Hydraulic regulation of Populus tomentosa and Acer truncatum under drought stress

doi:10.17521/cjpe.2021.0495

Abstract

Abstract:

Aims The tree decline and death caused by drought stress under global climate change is a topic of general interest in ecological research. Different tree species in the same habitat can adopt various hydraulic strategies to maintain water balance in order to deal with drought stress. Populus tomentosa and Acer truncatum are the main tree species in plantations in the North China Plain. Studies on their hydraulic structure and dynamics of non-structural carbohydrate (NSC) content during drought-rehydration can reveal their hydraulic regulation strategies and provide theoretical basis for scientific management of water balance in plantations in north China under the background of global climate change.

Methods By using the saplings of P. tomentosa and A. truncatum distributed in the same habitat, we measured the hydraulic structure parameters, such as the resistance to embolism and hydraulic safety margin of stem, hydraulic areas, osmotic potential at leaf turgor pressure loss point, etc. Dehydration and rehydration were carried out to investigate the dynamics of stem NSC content, and to examine the repair capacity of xylem embolism in the rehydration stage after drought stress removel.

Important findings The results showed that the water potential of P. tomentosa (-1.289 MPa) when xylem hydraulic conductivity lost 50% was higher than that of A. truncatum(-2.894 MPa). Populus tomentosa also presented lower osmotic potential at turgor pressure loss point, narrower hydraulic safety margin, smaller wood density, and tended to have anisohydry behavior of stomatal regulation, indicating that it was prone to embolism characterized with dehydration and drought tolerance at low water potential, and tended to have more risky water regulation strategies. Acer truncatum survived drought stress by “delayed dehydration” at high water potentials, and tended to have conservative water regulation strategy. In the dehydration-rehydration experiment, the contents of soluble sugar, starch and non-structural carbohydrate in stem of P. tomentosa decreased first and then increased, while those of A. truncatum increased first and then decreased, and P. tomentosa showed a higher embolic repair ability than A. truncatum, which was related to the difference of stem NSC content. The higher embolism repair ability of P. tomentosa can provide hydraulic safety guarantee for risky water regulation strategies and drought tolerance strategy. There were significant differences between P. tomentosa and A. truncatum in the regulation of hydraulics, which might be related to the characteristics of life history.

Key words: hydraulic regulation, water regulation countermeasure, non-structural carbohydrate, embolism repair, drought tolerance characteristic

WU Min, TIAN Yu, FAN Da-Yong, ZHANG Xiang-Xue. Hydraulic regulation of Populus tomentosa and Acer truncatum under drought stress[J]. Chin J Plant Ecol, 2022, 46(9): 1086-1097.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0495

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Figures/Tables 9

Fig. 1 Stem vulnerability curves of Populus tomentosa and Acer truncatum (mean ± SE, n = 6). Vertical dashed lines represent calculated xylem water potential when hydraulic conductivity lost 50% (Ψxylem-50) in P. tomentosa; vertical solid lines represent calculated Ψxylem-50 of A. truncatum.

Table 1 Vulnerability parameters of Populus tomentosa and Acer truncatum

树种 Tree species	导水率损失50% 对应的木质部水势 Xylem water potential corresponding to 50% loss of hydraulic conductivity (Ψ_xylem-50)(MPa)	水力安全阈 Hydraulic safety margin (HSM) (MPa)	木质部修复系数 Xylem recovery index (XRI)	相对于干旱期间的木质部修复系数 Xylem recovery index-drought (XRID)	导水率损失百分比的日变化 Diurnal changes in percentage loss of hydraulic conductivity (ΔPLC)(%)
毛白杨 P. tomentosa	-1.289	0.350	0.740	0.362	40.450
元宝槭 A. truncatum	-2.894	2.750	0.529	0.077	3.237

Fig. 2 Hydraulic area maps of Populus tomentosa and Acer truncatum. Gray areas indicate hydraulic area regions, numbers in parentheses are calculated hydraulic areas. Ψleaf-md, leaf water potential in the midday; Ψleaf-pd, leaf water potential predawn.

