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Long-Distance Signaling by Small RNAs

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Short and Long Distance Signaling

Part of the book series: Advances in Plant Biology ((AIPB,volume 3))

Abstract

The phloem is known as the main conduit for assimilates synthesized during photosynthesis, but also spreads signals coordinating important developmental decisions and physiological responses between plant organs. Among the wealth of potential signaling molecules, RNAs have outstanding potential, because they allow the transmission of sequence-specific information. Moreover, especially small RNAs in the size range of 20–26 nucleotides are likely to be phloem-mobile due to their small size. While RNAs were found to be absent from xylem sap, sieve elements seem to be a suitable route for RNA transport, since phloem samples have been shown to be free of RNase activity that could compromise RNA quality. Recently, a large number of small RNAs including micro (mi) and short interfering (si) RNAs have been identified in phloem samples what fueled the speculation that they could be long-distance information transmitters. However, that they can really be translocated through the phloem in vivo could so far only been demonstrated for siRNAs and a small number of miRNAs. siRNA translocation is thought to be essential for the plant-wide transmission of silencing of aberrant endogenous, viral- or transgene-derived RNAs. In contrast, the three miRNAs for which phloem mobility could as yet be verified are involved in tuber development (miR172) or nutrient deprivation responses (miR395 and miR399). Future experiments will be required to show whether additional small RNAs with distinct functions can also travel through the phloem or not.

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References

  • Alosi MC, Melroy DL, Park RB (1988) The regulation of gelation of phloem exudate from Cucurbita fruit by dilution, glutathione, and glutathione reductase. Plant Physiol 86:1089–1094

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Atkins CA, Smith PMC (2007) Translocation in legumes: assimilates, nutrients, and signaling molecules. Plant Physiol 144:550–561

    Article  PubMed  CAS  Google Scholar 

  • Aung K, Lin S, Wu C, Huang Y, Su C, Chiou T (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 

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

    Article  PubMed  CAS  Google Scholar 

  • Barnes A, Bale J, Constantinidou C, Ashton P, Jones A, Pritchard J (2004) Determining protein identity from sieve element sap in Ricinus communis L. by quadrupole time of flight (Q-TOF) mass spectrometry. J Exp Bot 55:1473–1481

    Article  PubMed  CAS  Google Scholar 

  • Bose JC (1947) Plants and their autographs. Longman Green & Co, London, p 154

    Google Scholar 

  • Brandt S, Kehr J, Walz C, Imlau A, Willmitzer L, Fisahn J (1999) A rapid method for detection of plant gene transcripts from single epidermal, mesophyll and campanion cells of intact leaves. Plant J 20:245–250

    Article  PubMed  CAS  Google Scholar 

  • Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749

    Article  PubMed  CAS  Google Scholar 

  • Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64

    Article  PubMed  Google Scholar 

  • Chailakhyan MK (1936) New facts in support of the hormonal theory of plant development. C. R. (Doklady) Acad. Sci URSS 13:79–83

    Google Scholar 

  • Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30: 323–332

    Article  PubMed  CAS  Google Scholar 

  • Dinant S, Bonnemain JL, Girousse C, Kehr J (2010) Phloem sap intricacy and interplay with aphid feeding. C R Biol 333:504–515

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Doering-Saad C, Newbury HJ, Couldridge CE, Bale JS, Pritchard J (2006) A phloem-enriched cDNA library from Ricinus: insights into phloem function. J Exp Bot 57:3183–3193

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Dunoyer P, Brosnan CA, Schott G, Wang Y, Jay F, Alioua A, Himber C, Voinnet O (2010a) An endogenous, systemic RNAi pathway in plants. EMBO J 29:1699–1712

    Article  PubMed  CAS  Google Scholar 

  • Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010b) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328:912–916

    Article  PubMed  CAS  Google Scholar 

  • Fisher DB, Frame JM (1984) A guide to the use of the exuding-stylet technique in phloem physiology. Planta 161:385–393

    Article  Google Scholar 

  • Fisher DB, Wu Y, Ku MSB (1992) Turnover of soluble proteins in the wheat sieve tube. Plant Physiol 100:1433–1441

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Gaupels F, Buhtz A, Knauer T, Deshmukh S, Waller F, van Bel AJE (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 

  • Giavalisco P, Kapitza K, Kolasa A, Buhtz A, Kehr J (2006) Towards the proteome of Brassica napus phloem sap. Proteomics 6:896–909

    Article  PubMed  CAS  Google Scholar 

  • Gomez G, Pallas V (2004) A long-distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with Hop Stunt Viroid RNA. J Virol 78:10104–10110

