BACKGROUND AND AIMS: Xylella fastidiosa (Xf) is the xylem-dwelling bacterium associated with Pierce's disease (PD), which causes mortality in agriculturally important species, such as grapevine (Vitis vinifera). The development of PD symptoms in grapevines depends on the ability of Xf to produce cell-wall-degrading enzymes to break up intervessel pit membranes and systematically spread through the xylem vessel network. Our objective here was to investigate whether PD resistance could be mechanistically linked to xylem vessel network local connectivity. METHODS: We used high-resolution X-ray micro-computed tomography (microCT) imaging to identify and describe the type, area and spatial distribution of intervessel connections for six different grapevine genotypes from three genetic backgrounds, with varying resistance to PD (four PD resistant and two PD susceptible). KEY RESULTS: Our results suggest that PD resistance is unlikely to derive from local xylem network connectivity. The intervessel pit area (Ai) varied from 0.07 ± 0.01 mm2 mm-3 in Lenoir to 0.17 ± 0.03 mm2 mm-3 in Blanc do Bois, both PD resistant. Intervessel contact fraction (Cp) was not statically significant, but the two PD-susceptible genotypes, Syrah (0.056 ± 0.015) and Chardonnay (0.041 ± 0.013), were among the most highly connected vessel networks. Neither Ai nor Cp explained differences in PD resistance among the six genotypes. Bayesian re-analysis of our data shows moderate evidence against the effects of the traits analysed: Ai (BF01 = 4.88), mean vessel density (4.86), relay diameter (4.30), relay density (3.31) and solitary vessel proportion (3.19). CONCLUSIONS: Our results show that radial and tangential xylem network connectivity is highly conserved within the six different Vitis genotypes we sampled. The way that Xf traverses the vessel network may limit the importance of local network properties to its spread and may confer greater importance on host biochemical responses.

Institute of Botany Czech Academy of Sciences Průhonice Czechia

School of the Environment Yale University New Haven CT USA

Komentář v

Ann Bot. 2024 Apr 23;133(4):i-ii. doi: 10.1093/aob/mcae020. PubMed

Zobrazit více v PubMed

Almeida RPP, Nunney L.. 2015. How do plant diseases caused by Xylella fastidiosa emerge? Plant Disease 99: 1457–1467. PubMed

Baccari C, Lindow SE.. 2011. Assessment of the process of movement of Xylella fastidiosa within susceptible and resistant grape cultivars. Phytopathology 101: 77–84. PubMed

Backus EA, Shugart HJ, Rogers EE, Morgan JK, Shatters R.. 2015. Direct evidence of egestion and salivation of Xylella fastidiosa suggests sharpshooters can be ‘flying syringes’. Phytopathology 105: 608–620. PubMed

Bouda M, Windt CW, McElrone AJ, Brodersen CR.. 2019. In vivo pressure gradient heterogeneity increases flow contribution of small diameter vessels in grapevine. Nature Communications 10: 5645. PubMed PMC

Bouda M, Huggett BA, Prats KA, Wason JW, Wilson JP, Brodersen CR.. 2022. Hydraulic failure as a primary driver of xylem network evolution in early vascular plants. Science 378: 642–646. PubMed

Brodersen CR, Lee EF, Choat B, et al.. 2011. Automated analysis of three-dimensional xylem networks using high-resolution computed tomography. The New Phytologist 191: 1168–1179. PubMed

Brodersen CR, Choat B, Chatelet DS, Shackel KA, Matthews MA, McElrone AJ.. 2013a. Xylem vessel relays contribute to radial connectivity in grapevine stems (Vitis vinifera and V. arizonica; Vitaceae). American Journal of Botany 100: 314–321. PubMed

Brodersen CR, McElrone AJ, Choat B, Lee EF, Shackel KA, Matthews MA.. 2013b. In vivo visualizations of drought-induced embolism spread in Vitis vinifera. Plant Physiology 161: 1820–1829. PubMed PMC

Buzombo P, Jaimes J, Lam V, et al.. 2006. An American hybrid vineyard in the Texas Gulf Coast: analysis within a Pierce’s disease hot zone. American Journal of Enology and Viticulture 57: 347–355.

