1932

Abstract

Although the phloem is a highly specialized tissue, certain pathogens, including phytoplasmas, spiroplasmas, and viruses, have evolved to access and live in this sequestered and protected environment, causing substantial economic harm. In particular, Liberibacter spp. are devastating citrus in many parts of the world. Given that most phloem pathogens are vectored, they are not exposed to applied chemicals and are therefore difficult to control. Furthermore, pathogens use the phloem network to escape mounted defenses. Our review summarizes the current knowledge of phloem anatomy, physiology, and biochemistry relevant to phloem/pathogen interactions. We focus on aspects of anatomy specific to pathogen movement, including sieve plate structure and phloem-specific proteins. Phloem sampling techniques are discussed. Finally, pathogens that cause particular harm to the phloem of crop species are considered in detail.

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2022-08-26
2024-06-16
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Literature Cited

  1. 1.
    Achor D, Welker S, Ben-Mahmoud S, Wang C, Folimonova SY et al. 2020. Dynamics of Candidatus Liberibacter asiaticus movement and sieve-pore plugging in citrus sink cells. Plant Physiol 182:882–91
    [Google Scholar]
  2. 2.
    Albrecht U, Bowman KD. 2008. Gene expression in Citrus sinensis (L.) Osbeck following infection with the bacterial pathogen Candidatus Liberibacter asiaticus causing Huanglongbing in Florida. Plant Sci 175:291–306
    [Google Scholar]
  3. 3.
    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 86:1089–94
    [Google Scholar]
  4. 4.
    Aung K, Kim P, Li Z, Joe A, Kvitko B et al. 2020. Pathogenic bacteria target plant plasmodesmata to colonize and invade surrounding tissues. Plant Cell 32:595–611
    [Google Scholar]
  5. 5.
    Bendix C, Lewis JD. 2018. The enemy within: phloem-limited pathogens. Mol. Plant Pathol. 19:238–54
    [Google Scholar]
  6. 6.
    Bostwick DE, Dannenhoffer JM, Skaggs MI, Lister RM, Larkins BA, Thompson GA. 1992. Pumpkin phloem lectin genes are specifically expressed in companion cells. Plant Cell 4:1539–48
    [Google Scholar]
  7. 7.
    Bové JM. 2006. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J. Plant Pathol. 88:7–37
    [Google Scholar]
  8. 8.
    Buoso S, Pagliari L, Musetti R, Martini M, Marroni F et al. 2019.. ‘ Candidatus Phytoplasma solani’ interferes with the distribution and uptake of iron in tomato. BMC Genom 20:703
    [Google Scholar]
  9. 9.
    Chen Q, Payyavula RS, Chen L, Zhang J, Zhang C, Turgeon R. 2018. FLOWERING LOCUS T mRNA is synthesized in specialized companion cells in Arabidopsis and Maryland Mammoth tobacco leaf veins. PNAS 115:2830–35
    [Google Scholar]
  10. 10.
    Chen X, Yao Q, Gao X, Jiang C, Harberd P, Fu X. 2016. Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr. Biol. 26:640–46
    [Google Scholar]
  11. 11.
    Chen Y, Bendix C, Lewis JD. 2020. Comparative genomics screen identifies microbe-associated molecular patterns from Candidatus Liberibacter sp. that elicit immune responses in plants. Mol. Plant-Microbe Interact. 33:539–52
    [Google Scholar]
  12. 12.
    Cheval C, Faulkner C. 2018. Plasmodesmal regulation during plant-pathogen interactions. New Phytol 217:62–67
    [Google Scholar]
  13. 13.
    Clark AM, Jacobsen KR, Bostwick DE, Dannenhoffer JM, Skaggs MI, Thompson GA. 1997. Molecular characterization of a phloem-specific gene encoding the filament protein, Phloem Protein 1 (PP1), from Cucurbita maxima. Plant J 12:49–61
    [Google Scholar]
  14. 14.
