1932

Abstract

For plant viruses, the ability to load into the vascular phloem and spread systemically within a host is an essential step in establishing a successful infection. However, access to the vascular phloem is highly regulated, representing a significant obstacle to virus loading, movement, and subsequent unloading into distal uninfected tissues. Recent studies indicate that during virus infection, phloem tissues are a source of significant transcriptional and translational alterations, with the number of virus-induced differentially expressed genes being four- to sixfold greater in phloem tissues than in surrounding nonphloem tissues. In addition, viruses target phloem-specific components as a means to promote their own systemic movement and disrupt host defense processes. Combined, these studies provide evidence that the vascular phloem plays a significant role in the mediation and control of host responses during infection and as such is a site of considerable modulation by the infecting virus. This review outlines the phloem responses and directed reprograming mechanisms that viruses employ to promote their movement through the vasculature.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-010320-072410
2020-09-29
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/virology/7/1/annurev-virology-010320-072410.html?itemId=/content/journals/10.1146/annurev-virology-010320-072410&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR et al. 2013. The plant vascular system: evolution, development and functions. J. Integr. Plant Biol. 55:4294–388
    [Google Scholar]
  2. 2. 
    Turgeon R, Wolf S. 2009. Phloem transport: cellular pathways and molecular trafficking. Annu. Rev. Plant Biol. 60:207–21
    [Google Scholar]
  3. 3. 
    Carella P, Wilson DC, Kempthorne CJ, Cameron RK 2016. Vascular sap proteomics: providing insight into long-distance signaling during stress. Front. Plant Sci. 7:651
    [Google Scholar]
  4. 4. 
    Turnbull CGN, Lopez-Cobollo RM. 2013. Heavy traffic in the fast lane: long-distance signalling by macromolecules. New Phytol 198:133–51
    [Google Scholar]
  5. 5. 
    Fu ZQ, Dong X. 2013. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64:1839–63
    [Google Scholar]
  6. 6. 
    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]
  7. 7. 
    Folimonova SY, Tilsner J. 2018. Hitchhikers, highway tolls and roadworks: the interactions of plant viruses with the phloem. Curr. Opin. Plant Biol. 43:82–88
    [Google Scholar]
  8. 8. 
    Bendix C, Lewis JD. 2018. The enemy within: phloem-limited pathogens. Mol. Plant Pathol. 19:1238–54
    [Google Scholar]
  9. 9. 
    Collum TD, Culver JN. 2017. Tobacco mosaic virus infection disproportionately impacts phloem associated translatomes in Arabidopsis thaliana and Nicotiana benthamiana. Virology 510:76–89
    [Google Scholar]
  10. 10. 
    Collum TD, Stone AL, Sherman DJ, Rogers EE, Dardick C, Culver JN 2019. Translatome profiling of plum pox virus infected leaves in European plum reveals temporal and spatial coordination of defense responses in phloem tissues. Mol. Plant-Microbe Interact. 33:66–77
    [Google Scholar]
  11. 11. 
    Ham BK, Lucas WJ. 2014. The angiosperm phloem sieve tube system: a role in mediating traits important to modern agriculture. J. Exp. Bot. 65:71799–816
    [Google Scholar]
  12. 12. 
    Otero S, Helariutta Y. 2017. Companion cells: a diamond in the rough. J. Exp. Bot. 68:171–78
    [Google Scholar]
  13. 13. 
    Van Bel AJE. 2003. The phloem, a miracle of ingenuity. Plant Cell Environ 26:1125–49
    [Google Scholar]
  14. 14. 
    Aaziz R, Dinant S, Epel BL 2001. Plasmodesmata and plant cytoskeleton. Trends Plant Sci 6:7326–30
    [Google Scholar]
  15. 15. 
    Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E et al. 2011. Arabidopsis plasmo-desmal proteome. PLOS ONE 6:4e18880
    [Google Scholar]
  16. 16. 
    Oparka KJ, Roberts AG, Boevink P, Cruz SS, Roberts I et al. 1999. Simple, but not branched, plasmo-desmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:6743–54
    [Google Scholar]
  17. 17. 
    Lee JY, Lu H. 2011. Plasmodesmata: the battleground against intruders. Trends Plant Sci 16:4201–10
    [Google Scholar]
  18. 18. 
