Next Article in Journal
Groundwater Defluoridation with Composite Oxyhydroxide Mineral Ores—The Case with Bauxite, a Systematic Review
Previous Article in Journal
Water Seepage in Rocks at Micro-Scale
Previous Article in Special Issue
Strawberry Growth under Current and Future Rainfall Scenarios
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Water
Volume 14
Issue 18
10.3390/w14182828
water-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Coordination among Water Transport, Photosynthesis and Nutrition under Climate Change: Stronger Responses of a Native than an Invasive Herb

by
Jin-Hua Qi
1,2,
Qiao-Shun Yan
1,2,
Rafa Tasnim
3,
Lan Zhang
4,
Pei-Li Fu
1,2,
Ze-Xin Fan
1,2 and
Yong-Jiang Zhang
3,5,*
1
Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China
2
Ailaoshan Station for Subtropical Forest Ecosystem Studies, Chinese Academy of Sciences, Jingdong 676200, China
3
School of Biology and Ecology, University of Maine, Orono, ME 04469, USA
4
State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
5
Climate Change Institute, University of Maine, Orono, ME 04469, USA
*
Author to whom correspondence should be addressed.
Water 2022, 14(18), 2828; https://doi.org/10.3390/w14182828
Submission received: 22 July 2022 / Revised: 7 September 2022 / Accepted: 7 September 2022 / Published: 11 September 2022
(This article belongs to the Special Issue Impacts of Climate Change on Plant Water Use, Carbon Balance, Nutrient Economy, and Their Interactions)
Browse Figures
Versions Notes

Abstract

:
Climate change will impact all plant physiological processes including water transport, photosynthesis, and nutrient assimilation. How these processes are coordinated in response to climate change is not fully understood. Here we tested how these processes will respond to elevated CO2 concentration ([CO2]) and temperatures for two herbaceous species (an invasive and a native Eupatorium species in East Asia; family Asteraceae) and whether these processes are coordinated using a controlled experiment. We also investigated the differences between these two species, and the structural basis for changes in physiology. Leaf photosynthetic capacity (Amax, measured under ambient conditions) increased significantly in the native species, while that of the invasive species did not change under elevated [CO2] and temperatures. The leaf hydraulic conductance (Kleaf) of both species tended to increase under elevated temperatures and [CO2], with that of the native species increasing to a greater extent. Changes in Kleaf and Amax were coordinated, and Kleaf was closely associated with leaf minor vein density across treatments. The increased photosynthetic capacity of the native species was probably related to an increased N investment in photosynthesis; its leaf N decreased but chlorophyll concentration increased inviting detailed studies in N partitioning. No coordination between water use (water transport, stomatal conductance, and water use efficiency) and leaf tissue nutrient (N, P) concentrations was found, probably owing to the active control in nutrient uptake. Thus, photosynthesis is coordinated with water transport in response to climate change, while the coordination between water use and nutrient accumulation can be absent due to active control. Our results also suggest that global climate change will not necessarily fuel more positive responses in invasive plants than native plants.

1. Introduction

Atmospheric CO2 concentration ([CO2]) and temperature have increased significantly in the past century, and the increases are predicted to accelerate in the future [1]. Atmospheric [CO2] is predicted to reach 600 to 850 ppm by the end of this century, while atmospheric temperatures will increase by 1.8 to 4 °C [1]. The change in atmospheric [CO2] and temperature will directly influence plant transpiration, nutrient uptake and transport, and photosynthesis. Plant physiological responses to global climate change have attracted great concerns and have been studied intensively, since plant biomes are the major carbon sinks to alleviate CO2 emissions from the burning of fossil fuels. Generally, photosynthesis (CO2 assimilation) tends to increase while stomatal conductance tends to decrease under elevated [CO2], and thus there is an increase in water use efficiency [2,3,4,5,6]. In spite of an increase in CO2 assimilation, the photosynthetic capacity of plants (i.e., maximum carboxylation rate) tends to decrease under elevated [CO2] [3,7,8,9,10]. In contrast, no general pattern has been revealed in the response of the plant water transport (xylem hydraulic conductance) to climate change. Plant water transport may increase, decrease, or maintain constant under elevated [CO2] [11,12,13,14,15,16,17,18,19,20,21] or under elevated temperatures [19,20,21,22,23,24,25]. Indeed, different plant functional groups and ecosystems can exhibit distinct responses to elevated [CO2] and temperatures [3,26,27], whereas the physiological mechanisms in explaining different responses are not fully understood.
Plant water transport, photosynthesis, and nutrient assimilation are all coupled, but their potential coordinated response to climate change remains poorly understood [24]. Plant water transport and photosynthetic gas exchange are coupled due to stomatal regulation, and thus water transport is one of the major determinants of leaf photosynthetic capacity [28,29,30,31,32]. However, climate change or seasonal changes in environmental conditions can shift or decouple this relationship [24,32,33]. Additionally, photosynthesis is strongly determined by leaf nutrient (especially nitrogen) concentrations and nutrient use efficiency [34,35,36,37,38], suggesting a coordinated response to climate change. Indeed, nitrogen (N) assimilation greatly regulates the response of plant photosynthesis and ecosystem carbon sequestration to global climate change [39]. Moreover, nutrient assimilation and water transport are coupled due to the facilitation of nutrient absorption and transportation by high transpiration [40,41,42]. Studying the coordination of these processes under global climate change will lead to a better understanding of plant performances under elevated [CO2] and temperatures at a mechanistic level [43,44].
It is hypothesized that invasive plants will have stronger positive responses to elevated [CO2] than their native counterparts because species with faster growth rates are found to be more stimulated by elevated [CO2] [26]. Higher growth increments in invasive than in native plants under elevated [CO2] have been reported [45,46,47,48], whereas contradictory results have also been reported [49,50,51]. Invasive species generally have higher photosynthetic and growth rates than their native counterparts under a common environment [52,53,54,55,56]. This is partially because invasive species have higher partitioning of N to photosynthetic vs. defense (e.g., cell walls), compared to their native counterparts [50,56,57]. Therefore, the N limitation on photosynthesis of invasive species should be weaker compared to their native counterparts under ambient conditions. Elevated atmospheric temperatures and [CO2] will enhance the photosynthetic N use efficiency of plants [8,10,58,59], thereby alleviating the N limitation on photosynthesis, especially in some native species with strong N limitation on photosynthesis. Elevated [CO2] and temperatures may also trigger changes in N partitioning, and small changes in nutrition partitioning may cause a great change in photosynthetic capacity [60]. Further, invasive and native plants have different water use strategies in general [61], therefore they may show different responses to global climate change.
In the present study, we compared the hydraulic, photosynthetic, and nutritional responses of Eupatorium adenophorum Sprengel (a worldwide noxious invasive plant species, cyn. Ageratina adenophora, family Asteraceae), and E. fortunei Turcz. (a widely distributed native species in China) to elevated [CO2] and temperatures. We also investigated changes in leaf structure to provide a structural explanation of the physiological response. The expansion of the invasive E. adenophorum in East Asia has already caused severe ecological and economic problems. It can replace native plants in pastures as well as the understory of natural forests and plantations with monocultures (e.g., Figure 1), imposing a large threat on regional biodiversity, forest regeneration, pollinator health, and economics. Additionally, its leaves and stems are poisonous to livestock, and its expansion can block irrigation ditches. Here, we aimed to quantify the different responses of these two species to climate change, and characterize the potential coordination among water transport, photosynthesis, and nutrient assimilation under climate change for those two herbaceous plants. Because E. fortunei is a congener and coexists with E. adenophorum in many regions in China, comparing their responses to climate change can provide implications for their competition in the future. We hypothesized that: (1) leaf water use (leaf vein density, hydraulic conductance, and stomatal conductance) of both species will increase under elevated temperatures owing to increased transpiration demand for cooling, but will decrease under elevated [CO2] owing to decreased demands for transpiration to get enough CO2; (2) because of a strong limitation of N on photosynthesis under ambient conditions, the photosynthetic capacity of the native species will increase under elevated [CO2] owing to increased N photosynthetic use efficiency, showing a stronger response than the invasive species; (3) the hydraulic, photosynthetic, and nutritional responses of these two species to elevated [CO2] and temperature are all coordinated and are associated with changes in leaf structure.