    Clark K, Franco JY, Schwizer S, Pang Z, Hawara E et al. 2018. An effector from the Huanglongbing-associated pathogen targets citrus proteases. Nature Comm 9:1718
    [Google Scholar]
  15. 15.
    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:E2740–E49
    [Google Scholar]
  16. 16.
    Cowan GH, Roberts AG, Jones S, Kumar P, Kalyandurg PB et al. 2018. Potato mop-top virus co-opts the stress sensor HIPP26 for long-distance movement. Plant Physiol 176:2052–70
    [Google Scholar]
  17. 17.
    Cronshaw J 1975. P-proteins. Phloem Transport S Aronoff, J Dainty, PR Gorham, LM Srivastava, CA Swanson 79–115 Boston: Springer
    [Google Scholar]
  18. 18.
    Cronshaw J, Sabnis DD 1990. Phloem proteins. Sieve Elements: Comparative Structure, Induction and Development HD Behnke, RD Sjolund 257–83 Berlin/Heidelberg: Springer
    [Google Scholar]
  19. 19.
    Curtolo M, Pacheco ID, Boava LP, Takita MA, Granato LM et al. 2020. Wide-ranging transcriptomic analysis of Poncirus trifoliata, Citrus sunki, Citrus sinensis and contrasting hybrids reveals HLB tolerance mechanisms. Sci. Rep. 10:20865
    [Google Scholar]
  20. 20.
    Dalio RJD, Paschoal D, Arena GD, Magalhaes DM, Oliveira TS et al. 2021. Hypersensitive response: from NLR pathogen recognition to cell death response. Ann. Appl. Biol. 178:268–80
    [Google Scholar]
  21. 21.
    de Abreu-Neto JB, Turchetto-Zolet AC, de Oliveira LFV, Zanettini MHB, Margis-Pinheiro M. 2013. Heavy metal-associated isoprenylated plant protein (HIPP): characterization of a family of proteins exclusive to plants. FEBS J 280:1604–16
    [Google Scholar]
  22. 22.
    De Marco F, Pagliari L, Degola F, Buxa SV, Loschi A et al. 2016. Combined microscopy and molecular analyses show phloem occlusions and cell wall modifications in tomato leaves in response to “Candidatus Phytoplasma solani. .” J. Microsc. 263:212–25
    [Google Scholar]
  23. 23.
    Deng H, Achor D, Exteberria E, Yu Q, Du D et al. 2019. Phloem regeneration is a mechanism for Huanglongbing-tolerance of “Bearss” lemon and “LB8–9” Sugar Belle mandarin. Front. Plant Sci. 10:277
    [Google Scholar]
  24. 24.
    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]
  25. 25.
    Ding F, Duan Y, Paul C, Brlansky RH, Hartung JS. 2015. Localization and distribution of ‘Candidatus Liberibacter asiaticus’ in citrus and periwinkle by direct tissue blot immuno assay with an anti-OmpA polyclonal antibody. PLOS ONE 10:e0123939
    [Google Scholar]
  26. 26.
    Du P, Zhang C, Zou X, Zhu Z, Yan H, Wuriyanghan H, Li W. 2021.. “ Candidatus Liberibacter asiaticus” secretes nonclassically secreted proteins that suppress host hypersensitive cell death and induce expression of plant pathogenesis-related proteins. Appl. Environ. Microbiol. 87:e00019–21
    [Google Scholar]
  27. 27.
    Ehlers K, Knoblauch M, van Bel AJE. 2000. Ultrastructural features of well-preserved and injured sieve elements: Minute clamps keep the phloem transport conduits free for mass flow. Protoplasma 214:80–92
    [Google Scholar]
  28. 28.
    Eleftheriou EP 1990. Monocotyledons. Sieve Elements: Comparative Structure, Induction and Development HD Behnke, RD Sjolund 139–59 Berlin/Heidelberg: Springer
    [Google Scholar]
  29. 29.