Table 2 Stem hydraulic structure parameters of Populus tomentosa and Acer truncatum (mean ± SE)

树种 Tree species	胡伯尔值 Huber value (Hv) (cm²·g^-1)	最大导水率 Maximum hydraulic conductivity (K_hmax) (kg·MPa^-1·m^-1·s^-1)	最大比导水率 Maximum specific conductivity (K_s) (kg·MPa^-1·m^-1·s^-1)	最大比叶导水率 Maximum leaf specific conductivity (LSC) (kg·MPa^-1·m^-1·s^-1)	最大导管长度 Maximum vessel length (MVL) (cm)	木材密度 Wood density (WD)(g·cm^-1)
毛白杨 P. tomentosa	0.031 ± 0.002^a	13.43 ± 4.65^a	10.17 ± 2.25^a	0.0017 ± 0.0003^a	22.29 ± 1.72^a	0.235 ± 0.009^a
元宝槭 A. truncatum	0.026 ± 0.001^a	1.30 ± 0.74^b	1.49 ± 0.57^b	0.0004 ± 0.0001^b	7.83 ± 0.77^b	0.361 ± 0.023^b

Table 3 Leaf hydraulic structure parameters of Populus tomentosa and Acer truncatum (mean ± SE)

树种 Tree species	比叶质量 Specific leaf mass (LMA)(g·cm^-2)	叶密度 Leaf density (LD)(g·cm^-1)	叶干物质含量 Leaf dry matter content (LDMC)
毛白杨 P. tomentosa	0.006 5 ± 0.000 3^a	0.149 ± 0.006^a	0.313 ± 0.007^a
元宝槭 A. truncatum	0.005 5 ± 0.000 2^b	0.240 ± 0.009^b	0.331 ± 0.008^a

Table 4 Comparison of pressure volume curve parameters between Populus tomentosa and Acer truncatum (mean ± SE)

树种 Tree species	饱和渗透势 Saturated osmotic potential (Ψ_sat) (-MPa)	膨压损失点时渗透势 Osmotic potential of turgor loss point (Ψ_tlp)(-MPa)	膨压损失点相对含水量 Relative water content of turgor loss point (RWC_tlp)(%)	最大弹性模量 Maximum modulus of elasticity (ε_max)(MPa)	水容 Water capacitance (C_leaf) (mol·m^-2·MPa^-1)	\|Ψ_sat - Ψ_tlp\| (MPa)
毛白杨 P. tomentosa	1.82 ± 0.30^a	2.44 ± 0.54^a	88.08 ± 1.02^a	13.70 ± 1.06^a	0.280 ± 0.009^a	0.62 ± 0.34^a
元宝槭 A. truncatum	1.51 ± 0.10^a	1.76 ± 0.10^b	86.41 ± 0.98^a	11.55 ± 1.43^a	0.557 ± 0.096^b	0.25 ± 0.06^b

Fig. 3 Changes of xylem water potential (Ψxylem) of Populus tomentosa and Acer truncatum during dehydration-rehydration (mean ± SE, n = 6). Compared with the control group, Ψxylem decreased during the drought treatment in the dehydration-rehydration group. In the 5th and 11th days of dehydration, the Ψxylem of P. tomentosa and A. truncatum reached the water potential when hydraulic conductivity lost 50% respectively, and then Ψxylem recovered when treated with rehydration.

Fig. 4 Changes of non-structural carbohydrates (NSC) and its components in the stems of Populus tomentosa and Acer truncatum under different water conditions (mean ± SE, n = 6). Different uppercase letters indicate the same substance has significant differences between the two tree species under the same moisture, and different lowercase letters indicate the same substance has significant differences among the treatments under the same tree species (p < 0.05). Ψxylem-50, water potential when hydraulic conductivity lost 50%.

Fig. 5 Response of soluble sugar content/starch content of Populus tomentosa and Acer truncatum stems to different moisture conditions (mean ± SE, n = 6). Ψxylem-50, water potential when hydraulic conductivity lost 50%.