2. Materials and Methods

2.1. Plant Materials and Treatments

Two Eupatorium species from the family Asteraceae, E. adenophorum, and E. fortunei were selected for this study. Eupatorium adenophorum (cyn. Ageratina adenophora), native to Mexico, is now a noxious invasive species in more than 30 countries or regions, including China, India, Sri Lanka, Australia, Nigeria, South Africa, and the United States of America [62]. Eupatorium fortunei is a species native to Asia, and widely distributed in twelve provinces of China [63]. Eupatorium adenophorum is a perennial herbaceous shrub that may grow up to 1 or 2 m and can spread vegetatively (its stems can sprout roots to initiate new individuals). Its seeds are mainly carried by the wind or water and the plants colonize disturbed areas, such as fields near human settlements. Eupatorium fortunei is an herbaceous perennial that grows 40 to 100 cm tall from procumbent rhizomes. Plant materials used in the present study were germinated from seeds collected around Kunming (25°06′ N, 102°50′ E, elevation 2200 m), Yunnan Province, Southwest China. When seedlings were 10 cm tall, they were transplanted to 5 L pots and subjected to different types of treatments in four close-top chambers (E-sheng Tech. Co., Beijing, China). The seedlings were watered when necessary. Homogenized forest topsoil was used, and no fertilizer was added during the experiment. The two species were planted and managed the same way.
The close-top chambers are located in Ailaoshan Station for Subtropical Forest Ecosystem Studies (24°32′ N, 101°01′ E, elevation 2460 m), Jingdong County, Yunnan Province, SW China. There were four types of treatments: control; elevated [CO2] (660–740 ppm); elevated temperatures (2–3 °C higher than the control); and elevated both [CO2] and temperatures. A computer-controlled CO2 supply system (LT/ACR-ePLC, E-Sheng Tech. Co., Beijing, China) was used to control [CO2]. The average temperature and hourly mean [CO2] in the control chamber during the treatment period were 21.1 ± 0.7 °C and 330–370 ppm (relatively low because the study site is in a high elevation remote primary forest), respectively. The chambers were located in an open area and apart from each other to avoid shading effects. Efforts had been made to minimize chamber effects and the effects of within-chamber heterogeneity. All the chambers had the same size, shape, orientation, and equipment placement to minimize any potential chamber effect. All chambers were octagon-shaped with an area of 14 m2 and a height of 2.6 m. To minimize undetected environmental heterogeneity within each chamber, each chamber was divided into five sections and each section contained four potted seedlings of each species. Within each section, we placed seedlings randomly. We performed the measurements after six to seven months after the beginning of the treatments during the same year when plants were established. Thus, all plants were the same age (less than one-year-old) during the measurements. All the variables were measured once during the peak growing season.

2.2. Leaf Gas Exchange and Hydraulic Conductance Measurements

Leaf light-saturated photosynthetic rate per leaf area (Aa), stomatal conductance (gs), and intercellular CO2 concentration (Ci) were determined with a portable photosynthetic system (LI-6400XT, LICOR, Nebraska, USA) under ambient [CO2] and temperatures (~20 °C). This is because the objective of this study was to examine the difference in photosynthetic capacity determined by structure and biochemistry. Since elevated [CO2] may decrease gs [3], the gs measured under ambient conditions were termed maximum gs without depression at high [CO2] in this study. Relative humidity was around 70%, and a saturating PPFD was used (1500 μmol m−2 s−1) during the measurements. Four to six sun-exposed youngest fully expanded leaves per species and treatment from different individuals were randomly selected for gas exchange measurements. Light-saturated mass-based photosynthetic rate (Am) was calculated as Aa divided by leaf mass per area (LMA; described below). All the gas exchange measurements were conducted from 0900 to 1100 (solar time) on sunny days.
Leaf hydraulic conductance (Kleaf) was measured using the evaporative flux method [29,64,65,66]. Five to six leaves from different individuals per species and treatment were cut underwater at the petioles in late afternoons, allowed to absorb water overnight, and then the steady state Kleaf was measured in the morning of the second day under full sunlight from 0900 to 1100 (solar time) on sunny days. The leaf petiole cut end was recut under water and connected to a water-filled hard tubing connecting a water pressure-drop flow meter [29,65,67] to monitor the transpiration flow rate (E). When a steady state E was reached (almost constant in 5 min), the leaf was removed into a Ziploc bag that had been exhaled into, to prevent dehydration of the leaf. Leaf water potential (ΨL) was determined after at least 30 min equilibration, using a pressure chamber (PMS, Corvallis, OR, USA). The Kleaf was then calculated as the steady state E/ΨL, normalized by leaf area.

2.3. Leaf Nutrient Concentrations, Chlorophyll Concentration, δ13C

Leaf total carbon (C) and nitrogen (N) concentrations were determined using a Vario MAX CN auto element analyzer (Elementar Analysensysteme, Langenselbold, Germany) after the leaf samples were digested with concentrated H2SO4. Leaf construction cost (CC) was calculated based on leaf carbon concentration according to McDowell [68]. Leaf chlorophyll concentration (CHL) was measured by a portable chlorophyll meter (SPAD 502, Minolta Corp., Osaka, Japan). Previous studies reported strong relationships between SPAD measurements and total extracted chlorophyll (a + b) per leaf area for multiple species varying strongly in nutrient composition, thickness, and surface features, and the majority tended to have statistically similar relationships [69,70]. Leaf δ13C was measured by a MAT 525 stable isotope ratio mass spectrometer (Finnigan-MAT, Bremen, Germany), and calculated as [(Rsample − RPDB)/RPDB] × 1000. Rsample and RPDB are the 13C/12C ratio in the samples and the PDB standard (RPDB = 0.0112372), respectively.

2.4. Leaf Structure and Anatomy

Leaf thickness was measured with a Vernier Caliper at multiple places on each fresh leaf. For leaf mass per area measurement, six sun-exposed mature leaves from different individuals were collected. After leaf area determination with a scanner and an image-analyzing program, the leaves were oven dried (80 °C) to constant weight and weighed. Leaf mass per area was expressed as the ratio of leaf dry mass to leaf area. The middle part of six sun-exposed mature leaves was used to measure leaf stomatal density, stomatal size (guard cell length), and leaf vein density. The epidermis was peeled off from the abaxial surface, and then was observed under a microscope. Stomatal density was counted under 10× magnification and expressed as stomatal numbers per mm2. Guard cell length was measured with a micro-scale under 40× magnification. Leaf vein density was measured according to Brodribb et al. [29]. After clearing with NaOH solution, the leaf samples were stained with toluidine blue, and images were taken under the microscope. The images were then analyzed using ImageJ, and leaf vein density was expressed as length per mm2.

2.5. Statistical Analyses

Statistical analyses were carried out using the SPSS V21 software (IBM Corp., Armonk, NY, USA) or in R v.4.1.3 (R Core Team, Vienna, Austria). Homogeneity and normality of the variance were tested, and data were log-transformed if needed. A three-way-ANOVA was used to test the effects of [CO2], temperature, species, and their interactions on all the structural and physiological traits [71]. Differences in trait means among different treatment types were further assessed using one-way-ANOVA and Tukey LSD tests for each species. Differences in means between two species under each treatment type were tested by one-way-ANOVA [71]. A linear mixed model was used to test the relationships across species and treatment between functional traits with species set as a random factor using the “lmer” function in the LmerTest package. The relationship between Amax and Kleaf was also tested with an exponential relationship. Linear regression was used to test the relationships between functional traits within species.

3. Results

3.1. Temperature and [CO2] Effects on Leaf Structure

The leaf thickness of E. adenophorum was always higher than that of E. fortunei under all the treatment types (Figure 2a), while the stomatal density of the former was always lower than that of E. fortunei (Figure 2d). The leaf size of E. adenophorum was larger than that of E. fortunei under the control conditions and both elevated temperature and [CO2] (Figure 2b). No difference in leaf size was found under elevated [CO2] and elevated temperatures between these two species (Figure 2b). Leaf vein density was higher in E. adenophorum than in E. fortunei under control conditions, while no significant difference was found under elevated [CO2], elevated temperatures, and elevated both (Figure 2f).
The temperature treatment had significant effects on leaf thickness, leaf size, and leaf vein density, while the [CO2] treatment had significant effects on leaf size, LMA, stomatal density, and vein density (Table 1, Figure 2). Elevated temperatures significantly decreased leaf thickness (Figure 2a) and leaf size (Figure 2b), but increased stomatal density (Figure 2d) and leaf vein density (Figure 2f) in both species, compared to the ambient temperature in control. Elevated [CO2] had no effect on leaf thickness (Figure 2a) and LMA (Figure 2c), but increased leaf vein density (Figure 2f) in both species. Elevated [CO2] decreased the leaf size of the invasive E. adenophorum, but had no effect on the leaf size of the native E. fortunei, compared to the control (Figure 2b). Elevated [CO2] had no significant effect on the stomatal density of the invasive E. adenophorum, but it significantly decreased the stomatal density of the native E. fortunei (Figure 2d).