    Article  PubMed  CAS  Google Scholar 

  • Gomez G, Torres H, Pallas V (2005) Identification of translocatable RNA-binding phloem proteins from melon, potential components of the long-distance RNA transport system. Plant J 41: 107–116

    Article  PubMed  CAS  Google Scholar 

  • Ham BK, Brandom JL, Xoconostle-Cazares B, Ringgold V, Lough TJ, Lucas WJ (2009) A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex. Plant Cell 21:197–215

    Article  PubMed  CAS  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952

    Article  PubMed  CAS  Google Scholar 

  • Haywood V, Kragler F, Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14:S303–S325

    PubMed  CAS  Google Scholar 

  • Haywood V, Yu T, Huang N, 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 

  • 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 

  • Hoffmann-Benning S, Gage DA, McIntosh L, Kende H, Zeevaart JAD (2002) Comparison of peptides in the phloem sap of flowering and non-flowering Perilla and lupine plants using microbore HPLC followed by matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry. Planta 216:140–147

    Article  PubMed  CAS  Google Scholar 

  • Irion U, St JD (2007) bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445:554–558

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  PubMed  CAS  Google Scholar 

  • Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MCP (2004) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88

    Article  PubMed  CAS  Google Scholar 

  • Kasai A, Kanehira A, Harada T (2010) miR172 can move long distances in Nicotiana benthamiana. Open Plant Sci J 4:1–6

    CAS  Google Scholar 

  • Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321

    Article  PubMed  CAS  Google Scholar 

  • Kehr J (2006) Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J Exp Bot 57:767–774

    Article  PubMed  CAS  Google Scholar 

  • Kehr J (2009) Long-distance transport of macromolecules through the phloem. F1000 Biol Rep 1, 31

    Google Scholar 

  • 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 

  • Kennedy JS, Mittler TE (1953) A method of obtaining phloem sap via the mouth parts of aphids. Nature 171:528

    Article  Google Scholar 

  • Kim I, Pai H (2009) Mobile macromolecules in plant development. J Plant Biol 52:186–192

    Article  Google Scholar 

  • King RW, Zeevaart JAD (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53:96–103

    Article  PubMed  CAS  Google Scholar 

  • Knoblauch M, van Bel AJE (1998) Sieve tubes in action. Plant Cell 10:35–50

    Article  CAS  Google Scholar 

  • Kollmann R, Dörr I, Kleinig H (1970) Protein filaments – structural components of the phloem exudate. Planta 95:86–94

    Article  CAS  Google Scholar 

  • Kragler F (2010) RNA in the phloem: a crisis or a return on investment? Plant Sci 178:99–104

    Article  CAS  Google Scholar 

  • Lee J, Cui W (2009) Non-cell autonomous RNA trafficking and long-distance signaling. J Plant Biol 52:10–18

    Article  CAS  Google Scholar 

  • Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Fu Y, Ji L, Wu C, Zheng C (2010) Characterization and expression analysis of the Arabidopsis mir169 family. Plant Sci 178:271–280

    Article  CAS  Google Scholar 

  • Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980–1983

    Article  PubMed  CAS  Google Scholar 

  • Lucas WJ, Yoo B, 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 

  • Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14:1035–1046

    Article  PubMed  CAS  Google Scholar 

  • Marentes E, Grusak MA (1998) Mass determination of low-molecular-weight proteins in phloem sap using matrix-assisted laser desorption/ionization time of flight mass spectrometry. J Exp Bot 49:903–911

    Article  CAS  Google Scholar 

  • Martin A, Adam H, Díaz-Mendoza M, Zurczak M, González-Schain ND, Suárez-López P (2009) Graft-transmissible induction of potato tuberization by the microRNA miR172. Development 136:2873–2881

    Article  PubMed  CAS  Google Scholar 

  • Martinez G, Donaire L, Llave C, Pallas V, Gomez G (2010) High-throughput sequencing of Hop stunt viroid-derived small RNAs from cucumber leaves and phloem. Mol Plant Pathol 11: 347–359

    Article  PubMed  CAS  Google Scholar 

  • Meng Y, Ma X, Chen D, Wu P, Chen M (2010) MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun 393:345–349

    Article  PubMed  CAS  Google Scholar 

  • Milburn JA (1970) Phloem exudation from castor bean: induction by massage. Planta 95: 272–276

    Article  Google Scholar 

  • Mlotshwa S, Voinnet O, Mette MF, Matzke M, Vaucheret H, Ding SW, Pruss G, Vance VB (2002) RNA silencing and the mobile silencing signal. Plant Cell 14:S289–301