    Esau K, Thorsch J. 1985. Sieve plate pores and plasmodesmata, the communication channels of the symplast: ultrastructural aspects and developmental relations. Am. J. Bot. 72:1641–53
    [Google Scholar]
  30. 30.
    Ernst AM, Jekat SB, Zielonka S, Müller B, Neumann U et al. 2012. Sieve element occlusion (SEO) genes encode structural phloem proteins involved in wound sealing of the phloem. PNAS 109:E1980–E89
    [Google Scholar]
  31. 31.
    Evert RF 1990. Dicotyledons. Sieve Elements: Comparative Structure, Induction and Development HD Behnke, RD Sjolund 103–37 Berlin: Springer
    [Google Scholar]
  32. 32.
    Evert RF, Eschrich W, Eichhorn SE. 1972. P-protein distribution in mature sieve elements of Cucurbita maxima. Planta 109:193–210
    [Google Scholar]
  33. 33.
    Fagoaga C, Pensabene-Bellavia G, Moreno P, Navarro L, Flores R, Pena L. 2011. Ectopic expression of the p23 silencing suppressor of Citrus tristeza virus differentially modifies viral accumulation and tropism in two transgenic woody hosts. Mol. Plant Pathol. 12:898–910
    [Google Scholar]
  34. 34.
    Fan J, Chen C, Yu Q, Khalaf A, Achor DS et al. 2012. Comparative transcriptional and anatomical analyses of tolerant rough lemon and susceptible sweet orange in response to ‘Candidatus Liberibacter asiaticus’ infection. Mol. Plant-Microbe Interact. 25:1396–407
    [Google Scholar]
  35. 35.
    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]
  36. 36.
    Froelich DR, Mullendore DL, Jensen KH, Ross-Elliott TJ, Anstead JA et al. 2011. Phloem ultrastructure and pressure flow: sieve-element-occlusion-related agglomerations do not affect translocation. Plant Cell 23:4428–45
    [Google Scholar]
  37. 37.
    Fu ZQ, Dong X. 2013. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64:839–63
    [Google Scholar]
  38. 38.
    Furch ACU, Hafke JB, Schulz A, van Bel AJE. 2007. Ca2+-mediated remote control of reversible sieve tube occlusion in Vicia faba. J. Exp. Bot. 58:2827–38
    [Google Scholar]
  39. 39.
    Furch ACU, Zimmermann MR, Will T, Hafke JB, van Bel AJE. 2010. Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J. Exp. Bot. 61:3697–708
    [Google Scholar]
  40. 40.
    Gai YP, 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]
  41. 41.
    Gai YP, Zhao HN, Zhao YN, Zhu BS, Yuan SS 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]
  42. 42.
    Gaupels F, Ghirardo A. 2013. The extrafascicular phloem is made for fighting. Front. Plant Sci. 4:187
    [Google Scholar]
  43. 43.
    Golecki B, Schulz A, Thompson GA. 1999. Translocation of structural P proteins in the phloem. Plant Cell 11:127–40
    [Google Scholar]
  44. 44.
    Gómez-Muñoz N, Velazquez K, Vives MC, Ruiz-Ruiz S, Pina JA et al. 2017. The resistance of sour orange to Citrus tristeza virus is mediated by both the salicylic acid and RNA silencing defence pathways. Mol. Plant Pathol. 18:1253–66
    [Google Scholar]
  45. 45.
    Gonella E, Tedeschi R, Crotti E, Alma A 2019. Multiple guests in a single host: interactions across symbiotic and phytopathogenic bacteria in phloem-feeding vectors—a review. Entomol. Exp. Appl. 167:171–85
    [Google Scholar]
  46. 46.
    Guo M, Tian F, Wamboldt Y, Alfano JR. 2009. The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Mol. Plant-Microbe Interact. 22:1069–80
    [Google Scholar]
  47. 47.
