Xylem networks are vulnerable to the formation and spread of gas embolisms that reduce water transport. Embolisms spread through interconduit pits, but the three-dimensional (3D) complexity and scale of xylem networks means that the functional implications of intervessel connections are not well understood. Here, xylem networks of grapevine (Vitis vinifera L.) were reconstructed from 3D high-resolution X-ray micro-computed tomography (microCT) images. Xylem network performance was then modeled to simulate loss of hydraulic conductivity under increasingly negative xylem sap pressure simulating drought stress conditions. We also considered the sensitivity of xylem network performance to changes in key network parameters. We found that the mean pit area per intervessel connection was constant across 10 networks from three, 1.5-m stem segments, but short (0.5 cm) segments fail to capture complete network connectivity. Simulations showed that network organization imparted additional resistance to embolism spread beyond the air-seeding threshold of pit membranes. Xylem network vulnerability to embolism spread was most sensitive to variation in the number and location of vessels that were initially embolized and pit membrane vulnerability. Our results show that xylem network organization can increase stem resistance to embolism spread by 40% (0.66 MPa) and challenge the notion that a single embolism can spread rapidly throughout an entire xylem network.

Crops Pathology and Genetics Research Unit USDA ARS Davis California

Department of Chemical Engineering University of California Davis Davis California

Department of Engineering Sciences Clackamas Community College Oregon City Oregon 97045

Department of Plant Science University of California Davis Davis California

Department of Viticulture and Enology University of California Davis Davis California

Institute of Botany Czech Academy of Sciences Průhonice Czechia

School of Forest Resources University of Maine Orono Maine 04469

School of the Environment Yale University New Haven CT 06520

See more in PubMed

Bouche PS, Larter M, Domec J-C, Burlett R, Gasson P, Jansen S, Delzon S (2014) A broad survey of hydraulic and mechanical safety in the xylem of conifers. J Exp Bot  65: 4419–4431 PubMed PMC

Bouda M, Windt CW, McElrone AJ, Brodersen CR (2019) In vivo pressure gradient heterogeneity increases flow contribution of small diameter vessels in grapevine. Nat Commun  10: 1–10 PubMed PMC

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). Am J Bot  100: 314–321 PubMed

Brodersen CR, Lee EF, Choat B, Jansen S, Phillips RJ, Shackel KA, McElrone AJ, Matthews MA (2011) Automated analysis of three-dimensional xylem networks using high-resolution computed tomography. New Phytol  191: 1168–1179 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 Physiol  161: 1820–1829 PubMed PMC

Brodersen CR, Roddy AB (2016) New frontiers in the three-dimensional visualization of plant structure and function. Am J Bot  103: 184–188 PubMed

Brodersen CR, Roddy AB, Wason JW, McElrone AJ (2019) Functional status of xylem through time. Annu Rev Plant Biol  70: 407–433 PubMed

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. Ann Bot  98: 483–494 PubMed PMC

Choat B, Badel E, Burlett R, Delzon S, Cochard H, Jansen S (2016) Noninvasive measurement of vulnerability to drought-induced embolism by X-ray microtomography. Plant Physiol  170: 273–282 PubMed PMC

Choat B, Brodersen CR, McElrone AJ (2015) Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytol  205: 1095–1105 PubMed

Choat B, Drayton WM, Brodersen C, Matthews MA, Shackel KA, Wada H, Mcelrone AJ (2010) Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. Plant Cell Environ  33: 1502–1512 PubMed

Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, et al. (2012) Global convergence in the vulnerability of forests to drought. Nature  491: 752–755 PubMed

Choat B, Lahr EC, Melcher PJ, Zwieniecki MA, Holbrook NM (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant Cell Environ  28: 1082–1089

Christman MA, Sperry JS, Adler FR (2009) Testing the ‘rare pit’ hypothesis for xylem cavitation resistance in three species of Acer. New Phytol  182: 664–674 PubMed

Christman MA, Sperry JS, Smith DD (2012) Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. New Phytol  193: 713–720 PubMed

Cochard H, Delzon S, Badel E (2015) X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees. Plant Cell Environ  38: 201–206 PubMed

Coles S (2001) An introduction to statistical modeling of extreme values. Springer Science & Business Media, London

Duursma R, Choat B (2017) fitplc—an R package to fit hydraulic vulnerability curves. J Plant Hydraul  4: e-002

Erdos P, Rényi A (1960) On the evolution of random graphs. Publ Math Inst Hung Acad Sci  5: 17–60

Fahn A, Leshem B (1963) Wood fibres with living protoplasts. New Phytol  62: 91–98

Johnson KM, Brodersen CR, Carins-Murphy MR, Choat B, Brodribb TJ (2020) Xylem embolism spreads by single-conduit events in three dry forest angiosperm stems. Plant Physiol (doi: 10.1104/pp.20.00464) PubMed PMC

Kaack L, Altaner CM, Carmesin C, Diaz A, Holler M, Kranz C, Neusser G, Odstrcil M, Schenk HJ, Schmidt V, et al. (2019) Function and three-dimensional structure of intervessel pit membranes in angiosperms: a review. IAWA J  40: 673–702

Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ, et al. (2011) TRY—a global database of plant traits. Glob Change Biol  17: 2905–2935

Knipfer T, Brodersen CR, Zedan A, Kluepfel DA, McElrone AJ (2015) Patterns of drought-induced embolism formation and spread in living walnut saplings visualized using X-ray microtomography. Tree Physiol  35: 744–755 PubMed

Knipfer T, Cuneo I, Brodersen C, McElrone AJ (2016) In-situ visualization of the dynamics in xylem embolism formation and removal in the absence of root pressure: a study on excised grapevine stems. Plant Physiol (doi: 10.1104/pp.16.00136) PubMed DOI PMC

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. J Theor Biol  333: 146–155 PubMed

Loepfe L, Martinez-Vilalta J, Pinol J, Mencuccini M (2007) The relevance of xylem network structure for plant hydraulic efficiency and safety. J Theor Biol  247: 788–803 PubMed

Louarn G, Guedon Y, Lecoeur J, Lebon E (2007) Quantitative analysis of the phenotypic variability of shoot architecture in two grapevine (Vitis vinifera) cultivars. Ann Bot  99: 425–437 PubMed PMC

Martínez-Vilalta J, Mencuccini M, Álvarez X, Camacho J, Loepfe L, Piñol J (2012) Spatial distribution and packing of xylem conduits. Am J Bot  99: 1189–1196 PubMed

Melcher PJ, Michele Holbrook N, Burns MJ, Zwieniecki MA, Cobb AR, Brodribb TJ, Choat B, Sack L (2012) Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods Ecol Evol  3: 685–694

Mencuccini M, Martinez-Vilalta J, Piñol J, Loepfe L, Burnat M, Alvarez X, Camacho J, Gil D (2010) A quantitative and statistically robust method for the determination of xylem conduit spatial distribution. Am J Bot  97: 1247–1259 PubMed

Mrad A, Domec J-C, Huang C-W, Lens F, Katul G (2018) A network model links wood anatomy to xylem tissue hydraulic behavior and vulnerability to cavitation. Plant Cell Environ (doi: 10.1111/pce.13415) PubMed

Pratt C (1974) Vegetative anatomy of cultivated grapes—a review. Am J Enol Vitic  25: 131–150

Schenk HJ, Espino S, Romo DM, Nima N, Do AYT, Michaud JM, Papahadjopoulos-Sternberg B, Yang J, Zuo YY, Steppe K, et al. (2017) Xylem surfactants introduce a new element to the cohesion-tension theory. Plant Physiol  173: 1177–1196 PubMed PMC

Schenk HJ, Steppe K, Jansen S (2015) Nanobubbles: a new paradigm for air-seeding in xylem. Trends Plant Sci  20: 199–205 PubMed

Scholz A, Klepsch M, Karimi Z, Jansen S (2013) How to quantify conduits in wood?  Front Plant Sci  4: 56. PubMed PMC

Shavrukov YN, Dry IB, Thomas MR (2004) Inflorescence and bunch architecture development in Vitis vinifera L. Aust J Grape Wine Res  10: 116–124

Shen F, Gao R, Liu W, Zhang W (2002) Physical analysis of the process of cavitation in xylem sap. Tree Physiol  22: 655–659 PubMed

Sperry JS, Hacke UG (2004) Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes. Am J Bot  91: 369–385 PubMed

Sperry JS, Hacke UG, Wheeler JK (2005) Comparative analysis of end wall resistivity in xylem conduits. Plant Cell Environ  28: 456–465

Steppe K, Cnudde V, Girard C, Lemeur R, Cnudde J-P, Jacobs P (2004) Use of X-ray computed microtomography for non-invasive determination of wood anatomical characteristics. J Struct Biol  148: 11–21 PubMed

Suuronen J-P, Peura M, Fagerstedt K, Serimaa R (2013) Visualizing water-filled versus embolized status of xylem conduits by desktop x-ray microtomography. Plant Methods  9: 11. PubMed PMC

Tyree MT, Zimmermann MH (2002) Xylem Structure and the Ascent of Sap. 2nd edn. Springer, Berlin, Heidelberg

Wason JW, Anstreicher KS, Stephansky N, Huggett BA, Brodersen CR (2018) Hydraulic safety margins and air‐seeding thresholds in roots, trunks, branches and petioles of four northern hardwood trees. New Phytol  219: 77–88 PubMed

Wason JW, Huggett BA, Brodersen CR (2017) MicroCT imaging as a tool to study vessel endings in situ. Am J Bot  104: 1424–1430 PubMed

Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ  28: 800–812

Zhang Y, Carmesin C, Kaack L, Klepsch MM, Kotowska M, Matei T, Schenk HJ, Weber M, Walther P, Schmidt V, et al. (2020) High porosity with tiny pore constrictions and unbending pathways characterize the 3D structure of intervessel pit membranes in angiosperm xylem. Plant Cell Environ  43: 116–130 PubMed

Zimmermann MH, Jeje AA (1981) Vessel-length distribution in stems of some American woody plants. Can J Bot  59: 1882–1892

Xylem-dwelling pathogen unaffected by local xylem vessel network properties in grapevines (Vitis spp.)