3.2. Temperature and [CO2] Effects on Leaf Hydraulic and Photosynthetic Characteristics

Under control conditions, leaf hydraulic conductance (Kleaf), light-saturated maximum photosynthetic rate per leaf area (Aa), and light-saturated maximum photosynthetic rate per leaf mass (Am) were significantly higher in E. adenophorum than in E. fortunei. Under elevated [CO2], elevated temperatures, and elevated both [CO2] and temperature, no significant difference in Aa and Am was found between the studied two species (Figure 2k,l). Kleaf was still significantly higher in E. adenophorum than in E. fortunei under elevated [CO2] and elevated both [CO2] and temperature, whereas no significant difference was found in Kleaf between the two species under elevated temperatures (Figure 2g).
The temperature treatment had significant effects on Kleaf, maximum stomatal conductance (gs), δ13C, (Aa), and Am, while the [CO2] treatment had significant effects on δ13C, Aa, and Am (Table 1, Figure 2). The increase in Kleaf of the invasive E. adenophorum was not significant, while that of the native E. fortunei was significant under elevated temperatures or elevated [CO2], compared to the control (Figure 2g). No significant difference was found in gs among different treatments in both species (Figure 2h). Elevated both [CO2] and temperature significantly reduced the δ13C of both species, while elevated temperatures had no significant effect on δ13C (Figure 2i). Elevated [CO2] reduced δ13C in E. adenophorum, but not in E. fortunei (Figure 2i). No significant difference was found in the leaf intercellular [CO2] concentration (Ci) of E. adenophorum among different treatments. Eupatorium fortunei under elevated temperatures or elevated [CO2] tended to have lower Ci than the control treatment, but not in a significant manner (Figure 2j). Elevated temperatures or [CO2] had no effect on photosynthetic capacity (Aa) in E. adenophorum, but significantly increased Aa in E. fortunei, compared to the control (Figure 2k). Eupatorium fortunei had a two-fold increase in Aa and Am when treated with elevated temperatures, elevated [CO2], and elevated both [CO2] and temperature, compared to the control conditions (Figure 2k,l). In E. adenophorum, Am was slightly but significantly higher in individuals under elevated [CO2], and under elevated both [CO2] and temperature than those under the control (Figure 2l). However, elevated temperatures had no effect on the Am of E. adenophorum (Figure 2l).

3.3. Temperature and [CO2] Effects on Leaf Nutrient Properties and Leaf Construction Cost

The invasive E. adenophorum had distinctly higher chlorophyll concentration (CHL), C/N ratio, photosynthetic nitrogen use efficiency (PNUE), and lower N than E. fortunei under control conditions, but the differences became smaller or absent when treated with elevated [CO2] or temperatures (Figure 3b–e). In contrast, no difference in leaf construction cost (CC) was found between these two species under control conditions, but E. adenophorum had significantly higher leaf CC than E. fortunei when treated with elevated [CO2] or temperatures (Figure 3f).
The temperature treatment had significant effects on leaf carbon (C) concentration, CHL, PNUE, and CC, while the [CO2] treatment had significant effects on leaf C and N concentrations, C/N ratio, PNUE, and leaf CC (Tabel 1, Figure 3). Elevated temperatures or elevated [CO2] significantly increased leaf total C and CC in E. adenophorum compared to the control (Figure 3a,f). No difference in leaf C and leaf CC was found among different treatments in E. fortunei (Figure 3a,f). Elevated temperatures significantly increased leaf N in E. adenophorum, but had no effect on leaf N in E. fortunei (Figure 3b). Elevated [CO2] significantly increased leaf N in E. adenophorum whereas significantly decreased leaf N in E. fortunei (Figure 3b). Elevated both temperature and [CO2] had no effect on leaf N in E. adenophorum, but significantly decreased leaf N in E. fortunei (Figure 3b). No difference was found in chlorophyll concentration (CHL) in E. adenophorum under different treatments, while CHL of E. fortunei was significantly higher under elevated temperature or [CO2] treatment compared to the control (Figure 3c). Photosynthetic N use efficiency increased greatly in E. fortunei when treated with elevated [CO2], or elevated temperatures, or elevated both [CO2] and temperatures, while that of E. adenophorum showed a decrease or no change, compared to the control (Figure 3e).

3.4. Coordination among Physiological Processes

Leaf intercellular [CO2] and Aa were positively related with maximum gs in the invasive species (E. adenophorum) across treatment types, but not in the native species (E. fortunei) (Figure 4a,c). In contrast, Aa was positively correlated with CHL in E. fortunei across treatment types, but not in E. adenophorum (Figure 4b). On the other hand, leaf intercellular [CO2] was negatively correlated with CHL in E. fortunei across treatments, but not in E. adenophorum (Figure 4d).
Photosynthetic rate per leaf area (Aa) was positively related with Kleaf across the studied species and treatments (Figure 5). Because Aa and Kleaf were not measured on the same individuals, we used species/treatment averages rather than individual data for this analysis. However, leaf water use efficiency (indicated by δ13C) was negatively related with maximum gs across the species and treatments (Figure 6). Also, stomatal density was negatively related with stomatal size (guard cell length), and leaf size across the species and treatments (Figure 7). Also, leaf hydraulic conductance was positively correlated with leaf vein density across the species and treatments (Figure 8). A relationship between maximum gs and stomatal density across the species and treatments was not found (relationships not shown). No significant relationship was found between water use traits (Kleaf, gs or iWUE) and leaf nutrient concentrations (N, P) across the species and treatments (relationships not shown).

4. Discussion

Our study provides some insights and potential mechanisms in explaining different responses of different species to elevated [CO2] and temperatures, and the coordination of different physiological processes under climate change. Moreover, climate change may not necessarily fuel more invasive species compared to native congeners. We found increased water use under both warming and elevated [CO2], partly supporting our first hypotheses. Between species, the invasive species (E. adenophorum) showed no change in photosynthetic capacity (measured under ambient conditions), while that of the native species (E. fortunei) increased in response to elevated [CO2] or temperatures. The native species also showed a stronger response in leaf hydraulics than the invasive species. This pattern supports our second hypothesis but is different from previous studies showing stronger or similar responses to elevated [CO2] in invasive species compared with native species [45,46,47,49,52]. Our results reveal coordinated changes in water transport, photosynthesis, and leaf structure in response to elevated [CO2] and temperatures in the two studied herbaceous species, but coupling between water use and nutrient (N and P) assimilation was not found. Thus, our hypothesis on the coupling among water use, carbon assimilation, and nutrition under climate change is only partly supported. The absence of a relationship between water use and assimilation of N and P could be because of the active control of uptake of these elements [42]. The water-nutrient coupling may only be detected for elements that are passively absorbed and lack relocation after assimilation [42].

4.1. Coordinated Changes in Water Transport and Photosynthesis, and Water Relations

We found strong coordination between water transport and photosynthesis of these two Eupatorium species in response to elevated [CO2] and temperatures (see Figure 5), which was absent in one previous study on soybean [24]. In that study, Kleaf of soybean showed no change under elevated [CO2] and temperatures [24], but the species studied here showed increases in Kleaf under elevated [CO2]. This could be because leaf water transport (hydraulic conductance) is a strong limiting factor in photosynthetic gas exchange of these two species under ambient conditions but not soybeans, while more carbohydrate accumulation under elevated [CO2] induces more investment in xylem enhancing leaf water transport. Increased carbohydrate accumulation under elevated [CO2] was found to stimulate tissue growth [72]. Notably, Kleaf of these two Eupatorium species (0.98 and 0.50 mmol m−2 s−1 MPa−2) are among the lowest in plants (Kleaf ranges from 0.50 to 21.10 mmol m−2 s−1 MPa−2; [29]). Low Kleaf of these two species are structurally determined by their low leaf minor vein densities compared to other angiosperms [29]. The limitation of leaf water transport on gas exchange in these two studied plants is supported by the positive relationship between Aa and Kleaf (or leaf vein density) across the species and treatments. Although Kleaf tended to increase under elevated [CO2] in these two species, it is still very low compared to other plants [29] and may still be a limiting factor in photosynthesis.
The limitation of leaf water transport on gas exchange is supported by the fact that both species are very sensitive to transpirational water loss. Leaf wilting is very common for both species in the late morning and at noon on sunny days (Unpublished observations by the authors). Since leaf water supply may limit gs and the time to maintain high gs without wilting during the day, an increase in Kleaf under elevated [CO2] could partially mitigate this limitation. Therefore, we suggest that leaf water supply being a strong limiting factor in gas exchange under ambient conditions may influence the responses of Kleaf to elevated [CO2]. This mechanism provides a possible explanation for the contradictory results in literature stating different responses of water transport to elevated [CO2] and temperatures, which could be further tested among different plant functional groups.
The significant decline in water use efficiency (indicated by δ13C) in the invasive species (E. adenophorum) under elevated [CO2] suggests an increase in long-term stomatal conductance under elevated [CO2]. The negative relationship between δ13C and maximum gs across species and treatment types suggests that the decline in water use efficiency was associated with increased gs. This is different from some other CO2 rising experiments showing increased water use efficiency and decreased gs [2,3,5,6,9], whereas some species showed no difference [12,73,74]. Since the photosynthetic capacity of the native species increased two-fold under elevated [CO2], it may need to maintain high stomatal conductance to facilitate gas exchange even under elevated [CO2]. For the invasive species, since its photosynthetic capacity is not limited by the leaf chlorophyll concentration but stomatal conductance (as suggested by the significantly positive relationship between Aa and gs; and between Ci and gs), elevated [CO2] does not necessarily result in reduced stomatal conductance. Notably, the δ13C data here needs to be interpreted with caution as it may be influenced by the isotope signature of the added CO2.