References 70

[1]	Alder NN, Sperry JS, Pockman WT (1996). Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia, 105, 293-301. DOI PMID
[2]	Anderegg WRL, Flint A, Huang CY, Flint L, Berry JA, Davis FW, Sperry JS, Field CB (2015). Tree mortality predicted from drought-induced vascular damage. Nature Geoscience, 8, 367-371. DOI URL
[3]	Bartlett MK, Scoffoni C, Sack L (2012). The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecology Letters, 15, 393-405. DOI PMID
[4]	Berry ZC, Espejel X, Williams-Linera G, Asbjornsen H (2019). Linking coordinated hydraulic traits to drought and recovery responses in a tropical montane cloud forest. American Journal of Botany, 106, 1316-1326. DOI PMID
[5]	Brodersen CR, McElrone AJ (2013). Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Frontiers in Plant Science, 4, 108. DOI: 10.3389/fpls.2013.00108. DOI
[6]	Carola P, Virginia W, Christopher S, Raphael T, Arndt SK (2020). Phenotypic plasticity and genetic adaptation of functional traits influences intra-specific variation in hydraulic efficiency and safety. Tree physiology, 40, 215-229. DOI PMID
[7]	Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martínez-Vilalta J, Mayr S, et al. (2012). Global convergence in the vulnerability of forests to drought. Nature, 491, 752-755. DOI URL
[8]	Cochard H, Cruiziat P, Tyree MT (1992). Use of positive pressures to establish vulnerability curves further support for the air-seeding hypothesis and implications for pressure-volume analysis. Plant Physiology, 100, 205-209. DOI PMID
[9]	Cochard H, Delzon S (2013). Hydraulic failure and repair are not routine in trees. Annals of Forest Science, 70, 659-661. DOI URL
[10]	Ewers FW, Fisher JB (1989). Techniques for measuring vessel lengths and diameters in stems of woody plants. American Journal of Botany, 76, 645-656. DOI URL
[11]	Hartmann H, Trumbore S (2016). Understanding the roles of nonstructural carbohydrates in forest trees—From what we can measure to what we want to know. New Phytologist, 211, 386-403. DOI PMID
[12]	He DP, Meng QY, Yang CY, Wu J, Hu Q (2021). Spatial and temporal distribution of extreme drought in North China Area. Technology Wind, (25), 121-123.
	[何东坡, 孟庆怡, 杨春艳, 吴静, 胡倩 (2021). 极端干旱频率在华北地区的变化. 科技风, (25), 121-123.]
[13]	Jacobsen AL, Ewers FW, Pratt RB, Paddock WA, Davis SD (2005). Do xylem fibers affect vessel cavitation resistance? Plant Physiology, 139, 546-556. PMID
[14]	Jiang PP, Meinzer FC, Fu XL, Kou L, Dai XQ, Wang HM (2020). Trade-offs between xylem water and carbohydrate storage among 24 coexisting subtropical understory shrub species spanning a spectrum of isohydry. Tree Physiology, 41, 403-415. DOI URL
[15]	Jin Y, Wang CK, Zhou ZH (2016). Mechanisms of xylem embolism repair in woody plants: research progress and questions. Chinese Journal of Plant Ecology, 40, 834-846. DOI
	[金鹰, 王传宽, 周正虎 (2016). 木本植物木质部栓塞修复机制: 研究进展与问题. 植物生态学报, 40, 834-846.] DOI
[16]	Johnson DM, Berry ZC, Baker KV, Smith DD, McCulloh KA, Domec JC (2018a). Leaf hydraulic parameters are more plastic in species that experience a wider range of leaf water potentials. Functional Ecology, 32, 894-903. DOI URL
[17]	Johnson DM, Domec JC, Carter Berry Z, Schwantes AM, McCulloh KA, Woodruff DR, Wayne Polley H, Wortemann R, Swenson JJ, Mackay Scott Mackay D, McDowell NG, Jackson RB (2018b). Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought. Plant, Cell & Environment, 41, 576-588.
[18]	Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC (2012). Hydraulic safety margins and embolism reversal in stems and leaves: Why are conifers and angiosperms so different? Plant Science, 195, 48-53. DOI PMID
[19]	Kannenberg SA, Phillips RP (2017). Soil microbial communities buffer physiological responses to drought stress in three hardwood species. Oecologia, 183, 631-641. DOI PMID
[20]	Karst J, Gaster J, Wiley E, Landhäusser SM (2016). Stress differentially causes roots of tree seedlings to exude carbon. Tree Physiology, 37, 154-164.
[21]	Klein T, Zeppel MJB, Anderegg WRL, Bloemen J, De Kauwe MG, Hudson P, Ruehr NK, Powell TL, von Arx G, Nardini A (2018). Xylem embolism refilling and resilience against drought-induced mortality in woody plants: processes and trade-offs. Ecological Research, 33, 839-855.
[22]	Li JY, Zhang JG (1993). Studies on classification models and mechanisms of drought tolerance of chief afforestation species in the northern part of China (I)—The classification of relationships between seedling leaf water potential and soil water content. Journal of Beijing Forestry University, 15(3), 1-11.
	[李吉跃, 张建国 (1993). 北方主要造林树种耐旱机理及其分类模型的研究(I)——苗木叶水势与土壤含水量的关系及分类. 北京林业大学学报, 15(3), 1-11.]
[23]	Li R, Jiang ZM, Zhang SX, Cai J (2015). A review of new research progress on the vulnerability of xylem embolism of woody plants. Chinese Journal of Plant Ecology, 39, 838-848. DOI
	[李荣, 姜在民, 张硕新, 蔡靖 (2015). 木本植物木质部栓塞脆弱性研究新进展. 植物生态学报, 39, 838-848.] DOI
[24]	Li XM, Blackman CJ, Peters JMR, Choat B, Rymer PD, Medlyn BE, Tissue DT (2019). More than iso/anisohydry: hydroscapes integrate plant water use and drought tolerance traits in 10 eucalypt species from contrasting climates. Functional Ecology, 33, 1035-1049. DOI URL
[25]	Li ZD, Chen ZC, Cao Z, Che LP, Liu SW, Zhang YT (2021). Xylem anatomical and hydraulic drought resistance characteristics of common tree species in hilly areas of North China. Acta Ecologica Sinica, 41, 69-78.
	[李泽东, 陈志成, 曹振, 车路平, 刘舒文, 张永涛 (2021). 华北低山丘陵区常用树种木质部解剖特征及水其力学抗旱性. 生态学报, 41, 69-78.]
[26]	Liang XY, Ye Q, Liu H, Brodribb TJ (2021). Wood density predicts mortality threshold for diverse trees. New Phytologist, 229, 3053-3057. DOI PMID
[27]	Luo DD, Wang CK, Jin Y (2017). Plant water-regulation strategies: isohydric versus anisohydric behavior. Chinese Journal of Plant Ecology, 41, 1020-1032. DOI URL
	[罗丹丹, 王传宽, 金鹰 (2017). 植物水分调节对策: 等水与非等水行为. 植物生态学报, 41, 1020-1032.] DOI
[28]	Ma Y, Su BL, Han YG, Wu XH, Zhou WM, Wang QW, Zhou L, Yu DP (2021). Response of photosynthetic characteristics and non-structural carbohydrate accumulation of Betula ermanii seedlings to drought stress. Chinese Journal of Applied Ecology, 32, 513-520.
	[马玥, 苏宝玲, 韩艳刚, 吴星慧, 周旺明, 王庆伟, 周莉, 于大炮 (2021). 岳桦幼苗光合特性和非结构性碳水化合物积累对干旱胁迫的响应. 应用生态学报, 32, 513-520.] DOI
[29]	Martorell S, Diaz-Espejo A, Medrano H, Ball MC, Choat B (2014). Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange. Plant, Cell & Environment, 37, 617-626.
[30]	McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M (2011). The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology & Evolution, 26, 523-532. DOI URL
[31]	Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009). Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Functional Ecology, 23, 922-930. DOI URL
[32]	Mirfenderesgi G, Matheny AM, Bohrer G (2019). Hydrodynamic trait coordination and cost-benefit trade-offs throughout the isohydric-anisohydric continuum in trees. Ecohydrology, 12, e2041. DOI: 10.1002/eco.2041. DOI
[33]	Mota-Gutiérrez D, Arreola-González G, Aguilar-Romero R, Paz H, Cavender-Bares J, Oyama K, Gonzalez-Rodriguez A, Pineda-García F (2019). Seasonal variation in native hydraulic conductivity between two deciduous oak species. Journal of Plant Ecology, 13, 78-86. DOI URL
[34]	Nardini A, Battistuzzo M, Savi T (2013). Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought. New Phytologist, 200, 322-329. DOI PMID
[35]	Nardini A, Lo Gullo MA, Salleo S (2011). Refilling embolized xylem conduits: Is it a matter of phloem unloading? Plant Science, 180, 604-611. DOI PMID
