1932

Abstract

There is now a wealth of data, from different plants and labs and spanning more than two decades, which unequivocally demonstrates that RNAs can be transported over long distances, from the cell where they are transcribed to distal cells in other tissues. Different types of RNA molecules are transported, including micro- and messenger RNAs. Whether these RNAs are selected for transport and, if so, how they are selected and transported remain, in general, open questions. This aspect is likely not independent of the biological function and relevance of the transported RNAs, which are in most cases still unclear. In this review, we summarize the experimental data supporting selectivity or nonselectivity of RNA translocation and review the evidence for biological functions. After discussing potential issues regarding the comparability between experiments, we propose criteria that need to be critically evaluated to identify important signaling RNAs.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-070121-033601
2022-05-20
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/arplant/73/1/annurev-arplant-070121-033601.html?itemId=/content/journals/10.1146/annurev-arplant-070121-033601&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alakonya A, Kumar R, Koenig D, Kimura S, Townsley B et al. 2012. Interspecific RNA interference of SHOOT MERISTEMLESS-like disrupts Cuscuta pentagona plant parasitism. Plant Cell 24:3153–66
    [Google Scholar]
  2. 2.
    Amsbury S, Kirk P, Benitez-Alfonso Y. 2017. Emerging models on the regulation of intercellular transport by plasmodesmata-associated callose. J. Exp. Bot. 69:105–15
    [Google Scholar]
  3. 3.
    Aoki K, Suzui N, Fujimaki S, Dohmae N, Yonekura-Sakakibara K et al. 2005. Destination-selective long-distance movement of phloem proteins. Plant Cell 17:944–56
    [Google Scholar]
  4. 4.
    Banerjee AK, Chatterjee M, Yu Y, Suh S-G, Miller WA, Hannapel DJ. 2006. Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18:3443–57
    [Google Scholar]
  5. 5.
    Bartusch K, Melnyk CW. 2020. Insights into plant surgery: an overview of the multiple grafting techniques for Arabidopsis thaliana. Front. Plant Sci. 11:613442
    [Google Scholar]
  6. 6.
    Bennett CW. 1940. Acquisition and transmission of viruses by dodder (Cuscuta subinclusa). Phytopathology 30:2
    [Google Scholar]
  7. 7.
    Bennett CW. 1944. Studies of dodder transmission of plant viruses. Phytopathology 34:905–32
    [Google Scholar]
  8. 8.
    Bhogale S, Mahajan AS, Natarajan B, Rajabhoj M, Thulasiram HV, Banerjee AK. 2014. MicroRNA156: A potential graft-transmissible microRNA that modulates plant architecture and tuberization in Solanum tuberosum ssp. andigena. Plant Physiol 164:1011–27
    [Google Scholar]
  9. 9.
    Bohnsack KE, Höbartner C, Bohnsack MT. 2019. Eukaryotic 5-methylcytosine (m5C) RNA methyltransferases: mechanisms, cellular functions, and links to disease. Genes 10:102
    [Google Scholar]
  10. 10.
    Branco R, Masle J. 2019. Systemic signalling through translationally controlled tumour protein controls lateral root formation in Arabidopsis. J. Exp. Bot. 70:3927–40
    [Google Scholar]
  11. 11.
    Buhtz A, Pieritz J, Springer F, Kehr J. 2010. Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64
    [Google Scholar]
  12. 12.
    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 53:739–49Identification of miRNAs in phloem sap as nutrient starvation signals in Brassicanapus.
    [Google Scholar]
  13. 13.
    Burch-Smith TM, Zambryski PC 2012. Plasmodesmata paradigm shift: regulation from without versus within. Annu. Rev. Plant Biol. 63:239–60
    [Google Scholar]
  14. 14.
    Calderwood A, Kopriva S, Morris RJ 2016. Transcript abundance explains mRNA mobility data in Arabidopsis thaliana. Plant Cell 28:610–15
    [Google Scholar]
  15. 15.