    Hao P, Liu C, Wang Y, Chen R, Tang M et al. 2008. Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol 146:1810–20
    [Google Scholar]
  48. 48.
    Hoshi A, Oshima K, Kakizawa S, Ishii Y, Ozeki J et al. 2009. A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. PNAS 106:6416–21
    [Google Scholar]
  49. 49.
    Huang C-Y, Araujo K, Sanchez JN, Kund G, Trumble J et al. 2021. A stable antimicrobial peptide with dual functions of treating and preventing citrus Huanglongbing. PNAS 118:6e2019628118
    [Google Scholar]
  50. 50.
    Huang W, MacLean AM, Sugio A, Maqbool A, Busscher M et al. 2021. Parasitic modulation of host development by ubiquitin-independent protein degradation. Cell 184:5201–14
    [Google Scholar]
  51. 51.
    Jarrell KF, McBride MJ. 2008. The surprisingly diverse ways that prokaryotes move. Nat. Rev. Microbiol. 6:466–76
    [Google Scholar]
  52. 52.
    Jiang Y, Zhang C-X, Chen R, He SY 2019. Challenging battles of plants with phloem-feeding insects and prokaryotic pathogens. PNAS 116:23390–97
    [Google Scholar]
  53. 53.
    Kappagantu M, Collum TD, Dardick C, Culver JN. 2020. Viral hacks of the plant vasculature: the role of phloem alterations in systemic virus infection. Annu. Rev. Virol. 7:351–70
    [Google Scholar]
  54. 54.
    Killiny N. 2019. Collection of the phloem sap, pros and cons. Plant Signal. Behav. 14:1618181
    [Google Scholar]
  55. 55.
    Kim J-S, Sagaram US, Burns JK, Li J-L, Wang N 2009. Response of sweet orange (Citrus sinensis) to ‘Candidatus Liberibacter asiaticus’ infection: microscopy and microarray analyses. Phytopathology 99:50–57
    [Google Scholar]
  56. 56.
    King RW, Zeevaart JAD. 1974. Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53:96–103
    [Google Scholar]
  57. 57.
    Kondhare KR, Patil NS, Banerjee AK. 2021. A historical overview of long-distance signalling in plants. J. Exp. Bot. 72:4218–36
    [Google Scholar]
  58. 58.
    Knoblauch J, Knoblauch M, Vasina VV, Peters WS. 2020. Sieve elements rapidly develop ‘nacreous walls’ following injury—a common wounding response?. Plant J 102:797–808
    [Google Scholar]
  59. 59.
    Knoblauch M, Knoblauch J, Mullendore DL, Savage JA, Babst BA et al. 2016. Testing the Münch hypothesis of long distance phloem transport in plants. eLife 5:e15341
    [Google Scholar]
  60. 60.
    Knoblauch M, Noll GA, Müller T, Prüfer D, Schneider-Hüther I et al. 2003. ATP-independent contractile proteins from plants. Nat. Mater. 2:600–3
    [Google Scholar]
  61. 61.
    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]
  62. 62.
    Knoblauch M, Peters WS, Ehlers K, van Bel AJ. 2001. Reversible calcium-regulated stopcocks in legume sieve tubes. Plant Cell 13:1221–30
    [Google Scholar]
  63. 63.
    Knoblauch M, Stubenrauch M, van Bel AJ, Peters WS. 2012. Forisome performance in artificial sieve tubes. Plant Cell Environ 35:1419–27
    [Google Scholar]
  64. 64.
    Knoblauch M, van Bel AJE. 1998. Sieve tubes in action. Plant Cell 10:35–50
    [Google Scholar]
  65. 65.
    Kuśnierczyk A, Winge P, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM. 2008. Towards global understanding of plant defence against aphids—timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ 31:1097–115
    [Google Scholar]
  66. 66.