    Sager R, Lee JY. 2014. Plasmodesmata in integrated cell signalling: insights from development and environmental signals and stresses. J. Exp. Bot. 65:226337–58
    [Google Scholar]
  19. 19. 
    Sevilem I, Miyashima S, Helariutta Y 2013. Cell-to-cell communication via plasmodesmata in vascular plants. Cell Adhes. Migr. 7:127–32
    [Google Scholar]
  20. 20. 
    Lee JY, Frank M. 2018. Plasmodesmata in phloem: different gateways for different cargoes. Curr. Opin. Plant Biol. 43:119–24
    [Google Scholar]
  21. 21. 
    Oparka KJ, Turgeon R. 1999. Sieve elements and companion cells—traffic control centers of the phloem. Plant Cell 11:4739–50
    [Google Scholar]
  22. 22. 
    Lee JY, Yoo BC, Rojas MR, Gomez-Ospina N, Staehelin LA, Lucas WJ 2003. Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:5605392–96
    [Google Scholar]
  23. 23. 
    Hong JS, Ju H. 2017. The plant cellular systems for plant virus movement. Plant Pathol. J. 33:3213–28
    [Google Scholar]
  24. 24. 
    Kumar D, Kumar R, Hyun TK, Kim JY 2014. Cell-to-cell movement of viruses via plasmodesmata. J. Plant Res. 128:137–47
    [Google Scholar]
  25. 25. 
    Kragler F. 2010. RNA in the phloem: a crisis or a return on investment. ? Plant Sci 178:299–104
    [Google Scholar]
  26. 26. 
    Radford JE, Vesk M, Overall RL 1998. Callose deposition at plasmodesmata. Protoplasma 201:30–37
    [Google Scholar]
  27. 27. 
    Chen XY, Kim JY. 2009. Callose synthesis in higher plants. Plant Signal. Behav. 4:6489–92
    [Google Scholar]
  28. 28. 
    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 28:92016–25
    [Google Scholar]
  29. 29. 
    Schulz A. 2017. Long-distance trafficking: lost in transit or stopped at the gate. ? Plant Cell 29:3426–30
    [Google Scholar]
  30. 30. 
    Kehr J, Buhtz A. 2008. Long distance transport and movement of RNA through the phloem. J. Exp. Bot. 59:185–92
    [Google Scholar]
  31. 31. 
    Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK 2002. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. . Nature 419:399–403
    [Google Scholar]
  32. 32. 
    Xoconostle-Cázares 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]
  33. 33. 
    Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W et al. 2015. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat. Plants 1:15025
    [Google Scholar]
  34. 34. 
    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]
  35. 35. 
    Lin MK, Lee YJ, Lough TJ, Phimmey BS, Lucas WJ 2009. Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol. Cell. Proteom. 8:2343–56
    [Google Scholar]
  36. 36. 
    Zhang W, Thieme CJ, Kollwig G, Apelt F, Yang L et al. 2016. tRNA-related sequences trigger systemic mRNA transport in plants. Plant Cell 28:61237–49
    [Google Scholar]
  37. 37. 
    Melnyk CW, Molnar A, Baulcombe DC 2011. Intercellular and systemic movement of RNA silencing signals. EMBO J 30:173553–63
    [Google Scholar]
  38. 38. 
    Yoo AB, Kragler F, Varkonyi-Gasic E, Haywood V, Lee YM et al. 2004. A systemic small RNA signaling system in plants. Plant Cell 16:81979–2000
    [Google Scholar]
  39. 39. 
    Qiao W, Medina V, Falk BW 2017. Inspirations on virus replication and cell-to-cell movement from studies examining the cytopathology induced by Lettuce infectious yellows virus in plant cells. Front. Plant Sci. 8:1672
    [Google Scholar]
  40. 40. 
    Tilsner J, Oparka KJ. 2012. Missing links?—The connection between replication and movement of plant RNA viruses. Curr. Opin. Virol. 2:6705–11
    [Google Scholar]
  41. 41. 
    den Boon JA, Ahlquist P 2010. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 64:241–56
    [Google Scholar]
  42. 42. 
