Is Decreased Xylem Sap Surface Tension Associated With Embolism and Loss of Xylem Hydraulic Conductivity in Pathogen-Infected Norway Spruce Saplings?

Increased abiotic stress along with increasing temperatures, dry periods and forest disturbances may favor biotic stressors such as simultaneous invasion of bark beetle and ophiostomatoid fungi. It is not fully understood how tree desiccation is associated with colonization of sapwood by fungi. A decrease in xylem sap surface tension (σxylem) as a result of infection has been hypothesized to cause xylem embolism by lowering the threshold for air-seeding at the pits between conduits and disruptions in tree water transport. However, this hypothesis has not yet been tested. We investigated tree water relations by measuring the stem xylem hydraulic conductivity (Kstem), σxylem, stem relative water content (RWCstem), and water potential (Ψstem), and canopy conductance (gcanopy), as well as the compound composition in xylem sap in Norway spruce (Picea abies) saplings. We conducted our measurements at the later stage of Endoconidiophora polonica infection when visible symptoms had occurred in xylem. Saplings of two clones (44 trees altogether) were allocated to treatments of inoculated, wounded control and intact control trees in a greenhouse. The saplings were destructively sampled every second week during summer 2016. σxylem, Kstem and RWCstem decreased following the inoculation, which may indicate that decreased σxylem resulted in increased embolism. gcanopy did not differ between treatments indicating that stomata responded to Ψstem rather than to embolism formation. Concentrations of quinic acid, myo-inositol, sucrose and alkylphenol increased in the xylem sap of inoculated trees. Myo-inositol concentrations also correlated negatively with σxylem and Kstem. Our study is a preliminary investigation of the role of σxylem in E. polonica infected trees based on previous hypotheses. The results suggest that E. polonica infection can lead to a simultaneous decrease in xylem sap surface tension and a decline in tree hydraulic conductivity, thus hampering tree water transport.

[1]  B. Lachenbruch,et al.  Effects of Phloem on Canopy Dieback, Tested with Manipulations and a Canker Pathogen in the Corylus avellana/Anisogramma anomala Host/Pathogen System. , 2019, Tree physiology.

[2]  P. Hietz,et al.  Transpiration deficits increase host susceptibility to bark beetle attack: Experimental observations and practical outcomes for Ips typographus hazard assessment , 2018, Agricultural and Forest Meteorology.

[3]  P. Poot,et al.  Tree host–pathogen interactions as influenced by drought timing: linking physiological performance, biochemical defence and disease severity , 2018, Tree physiology.

[4]  B. Heinze,et al.  Prediction of hydraulic conductivity loss from relative water loss: new insights into water storage of tree stems and branches , 2018, Physiologia plantarum.

[5]  M. Peltoniemi,et al.  Quantifying in situ phenotypic variability in the hydraulic properties of four tree species across their distribution range in Europe , 2018, PloS one.

[6]  T. Takanashi,et al.  Pine wilt disease causes cavitation around the resin canals and irrecoverable xylem conduit dysfunction , 2018, Journal of experimental botany.

[7]  S. Junttila,et al.  Effects of water availability on a forestry pathosystem: fungal strain-specific variation in disease severity , 2017, Scientific Reports.

[8]  A. Losso,et al.  Xylem Sap Surface Tension May Be Crucial for Hydraulic Safety1[OPEN] , 2017, Plant Physiology.

[9]  M. Wingfield,et al.  Testing Projected Climate Change Conditions on the Endoconidiophora polonica / Norway spruce Pathosystem Shows Fungal Strain Specific Effects , 2017, Front. Plant Sci..

[10]  Ronald J. Hall,et al.  Biotic disturbances in Northern Hemisphere forests – a synthesis of recent data, uncertainties and implications for forest monitoring and modelling , 2017 .

[11]  S. Jansen,et al.  Xylem Surfactants Introduce a New Element to the Cohesion-Tension Theory1[OPEN] , 2016, Plant Physiology.

[12]  S. Jansen,et al.  The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought , 2016, Proceedings of the National Academy of Sciences.

[13]  A. Pappinen,et al.  Seasonal Succession of Fungi Associated with Ips typographus Beetles and Their Phoretic Mites in an Outbreak Region of Finland , 2016, PloS one.

[14]  S. Bojovic,et al.  Pathogenicity of ophiostomatoid fungi on Picea abies in Slovenia , 2015 .

