1932

Abstract

A group of aggressive pathogens have evolved to colonize the plant xylem. In this vascular tissue, where water and nutrients are transported from the roots to the rest of the plant, pathogens must be able to thrive under acropetal xylem sap flow and scarcity of nutrients while having direct contact only with predominantly dead cells. Nevertheless, a few bacteria have adapted to exclusively live in the xylem, and various pathogens may colonize other plant niches without causing symptoms unless they reach the xylem. Once established, the pathogens modulate its physicochemical conditions to enhance their growth and virulence. Adaptation to the restrictive lifestyle of the xylem leads to genome reduction in xylem-restricted bacteria, as they have a higher proportion of pseudogenes in their genome. The basis of xylem adaptation is not completely understood; therefore, a need still exists for model systems to advance the knowledge on this topic.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021021-041716
2022-08-26
2024-05-10
Loading full text...

Full text loading...

/deliver/fulltext/phyto/60/1/annurev-phyto-021021-041716.html?itemId=/content/journals/10.1146/annurev-phyto-021021-041716&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Atsumi T, Maekawa Y, Yamada T, Kawagishi I, Imae Y, Homma M. 1996. Effect of viscosity on swimming by the lateral and polar flagella of Vibrio alginolyticus. J. Bacteriol. 178:5024–26
    [Google Scholar]
  2. 2.
    Bae C, Han SW, Song YR, Kim BY, Lee HJ et al. 2015. Infection processes of xylem-colonizing pathogenic bacteria: possible explanations for the scarcity of qualitative disease resistance genes against them in crops. Theor. Appl. Genet. 128:1219–29
    [Google Scholar]
  3. 3.
    Bahar O, De La Fuente L, Burdman S. 2010. Assessing adhesion, biofilm formation and motility of Acidovorax citrulli using microfluidic flow chambers. FEMS Microbiol. Lett. 312:33–39
    [Google Scholar]
  4. 4.
    Bahar O, Goffer T, Burdman S. 2009. Type IV pili are required for virulence, twitching motility, and biofilm formation of Acidovorax avenae subsp. citrulli. Mol. Plant-Microbe Interact. 22:909–20
    [Google Scholar]
  5. 5.
    Benhamou N, Garand C. 2001. Cytological analysis of defense-related mechanisms induced in pea root tissues in response to colonization by nonpathogenic Fusarium oxysporum Fo47. Phytopathology 91:730–40
    [Google Scholar]
  6. 6.
    Bentrup F-W. 2017. Water ascent in trees and lianas: the cohesion-tension theory revisited in the wake of Otto Renner. Protoplasma 254:627–33
    [Google Scholar]
  7. 7.
    Berry MC, McGhee GC, Zhao Y, Sundin GW. 2009. Effect of a waaL mutation on lipopolysaccharide composition, oxidative stress survival, and virulence in Erwinia amylovora. FEMS Microbiol. Lett. 291:80–87
    [Google Scholar]
  8. 8.
    Bollard EG. 1960. Transport in the xylem. Annu. Rev. Plant Physiol. 11:141–66
    [Google Scholar]
  9. 9.
    Bové J, Garnier M. 2003. Phloem-and xylem-restricted plant pathogenic bacteria. Plant Sci. 164:423–38
    [Google Scholar]
  10. 10.
    Brodersen CR, Roddy AB, Wason JW, McElrone AJ. 2019. Functional status of xylem through time. Annu. Rev. Plant Biol. 70:407–33
    [Google Scholar]
  11. 11.
    Burbank L, Mohammadi M, Roper MC. 2015. Siderophore-mediated iron acquisition influences motility and is required for full virulence of the xylem-dwelling bacterial phytopathogen Pantoeastewartii subsp. stewartii. Appl. Environ. Microbiol. 81:139–48
    [Google Scholar]
  12. 12.
    Caldwell D, Kim BS, Iyer-Pascuzzi AS. 2017. Ralstonia solanacearum differentially colonizes roots of resistant and susceptible tomato plants. Phytopathology 107:528–36
    [Google Scholar]
  13. 13.
    Chatterjee S, Almeida RPP, Lindow S. 2008. Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annu. Rev. Phytopathol. 46:243–71
    [Google Scholar]
  14. 14.
    Chatterjee S, Newman KL, Lindow SE. 2008. Cell-to-cell signaling in Xylella fastidiosa suppresses movement and xylem vessel colonization in grape. Mol. Plant-Microbe Interact. 21:1309–15
    [Google Scholar]
  15. 15.
    Chatterjee S, Wistrom C, Lindow SE. 2008. A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. PNAS 105:2670–75
    [Google Scholar]
  16. 16.
    Cheetham SW, Faulkner GJ, Dinger ME. 2020. Overcoming challenges and dogmas to understand the functions of pseudogenes. Nat. Rev. Genet. 21:191–201
    [Google Scholar]
  17. 17.