    Lalonde S, Franceschi VR, Frommer WB 2007. Companion cells. Handbook of Plant Sciences K Roberts 190–95 Chichester, UK: Wiley
    [Google Scholar]
  67. 67.
    Lavy M, Estelle M 2016. Mechanisms of auxin signaling. Development 143:3226–29
    [Google Scholar]
  68. 68.
    Li J, Pang Z, Trivedi P, Zhou X, Ying X et al. 2017.. ‘ Candidatus Liberibacter asiaticus’ encodes a functional salicylic acid (SA) hydroxylase that degrades SA to suppress plant defenses. Mol. Plant-Microbe Interact. 30:620–30
    [Google Scholar]
  69. 69.
    Liu DD, Chao WM, Turgeon R. 2012. Transport of sucrose, not hexose, in the phloem. J. Exp. Bot. 63:4315–20
    [Google Scholar]
  70. 70.
    Liu Y, Lin T, Valencia MV, Zhang C, Lv Z. 2021. Unraveling the roles of vascular proteins using proteomics. Molecules 26:667
    [Google Scholar]
  71. 71.
    MacLean AM, Orlovskis Z, Kowitwanich K, Zdziarska AM, Angenent GC et al. 2014. Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. PLOS Biol 12:e1001835
    [Google Scholar]
  72. 72.
    Medina-Ortega KJ, Walker GP 2015. Faba bean forisomes can function in defence against generalist aphids. Plant Cell Environ 38:1167–77
    [Google Scholar]
  73. 73.
    Merfa MV, Pérez-López E, Naranjo E, Jain M, Gabriel DW, De La Fuente L. 2019. Progress and obstacles in culturing ‘Candidatus Liberibacter asiaticus’, the bacterium associated with Huanglongbing. Phytopathology 109:1092–101
    [Google Scholar]
  74. 74.
    Minato N, Himeno M, Hoshi A, Maejima K, Komatsu K et al. 2014. The phytoplasmal virulence factor TENGU causes plant sterility by downregulating of the jasmonic acid and auxin pathways. Sci. Rep. 4:7399
    [Google Scholar]
  75. 75.
    Mondal HA. 2020. Aphid saliva: a powerful recipe for modulating host resistance towards aphid clonal propagation. Arthropod-Plant Interact 14:547–58
    [Google Scholar]
  76. 76.
    Mullendore DL, Windt CW, van As H, Knoblauch M. 2010. Sieve tube geometry in relation to phloem flow. Plant Cell 22:579–93
    [Google Scholar]
  77. 77.
    Nakashima J, Laosinchai W, Cui X, Brown RM. 2003. New insight into the mechanism of cellulose and callose biosynthesis: proteases may regulate callose biosynthesis upon wounding. Cellulose 10:369–89
    [Google Scholar]
  78. 78.
    Nan J, Zhang S, Zhan P, Jiang L. 2021. Discovery of novel GMPS inhibitors of Candidatus Liberibacter asiaticus by structure based design and enzyme kinetic. Biology 10:594
    [Google Scholar]
  79. 79.
    Oparka KJ, Turgeon R 1999. Sieve elements and companion cells—traffic control centers of the phloem. Plant Cell 11:739–50
    [Google Scholar]
  80. 80.
    Owens RA, Blackburn M, Ding B. 2001. Possible involvement of the phloem lectin in long-distance viroid movement. Mol. Plant-Microbe Interact. 14:905–09
    [Google Scholar]
  81. 81.
    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. 19:864–73
    [Google Scholar]
  82. 82.
    Pagliaccia D, Shi JX, Pang ZQ, Hawara E, Clark K et al. 2017. A pathogen secreted protein as a detection marker for citrus Huanglongbing. Front. Microbiol. 8:2041
    [Google Scholar]
  83. 83.
    Pagliari L, Buoso S, Santi S, Furch ACU, Martini M et al. 2017. Filamentous sieve element proteins are able to limit phloem mass flow, but not phytoplasma spread. J. Exp. Bot. 68:3673–88
    [Google Scholar]
  84. 84.