[15]  Kathy Steppe,et al.  Nanobubbles: a new paradigm for air-seeding in xylem. , 2015, Trends in plant science.

[16]  Bradley Matthews,et al.  Do water-limiting conditions predispose Norway spruce to bark beetle attack? , 2014, The New phytologist.

[17]  N. Prisle,et al.  Cloud droplet activation of mixed model HULIS and NaCl particles: Experimental results and κ-Köhler theory , 2014 .

[18]  P. Krokene,et al.  Conifer Stored Resources and Resistance to a Fungus Associated with the Spruce Bark Beetle Ips typographus , 2013, PloS one.

[19]  M. Garbelotto,et al.  Characterization of fungal communities associated with the bark beetle Ips typographus varies depending on detection method, location, and beetle population levels , 2013, Mycological Progress.

[20]  Jianchi Chen,et al.  Grapevine phenolic compounds in xylem sap and tissues are significantly altered during infection by Xylella fastidiosa. , 2012, Phytopathology.

[21]  S. Jansen,et al.  Plasmodesmatal pores in the torus of bordered pit membranes affect cavitation resistance of conifer xylem. , 2012, Plant, cell & environment.

[22]  M. Wingfield,et al.  Associations of Conifer-Infesting Bark Beetles and Fungi in Fennoscandia , 2012, Insects.

[23]  A. Porcar-Castell,et al.  Cavitation induced by a surfactant leads to a transient release of water stress and subsequent ‘run away’ embolism in Scots pine (Pinus sylvestris) seedlings , 2011, Journal of experimental botany.

[24]  R. Valluru,et al.  Myo-inositol and beyond--emerging networks under stress. , 2011, Plant science : an international journal of experimental plant biology.

[25]  M. Tyree,et al.  Surface tension phenomena in the xylem sap of three diffuse porous temperate tree species. , 2011, Tree physiology.

[26]  Jean-Christophe Domec,et al.  Let's not forget the critical role of surface tension in xylem water relations. , 2011, Tree physiology.

[27]  C. Douthe,et al.  Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding , 2010, Plant, cell & environment.

[28]  A. Laaksonen,et al.  Surfactants in cloud droplet activation: mixed organic-inorganic particles , 2009 .

[29]  Sylvain Delzon,et al.  New Insights into the Mechanisms of Water-Stress-Induced Cavitation in Conifers , 2009, Plant Physiology.

[30]  T. Brodribb,et al.  Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers[OA] , 2008, Plant Physiology.

[31]  Tomi Raatikainen,et al.  Ternary solution of sodium chloride, succinic acid and water; surface tension and its influence on cloud droplet activation , 2008 .

[32]  P. Hietz,et al.  Comparison of methods to quantify loss of hydraulic conductivity in Norway spruce , 2008, Annals of Forest Science.

[33]  N. McDowell,et al.  Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? , 2008, The New phytologist.

[34]  K. A. Flynn A review of The Permeability, Fluid Flow, and Anatomy of Spruce ( Picea SPP.) , 2007 .

[35]  N. Matubayasi,et al.  Thermodynamic quantities of surface formation of aqueous electrolyte solutions. VI. Comparison with typical nonelectrolytes, sucrose and glucose. , 2006, Journal of colloid and interface science.

[36]  K. Kuroda Xylem dysfunction in Yezo spruce (Picea jezoensis) after inoculation with the blue‐stain fungus Ceratocystis polonica , 2005 .

[37]  F. Lieutier,et al.  Fungal flora associated with Ips typographus: frequency, virulence, and ability to stimulate the host defence reaction in relation to insect population levels , 2005 .

[38]  F. Meinzer,et al.  Native root xylem embolism and stomatal closure in stands of Douglas-fir and ponderosa pine: mitigation by hydraulic redistribution , 2004, Oecologia.

[39]  S. Jansen,et al.  Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. , 2004, Journal of experimental botany.

[40]  T. Munnik,et al.  Phospholipid-based signaling in plants. , 2003, Annual review of plant biology.

[41]  I. Offenthaler,et al.  Xylem sap flow of Norway spruce after inoculation with the blue‐stain fungus Ceratocystis polonica , 2002 .

[42]  Thomas Kirisits,et al.  Defence reactions of Norway spruce against bark beetles and the associated fungus Ceratocystis polonica in secondary pure and mixed species stands , 2002 .

[43]  E. Christiansen,et al.  Wound-induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy and cytochemical traits. , 2000, American journal of botany.

[44]  F. Loewus,et al.  myo-Inositol metabolism in plants , 2000 .

[45]  Frances S. Ligler,et al.  Comparison of chemical cleaning methods of glass in preparation for silanization , 1999 .

[46]  Krokene,et al.  Induced resistance to pathogenic fungi in norway spruce , 1999, Plant physiology.

[47]  R. Bhat,et al.  Thermal Stability of Proteins in Aqueous Polyol Solutions: Role of the Surface Tension of Water in the Stabilizing Effect of Polyols , 1998 .

[48]  C. V. Willigen,et al.  A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. , 1998, Tree physiology.

[49]  A. Berryman,et al.  Specialized phloem parenchyma cells in Norway spruce (Pinaceae) bark are an important site of defense reactions. , 1998, American journal of botany.

[50]  H. Solheim Oxygen deficiency and spruce resin inhibition of growth of blue stain fungi associated with Ips typographus , 1991 .

[51]  W. R. N. Edwards,et al.  The refilling of embolized xylem in Pinus sylvestris L. , 1991 .

[52]  M. Tyree,et al.  Water-storage capacity ofThuja, Tsuga andAcer stems measured by dehydration isotherms , 1990, Planta.

[53]  J. Sperry,et al.  Mechanism of water stress-induced xylem embolism. , 1988, Plant physiology.

[54]  N. Turner Measurement of plant water status by the pressure chamber technique , 1988, Irrigation Science.

[55]  R. B. Pearce,et al.  Wound-associated responses in Sitka spruce root bark challenged with Phaeolus schweinitzii , 1988 .

[56]  E. Christiansen Ceratocysts polonica inoculated in Norway spruce: Blue‐staining in relation to inoculum density, resinosis and tree growth , 1985 .

[57]  W. E. Cole,et al.  Blue-stain fungi in xylem of lodgepole pine: a light-microscope study on extent of hyphal distribution , 1982 .

[58]  A. Lawrence Surface Chemistry for Industrial Research , 1948, Nature.

[59]  R. F. Makens,et al.  THE SURFACE RELATIONS OF THE COMPONENTS OF PINE OIL AND OF POTASSIUM ETHYL XANTHATE. II1 , 1932 .

[60]  S. Jansen,et al.  The Role of Xylem Parenchyma in the Storage and Utilization of Nonstructural Carbohydrates , 2015 .

[61]  L. Hildemann,et al.  Measuring and modeling the composition and temperature-dependence of surface tension for organic solutions , 2010 .

[62]  Puertolas Jaime,et al.  光と穏和な水ストレスに対するQuercus suber L.苗の相互作用的応答:形態およびガス交換特性 , 2008 .

[63]  H. Lihavainen,et al.  Surface Tensions and Densities of Oxalic, Malonic, Succinic, Maleic, Malic, and cis-Pinonic Acids , 2006 .

[64]  M. Hipkins,et al.  Maximum sustainable xylem sap tensions in Rhododendron and other species , 2004, Planta.

[65]  M. Zimmermann,et al.  Hydraulic Architecture of Whole Plants and Plant Performance , 2002 .

[66]  V. Kitunen,et al.  Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica , 2001, Trees.

[67]  H. Solheim,et al.  Pathogenicity of four blue-stain fungi associated with aggressive and nonaggressive bark beetles. , 1998, Phytopathology.

[68]  S. Davis,et al.  Biophysical Perspectives of Xylem Evolution: is there a Tradeoff of Hydraulic Efficiency for Vulnerability to Dysfunction? , 1994 .

[69]  E. Christiansen,et al.  Pruning enhances the susceptibility of Picea abies to infection by the bark beetle‐transmitted blue‐stain fungus, Ophiostoma polonicum , 1993 .

[70]  T. Yamada Biochemistry of Gymnosperm Xylem Responses to Fungal Invasion , 1992 .

[71]  T. Perry A Synopsis of the Taxonomic Revisions in the Genus Ceratocystis Including a Review of Blue-Staining Species Associated with Dendroctonus Bark Beetles , 1991 .

[72]  A. Tyree,et al.  Vulnerability of Xylem to Cavitation and Embolism , 1989 .

[73]  Melvin T. Tyree,et al.  A method for measuring hydraulic conductivity and embolism in xylem , 1988 .

[74]  E. Christiansen,et al.  Artificial inoculation with Ips typographus-associated blue-stain fungi can kill healthy Norway spruce trees [Ceratocystis polonica, Ceratocystis penicillata, water stress] , 1983 .