    Grangeon R, Jiang J, Laliberté JF 2012. Host endomembrane recruitment for plant RNA virus replication. Curr. Opin. Virol. 2:6683–90
    [Google Scholar]
  43. 43. 
    Tilsner J, Linnik O, Louveaux M, Roberts IM, Chapman SN, Oparka KJ 2013. Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata. J. Cell Biol. 201:7981–95
    [Google Scholar]
  44. 44. 
    Lucas WJ. 2006. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–84
    [Google Scholar]
  45. 45. 
    Schoelz JE, Harries PA, Nelson RS 2011. Intracellular transport of plant viruses: finding the door out of the cell. Mol. Plant. 4:5813–31
    [Google Scholar]
  46. 46. 
    Heinlein M. 2015. Plant virus replication and movement. Virology 479–80:657–71
    [Google Scholar]
  47. 47. 
    Citovsky V, Wong ML, Shaw AL, Prasad BV, Zambryski P 1992. Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397–411
    [Google Scholar]
  48. 48. 
    Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper SJ et al. 1998. Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10:71107–20
    [Google Scholar]
  49. 49. 
    Atkins D, Hull R, Wells B, Roberts K, Moore P, Beachy RN 1991. The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. J. Gen. Virol. 72:209–11
    [Google Scholar]
  50. 50. 
    Waigmann E, Lucas WJ, Citovsky V, Zambryski P 1994. Direct functional assay for tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability. PNAS 91:41433–37
    [Google Scholar]
  51. 51. 
    Ganusova EE, Burch-Smith TM. 2019. Review: plant-pathogen interactions through the plasmodesma prism. Plant Sci 279:70–80
    [Google Scholar]
  52. 52. 
    Scholthof HB. 2005. Plant virus transport: motions of functional equivalence. Trends Plant Sci 10:8376–82
    [Google Scholar]
  53. 53. 
    Savenkov EI, Valkonen JPT. 2001. Potyviral helper-component proteinase expressed in transgenic plants enhances titers of Potato leaf roll virus but does not alleviate its phloem limitation. Virology 283:2285–93
    [Google Scholar]
  54. 54. 
    Peter KA, Gildow F, Palukaitis P, Gray SM 2009. The C terminus of the polerovirus P5 readthrough domain limits virus infection to the phloem. J. Virol. 83:115419–29
    [Google Scholar]
  55. 55. 
    Deblasio SL, Johnson R, Sweeney MM, Karasev A, Gray SM et al. 2015. Potato leafroll virus structural proteins manipulate overlapping, yet distinct protein interaction networks during infection. Proteomics 15:122098–112
    [Google Scholar]
  56. 56. 
    Leisner SM, Turgeon R. 1993. Movement of virus and photoassimilate in the phloem: a comparative analysis. BioEssays 15:11741–48
    [Google Scholar]
  57. 57. 
    Silva MS, Wellink J, Goldbach RW, van Lent JWM 2002. Phloem loading and unloading of Cowpea mosaic virus in Vigna unguiculata. J. Gen. . Virol 83:61493–504
    [Google Scholar]
  58. 58. 
    Cheng NH, Su CL, Carter SA, Nelson RS 2000. Vascular invasion routes and systemic accumulation patterns of tobacco mosaic virus in Nicotiana benthamiana. . Plant J 23:3349–62
    [Google Scholar]
  59. 59. 
    Slewinski TL, Zhang C, Turgeon R 2013. Structural and functional heterogeneity in phloem loading and transport. Front. Plant Sci. 4:244
    [Google Scholar]
  60. 60. 
    Turgeon R, Beebe DU, Gowan E 1993. The intermediary cell: minor-vein anatomy and raffinose oligosaccharide synthesis in the Scrophulariaceae. Planta 191:4446–56
    [Google Scholar]
  61. 61. 
    Jensen S. 1969. Occurrence of virus particles in the phloem tissue of BYDV-infected barley. Virology 38:83–91
    [Google Scholar]
  62. 62. 
    Esau K, Cronshaw J, Hoefert LL 1967. Relation of beet yellows virus to the phloem and to movement in the sieve tube. J. Cell Biol. 32:171–87
    [Google Scholar]
  63. 63. 
