Variations in xylem embolism susceptibility under drought between intact saplings of three walnut species

A germplasm collection containing varied Juglans genotypes holds potential to improve drought resistance of plant materials for commercial production. We used X-ray computed microtomography to evaluate stem xylem embolism susceptibility/repair in relation to vessel anatomical features (size, arrangement, connectivity and pit characteristics) in 2-year-old saplings of three Juglans species. In vivo analysis revealed interspecific variations in embolism susceptibility among Juglans microcarpa, J. hindsii (both native to arid habitats) and J. ailantifolia (native to mesic habitats). Stem xylem of J. microcarpa was more resistant to drought-induced embolism as compared with J. hindsii and J. ailantifolia (differences in embolism susceptibility among older and current year xylem were not detected in any species). Variations in most vessel anatomical traits were negligible among the three species; however, we detected substantial interspecific differences in intervessel pit characteristics. As compared with J. hindsii and J. ailantifolia, low embolism susceptibility in J. microcarpa was associated with smaller pit size in larger diameter vessels, a smaller area of the shared vessel wall occupied by pits, lower pit frequency and no changes in pit characteristics as vessel diameters increased. Changes in amount of embolized vessels following 40 days of re-watering were minor in intact saplings of all three species highlighting that an embolism repair mechanism did not contribute to drought recovery. In conclusion, our data indicate that interspecific variations in drought-induced embolism susceptibility are associated with species-specific pit characteristics, and these traits may provide a future target for breeding efforts aimed at selecting walnut germplasm with improved drought resistance.

[1]  C. Guillaume,et al.  Assessing frost damages using dynamic models in walnut trees: exposure rather than vulnerability controls frost risks. , 2018, Plant, cell & environment.

[2]  Storage Compartments for Capillary Water Rarely Refill in an Intact Woody Plant1[OPEN] , 2017, Plant Physiology.

[3]  T. Brodribb,et al.  Xylem and stomata, coordinated through time and space. , 2017, Plant, cell & environment.

[4]  Sylvain Delzon,et al.  Evidence for Hydraulic Vulnerability Segmentation and Lack of Xylem Refilling under Tension1[OPEN] , 2016, Plant Physiology.

[5]  A. McElrone,et al.  In Situ Visualization of the Dynamics in Xylem Embolism Formation and Removal in the Absence of Root Pressure: A Study on Excised Grapevine Stems1[OPEN] , 2016, Plant Physiology.

[6]  S. Mayr,et al.  Cavitation and water fluxes driven by ice water potential in Juglans regia during freeze–thaw cycles , 2015, Journal of experimental botany.

[7]  Sylvain Delzon,et al.  Noninvasive Measurement of Vulnerability to Drought-Induced Embolism by X-Ray Microtomography1 , 2015, Plant Physiology.

[8]  A. McElrone,et al.  Grapevine species from varied native habitats exhibit differences in embolism formation/repair associated with leaf gas exchange and root pressure. , 2015, Plant, cell & environment.

[9]  A. McElrone,et al.  Patterns of drought-induced embolism formation and spread in living walnut saplings visualized using X-ray microtomography. , 2015, Tree physiology.

[10]  Brendan Choat,et al.  Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. , 2015, The New phytologist.

[11]  E Badel,et al.  X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees. , 2015, Plant, cell & environment.

[12]  Sylvain Delzon,et al.  Direct X-Ray Microtomography Observation Confirms the Induction of Embolism upon Xylem Cutting under Tension1 , 2014, Plant Physiology.

[13]  H. Medrano,et al.  Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange. , 2014, Plant, cell & environment.

[14]  L. Wegner Root pressure and beyond: energetically uphill water transport into xylem vessels? , 2014, Journal of experimental botany.

[15]  Sylvain Delzon,et al.  Methods for measuring plant vulnerability to cavitation: a critical review. , 2013, Journal of experimental botany.

[16]  N. Holbrook,et al.  Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. , 2013, Plant, cell & environment.

[17]  Dilworth Y Parkinson,et al.  Using high resolution computed tomography to visualize the three dimensional structure and function of plant vasculature. , 2013, Journal of visualized experiments : JoVE.