    Cho SK, Sharma P, Butler NM, Kang I-H, Shah S et al. 2015. Polypyrimidine tract-binding proteins of potato mediate tuberization through an interaction with StBEL5 RNA. J. Exp. Bot. 66:6835–47
    [Google Scholar]
  16. 16.
    Dalmadi Á, Gyula P, Bálint J, Szittya G, Havelda Z. 2019. AGO-unbound cytosolic pool of mature miRNAs in plant cells reveals a novel regulatory step at AGO1 loading. Nucleic Acids Res 47:9803–17
    [Google Scholar]
  17. 17.
    David-Schwartz R, Runo S, Townsley B, Machuka J, Sinha N 2008. Long-distance transport of mRNA via parenchyma cells and phloem across the host-parasite junction in Cuscuta. New Phytol 179:1133–41
    [Google Scholar]
  18. 18.
    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 55:746–59
    [Google Scholar]
  19. 19.
    Dinant S, Bonnemain J-L, Girousse C, Kehr J 2010. Phloem sap intricacy and interplay with aphid feeding. C. R. Biol. 333:504–15
    [Google Scholar]
  20. 20.
    Dinant S, Kehr J. 2013. Sampling and analysis of phloem sap. Methods Mol. Biol. 953:185–94
    [Google Scholar]
  21. 21.
    Ding B. 2009. The biology of viroid-host interactions. Annu. Rev. Phytopathol. 47:105–31Discovery that viroid RNAs form distinct motifs that are necessary for movement through plasmodesmata.
    [Google Scholar]
  22. 22.
    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. 53:631–37
    [Google Scholar]
  23. 23.
    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. 57:3183–93
    [Google Scholar]
  24. 24.
    Fisher DB, Wu Y, Ku MSB. 1992. Turnover of soluble proteins in the wheat sieve tube. Plant Physiol 100:1433–41
    [Google Scholar]
  25. 25.
    Gai Y-P, Yuan SS, Liu ZY, Zhao HN, Liu Q et al. 2018. Integrated phloem sap mRNA and protein expression analysis reveals phytoplasma-infection responses in mulberry. Mol. Cell Proteom. 17:1702–19
    [Google Scholar]
  26. 26.
    Gai Y-P, Zhao H-N, Zhao Y-N, Zhu B-S, Yuan S-S et al. 2018. MiRNA-seq-based profiles of miRNAs in mulberry phloem sap provide insight into the pathogenic mechanisms of mulberry yellow dwarf disease. Sci. Rep. 8:812
    [Google Scholar]
  27. 27.
    Gaupels F, Buhtz A, Knauer T, Deshmukh S, Waller F et al. 2008. Adaptation of aphid stylectomy for analyses of proteins and mRNAs in barley phloem sap. J. Exp. Bot. 59:3297–306
    [Google Scholar]
  28. 28.
    Giavalisco P, Kapitza K, Kolasa A, Buhtz A, Kehr J. 2006. Towards the proteome of Brassica napus phloem sap. Proteomics 6:896–909
    [Google Scholar]
  29. 29.
    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. 78:10104–10
    [Google Scholar]
  30. 30.
    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
    [Google Scholar]
  31. 31.
    Hannapel DJ, Banerjee AK. 2017. Multiple mobile mRNA signals regulate tuber development in potato. Plants 6:8
    [Google Scholar]
  32. 32.
    Haywood V, Kragler F, Lucas WJ. 2002. Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell Suppl. 2002 S303–25
    [Google Scholar]
  33. 33.
    Haywood V, Yu T-S, Huang N-C, Lucas WJ. 2005. Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant J 42:49–68
    [Google Scholar]
  34. 34.
    Hipper C, Brault V, Ziegler-Graff V, Revers F. 2013. Viral and cellular factors involved in phloem transport of plant viruses. Front. Plant Sci. 4:154
    [Google Scholar]
  35. 35.