    Pandy SS, Vasconcelos FNC, Wang N. 2021. Spatiotemporal dynamics of ‘Candidatus Liberibacter asiaticus’ colonization inside citrus plant and Huanglongbing disease development. Phytopathology 10:1094
    [Google Scholar]
  85. 85.
    Pang ZQ, Zhang L, Coaker G, Ma WB, He SY, Wang N 2020. Citrus CsACD2 is a target of Candidatus Liberibacter asiaticus in Huanglongbing disease. Plant Physiol 184:792–805
    [Google Scholar]
  86. 86.
    Pate JS, Sharkey PJ, Lewis OAM. 1974. Phloem bleeding from legume fruits: a technique for study of fruit nutrition. Planta 120:229–43
    [Google Scholar]
  87. 87.
    Paultre DSG, Gustin MP, 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]
  88. 88.
    Pelissier HC, Peters WS, Collier R, Bel AJ, Knoblauch M. 2008. GFP tagging of sieve element occlusion (SEO) proteins results in green fluorescent forisomes. Plant Cell Physiol 49:1699–710
    [Google Scholar]
  89. 89.
    Peng AH, Zou XP, He YR, Chen SC, Liu XF et al. 2021. Overexpressing a NPR1-like gene from Citrus paradisi enhanced Huanglongbing resistance in C. sinensis. Plant Cell Rep 40:529–41
    [Google Scholar]
  90. 90.
    Peters WS, Knoblauch M, Warmann SA, Pickard WF, Shen AQ. 2008. Anisotropic contraction in forisomes: simple models won't fit. Cell Motil. Cytoskelet. 65:368–78
    [Google Scholar]
  91. 91.
    Raiol-Junior LL, Cifuentes-Arenas JC, Cunniffe NJ, Turgeon R, Lopes SA. 2021. Modelling ‘Candidatus Liberibacter asiaticus’ movement within citrus plants. Phytopathology 111:101711–19
    [Google Scholar]
  92. 92.
    Read SM, Northcote DH. 1983. Subunit structure and interactions of the phloem proteins of Cucurbita maxima (pumpkin). Eur. J. Biochem. 134:561–69
    [Google Scholar]
  93. 93.
    Reyes-Caldas PA, Zhu J, Breakspear A, Thapa SP, Toruno T et al. 2021. Effectors from a bacterial vector-borne pathogen exhibit diverse subcellular localization, expression profiles and manipulation of plant defense. bioRxiv 459857. https://doi.org/10.1101/2021.09.10.459857
    [Crossref]
  94. 94.
    Ross-Elliott TJ, Jensen KH, Haaning KS, Wager BM, Knoblauch J et al. 2017. Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. eLife 6:e24125
    [Google Scholar]
  95. 95.
    Rüping B, Ernst AM, Jekat SB, Nordzieke S, Reineke AR et al. 2010. Molecular and phylogenetic characterization of the sieve element occlusion gene family in Fabaceae and non-Fabaceae plants. BMC Plant Biol 10:219
    [Google Scholar]
  96. 96.
    Saheed SA, Cierlik I, Larsson KA, Delp G, Bradley G, Jonsson LM, Botha CE. 2009. Stronger induction of callose deposition in barley by Russian wheat aphid than bird cherry-oat aphid is not associated with differences in callose synthase or β-1,3-glucanase transcript abundance. Physiol. Plant. 135:150–61
    [Google Scholar]
  97. 97.
    Santi S, Grisan S, Pierasco A, De Marco F, Musetti R. 2013. Laser microdissection of grapevine leaf phloem infected by stolbur reveals site-specific gene responses associated to sucrose transport and metabolism. Plant Cell Environ 36:343–55
    [Google Scholar]
  98. 98.
