1932

Abstract

The plant vascular system plays a central role in coordinating physiological and developmental events through delivery of both essential nutrients and long-distance signaling agents. The enucleate phloem sieve tube system of the angiosperms contains a broad spectrum of RNA species. Grafting and transcriptomics studies have indicated that several thousand mRNAs move long distances from source organs to meristematic sink tissues. Ribonucleoprotein complexes play a pivotal role as stable RNA-delivery systems for systemic translocation of cargo RNA. In this review, we assess recent progress in the characterization of phloem and plasmodesmal transport as an integrated local and systemic communication network. We discuss the roles of phloem-mobile small RNAs in epigenetic events, including meristem development and genome stability, and the delivery of mRNAs to specific tissues in response to environmental inputs. A large body of evidence now supports a model in which phloem-mobile RNAs act as critical components of gene regulatory networks involved in plant growth, defense, and crop yield at the whole-plant level.

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2017-04-28
2024-03-28
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Literature Cited

  1. Alakonya A, Kumar R, Koenig D, Kimura S, Townsley B. 1.  et al. 2012. Interspecific RNA interference of SHOOT MERISTEMLESS-like disrupts Cuscuta pentagona plant parasitism. Plant Cell 24:3153–66 [Google Scholar]
  2. Allen E, Xie Z, Gustafson AM, Carrington JC. 2.  2005. MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–21 [Google Scholar]
  3. Aly R, Cholakh H, Joel DM, Leibman D, Steinitz B. 3.  et al. 2009. Gene silencing of mannose 6-phosphate reductase in the parasitic weed Orobanche aegyptiaca through the production of homologous dsRNA sequences in the host plant. Plant Biotechnol. J. 7487–98
  4. Aoki K, Suzui N, Fujimaki S, Dohmae N, Yonekura-Sakakibara K. 4.  et al. 2005. Destination-selective long-distance movement of phloem proteins. Plant Cell 17:1801–14 [Google Scholar]
  5. Araya T, von Wiren N, Takahashi H. 5.  2016. CLE peptide signaling and nitrogen interactions in plant root development. Plant Mol. Biol. 91607–15
  6. Asano T, Masumura T, Kusano H, Kikuchi S, Kurita A. 6.  et al. 2002. Construction of a specialized cDNA library from plant cells isolated by laser capture microdissection: toward comprehensive analysis of the genes expressed in the rice phloem. Plant J 32401–8
  7. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ. 7.  2006. pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 141:1000–11 [Google Scholar]
  8. Axtell MJ.8.  2013. Classification and comparison of small RNAs from plants. Annu. Rev. Plant Biol. 64137–159
  9. Baek D, Kim MC, Chun HJ, Kang S, Park HC. 9.  et al. 2013. Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol 161:362–73 [Google Scholar]
  10. Balachandran S, Xiang Y, Schobert C, Thompson GA, Lucas WJ. 10.  1997. Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. PNAS 9414150–55
  11. Banerjee AK, Chatterjee M, Yu Y, Suh SG, Miller WA, Hannapel DJ. 11.  2006. Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18:3443–57 [Google Scholar]
  12. Banerjee AK, Lin T, Hannapel DJ. 12.  2009. Untranslated regions of a mobile transcript mediate RNA metabolism. Plant Physiol 151:1831–43 [Google Scholar]
  13. Bari R, Datt Pant B, Stitt M, Scheible WR. 13.  2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–99 [Google Scholar]
  14. Bennetzen JL, Wang H. 14.  2014. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu. Rev. Plant Biol. 65505–30
  15. Bologna NG, Voinnet O. 15.  2014. The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol. 65473–503
  16. Borges F, Martienssen RA. 16.  2015. The expanding world of small RNAs in plants. Nat. Rev. Mol. Cell Biol. 16:727–41 [Google Scholar]
  17. Buhtz A, Pieritz J, Springer F, Kehr J. 17.  2010. Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 1064