[36]	Nardini A, Savi T, Losso A, Petit G, Pacilè S, Tromba G, Mayr S, Trifilò P, Lo Gullo MA, Salleo S (2017). X-ray microtomography observations of xylem embolism in stems of Laurus nobilis are consistent with hydraulic measurements of percentage loss of conductance. New Phytologist, 213, 1068-1075. DOI PMID
[37]	Nolf M, Lopez R, Peters JMR, Flavel RJ, Koloadin LS, Young IM, Choat B (2017). Visualization of xylem embolism by X-ray microtomography: a direct test against hydraulic measurements. New Phytologist, 214, 890-898. DOI PMID
[38]	Ogasa M, Miki NH, Murakami Y, Yoshikawa K (2013). Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate deciduous tree species. Tree Physiology, 33, 335-344. DOI PMID
[39]	Oliveira RS, Eller CB, de V Barros F, Hirota M, Brum M, Bittencourt P (2021). Linking plant hydraulics and the fast-slow continuum to understand resilience to drought in tropical ecosystems. New Phytologist, 230, 904-923. DOI PMID
[40]	Osaki M, Shinano T, Tadano T (1991). Redistribution of carbon and nitrogen compounds from the shoot to the harvesting organs during maturation in field crops. Soil Science and Plant Nutrition, 37, 117-128. DOI URL
[41]	Pagliarani C, Casolo V, Ashofteh Beiragi M, Cavalletto S, Siciliano I, Schubert A, Gullino ML, Zwieniecki MA, Secchi F (2019). Priming xylem for stress recovery depends on coordinated activity of sugar metabolic pathways and changes in xylem sap pH. Plant, Cell & Environment, 42, 1775-1787.
[42]	Ramírez-Valiente JA, Center A, Sparks JP, Sparks KL, Etterson JR, Longwell T, Pilz G, Cavender-Bares J (2017). Population- level differentiation in growth rates and leaf traits in seedlings of the neotropical live oak Quercus oleoides grown under natural and manipulated precipitation regimes. Frontiers in Plant Science, 8, 585. DOI: 10.3389/fpls.2017.00585. DOI
[43]	Rosas T, Galiano L, Ogaya R, Peñuelas J, Martínez-Vilalta J (2013). Dynamics of non-structural carbohydrates in three Mediterranean woody species following long-term experimental drought. Frontiers in Plant Science, 4, 400. DOI: 10.3389/fpls.2013.00400. DOI
[44]	Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003). The “hydrology” of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell & Environment, 26, 1343-1356.
[45]	Salleo S, Lo gullo MA, Trifilò P, Nardini A (2004). New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant, Cell & Environment, 27, 1065-1076.
[46]	Savi T, Casolo V, Luglio J, Bertuzzi S, Trifilò P, Lo Gullo MA, Nardini A (2016). Species-specific reversal of stem xylem embolism after a prolonged drought correlates to endpoint concentration of soluble sugars. Plant Physiology and Biochemistry, 106, 198-207. DOI PMID
[47]	Savi T, Love VL, dal Borgo A, Martellos S, Nardini A (2017a). Morpho-anatomical and physiological traits in saplings of drought-tolerant Mediterranean woody species. Trees, 31, 1137-1148. DOI URL
[48]	Savi T, Miotto A, Petruzzellis F, Losso A, Pacilè S, Tromba G, Mayr S, Nardini A (2017b). Drought-induced embolism in stems of sunflower: a comparison of in vivo micro-CT observations and destructive hydraulic measurements. Plant Physiology and Biochemistry, 120, 24-29. DOI URL
[49]	Schenk HJ, Espino S, Mendez AN, McElrone AJ (2013). Limitations in the hydraulic pathway: effects of xylem embolisms on sap velocity and flow. Acta Horticulturae, 323-332.
[50]	Secchi F, Zwieniecki MA (2011). Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant, Cell & Environment, 34, 514-524.
[51]	Simone F, Christoforos P, Jakob Z, Sebastian L (2019). Modelling carbon sources and sinks in terrestrial vegetation. New Phytologist, 221, 652-668. DOI PMID
[52]	Sperry JS (1986). Relationship of xylem embolism to xylem pressure potential, stomatal closure, and shoot morphology in the palm Rhapis excelsa. Plant Physiology, 80, 110-116.
[53]	Sperry JS (2003). Evolution of water transport and xylem structure. International Journal of Plant Sciences, 164, S115-S127.