    Ding X, Shintaku MH, Carter SA, Nelson RS 1996. Invasion of minor veins of tobacco leaves inoculated with tobacco mosaic virus mutants defective in phloem-dependent movement. PNAS 93:2011155–60
    [Google Scholar]
  64. 64. 
    Dawson WO. 1988. Modifications of the tobacco mosaic virus coat protein gene affecting replication, movement, and symptomatology. Phytopathology 78:6783–89
    [Google Scholar]
  65. 65. 
    Hilf ME, Dawson WO. 1993. Tobamovirus capsid protein functions as a host-specific determinant of long-distance movement. Virology 193:106–14
    [Google Scholar]
  66. 66. 
    Qiao W, Medina V, Kuo YW, Falk BW 2018. A distinct, non-virion plant virus movement protein encoded by a crinivirus essential for systemic infection. mBio 9:6e02230-18
    [Google Scholar]
  67. 67. 
    Prokhnevsky AI, Peremyslov VV, Napuli AJ, Dolja VV 2002. Interaction between long-distance transport factor and Hsp70-related movement protein of Beet yellows virus. J. . Virol 76:2111003–11
    [Google Scholar]
  68. 68. 
    Rajamäki ML, Valkonen JPT. 1999. The 6K2 protein and the VPg of potato virus A are determinants of systemic infection in Nicandra physaloides. Mol. . Plant-Microbe Interact 12:121074–81
    [Google Scholar]
  69. 69. 
    Wright KM, Cowan GH, Lukhovitskaya NI, Tilsner J, Roberts AG et al. 2010. The N-terminal domain of PMTV TGB1 movement protein is required for nucleolar localization, microtubule association, and long-distance movement. Mol. Plant-Microbe Interact. 23:111486–97
    [Google Scholar]
  70. 70. 
    Canetta E, Kim SH, Kalinina NO, Shaw J, Adya AK et al. 2008. A plant virus movement protein forms ringlike complexes with the major nucleolar protein, fibrillarin. in vitro. J. Mol. Biol. 376:4932–37
    [Google Scholar]
  71. 71. 
    Gómez 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. 78:1810104–10
    [Google Scholar]
  72. 72. 
    Opalka N, Brugidou C, Bonneau C, Nicole M, Beachy RN et al. 1998. Movement of rice yellow mottle virus between xylem cells through pit membranes. PNAS 95:63323–28
    [Google Scholar]
  73. 73. 
    Wan J, Cabanillas DG, Zheng H, Laliberté JF 2015. Turnip mosaic virus moves systemically through both phloem and xylem as membrane-associated complexes. Plant Physiol 167:41374–88
    [Google Scholar]
  74. 74. 
    Verchot J, Driskel BA, Zhu Y, Hunger RM, Littlefield LJ 2001. Evidence that soilborne wheat mosaic virus moves long distance through the xylem in wheat. Protoplasma 218:1–257–66
    [Google Scholar]
  75. 75. 
    Fisher DB, Wu Y, Ku MSB 1992. Turnover of soluble proteins in the wheat sieve tube. Plant Physiol 100:31433–41
    [Google Scholar]
  76. 76. 
    Sasaki T, Chino M, Hayashi H, Fujiwara T 1998. Detection of several mRNA species in rice phloem sap. Plant Cell Physiol 39:8895–97
    [Google Scholar]
  77. 77. 
    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. 53:369631–37
    [Google Scholar]
  78. 78. 
    Asano T, Masumura T, Kusano H, Kikuchi S, Kurita A 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 32:401–8
    [Google Scholar]
  79. 79. 
    Nelson T, Tausta SL, Gandotra N, Liu T 2006. Laser microdissection of plant tissue: What you see is what you get. Annu. Rev. Plant Biol. 57:181–201
    [Google Scholar]
  80. 80. 
    Faulkner C, Bayer MF. 2017. Isolation of plasmodesmata. Isolation of Plant Organelles and Structures: Methods and Protocols NL Taylor, AH Millar 187–98 New York: Humana
    [Google Scholar]
  81. 81. 
    Maule AJ, Benitez-Alfonso Y, Faulkner C 2011. Plasmodesmata—membrane tunnels with attitude. Curr. Opin. Plant Biol. 14:6683–90
    [Google Scholar]
  82. 82. 