    Huang N-C, Yu T-S. 2009. The sequences of Arabidopsis GA-INSENSITIVE RNA constitute the motifs that are necessary and sufficient for RNA long-distance trafficking. Plant J 59:921–29
    [Google Scholar]
  36. 36.
    Huen AK, Rodriguez-Medina C, Ho AYY, Atkins CA, Smith PMC. 2017. Long-distance movement of phosphate starvation-responsive microRNAs in Arabidopsis. Plant Biol 19:643–49
    [Google Scholar]
  37. 37.
    Kanehira A, Yamada K, Iwaya T, Tsuwamoto R, Kasai A et al. 2010. Apple phloem cells contain some mRNAs transported over long distances. Tree Genet. Genomes 6:635–42
    [Google Scholar]
  38. 38.
    Kasai A, Kanehira A, Harada T. 2010. miR172 can move long distances in Nicotiana benthamiana. Open Plant Sci. J. 4:1–6
    [Google Scholar]
  39. 39.
    Kehr J, Kragler F. 2018. Long distance RNA movement. New Phytol 218:29–40
    [Google Scholar]
  40. 40.
    Kim G, LeBlanc ML, Wafula EK, dePamphilis CW, Westwood JH. 2014. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345:808–11
    [Google Scholar]
  41. 41.
    Kim M, Canio W, Kessler S, Sinha N. 2001. Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293:287–89
    [Google Scholar]
  42. 42.
    Knoblauch M, Peters WS, Bell K, Ross-Elliott TJ, Oparka KJ. 2018. Sieve-element differentiation and phloem sap contamination. Curr. Opin. Plant Biol. 43:43–49
    [Google Scholar]
  43. 43.
    Kühn 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 275:1298–300
    [Google Scholar]
  44. 44.
    Li S, Wang X, Xu W, Liu T, Cai C et al. 2021. Unidirectional movement of small RNAs from shoots to roots in interspecific heterografts. Nat. Plants 7:50–59
    [Google Scholar]
  45. 45.
    Lin MK, Lee YJ, Lough TJ, Phinney BS, Lucas WJ. 2009. Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol. Cell Proteom. 8:343–56
    [Google Scholar]
  46. 46.
    Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY et al. 2008. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–46
    [Google Scholar]
  47. 47.
    Liu N, Shen G, Xu Y, Liu H, Zhang J et al. 2020. Extensive inter-plant protein transfer between Cuscuta parasites and their host plants. Mol. Plant 13:573–85
    [Google Scholar]
  48. 48.
    Liu N, Yang J, Guo S, Xu Y, Zhang M. 2013. Genome-wide identification and comparative analysis of conserved and novel microRNAs in grafted watermelon by high-throughput sequencing. PLOS ONE 8:e57359
    [Google Scholar]
  49. 49.
    Lopez-Cobollo RM, Filippis I, Bennett MH, Turnbull CG 2016. Comparative proteomics of cucurbit phloem indicates both unique and shared sets of proteins. Plant J 88:633–47
    [Google Scholar]
  50. 50.
    Lucas WJ. 1995. Plasmodesmata: intercellular channels for macromolecular transport in plants. Curr. Opin. Cell Biol. 7:673–80
    [Google Scholar]
  51. 51.
    Lucas WJ. 2006. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–84
    [Google Scholar]
  52. 52.
    Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L et al. 1995. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980–83
    [Google Scholar]
  53. 53.
    Luo K-R, Huang N-C, Yu T-S. 2018. Selective targeting of mobile mRNAs to plasmodesmata for cell-to-cell movement. Plant Physiol 177:604–14Demonstration that targeting of mRNAs to PD is selective.
    [Google Scholar]
  54. 54.
    Martin A, Adam H, Diaz-Mendoza M, Zurczak M, Gonzalez-Schain ND, Suarez-Lopez P. 2009. Graft-transmissible induction of potato tuberization by the microRNA miR172. Development 136:2873–81
    [Google Scholar]
  55. 55.