4.2. Changes in Photosynthetic Capacity in Relation to N

The different photosynthetic responses of these two species could be due to different responses in N investment in photosynthesis (N partitioning). Photosynthetic capacity of the invasive E. adenophorum did not decline under elevated [CO2] as found in other species, probably owing to its increased N accumulation. Reductions in photosynthetic capacity (not actual photosynthesis under elevated [CO2]) are common in plants under elevated [CO2] due to a decreased amount of Rubisco [3,7,8,9]. The absence of a decline in photosynthetic capacity (Aa) of the invasive E. adenophorum could be explained by its increased leaf N concentration and thus no reduction in N investment in Rubisco. Our result, therefore, suggests that species with the capability to increase N absorption/accumulation may not necessarily show a reduction in photosynthetic capacity under elevated [CO2] as found in other species. This pattern agrees with previous studies on N-fixing plants [3] and two Eucalyptus species under well-fertilized conditions [75].
Meanwhile, the distinct increase in photosynthetic capacity of the native species under elevated [CO2] and temperatures is probably because its photosynthetic capacity under ambient conditions is strongly limited by the low N partitioning to photosynthesis, which is changed by elevated [CO2] and temperatures. The native species showed significantly lower CHL and Aa than the invasive species under ambient conditions. The photosynthetic capacity of the native E. fortunei also is lower than that of another two native Eupatorium species (E. japonicum and E. chinensis) [76]. However, leaf N concentration of the native species is significantly higher than for the invasive species under ambient conditions, suggesting that the low Aa in E. fortunei under ambient conditions is not because of a low tissue N but is probably owing to its low N partitioning into photosynthesis. The strong photosynthetic-N limitation on photosynthesis in E. fortunei was supported by the strong relationship between Aa and CHL, and between Ci and CHL. In contrast, the N partitioning in photosynthesis of the invasive E. adenophorum is higher than for E. fortunei and other two native Eupatorium species (E. japonicum and E. chinensis) [76], probably due to its low investment in cell walls for herbivore defense [57].
Elevated temperature and [CO2] altered the N partitioning of the native E. fortunei. Although leaf N of the native species did not change under elevated temperature and declined under elevated [CO2], its CHL concentration increased significantly under elevated [CO2] or temperatures, suggesting an increased partitioning of N to chlorophyll and photosynthesis. A small change in nutrition partitioning would cause a great change in photosynthetic capacity [60], and we believe that the increased photosynthetic capacity of E. fortunei is at least partially due to the changes in N partitioning, inviting further detailed chemical examinations. The increased N partitioning to photosynthesis under elevated [CO2] could be due to the decrease in structural N concentration triggered by the increase in [CO2] [8]. Therefore, species with photosynthetic capacity strongly limited by low N partitioning to photosynthesis under ambient conditions may show an increase in photosynthetic capacity under elevated [CO2]. In contrast, the invasive species increased its leaf N concentration, while its CHL concentration remained the same under elevated [CO2] and temperatures. Thus, the increased leaf N of the invasive species under elevated [CO2] or temperatures is probably invested in leaf construction, or the regeneration process of RuBP, since photosynthesis would become more limited by RuBP regeneration under elevated [CO2] [3].

4.3. Coordinated Changes in Leaf Structure and Function

Changes in leaf structure and function under climate change are coordinated; changes in Kleaf are explained by leaf vein density, and changes in stomatal density are strongly associated with leaf size. These structural changes are related to changes in cell expansion and leaf development under elevated [CO2] and temperatures. Leaf vein density is critical in determining Kleaf [29,77], while stomatal density indicates the potential maximum gs in general [78]. Additionally, our results suggest that, in terms of structural limitation, leaf vein density rather than stomatal density limits the stomatal conductance of these two species. The decline in stomatal density under elevated [CO2] in these two species did not result in a decline in maximum stomatal conductance and photosynthesis, suggesting that stomatal density is not the limiting factor in gas exchange in these two herbaceous species. Generally, leaf vein density and stomatal density are coordinated in acclimation to different environmental conditions [79,80]. However, our study suggests that for species whose gs is limited by leaf hydraulic conductance rather than stomatal density, leaf vein density and stomatal density may not respond to environmental changes in the same way.
Further, stomatal and leaf vein densities had same responses to elevated temperatures but different responses to elevated [CO2]. The stomatal response observed in the present study is consistent with some previous studies showing an increase in stomatal density under elevated temperatures [81,82], while some other studies showed lower stomatal density in some species growing under warmer temperatures [83,84]. On the other hand, elevated [CO2] tends to decrease stomatal density in some species [81,85,86], whereas the stomatal density of some species was not affected under the elevated [CO2] [82,87]. Agreeing with increased stomatal density under elevated temperatures, leaf vein densities of the studied species also increased. However, in contrast to the decrease in stomatal density under elevated [CO2], the leaf vein density of both species tended to increase. Different responses to elevated [CO2] between stomatal density and leaf vein density may be because leaf water transport (Kleaf) is a strong limiting factor in gas exchange while stomatal density is not, as indicated by the absence of a relationship between maximum gs and stomatal density across species and treatments.

5. Conclusions

Overall, our results suggest that some native congeners could be more advantageous under climate change compared to invasive herbs, and the hypothesis that invasive plants have stronger positive responses to elevated [CO2] than native plants is not always true. The native E. fortunei had stronger hydraulic and photosynthetic responses to elevated [CO2] and temperatures than the invasive E. adenophorum. Different responses of these two congeners to climate change could be related to different limiting factors on photosynthesis under ambient conditions. Thus, understanding the limiting factor in photosynthesis of the species could help predict plant responses to global climate change. N investment (partitioning) in photosynthesis is a strong limiting factor on photosynthesis of E. fortunei under ambient conditions, while our results suggest that the increase in photosynthetic capacity of the native E. fortunei could be related to an increased N partitioning in photosynthesis under elevated [CO2] and temperatures, suggested by no change in leaf N but an increase in CHL. In addition, the increase in leaf water use and leaf hydraulic conductance under elevated [CO2] and temperatures may be because leaf water transport is a strong limiting factor in photosynthetic gas exchange of these two species. Moreover, our results suggest coordinated changes in water transport and photosynthesis in these two species with low hydraulic conductance, inviting studies across species with a great range of water transport capacity. The absence of coupling between water use and nutrient (N, P) accumulation under climate change invites more mechanistic studies to distinguish passive and active nutrient uptake processes.

Author Contributions

Conceptualization, Y.-J.Z.; methodology, Y.-J.Z. and J.-H.Q.; formal analysis, L.Z. and Y.-J.Z.; resources, Y.-J.Z. and Z.-X.F.; writing—original draft preparation, Y.-J.Z. and R.T.; writing—review and editing, J.-H.Q., Q.-S.Y., L.Z., P.-L.F., Z.-X.F. and R.T.; visualization, Y.-J.Z.; supervision, Y.-J.Z.; project administration, Y.-J.Z. and Z.-X.F.; funding acquisition, Y.-J.Z., P.-L.F. and Z.-X.F. All authors have read and agreed to the published version of the manuscript.