    Stonebloom S, Burch-Smith T, Kim I, Meinke D, Mindrinos M, Zambryski P 2009. Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. PNAS 106:4017229–34
    [Google Scholar]
  83. 83. 
    Malter D, Wolf S. 2011. Melon phloem-sap proteome: developmental control and response to viral infection. Protoplasma 248:217–24
    [Google Scholar]
  84. 84. 
    Serra-Soriano M, Navarro JA, Genoves A, Pallás V 2015. Comparative proteomic analysis of melon phloem exudates in response to viral infection. J. Proteom. 124:11–24
    [Google Scholar]
  85. 85. 
    Ruiz-Medrano R, Moya JH, Xoconostle-Cázares B, Lucas WJ 2007. Influence of cucumber mosaic virus infection on the mRNA population present in the phloem translocation stream of pumpkin plants. Funct. Plant Biol. 34:4292–301
    [Google Scholar]
  86. 86. 
    Miozzi L, Napoli C, Sardo L, Accotto GP 2014. Transcriptomics of the interaction between the monopartite phloem-limited geminivirus tomato yellow leaf curl sardinia virus and Solanum lycopersicum highlights a role for plant hormones, autophagy and plant immune system fine tuning during infection. PLOS ONE 9:2e89951
    [Google Scholar]
  87. 87. 
    Shen J, Chen X, Chen J, Sun L 2016. A phloem-limited fijivirus induces the formation of neoplastic phloem tissues that house virus multiplication in the host plant. Sci. Rep. 6:2984829848
    [Google Scholar]
  88. 88. 
    Cheng C, Zhang Y, Zhong Y, Yang J, Yan S 2016. Gene expression changes in leaves of Citrus sinensis (L.) Osbeck infected by Citrus tristeza virus. J. Hortic. Sci. . Biotechnol 91:5466–75
    [Google Scholar]
  89. 89. 
    Mustroph A, Zanetti ME, Jang CJH, Holtan HE, Repetti PP et al. 2009. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. . PNAS 106:4418843–48
    [Google Scholar]
  90. 90. 
    Reynoso M, Juntawong P, Lancia M, Blanco F, Bailey-Serres J, Zanetti ME 2015. Translating ribosome affinity purification (TRAP) followed by RNA sequencing technology (TRAP-SEQ) for quantitative assessment of plant translatomes. Plant Functional Genomics JM Alonso, AN Stepanova 257–85Methods Mol. Biol. Vol. 1284 New York: Humana
    [Google Scholar]
  91. 91. 
    Yu K, Soares JM, Mandal MK, Wang C, Chanda B et al. 2013. A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep 3:1266–78
    [Google Scholar]
  92. 92. 
    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 328:5980872–75
    [Google Scholar]
  93. 93. 
    Czech B, Hannon GJ. 2011. Small RNA sorting: matchmaking for argonautes. Nat. Rev. Genet. 12:19–31
    [Google Scholar]
  94. 94. 
    Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y 2008. The mechanism selecting the guide strand from small RNA duplexes is different among Argonaute proteins. Plant Cell Physiol 49:4493–500
    [Google Scholar]
  95. 95. 
    Padmanabhan MS, Goregaoker SP, Golem S, Shiferaw H, Culver JN 2005. Interaction of the Tobacco mosaic virus replicase protein with the Aux/IAA protein PAP1/IAA26 is associated with disease development. J. Virol. 79:42549–58
    [Google Scholar]
  96. 96. 
    Padmanabhan MS, Kramer SR, Wang X, Culver JN 2008. Tobacco mosaic virus replicase-auxin/indole acetic acid protein interactions: reprogramming the auxin response pathway to enhance virus infection. J. Virol. 82:52477–85
    [Google Scholar]
  97. 97. 
    Padmanabhan MS, Shiferaw H, Culver JN 2006. The Tobacco mosaic virus replicase protein disrupts the localization and function of interacting Aux/IAA proteins. Mol. Plant-Microbe Interact. 19:8864–73
    [Google Scholar]
  98. 98. 