    McNaught AD, Wilkinson A, eds. 1997. Compendium of Chemical Terminology: IUPAC Recommendations Oxford: Blackwell Scientific Publications. , 2nd ed..
    [Google Scholar]
  56. 56.
    Molnar A, Melnyk C, Bassett A, Hardcastle T, Dunn R, Baulcombe D. 2010. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–75
    [Google Scholar]
  57. 57.
    Notaguchi M, Higashiyama T, Suzuki T. 2015. Identification of mRNAs that move over long distances using an RNA-Seq analysis of Arabidopsis/Nicotiana benthamiana heterografts. Plant Cell Physiol 56:311–21
    [Google Scholar]
  58. 58.
    Notaguchi M, Wolf S, Lucas WJ 2012. Phloem-mobile Aux/IAA transcripts target to the root tip and modify root architecture. J. Integr. Plant Biol. 54:760–72
    [Google Scholar]
  59. 59.
    Okuma N, Soyano T, Suzaki T, Kawaguchi M. 2020. MIR2111–5 locus and shoot-accumulated mature miR2111 systemically enhance nodulation depending on HAR1 in Lotus japonicus. Nat. Commun. 11:5192
    [Google Scholar]
  60. 60.
    Omid A, Keilin T, Glass A, Leshkowitz D, Wolf S 2007. Characterization of phloem-sap transcription profile in melon plants. J. Exp. Bot. 58:3645–56
    [Google Scholar]
  61. 61.
    Oparka KJ, Cruz SS. 2000. The great escape: phloem transport and unloading of macromolecules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:323–47
    [Google Scholar]
  62. 62.
    Ostendorp A, Pahlow S, Krüßel L, Hanhart P, Garbe MY et al. 2017. Functional analysis of Brassica napus phloem protein and ribonucleoprotein complexes. New Phytol 214:1188–97
    [Google Scholar]
  63. 63.
    Pahlow S, Ostendorp A, Krüßel L, Kehr J. 2018. Phloem sap sampling from Brassica napus for 3D-PAGE of protein and ribonucleoprotein complexes. J. Vis. Exp. 2018.131e57097
    [Google Scholar]
  64. 64.
    Pant BD, Buhtz A, Kehr J, Scheible WR. 2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–38
    [Google Scholar]
  65. 65.
    Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A et al. 2009. Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150:1541–55
    [Google Scholar]
  66. 66.
    Paultre DSG, Gustin M-P, Molnar A, Oparka KJ. 2016. Lost in transit: long-distance trafficking and phloem unloading of protein signals in Arabidopsis homografts. Plant Cell 28:2016–25
    [Google Scholar]
  67. 67.
    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 16:1741–52
    [Google Scholar]
  68. 68.
    Robards AW, Lucas WJ. 1990. Plasmodesmata. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:369–419
    [Google Scholar]
  69. 69.
    Rodriguez-Medina C, Atkins CA, Mann AJ, Jordan ME, Smith PMC 2011. Macromolecular composition of phloem exudate from white lupin (Lupinus albus L.). BMC Plant Biol 11:36
    [Google Scholar]
  70. 70.
    Sasaki T, Chino M, Hayashi H, Fujiwara T. 1998. Detection of several mRNA species in rice phloem sap. Plant Cell Physiol 39:895–97
    [Google Scholar]
  71. 71.
    Sinha NR, Williams RE, Hake S 1993. Overexpression of the maize homeo box gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7:787–95First evidence for intercellular transport of endogenous mRNA and protein.
    [Google Scholar]
  72. 72.
    Tangl E. 1880. Ueber offene Communicationen zwischen den Zellen des Endosperms einiger Samen. Jahrb. Wiss. Bot. 12:170–90
    [Google Scholar]
  73. 73.
    Taoka K-i, Ham B-K, Xoconostle-Cázares B, Rojas MR, Lucas WJ 2007. Reciprocal phosphorylation and glycosylation recognition motifs control NCAPP1 interaction with pumpkin phloem proteins and their cell-to-cell movement. Plant Cell 19:1866–84
    [Google Scholar]
  74. 74.
    Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W et al. 2015. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat. Plants 1:15025First demonstration of the genomic scale of long-distance mRNA transport across graft junctions in two Arabidopsis ecotypes.
    [Google Scholar]
  75. 75.
    Tolstyko E, Lezzhov A, Solovyev A 2019. Identification of miRNA precursors in the phloem of Cucurbita maxima. PeerJ 7:e8269
    [Google Scholar]
  76. 76.
    Tsikou D, Yan Z, Holt DB, Abel NB, Reid DE et al. 2018. Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA. Science 362:233–36
    [Google Scholar]
  77. 77.
    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
    [Google Scholar]
  78. 78.
    Walther D, Kragler F 2016. Limited phosphate: Mobile RNAs convey the message. Nat. Plants 2:16040
    [Google Scholar]
  79. 79.
    Wang J, Jiang L, Wu R. 2017. Plant grafting: how genetic exchange promotes vascular reconnection. New Phytol 214:56–65
    [Google Scholar]
  80. 80.
    Wang Y. 2011. Plant grafting and its application in biological research. Chin. Sci. Bull. 56:3511–17
    [Google Scholar]
  81. 81.
    Wang Y, Wang L, Xing N, Wu X, Wu X et al. 2020. A universal pipeline for mobile mRNA detection and insights into heterografting advantages under chilling stress. Hort. Res. 7:13
    [Google Scholar]
  82. 82.
    Xia C, Huang J, Lan H, Zhang C 2020. Long-distance movement of mineral deficiency-responsive mRNAs in Nicotiana benthamiana/tomato heterografts. Plants 9:876
    [Google Scholar]
  83. 83.
    Xia C, Zheng Y, Huang J, Zhou X, Li R et al. 2018. Elucidation of the mechanisms of long-distance mRNA movement in a Nicotiana benthamiana/tomato heterograft system. Plant Physiol 177:745–58
    [Google Scholar]
  84. 84.
    Xoconostle-Cazares B, Xiang Y, Ruiz-Medrano R, Wang HL, Monzer J et al. 1999. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283:94–98
    [Google Scholar]
  85. 85.
    Xu H, Iwashiro R, Li T, Harada T 2013. Long-distance transport of Gibberellic Acid Insensitive mRNA in Nicotiana benthamiana. BMC Plant Biol 13:165
    [Google Scholar]
  86. 86.
    Yang L, Perrera V, Saplaoura E, Apelt F, Bahin M et al. 2019. m5C methylation guides systemic transport of messenger RNA over graft junctions in plants. Curr. Biol. 29:2465–76.e5
    [Google Scholar]
  87. 87.
    Yang Y, Mao L, Jittayasothorn Y, Kang Y, Jiao C et al. 2015. Messenger RNA exchange between scions and rootstocks in grafted grapevines. BMC Plant Biol 15:251
    [Google Scholar]
  88. 88.
    Yoo B-C, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S et al. 2004. A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000
    [Google Scholar]
  89. 89.
    Zambryski P, Crawford K. 2000. Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu. Rev. Cell Dev. Biol. 16:393–421
    [Google Scholar]
  90. 90.
    Zhang S, Sun L, Kragler F 2009. The phloem-delivered RNA pool contains small noncoding RNAs and interferes with translation. Plant Physiol 150:378–87
    [Google Scholar]
  91. 91.
    Zhang W, Thieme CJ, Kollwig G, Apelt F, Yang L et al. 2016. tRNA-related sequences trigger systemic mRNA transport in plants. Plant Cell 28:1237–49
    [Google Scholar]
  92. 92.
    Zhang Z, Zheng Y, Ham B-K, Chen J, Yoshida A et al. 2016. Vascular-mediated signalling involved in early phosphate stress response in plants. Nat. Plants 2:16033
    [Google Scholar]
  93. 93.
    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 26:3836–46
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-070121-033601
Loading
/content/journals/10.1146/annurev-arplant-070121-033601
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error