Funding

Y.-J.Z. is supported by USDA National Institute of Food and Agriculture, Hatch Project Number ME0-22021 through the Maine Agricultural and Forest Experiment Station. R.T. is supported by the Ellen Keough Hodosh Fellowship. Z.-X.F., P.-L.F., Q.-S.Y., and J.-H.Q. are supported by the Open Fund of CAS Key Laboratory of Tropical Forest Ecology (20-CAS-TFE-03; 20-CAS-TFE-04).

Data Availability Statement

Data is available upon request from the corresponding author Yong-Jiang Zhang (email ID: [email protected]).

Acknowledgments

We thank the Ailaoshan Station for Subtropical Forest Ecosystem Studies for providing logistical support. We thank the Institutional Center for Shared Technologies and Facilities of Xishuangbanna Tropical Botanical Garden, CAS for the determination of nutrient concentrations. We also thank Yanbao Lei, Shuai Li, Xuewei Fu, Qiuyun Yang, and Ke Ai for their assistance in the measurements.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. IPCC. Climate Change 2022: Impacts, Adaptation, and Vulnerability. In Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change; Pörtner, H.-O., Roberts, D.C., Tignor, M., Poloczanska, E.S., Mintenbeck, K., Alegría, A., Craig, M., Langsdorf, S., Löschke, S., Möller, V., et al., Eds.; Cambridge University Press: Cambridge, UK, 2022. [Google Scholar]
  2. Medlyn, B.E.; Barton, C.V.M.; Broadmeadow, M.S.J.; Ceulemans, R.; De Angelis, P.; Forstreuter, M.; Freeman, M.; Jackson, S.B.; Kellomaki, S.; Laitat, E.; et al. Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: A synthesis. New Phytol. 2001, 149, 247–264. [Google Scholar] [CrossRef] [PubMed]
  3. Ainsworth, E.A.; Rogers, A. The response of photosynthesis and stomatal conductance to rising [CO2]: Mechanisms and environmental interactions. Plant Cell Environ. 2007, 30, 258–270. [Google Scholar] [CrossRef] [PubMed]
  4. Lammertsma, E.I.; de Boer, H.J.; Dekker, S.C.; Dilcher, D.L.; Lotter, A.F.; Wagner-Cremer, F. Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation. Proc. Natl. Acad. Sci. USA 2011, 108, 4035–4040. [Google Scholar] [CrossRef]
  5. Guerrieri, R.; Belmecheri, S.; Ollinger, S.V.; Asbjornsen, H.; Jennings, K.; Xiao, J.; Stocker, B.D.; Martin, M.; Hollinger, D.Y.; Bracho-Garrillo, R.; et al. Disentangling the role of photosynthesis and stomatal conductance on rising forest water-use efficiency. Proc. Natl. Acad. Sci. USA 2019, 116, 16909–16914. [Google Scholar] [CrossRef] [PubMed]
  6. Mathias, J.M.; Thomas, R.B. Global tree intrinsic water use efficiency is enhanced by increased atmospheric CO2 and modulated by climate and plant functional types. Proc. Natl. Acad. Sci. USA 2021, 118, e2014286118. [Google Scholar] [CrossRef] [PubMed]
  7. Rogers, A.; Humphries, S.W. A mechanistic evaluation of photosynthetic acclimation at elevated CO2. Glob. Change Biol. 2000, 6, 1005–1011. [Google Scholar] [CrossRef]
  8. Luomala, E.M.; Laitinen, K.; Kellomaki, S.; Vapaavuori, E. Variable photosynthetic acclimation in consecutive cohorts of Scots pine needles during 3 years of growth at elevated CO2 and elevated temperature. Plant Cell Environ. 2003, 26, 645–660. [Google Scholar] [CrossRef]
  9. Ainsworth, E.A.; Long, S.P. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol. 2005, 165, 351–371. [Google Scholar] [CrossRef]
  10. Dusenge, M.E.; Duarte, A.G.; Way, D.A. Plant carbon metabolism and climate change: Elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol. 2019, 221, 32–49. [Google Scholar] [CrossRef]
  11. Atkinson, C.J.; Taylor, J.M. Effects of elevated CO2 on stem growth, vessel area and hydraulic conductivity of oak and cherry seedlings. New Phytol. 1996, 133, 617–626. [Google Scholar] [CrossRef]
  12. Heath, J.; Kerstiens, G.; Tyree, M.T. Stem hydraulic conductance of European beech (Fagus sylvatica L.) and pedunculate oak (Quercus robur L.) grown in elevated CO2. J. Exp. Bot. 1997, 48, 1487–1489. [Google Scholar] [CrossRef]
  13. Bunce, J.A.; Ziska, L.H. Decreased hydraulic conductance in plants at elevated carbon dioxide. Plant Cell Environ. 1998, 21, 121–126. [Google Scholar] [CrossRef]
  14. Tognetti, R.; Longobucco, A.; Miglietta, F.; Raschi, A. Water relations, stomatal response and transpiration of Quercus pubescens trees during summer in a Mediterranean carbon dioxide spring. Tree Physiol. 1999, 19, 261–270. [Google Scholar] [CrossRef] [PubMed]
  15. Tognetti, R.; Longobucco, A.; Raschi, A.; Miglietta, F.; Fumagalli, I. Responses of two Populus clones to elevated atmospheric CO2 concentration in the field. Ann. For. Sci. 1999, 56, 493–500. [Google Scholar] [CrossRef]
  16. Wullschleger, S.D.; Tschaplinski, T.J.; Norby, R.J. Plant water relations at elevated CO2—Implications for water-limited environments. Plant Cell Environ. 2002, 25, 319–331. [Google Scholar] [CrossRef]
  17. Eguchi, N.; Morii, N.; Ueda, T.; Funada, R.; Takagi, K.; Hiura, T.; Sasa, K.; Koike, T. Changes in petiole hydraulic properties and leaf water flow in birch and oak saplings in a CO2-enriched atmosphere. Tree Physiol. 2008, 28, 287–295. [Google Scholar] [CrossRef] [PubMed]
  18. Domec, J.C.; Palmroth, S.; Ward, E.; Maier, C.A.; Therezien, M.; Oren, R. Acclimation of leaf hydraulic conductance and stomatal conductance of Pinus taeda (loblolly pine) to long-term growth in elevated CO2 (free-air CO2 enrichment) and N-fertilization. Plant Cell Environ. 2009, 32, 1500–1512. [Google Scholar] [CrossRef]
  19. Sperry, J.S.; Venturas, M.D.; Todd, H.N.; Trugman, A.T.; Anderegg, W.R.; Wang, Y.; Tai, X. The impact of rising CO2 and acclimation on the response of US forests to global warming. Proc. Natl. Acad. Sci. USA 2019, 116, 25734–25744. [Google Scholar] [CrossRef]
  20. Hao, G.Y.; Holbrook, N.M.; Zwieniecki, M.A.; Gutschick, V.P.; BassiriRad, H. Coordinated responses of plant hydraulic architecture with the reduction of stomatal conductance under elevated CO2 concentration. Tree Physiol. 2018, 38, 1041–1052. [Google Scholar] [CrossRef]
  21. Medeiros, J.S.; Ward, J.K. Increasing atmospheric [CO2] from glacial to future concentrations affects drought tolerance via impacts on leaves, xylem and their integrated function. New Phytol. 2013, 199, 738–748. [Google Scholar] [CrossRef] [Green Version]
  22. Thomas, D.S.; Montagu, K.D.; Conroy, J.P. Changes in wood density of Eucalyptus camaldulensis due to temperature: The physiological link between water viscosity and wood anatomy. For. Ecol. Manag. 2004, 193, 157–165. [Google Scholar] [CrossRef]
  23. Phillips, N.G.; Attard, R.D.; Ghannoum, O.; Lewis, J.D.; Logan, B.A.; Tissue, D.T. Impact of variable [CO2] and temperature on water transport structure-function relationships in Eucalyptus. Tree Physiol. 2011, 31, 945–952. [Google Scholar] [CrossRef] [PubMed]
  24. Locke, A.M.; Sack, L.; Bernacchi, C.J.; Ort, D.R. Soybean leaf hydraulic conductance does not acclimate to growth at elevated [CO2] or temperature in growth chambers or in the field. Ann. Bot. 2013, 112, 911–918. [Google Scholar] [CrossRef] [PubMed]
  25. Way, D.A.; Domec, J.C.; Jackson, R.B. Elevated growth temperatures alter hydraulic characteristics in trembling aspen (Populus tremuloides) seedlings: Implications for tree drought tolerance. Plant Cell Environ. 2013, 36, 103–115. [Google Scholar] [CrossRef] [PubMed]
  26. Poorter, H.; Navas, M.L. Plant growth and competition at elevated CO2: On winners, losers and functional groups. New Phytol. 2003, 157, 175–198. [Google Scholar] [CrossRef] [PubMed]