Carlquist S. 1984. Vessel grouping in dicotyledon wood: significance and relationship to imperforate tracheary elements. Aliso 10: 505–525.

Carlquist S. 1988. Comparative wood anatomy. Berlin: Springer.

Chalk L, Huber B, Normand D, Phillips EWJ, Rendle BJ.. 1964. Multilingual glossary of terms used in wood anatomy. Verlaganstadt Buchdruckerei Konkordia: IAWA – Committee on nomenclature. International Association of Wood Anatomists, 1–46.

Chatelet DS, Matthews MA, Rost TL.. 2006. Xylem structure and connectivity in grapevine (Vitis vinifera) shoots provides a passive mechanism for the spread of bacteria in grape plants. Annals of Botany 98: 483–494. PubMed PMC

Chatterjee S, Almeida RPP, Lindow S.. 2008. Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annual Review of Phytopathology 46: 243–271. PubMed

Choat B, Drayton WM, Brodersen C, et al.. 2010. Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species: comparison of vulnerability curve technique in grapevine. Plant, Cell & Environment 33: no–no. PubMed

Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE.. 2018. Triggers of tree mortality under drought. Nature 558: 531–539. PubMed

Coletta‐Filho HD, Pereira EO, Souza AA, Takita MA, Cristofani‐Yale M, Machado MA.. 2007. Analysis of resistance to Xylella fastidiosa within a hybrid population of Pera sweet orange × Murcott tangor. Plant Pathology 56: 661–668.

Fanton AC, Brodersen C.. 2021. Hydraulic consequences of enzymatic breakdown of grapevine pit membranes. Plant Physiology 186: 1919–1931. PubMed PMC

Fanton AC, Furze ME, Brodersen CR.. 2022. Pathogen‐induced hydraulic decline limits photosynthesis and starch storage in grapevines (Vitis sp.). Plant, Cell & Environment 45: 1829–1842. PubMed

Faulkenberry TJ. 2018. Computing Bayes factors to measure evidence from experiments: an extension of the BIC approximation. Biometrical Letters 55: 31–43.

Fritschi FB, Lin H, Walker MA.. 2007. Xylella fastidiosa population dynamics in grapevine genotypes differing in susceptibility to Pierce’s disease. American Journal of Enology and Viticulture 58: 326–332.

Fry SM, Milholland RD.. 1990. Multiplication and translocation of Xylella fastidiosa in petioles and stems of grapevine resistant, tolerant, and susceptible to Pierce’s disease. Phytopathology 80: 61–65.

Gerzon E, Biton I, Yaniv Y, et al.. 2015. Grapevine anatomy as a possible determinant of isohydric or anisohydric behavior. American Journal of Enology and Viticulture 66: 340–347.

Gürsoy D, De Carlo F, Xiao X, Jacobsen C.. 2014. TomoPy: a framework for the analysis of synchrotron tomographic data. Journal of Synchrotron Radiation 21: 1188–1193. PubMed PMC

Hoekstra R, Monden R, Van Ravenzwaaij D, Wagenmakers E-J.. 2018. Bayesian reanalysis of null results reported in medicine: strong yet variable evidence for the absence of treatment effects. PLoS One 13: e0195474. PubMed PMC

Ingel B, Jeske DR, Sun Q, Grosskopf J, Roper MC.. 2019. Xylella fastidiosa endoglucanases mediate the rate of Pierce’s disease development in Vitis vinifera in a cultivar-dependent manner. Molecular Plant-Microbe Interactions 32: 1402–1414. PubMed

Jacobsen AL, Rodriguez-Zaccaro FD, Lee TF, Valdovinos J, Toschi HS, Martinez JA, Pratt RB.. 2015. Grapevine xylem development, architecture, and function. In: Hacke UG. ed. Functional and ecological xylem anatomy. Cham: Springer International Publishing.

