Divergence between ring- and diffuse-porous wood types in broadleaf trees of Changbai Mountains results in substantial differences in hydraulic traits.

doi:10.13287/j.1001-9332.201802.035

Abstract

Abstract: Hydraulic characteristics of trees are strongly influenced by their xylem structures. The divergence in wood type between ring-porous and diffuse-porous species is expected to lead to significantly different hydraulic architecture between these two functional groups. However, there is a lack of comprehensive comparative studies in hydraulic traits between the two groups, in that no study has compared the whole-shoot level hydraulic conductance and detailed pit-level xylem anatomy has not been reported yet. In the present study, detailed hydraulic related traits were stu-died in three ring-porous and four diffuse-porous tree species commonly found in the broadleaf tree species of the Changbai Mountains, including whole-shoot hydraulic conductance (K_shoot), resis-tance to drought-induced embolism (P₅₀), and detailed tissue- and pit-level anatomical characteristics. Our results showed that: 1) consistent with the differences in stem hydraulic conductivity, ring-porous species showed significantly higher K_shoot but significantly lower resistance to drought-induced embolism, i.e., higher P₅₀, indicating a trade-off between hydraulic efficiency and safety in those two functional groups; 2) consistent with their significant divergence in hydraulic functions, the two functional groups showed significant differences in a suite of xylem anatomical characteristics at both the tissue and pit levels, such as maximum vessel length, vessel diameter, pit aperture area and aperture fraction; 3) significant correlations were identified between xylem structural characteristics and between structure and functions across both functional groups, indicating that differences in hydraulic functions were underlain by divergences in a suite structural traits. The competing structural requirements between different hydraulic traits, such as between shoot hydraulic conductance and resistance to drought-induced embolism, reflected the biophysical constraints of xylem design that could not fulfill multiple requirements of xylem functioning at the same time.

YIN Xiao-han, HAO Guang-you. Divergence between ring- and diffuse-porous wood types in broadleaf trees of Changbai Mountains results in substantial differences in hydraulic traits.[J]. Chinese Journal of Applied Ecology, 2018, 29(2): 352-360.