  27. Zhang, Y.J.; Cristiano, P.M.; Zhang, Y.F.; Campanello, P.I.; Tan, Z.H.; Zhang, Y.P.; Cao, K.; Goldstein, G. Carbon economy of subtropical forests. In Tropical Tree Physiology; Goldstein, G., Santiago, L.S., Eds.; Springer: Berlin/Heidelberg, Germany, 2016; pp. 337–355. [Google Scholar]
  28. Santiago, L.S.; Goldstein, G.; Meinzer, F.C.; Fisher, J.B.; Machado, K.; Woodruff, D.; Jones, T. Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 2004, 140, 543–550. [Google Scholar] [CrossRef] [PubMed]
  29. Brodribb, T.J.; Feild, T.S.; Jordan, G.J. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol. 2007, 144, 1890–1898. [Google Scholar] [CrossRef]
  30. Zhang, J.L.; Cao, K.F. Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. Funct. Ecol. 2009, 23, 658–667. [Google Scholar] [CrossRef]
  31. Zhang, Y.J.; Meinzer, F.C.; Qi, J.H.; Goldstein, G.; Cao, K.F. Midday stomatal conductance is more related to stem rather than leaf water status in subtropical deciduous and evergreen broadleaf trees. Plant Cell Environ. 2013, 36, 149–158. [Google Scholar] [CrossRef]
  32. Siddiq, Z.; Zhang, Y.-J. Cool-dry season depression in gas exchange of canopy leaves and water flux of tropical trees at the northern limit of Asian tropics. Plant Ecol. 2022, 223, 171–183. [Google Scholar] [CrossRef]
  33. Sack, L.; Tyree, M.T.; Holbrook, N.M. Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytol. 2005, 167, 403–413. [Google Scholar] [CrossRef] [PubMed]
  34. Field, C.; Mooney, H.A. The photosynthesis-nitrogen relationship in wild plants. In On the Economy of Plant Form and Function; Givnish, T., Ed.; Cambridge University Press: London, UK, 1986; pp. 25–55. [Google Scholar]
  35. Reich, P.B.; Walters, M.B.; Ellsworth, D.S. From tropics to tundra: Global convergence in plant functioning. Proc. Natl. Acad. Sci. USA 1997, 94, 13730–13734. [Google Scholar] [CrossRef] [PubMed]
  36. Wright, I.J.; Reich, P.B.; Westoby, M.; Ackerly, D.D.; Baruch, Z.; Bongers, F.; Cavender-Bares, J.; Chapin, T.; Cornelissen, J.H.C.; Diemer, M.; et al. The worldwide leaf economics spectrum. Nature 2004, 428, 821–827. [Google Scholar] [CrossRef] [PubMed]
  37. Zhang, Y.J.; Cao, K.F.; Sack, L.; Li, N.; Wei, X.M.; Goldstein, G. Extending the generality of leaf economic design principles in the cycads, an ancient lineage. New Phytol. 2015, 206, 817–829. [Google Scholar] [CrossRef]
  38. Zhang, Y.-B.; Yang, D.; Zhang, K.-Y.; Bai, X.-L.; Wang, Y.-S.-D.; Wu, H.-D.; Ding, L.-Z.; Zhang, Y.-J.; Zhang, J.-L. Higher water and nutrient use efficiencies in savanna than in rainforest lianas result in no difference in photosynthesis. Tree Physiol. 2021, 42, 145–159. [Google Scholar] [CrossRef]
  39. Niu, S.L.; Sherry, R.A.; Zhou, X.H.; Wan, S.Q.; Luo, Y.Q. Nitrogen regulation of the climate-carbon feedback: Evidence from a long-term global change experiment. Ecology 2010, 91, 3261–3273. [Google Scholar] [CrossRef]
  40. Barber, S.A. A diffusion and mass-flow concept of soil nutrient availability. Soil Sci. 1962, 93, 39–49. [Google Scholar] [CrossRef]
  41. Zhang, Y.-J.; Sack, L.; Goldstein, G.; Cao, K.-F. Hydraulic determination of leaf nutrient concentrations in cycads. Mem. NY Bot. Gard 2018, 117, 179–192. [Google Scholar]
  42. Yin, Y.; Zhou, Y.-B.; Li, H.; Zhang, S.-Z.; Fang, Y.-T.; Zhang, Y.-J.; Zou, X. Linking tree water use efficiency with calcium and precipitation. Tree Physiol. 2022; in press. [Google Scholar] [CrossRef]
  43. Tyree, M.T.; Alexander, J.D. Plant water relations and the effects of elevated CO2—A review and suggestions for future research. Vegetatio 1993, 104, 47–62. [Google Scholar] [CrossRef]
  44. McDowell, N.G.; Sapes, G.; Pivovaroff, A.; Adams, H.D.; Allen, C.D.; Anderegg, W.R.; Arend, M.; Breshears, D.D.; Brodribb, T.; Choat, B.; et al. Mechanisms of woody-plant mortality under rising drought, CO2 and vapour pressure deficit. Nat. Rev. Earth Environ. 2022, 3, 294–308. [Google Scholar] [CrossRef]
  45. Smith, S.D.; Huxman, T.E.; Zitzer, S.F.; Charlet, T.N.; Housman, D.C.; Coleman, J.S.; Fenstermaker, L.K.; Seemann, J.R.; Nowak, R.S. Elevated CO2 increases productivity and invasive species success in an arid ecosystem. Nature 2000, 408, 79–82. [Google Scholar] [CrossRef] [PubMed]
  46. Raizada, P.; Singh, A.; Raghubanshi, A.S. Comparative response of seedlings of selected native dry tropical and alien invasive species to CO2 enrichment. J. Plant Ecol. 2009, 2, 69–75. [Google Scholar] [CrossRef]
  47. Song, L.Y.; Wu, J.R.; Li, C.H.; Li, F.R.; Peng, S.L.; Chen, B.M. Different responses of invasive and native species to elevated CO2 concentration. Acta Oecologica.-Int. J. Ecol. 2009, 35, 128–135. [Google Scholar] [CrossRef]
  48. Stephens, K.L.; Dantzler-Kyer, M.E.; Patten, M.A.; Souza, L. Differential responses to global change of aquatic and terrestrial invasive species: Evidences from a meta-analysis. Ecosphere 2019, 10, e02680. [Google Scholar] [CrossRef]
  49. Bradford, M.A.; Schumacher, H.B.; Catovsky, S.; Eggers, T.; Newingtion, J.E.; Tordoff, G.M. Impacts of invasive plant species on riparian plant assemblages: Interactions with elevated atmospheric carbon dioxide and nitrogen deposition. Oecologia 2007, 152, 791–803. [Google Scholar] [CrossRef]
  50. Qing, H.; Cai, Y.; Xiao, Y.; Yao, Y.; An, S. Leaf nitrogen partition between photosynthesis and structural defense in invasive and native tall form Spartina alterniflora populations: Effects of nitrogen treatments. Biol. Invasions 2012, 14, 2039–2048. [Google Scholar] [CrossRef]
  51. Manea, A.; Leishman, M.R. Competitive interactions between native and invasive exotic plant species are altered under elevated carbon dioxide. Oecologia 2011, 165, 735–744. [Google Scholar] [CrossRef]
  52. He, L.; Kong, J.; Li, G.; Meng, G.; Chen, K. Similar responses in morphology, growth, biomass allocation, and photosynthesis in invasive Wedelia trilobata and native congeners to CO2 enrichment. Plant Ecol. 2018, 219, 145–157. [Google Scholar] [CrossRef]
  53. Pattison, R.R.; Goldstein, G.; Ares, A. Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 1998, 117, 449–459. [Google Scholar] [CrossRef]
  54. Baruch, Z.; Goldstein, G. Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 1999, 121, 183–192. [Google Scholar] [CrossRef]
  55. Stratton, L.C.; Goldstein, G. Carbon uptake, growth and resource-use efficiency in one invasive and six native Hawaiian dry forest tree species. Tree Physiol. 2001, 21, 1327–1334. [Google Scholar] [CrossRef] [PubMed]
  56. Feng, Y.L.; Auge, H.; Ebeling, S.K. Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 2007, 153, 501–510. [Google Scholar] [CrossRef] [PubMed]
  57. Feng, Y.L.; Lei, Y.B.; Wang, R.F.; Callaway, R.M.; Valiente-Banuet, A.; Inderjit; Li, Y.P.; Zheng, Y.L. Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc. Natl. Acad. Sci. USA 2009, 106, 1853–1856. [Google Scholar] [CrossRef]
  58. Hobbie, E.A.; Olszyk, D.M.; Rygiewicz, P.T.; Tingey, D.T.; Johnson, M.G. Foliar nitrogen concentrations and natural abundance of N-15 suggest nitrogen allocation patterns of Douglas-fir and mycorrhizal fungi during development in elevated carbon dioxide concentration and temperature. Tree Physiol. 2001, 21, 1113–1122. [Google Scholar] [CrossRef]
  59. An, Y.A.; Wan, S.Q.; Zhou, X.H.; Subedar, A.A.; Wallace, L.L.; Luo, Y.Q. Plant nitrogen concentration, use efficiency, and contents in a tallgrass prairie ecosystem under experimental warming. Glob. Change Biol. 2005, 11, 1733–1744. [Google Scholar] [CrossRef]
  60. Takashima, T.; Hikosaka, K.; Hirose, T. Photosynthesis or persistence: Nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ. 2004, 27, 1047–1054. [Google Scholar] [CrossRef]