    Chen J-Y, Liu C, Gui Y-J, Si K-W, Zhang D-D et al. 2018. Comparative genomics reveals cotton-specific virulence factors in flexible genomic regions in Verticillium dahliae and evidence of horizontal gene transfer from Fusarium. New Phytol. 217:756–70
    [Google Scholar]
  18. 18.
    Chen LQ. 2014. SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol. 201:1150–55
    [Google Scholar]
  19. 19.
    Choat B, Jansen S, Zwieniecki MA, Smets E, Holbrook NM. 2004. Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. J. Exp. Bot. 55:1569–75
    [Google Scholar]
  20. 20.
    Choi HK, Iandolino A, da Silva FG, Cook DR. 2013. Water deficit modulates the response of Vitis vinifera to the Pierce's disease pathogen Xylella fastidiosa. Mol. Plant-Microbe Interact. 26:643–57
    [Google Scholar]
  21. 21.
    Clifford JC, Rapicavoli JN, Roper MC. 2013. A rhamnose-rich O-antigen mediates adhesion, virulence, and host colonization for the xylem-limited phytopathogen Xylella fastidiosa. Mol. Plant-Microbe Interact. 26:676–85
    [Google Scholar]
  22. 22.
    Cobine PA, Cruz LF, Navarrete F, Duncan D, Tygart M, De La, Fuente L. 2013. Xylella fastidiosa differentially accumulates mineral elements in biofilm and planktonic cells. PLOS ONE 8:e54936
    [Google Scholar]
  23. 23.
    Coleman JJ, Wasmann CC, Usami T, White GJ, Temporini ED et al. 2011. Characterization of the gene encoding pisatin demethylase (FoPDA1) in Fusarium oxysporum. Mol. Plant-Microbe Interact. 24:1482–91
    [Google Scholar]
  24. 24.
    Corral J, Sebastià P, Coll NS, Barbé J, Aranda J, Valls M. 2020. Twitching and swimming motility play a role in Ralstonia solanacearum pathogenicity. mSphere 5:e00740–19
    [Google Scholar]
  25. 25.
    Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711–45
    [Google Scholar]
  26. 26.
    Cruz LF, Cobine PA, De La, Fuente L. 2012. Calcium increases Xylella fastidiosa surface attachment, biofilm formation, and twitching motility. Appl. Environ. Microbiol. 78:1321–31
    [Google Scholar]
  27. 27.
    Cruz LF, Parker JK, Cobine PA, De La, Fuente L. 2014. Calcium-enhanced twitching motility in Xylella fastidiosa is linked to a single PilY1 homolog. Appl. Environ. Microbiol. 80:7176–85
    [Google Scholar]
  28. 28.
    Cursino L, Galvani CD, Athinuwat D, Zaini PA, Li Y et al. 2011. Identification of an operon, Pil-Chp, that controls twitching motility and virulence in Xylella fastidiosa. Mol. Plant-Microbe Interact. 24:1198–206
    [Google Scholar]
  29. 29.
    D'Attoma G, Morelli M, Saldarelli P, Saponari M, Giampetruzzi A et al. 2019. Ionomic differences between susceptible and resistant olive cultivars infected by Xylella fastidiosa in the outbreak area of Salento, Italy. Pathogens 8:272
    [Google Scholar]
  30. 30.
    Das A, Rangaraj N, Sonti RV. 2009. Multiple adhesin-like functions of Xanthomonas oryzae pv. oryzae are involved in promoting leaf attachment, entry, and virulence on rice. Mol. Plant-Microbe Interact. 22:73–85
    [Google Scholar]
  31. 31.
    Davey ME, O'Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847–67
    [Google Scholar]
  32. 32.
    de Jonge R, Bolton MD, Kombrink A, van den Berg GC, Yadeta KA, Thomma BP. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23:1271–82
    [Google Scholar]
  33. 33.
    De La Fuente L, Montanes E, Meng YZ, Li YX, Burr TJ et al. 2007. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber. Appl. Environ. Microbiol. 73:2690–96
    [Google Scholar]
  34. 34.
    De La Fuente L, Parker JK, Oliver JE, Granger S, Brannen PM et al. 2013. The bacterial pathogen Xylella fastidiosa affects the leaf ionome of plant hosts during infection. PLOS ONE 8:e62945
    [Google Scholar]
  35. 35.
    de Lamo FJ, Takken FLW. 2020. Biocontrol by Fusarium oxysporum using endophyte-mediated resistance. Front. Plant Sci. 11:37
    [Google Scholar]
  36. 36.
    Doblas-Ibáñez P, Deng K, Vasquez MF, Giese L, Cobine PA et al. 2019. Dominant, heritable resistance to Stewart's wilt in maize is associated with an enhanced vascular defense response to infection with Pantoea stewartii. Mol. Plant-Microbe Interact. 32:1581–97
    [Google Scholar]
  37. 37.
    Fanton AC, Brodersen C. 2021. Hydraulic consequences of enzymatic breakdown of grapevine pit membranes. Plant Physiol. 186:1919–31
    [Google Scholar]
  38. 38.