  18. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J. 18.  2008. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J. 53739–49
  19. Burleigh SH, Harrison MJ. 19.  1999. The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol 119:241–48 [Google Scholar]
  20. Caetano-Anolles G, Gresshoff PM. 20.  1991. Plant genetic control of nodulation. Annu. Rev. Microbiol. 45345–82
  21. Calderwood A, Kopriva S, Morris RJ. 21.  2016. Transcript abundance explains mRNA mobility data in Arabidopsis thaliana. Plant Cell 28:610–15 [Google Scholar]
  22. Chen JJ, Janssen BJ, Williams A, Sinha N. 22.  1997. A gene fusion at a homeobox locus: alterations in leaf shape and implications for morphological evolution. Plant Cell 91289–304
  23. Chiou TJ, Lin SI. 23.  2011. Signaling network in sensing phosphate availability in plants. Annu. Rev. Plant Biol. 62185–206
  24. Cho SK, Sharma P, Butler NM, Kang IH, Shah S. 24.  et al. 2015. Polypyrimidine tract-binding proteins of potato mediate tuberization through an interaction with StBEL5 RNA. J. Exp. Bot. 666835–47
  25. Cui X, Cao X. 25.  2014. Epigenetic regulation and functional exaptation of transposable elements in higher plants. Curr. Opin. Plant Biol. 21:83–88 [Google Scholar]
  26. David-Schwartz R, Runo S, Townsley B, Machuka J, Sinha N. 26.  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]
  27. Deeken R, Ache P, Kajahn I, Klinkenberg J, Bringmann G, Hedrich R. 27.  2008. Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. Plant J 55746–59
  28. Dodsworth S, Leitch AR, Leitch IJ. 28.  2015. Genome size diversity in angiosperms and its influence on gene space. Curr. Opin. Genet. Dev. 3573–78
  29. Doering-Saad C, Newbury HJ, Couldridge CE, Bale JS, Pritchard J. 29.  2006. A phloem-enriched cDNA library from Ricinus: insights into phloem function. J. Exp. Bot. 573183–93
  30. Forde BG.30.  2002. Local and long-range signaling pathways regulating plant responses to nitrate. Annu. Rev. Plant Biol. 53203–24
  31. Franco-Zorrilla JM, Martin AC, Leyva A, Par-Ares JP. 31.  2005. Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol. 138:847–57 [Google Scholar]
  32. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK. 32.  2005. A miRNA involved in phosphate-starvation response in Arabidopsis. Curr. Biol. 15:2038–43 [Google Scholar]
  33. Gaupels F, Buhtz A, Knauer T, Deshmukh S, Waller F. 33.  et al. 2008. Adaptation of aphid stylectomy for analyses of proteins and mRNAs in barley phloem sap. J. Exp. Bot. 593297–306
  34. Gómez G, Pállas V. 34.  2004. A long-distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with Hop stunt viroid RNA. J. Virol. 7810104–10
  35. Guo S, Zhang J, Sun H, Salse J, Lucas WJ. 35.  et al. 2013. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat. Genet. 4551–58
  36. Ham BK, Brandom JL, Xoconostle-Cázares B, Ringgold V, Lough TJ, Lucas WJ. 36.  2009. A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex. Plant Cell 21:197–215 [Google Scholar]
  37. Ham BK, Li G, Jia W, Leary JA, Lucas WJ. 37.  2014. Systemic delivery of siRNA in pumpkin by a plant PHLOEM SMALL RNA-BINDING PROTEIN 1-ribonucleoprotein complex. Plant J 80683–94
  38. Ham BK, Lucas WJ. 38.  2014. The angiosperm phloem sieve tube system: a role in mediating traits important to modern agriculture. J. Exp. Bot. 651799–816
  39. Haywood V, Yu TS, Huang NC, Lucas WJ. 39.  2005. Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant J 4249–68
  40. Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY. 40.  et al. 2009. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–32 [Google Scholar]
  41. Hu C, Ham BK, El-Shabrawi HM, Alexander D, Zhang D. 41.  et al. 2016. Proteomics and metabolomics analyses reveal the cucurbit sieve tube system as a complex metabolic space. Plant J 87:442–54 [Google Scholar]
  42. Huang NC, Yu TS. 42.  2009. The sequences of Arabidopsis GA-INSENSITIVE RNA constitute the motifs that are necessary and sufficient for RNA long-distance trafficking. Plant J 59921–29
  43. Jones-Rhoades MW, Bartel DP. 43.  2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14:787–99 [Google Scholar]