  61. Cavaleri, M.A.; Sack, L. Comparative water use of native and invasive plants at multiple scales: A global meta-analysis. Ecology 2010, 91, 2705–2715. [Google Scholar] [CrossRef] [PubMed]
  62. Cronk, Q.C.B.; Fuller, J.L. Plant Invaders: The Threat to Natural Ecosystems; Chapman Hall: London, UK, 1995. [Google Scholar]
  63. Lin, R.; Chen, Y. Flora of China; Science Press: Beijing, China, 1985; p. 74. [Google Scholar]
  64. Sack, L.; Melcher, P.J.; Zwieniecki, M.A.; Holbrook, N.M. The hydraulic conductance of the angiosperm leaf lamina: A comparison of three measurement methods. J. Exp. Bot. 2002, 53, 2177–2184. [Google Scholar] [CrossRef]
  65. Brodribb, T.J.; Holbrook, N.M. Declining hydraulic efficiency as transpiring leaves desiccate: Two types of response. Plant Cell Environ. 2006, 29, 2205–2215. [Google Scholar] [CrossRef]
  66. Sack, L.; Scoffoni, C. Measurement of leaf hydraulic conductance and stomatal conductance and their responses to irradiance and dehydration using the evaporative flux method (EFM). J. Vis. Exp. 2012, 70, e4179. [Google Scholar] [CrossRef] [Green Version]
  67. Melcher, P.J.; Michele Holbrook, N.; Burns, M.J.; Zwieniecki, M.A.; Cobb, A.R.; Brodribb, T.J.; Choat, B.; Sack, L. Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods Ecol. Evol. 2012, 3, 685–694. [Google Scholar] [CrossRef]
  68. McDowell, S.C. Photosynthetic characteristics of invasive and noninvasive species of Rubus (Rosaceae). Am. J. Bot. 2002, 89, 1431–1438. [Google Scholar] [CrossRef] [PubMed]
  69. Marquard, R.; Tipton, J. Relationship between extractable chlorophyll and an in-situ method to estimate leaf greenness. Hortscience 1987, 22, 1327. [Google Scholar]
  70. Marenco, R.A.; Antezana-Vera, S.A.; Nascimento, H.C.S. Relationship between specific leaf area, leaf thickness, leaf water content and SPAD-502 readings in six Amazonian tree species. Photosynthetica 2009, 47, 184–190. [Google Scholar] [CrossRef]
  71. Sokal, R.R.; Rohlf, F.J. Biometry: The Principles and Practice of Statistics in Biological Research, 4th ed.; W. H. Freeman and Co.: New York, NY, USA, 2011. [Google Scholar]
  72. Vu, J.C.V.; Allen Jr, L.H.; Bowes, G. Leaf ultrastructure, carbohydrates and protein of soybeans grown under CO2 enrichment. Environ. Exp. Bot. 1989, 29, 141–147. [Google Scholar] [CrossRef]
  73. Ellsworth, D.S. CO2 enrichment in a maturing pine forest: Are CO2 exchange and water status in the canopy affected? Plant Cell Environ. 1999, 22, 461–472. [Google Scholar] [CrossRef]
  74. Apple, M.E.; Olszyk, D.M.; Ormrod, D.P.; Lewis, J.; Southworth, D.; Tingey, D.T. Morphology and stomatal function of Douglas Fir needles exposed to climate change: Elevated CO2 and temperature. Int. J. Plant Sci. 2000, 161, 127–132. [Google Scholar] [CrossRef]
  75. Ghannoum, O.; Phillips, N.G.; Sears, M.A.; Logan, B.A.; Lewis, J.D.; Conroy, J.P.; Tissue, D.T. Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature. Plant Cell Environ. 2010, 33, 1671–1681. [Google Scholar] [CrossRef]
  76. Feng, Y.L. Photosynthesis, nitrogen allocation and specific leaf area in invasive Eupatorium adenophorum and native Eupatorium japonicum grown at different irradiances. Physiol. Plant. 2008, 133, 318–326. [Google Scholar] [CrossRef]
  77. Brodribb, T.J.; Feild, T.S. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol. Lett. 2010, 13, 175–183. [Google Scholar] [CrossRef]
  78. Eamus, D.; Berryman, C.A.; Duff, G.A. Assimilation, stomatal conductance, specific leaf area and chlorophyll responses to elevated CO2 of Maranthes Corymbosa, a tropical monsoon rain-forest species. Aust. J. Plant Physiol. 1993, 20, 741–755. [Google Scholar] [CrossRef]
  79. Brodribb, T.J.; Jordan, G.J. Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytol. 2011, 192, 437–448. [Google Scholar] [CrossRef] [PubMed]
  80. Wen, Y.; Zhao, W.-l.; Cao, K.F. Global convergence in the balance between leaf water supply and demand across vascular land plants. Funct. Plant Biol. 2020, 47, 904–911. [Google Scholar] [CrossRef] [PubMed]
  81. Ferris, R.; Nijs, I.; Behaeghe, T.; Impens, I. Elevated CO2 and temperature have different effects on leaf anatomy of perennial ryegrass in spring and summer. Ann. Bot. 1996, 78, 489–497. [Google Scholar] [CrossRef]
  82. Reddy, K.R.; Robana, R.R.; Hodges, H.F.; Liu, X.J.; McKinion, J.M. Interactions of CO2 enrichment and temperature on cotton growth and leaf characteristics. Environ. Exp. Bot. 1998, 39, 117–129. [Google Scholar] [CrossRef]
  83. Beerling, D.J.; Chaloner, W.G. The impact of atmospheric CO2 and temperature change on stomatal density: Observations from Quercus robur Lammas leaves. Ann. Bot. 1993, 71, 231–235. [Google Scholar] [CrossRef]
  84. Luomala, E.M.; Laitinen, K.; Sutinen, S.; Kellomaki, S.; Vapaavuori, E. Stomatal density, anatomy and nutrient concentrations of Scots pine needles are affected by elevated CO2 and temperature. Plant Cell Environ. 2005, 28, 733–749. [Google Scholar] [CrossRef]
  85. Woodward, F.I. Stomatal numbers are sensitive to increases in CO2 from preindustrial levels. Nature 1987, 327, 617–618. [Google Scholar] [CrossRef]
  86. Woodward, F.I.; Kelly, C.K. The influence of CO2 concentration on stomatal density. New Phytol. 1995, 131, 311–327. [Google Scholar] [CrossRef]
  87. Ferris, R.; Long, L.; Bunn, S.M.; Robinson, K.M.; Bradshaw, H.D.; Rae, A.M.; Taylor, G. Leaf stomatal and epidermal cell development: Identification of putative quantitative trait loci in relation to elevated carbon dioxide concentration in poplar. Tree Physiol. 2002, 22, 633–640. [Google Scholar] [CrossRef] [Green Version]
Water 14 02828 g001 550
Figure 1. Replacement of native species by invasive Eupatorium adenophorum, forming a monoculture in the understory of a plantation in SW China. Photo credit: XiaoXue Mo.
Figure 1. Replacement of native species by invasive Eupatorium adenophorum, forming a monoculture in the understory of a plantation in SW China. Photo credit: XiaoXue Mo.
Water 14 02828 g001
Water 14 02828 g002 550
Figure 2. Leaf structural, hydraulic, and photosynthetic properties of Eupatorium adenophorum (invasive species) and E. fortunei (native species) under different treatments: control, elevated temperature (T↑), Elevated CO2 concentration (CO2↑), and elevated both temperature and CO2 concentration [(CO2 + T)↑]. (a) Leaf thickness; (b) leaf size; (c) leaf mass per area (LMA); (d) stomatal density; (e) guard cell length; (f) leaf vein density; (g) leaf hydraulic conductance (Kleaf); (h) maximum stomatal conductance; (i) δ13C; (j) intercellular CO2 concentration; (k) light-saturated photosynthetic rate per area (Aa); (l) photosynthetic rate per mass (Am). Bars topped by the same letter do not differ significantly between treatment types within the species. Bars topped by * differ significantly between species within the treatment type.
Figure 2. Leaf structural, hydraulic, and photosynthetic properties of Eupatorium adenophorum (invasive species) and E. fortunei (native species) under different treatments: control, elevated temperature (T↑), Elevated CO2 concentration (CO2↑), and elevated both temperature and CO2 concentration [(CO2 + T)↑]. (a) Leaf thickness; (b) leaf size; (c) leaf mass per area (LMA); (d) stomatal density; (e) guard cell length; (f) leaf vein density; (g) leaf hydraulic conductance (Kleaf); (h) maximum stomatal conductance; (i) δ13C; (j) intercellular CO2 concentration; (k) light-saturated photosynthetic rate per area (Aa); (l) photosynthetic rate per mass (Am). Bars topped by the same letter do not differ significantly between treatment types within the species. Bars topped by * differ significantly between species within the treatment type.