[54]	Sperry JS, Adler FR, Campbell GS, Comstock JP (1998). Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant, Cell & Environment, 21, 347-359.
[55]	Tomasella M, Casolo V, Aichner N, Petruzzellis F, Savi T, Trifilò P, Nardini A (2019a). Non-structural carbohydrate and hydraulic dynamics during drought and recovery in Fraxinus ornus and Ostrya carpinifolia saplings. Plant Physiology and Biochemistry, 145, 1-9. DOI URL
[56]	Tomasella M, Petrussa E, Petruzzellis F, Nardini A, Casolo V (2019b). The possible role of non-structural carbohydrates in the regulation of tree hydraulics. International Journal of Molecular Sciences, 21, 144. DOI: 10.3390/ijms21010144. DOI
[57]	Trifilò P, Barbera PM, Raimondo F, Nardini A, Gullo MAL (2014a). Coping with drought-induced xylem cavitation: coordination of embolism repair and ionic effects in three Mediterranean evergreens. Tree Physiology, 34, 109-122. DOI URL
[58]	Trifilò P, Kiorapostolou N, Petruzzellis F, Vitti S, Petit G, Lo Gullo MA, Nardini A, Casolo V (2019). Hydraulic recovery from xylem embolism in excised branches of twelve woody species: relationships with parenchyma cells and non-structural carbohydrates. Plant Physiology and Biochemistry, 139, 513-520. DOI PMID
[59]	Trifilò P, Raimondo F, Lo Gullo MA, Barbera PM, Salleo S, Nardini A (2014b). Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values. Plant, Cell & Environment, 37, 2491-2499.
[60]	Tyree MT, Sperry JS (1989). Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology, 40, 19-36. DOI URL
[61]	Wang K, Lin TT, Lü LY, Liu JH, Huang SM (2019). Effects of water stress on non-structural carbohydrates distribution in poplar seedlings. Chinese Journal of Ecology, 38, 3283-3290.
	[王凯, 林婷婷, 吕林有, 刘建华, 黄舒漫 (2019). 水分胁迫对杨树幼苗非结构性碳水化合物分配的影响. 生态学杂志, 38, 3283-3290.]
[62]	Wang L, Dai YX, Guo JP, Gao RM, Wan XC (2016). Interaction of hydraulic failure and carbon starvation on Robinia pseudoacacia seedlings during drought. Scientia Silvae Sinicae, 52(6), 1-9.
	[王林, 代永欣, 郭晋平, 高润梅, 万贤崇 (2016). 刺槐苗木干旱胁迫过程中水力学失败和碳饥饿的交互作用. 林业科学, 52(6), 1-9.]
[63]	Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM (2013). Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant, Cell & Environment, 36, 1938-1949.
[64]	Yan ZJ, Zhao X, Hao L, Wang Y, Bai YR, Zhang GS, Li XL (2017). Drought resistance evaluation of 16 plants based on pressure-volume curve water parameters. Journal of West China Forestry Science, 46(1), 112-116.
	[闫子娟, 赵鑫, 郝蕾, 王颖, 白玉荣, 张国盛, 李小龙 (2017). 利用PV曲线水分参数评价16种植物抗旱性. 西部林业科学, 46(1), 112-116.]
[65]	Yin JJ, Bauerle TL (2017). A global analysis of plant recovery performance from water stress. Oikos, 126, 1377-1388. DOI URL
[66]	Yin XJ, Li YL, Bu ZG, Shang GL (2008). Evaluation of water-saving and drought resistance of landscape tree species in North China. Journal Agricultural University of Hebei, 31(4), 22-29.
	[殷晓洁, 李玉灵, 卜志国, 尚国亮 (2008). 华北地区几种常见园林绿化树种节水性和抗旱性评价. 河北农业大学学报, 31(4), 22-29.]
[67]	Zeppel MJB, Anderegg WRL, Adams HD, Hudson P, Cook A, Rumman R, Eamus D, Tissue DT, Pacala SW (2019). Embolism recovery strategies and nocturnal water loss across species influenced by biogeographic origin. Ecology and Evolution, 9, 5348-5361. DOI URL
[68]	Zhang SX, Shen WJ, Zhang YY, Zhou XX (1997). The vulnerability of xylem embolism in twigs of some drought-resistent tree species. Journal of Northwest Forestry College, 12(2), 1-6.
	[张硕新, 申卫军, 张远迎, 周新霞 (1997). 几个抗旱树种木质部栓塞脆弱性的研究. 西北林学院学报, 12(2), 1-6.]
[69]	Ziv A, Jean-Christophe D, Ram O, A WD, Menachem M (2015). Growth and physiological responses of isohydric and anisohydric poplars to drought. Journal of Experimental Botany, 66, 4373-4381. DOI PMID
[70]	Zwieniecki MA, Holbrook NM (2009). Confronting Maxwell’s demon: biophysics of xylem embolism repair. Trends in Plant Science, 14, 530-534. DOI PMID