAS  Google Scholar 

  26. Kuhn C, Quick WP, Schulz A, Riesmeier JW, Sonnewald U, Frommer WB (1996) Companion cell-specific inhibition of the potato sucrose transporter SUT1. Plant Cell Environ 19:1115–1123

    Article  Google Scholar 

  27. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    Article  PubMed  CAS  Google Scholar 

  28. Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232

    Article  PubMed  CAS  Google Scholar 

  29. Lucas WJ, Lee JY (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712–726

    Article  PubMed  CAS  Google Scholar 

  30. Lucas WJ, Yoo BC, Kragler F (2001) RNA as a long-distance information macromolecule in plants. Nat Rev Mol Cell Biol 2:849–857

    Article  PubMed  CAS  Google Scholar 

  31. Omid A, Keilin T, Glass A, Leshkowitz D, Wolf S (2007) Characterization of phloem-sap transcription profile in melon plants. J Exp Bot 58:3645–3656

    Article  PubMed  CAS  Google Scholar 

  32. Oparka KJ, Cruz SS (2000) The great escape: phloem transport and unloading of macromolecules. Annu Rev Plant Physiol Plant Mol Biol 51:323–347

    Article  PubMed  CAS  Google Scholar 

  33. Oparka KJ, Turgeon R (1999) Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell 11:739–750

    Article  PubMed  CAS  Google Scholar 

  34. Palauqui JC, Elmayan T, Pollien JM, Vaucheret H (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. Embo J 16:4738–4745

    Article  PubMed  CAS  Google Scholar 

  35. Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738

    Article  PubMed  CAS  Google Scholar 

  36. Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205

    Article  PubMed  CAS  Google Scholar 

  37. Qi Y, Pelissier T, Itaya A, Hunt E, Wassenegger M, Ding B (2004) Direct role of a viroid RNA motif in mediating directional RNA trafficking across a specific cellular boundary. Plant Cell 16:1741–1752

    Article  PubMed  CAS  Google Scholar 

  38. Roberts AG, Oparka KJ (2003) Plasmodesmata and the control of symplastic transport. Plant Cell Environ 26:103–124

    Article  Google Scholar 

  39. Ruiz-Medrano R, Xoconostle-Cazares B, Lucas WJ (1999) Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126:4405–4419

    PubMed  CAS  Google Scholar 

  40. Ruiz-Medrano R, Xoconostle-Cazares B, Lucas WJ (2001) The phloem as a conduit for inter-organ communication. Curr Opin Plant Biol 4:202–209

    Article  PubMed  CAS  Google Scholar 

  41. Schmitt B, Stadler R, Sauer N (2008) Immunolocalization of solanaceous SUT1 proteins in companion cells and xylem parenchyma: new perspectives for phloem loading and transport. Plant Physiol 148:187–199

    Article  PubMed  CAS  Google Scholar 

  42. Tsiantis M (2001) Control of shoot cell fate: beyond homeoboxes. Plant Cell 13:733–738

    Article  PubMed  CAS  Google Scholar 

  43. Voinnet O (2005a) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220

    Article  PubMed  CAS  Google Scholar 

  44. Voinnet O (2005b) Non-cell autonomous RNA silencing. FEBS Lett 579:5858–5871

    Article  PubMed  CAS  Google Scholar 

  45. Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, Lough TJ, Lucas WJ (2004) A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000

    Article  PubMed  CAS  Google Scholar 

  46. Zambryski P, Crawford K (2000) Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Ann Rev Cell Dev Biol 16:393–421

    Article  CAS  Google Scholar 

  47. Zhong X, Archual AJ, Amin AA, Ding B (2008) A genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 20:35–47

    Article  PubMed  CAS  Google Scholar 

  48. Zhong X, Leontis N, Qian S, Itaya A, Qi Y, Boris-Lawrie K, Ding B (2006) Tertiary structural and functional analyses of a viroid RNA motif by isostericity matrix and mutagenesis reveal its essential role in replication. J Virol 80:8566–8581

    Article  PubMed  CAS  Google Scholar 

  49. Zhong X, Tao X, Stombaugh J, Leontis N, Ding B (2007) Tertiary structure and function of an RNA motif required for plant vascular entry to initiate systemic trafficking. Embo J 26:3836–3846

    Article  PubMed  CAS  Google Scholar 

  50. Zhu Y, Green L, Woo YM, Owens R, Ding B (2001) Cellular basis of potato spindle tuber viroid systemic movement. Virology 279:69–77

    Article  PubMed  CAS  Google Scholar 

  51. Zhu YL, Qi YJ, Xun Y, Owens R, Ding B (2002) Movement of potato spindle tuber viroid reveals regulatory points of phloem-mediated RNA traffic. Plant Physiol 130:138–146

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We apologize to our colleagues whose important works could not be directly cited in this review due to the page limitations. We appreciate Lee lab members R. Sager and F. Pan for proofreading this manuscript and for helpful suggestions, respectively. This work was supported by the National Science Foundation (grant no. MCB 0445626 to J.-Y. L.).

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Correspondence to Jung-Youn Lee.

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Lee, JY., Cui, W. Non-cell Autonomous RNA Trafficking and Long-Distance Signaling. J. Plant Biol. 52, 10–18 (2009). https://doi.org/10.1007/s12374-008-9001-y

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