Water 14 02828 g002
Water 14 02828 g003 550
Figure 3. Leaf nutrient concentrations and nutrient relations of an invasive Eupatorium species (E. adenophorum) and a native Eupatorium species (E. fortunei) under different treatments: control, elevated temperature (T↑), elevated CO2 concentration (CO2↑), and elevated both temperature and CO2 concentration [(CO2 + T)↑]. (a) Leaf carbon concentration (C); (b) leaf nitrogen concentration (N); (c) leaf chlorophyll concentration (CHL); (d) leaf carbon: nitrogen (C/N); (e) photosynthetic nitrogen use efficiency (PNUE); (f) leaf construction cost (CC). Bars topped by the same letter do not differ significantly between treatment types within the species. Bars topped by * differ significantly between species within the treatment type.
Figure 3. Leaf nutrient concentrations and nutrient relations of an invasive Eupatorium species (E. adenophorum) and a native Eupatorium species (E. fortunei) under different treatments: control, elevated temperature (T↑), elevated CO2 concentration (CO2↑), and elevated both temperature and CO2 concentration [(CO2 + T)↑]. (a) Leaf carbon concentration (C); (b) leaf nitrogen concentration (N); (c) leaf chlorophyll concentration (CHL); (d) leaf carbon: nitrogen (C/N); (e) photosynthetic nitrogen use efficiency (PNUE); (f) leaf construction cost (CC). Bars topped by the same letter do not differ significantly between treatment types within the species. Bars topped by * differ significantly between species within the treatment type.
Water 14 02828 g003
Water 14 02828 g004 550
Figure 4. The relationship between stomatal conductance (gs) and light-saturated photosynthetic rate per leaf area Aa; (a), between Chlorophyll concentration (CHL) and Aa (b), between gs and intercellular CO2 concentration Ci (c), and between CHL and Ci (d). Each point represents a value of a leaf from a specific individual (one leaf per individual). Solid lines are regressions fitted to Eupatorium adenophorum, while dash lines are regressions fitted to E. fortunei. The relationship between Chlorophyll concentration and Aa in E. fortunei was described by an exponential function, while other relationships were fitted with linear regressions.
Figure 4. The relationship between stomatal conductance (gs) and light-saturated photosynthetic rate per leaf area Aa; (a), between Chlorophyll concentration (CHL) and Aa (b), between gs and intercellular CO2 concentration Ci (c), and between CHL and Ci (d). Each point represents a value of a leaf from a specific individual (one leaf per individual). Solid lines are regressions fitted to Eupatorium adenophorum, while dash lines are regressions fitted to E. fortunei. The relationship between Chlorophyll concentration and Aa in E. fortunei was described by an exponential function, while other relationships were fitted with linear regressions.
Water 14 02828 g004
Water 14 02828 g005 550
Figure 5. The relationship between leaf hydraulic conductance (Kleaf) and light-saturated maximum photosynthetic rate per leaf area (Aa). Points are means ± SE per treatment and species. The line indicate an exponential function. A linear mixed model (LMM) was also used to test the data with species as a random factor.
Figure 5. The relationship between leaf hydraulic conductance (Kleaf) and light-saturated maximum photosynthetic rate per leaf area (Aa). Points are means ± SE per treatment and species. The line indicate an exponential function. A linear mixed model (LMM) was also used to test the data with species as a random factor.
Water 14 02828 g005
Water 14 02828 g006 550
Figure 6. The relationship between leaf water use efficiency (indicated by δ13C) and maximum stomatal conductance (gs) across species and treatments. Points are means ± SE per species and treatment. A linear mixed model was fitted to the data with species as a random factor.
Figure 6. The relationship between leaf water use efficiency (indicated by δ13C) and maximum stomatal conductance (gs) across species and treatments. Points are means ± SE per species and treatment. A linear mixed model was fitted to the data with species as a random factor.
Water 14 02828 g006
Water 14 02828 g007 550
Figure 7. The relationship between stomatal density and leaf size across species and treatments. Points are means ± SE per treatment and species. A linear mixed model was fitted to the data with species as a random factor.
Figure 7. The relationship between stomatal density and leaf size across species and treatments. Points are means ± SE per treatment and species. A linear mixed model was fitted to the data with species as a random factor.
Water 14 02828 g007
Water 14 02828 g008 550
Figure 8. The relationship between leaf vein density and leaf hydraulic conductance (Kleaf) across species and treatments. A linear mixed model was fitted to the data with species as a random factor.
Figure 8. The relationship between leaf vein density and leaf hydraulic conductance (Kleaf) across species and treatments. A linear mixed model was fitted to the data with species as a random factor.
Water 14 02828 g008
Table
Table 1. The three-way-ANOVA results showing the effects of [CO2], temperature (T), species, and their interactions on all the structural and physiological traits.
Table 1. The three-way-ANOVA results showing the effects of [CO2], temperature (T), species, and their interactions on all the structural and physiological traits.
TCO2SpeciesT × CO2T × SpeciesCO2 × Species
Structure
Leaf thickness*ns*nsnsns
Leaf size****nsns
LMAns*nsnsnsns
Stomatal densityns***nsns
Guard cell lengthnsns*nsnsns
Leaf vein density**ns*nsns
Physiology
Kleaf*nsns*nsns
Maximum gs*nsnsnsnsns
δ13C***nsnsns
Cinsns*nsnsns
Aa*****ns
Am*****ns
Nutrition
C****ns*
Nns*ns*ns*
CHL*ns*ns*ns
C/Nns***ns*
PNUE**nsns**
Leaf CC****ns*
Notes: * indicates a significant effect or interaction, while ns indicates no significant effect or interaction; LMA: leaf mass per area; Kleaf: leaf hydraulic conductance; Ci: intercellular CO2 concentration; Aa: light-saturated photosynthetic rate per area; Am: photosynthetic rate per mass; C: Leaf carbon concentration; N: leaf nitrogen concentration; CHL: leaf chlorophyll concentration; C/N: leaf carbon: nitrogen ratio; PNUE: photosynthetic nitrogen use efficiency; CC: leaf construction cost.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Qi, J.-H.; Yan, Q.-S.; Tasnim, R.; Zhang, L.; Fu, P.-L.; Fan, Z.-X.; Zhang, Y.-J. Coordination among Water Transport, Photosynthesis and Nutrition under Climate Change: Stronger Responses of a Native than an Invasive Herb. Water 2022, 14, 2828. https://doi.org/10.3390/w14182828

AMA Style

Qi J-H, Yan Q-S, Tasnim R, Zhang L, Fu P-L, Fan Z-X, Zhang Y-J. Coordination among Water Transport, Photosynthesis and Nutrition under Climate Change: Stronger Responses of a Native than an Invasive Herb. Water. 2022; 14(18):2828. https://doi.org/10.3390/w14182828

Chicago/Turabian Style

Qi, Jin-Hua, Qiao-Shun Yan, Rafa Tasnim, Lan Zhang, Pei-Li Fu, Ze-Xin Fan, and Yong-Jiang Zhang. 2022. "Coordination among Water Transport, Photosynthesis and Nutrition under Climate Change: Stronger Responses of a Native than an Invasive Herb" Water 14, no. 18: 2828. https://doi.org/10.3390/w14182828

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop