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Tree Physiology 40, 1178–1191
doi:10.1093/treephys/tpaa069
Research paper
Eect of summer warming on growth, photosynthesis and water
status in female and male Populus cathayana: implications for
sex-specic drought and heat tolerances
Junyan Liu1,2,†, Rong Zhang1,3,†, Xiao Xu1, Joshua C. Fowler4, Tom E. X. Miller4and
Tingfa Dong1,2,5
1Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong, 637009, Sichuan, China; 2Key
Laboratory of Environmental Science and Biodiversity Conservation (Sichuan Province), and Institute of Plant Adaptation and Utilization in Southwest Mountains, China West
Normal University, Nanchong, Sichuan 637009, China; 3College of Life Sciences, Sichuan University, Chengdu 610064, China; 4Department of BioSciences, Program in
Ecology and Evolutionary Biology, Rice University, Houston, TX 77005, USA; 5Corresponding author (dongfar@163.com; dongtf@aliyun.com)
Received January 31, 2020; accepted May 27, 2020; handling Editor Roberto Tognetti
Eects of climate warming on tree growth and physiology may be driven by direct thermal eects and/or by changes in
soil moisture. Dioecious tree species usually show sexual spatial segregation along abiotic gradients; however, few studies
have assessed the sex-specic responses to warming in dioecious trees. We investigated the sex-specic responses in
growth, photosynthesis, nonstructural carbohydrate (NSC), water-use eciency and whole-plant hydraulic conductance
(KP) of the dioecious tree species Populus cathayana Rehd. under +4◦C elevated temperature with and without
supplemental water. For both sexes, high-temperature treatments signicantly decreased growth (height and biomass),
photosynthetic rate (A), the ratio of Ato dark respiration rate, stomatal conductance (gs), transpiration rate, NSC,
leaf water potential and KP, but increased water-use eciency (estimated from carbon isotope composition). Under
warming with supplemental water, most traits of females did not change relative to ambient conditions, but traits of
males decreased, resulting in greater sexual dierences. Females showed a lower KP,andtheirgsand Aresponded
more steeply with water-related traits than males. These results show that the eect of summer warming on growth and
photosynthesis was driven mainly by soil moisture in female P. cathayana, while male performance was mainly related to
temperature. Females may experience less thermal stress than males due to exible water balance strategy via stomata
regulation and water use.
Keywords: dioecy, poplar, sexual dimorphism, summer heat, water use strategy.
Introduction
For many parts of the planet, climate change projections predict
not only increases in surface temperature but also changes
in precipitation and evapotranspiration, which aect the soil
moisture available to plants (Dai 2013). Evapotranspiration may
increase more than precipitation in temperate and boreal forest
ecosystems under climate warming, while the reverse may occur
in tropical and subtropical forest ecosystems (Sherwood and
Fu 2014,Perez and Feeley 2018). Temperature and water
are key drivers of plant growth, survival and distribution across
terrestrial ecosystems. Extreme high temperature and/or heat-
induced soil moisture changes may threaten tree growth and
survivorship (Allen et al. 2010,Park Williams et al. 2013,
Grossiord et al. 2017). It is important for studies on the eect of
climate warming to consider the eect of soil moisture changes
induced by warming, which is crucial for predicting impacts on
forest ecosystems and for modeling carbon and water cycles
under novel climatic conditions (Allen et al. 2010,Perez and
Feeley 2018,Reich et al. 2018).
†These authors contributed equally to this work.
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Males suer more negative eects of summer heat stress than females 1179
Under high temperature, plant physiological responses gener-
ally minimize heat absorption and maximize dissipation. Higher
temperatures inhibit photosynthesis through Rubisco deactiva-
tion, photo-oxidation and/or membrane denaturation, while tran-
spiration might be improved as warming usually increases the
vapor pressure decit (VPD) between leaf and air (Rennenberg
et al. 2006,Garcia-Forner et al. 2016,Kumarathunge et al.
2019). Since photosynthetic and transpiration processes are
shaped by stoma, stomatal regulation may be more important
under warming climates (Garcia-Forner et al. 2016). Higher
stomatal conductance (gs) leads to higher rates of photosynthe-
sis and transpiration under adequate water resources, but may
increase water loss when water is scarce. There are species-
specic adaptive responses in gsto water loss to VPD (Oren
et al. 1999). To maintain function, some species will decrease
gswhile increasing VPD to limit transpiration and water use;
however, decreasing transpiration and stomatal closure to avoid
leaf desiccation can lead to increases in heat risk to leaves
when warming beyond the thermal optimum for photosynthesis
(Marchin et al. 2016,Vico et al. 2019). Other species will
maintain gsthrough increasing the leaf water supply to deal
with elevated VPD (Wu et al. 2018). Therefore, the mechanism
of water balance may mediate the eects of high temperature
when soil moisture is low (Rennenberg et al. 2006).
At a given soil moisture, leaf water status is determined
by plant hydraulic characteristics and transpiration (Sperry
et al. 2002). Some studies in woody plant species found that
hydraulic conductance (KP)candetermineleafwaterstatus,
inuencing gas exchange (Tyree 2003,Brodribb et al. 2007,
McCulloh et al. 2016). Hydraulic conductance can also control
plant responses to stresses associated with water (Mitchell
et al. 2013,Nardini et al. 2013) and temperature (Sellin and
Kupper 2007,McCulloh et al. 2016). Recent studies found
that elevated temperature can exacerbate the risks of hydraulic
failure and carbon starvation when soil moisture is limited (Yan
et al. 2020). However, studies on how plants adjust water
physiology for maximizing carbon assimilation under warming
remain limited (Vico et al. 2019). More intra- and inter-species
studies of whole-plant vascular systems under warming condi-
tions are needed to predict the responses of whole plants to
changes in atmospheric (e.g., temperature) and soil conditions
(Way and Oren 2010).