  44. Kanehira A, Yamada K, Iwaya T, Tsuwamoto R, Kasai A. 44.  et al. 2010. Apple phloem cells contain some mRNAs transported over long distances. Tree Genet. Genomes 6635–42
  45. Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K. 45.  et al. 2009. Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57313–21
  46. Kim G, LeBlanc ML, Wafula EK, dePamphilis CW, Westwood JH. 46.  2014. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345808–11
  47. Kim G, Westwood JH. 47.  2015. Macromolecule exchange in Cuscuta-host plant interactions. Curr. Opin. Plant Biol. 26:20–25 [Google Scholar]
  48. Kim M, Canio W, Kessler S, Sinha N. 48.  2001. Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293:287–89 [Google Scholar]
  49. Knoblauch M, Knoblauch J, Mullendore DL, Savage JA, Babst BA. 49.  et al. 2016. Testing the Münch hypothesis of long distance phloem transport in plants. eLife 5e15341
  50. Kollmann R, Dörr I, Kleinig H. 50.  1970. Protein filaments—structural components of the phloem exudate: I. Observations with Cucurbita and Nicotiana. Planta 9586–94
  51. Kuo HF, Chiou TJ. 51.  2011. The role of microRNAs in phosphorus deficiency signaling. Plant Physiol 156:1016–24 [Google Scholar]
  52. Lappartient AG, Vidmar JJ, Leustek T, Glass AD, Touraine B. 52.  1999. Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18:89–95 [Google Scholar]
  53. LeBlanc M, Kim G, Patel B, Stromberg V, Westwood J. 53.  2013. Quantification of tomato and Arabidopsis mobile RNAs trafficking into the parasitic plant Cuscuta pentagona. New Phytol. 200:1225–33 [Google Scholar]
  54. Lee JY, Yoo BC, Rojas MR, Gomez-Ospina N, Staehelin LA, Lucas WJ. 54.  2003. Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:392–96 [Google Scholar]
  55. Leustek T, Martin MN, Bick JA, Davies JP. 55.  2000. Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51141–65
  56. Lewsey MG, Hardcastle TJ, Melnyk CW, Molnar A, Valli A. 56.  et al. 2016. Mobile small RNAs regulate genome-wide DNA methylation. PNAS 113:E801–10 [Google Scholar]
  57. Li P, Ham BK, Lucas WJ. 57.  2011. CmRBP50 protein phosphorylation is essential for assembly of a stable phloem-mobile high-affinity ribonucleoprotein complex. J. Biol. Chem. 286:23142–49 [Google Scholar]
  58. Liang D, White RG, Waterhouse PM. 58.  2012. Gene silencing in Arabidopsis spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement. Plant Physiol 159984–1000
  59. Liang G, He H, Yu D. 59.  2012. Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLOS ONE 7e48951
  60. Lin MK, Lee YJ, Lough TJ, Phinney BS, Lucas WJ. 60.  2009. Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol. Cell. Proteom. 8343–56
  61. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY. 61.  et al. 2008. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–46 [Google Scholar]
  62. Lin SI, Santi C, Jobet E, Lacut E, El Kholti N. 62.  et al. 2010. Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 512119–31
  63. Lin T, Lashbrook CC, Cho SK, Butler NM, Sharma P. 63.  et al. 2015. Transcriptional analysis of phloem-associated cells of potato. BMC Genom. 16665
  64. Lin T, Sharma P, Gonzalez DH, Viola IL, Hannapel DJ. 64.  2013. The impact of the long-distance transport of a BEL1-like messenger RNA on development. Plant Physiol 161:760–72 [Google Scholar]
  65. Lin WY, Huang TK, Chiou TJ. 65.  2013. Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell 25:4061–74 [Google Scholar]
  66. Liu CM, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG. 66.  1998. Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol 116:91–99 [Google Scholar]
  67. Liu Q, Chen XB, Wu K, Fu XD. 67.  2015. Nitrogen signaling and use efficiency in plants: What's new?. Curr. Opin. Plant Biol. 27:192–98 [Google Scholar]
  68. Liu TY, Chang CY, Chiou TJ. 68.  2009. The long-distance signaling of mineral macronutrients. Curr. Opin. Plant Biol. 12:312–19 [Google Scholar]
  69. Lough TJ, Lucas WJ. 69.  2006. Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu. Rev. Plant Biol. 57203–32
  70. Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR. 70.  et al. 2013. The plant vascular system: evolution, development and functions. J. Integr. Plant Biol. 55294–388
  71. Lucas WJ, Ham BK, Kim JY. 71.  2009. Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503 [Google Scholar]
  72. Lundmark M, Korner CJ, Nielsen TH. 72.  2010. Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol. Plant. 140:57–68 [Google Scholar]
  73. Ma Y, Miura E, Ham BK, Cheng HW, Lee YJ, Lucas WJ. 73.  2010. Pumpkin eIF5A isoforms interact with components of the translational machinery in the cucurbit sieve tube system. Plant J 64536–50
  74. Mahajan A, Bhogale S, Kang IH, Hannapel DJ, Banerjee AK. 74.  2012. The mRNA of a Knotted1-like transcription factor of potato is phloem mobile. Plant Mol. Biol. 79595–608
  75. Matzke MA, Kanno T, Matzke AJM. 75.  2015. RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu. Rev. Plant Biol. 66243–67
  76. Melnyk CW, Molnar A, Bassett A, Baulcombe DC. 76.  2011. Mobile 24 nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr. Biol 21:1678–83 [Google Scholar]
  77. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC. 77.  2010. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–75 [Google Scholar]
  78. Nakazono M, Qiu F, Borsuk LA, Schnable PS. 78.  2003. Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15:583–96 [Google Scholar]
  79. Notaguchi M, Wolf S, Lucas WJ. 79.  2012. Phloem-mobile Aux/IAA transcripts target to the root tip and modify root architecture. J. Integr. Plant Biol. 54760–72
  80. Omid A, Keilin T, Glass A, Leshkowitz D, Wolf S. 80.  2007. Characterization of phloem-sap transcription profile in melon plants. J. Exp. Bot. 583645–56
  81. Palauqui JC, Elmayan T, Pollien JM, Vaucheret H. 81.  1997. Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16:4738–45 [Google Scholar]
  82. Pant BD, Buhtz A, Kehr J, Scheible WR. 82.  2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53731–38
  83. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A. 83.  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]
  84. Paul S, Datta SK, Datta K. 84.  2015. miRNA regulation of nutrient homeostasis in plants. Front. Plant Sci. 6232
  85. Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ. 85.  2007. A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50320–37
  86. Qi Y, Pelissier T, Itaya A, Hunt E, Wassenegger M, Ding B. 86.  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]
  87. Rodriguez-Medina C, Atkins CA, Mann AJ, Jordan ME, Smith PM. 87.  2011. Macromolecular composition of phloem exudate from white lupin (Lupinus albus L.). BMC Plant Biol 1136
  88. Roney JK, Khatibi PA, Westwood JH. 88.  2007. Cross-species translocation of mRNA from host plants into the parasitic plant dodder. Plant Physiol 143:1037–43 [Google Scholar]
  89. Ruffel S, Poitout A, Krouk G, Coruzzi GM, Lacombe B. 89.  2016. Long-distance nitrate signaling displays cytokinin dependent and independent branches. J. Integr. Plant Biol. 58226–29
  90. Ruiz-Medrano R, Xoconostle-Cázares B, Lucas WJ. 90.  1999. Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126:4405–19 [Google Scholar]
  91. Saini P, Eyler DE, Green R, Dever TE. 91.  2009. Hypusine-containing protein eIF5A promotes translation elongation. Nature 459118–21
  92. Schwarz D, Rouphael Y, Colla G, Venema JH. 92.  2010. Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants. Sci. Horticult. 127:162–71 [Google Scholar]
  93. Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I. 93.  et al. 2003. Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–12 [Google Scholar]
  94. Secco D, Wang C, Arpat BA, Wang Z, Poirier Y. 94.  et al. 2012. The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol 193:842–51 [Google Scholar]
  95. Singh G, Pratt G, Yeo GW, Moore MJ. 95.  2015. The clothes make the mRNA: past and present trends in mRNP fashion. Annu. Rev. Biochem. 84325–54
  96. Stadler R, Wright KM, Lauterbach C, Amon G, Gahrtz M. 96.  et al. 2005. Expression of GFP-fusions in Arabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots. Plant J 41319–31
  97. Sunkar R, Zhu JK. 97.  2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–19 [Google Scholar]
  98. Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 98.  2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346343–46
  99. Takeda R, Petrov AI, Leontis NB, Ding B. 99.  2011. A three-dimensional RNA motif in Potato spindle tuber viroid mediates trafficking from palisade mesophyll to spongy mesophyll in Nicotiana benthamiana. Plant Cell 23:258–72 [Google Scholar]
  100. Taoka K, Ham BK, Xoconostle-Cázares B, Rojas MR, Lucas WJ. 100.  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]
  101. Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A. 101.  et al. 2010. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J. 4775–89
  102. Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W. 102.  et al. 2015. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat. Plants 115025
  103. Voinnet O, Baulcombe DC. 103.  1997. Systemic signalling in gene silencing. Nature 389553
  104. Voinnet O, Vain P, Angell S, Baulcombe DC. 104.  1998. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95177–87
  105. Warschefsky EJ, Klein LL, Frank MH, Chitwood DH, Londo JP. 105.  et al. 2016. Rootstocks: diversity, domestication, and impacts on shoot phenotypes. Trends Plant Sci 21:418–37 [Google Scholar]
  106. Wendel JF, Jackson SA, Meyers BC, Wing RA. 106.  2016. Evolution of plant genome architecture. Genome Biol 1737
  107. Wu R, Wang X, Lin Y, Ma Y, Liu G. 107.  et al. 2013. Inter-species grafting caused extensive and heritable alterations of DNA methylation in Solanaceae plants. PLOS ONE 8e61995
  108. Xoconostle-Cázares B, Xiang Y, Ruiz-Medrano R, Wang HL, Monzer J. 108.  et al. 1999. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283:94–98 [Google Scholar]
  109. Yang YZ, Mao LY, Jittayasothorn Y, Kang YM, Jiao C. 109.  et al. 2015. Messenger RNA exchange between scions and rootstocks in grafted grapevines. BMC Plant Biol 15251
  110. Yoder JI, Gunathilake P, Wu B, Tomilova N, Tomilov AA. 110.  2009. Engineering host resistance against parasitic weeds with RNA interference. Pest Manag. Sci. 65460–66
  111. Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S. 111.  et al. 2004. A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000 [Google Scholar]
  112. Zambryski P.112.  2004. Cell-to-cell transport of proteins and fluorescent tracers via plasmodesmata during plant development. J. Cell Biol. 164:165–68 [Google Scholar]
  113. Zhang S, Sun L, Kragler F. 113.  2009. The phloem-delivered RNA pool contains small noncoding RNAs and interferes with translation. Plant Physiol 150:378–87 [Google Scholar]
  114. Zhang W, Kollwig G, Stecyk E, Apelt F, Dirks R, Kragler F. 114.  2014. Graft-transmissible movement of inverted-repeat-induced siRNA signals into flowers. Plant J 80106–21
  115. Zhang W, Thieme CJ, Kollwig G, Apelt F, Yang L. 115.  et al. 2016. tRNA-related sequences trigger systemic mRNA transport in plants. Plant Cell 28:1237–49 [Google Scholar]
  116. Zhang Z, Liao H, Lucas WJ. 116.  2014. Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J. Integr. Plant Biol. 56192–220
  117. Zhang Z, Zheng Y, Ham BK, Chen J, Yoshida A. 117.  et al. 2016. Vascular-mediated signalling involved in early phosphate stress response in plants. Nat. Plants 216033
  118. Zhong X, Archual AJ, Amin AA, Ding B. 118.  2008. A genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 20:35–47 [Google Scholar]
  119. Zhong X, Tao X, Stombaugh J, Leontis N, Ding B. 119.  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]
  120. Zhu Y, Green L, Woo YM, Owens R, Ding B. 120.  2001. Cellular basis of potato spindle tuber viroid systemic movement. Virology 279:69–77 [Google Scholar]
  121. Zhu Y, Qi Y, Xun Y, Owens R, Ding B. 121.  2002. Movement of potato spindle tuber viroid reveals regulatory points of phloem-mediated RNA traffic. Plant Physiol 130:138–46 [Google Scholar]
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