    Schreiber KJ, Chau-Ly IJ, Lewis JD 2021. What the wild things do: mechanisms of plant host manipulation by bacterial type III-secreted effector proteins. Microorganisms 9:48
    [Google Scholar]
  99. 99.
    Schulz A 1990. Wound sieve elements. Sieve Elements HD Behnke, RD Sjolund 199–217 Berlin/Heidelberg: Springer
    [Google Scholar]
  100. 100.
    Selvaraj V, Maheshwari Y, Hajeri S, Chen JC, McCollum TG, Yokomi R. 2018. Development of a duplex droplet digital PCR assay for absolute quantitative detection of “Candidatus Liberibacter asiaticus. .” PLOS ONE 13:e0197184
    [Google Scholar]
  101. 101.
    Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA. 2011. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. PNAS 108:E1254–E63
    [Google Scholar]
  102. 102.
    Sui X, Nie J, Li X, Scanlon MJ, Zjang C, Zheng Y, Ma S et al. 2018. Transcriptomic and functional analysis of cucumber (Cucumis sativus L.) fruit phloem during early development. Plant J 96:982–96
    [Google Scholar]
  103. 103.
    Sui X, Nie J, Lin T, Yao X, Turgeon R. 2021. Complexity untwined: the structure and function of cucumber (Cucumis sativus L.) shoot phloem. Plant J 106:1163–76
    [Google Scholar]
  104. 104.
    Sun YD, Folimonova SY. 2019. The p33 protein of Citrus tristeza virus affects viral pathogenicity by modulating a host immune response. New Phytol 221:2039–53
    [Google Scholar]
  105. 105.
    Tatineni S, French R. 2014. The C-terminus of Wheat streak mosaic virus coat protein is involved in differential infection of wheat and maize through host-specific long-distance transport. Mol. Plant-Microbe Interact. 27:150–62
    [Google Scholar]
  106. 106.
    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]
  107. 107.
    Tomlinson PB, Huggett BA. 2012. Cell longevity and sustained primary growth in palm stems. Am. J. Bot. 99:1891–902
    [Google Scholar]
  108. 108.
    Turgeon R. 2010. The puzzle of phloem pressure. Plant Physiol 154:578–81
    [Google Scholar]
  109. 109.
    van Bel AJE, Furch ACU, Will T, Buxa SV, Musetti R, Hafke JB. 2014. Spread the news: systemic dissemination and local impact of Ca2+ signals along the phloem pathway. J. Exp. Bot. 65:1761–87
    [Google Scholar]
  110. 110.
    van Bel AJE, Musetti R. 2019. Sieve element biology provides leads for research on phytoplasma lifestyle in plant hosts. J. Exp. Bot. 70:3737–55
    [Google Scholar]
  111. 111.
    Venturuzzi AL, Rodriguez MC, Conti G, Leone M, Caro MD et al. 2021. Negative modulation of SA signaling components by the capsid protein of tobacco mosaic virus is required for viral long-distance movement. Plant J 106:896–912
    [Google Scholar]
  112. 112.
    Verma DP, Hong Z. 2001. Plant callose synthase complexes. Plant Mol. Biol. 47:693–701
    [Google Scholar]
  113. 113.
    Walker GP, Medina-Ortega KJ. 2012. Penetration of faba bean sieve elements by pea aphid does not trigger forisome dispersal. Entomol. Exp. Appl. 144:326–35
    [Google Scholar]
  114. 114.
    Wang N, Trivedi P. 2013. Citrus Huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 103:652–65
    [Google Scholar]
  115. 115.
    Wergin WP, Newcomb EH. 1970. Formation and dispersal of crystalline P-protein in sieve elements of soybean (Glycine max L.). Protoplasma 71:365–88
    [Google Scholar]
  116. 116.
    Will T, Furch ACU, Zimmermann MR. 2013. How phloem-feeding insects face the challenge of phloem-located defenses. Front. Plant Sci. 4:336
    [Google Scholar]
  117. 117.
    Will T, Tjallingii WF, Thönnessen A, van Bel AJE. 2007. Molecular sabotage of plant defense by aphid saliva. PNAS 104:10536–41
    [Google Scholar]
  118. 118.
    Wu J, Alferez FM, Johnson EG, Graham JH 2018. Up-regulation of PR1 and less disruption of hormone and sucrose metabolism in roots is associated with lower susceptibility to “Candidatus Liberibacter asiaticus.”. Plant Pathol. 67:1426–35
    [Google Scholar]
  119. 119.
    Xia C, Zhang C 2020. Long-distance movement of mRNAs in plants. Plants 9:731
    [Google Scholar]
  120. 120.
    Xie B, Wang X, Zhu M, Zhang Z, Hong Z. 2011. CalS7 encodes a callose synthase responsible for callose deposition in the phloem. Plant J 65:1–14
    [Google Scholar]
  121. 121.
    Xu Q, Ren Y, Liesche J. 2019. Studying phloem loading with EDTA-facilitated phloem exudate collection and analysis. Methods Mol. Biol. 2014:125–32
    [Google Scholar]
  122. 122.
    Yu QB, Chen CX, Du DL, Huang M, Yao JQ et al. 2017. Reprogramming of a defense signaling pathway in rough lemon and sweet orange is a critical element of the early response to ‘Candidatus Liberibacter asiaticus. ’. Hortic. Res. 4:17063d
    [Google Scholar]
  123. 123.
    Zhang B, Tolstikov V, Turnbull C, Hicks LM, Fiehn O. 2010. Divergent metabolome and proteome suggest functional independence of dual phloem transport systems in cucurbits. PNAS 107:13532–37
    [Google Scholar]
  124. 124.
    Zhang C, Du PX, Yan HL, Zhu ZC, Wang XF, Li WM. 2020. A Sec-dependent secretory protein of the Huanglongbing-associated pathogen suppresses hypersensitive cell death in Nicotiana benthamiana. Front. Microbiol. 11:11
    [Google Scholar]
  125. 125.
    Zhang C, Yu X, Ayre BG, Turgeon R. 2012. The origin and composition of cucurbit “phloem” exudate. Plant Physiol 158:1873–82
    [Google Scholar]
  126. 126.
    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]
  127. 127.
    Zhao H, Sun R, Albrecht U, Padmanabhan C, Wang A et al. 2013. Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus Huanglongbing disease. Mol. Plant 6:301–10
    [Google Scholar]
  128. 128.
    Zhao PZ, Yao XM, Cai CX, Li R, Du J et al. 2019. Viruses mobilize plant immunity to deter nonvector insect herbivores. Sci. Adv. 5:14
    [Google Scholar]
  129. 129.
    Zielonka S, Ernst AM, Hawat S, Twyman RM, Prüfer D et al. 2014. Characterization of five subgroups of the sieve element occlusion gene family in Glycine max reveals genes encoding non-forisome P-proteins, forisomes and forisome tails. Plant Mol. Biol. 86:51–67
    [Google Scholar]
  130. 130.
    Zimmermann MH, Ziegler H 1975. List of sugars and sugar alcohols in sieve-tube exudates. Transport in Plants I. Phloem Transport, eds. MH Zimmermann, JA Milburn 480–503 New York Springer-Verlag:
    [Google Scholar]
  131. 131.
    Zimmermann MR, Hafke JB, van Bel AJE, Furch ACU. 2013. Interaction of xylem and phloem during exudation and wound occlusion in Cucurbita maxima. Plant Cell Environ 36:237–47
    [Google Scholar]
  132. 132.
    Zschiesche W, Barth O, Daniel K, Bohme S, Rausche J, Humbeck K. 2015. The zinc-binding nuclear protein HIPP3 acts as an upstream regulator of the salicylate-dependent plant immunity pathway and of flowering time in Arabidopsis thaliana. New Phytol 207:1084–96
    [Google Scholar]
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