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Journal of Arid Land  2022, Vol. 14 Issue (12): 1456-1469    DOI: 10.1007/s40333-022-0039-3
Research article     
Morphological and physiological differences in heteromorphic leaves of male and female Populus euphratica Oliv.
LI Xiu1,2, ZHAI Juntuan1,2, LI Zhijun1,2,*()
1College of Life Sciences and Technology, Tarim University, Alar 843300, China
2Key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin of Xinjiang Production & Construction Corps, Alar 843300, China
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Leaf traits can directly reflect the adaptation strategies of plants to the environment. However, there is limited knowledge on the adaptation strategies of heteromorphic leaves of male and female Populus euphratica Oliv. in response to individual developmental stages (i.e., diameter class) and canopy height changes. In this study, morphological and physiological properties of heteromorphic leaves of male and female P. euphratica were investigated. Results showed that both male and female P. euphratica exhibited increased leaf area (LA), leaf dry weight (LDW), leaf thickness (LT), net photosynthetic rate (Pn), transpiration rate (Tr), stomatal conductance (gs), proline (Pro), and malondialdehyde (MDA) concentration, decreased leaf shape index (LI) and specific leaf area (SLA) with increasing diameter and canopy height. Leaf water potential (LWP) increased with increasing diameter, LWP decreased significantly with increasing canopy height in both sexes, and carbon isotope fraction (δ13C) increased significantly with canopy height in both sexes, all of which showed obvious resistance characteristics. However, males showed greater LA, LT, Pn, Tr, and Pro than females at the same canopy height, and males showed significantly higher LA, SLA, LT, Pn, Tr, gs, and MDA, but lower LWP and δ13C than females at the same canopy height, suggesting that male P. euphratica have stronger photosynthetic and osmoregulatory abilities, and are sensitive to water deficiency. Moreover, difference between male and female P. euphratica is closely related to the increase in individual diameter class and canopy height. In summary, male plants showed higher stress tolerance than female plants, and differences in Pn, gs, Tr, Pro, MDA, δ13C, and LWP between females and males were related to changes in leaf morphology, diameter class, and canopy height. The results of this study provide a theory for the differences in growth adaptation strategies during individual development of P. euphratica.

Key wordsarid area      canopy height      dioecious plants      morphology      physiological characteristics     
Received: 15 August 2022      Published: 31 December 2022
Corresponding Authors: *LI Zhijun (E-mail:
About author: First author contact:The first and second authors contributed equally to this work.
Cite this article:

LI Xiu, ZHAI Juntuan, LI Zhijun. Morphological and physiological differences in heteromorphic leaves of male and female Populus euphratica Oliv.. Journal of Arid Land, 2022, 14(12): 1456-1469.

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Fig. S1 Female and male inflorescences of P. euphratica. (a), male inflorescence; (b), female inflorescence.
Sex Diameter class (cm) Average diameter at breast height (cm) Average tree height (m) Average tree age (a)
Female 8 8.33e 7.53e 8.10e
12 14.30d 9.47d 9.30d
16 17.67c 11.27b 10.37b
20 23.23ab 12.87a 11.17a
Male 8 9.33e 7.97e 8.37e
12 14.37d 10.00cd 9.70cd
16 17.33c 10.93be 10.13bc
20 24.83a 12.70a 11.10a
Table S1 Basic information of male and female P. euphratica
Sex DC LI LA (cm2) SLA (cm2/g) LT (mm) LDW (g)
Female 8 2.45±0.77a 10.52±2.03de 107.31±6.37a 0.35±0.01bc 0.14±0.04c
12 2.63±0.67a 13.99±2.96d 96.79±10.00ab 0.35±0.02bc 0.15±0.03bc
16 2.37±0.89ab 12.22±4.36e 96.91±15.51ab 0.38±0.03b 0.15±0.04bc
20 1.84±0.19abc 22.41±2.32bc 83.83±9.77b 0.38±0.03b 0.25±0.03a
Male 8 1.73±0.68bc 14.58±2.71e 113.31±11.69a 0.38±0.02b 0.14±0.06c
12 2.02±0.34a 15.28±2.75cde 108.09±9.34a 0.39±0.02ab 0.18±0.03b
16 1.85±0.31abc 18.75±5.07cd 106.31±16.13a 0.41±0.04a 0.18±0.05b
20 1.68±0.17c 30.04±2.57a 89.61±8.96b 0.41±0.04a 0.27±0.05a
PS * ** ns ** ns
PDC ns *** * ns **
PS×PDC ns ns ns ns ns
Table 1 Comparison of morphological characteristics of heteromorphic leaves of male and female P. euphratica at different developmental stages
Fig. 1 Comparison of morphological characteristics of heteromorphic leaves between male and female P. euphratica at different canopy heights and diameter classes. Different lowercase letters within the same class are significant differences among different heights at P<0.05 level. 8 F-20 F, females of 8-20 cm diameter classes; 8 M-20 M, males of 8-20 cm diameter classes. S, sex, CH, canopy height; DC, diameter class; S×DC, interaction of sex and diameter class; DC×CH, interaction of diameter class and canopy height; S×CH, interaction of sex and canopy height; S×DC×CH, interaction among sex, diameter class, and canopy height. *, P<0.05 level; **, P<0.01 level; ***, P<0.001 level. The abbreviations are the same as in the following figures.
Fig. 2 Comparison of photosynthetic characteristics of heteromorphic leaves between male and female P. euphratica at different developmental stages. Pn, net photosynthetic rate (a); Tr, transpiration rate (b); gs, stomatal conductance (c); Ci, intercellular CO2 concentration (d); WUE, water use efficiency (e). Different lowercase letters indicate significant differences among different diameter classes at P<0.05 level. The abbreviations are the same as in the following figures.
Fig. 3 Comparison of photosynthetic characteristics of heteromorphic leaves between male and female P. euphratica at different canopy heights and diameter classes. Pn, net photosynthetic rate (a); gs, stomatal conductance (b); Ci, intercellular CO2 concentration (c); Tr, transpiration rate (d); WUE, water use efficiency (e).
Fig. 4 Comparison of water physiological characteristics of heteromorphic leaves between male and female P. euphratica at different canopy heights and diameter classes. (a and b), leaf water potential; (c and d), δ13C.
Fig. 5 Comparison of proline (Pro, a and b) and malondialdehyde (MDA, c and d) concentrations in heteromorphic leaves between male and female P. euphratica at different canopy heights and diameter classes
Sex Index LI LA LDW SLA LT Pn gs Ci Tr WUE Pro MDA δ13C LWP
Female DC -0.23 0.63** 0.71** -0.60** 0.31 0.52* 0.54* -0.20 0.36 0.78** 0.24 0.43 -0.29 -0.86**
Female CH -0.63** 0.75** 0.70** -0.89** 0.87** 0.94** 0.83** -0.94** 0.96** 0.28 0.86** 0.81** 0.68** 0.00
Male DC -0.17 0.65** 0.68** -0.61** -0.01 0.27 0.51* 0.00 0.28 0.24 0.03 0.55* 0.32 0.91**
Male CH -0.72** 0.85** 0.81** -0.86** 0.74** 0.92** 0.83** -0.88** 0.92** 0.34 0.85** 0.86** 0.80** 0.02
Table 2 Correlation among functional trait of heteromorphic leaves between male and female P. euphratica, developmental stage, and canopy height
Index LI LA LDW SLA LT Pn gs Ci Tr WUE Pro MDA δ13C LWP
LI 1.00 -0.72** -0.67** 0.72** -0.87** -0.70** -0.52* 0.62** -0.70** -0.39 -0.53* -0.74** -0.76** 0.10
LA -0.65** 1.00 0.94** -0.97** 0.59** 0.78** 0.73** -0.63** 0.73** 0.52* 0.57* 0.88** 0.87** 0.40
LDW -0.66** 0.96** 1.00 -0.92** 0.50* 0.69** 0.68** -0.58** 0.62** 0.44 0.57* 0.87** 0.82** 0.48*
LSA 0.68** -0.93** -0.87** 1.00 -0.60** -0.76** -0.66** 0.68** -0.73** -0.42 -0.58** -0.85** -0.92** -0.37
LT -0.59** 0.59** 0.60** -0.71** 1.00 0.70** 0.62** -0.67** 0.75** 0.30 0.61** 0.73** 0.61** -0.29
Pn -0.72** 0.78** 0.77** -0.90** 0.90** 1.00 0.85** -0.81** 0.93** 0.51* 0.83** 0.74** 0.72** -0.10
gs -0.42 0.57* 0.58** -0.74** 0.77** 0.89** 1.00 -0.57* 0.85** 0.42 0.67** 0.78** 0.47* 0.17
Ci 0.54* -0.68** -0.59** 0.81** -0.75** -0.82** -0.70** 1.00 -0.82** -0.13 -0.90** -0.61** -0.77** 0.32
Tr -0.73** 0.69** 0.68** -0.84** 0.90** 0.97** 0.85** -0.85** 1.00 0.22 0.82** 0.74** 0.66** -0.11
WUE -0.24 0.62** 0.55* -0.56* 0.09 0.33 0.31 -0.25 0.15 1.00 0.14 0.45 0.38 0.16
Pro -0.55* 0.52* 0.52* -0.67** 0.76** 0.86** 0.89** -0.82** 0.87** 0.13 1.00 0.52* 0.65** -0.30
MDA -0.41 0.81** 0.77** -0.81** 0.58** 0.67** 0.52* -0.78** 0.65** 0.37 0.57* 1.00 0.72** 0.30
δ13C -0.51* 0.36 0.22 -0.49* 0.57* 0.54* 0.36 -0.80** 0.65** 0.00 0.58** 0.41 1.00 0.10
LWP -0.07 0.48* 0.60** -0.30 0.04 0.18 0.17 0.15 -0.02 0.57* -0.10 0.23 -0.59** 1.00
Table 3 Correlation between functional traits of heteromorphic leaves of male and female P. euphratica
Fig. 6 Principal component analysis (PCA) of functional traits of heteromorphic leaves between male and female plants at different developmental stages (a) and canopy heights (b). Open symbols, male plants; filled symbols, female plants. PC, principal component; LI, leaf index; LA, leaf area; LT, leaf thickness; SLA, specific leaf area; LDW, leaf dry weight; Pn, net photosynthetic rate; gs, stomatal conductance; Ci, intercellular CO2 concentration; Tr, transpiration rate; WUE, water use efficiency; Pro, proline; MDA, malondialdehyde content; LWP, leaf water potential.
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