    Collum TD, Padmanabhan MS, Hsieh Y-C, Culver JN 2016. Tobacco mosaic virus-directed reprogramming of auxin/indole acetic acid protein transcriptional responses enhances virus phloem loading. PNAS 113:19E2740–2740
    [Google Scholar]
  99. 99. 
    Dorokhov YL, Komarova TV, Petrunia IV, Frolova OY, Pozdyshev DV, Gleba YY 2012. Airborne signals from a wounded leaf facilitate viral spreading and induce antibacterial resistance in neighboring plants. PLOS Pathog 8:4e1002640
    [Google Scholar]
  100. 100. 
    Chen MH, Citovsky V. 2003. Systemic movement of a tobamovirus requires host cell pectin methylesterase. Plant J 35:3386–92
    [Google Scholar]
  101. 101. 
    Brandner K, Sambade A, Boutant E, Didier P, Mély Y et al. 2008. Tobacco mosaic virus movement protein interacts with green fluorescent protein-tagged microtubule end-binding protein. Plant Physiol 147:611–23
    [Google Scholar]
  102. 102. 
    Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L et al. 2010. A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLOS Pathog 6:9e1001119
    [Google Scholar]
  103. 103. 
    Micheli F. 2001. Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:9414–19
    [Google Scholar]
  104. 104. 
    Dorokhov YL, Mäkinen K, Frolova OY, Merits A, Saarinen J et al. 1999. A novel function for a ubiquitous plant enzyme pectin methylesterase: the host-cell receptor for the tobacco mosaic virus movement protein. FEBS Lett 461:3223–28
    [Google Scholar]
  105. 105. 
    Chen MH, Sheng J, Hind G, Handa AK, Citovsky V 2000. Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J 19:5913–20
    [Google Scholar]
  106. 106. 
    Dorokhov YL, Sheshukova EV, Komarova TV 2018. Methanol in plant life. Front. Plant Sci. 9:1623
    [Google Scholar]
  107. 107. 
    Ueki S, Citovsky V. 2002. The systemic movement of a tobamovirus is inhibited by a cadmium-ion-induced glycine-rich protein. Nat. Cell Biol. 4:7478–85
    [Google Scholar]
  108. 108. 
    Citovsky V, Ghoshroy S, Tsui F, Klessig D 1998. Non-toxic concentrations of cadmium inhibit systemic movement of turnip vein clearing virus by a salicylic acid-independent mechanism. Plant J 16:113–20
    [Google Scholar]
  109. 109. 
    Iglesias VA, Meins F. 2000. Movement of plant viruses is delayed in a β-1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J 21:2157–66
    [Google Scholar]
  110. 110. 
    Ueki S, Citovsky V. 2005. Identification of an interactor of cadmium ion-induced glycine-rich protein involved in regulation of callose levels in plant vasculature. PNAS 102:3412089–94
    [Google Scholar]
  111. 111. 
    Kittelmann K, Rau P, Gronenborn B, Jeske H 2009. Plant geminivirus Rep protein induces rereplication in fission yeast. J. Virol. 83:136769–78
    [Google Scholar]
  112. 112. 
    Xie Q, Suárez-López P, Gutiérrez C 1995. Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus: requirement for efficient viral DNA replication. EMBO J 14:164073–82
    [Google Scholar]
  113. 113. 
    Xie L, Lv MF, Zhang HM, Yang J, Li JM, Chen JP 2014. Tumours induced by a plant virus are derived from vascular tissue and have multiple intercellular gateways that facilitate virus movement. J. Exp. Bot. 65:174873–86
    [Google Scholar]
  114. 114. 
    Heil M, Ton J. 2008. Long-distance signalling in plant defence. Trends Plant Sci 13:6264–72
    [Google Scholar]
  115. 115. 
    Huber AE, Bauerle TL. 2016. Long-distance plant signaling pathways in response to multiple stressors: the gap in knowledge. J. Exp. Bot. 67:72063–79
    [Google Scholar]
  116. 116. 
    Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE 2013. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500:7463422–26
    [Google Scholar]
  117. 117. 
    Calil IP, Fontes EPB. 2017. Plant immunity against viruses: antiviral immune receptors in focus. Ann. Bot. 119:5711–23
    [Google Scholar]
  118. 118. 