Despite making up only 5–6% of total plant species (Renner
2014), dioecious plant species (those with separate female and
male individuals) play important pioneer roles in the structure
and function of forest ecosystems (such as Salix,Ilex and Pop-
ulus species). Previous studies have found tree species show
sexual dimorphism in plant morphology, reproductive allocation,
resource eciency and even sexual spatial segregation along
environmental gradients (Li et al. 2007,Hultine et al. 2013,
Lei et al. 2017,Melnikova et al. 2017,Zhang et al. 2020).
How these sex-specic responses could change under climate
change is still an open question (Xu et al. 2008b,Tognetti 2012,
Hultine et al. 2013,Munné-Bosch 2015). To compensate for
higher reproductive costs, females might be more ecient
than males in photosynthesis and water use (Tognetti 2012,
Hultine et al. 2016). However, studies that contrast the hydraulic
response of females and males are rare. One study of the
dioecious tree species Juniperus thurifera L. (evergreen conifer)
showed that females have a greater hydraulic eciency than
males (Olano et al. 2017). Compared with evergreen trees,
deciduous species usually have a higher growth rate, resulting
in more susceptibility to warming-induced responses in growth
(Way and Oren 2010,Dusenge et al. 2020). To the best of our
knowledge, no previous studies have investigated the impact
of warming on hydraulic conductance of dioecious deciduous
trees.
Populus cathayana Rehd. is a fast-growing, dioecious tree that
is widely distributed in the northern hemisphere. During recent
decades, this species’ geographic range has experienced high
summer temperatures, which results in declining growth and
increasing mortality (Zhou and Ren 2011,Liu et al. 2013).
Previous studies have found that P. cathayana is responsive
to environmental stress and that females usually suer from
more negative eects in growth and physiology than do males
with increasing drought stress (Xu et al. 2008a,2008b,Zhang
et al. 2010,2012,Li et al. 2015). Moreover, dierences in P.
cathayana photosynthesis between sexes under warming may
be related to soil moisture and/or warming strength (Xu et al.
2008b,Zhao et al. 2012) and warming season (Yu et al .
2018). However, it is still unclear whether the eects on growth,
photosynthesis and hydraulic characteristics of P. cathayana
result from thermal eects or from changes in soil moisture
induced by increased temperature. Here, we hypothesized that
there are sex-specic responses to warming in P. cathayana
growth, photosynthesis and hydraulic characteristics. We investi-
gated the sex-related responses in growth, photosynthesis and
hydraulic conductance to summer high temperature with and
without supplemental water, allowing us to distinguish between
the direct eects of temperature alone and the joint eects of
elevated temperature and reduced soil moisture. We ask the
following questions. (i) Are there sex dierences in plant growth,
carbon assimilation and hydraulic conductance under elevated
temperature (no supplemental water)? (ii) Does elevated soil
moisture (supplemental water) modify the eect of elevated
temperature on sex-specic growth and physiology? (iii) Do
female and male plants have dierent sensitivities in balances
of carbon and water to warming? Our results have signicance
for predicting physiological responses of dioecious species to
global climate change.
Materials and methods
Study species and experimental design
Healthy shoots of female and male P. cathayana were collected
from 30 dierent trees (∼15 years old) from ve populations
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1180 Liu et al.
in the Qinghai Province, China (36◦31N, 102◦28E) at the
beginning of mid-March. Populations were at least 400 m apart,
and we took six cuttings from each population from at least three
individuals (some cuttings were genetic clones). The cuttings
(10 cm in length) were planted in a glasshouse at China West
Normal University (30◦48N, 106◦03E) that blocked ambient
rainfall but otherwise maintained ambient light and temperature
(light transition rate was over 90% and temperature inside
and outside the glasshouse diered by <0.3 ◦C). Summer
climate in this site is typically hot and wet; the average rainfall
total and temperature from June to September are 141 mm
and 29.9 ◦C, respectively. Over recent decades, the frequency
of high temperature (∼40 ◦C) and low precipitation during
the mid-summer season has increased (from Meteorological
Bureau of Nanchong (http://sc.cma.gov.cn/ds/nc/)). After 8
weeks of clonal propagation, 180 cuttings (90 males and
90 females) of similar size (15 cm in length and 0.5 cm
in diameter) were chosen randomly from all cuttings across
populations and transplanted to plastic pots (15 cm ×20 cm)
lled with an 8-kg homogenized soil (1 cutting per pot). The
surface soil (0–20 cm) was collected from farmland near the
experimental site. The soil was sifted with a 0.35-mm-diameter
sieve. The soil was a Cambisol (pH 7.9), which contained
12.22 g kg−1organic carbon, 0.88 g kg−1total nitrogen,
0.92 g kg−1total phosphorus and 74.8 mg kg−1available
potassium.
Experimental treatments were applied to potted individuals in
a completely randomized design. There were three treatments
applied to each sex: (i) CK (control, where temperature and
soil moisture matched ambient conditions (average 31% soil
moisture by irrigation with 600 ml pot−1day−1)), (ii) WA (+4◦C
warming with the same amount of irrigated water as CK (600 ml
pot−1day−1; no supplemental water)) and (iii) WM (+4◦C with
supplemental water to match the average 31% soil moisture
of the CK treatment). This design allows us to separate the
eects of warming that are due to increased temperature versus
decreased soil moisture. A ∼4.0 ◦C air temperature increase
(widely used to study the eect of warming in plants (e.g.,
Duan et al. 2018,Hoeppner and Dukes 2012,Dusenge et al.
2020)) was accomplished with infrared lamp heaters placed
∼1 m above the plant canopy. Warming and control plants were
separated by 10 m. The positions of pots were rotated weekly
to ensure equal light availability and minimize dierences under
heaters. Elevated air temperature was maintained throughout
the growing season (from 1 May to 1 September). The air
temperature of warming plants or ambient plants was mon-
itored by two TP-2000-W1 Temperature Data loggers (Anfu
Electronic Technique Co., Ltd Beijing, China), which were placed
0.2 m above the plant canopy. All plants were watered each
day of the experiment, and the soil moisture content was
measured after watering using a time-domain reectometer
(Dong et al. 2016).
Measurement of morphology and biomass
At the end of experiment, four cuttings from each treatment
were randomly selected to measure height, total leaf area (TA)
and biomass accumulation. The trees were harvested and their
biomass was separated into leaves, stem, ne roots (<2mm
in diameter) and coarse roots (>2 mm in diameter). The area
of total leaves was measured using a leaf area meter (LI-COR
3000C, LI-COR Inc., Lincoln, NE, USA). Dry mass of all biomass
was measured after oven-drying at 70 ◦C to a constant mass.
Plant total dry mass (TM) was calculated as the sum of dry
masses of all tissue. The specic leaf area (SLA) was estimated
as the ratio of leaf area to leaf dry mass.
Measurement of photosynthesis
One individual with healthy, fully expanded, exterior leaves in
each treatment was chosen to measure gas exchange and
chlorophyll uorescence characteristics. Leaf gas exchange
rates were measured using a LI-6400 portable photosynthesis
system (LI-COR Inc.) with a standard LED leaf chamber (2 ×
3cm
2). The measurement conditions were leaf temperature
of 28 ◦C; relative air humidity of 60%; CO2concentration of
400 ±5 μmol mol−1and photosynthetic photon ux density
(PPFD) of 1500 μmol m−2s−1. Once steady-state gas exchange
rates were observed at these conditions, light-saturated photo-
synthetic rate (A), stomatal conductance (gs), intercellular CO2
concentration (Ci) and transpiration (E) were recorded. The
leaf dark respiration rate (Rd) was measured under the same
conditions except for the absence of light after the leaves were
darkened for at least 5 min before recording the rates (Dong
et al. 2019).
The response of Ato changing CO2was measured at 400
μmol mol−1, which was decreased to 300, 200, 150, 100
and 50 μmol mol−1, then returned to 400 and subsequently
increased to 500, 600, 800, 1000 and 1200 μmol mol−1
under saturating irradiance (1500 μmol m−2s−1PPFD). The
maximum rate of Rubisco carboxylation (Vcmax ) and maxi-
mum electron transport rate (Jmax) were estimated according
to Long and Bernacchi (2003).
Chlorophyll uorescence measurements were performed on
the same leaves used for gas exchange observation with a
Junior-PAM chlorophyll uorometer (Walz, Eeltrich, Germany).
A measurement leaf was dark-adapted for at least 30 min
prior to the measurements by an aluminum foil cover, and the
minimum dark-adapted uorescence yield (F0) was measured.
Thereafter, a saturating white light pulse of 8000 μmol m−2
s−1was applied for 0.8 s to measure the maximum dark-
adapted uorescence yield (Fm). Then, the leaf was illuminated
with an actinic light at an intensity of 600 μmol m−2s−1
corresponding to the ambient light intensity at the time of
measurements, and a saturating white light pulse was applied
again to measure the light-adapted maximum uorescence
yield (Fm). Then, the actinic light was further switched o,
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Males suer more negative eects of summer heat stress than females 1181
Figure 1. Air temperature during warming treatment (a) and dierences in vapor pressure decit (b) and average soil moisture content (c) in female
(black bar) and male (white bar) P. c a t h a y a n a cuttings under warming with water supply. CK, ambient temperature and irrigated to match the
ambient soil moisture; WA, +4◦C keeping the same amount of irrigated water as CK (no supplemental water); WM, +4◦C and keeping the same
soil moisture content as CK (with supplemental water). The dierent letters above the bars indicate the signicant dierence among treatments at
P<0.05 according to Tukey’s HSD test.
the leaf was illuminated for 3 s with far-red light, and the
minimal uorescence yield (F0) was determined. From these
measurements, the maximum photochemical quantum yield of
photosystem II (PSII) (Fv/Fm), eective photochemical quantum
yield of PSII (Φ), coecient of photochemical uorescence (qP)
and non-photochemical uorescence quenching (NPQ) were
calculated. These were calculated as follows: Fv/Fm=(Fm-
F0)/Fm;Φ=(Fm-F)/Fm;qP=(Fm-F)/(Fm-F0);
NPQ = Fm/Fm-1.
Measurement of soil-to-leaf hydraulic conductance
Whole-plant hydraulic conductance (KP) corresponds to the
following equation (Tyree 2003): KP=EL/(soil -leaf),
where ELis the whole-plant transpiration (mmol m−2s−1),
soil (MPa) is bulk soil water potential and leaf (MPa) is
leaf water potential. soil are leaf estimated from predawn
(06:00–7:00 h) and midday (13:00–14:00 h) leaf water
potential, respectively (Mitchell et al. 2013). The leaf water
potential was determined with a thermocouple psychrometer
(Wescor PSYPRO, Logan, UT, USA). ELwascalculatedasthe
weight lost over the measurement interval at midday according
to Mitchell et al. (2013).
Carbon isotope composition and carbohydrate analyses
Dried samples of leaf, stem, coarse root and ne root were then
ground in a ball mill. We determined the foliar carbon isotope
composition (δ13C) and nonstructural carbohydrate (NSC) con-
tent of leaves, stems, coarse roots and ne roots according to
Dong et al. (2019).
Statistical analysis
We used a two-way analysis of variance (ANOVA) to test
the eects of sex, warming treatments and their interaction
on morphological, biomass and physiological parameters. Trait
dierences among the treatments were tested by Tukey’s honest
signicant dierence (HSD) tests. Simple linear regressions
were used to assess the relationships between A,A/Rdor gs
and water-related (leaf water potential, leaf water content, leaf
water-use eciency and whole-plant hydraulic conductance)
or leaf temperature variables. The eects were considered
signicant if P<0.05. Principal component analysis (PCA)
of ecophysiological traits was also undertaken to examine the
eects of warming in each sex. All data were analyzed with SPSS
(Chicago, IL, USA) version 16.0.
Results
From May to September, the average ambient air temperature
was 31.10/20.31 ◦C (day/night; varied from 9.2 to 41.6 ◦C
across the growing season), and the warming treatment had
an average 4.04 ◦C increase (Figure 1a). The mean vapor
pressure decits (VPD; Figure 1b) under ambient and warming
treatments were 1.55 ±0.04 kPa and 2.00 ±0.03 kPa,
respectively. Warming signicantly increased VPD, but VPD was
similar between WA (warming with same irrigation amount as
the control) and WM (warming with same soil moisture as the
control) treatments. During the growing season, the average soil
moisture content under CK and WM was, respectively, 0.312 ±
0.01 (∼81% soil eld capacity) cm3cm−3and 0.219 ±0.02
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1182 Liu et al.
Table 1. Eect of warming on morphology and biomass accumulation and allocation in female and male P. c a t h a y a n a cuttings under dierent water
supply.
Sex Treatment Height (cm) TA (cm2plant−1)SLA(cm
2mg−1)TM(mgplant
−1)R/S FR/TR
Female CK 55.55 ±5.42b 689.41 ±40.65a 135.1 ±0.4bc 11.86 ±0.75a 0.43 ±0.02ab 0.31 ±0.01b
WA 43 ±4.21c 376.03 ±41c 122.17 ±2.47cd 7.21 ±0.57c 0.53 ±0.04a 0.58 ±0.03a
WM 58.18 ±2.93b 681.58 ±24.43a 143.9 ±2.05b 11.16 ±0.24ab 0.34 ±0.02bc 0.4 ±0.02b
Male CK 81.58 ±3.73a 530.16 ±16.33b 151.22 ±4.94b 9.72 ±0.31b 0.3 ±0.02c 0.39 ±0.03b
WA 59.13 ±3.23b 227.59 ±28.9d 114.09 ±5.81d 6.38 ±0.31c 0.41 ±0.02b 0.51 ±0.01a
WM 92.58 ±1.57a 404.92 ±24.72c 172.59 ±6.55a 7.66 ±0.3c 0.26 ±0.02c 0.37 ±0.03b
S 71.048∗∗∗ 60.506∗∗∗ 12.099∗∗ 34.259∗∗∗ 33.699∗∗∗ 0.256NS
T 22.885∗∗∗ 55.843∗∗∗ 44.182∗∗∗ 40.313∗∗∗ 26.479∗∗∗ 37.299∗∗∗
S×T 3.044NS 2.688NS 9.392∗∗ 4.371∗0.798NS 4.807∗
TA, total leaf area; SLA, specic leaf area; TM, total dry mass; R/S, root-to-shoot ratio; FR/TR, the ratio of ne root mass to total root mass. S, sex
eect; T, treatment eect; S ×T, s e x ×treatment eect. The value is mean ±SE (n= 4). Dierent lowercases in the same column indicate a
signicant dierence at 0.05 level according to Turkey’s HSD test. Fvalue and Pvalue are shown. NS, P>0.05; ∗P<0.05; ∗∗P<0.01; ∗∗∗P≤
0.001. Treatments are as dened in Figure 1.
(∼55% soil eld capacity) cm3cm−3, and there was a signicant
29.86% decrease under the warming without water supplement
treatment (Figure 1c).
Sex-specic eects of warming on morphology, biomass
accumulation and allocation under water supply
After the 4-month warming treatment, we found that plant
height, total leaf area (TA), specic leaf area (SLA), total dry
mass (TM; including leaf, stem, coarse root and ne root dry
mass; Table S 1 available as Supplementary Data at Tree Phys-
iology Online) and root-to-shoot ratio (R/S) were signicantly
aected by sex and warming treatments (Table 1). Compared
with the control (CK), warming without water supplement (WA)
decreased leaf area and dry mass in both sexes, but increased
the ne root dry mass to total root dry mass ratio (FR/TR).
When water was supplied to match the soil moisture of CK (WM
treatment), female height, TA, SLA, TM, R/S and FR/TR were
similar to the CK, while male TA and TM were lower than the
CK. Female height was always lower than that of males in each
treatment, but TA and leaf dry mass of females were always
higher. Under CK and WM treatments, female TM and coarse
root dry mass were higher than males. The highest ne root
mass, R/S and FR/TR but the lowest TM (including leaf mass,
stem mass, coarse root mass) and TA among all treatments
were found in WA treatment (Ta bles 1 and S1 available as
Supplementary Data at Tree Physiology Online).
Sex-specic eects of warming on gas exchange and
chlorophyll uorescence with water supply
Warming treatment signicantly inuenced gas exchange and
chlorophyll uorescence (Figure 2 and Table 2). The light-
saturated photosynthetic rate (A), stomatal conductance (gs),
leaf dark respiration rate (Rd), transpiration (E) and eective
photochemical quantum yield of PSII (Φ) were signicantly
inuenced by sex and the interaction of sex and warming.
Compared with CK, there was signicantly lower A,gs,E,
maximum photochemical quantum yield of PSII (Fv/Fm), Φ
and coecient of photochemical uorescence (qP) under WA
treatment in both sexes, while most of these traits were similar
across sexes; we observed even higher gs,Rd,E,Jmax and
non-photochemical uorescence quenching (NPQ) in females
under WM treatment. Warming treatment did not inuence the
maximum rate of Rubisco carboxylation (Vcmax ), but lowered
the ratio of intercellular CO2concentration to ambient CO2con-
centration (Ci/Ca) of females under WA treatment and raised the
Ci/Caratio of male under WM treatment compared with controls.
In addition, warming always decreased male Fv/Fmand NPQ but
increased Rd. Compared with females, male gsand NPQ were
lower in each treatment, Aand Ein males were higher under
WA treatment, and E,Jmax,Fv/Fmand Φof males were lower
under WM treatment.
In addition, warming with and without supplemental
water always decreased the ratio of net photosynthetic rate to
dark respiration rate (A/Rd)ineachsex(Figure 3). The A/Rd
of females under WM treatment was higher than under WA
treatment, but A/Rdof males was similar between WM and WA
treatments. Compared with females, male A/Rdwas higher than
females under control, but it was lower than females under WM
treatment.