Keysers C, Gazzola V, Wagenmakers E-J.. 2020. Using Bayes factor hypothesis testing in neuroscience to establish evidence of absence. Nature Neuroscience 23: 788–799. PubMed PMC

Krivanek AF, Walker MA.. 2005. Vitis resistance to Pierce’s disease is characterized by differential Xylella fastidiosa populations in stems and leaves. Phytopathology 95: 44–52. PubMed

Krivanek AF, Stevenson JF, Walker MA.. 2005. Development and comparison of symptom indices for quantifying grapevine resistance to Pierce’s disease. Phytopathology 95: 36–43. PubMed

Krivanek AF, Riaz S, Walker MA.. 2006. Identification and molecular mapping of PdR1, a primary resistance gene to Pierce’s disease in Vitis. TAG. Theoretical and Applied Genetics. Theoretische und angewandte Genetik 112: 1125–1131. PubMed

Landa BB, Saponari M, Feitosa-Junior OR, et al.. 2022. Xylella fastidiosa’s relationships: the bacterium, the host plants, and the plant microbiome. The New Phytologist 234: 1598–1605. PubMed

Lee EF, Matthews MA, McElrone AJ, Phillips RJ, Shackel KA, Brodersen CR.. 2013. Analysis of HRCT-derived xylem network reveals reverse flow in some vessels. Journal of Theoretical Biology 333: 146–155. PubMed

Loepfe L, Martinez-Vilalta J, Piñol J, Mencuccini M.. 2007. The relevance of xylem network structure for plant hydraulic efficiency and safety. Journal of Theoretical Biology 247: 788–803. PubMed

Maddox CE, Laur LM, Tian L.. 2010. Antibacterial activity of phenolic compounds against the phytopathogen Xylella fastidiosa. Current Microbiology 60: 53–58. PubMed PMC

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: 1–12. PubMed PMC

Meng Y, Li Y, Galvani CD, et al.. 2005. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. Journal of Bacteriology 187: 5560–5567. PubMed PMC

Morris H, Brodersen C, Schwarze FWMR, Jansen S.. 2016. The parenchyma of secondary xylem and its critical role in tree defense against fungal decay in relation to the CODIT model. Frontiers in Plant Science 7: 1–18. PubMed PMC

Morris H, Hietala AM, Jansen S, et al.. 2020. Using the CODIT model to explain secondary metabolites of xylem in defence systems of temperate trees against decay fungi. Annals of Botany 125: 701–720. PubMed PMC

Mrad A, Domec J-C, Huang C-W, Lens F, Katul G.. 2018. A network model links wood anatomy to xylem tissue hydraulic behaviour and vulnerability to cavitation. Plant, Cell & Environment 41: 2718–2730. PubMed

Mrad A, Johnson DM, Love DM, Domec J-C.. 2021. The roles of conduit redundancy and connectivity in xylem hydraulic functions. The New Phytologist 231: 996–1007. PubMed

Nascimento R, Gouran H, Chakraborty S, et al.. 2016. The type II secreted lipase/esterase LesA is a key virulence factor required for Xylella fastidiosa pathogenesis in grapevines. Scientific Reports 6: 18598. doi: 10.1038/srep18598. PubMed DOI PMC

Pearce RB. 1996. Antimicrobial defences in the wood of living trees. New Phytologist 132: 203–233.

Pérez-Donoso AG, Lenhof JJ, Pinney K, Labavitch JM.. 2016. Vessel embolism and tyloses in early stages of Pierce’s disease. Australian Journal of Grape and Wine Research 22: 81–86.

Pouzoulet J, Pivovaroff AL, Santiago LS, Rolshausen PE.. 2014. Can vessel dimension explain tolerance toward fungal vascular wilt diseases in woody plants? Lessons from Dutch elm disease and esca disease in grapevine. Frontiers in Plant Science 5: 1–11. PubMed PMC

Pouzoulet J, Scudiero E, Schiavon M, Rolshausen PE.. 2017. Xylem vessel diameter affects the compartmentalization of the vascular pathogen Phaeomoniella chlamydospora in grapevine. Frontiers in Plant Science 8: 1–13. PubMed PMC

Prats KA, Fanton AC, Brodersen CR, Furze ME.. 2023. Starch depletion in the xylem and phloem ray parenchyma of grapevine stems under drought. AoB Plants 15: 1–12. PubMed PMC

Redak RA, Purcell AH, Lopes JRS, Blua MJ, Mizell RF III, Andersen PC.. 2004. The biology of xylem fluid–feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annual Review of Entomology 49: 243–270. PubMed