    Article  PubMed  CAS  Google Scholar 

  • Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328: 872–875

    Article  PubMed  CAS  Google Scholar 

  • Müller M, Heuck A, Niessing D (2007) Directional mRNA transport in eukaryotes: lessons from yeast. Cell Mol Life Sci 64:171–180

    Article  PubMed  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Palauqui J, Elmayan T, Pollien J, 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 

  • 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 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible W (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150: 1541–1555

    Article  PubMed  Google Scholar 

  • Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18:2237–2242

    Article  PubMed  CAS  Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12: 1484–1495

    Article  PubMed  CAS  Google Scholar 

  • Raps A, Kehr J, Gugerli P, Moar WJ, Bigler F, Hilbeck A (2001) Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol Ecol 10:525–533

    Article  PubMed  CAS  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Medrano R, Xoconostle-Cázares 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 

  • Sasaki T, Chino M, Hayashi H, Fujiwara T (1998) Detection of several mRNA species in rice phloem sap. Plant Cell Physiol 39:895–897

    PubMed  CAS  Google Scholar 

  • Sessions A, Yanofsky MF, Weigel D (2000) Cell-cell signaling and movement by the floral ­transcription factors LEAFY and APETALA1. Science 289:779–781

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Zhu JK (2007) Micro RNAs and short-interfering RNAs in plants. J Integr Plant Biol 49:817–826

    Article  CAS  Google Scholar 

  • Tomilov AA, Tomilova NB, Wroblewski T, Michelmore R, Yoder JI (2008) Trans-specific gene silencing between host and parasitic plants. Plant J 56:389–397

    Article  PubMed  CAS  Google Scholar 

  • Tournier B, Tabler M, Kalantidis K (2006) Phloem flow strongly influences the systemic spread of silencing in GFP Nicotiana benthamiana plants. Plant J 47:383–394

    Article  PubMed  CAS  Google Scholar 

  • Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–221

    Article  PubMed  CAS  Google Scholar 

  • Valoczi A, Varallyay E, Kauppinen S, Burgyan J, Havelda Z (2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J 47:140–151

    Article  PubMed  CAS  Google Scholar 

  • Varkonyi-Gasic E, Gould N, Sandanayaka M, Sutherland P, MacDiarmid RM (2010) Characterisation of microRNAs from apple (Malus domestica ‘Royal Gala’) vascular tissue and phloem sap. BMC Plant Biol 10:159

    Article  PubMed  Google Scholar 

  • Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutierrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:4477–4482

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O, Baulcombe DC (1997) Systemic signalling in gene silencing. Nature 389:553–553

    Article  PubMed  CAS  Google Scholar 

  • Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J (2004) Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65:1795–1804

    Article  PubMed  CAS  Google Scholar 

  • Waterhouse PM, Wang M, Lough T (2001) Gene silencing as an adaptive defence against viruses. Nature 411:834–842

    Article  PubMed  CAS  Google Scholar 

  • Xoconostle-Cazares B, Xiang Y, Ruiz-Medrano R, Wang HL, Monzer J, Yoo BC, McFarland KC, Franceschi VR, Lucas WJ (1999) Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283:94–98

    Article  PubMed  CAS  Google Scholar 

  • Yoo B, 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 

  • Zhang S, Sun L, Kragler F (2009) The phloem-delivered RNA pool contains small noncoding RNAs and interferes with translation. Plant Physiol 150:378–387

    Article  PubMed  CAS  Google Scholar 

  • Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29

    Article  PubMed  Google Scholar 

  • Zhu X, Shaw PN, Pritchard J, Newbury J, Hunt EJ, Barrett DA (2005) Amino acid analysis by micellar electrokinetic chromatography with laser-induced fluorescence detection: application to nanolitre-volume biological samples from Arabidopsis thaliana and Myzus persicae. Electrophoresis 26:911–919

    Article  PubMed  CAS  Google Scholar 

  • Ziegler H, Kluge M (1962) Die Nucleinsäuren und ihre Bausteine im Siebröhrensaft von Robinia pseudoacacia L. Planta 58:144–153

    Article  CAS  Google Scholar 

  • Zimmermann MH, Ziegler H (1975) List of sugars and sugar alcohols in sieve-tube exudates. In: Zimmermann MH, Milburn JA (eds) Encyclopedia of plant physiology, vol 1. Springer, Berlin, pp 480–503

    Google Scholar 

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Acknowledgments

The author is grateful for the financial support from the Spanish Ministry of Science and Innovation (MICINN, grant BIO2008-03432 and the I3 program).

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Kehr, J. (2012). Long-Distance Signaling by Small RNAs. In: Kragler, F., Hülskamp, M. (eds) Short and Long Distance Signaling. Advances in Plant Biology, vol 3. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1532-0_6

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