Sex-specic eects of warming on nonstructural
carbohydrates with water supply
Whole-plant soluble sugars (SSP), starch (STP) and total non-
structural carbohydrate (NSCP) (including the stem and coarse
root) were signicantly inuenced by sex (except NSCP)and
warming treatments (except NSC in coarse root) (Table s 3 and
S2 available as Supplementary Data at Tree Physiology Online).
The highest values of SSP,NSC
P, leaf SS and NSC were found
in females under WA treatment, while the lowest values of SSP
and NSCPwere found in males under WM treatment. In females,
warming with water supplement decreased the contents of SSP
and NSCP.FemaleST
Pwas similar among the three treatments,
whereas male STPunder WA or WM treatment was lower than its
control. Warming did not inuence the leaf SS and NSC and ne
root SS contents, but decreased the coarse root SS, ST and NSC
contents in both sexes (Tabl e S2 available as Supplementary
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Males suer more negative eects of summer heat stress than females 1183
Figure 2. Eect of warming on light-saturated photosynthetic rate (A; a), stomatal conductance (gs; b), the leaf dark respiration rate (Rd;c)and
transpiration (E; d) in female (black bar) and male (white bar) P. c a t h a y a n a cuttings under dierent water supply levels. S, sex eect; T, treatment
eect; S ×T, s e x ×treatment eect. The dierent letters above the bars indicate the signicant dierence among treatments at P<0.05 according
to Tukey’s HSD test. Fvalue and Pvalue are shown. ∗P<0.05; ∗∗P<0.01; ∗∗∗P≤0.001. Treatments are as dened in Figure 1.
Table 2. Eect of warming on traits of photosynthetic-related biochemistry and chlorophyll uorescence in female and male P. c a t h a y a n a cuttings
under dierent water supply.
Sex Treatment Ci/CaVcmax (μmol m−2s−1)Jmax (μmol m−2s−1)Fv/FmΦqP NPQ
Female CK 0.68 ±0.01ab 75.78 ±1.38 96.82 ±1.61c 0.78 ±0.02ab 0.48 ±0.02a 0.68 ±0.02a 0.34 ±0.02c
WA 0.57 ±0.01d 72.07 ±1.87 91.92 ±2.36c 0.61 ±0.02c 0.33 ±0.01bc 0.59 ±0.01b 0.49 ±0.01a
WM 0.63 ±0.02bc 76.12 ±4.51 119.51 ±4a 0.75 ±0.01b 0.50 ±0.01a 0.72 ±0.02a 0.41 ±0.02b
Male CK 0.63 ±0.01c 80.26 ±1.12 108.56 ±3.24ab 0.84 ±0.01a 0.50 ±0.01a 0.73 ±0.02a 0.26 ±0.01d
WA 0.61 ±0.02cd 72.61 ±0.99 88.41 ±1.06c 0.66 ±0.01c 0.33 ±0.01c 0.56 ±0.01b 0.38 ±0.02c
WM 0.7 ±0.01a 75.06 ±0.91 98.57 ±2.22bc 0.65 ±0.02c 0.39 ±0.01b 0.66 ±0.01ab 0.33 ±0.01c
S 2.474NS 0.544NS 3.974NS 0.068NS 6.260∗0.418NS 70.801∗∗∗
T 20.296∗∗∗ 3.38NS 27.223∗∗∗ 54.777∗∗∗ 68.138∗∗∗ 29.777∗∗∗ 52.782∗∗∗
S×T 11.922∗∗ 0.845NS 19.736∗∗∗ 14.537∗∗∗ 11.026∗∗∗ 5.161∗0.891NS
Ci/Ca, the ratio of intercellular CO2concentration to ambient CO2concentration; Vcmax, the maximum rate of Rubisco carboxylation; Jmax, maximum
electron transport rates; Fv/Fm, maximum photochemical quantum yield of PSII; Φ, eective photochemical quantum yield of PSII; qP, coecient of
photochemical uorescence; NPQ, non-photochemical uorescence quenching. S, sex eect; T, treatment eect; S ×T, s e x ×treatment eect. The
value is mean ±SE (n= 4). Dierent lowercases in the same column indicate a signicant dierence at 0.05 level according to Turkey’s HSD test.
Fvalue and Pvalue are shown. NS, P>0.05; ∗P<0.05; ∗∗P<0.01; ∗∗∗P≤0.001. Treatments are as dened in Figure 1.
Data at Tree Physiology Online). Although male STPand NSCP
under control conditions were similar to females, these traits
were lower than females in the warming treatment.
Sex-specic eects of warming on water use and leaf
temperature with water supply
Predawn leaf water potential (Ψ) and whole-plant hydraulic
conductance (KP) under WA treatment decreased in both
sexes, relative to the ambient control (CK), while under
WM treatment they increased in females and were similar in
males (Figure 4a and d). The leaf carbon isotope composition
increased under WA treatment in both sexes, while this trait
under WM treatment was lower in females and higher in
males than the control (Figure 4c). Male KPwas higher
than females in the CK and WA treatment, but was similar
between females and males under the WM treatment. The leaf
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1184 Liu et al.
Figure 3. Eect of warming on the ratio of leaf photosynthetic rate
to dark respiration rate (A/Rd) in female (black bar) and male (white
bar) P. c a t h a y a n a cuttings under dierent water supply. S, sex eect;
T, treatment eect; S ×T, s e x ×treatment eect. The dierent letters
above the bars indicate the signicant dierence among treatments at
P<0.05 according to Tukey’s HSD test. Fvalue and Pvalue are shown.
NS, P>0.05; ∗∗∗P≤0.001. Treatments are as dened in Figure 1.
water content was similar between sexes in each treatment
(Figure 4b).
Leaf temperature was signicantly inuenced by sex and
warming treatments (Figure 5). Warming treatment always
increased leaf temperature. Female leaf temperature under
warming decreased with water supplement, but water supple-
ment had no eect on leaf temperature in males. Female leaf
temperature was lower than that of males in each treatment.
Sex-specic relationships between A or gsand water-related
traits among treatments
In both sexes, we observed positive correlations between Aand
gs;Ψ, leaf water content and gs;andΨand leaf water content
(except in males) and negative correlations between Aor gsand
leaf carbon isotope composition (δ13C) across all treatments
(Figure 6). Female Awas higher than males at a given gs
(Figure 6a)orδ13C(Figure 6d). We saw steeper relationships
between Aor gsand water-related traits (Ψ, leaf water content
or δ13C) in females than that in males, especially the relationship
of gswith Ψ, leaf water content or δ13 C(Figure 6b–g).
In addition, Aand gswere positively related with whole-plant
hydraulic conductance (KP) in both sexes (Figure 7a and b).
Both of their relationships were steeper in females than in males.
Sex-specic relationships between A, A/Rdor gsand leaf
temperature among treatments
There were negative correlations between A,A/Rdor gsand
leaf temperature in both sexes (Figure 8a–c). We observed
a steeper negative relationship between Aor A/Rdand leaf
temperature in males than in females, especially on A/Rdand
leaf temperature. Males had higher Athan females at a given leaf
temperature (Figure 8a). Female gsshowed a steeper negative
relationship with leaf temperature than in males (Figure 8c).
Relationships among all traits in each sex under dierent
treatments
The PCA showed clear delineation based on trait combina-
tions in the dierent treatments (Figure 9a). Warming with
water supply treatments was well separated from each other in
females (Figure 9b)andmales(Figure 9c). The two-component
PCA models explained 73.79%, 82.97% and 86.68% of the
observed total variance in total individuals, female plants and
male plants, respectively. Principal component 1 (PC1) was
strongly inuenced by leaf area, total dry mass, photosynthetic
Table 3. Eect of warming on whole-plant soluble sugar (SSP), starch (SSP) and total nonstructural carbohydrate (NSCP)infemaleandmaleP.
cathayana cuttings under dierent water supply.
Sex Treatment SSP(mg g−1)ST
P(mg g−1)NSC
P(mg g−1)
Female CK 62.52 ±1.22ab 60.72 ±1.64a 123.24 ±0.83ab
WA 67.59 ±2.3a 56.97 ±2.08a 124.56 ±2.45a
WM 54.74 ±1.8cd 55.63 ±1.23a 110.37 ±1.6bcd
Male CK 57.34 ±1.25bc 59.83 ±0.75a 117.17 ±1.03bc
WA 60.12 ±1.56bc 44.77 ±0.81b 104.89 ±1.42de
WM 49.24 ±1.32d 49.62 ±0.72b 98.86 ±1.79e
S 20.86∗∗∗ 27.775∗∗∗ 0.291NS
T 35.607∗∗∗ 29.303∗∗∗ 9.392∗∗∗
S×T 89.138∗∗∗ 48.237∗∗∗ 9.026∗∗∗
S, sex eect; T, treatment eect; S ×T, s e x ×treatment eect. The value is mean ±SE (n= 4). Dierent lowercases in the same column indicate
a signicant dierence at 0.05 level according to Turkey’s HSD test. Fvalue and Pvalue are shown. NS, P>0.05; ∗∗∗P≤0.001. Treatments are
as dened in Figure 1.
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Males suer more negative eects of summer heat stress than females 1185
Figure 4. Eect of warming on predawn leaf water potential (Ψ; a), leaf water content (b), leaf carbon isotope composition (δ13C; c) and whole-plant
hydraulic conductance (KP; d) of female (black bar) and male (white bar) P. c a t h a y a n a cuttings under dierent water supply. S, sex eect; T, treatment
eect; S ×T, s e x ×treatment eect. The dierent letters above the bars indicate the signicant dierence among treatments at P<0.05 according
to Tukey’s HSD test. Fvalue and Pvalue are shown. NS, P>0.05; ∗∗∗P≤0.001. Treatments are as dened in Figure 1.
rate, transpiration rate, water potential, KP,gs,F
v/Fm,δ13C, NPQ
and leaf temperature. PC2 was strongly inuenced by leaf dark
respiration rate and whole-plant soluble sugar contents.
Discussion
In this study, we demonstrated the sex dierences in growth,
photosynthesis and water use of a dioecious tree species, P.
cathayana, under an elevated temperature, and that the eect of
warming was related to soil moisture. Warming without supple-
mental water treatment decreased plant growth, photosynthesis
and water status in both sexes. However, adding supplemental
water alleviated the eects of warming on females but not
males. In addition, warming always decreased the ratio of pho-
tosynthetic rate to dark respiration rate (A/Rd) and plant NSC
content, especially in coarse roots. Across all treatments, female
stomatal conductance (gs) and light-saturated photosynthetic
rate (A) showed steeper relationships with water-related traits
than males, while A/Rdshowed steeper relationships with leaf
temperature in males than in females. These results suggest
that the eect of high temperature in P. cathayana was mainly
determined by soil moisture for females, while males were
more sensitive in carbon assimilation and water balance to
the direct eects of temperature per se. Sex dierences in
adaptive responses to heat may be related to diering water
use strategies and thermal sensitivities.
Male growth and photosynthesis suered more than females
under heat
In this study, we found that most traits involved in growth, pho-
tosynthesis and water use of P. cathayana were similar between
the sexes under ambient conditions (CK), but most of these
traits were lower in males than in females under +4◦Cwarming
with similar soil moisture (WM). Previous studies in this species
usually showed that plant responses to warming can promote
growth and biochemical processes (Xu et al. 2008b,Zhao et al.
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1186 Liu et al.
Figure 5. Eect of warming on leaf temperature of female (black bar)
and male (white bar) P. c a t h a y a n a cuttings under dierent water supply.
S, sex eect; T, treatment eect; S ×T, s e x ×treatment eect. The
dierent letters above the bars indicate the signicant dierence among
treatments at P<0.05 according to Tukey’s HSD test. Fvalue and P
value are shown. NS, P>0.05; ∗∗∗P≤0.001. Treatments are as dened
in Figure 1.
2012,Yu et al. 2018). The apparent discrepancy of current and
previous results reects the dierences in absolute temperature
in the warming treatments. Plant responses to warming in
growth and biochemical processes are often parabolic, where
warming will promote photosynthesis when the temperature is
below the optimum and impede it above the optimum (Saxe
et al. 2001,Lin et al. 2012,Reich et al. 2018). Also, rising
temperature often results in increased rates of respiratory and
photorespiratory CO2release exceeding carboxylation rates,
which impedes gains in biomass (Ameye et al. 2012,Zhu et al.
2018).
Our warming treatment led to leaf temperature increases
in both sexes (Figure 5). The average temperatures of air
and leaves (33.2 and 35.6 ◦C, respectively) were beyond
optimal photosynthetic temperatures for P. cathayana (∼28 ◦C;
Figure S1 available as Supplementary Data at Tree Physiology
Online), and there was a negative relationship between Aor gs
and leaf temperature, such that Awas reduced in response to
heat stress (Vico et al. 2019,Winkler et al. 2019). Moreover,
warming increased the leaf dark respiration rate (Figure 2c)
and decreased the ratio of leaf photosynthetic rate to dark
respiration rate (Figure 3), and this led to decreases in biomass
accumulation. In addition, our present results show that the
optimum temperature for photosynthesis in males was lower
than in females (27.1 versus 28.9 ◦C; Figure S1 available as
Supplementary Data at Tree Physiology Online), and we found
higher leaf temperature (Figure 8a) for males than for females at
agivenA, which explains why males suered more heat stress
than females. Thus, the sex-specic responses in growth and
photosynthesis to heat stress were mainly caused by a decrease
in males rather than in females under heat. These results are
Figure 6. Relationship between light-saturated photosynthetic rate (A)
and stomatal conductance (gs; a), predawn leaf water potential (Ψ;b),
leaf water content (c) and leaf carbon isotope composition (δ13C; d);
and between stomatal conductance (gs) and predawn leaf water poten-
tial (Ψ; e), leaf water content (f) and leaf carbon isotope composition
(δ13C; g) across treatments in each sex. Fvalue and Pvalue are shown.
NS, P>0.05; ∗P<0.05; ∗∗P<0.01; ∗∗∗P≤0.001.
consistent with the previous studies in Populus showing that
environmental stress (e.g., drought, nutrient deciency, heavy
metals) usually magnies dierences in growth and photosyn-
thesis between the sexes (Xu et al. 2008a,Zhang et al. 2012,
Melnikova et al. 2017,Liu et al. 2020,Xia et al. 2020).
Heat stress can directly aect plant metabolism, and leaves
can minimize heat absorption and maximize dissipation of latent
heat through biochemistry and stoma adjustment (Rennenberg
et al. 2006). We found that warming always increased non-
photochemical uorescence quenching (NPQ). Higher NPQ can
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Males suer more negative eects of summer heat stress than females 1187
Figure 7. Relationship between stomatal conductance (gs;a)and
light-saturated photosynthetic rate (A; b) and whole-plant hydraulic
conductance (KP) across treatments in each sex. Fvalue and Pvalue
are shown. ∗∗P<0.01; ∗∗∗P≤0.001.
transfer and dissipate excitation energy, which can protect plants
against heat and photoinhibition (Ruban 2016). On the other
hand, heat stress from exceeding photosynthetic optima usually
decreases the maximum rate of Rubisco carboxylation (Vcmax)
and maximum electron transport rate (Jmax)(Rennenberg et al.
2006,Way and Yamori 2014,Kumarathunge et al. 2019).
However, we found that Vcmax and Jmax of P. cathayana were
not signicantly aected by WM treatment, which suggests that
the decrease in photosynthesis in males was not driven by
photosynthetic biochemical limitation.
Besides biochemistry, stoma adjustment is also crucial for
plant responses to heat, as stoma regulates CO2uptake and
controls transpiration. We found that warming increased transpi-
ration rate (E) as well as stomatal conductance (gs)infemales,
but these traits in males were not aected (Figure 2b and d).
Higher gsin females may have two benets: (i) for plant carbon
assimilation by decreasing limitation of CO2entering cells and
(ii) for heat tolerance by decreasing leaf temperature, which is
important for responses to high temperature stress (Grossiord
et al. 2017). So, sex-specic dierences in photosynthesis
under heat may be mainly aected by stoma adjustment. Male
P. cathayana suered more suppression in growth and photo-
synthesis than females under heat with no soil water limitation,
which may explain observations of female bias in lower elevation
riparian populations (Meng et al. 2018).
Female responses were related with soil moisture rather than
air temperature
Heat-induced declines in soil moisture usually increase plants’
water decit (Grossiord et al. 2017). In this study, we found a
decrease in the average soil moisture content under warming
without supplemental water (WA) treatment, and plant predawn
leaf water potential and leaf water content were lower than
under control conditions. These results indicate that plants
suered a water decit under WA treatment, which supports
the previous conclusion that P. cathayana is very responsive to
soil moisture (Xu et al. 2008a,2008b,Zhang et al. 2012).
Xu et al. (2008b) found that female P. cathayana suered
a more negative eect on growth than do males under a
combination of +4◦C warming and drought, similar to our
ndings that females had a lower Aand that their biomass
decreased more than males under WA treatment. Therefore,
our results suggest that suppressed growth and leaf carbon
assimilation of P. cathayana under WA treatment may be induced
by heat and the concurrent water decit (Hoeppner and Dukes
2012). Moreover, high-temperature treatments (including WA
and WM) always decreased the ratio of leaf Ato dark respiration
rate by nearly 50% (A/Rd;Figure 3), and signicantly negative
relationships between Aor A/Rdand leaf temperature could
result in a higher risk of carbohydrate depletion and even
mortality (Allen et al. 2010,Drake et al. 2016,Duan et al.
2018).
However, when growing under +4◦C with the same soil
moisture content as CK (WM), female growth and photosyn-
thetic rate were similar to those under CK, and they were
higher than under WA treatment. These results indicate that the
decrease of growth and photosynthesis of females under warm-
ing was related with soil moisture rather than air temperature.
Higher temperatures will increase water transfer requirements at
a given soil moisture (Vico et al. 2019). Our results showed that
WM treatment led to a higher whole-plant hydraulic conductance
(KP) of females (Figure 4d). Increased KPmay directly increase
leaf water supply and leaf water status (Sperry et al. 2002).
Higher female KPunder WM treatment may compensate for
higher E. These results indicate that females adjust water
balance mechanisms under warming through changing water
uptake, hydraulic transfer and use (Marchin et al. 2016).
Sex-specic water balance with warming
Previous ndings have found that female Aor gswas more
sensitive to changes in leaf water status than males (Xu et al.
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1188 Liu et al.
Figure 8. Relationship between light-saturated photosynthetic rate (A; a), carbon accumulation eciency (A/Rd; b), stomatal conductance (gs;c)and
leaf temperature across treatments in each sex. Fvalue and Pvalue are shown. ∗P<0.05; ∗∗∗P≤0.001.
Figure 9. PCA based on the growth, photosynthesis and water use traits in each treatment (as dened in Figure 2; CK, circle; WA, square; WM,
rhombus) in total (a), female (b) and male (c) P. c a t h a y a n a cuttings. H, height; TA, total leaf area; SLA, special leaf area; TM, total dry mass; R/S, root-
to-shoot ratio; FR/TR, the ratio of ne root mass to total root mass; A, photosynthetic rate; gs, stomatal conductance; Rd, dark respiration rate of leaf; E,
transpiration rate; SSP,ST
Pand NSCP, soluble sugars, starch and NSC concentration of whole plant; Ψ, leaf predawn water potential; Ci/Ca, the ratio of
intercellular CO2concentration to ambient CO2concentration; Vcmax, the maximum rate of Rubisco carboxylation; Jmax,maximumelectrontransport
rates; Fv/Fm, maximum photochemical quantum yield of PSII; Φ, eective photochemical quantum yield of PSII, qP, coecient of photochemical
uorescence; NPQ, non-photochemical uorescence quenching; TL, leaf temperature; δ13 C, carbon isotope composition; KP, whole-plant hydraulic
conductance.
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Males suer more negative eects of summer heat stress than females 1189
2008a,2008b,Zhang et al. 2012). In this study, we observed
steeper positive relationships between Aor gsand leaf water
status in females than in males (Figure 6b–g). These results
support the previous ndings. However, we also found that there
were positive relationships between KPand gsor A,andfemales
showed higher gsor Aat a given KPthan males. Moreover,
WM treatment led to higher KPof females but lower KPof
males, while male KPwas higher than females under CK and
WA condition. Hydraulic conductance is a crucial trait for leaf
water status, as it may decrease the stomatal sensitivity to water
loss via transpiration (Sperry et al. 2002,Mitchell et al. 2013).
These results suggest that sex-specic adaptive responses in
hydraulic characteristics contribute to plant gsor Aadjustments
in varied temperature and soil moisture environment. Up to now,
there has been no study of sex-specic responses in hydraulic
characteristic in dioecious woody trees to warming. Further
study is needed to investigate the hydraulic characteristics of
water transfer eciency, which may help explain sex-related
ecological strategies related to water sensitivity and population
distributions, especially in a warming world (Olano et al. 2017).
On the other hand, we further found that leaf carbon iso-
tope composition (δ13C, widely used to represent plant long-
term water-use eciency) in females was lower under CK but
higher under WA or WM treatment than in males (Figure 4c).
These results suggest that females and males responding to
heat in water-use strategies are dierent, and female strate-
gies may be more variable, whereas male strategies may
be more conservative (Tognetti 2012,Hultine et al. 2016).
Thus, our results collectively suggest that the dierences in
water balance strategies through the regulation of stomatal
aperture, water-use eciency and eciency of the hydraulic
system between sexes may aect their drought and heat resis-
tances (Grossiord et al. 2017). Female P. cathayana responses
showed greater sensitivity in water balance and a more liberal
water-use eciency than males, which may help compensate
for female costs of reproduction (Barrett and Hough 2012,
Lei et al. 2017).
Conclusions
In summary, we found that the eects of warming on growth and
physiology were mediated by soil moisture. Carbon assimilation
in female plants was more aected by water-related traits (e.g.,
leaf potential, whole-plant hydraulic conductance) than that of
males, while males were more aected by leaf temperature.
Sexually divergent responses of P. cathayana to warming and
a exible water balance strategy via stomatal regulation and
water use mean that females show a higher heat tolerance
than males. Future studies on sexual responses to environmental
changes should consider traits in plant hydraulic characteristics.
The predicted warmer conditions in wet areas are likely to
amplify dierences between sexes in dioecious species, which
could lead to skewed sex ratios, sexual spatial segregation and
potentially less successful reproduction.
Supplementary Data
Supplementary Data for this article are available at Tree Physiol-
ogy Online.
Acknowledgments
We are very grateful to Lei Yu, Xuemei Huang, Xiaomei Wen, Na
Du and Shan Huang for their assistance during the eld work.
Conict of interest
The authors declare that they have no conict of interest.
Funding
The work was supported by the National Natural Science Foun-
dation of China (31600487; 31700536), Sichuan Science
and Technology Program (2019YFS0464) and the program of
China Scholarships Council (No. 201808515138).
Authors’ contributions
J.L., R.Z. and T.D. had the main responsibility for data collection,
analysis and writing, X.X. had a signicant contribution to
experimental design, J.F. and T.E.X.M. had signicant contribution
to the interpretation of data and manuscript preparation, and
T.D. (the corresponding author) had the overall responsibility
for experimental design and project management.
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