Riaz S, Tenscher AC, Rubin J, Graziani R, Pao SS, Walker MA.. 2008. Fine-scale genetic mapping of two Pierce’s disease resistance loci and a major segregation distortion region on chromosome 14 of grape. TAG. Theoretical and Applied Genetics. Theoretische und angewandte Genetik 117: 671–681. PubMed

Riaz S, Tenscher AC, Heinitz CC, Huerta-Acosta KG, Walker MA.. 2020. Genetic analysis reveals an east-west divide within North American Vitis species that mirrors their resistance to Pierce’s disease. PLoS One 15: e0243445. PubMed PMC

Roper MC, Greve LC, Warren JG, Labavitch JM, Kirkpatrick BC.. 2007. Xylella fastidiosa requires polygalacturonase for colonization and pathogenicity in Vitis vinifera grapevines. Molecular Plant-Microbe Interactions 20: 411–419. PubMed

Roper C, Castro C, Ingel B.. 2019. Xylella fastidiosa: bacterial parasitism with hallmarks of commensalism. Current Opinion in Plant Biology 50: 140–147. PubMed

Schubert A, Lovisolo C, Peterlunger E.. 1999. Shoot orientation affects vessel size, shoot hydraulic conductivity and shoot growth rate in Vitis vinifera L. Plant, Cell & Environment 22: 197–204. PubMed

Shigo AL. 1985. Compartmentalization of decay in trees. Scientific American 252: 96–103.

Shtein I, Hayat Y, Munitz S, et al.. 2017. From structural constraints to hydraulic function in three Vitis rootstocks. Trees 31: 851–861.

Sun Q, Greve LC, Labavitch JM.. 2011. Polysaccharide compositions of intervessel pit membranes contribute to Pierce’s disease resistance of grapevines. Plant Physiology 155: 1976–1987. PubMed PMC

Sun Q, Sun Y, Walker MA, Labavitch JM.. 2013. Vascular occlusions in grapevines with Pierce’s disease make disease symptom development worse. Plant Physiology 161: 1529–1541. PubMed PMC

Sun Q, Sun Y, Juzenas K.. 2017. Immunogold scanning electron microscopy can reveal the polysaccharide architecture of xylem cell walls. Journal of Experimental Botany 68: 2231–2244. PubMed PMC

Thorne ET, Stevenson JF, Rost TL, Labavitch JM, Matthews MA.. 2006. Pierce’s disease symptoms: comparison with symptoms of water deficit and the impact of water deficits. American Journal of Enology and Viticulture 57: 11.

Tyree MT, Zimmermann MH.. 2002. Xylem structure and the ascent of sap. Berlin: Springer.

Varela LG, Smith RJ, Phillips PA.. 2001. Pierce’s disease. Oakland, CA: University of California, Division of Agricultural and Natural Resources.

Walker NC, Ruiz SA, Ferreira TR, et al.. 2023a. A high‐throughput analysis of high‐resolution X‐ray CT images of stems of olive and citrus plants resistant and susceptible to Xylella fastidiosa. Plant Pathology 00: 1–14.

Walker NC, White SM, McKay Fletcher D, et al.. 2023b. The impact of xylem geometry on olive cultivar resistance to Xylella fastidiosa: an image‐based study. Plant Pathology 72: 521–535.

Wason J, Bouda M, Lee EF, et al.. 2021. Xylem network connectivity and embolism spread in grapevine (Vitis vinifera L.). Plant Physiology 186: 373–387. PubMed PMC

Wells JM, Raju BC, Hung H-Y, Weisburg WG, Mandelco-Paul L, Brenner DJ.. 1987. Xylella fastidiosa gen. nov., sp. nov: gram-negative, xylem-limited, fastidious plant bacteria related to Xanthomonas spp. International Journal of Systematic Bacteriology 37: 136–143.

Yadeta KA, Thomma BPHJ.. 2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Frontiers in Plant Science 4: 1–12. PubMed PMC

Zaini PA, Nascimento R, Gouran H, et al.. 2018. Molecular profiling of Pierce’s disease outlines the response circuitry of Vitis vinifera to Xylella fastidiosa infection. Frontiers in Plant Science 9: 771. PubMed PMC