    Fatima U, Senthil-Kumar M. 2015. Plant and pathogen nutrient acquisition strategies. Front. Plant Sci. 6:750
    [Google Scholar]
  39. 39.
    Feil H, Feil WS, Lindow SE. 2007. Contribution of fimbrial and afimbrial adhesins of Xylella fastidiosa to attachment to surfaces and virulence to grape. Phytopathology 97:318–24
    [Google Scholar]
  40. 40.
    Garcia-Ceron D, Dawson CS, Faou P, Bleackley MR, Anderson MA. 2021. Size-exclusion chromatography allows the isolation of EVs from the filamentous fungal plant pathogen Fusarium oxysporum f. sp. vasinfectum (Fov). Proteomics 21:e2000240
    [Google Scholar]
  41. 41.
    Ge Q, Cobine PA, De La, Fuente L. 2021. The influence of copper homeostasis genes copA and copB on Xylella fastidiosa virulence is affected by sap copper concentration. Phytopathology 111:91520–29
    [Google Scholar]
  42. 42.
    Ge Q, Cobine PA, De La, Fuente L. 2020. Copper supplementation in watering solution reaches the xylem but does not protect tobacco plants against Xylella fastidiosa infection. Plant Dis. 104:724–30
    [Google Scholar]
  43. 43.
    Gerlin L, Escourrou A, Cassan C, Maviane Macia F, Peeters N et al. 2021. Unravelling physiological signatures of tomato bacterial wilt and xylem metabolites exploited by Ralstonia solanacearum. Environ. Microbiol. 23:5962–78
    [Google Scholar]
  44. 44.
    Gharbi Y, Alkher H, Triki MA, Barkallah M, Emna B et al. 2015. Comparative expression of genes controlling cell wall-degrading enzymes in Verticillium dahliae isolates from olive, potato and sunflower. Physiol. Mol. Plant Pathol. 91:56–65
    [Google Scholar]
  45. 45.
    Giampetruzzi A, Morelli M, Saponari M, Loconsole G, Chiumenti M et al. 2016. Transcriptome profiling of two olive cultivars in response to infection by the CoDiRO strain of Xylella fastidiosa subsp. pauca. BMC Genom. 17:475
    [Google Scholar]
  46. 46.
    Gluck-Thaler E, Cerutti A, Perez-Quintero AL, Butchacas J, Roman-Reyna V et al. 2020. Repeated gain and loss of a single gene modulates the evolution of vascular plant pathogen lifestyles. Sci. Adv. 6:eabc4516
    [Google Scholar]
  47. 47.
    Goodhead I, Blow F, Brownridge P, Hughes M, Kenny J et al. 2020. Large-scale and significant expression from pseudogenes in Sodalis glossinidius: a facultative bacterial endosymbiont. Microb. Genom. 6:e000285
    [Google Scholar]
  48. 48.
    Guilhabert MR, Kirkpatrick BC. 2005. Identification of Xylella fastidiosa antivirulence genes: hemagglutinin adhesins contribute to X. fastidiosa biofilm maturation and colonization and attenuate virulence. Mol. Plant-Microbe Interact. 18:856–68
    [Google Scholar]
  49. 49.
    Haas H, Eisendle M, Turgeon BG. 2008. Siderophores in fungal physiology and virulence. Annu. Rev. Phytopathol. 46:149–87
    [Google Scholar]
  50. 50.
    Hamilton CD, Steidl OR, MacIntyre AM, Hendrich CG, Allen C 2021. Ralstonia solanacearum depends on catabolism of myo-inositol, sucrose, and trehalose for virulence in an infection stage–dependent manner. Mol. Plant-Microbe Interact. 34:669–79
    [Google Scholar]
  51. 51.
    Herrera CM, Koutsoudis MD, Wang X, von Bodman SB 2008. Pantoea stewartii subsp. stewartii exhibits surface motility, which is a critical aspect of Stewart's wilt disease development on maize. Mol. Plant-Microbe Interact. 21:1359–70
    [Google Scholar]
  52. 52.
    Huertas-González MD, Ruiz-Roldán MC, García Maceira FI, Roncero MI, Di Pietro A 1999. Cloning and characterization of pl1 encoding an in planta-secreted pectate lyase of Fusarium oxysporum. Curr. Genet. 35:36–40
    [Google Scholar]
  53. 53.
    Ingel B, Caldwell D, Duong F, Parkinson D, McCulloh K et al. 2021. Revisiting the source of wilt symptoms: X-ray microcomputed tomography provides direct evidence that Ralstonia biomass clogs xylem vessels. PhytoFrontiers https://doi.org/10.1101/2021.03.19.436187
    [Crossref] [Google Scholar]
  54. 54.
    Ingel B, Reyes C, Massonnet M, Boudreau B, Sun Y et al. 2021. Xylella fastidiosa causes transcriptional shifts that precede tylose formation and starch depletion in xylem. Mol. Plant Pathol. 22:175–88
    [Google Scholar]
  55. 55.
    Inoue I, Namiki F, Tsuge T. 2002. Plant colonization by the vascular wilt fungus Fusarium oxysporum requires FOW1, a gene encoding a mitochondrial protein. Plant Cell 14:1869–83
    [Google Scholar]
  56. 56.
    Ionescu M, Zaini PA, Baccari C, Tran S, da Silva AM, Lindow SE. 2014. Xylella fastidiosa outer membrane vesicles modulate plant colonization by blocking attachment to surfaces. PNAS 111:E3910–98
    [Google Scholar]
  57. 57.
    Jacobs JM, Babujee L, Meng F, Milling A, Allen C. 2012. The in planta transcriptome of Ralstonia solanacearum: conserved physiological and virulence strategies during bacterial wilt of tomato. mBio 3:4e00114–12
    [Google Scholar]
  58. 58.
    Jangir P, Mehra N, Sharma K, Singh N, Rani M, Kapoor R 2021. Secreted in xylem genes: drivers of host adaptation in Fusarium oxysporum. Front. Plant Sci. 12:628611
    [Google Scholar]
  59. 59.
    Jarrell KF, McBride MJ. 2008. The surprisingly diverse ways that prokaryotes move. Nat. Rev. Microbiol. 6:466–76
    [Google Scholar]
  60. 60.
    Kang Y, Liu H, Genin S, Schell MA, Denny TP. 2002. Ralstonia solanacearum requires type 4 pili to adhere to multiple surfaces and for natural transformation and virulence. Mol. Microbiol. 2:427–37
    [Google Scholar]
  61. 61.
    Kharadi RR, Sundin GW. 2020. Dissecting the process of xylem colonization through biofilm formation in Erwinia amylovora. J. Plant Pathol. 103:41–49
    [Google Scholar]
  62. 62.
    Khokhani D, Lowe-Power TM, Tran TM, Allen C. 2017. A single regulator mediates strategic switching between attachment/spread and growth/virulence in the plant pathogen Ralstonia solanacearum. mBio 8:e00895–17
    [Google Scholar]
  63. 63.
    Killiny N, Almeida RPP. 2009. Xylella fastidiosa afimbrial adhesins mediate cell transmission to plants by leafhopper vectors. Appl. Environ. Microbiol. 75:521–28
    [Google Scholar]
  64. 64.
    Killiny N, Martinez RH, Dumenyo CK, Cooksey DA, Almeida RP. 2013. The exopolysaccharide of Xylella fastidiosa is essential for biofilm formation, plant virulence, and vector transmission. Mol. Plant-Microbe Interact. 26:1044–53
    [Google Scholar]
  65. 65.
    Klimes A, Dobinson KF, Thomma BPHJ, Klosterman SJ. 2015. Genomics spurs rapid advances in our understanding of the biology of vascular wilt pathogens in the genus Verticillium. Annu. Rev. Phytopathol. 53:181–98
    [Google Scholar]
  66. 66.
    Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE et al. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLOS Pathog. 7:e1002137
    [Google Scholar]
  67. 67.
    Koczan JM, McGrath MJ, Zhao Y, Sundin GW. 2009. Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: implications in pathogenicity. Phytopathology 99:1237–44
    [Google Scholar]
  68. 68.
    Koutsoudis MD, Tsaltas D, Minogue TD, von Bodman SB 2006. Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoeastewartii subspecies stewartii. PNAS 103:5983–88
    [Google Scholar]
  69. 69.
    Labroussaa F, Ionescu M, Zeilinger AR, Lindow SE, Almeida RPP. 2017. A chitinase is required for Xylella fastidiosa colonization of its insect and plant hosts. Microbiology 163:502–9
    [Google Scholar]
  70. 70.
    Leite B, Ishida ML, Alves E, Carrer H, Pascholati SF, Kitajima EW. 2002. Genomics and X-ray microanalysis indicate that Ca2+ and thiols mediate the aggregation and adhesion of Xylella fastidiosa. Braz. J. Med. Biol. Res. 35:645–50
    [Google Scholar]
  71. 71.
    Li J, Fokkens L, van Dam P, Rep M. 2020. Related mobile pathogenicity chromosomes in Fusarium oxysporum determine host range on cucurbits. Mol. Plant Pathol. 21:761–76
    [Google Scholar]
  72. 72.
    Lim SH, So BH, Wang JC, Song ES, Park YJ et al. 2008. Functional analysis of pilQ gene in Xanthomonas oryzae pv. oryzae, bacterial blight pathogen of rice. J. Microbiol. 46:214–20
    [Google Scholar]
  73. 73.
    Liu H, Kang Y, Genin S, Schell MA, Denny TP. 2001. Twitching motility of Ralstonia solanacearum requires a type IV pilus system. Microbiology 147:3215–29
    [Google Scholar]
  74. 74.
    López-Berges MS. 2020. ZafA-mediated regulation of zinc homeostasis is required for virulence in the plant pathogen Fusarium oxysporum. Mol. Plant Pathol. 21:244–49
    [Google Scholar]
  75. 75.