References

[1] Hultine KR. Wood anatomy constrains stomatal responses to atmospheric vapor pressure deficit in irrigated, urban trees. Oecologia, 2008, 156: 13-20
[2] Loepfe L, Martinez-Vilalta J, Piñol J, et al. The relevance of xylem network structure for plant hydraulic efficiency and safety. Journal of Theoretical Biology, 2007, 247: 788-803
[3] Choat B, Cobb AR, Jansen S. Structure and function of bordered pits: New discoveries and impacts on whole-plant hydraulic function. New Phytologist, 2008, 177: 608-626
[4] Scholz A, Rabaey D, Stein A, et al. The evolution and function of vessel and pit characters with respect to cavitation resistance across 10 Prunus species. Tree Physiology, 2013, 33: 684-694
[5] Sperry JS. Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species. Plant Physiology, 1992, 100: 605-613
[6] Sperry JS, Nichols KL, Eastlack SE. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology, 1994, 75: 1736-1752
[7] Niu CY, Meinzer FC, Hao GY. Divergence in strategies for coping with winter embolism among co-occurring temperate tree species: The role of positive xylem pressure, wood type and tree stature. Functional Ecology, 2017, 31: 1550-1560
[8] Hacke UG, Sperry JS. Functional and ecological xylem anatomy. Perspectives in Plant Ecology, Evolution & Systematics, 2001, 4: 97-115
[9] Cochard H, Tyree MT. Xylem dysfunction in Quercus: Vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiology, 1990, 6: 393-407
[10] Hacke U, Sauter JJ. Drought-induced xylem dysfunction in petioles, branches, and roots of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn. Plant Physiology, 1996, 111: 413-417
[11] Kitin P, Funada R. Earlywood vessels in ring-porous trees become functional for water transport after bud burst and before the maturation of the current-year leaves. Iawa Journal, 2016, 37: 315-331
[12] Hammel HT. Freezing of xylem sap without cavitation. Plant Physiology, 1967, 42: 55-66
[13] Davis SD, Sperry JS, Hacke UG. The relationship between xylem conduit diameter and cavitation caused by freezing. American Journal of Botany, 1999, 86: 1367-1372
[14] Jiménez-Castillo M, Lusk CH. Vascular performance of woody plants in a temperate rain forest: Lianas suffer higher levels of freeze-thaw embolism than associated trees. Functional Ecology, 2013, 27: 403-412
[15] Cobb AR, Choat B, Holbrook NM. Dynamics of freeze-thaw embolism in Smilax rotundifolia (Smilacaceae). American Journal of Botany, 2007, 94: 640-649
[16] Hacke UG, Sperry JS, Wheeler JK, et al. Scaling of angiosperm xylem structure with safety and efficience. Tree Physiology, 2006, 26: 689-701
[17] Jansen S, Choat B, Pletsers A. Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. American Journal of Botany, 2009, 96: 409-419
[18] Wheeler JK, Sperry JS, Hacke UG, 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. Plant, Cell & Environment, 2005, 28: 800-812
[19] Choat B, Brodie TW, Cobb AR, et al. Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. American Journal of Botany, 2006, 93: 993-1000
[20] Sperry JS, Tyree MT. Mechanism of water stress-induced xylem embolism. Plant Physiology, 1988, 88: 581-587
[21] Lens F, Sperry JS, Christman MA, et al. Testing hypotheses that link wood anatomy to cavitation resis-tance and hydraulic conductivity in the genus Acer. New Phytologist, 2011, 190: 709-723
[22] Li S, Lens F, Espino S, et al. Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. Iawa Journal, 2016, 37: 152-171
[23] Taneda H, Sperry JS. A case-study of water transport in co-occurring ring- vs. diffuse-porous trees: Contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiology, 2008, 28: 1641-1651
[24] Brodribb TJ, Holbrook NM, Zwieniecki MA, et al. Leaf hydraulic capacity in ferns, conifers and angiosperms: Impacts on photosynthetic maxima.New Phytologist, 2005, 165: 839-846
[25] Li J-H (李俊辉), Li Y-Y (李秧秧), Zhao L-M (赵丽敏), et al. Effects of site conditions and tree age on Robinia pseudoacacia and Populus simonii leaf hydraulic traits and drought resistance. Chinese Journal of Applied Ecology (应用生态学报), 2012, 23(9): 2397-2403 (in Chinese)
[26] Ai S-S (艾绍水), Li Y-Y (李秧秧), Chen J-C (陈佳村), et al. Root anatomical structure and hydraulic traits of three typical shrubs on the sandy lands of northern Shaanxi Province, China. Chinese Journal of Applied Ecology (应用生态学报), 2015, 26(11): 3277-3284 (in Chinese)
[27] Wang AY, Wang M, Yang D, et al. Responses of hydraulics at the whole-plant level to simulated nitrogen deposition of different levels in Fraxinus mandshurica. Tree Physiology, 2016, 36: 1045-1055
[28] Song J, Yang D, Niu CY, et al. Correlation between leaf size and hydraulic architecture in five compound-leaved tree species of a temperate forest in NE China. Forest Ecology and Management, 2017, doi: org/10.1016/j.foreco.2017.08.005
[29] Choat B, Medek DE, Stuart SA, et al. Xylem traits mediate a trade-off between resistance to freeze-thaw-induced embolism and photosynthetic capacity in overwintering evergreens. New Phytologist, 2011, 191: 996-1005
[30] Niinemets Ü, Bilger W, Kull O, et al. Acclimation to high irradiance in temperate deciduous trees in the field: Changes in xanthophyll cycle pool size and in photosynthetic capacity along a canopy light gradient. Plant, Cell & Environment, 1998, 21: 1205-1218
[31] Améglio T, Bodet C, Lacointe A, et al. Winter embolism, mechanisms of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees. Tree Physiology, 2002, 22: 1211-1220
[32] Greenidge KNH. An approach to the study of vessel length in hardwood species. American Journal of Botany, 1952, 39: 570-574
[33] Cohen S, Bennink J, Tyree MT. Air method measurements of apple vessel length distributions with improved apparatus and theory. Journal of Experimental Botany, 2003, 54: 1889-1897
[34] Tyree MT, Sinclair B, Lu P, et al. Whole shoot hydraulic resistance in Quercus species measured with a new high-pressure flowmeter. Annals of Forest Science, 1993, 50: 417-423
[35] Zwieniecki MA, Peter J, Melcher N, et al.Hydraulic properties of individual xylem vessels of Fraxinus americana. Journal of Experimental Botany, 2001, 52: 257-264
[36] Christman MA, Sperry JS, Adler FR. Testing the ‘rare pit’ hypothesis for xylem cavitation resistance in three species of Acer. New Phytologist, 2009, 182: 664-674
[37] Christman MA, Sperry JS, Smith DD. Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. New Phytologist, 2012, 193 : 713-720
[38] Steppe K, Lemeur R. Effects of ring-porous and diffuse-porous stem wood anatomy on the hydraulic parameters used in a water flow and storage model. Tree Physiology, 2007, 27: 43-52
[39] Sperry JS, Tyree MT. Mechanism of water stress-induced xylem embolism. Plant Physiology, 1988, 88: 581-587
[40] Tyree MT, Davis SD, Cochard H. Biophysical perspectives of xylem evolution: Is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? Iawa Journal, 1994, 15: 335-360
[41] Cochard H, Cruiziat P, Tyree MT. Use of positive pressures to establish vulnerability curves: Further support for the air-seeding hypothesis and implications for pressure-volume analysis. Plant Physiology, 1992, 100: 205-209
[42] Choat B, Ball MC, Luly JG, et al. Hydraulic architecture of deciduous and evergreen dry rainforest tree species from north-eastern Australia. Trees, 2005, 19: 305-311
[43] Lewis AM, Boose ER. Estimating volume flow-rates through xylem conduits. American Journal of Botany, 1995, 82: 1112-1116
[44] Sperry JS, Hacke UG. Analysis of circular bordered pit function. Ⅰ. Angiosperm vessels with homogenous pit membranes. American Journal of Botany, 2004, 91: 369-385