    Mandadi KK, Scholthof KBG. 2013. Plant immune responses against viruses: How does a virus cause disease. ? Plant Cell 25:51489–505
    [Google Scholar]
  119. 119. 
    Ádám AL, Nagy Z, Kátay G, Mergenthaler E, Viczián O 2018. Signals of systemic immunity in plants: progress and open questions. Int. J. Mol. Sci. 19:1146
    [Google Scholar]
  120. 120. 
    Aragones CG, Sanchez-Pina MA, Diaz-Pendon JA, Pena EJ, Heinlein M, Martin-Hernandez AM 2016. cmv1 is a gate for Cucumber mosaic virus transport from bundle sheath cells to phloem in melon. Mol. Plant Pathol. 17:6973–84
    [Google Scholar]
  121. 121. 
    Decroocq V, Sicard O, Alamillo JM, Lansac M, Eyquard JP et al. 2006. Multiple resistance traits control Plum pox virus infection in Arabidopsis thaliana. Mol. . Plant-Microbe Interact 19:5541–49
    [Google Scholar]
  122. 122. 
    Revers F, Guiraud T, Houvenaghel MC, Mauduit T, Le Gall O, Candresse T 2003. Multiple resistance phenotypes to Lettuce mosaic virus among Arabidopsis thaliana accessions. Mol. Plant-Microbe Interact. 16:7608–16
    [Google Scholar]
  123. 123. 
    Chisholm ST, Parra MA, Anderberg RJ, Carrington JC 2001. Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of tobacco etch virus. Plant Physiol 127:41667–75
    [Google Scholar]
  124. 124. 
    Cosson P, Schurdi-Levraud V, Le QH, Sicard O, Caballero M et al. 2012. The RTM resistance to potyviruses in Arabidopsis thaliana: natural variation of the RTM genes and evidence for the implication of additional genes. PLOS ONE 7:6e39169
    [Google Scholar]
  125. 125. 
    Cayla T, Batailler B, Le Hir R, Revers F, Anstead JA et al. 2015. Live imaging of companion cells and sieve elements in Arabidopsis leaves. PLOS ONE 10:2e0118122
    [Google Scholar]
  126. 126. 
    Miller G, Schlauch K, Tam R, Cortes D, Torres MA et al. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Plant Biol 2:84ra45
    [Google Scholar]
  127. 127. 
    Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R 2011. Respiratory burst oxidases: the engines of ROS signaling. Curr. Opin. Plant Biol. 14:691–99
    [Google Scholar]
  128. 128. 
    Sun YD, Folimonova SY. 2019. The p33 protein of Citrus tristeza virus affects viral pathogenicity by modulating a host immune response. New Phytol 221:42039–53
    [Google Scholar]
  129. 129. 
    Hyodo K, Hashimoto K, Kuchitsu K, Suzuki N, Okuno T 2017. Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus. PNAS 114:7E1282–1282
    [Google Scholar]
  130. 130. 
    Kovalchuk I, Kovalchuk O, Kalck V, Boyko V, Filkowski J et al. 2003. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423:6941760–62
    [Google Scholar]
  131. 131. 
    Brakke MK. 1984. Mutations, the abberant ratio phenomenon, and virus infection of maize. Annu. Rev. Phytopathol. 22:177–94
    [Google Scholar]
  132. 132. 
    Boyko A, Kathiria P, Zemp FJ, Yao Y, Pogribny I, Kovalchuk I 2007. Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virus-induced plant genome instability). Nucleic Acids Res 35:51714–25
    [Google Scholar]
  133. 133. 
    Kathiria P, Sidler C, Golubov A, Kalischuk M, Kawchuk LM, Kovalchuk I 2010. Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol 153:41859–70
    [Google Scholar]
  134. 134. 
    Wang C, Wang C, Zou J, Yang Y, Li Z, Zhu S 2019. Epigenetics in the plant-virus interaction. Plant Cell Rep 38:1031–38
    [Google Scholar]
  135. 135. 
    Mason G, Noris E, Lanteri S, Acquadro A, Accotto GP, Portis E 2008. Potentiality of methylation-sensitive amplification polymorphism (MSAP) in identifying genes involved in tomato response to tomato yellow leaf curl Sardinia virus. Plant Mol. Biol. Report. 26:156–73
    [Google Scholar]
  136. 136. 