[18]  S. Jansen,et al.  How to quantify conduits in wood? , 2013, Front. Plant Sci..

[19]  Brendan Choat,et al.  In Vivo Visualizations of Drought-Induced Embolism Spread in Vitis vinifera1[W][OA] , 2013, Plant Physiology.

[20]  Jian-Kang Zhu,et al.  Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase , 2013, Front. Plant Sci..

[21]  M. Mckenry,et al.  THE QUEST TO IDENTIFY DISEASE RESISTANCE IN THE USDA-ARS JUGLANS GERMPLASM COLLECTION , 2012 .

[22]  Daniel M. Johnson,et al.  Hydraulic architecture of two species differing in wood density: opposing strategies in co-occurring tropical pioneer trees. , 2012, Plant, cell & environment.

[23]  T. Améglio,et al.  Are budburst dates, dormancy and cold acclimation in walnut trees (Juglans regia L.) under mainly genotypic or environmental control? , 2011, International journal of biometeorology.

[24]  Brendan Choat,et al.  Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. , 2011, The New phytologist.

[25]  M. Zwieniecki,et al.  Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. , 2011, Plant, cell & environment.

[26]  Brendan Choat,et al.  The Dynamics of Embolism Repair in Xylem: In Vivo Visualizations Using High-Resolution Computed Tomography1[C][W][OA] , 2010, Plant Physiology.

[27]  W. Fricke,et al.  Root pressure and a solute reflection coefficient close to unity exclude a purely apoplastic pathway of radial water transport in barley (Hordeum vulgare). , 2010, The New phytologist.

[28]  J. Sperry,et al.  Testing the 'rare pit' hypothesis for xylem cavitation resistance in three species of Acer. , 2009, The New phytologist.

[29]  S. Jansen,et al.  Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. , 2009, American journal of botany.

[30]  P. Trifilò,et al.  Vessel wall vibrations: trigger for embolism repair? , 2008, Functional plant biology : FPB.

[31]  M. Aradhya,et al.  Molecular phylogeny of Juglans (Juglandaceae): a biogeographic perspective , 2007, Tree Genetics & Genomes.

[32]  J. Sperry,et al.  Inter‐vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade‐off in xylem transport , 2005 .

[33]  J. Marsal,et al.  Growth, yield and physiological behavior of size-controlling peach rootstocks developed in California , 2004 .

[34]  R. Morillon,et al.  Plasma Membrane Aquaporins Are Involved in Winter Embolism Recovery in Walnut Tree1 , 2003, Plant Physiology.

[35]  L. Christensen Wine Grape Varieties in California , 2003 .

[36]  N. Holbrook,et al.  Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees , 2003 .

[37]  Uwe G. Hacke,et al.  Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo , 2003 .

[38]  B. Choat,et al.  Pit Membrane Porosity and Water Stress-Induced Cavitation in Four Co-Existing Dry Rainforest Tree Species , 2003, Plant Physiology.

[39]  H. Cochard,et al.  Winter embolism, mechanisms of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees. , 2002, Tree physiology.

[40]  Hervé Cochard,et al.  Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. , 2002, Plant physiology.

[41]  M. Vandame,et al.  Seasonal variation in xylem pressure of walnut trees: root and stem pressures. , 2001, Tree physiology.

[42]  E T Ahrens,et al.  In vivo observation of cavitation and embolism repair using magnetic resonance imaging. , 2001, Plant physiology.

[43]  J. Sparks,et al.  Regulation of water loss in populations of Populus trichocarpa: the role of stomatal control in preventing xylem cavitation. , 1999, Tree physiology.

[44]  F. Ewers,et al.  Conduit diameter and drought‐induced embolism in Salvia mellifera Greene (Labiatae) , 1994 .

[45]  Hervé Cochard,et al.  Drought‐induced leaf shedding in walnut: evidence for vulnerability segmentation , 1993 .

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

[47]  S. Carlquist Comparative Wood Anatomy: Systematic, Ecological, and Evolutionary Aspects of Dicotyledon Wood , 1990 .