    López-Berges MS, Capilla J, Turrà D, Schafferer L, Matthijs S et al. 2012. HapX-mediated iron homeostasis is essential for rhizosphere competence and virulence of the soilborne pathogen Fusarium oxysporum. Plant Cell 24:3805–22
    [Google Scholar]
  76. 76.
    Lowe-Power TM, Hendrich CG, von Roepenack-Lahaye E, Li B, Wu D et al. 2018. Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease. Environ. Microbiol. 20:1330–49
    [Google Scholar]
  77. 77.
    Lowe-Power TM, Khokhani D, Allen C 2018. How Ralstonia solanacearum exploits and thrives in the flowing plant xylem environment. Trends Microbiol. 26:929–42
    [Google Scholar]
  78. 78.
    Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–73
    [Google Scholar]
  79. 79.
    Mah TFC, O'Toole GA. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34–39
    [Google Scholar]
  80. 80.
    Martínez-Cano DJ, Reyes-Prieto M, Martínez-Romero E, Partida-Martínez LP, Latorre A et al. 2015. Evolution of small prokaryotic genomes. Front. Microbiol. 5:742
    [Google Scholar]
  81. 81.
    Masachis S, Segorbe D, Turrà D, Leon-Ruiz M, Fürst U et al. 2016. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat. Microbiol. 1:16043
    [Google Scholar]
  82. 82.
    Mattick JS. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289–314
    [Google Scholar]
  83. 83.
    McCarthy Y, Ryan RP, O'Donovan K, He YQ, Jiang BL et al. 2008. The role of PilZ domain proteins in the virulence of Xanthomonas campestris pv. campestris. Mol. Plant Pathol. 9:819–24
    [Google Scholar]
  84. 84.
    McElrone AJ, Jackson S, Habdas P 2008. Hydraulic disruption and passive migration by a bacterial pathogen in oak tree xylem. J. Exp. Bot. 59:2649–57
    [Google Scholar]
  85. 85.
    McElrone AJ, Manuck CM, Brodersen CR, Patakas A, Pearsall KR, Williams LE. 2021. Functional hydraulic sectoring in grapevines as evidenced by sap flow, dye infusion, leaf removal and micro-computed tomography. AoB Plants 13:plab003
    [Google Scholar]
  86. 86.
    McElrone AJ, Sherald JL, Forseth IN. 2003. Interactive effects of water stress and xylem-limited bacterial infection on the water relations of a host vine. J. Exp. Bot. 54:419–30
    [Google Scholar]
  87. 87.
    Meng Y, Li Y, Galvani CD, Hao G, Turner JN et al. 2005. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J. Bacteriol. 187:5560–67
    [Google Scholar]
  88. 88.
    Monteiro-Vitorello CB, Camargo LEA, Van Sluys MA, Kitajima JP, Truffi D et al. 2004. The genome sequence of the gram-positive sugarcane pathogen Leifsonia xyli subsp. xyli. Mol. Plant-Microbe Interact. 17:827–36
    [Google Scholar]
  89. 89.
    Mori Y, Inoue K, Ikeda K, Nakayashiki H, Higashimoto C et al. 2016. The vascular plant-pathogenic bacterium Ralstonia solanacearum produces biofilms required for its virulence on the surfaces of tomato cells adjacent to intercellular spaces. Mol. Plant Pathol. 17:890–902
    [Google Scholar]
  90. 90.
    Morris CE, Monier JM. 2003. The ecological significance of biofilm formation by plant-associated bacteria. Annu. Rev. Phytopathol. 41:429–53
    [Google Scholar]
  91. 91.
    Morris CE, Moury B. 2019. Revisiting the concept of host range of plant pathogens. Annu. Rev. Phytopathol. 57:63–90
    [Google Scholar]
  92. 92.
    Myburg AA, Lev-Yadun S, Sederoff RR. 2001. Xylem structure and function. eLS https://doi.org/10.1038/npg.els.0001302
    [Crossref] [Google Scholar]
  93. 93.
    Nardini A, Salleo S, Jansen S. 2011. More than just a vulnerable pipeline: xylem physiology in the light of ion-mediated regulation of plant water transport. J. Exp. Bot. 62:4701–18
    [Google Scholar]
  94. 94.
    Nascimento R, Gouran H, Chakraborty S, Gillespie HW,Almeida-Souza HO et al. 2016. The type II secreted lipase/esterase LesA is a key virulence factor required for Xylella fastidiosa pathogenesis in grapevines. Sci. Rep. 6:18598
    [Google Scholar]
  95. 95.
    Navarrete F, De La, Fuente L. 2014. Xylella fastidiosa response to zinc: decreased culturability, increased exopolysaccharide production, and resilient biofilms under flow conditions. Appl. Environ. Microbiol. 80:1097–107
    [Google Scholar]
  96. 96.
    Navarrete F, De La, Fuente L. 2015. Zinc detoxification is required for full virulence and modification of the host leaf ionome by Xylella fastidiosa. Mol. Plant-Microbe Interact. 28:497–507
    [Google Scholar]
  97. 97.
    Niño-Sánchez J, Tello V, Casado-del Castillo V, Thon MR, Benito EP, Díaz-Mínguez JM 2015. Gene expression patterns and dynamics of the colonization of common bean (Phaseolus vulgaris L.) by highly virulent and weakly virulent strains of Fusarium oxysporum. Front. Microbiol. 6:234
    [Google Scholar]
  98. 98.
    Olawole OI, Liu Q, Chen C, Gleason ML, Beattie GA. 2021. The contributions to virulence of the effectors Eop1 and DspE differ between two clades of Erwinia tracheiphila strains. Mol. Plant-Microbe Interact. 34:121399–408
    [Google Scholar]
  99. 99.
    Oliver JE, Cobine PA, De La, Fuente L. 2015. Xylella fastidiosa isolates from both subsp. multiplex and fastidiosa cause disease on southern highbush blueberry (Vaccinium sp.) under greenhouse conditions. Phytopathology 105:855–62
    [Google Scholar]
  100. 100.
    Oliver JE, Sefick SA, Parker JK, Arnold T, Cobine PA, De La, Fuente L. 2014. Ionome changes in Xylella fastidiosa-infected Nicotiana tabacum correlate with virulence and discriminate between subspecies of bacterial isolates. Mol. Plant-Microbe Interact. 27:1048–58
    [Google Scholar]
  101. 101.
    Parker JK, Chen HY, McCarty SE, Liu LY, De La, Fuente L. 2016. Calcium transcriptionally regulates the biofilm machinery of Xylella fastidiosa to promote continued biofilm development in batch cultures. Environ. Microbiol. 18:1620–34
    [Google Scholar]
  102. 102.
    Parker JK, Cruz LF, Evans MR, De La, Fuente L. 2015. Presence of calcium-binding motifs in PilY1 homologs correlates with Ca-mediated twitching motility and evolutionary history across diverse bacteria. FEMS Microbiol. Lett. https://doi.org/10.1093/femsle/fnu063
    [Crossref] [Google Scholar]
  103. 103.
    Peuke AD, Rokitta M, Zimmermann U, Schreiber L, Haase A. 2001. Simultaneous measurement of water flow velocity and solute transport in xylem and phloem of adult plants of Ricinus communis over a daily time course by nuclear magnetic resonance spectrometry. Plant Cell Environ. 24:491–503
    [Google Scholar]
  104. 104.
    Pierce BK, Kirkpatrick BC. 2015. The PhoP/Q two-component regulatory system is essential for Xylella fastidiosa survival in Vitis vinifera grapevines. Physiol. Mol. Plant Pathol. 89:55–61
    [Google Scholar]
  105. 105.
    Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R et al. 2012. Genomic insights into strategies used by Xanthomonas albilineans with its reduced artillery to spread within sugarcane xylem vessels. BMC Genom. 13:658
    [Google Scholar]
  106. 106.
    Poueymiro M, Cazalé AC, François JM, Parrou JL, Peeters N, Genin S. 2014. A Ralstonia solanacearum type III effector directs the production of the plant signal metabolite trehalose-6-phosphate. mBio 5:6e02065–14
    [Google Scholar]
  107. 107.
    Pradhan BB, Ranjan M, Chatterjee S. 2012. XadM, a novel adhesin of Xanthomonas oryzae pv. oryzae, exhibits similarity to Rhs family proteins and is required for optimum attachment, biofilm formation, and virulence. Mol. Plant-Microbe Interact. 25:1157–70
    [Google Scholar]
  108. 108.
    Prima-Putra D, Botton B. 1998. Organic and inorganic compounds of xylem exudates from five woody plants at the stage of bud breaking. J. Plant Physiol. 153:670–76
    [Google Scholar]
  109. 109.
    Prusky D, Yakoby N. 2003. Pathogenic fungi: leading or led by ambient pH?. Mol. Plant Pathol. 4:509–16
    [Google Scholar]
  110. 110.
    Purcell AH, Hopkins DL. 1996. Fastidious xylem-limited bacterial plant pathogens. Annu. Rev. Phytopathol. 34:131–51
    [Google Scholar]
  111. 111.
    Quecine MC, Silva TM, Carvalho G, Saito S, Mondin M et al. 2016. A stable Leifsonia xyli subsp. xyli GFP-tagged strain reveals a new colonization niche in sugarcane tissues. Plant Pathol. 65:154–62
    [Google Scholar]
  112. 112.
    Ray SK, Rajeshwari R, Sharma Y, Sonti RV. 2002. A high-molecular-weight outer membrane protein of Xanthomonas oryzae pv. oryzae exhibits similarity to non-fimbrial adhesins of animal pathogenic bacteria and is required for optimum virulence. Mol. Microbiol. 46:637–47
    [Google Scholar]
  113. 113.
    Rizzo J, Rodrigues ML, Janbon G. 2020. Extracellular vesicles in fungi: past, present, and future perspectives. Front. Cell. Infection Microbiol. 10:346
    [Google Scholar]
  114. 114.
    Rojas CM, Ham JH, Deng WL, Doyle JJ, Collmer A. 2002. HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. PNAS 99:13142–47
    [Google Scholar]
  115. 115.
    Rooney LM, Amos WB, Hoskisson PA, McConnell G. 2020. Intra-colony channels in E. coli function as a nutrient uptake system. ISME J. 14:2461–73
    [Google Scholar]
  116. 116.
    Rutherford JC, Bird AJ. 2004. Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot. Cell 3:1–13
    [Google Scholar]
  117. 117.
    Sabella E, Aprile A, Genga A, Siciliano T, Nutricati E et al. 2019. Xylem cavitation susceptibility and refilling mechanisms in olive trees infected by Xylella fastidiosa. Sci. Rep. 9:9602
    [Google Scholar]
  118. 118.
    Schenk HJ, Espino S, Romo DM, Nima N, Do AYT et al. 2017. Xylem surfactants introduce a new element to the cohesion-tension theory. Plant Physiol. 173:1177–96
    [Google Scholar]
  119. 119.
    Schenk HJ, Jansen S, Holtta T. 2021. Positive pressure in xylem and its role in hydraulic function. New Phytol. 230:27–45
    [Google Scholar]
  120. 120.
    Schwechheimer C, Kuehn MJ. 2015. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat. Rev. Microbiol. 13:605–19
    [Google Scholar]
  121. 121.
    Schwechheimer C, Sullivan CJ, Kuehn MJ. 2013. Envelope control of outer membrane vesicle production in Gram-negative bacteria. Biochemistry 52:3031–40
    [Google Scholar]
  122. 122.
    Scortichini M, Chen J, de Caroli M, Dalessandro G, Pucci N et al. 2018. A zinc, copper and citric acid biocomplex shows promise for control of Xylella fastidiosa subsp. pauca in olive trees in Apulia region (southern Italy). Phytopathol. Mediterr. 57:48–72
    [Google Scholar]
  123. 123.
    Shi X, Lin H. 2018. The chemotaxis regulator pilG of Xylella fastidiosa is required for virulence in Vitis vinifera grapevines. Eur. J. Plant Pathol. 150:351–62
    [Google Scholar]
  124. 124.
    Singh S, Braus-Stromeyer SA, Timpner C, Tran VT, Lohaus G et al. 2010. Silencing of Vlaro2 for chorismate synthase revealed that the phytopathogen Verticillium longisporum induces the cross-pathway control in the xylem. Appl. Microbiol. Biotechnol. 85:1961–76
    [Google Scholar]
  125. 125.
    Stevenson JF, Matthews MA, Rost TL. 2004. Grapevine susceptibility to Pierce's disease I: relevance to hydraulic architecture. Am. J. Enol. Vitic. 55:228–37
    [Google Scholar]
  126. 126.
    Sun Q, Sun Y, Walker MA, Labavitch JM. 2013. Vascular occlusions in grapevines with Pierce's disease make disease symptom development worse. Plant Physiol. 161:1529–41
    [Google Scholar]
  127. 127.
    Tans-Kersten J, Huang H, Allen C 2001. Ralstonia solanacearum needs motility for invasive virulence on tomato. J. Bacteriol. 183:3597–605
    [Google Scholar]
  128. 128.
    Thor K. 2019. Calcium—nutrient and messenger. Front. Plant Sci. 10:440
    [Google Scholar]
  129. 129.
    Thorne ET, Young BM, Young GM, Stevenson JF, Labavitch JM et al. 2006. The structure of xylem vessels in grapevine (Vitaceae) and a possible passive mechanism for the systemic spread of bacterial disease. Am. J. Bot. 93:497–504
    [Google Scholar]
  130. 130.
    Timpner C, Braus-Stromeyer SA, VT Tran, Braus GH. 2013. The Cpc1 regulator of the cross-pathway control of amino acid biosynthesis is required for pathogenicity of the vascular pathogen Verticillium longisporum. Mol. Plant-Microbe Interact. 26:1312–24
    [Google Scholar]
  131. 131.
    Toyofuku M, Nomura N, Eberl L. 2019. Types and origins of bacterial membrane vesicles. Nat. Rev. Microbiol. 17:13–24
    [Google Scholar]
  132. 132.
    Tran TM, MacIntyre A, Khokhani D, Hawes M, Allen C 2016. Extracellular DNases of Ralstonia solanacearum modulate biofilms and facilitate bacterial wilt virulence. Environ. Microbiol. 18:4103–17
    [Google Scholar]
  133. 133.
    Tran V-T, Braus-Stromeyer SA, Kusch H, Reusche M, Kaever A et al. 2014. Verticillium transcription activator of adhesion Vta2 suppresses microsclerotia formation and is required for systemic infection of plant roots. New Phytol. 202:565–81
    [Google Scholar]
  134. 134.
    Tzima AK, Paplomatas EJ, Rauyaree P, Ospina-Giraldo MD, Kang S 2011. VdSNF1, the sucrose nonfermenting protein kinase gene of Verticillium dahliae, is required for virulence and expression of genes involved in cell-wall degradation. Mol. Plant-Microbe Interact. 24:129–42
    [Google Scholar]
  135. 135.
    Vaghefi N, Adorada DL, Huth L, Kelly LA, Poudel B et al. 2021. Whole-genome data from Curtobacterium flaccumfaciens pv. flaccumfaciens strains associated with tan spot of mungbean and soybean reveal diverse plasmid profiles. Mol. Plant-Microbe Interact. 34:101216–22
    [Google Scholar]
  136. 136.
    van Dam P, Fokkens L, Ayukawa Y, van der Gragt M, ter Horst A et al. 2017. A mobile pathogenicity chromosome in Fusarium oxysporum for infection of multiple cucurbit species. Sci. Rep. 7:9042
    [Google Scholar]
  137. 137.
    van der Burgt A, Karimi Jashni M, Bahkali AH, de Wit PJ 2014. Pseudogenization in pathogenic fungi with different host plants and lifestyles might reflect their evolutionary past. Mol. Plant Pathol. 15:133–44
    [Google Scholar]
  138. 138.
    Van Sluys MA, de Oliveira MC, Monteiro-Vitorello CB, Miyaki CY, Furlan LR et al. 2003. Comparative analyses of the complete genome sequences of Pierce's disease and citrus variegated chlorosis strains of Xylella fastidiosa. J. Bacteriol. 185:1018–26
    [Google Scholar]
  139. 139.
    Wagner S, Grin I, Malmsheimer S, Singh N, Torres-Vargas CE, Westerhausen S. 2018. Bacterial type III secretion systems: a complex device for the delivery of bacterial effector proteins into eukaryotic host cells. FEMS Microbiol. Lett. 365:19fny201
    [Google Scholar]
  140. 140.
    Wang D, Chen J-Y, Song J, Li J-J, Klosterman SJ et al. 2021. Cytotoxic function of xylanase VdXyn4 in the plant vascular wilt pathogen Verticillium dahliae. Plant Physiol. 187:409–29
    [Google Scholar]
  141. 141.
    Wang JC, So BH, Kim JH, Park YJ, Lee BM, Kang HW. 2008. Genome-wide identification of pathogenicity genes in Xanthomonas oryzae pv. oryzae by transposon mutagenesis. Plant Pathol. 57:1136–45
    [Google Scholar]
  142. 142.
    Wang L, Makino S, Subedee A, Bogdanove AJ. 2007. Novel candidate virulence factors in rice pathogen Xanthomonas oryzae pv. oryzicola as revealed by mutational analysis. Appl. Environ. Microbiol. 73:8023–27
    [Google Scholar]
  143. 143.
    Wang Y, Deng C, Tian L, Xiong D, Tian C, Klosterman SJ. 2018. The transcription factor VdHapX controls iron homeostasis and is crucial for virulence in the vascular pathogen Verticillium dahliae. mSphere 3:e00400–18
    [Google Scholar]
  144. 144.
    Wilkinson S, Davies WJ. 1997. Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiol. 113:559–73
    [Google Scholar]
  145. 145.
    Windt CW, Vergeldt FJ, de Jager PA, van As H. 2006. MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant Cell Environ. 29:1715–29
    [Google Scholar]
  146. 146.
    Xian L, Yu G, Macho AP 2021. The GABA transaminase GabT is required for full virulence of Ralstonia solanacearum in tomato. MicroPubl. Biol https://doi.org/10.17912/micropub.biology.000478
    [Crossref] [Google Scholar]
  147. 147.
    Xian L, Yu G, Wei Y, Rufian JS, Li Y et al. 2020. A bacterial effector protein hijacks plant metabolism to support pathogen nutrition. Cell Host Microbe 28:548–57.e7
    [Google Scholar]
  148. 148.
    Yadeta K, Thomma B. 2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Front. Plant Sci. 4:97
    [Google Scholar]
  149. 149.
    Yang JL, Michaud JM, Jansen S, Schenk HJ, Zuo YY. 2020. Dynamic surface tension of xylem sap lipids. Tree Physiol. 40:433–44
    [Google Scholar]
  150. 150.
    Zaini PA, Fogaça AC, Lupo FGN, Nakaya HI, Vêncio RZN, da Silva AM. 2008. The iron stimulon of Xylella fastidiosa includes genes for type IV pilus and colicin V-like bacteriocins. J. Bacteriol. 190:2368–78
    [Google Scholar]
  151. 151.
    Zhang S, Chakrabarty PK, Fleites LA, Rayside PA, Hopkins DL, Gabriel DW. 2015. Three new Pierce's disease pathogenicity effectors identified using Xylella fastidiosa biocontrol strain EB92–1. PLOS ONE 10:e0133796
    [Google Scholar]
  152. 152.
    Zimmermann MH. 1983. Pathology of the xylem. Xylem Structure and the Ascent of Sap107–23 Berlin: Springer
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-021021-041716
Loading
/content/journals/10.1146/annurev-phyto-021021-041716
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • 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