    Wang C, Wang C, Xu W, Zou J, Qiu Y et al. 2018. Epigenetic changes in the regulation of Nicotiana tabacum response to Cucumber mosaic virus infection and symptom recovery through single-base resolution methylomes. Viruses 10:8402
    [Google Scholar]
  137. 137. 
    Muhammad T, Zhang F, Zhang Y, Liang Y 2019. RNA interference: a natural immune system of plants to counteract biotic stressors. Cells 8:38
    [Google Scholar]
  138. 138. 
    Ham BK, Li G, Jia W, Leary JA, Lucas WJ 2014. Systemic delivery of siRNA in pumpkin by a plant PHLOEM SMALL RNA-BINDING PROTEIN 1-ribonucleoprotein complex. Plant J 80:683–94
    [Google Scholar]
  139. 139. 
    Csorba T, Kontra L, Burgyán J 2015. Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–80:85–103
    [Google Scholar]
  140. 140. 
    Havelda Z, Hornyik C, Crescenzi A, Burgyan J 2003. In situ characterization of Cymbidium ringspot tombusvirus infection-induced posttranscriptional gene silencing in Nicotiana benthamiana. J. Virol 77:106082–86
    [Google Scholar]
  141. 141. 
    Kasschau KD, Carrington JC. 2001. Long-distance movement and replication maintenance functions correlate with silencing suppression activity of potyviral HC-Pro. Virology 285:171–81
    [Google Scholar]
  142. 142. 
    Baumberger N, Tsai CH, Lie M, Havecker E, Baulcombe DC 2007. The polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17:181609–14
    [Google Scholar]
  143. 143. 
    Burgyán J, Havelda Z. 2011. Viral suppressors of RNA silencing. Trends Plant Sci 16:5265–72
    [Google Scholar]
  144. 144. 
    Lacombe S, Bangratz M, Vignols F, Brugidou C 2010. The rice yellow mottle virus P1 protein exhibits dual functions to suppress and activate gene silencing. Plant J 61:371–82
    [Google Scholar]
  145. 145. 
    Islam W, Naveed H, Zaynab M, Huang Z, Chen HYH 2019. Plant defense against virus diseases; growth hormones in highlights. Plant Signal. Behav. 14:61596719
    [Google Scholar]
  146. 146. 
    Collum TD, Culver JN. 2016. The impact of phytohormones on virus infection and disease. Curr. Opin. Virol. 17:25–31
    [Google Scholar]
  147. 147. 
    Wang X, Sager R, Cui W, Zhang C, Lu H, Lee JY 2013. Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. . Plant Cell 25:62315–29
    [Google Scholar]
  148. 148. 
    Oide S, Bejai S, Staal J, Guan N, Kaliff M, Dixelius C 2013. A novel role of PR2 in abscisic acid (ABA) mediated, pathogen-induced callose deposition in Arabidopsis thaliana. . New Phytol 200:1187–99
    [Google Scholar]
  149. 149. 
    Felle HH, Zimmermann MR. 2007. Systemic signalling in barley through action potentials. Planta 226:203–14
    [Google Scholar]
  150. 150. 
    Volkov AG. 2006. Plant Electrophysiology: Theory and Methods Berlin: Springer-Verlag
    [Google Scholar]
  151. 151. 
    Paulmann MK, Kunert G, Zimmermann MR, Theis N, Ludwig A et al. 2018. Barley yellow dwarf virus infection leads to higher chemical defense signals and lower electrophysiological reactions in susceptible compared to tolerant barley genotypes. Front. Plant Sci. 9:145
    [Google Scholar]
  152. 152. 
    Hokkanen A, Stuns I, Schmid P, Kokkonen A, Gao F et al. 2015. Microfluidic sampling system for tissue analytics. Biomicrofluidics 9:5054109
    [Google Scholar]
  153. 153. 
    Yu F, Hunziker W, Choudhury D 2019. Engineering microfluidic organoid-on-a-chip platforms. Micromachines 10:3165
    [Google Scholar]
/content/journals/10.1146/annurev-virology-010320-072410
Loading
/content/journals/10.1146/annurev-virology-010320-072410
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