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Article

Relationships between Xylem Transport, Anatomical, and Mechanical Traits at Organ Level of Two Cupressaceae Species

by
Jiang-Bo Xie
†,
Bo-Na Zhang
† and
Zhong-Yuan Wang
*
State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University, 666 Wu-Su Street, Lin-An District, Hangzhou 311300, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2022, 13(10), 1564; https://doi.org/10.3390/f13101564
Submission received: 19 July 2022 / Revised: 13 September 2022 / Accepted: 20 September 2022 / Published: 25 September 2022
(This article belongs to the Special Issue New Insights into Hydraulic Anatomy and Function of Trees)
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Abstract

:
Compared to arid regions, forests in humid regions can be more vulnerable to drought as they are not used to, and thus not adapted to, water stress. Therefore, it is vital to understand the drought responses of woodland species in humid areas. Xylem structures and functions of species growing in the humid regions are the key to their drought responses. Two Cupressaceae species (including three taxa: Sequoia sempervirens, Taxodium distichum and its variety Taxodium distichum var. imbricatum) grown in a mesic common garden were targeted, and their xylem hydraulic function (hydraulic conductivity, Ks; cavitation resistance, P50), anatomical structure (tracheid and pit structure), and mechanical support (wood density, WD; tracheid thickness-to-span ratio, Ttob) were measured. Likewise, we analyzed the differences in hydraulic function and anatomical structure of xylem in branches and roots, and the quantitative relationship between xylem water transport, anatomical structure, and mechanical support. Our results showed that roots had a higher hydraulic conductivity and a weaker cavitation resistance than branches. There was no safety–efficiency trade-off in the branches and roots within species. Tracheid mechanical support had a trade-off relationship with Ks or P50 (negative correlation appeared in branch Ks ~ WD and root Ks ~ Ttob of S. sempervirens, root P50 ~ Ttob of T. distichum var. imbricatum, and branch P50 ~ WD). There was no trade-off in anatomical structure, which led to no safety–efficiency trade-off in xylem function. Our results suggest that the two species exhibit both low efficiency and low safety in xylem, and that there is no safety–efficiency trade-off in branches and roots. The reason behind this is that the structural demand for high safety and high efficiency differs (i.e., the root Ks of S. sempervirens was strongly controlled by Dh; in contrast, the root P50 of S. sempervirens was strongly determined by tracheid density, N). Namely, the structural basis for a safety–efficiency trade-off does not exist and therefore trade-offs cannot be achieved.

1. Introduction

The surface of the Earth will keep warming, and shifting precipitation patterns will result in greater drought severity and frequency [1,2]. The ability of trees to grow, survive and recover from drought is strongly related to their xylem transport traits (hydraulic efficiency and cavitation resistance). These properties are largely determined by the anatomical structure of xylem [3,4,5,6,7,8,9]. It has been reported that 70% of 226 forest species from 81 sites around the world have narrow (<1 MPa) hydraulic safety margins, and therefore all forest biomes are equally vulnerable to drought [10]. Like woodland plants in arid regions, forest species in humid regions are also susceptible to hydraulic failure [10]. However, previous studies mainly focused on species from arid and semi-arid regions, rather than species from humid regions. In this sense, a comprehensive study focusing on plant xylem structures and physiological and ecological changes will deepen our understanding of plant responses to future climate change [11,12].
In evaluating xylem water transport there are two important hydraulic functional traits: specific sapwood conductivity (Ks), and the xylem water potential at a loss of 50% water conductivity (P50). The Ks directly reflects species hydraulic efficiency, and P50 represents the cavitation resistance. When xylem water potential falls below the P50, the water transport function of the xylem is markedly impaired, and the plant is exposed to considerable risk of accelerated cavitation leading to reductions in productivity, tissue damage, and ultimately death [10]. Cavitation resistance varies greatly between different taxa, even among related species growing under the same climatic conditions [13,14].
The trade-off between hydraulic efficiency and cavitation resistance in xylem is one of the internal mechanisms that restricts plant growth [15]. In plant xylem, “safe” hydraulic conducting systems usually come at the expense of lower conductivity, whereas “efficient” systems are more prone to cavitation [16]. Recently, there has been increasing evidence that the safety–efficiency trade-off does not exist, or that there is a weak trade-off between xylem safety and hydraulic efficiency in woodland plant species [10]. The trade-off at a series of anatomical traits, or even at a single anatomical trait, were potentially involved in a cause-and-effect explanation for the observed safety–efficiency trade-off in xylem functions [17,18,19]. However, the xylem structure–function relationships under no safety–efficiency trade-off have never been studied. Here, we hypothesized that the structural demands for high safety and high efficiency differ. Namely, the structural basis for a safety–efficiency trade-off does not exist, and thus trade-offs cannot be achieved.
In addition, recent evidence has shifted attention from the safety–efficiency trade-off [16,20] toward the trade-off between xylem safety, hydraulic efficiency, and mechanical strength [21,22]. Cavitation-resistant plants tend to have more negative sap pressures, and hence need stronger walls [23]. Lens et al. [19] confirmed that many species showed strong positive correlations between mean cavitation resistance, wood density and the thickness-to-span ratio of vessels [19,24,25,26]. The involvement of the thickness-to-span ratio and wood density in the trade-off is more ambiguous. Although these features can be linked to mean cavitation resistance, either causally or convergently, their link to hydraulic efficiency is less obvious. There seems to be a complex trade-off between these three traits [20], but there seems to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge when attempting to understand xylem evolution [27]. During drought stress, the branches and roots of plants respond by adopting adaptive strategies. The hydraulic segmentation hypothesis, proposed by Zimmermann [28], is that peripheral tissues are the first to become cavitated during drought, thereby protecting more important tissues such as stems. Furthermore, it has been shown that roots have a higher hydraulic efficiency, but are more vulnerable to cavitation than stems [29,30]. Bouche et al. [31] found that leaf and branch cavitation resistance in subtropical forest species was similar, with no segmentation. These inconsistent, and even contradictory, results suggest that it is necessary to further investigate the xylem hydraulic functions and structures at the organ level.
Most of the Cupressaceae species are found in warm and humid environments with sufficient rainfall and high relative humidity. In China, they are mostly distributed in the Yangtze River Basin, from the southern part of the Qinling mountains to the shore of the South China Sea. Previous physiological and ecological studies focused on the leaf epidermis and stem, leaf anatomy, stomatal conductance, net photosynthetic rate, respiratory rate, water potential, and other traits [32,33]. There have been few physiological studies on the Cupressaceae species’ responses to drought, especially ones based on hydraulic functional traits and the structural traits of xylem. The cavitation resistance of the xylem structure in Cupressaceae species may not be as strong as that for species growing in water-deficient environments. Therefore, Cupressaceae species in humid areas may face greater threats within the context of increased intensity and frequency of drought resulted from global change.
Burgess et al. [34] have revealed that hydraulic efficiency and safety of branch xylem both increased with height in Sequoia sempervirens. A recent study has also shown no safety–efficiency trade-off in Cupressaceae species [16]. Thus, in the current study, we measured xylem hydraulic function traits, anatomical structural traits, and the mechanical support of two Cupressaceae species (including three taxa: S. sempervirens, Taxodium distichum and its variety Taxodium distichum var. imbricatum). The differences in hydraulic function and anatomical structure of xylem in the branches and roots of the two species were compared, and the quantitative relationships between xylem water transport, anatomical structure and mechanical support were discussed. We evaluate the above-mentioned hypothesis: Can the anatomical basis of the xylem can be causally linked to the trade-off in xylem functions at the organ level and intraspecies level?

2. Materials and Methods

2.1. Site Description

The target plants (S. sempervirens, T. distichum and its variety T. distichum var. imbricatum) were grown in a mesic common garden at the Conifer Garden of Zhejiang A & F University, which is located at the Tianmu Mountain, Zhejiang Province (30°18′30″–30°24′55″ N, 119°24′47″–119°28′27″ E), China. The garden is in the hilly and mountainous area of the southeast coast of China, the north margin of the central subtropical zone, and the south margin of the north subtropical zone. Its climate is characterized by a transition from the central subtropical zone to the north subtropical zone [16]. The strong influence of oceanic warm and humid air currents has led to a climate with four distinct seasons, abundant rain (mean annual precipitation: 1420 mm, annual rain days: 159.2–183.1, annual average relative humidity: 76%–81%, frost-free period: 209–235 days), and suitable illumination (annual sunshine hours: 1550–2000 h, and annual solar radiation: 4460–3270 MJ∙m−2, mean annual temperature: 15.6 °C, ranging from 24 °C in July to 3 °C in January) [16,34].

2.2. Material Description

The experiment took place in October 2020. We chose to examine relatively closely related taxa (three taxa belong to two Cupressaceae species) from similar environments (Table 1), to help control for taxonomic and environmental effects on water stress tolerance and life history traits. We selected 10 to 15 plants in each taxon that had similar heights, diameters at breast height (DBH), and canopies (Table 1). Healthy branches in the middle of the south-facing crown of the tree (using a mobile scaffold; maximum scaffold height 15 m) were collected in the morning [35]. The length of the branches was more than 1 m, and there were twigs (1–2 years old) on the long branches that were used to measure the hydraulic conductivity. These twigs were 10–20 cm long and 4–6 mm in diameter. Roots (horizontal roots) with a diameter of 4–6 mm and a root length of 20–40 cm were collected at 10–20 cm below the soil surface without damaging the root tip. The sampled branches and roots were quickly placed in a black plastic bag containing wet paper (to prevent moisture loss and outside air from entering the cut catheter) and immediately taken back to the laboratory.

2.3. Hydraulic Conductivity and Cavitation Resistance in Branch/Root Xylem

The collected samples were placed in the dark for 60 min. Then they were cut under water and the incision was made smoothly. The lengths and diameters of the branch or root segments were measured with an electronic caliper. Then the samples were placed in the pressure chamber with both ends exposed, the pressure gauge was connected to the pressure chamber, and the near-axial end of the samples was connected to the xylem cavitation tester (XYL’ EM-Plus, Bronkhorst, Jacques Verniol, Montigny-les-Cormeilles, France) [36].
Before the hydraulic conductivity measurements, the samples were repeatedly flushed at high pressure (120 kPa) for 20 min (potential cavitation was removed). Afterwards, the maximum hydraulic conductivity (Khmax kg·s−1·MPa−1) of the stem or root segments was measured at low pressure (6 kPa) [37]. The measured solution contained 20 mmol·L−1 KCl + 1 mmol·L−1 CaCl2 [38]. Specific sapwood conductivity (Ks, kg·s−1·m−1·Mpa−1) was obtained by dividing Khmax by the sapwood cross-sectional sapwood area, and then multiplying by the length of the samples. The cross-sectional sapwood area was measured with a microscope (Leica DM3000, Leica, Wetzlar, Germany) and image-analysis software (ImageJ 1.8.0v for PC, W. Rasband, National Institute of Health, Bethesda, MD, USA).
Following that, the vulnerability curve was measured by the air injection method [38]. Pressure was applied for 5 min at the first set pressure to induce the formation of cavitation. The corresponding hydraulic conductivity (Khi, kg·s−1·Mpa−1) was measured. This process was repeated in increments of 0.2 or 0.3 Mpa (depending on the plant or organ) until the loss of hydraulic conductivity reached more than 90%. The formula for hydraulic conductivity loss percentage (PLC) is as follows: PLC = (1 − Khi/Kmax) × 100. The relationship curves between the pressure gradients and the corresponding PLC are the vulnerability curves of the samples. The Fitplc package in R was used to fit the vulnerability curves between PLC and water potential [39,40], and the corresponding P50 was extracted from the curve.

2.4. The Anatomical Structure of Xylem

Segments 3–5 cm long were cut from the branches that had been used to measure the vulnerability curves. These were then cut into four small segments (0.5 cm), and the root operation method was the same as the branches. They were stored in FAA fixed solution (a 5:5:50:40 concentrations, Formaldehyde, Glacial Acetic Acid, 95% ETOH and distilled Water). After the plant material was removed from the stationary solution, it was softened, washed, dehydrated, and embedded. Following this transverse and tangential sections of 10 μm thickness were cut using a sliding microtome. Then, the sections were stained for 15 s with a 1:2 mixture of safranin (0.5% in 50% ethanol) and alcian blue (1% in water), dehydrated in an ethanol series (50%, 75%, 96%), and made into permanent sections that were photographed under a Leica DM3000 microscope. The tracheid structures (transverse sections under 50× magnification) and pits (tangential sections under 400× magnification) were observed.
The tracheid areas (A, μm2), tracheid circumferences (L, μm), tracheid diameters (D, μm) and tracheid wall thicknesses (T, μm) were measured with ImageJ software in transverse sections. The pit membrane areas (Apm, μm2), pit aperture areas (Apa, μm2), pit membrane diameters (Dpm, μm), and pit aperture diameters (Dpa, μm) were measured in tangential sections. Then, the hydraulic diameters (Dh = ΣD5/ΣD4), tracheid densities (N = number of tracheids in the cross section/the area of cross section), aperture opening ratios (Fa = Dpa/Dpm), and pit densities (Np = number of pit holes in the longitudinal section/area of the longitudinal section) were calculated accordingly.

2.5. Mechanical Support

Three 3–5 cm segments were cut from the branches that had been used to measure the vulnerability curves and these were used to measure the wood density. The volume (fresh volume after removing the bark, V, cm3) of the sampling sections was measured by the drainage method and then dried at 75 °C for 48 h. The dry wood was weighted, and the wood density calculated using WD = M/V, g·cm−3 [41]. The thickness-to-span ratio was computed using the formula Ttob = (2T/D)2.

2.6. Statistical Analysis

The differences in traits among organs and taxa were tested by two-way ANOVA, followed by multiple comparisons of treatments by means of a Tukey test. The box and violin plots were constructed to seek variations in different traits of branches and roots of the three taxa. The intercorrelation of traits (data were loge-transformed to improve the linearity of the relationships) was tested by Pearson’s correlation coefficient.
Here, we aim to identify which structural traits are more important for the interpretation of functional traits. Furthermore, most studied structural traits are correlated with one another (collinear); redundancy analysis (RDA) corrected the collinearity among structural traits and simultaneously obtained a reasonable number of predictors variables (structural traits) that affected functional trait variability. Thus, we employed RDA to search the structure–function relationships. All variables were checked for normality and loge-transformed whenever required to ensure normality. The structural traits, which were significantly correlated with the functional traits used in the RDA, were stressed in the plots. The collinearity among structural traits was also corrected in RDA. The relative contribution of each structural trait to the functional traits was determined by the inertia from the conditional (or partial) effects, which show the amount of additional variation each variable contributes when it is added to the model [42].
All analyses were performed in R (version 3.5.3; R Core Team 2019) [43].

3. Results

3.1. Hydraulic Functional Traits

Ks and P50 were significantly affected by taxa, organs and their interactions (Table S1). The root Ks was always higher than the branch Ks (Figure 1A). Furthermore, the branch P50 for the three taxa were lower than those for the roots (Figure 1B; Table 2). Hydraulic conductivity was highest in the branches of T. distichum var. imbricatum and the roots of S. sempervirens. The cavitation resistance was strongest in the branches of S. sempervirens and in the roots of T. distichum.

3.2. Xylem Anatomical Structure

All structural traits were significantly affected by taxa (except for Dpa), organs (except for T and Dpa), and their interactions (except for T; Table S1).
The Dh of the three taxa (Figure 2) were larger in the roots than in the branches (branch Dh: 17.15–28.60 μm, root Dh: 29.23–34.50 μm; Table 2; Figure 3A), but the N showed the opposite tendency (branch N: 2114.44–3006.42 mm−2, root N: 1000.62–1462.34 mm−2; Table 2; Figure 3C). The root T in S. sempervirens was clearly thicker than the branches (branch T: 3.44 μm, root T: 3.95 μm; Table 2), but there was very little difference in T. distichum var. imbricatum (branch T: 2.34 μm, root T: 2.38 μm; Table 2) and T. distichum (branch T: 2.28 μm, root T: 2.16 μm; Table 2; Figure 3B). Dh was greatest for the roots of T. distichum and branches of S. sempervirens. In terms of T and N, the branches and roots of S. sempervirens were all the greatest.
The root Dpa of T. distichum var. imbricatum (branch Dpa: 3.82 μm2, root Dpa: 4.32 μm2; Table 2) and T. distichum (branch Dpa: 4.04 μm2, root Dpa: 4.15 μm2; Table 2) were larger than that of the branches, while S. sempervirens (branch Dpa: 3.92 μm2, root Dpa: 3.77 μm2; Table 2) showed the opposite tendency (Figure 4A). The Dpm of the three taxa were larger in the roots than in the branches (branch Dpm:9.96–10.69 μm2, root Dpm: 10.39–12.69 μm2; Table 2; Figure 4B), and the Fa and Np of the branches were larger than those of roots in the three taxa (branch Fa: 0.37–0.40, root Fa: 0.11–0.17, branch Np: 3149.25–4479.59 mm2, root Np: 2583.25–3436.32 mm2; Table 2; Figure 4C,D). There was no significant difference in the branch Dpa between the three taxa, but the root Dpa of T. distichum var. imbricatum was larger than that of the other two taxa. The Dpm in both branches and roots of S. sempervirens was the greatest. The Fa was greatest in the branches of T. distichum and in the roots of T. distichum var. imbricatum, while the Np was greatest in the branches of T. distichum var. imbricatum and in the roots of T. distichum.
The WD and the Ttob were greater in the branches than in the roots for all three taxa (branch WD: 0.36–0.41 g cm−3, root WD: 0.25–0.38 g cm−3, branch Ttob: 0.03–0.10, root Ttob: 0.01–0.07; Table 2; Figure 5A,B).
The WD of the T. distichum var. imbricatum branches was the highest, followed by S. sempervirens and T. distichum, and the Ttob of S. sempervirens was the largest, followed by T. distichum var. imbricatum and T. distichum. In the roots, S. sempervirens had the highest WD, followed by T. distichum and T. distichum var. imbricatum, and S. sempervirens had the largest Ttob, followed by T. distichum var. imbricatum and T. distichum.

3.3. Quantitative Relationship between Functional Traits and Xylem Anatomical Structure

At the intraspecific level, Ks and P50 in branches and roots of S. sempervirens were positively correlated (branch: r2 = 0.53, p < 0.001, Figure S1A; root: r2 = 0.26, p = 0.11, Figure S1D). Weak positive correlations were found between Ks and P50 in branches and roots of T. distichum, respectively (branch: r2 = 0.18, p = 0.14, Figure S1B; root: r2 = 0.25, p = 0.06, Figure S1E). In T. distichum var. imbricatum, the r2 between Ks and P50 was only 0.01 in branches (p = 0.77, Figure S1C), and there was a significant positive correlation between Ks and P50 in roots (r2 = 0.38, p = 0.01, Figure S1F). These results indicated that there was no efficiency–safety trade-off in the branch and root hydraulic systems.
The structural traits had a complex relationship with functional traits at the intraspecific level. In S. sempervirens, the T, Dpa, and Fa were positively correlated with branch Ks, and branch P50, and Dh and WD were negatively correlated with branch Ks and branch P50 (Figure 6A). In roots, when Dh and N increased, Ks and P50 also increased (Figure 6D).
In T. distichum var. imbricatum, Dh, N, Dpm, and Fa had the same positive or negative effect on Ks and P50 in roots (Figure 6F), and Dpm was positively correlated with branch P50 in branches (Figure 6C). In T. distichum, only the Np was positively correlated with root P50 (Figure 6E).
In S. sempervirens, branch Ks was controlled by Dh (72.4%, p = 0.002) and Dpa (14.6%, p = 0.04), and Dh (43.9%, p = 0.07) made the largest contribution to branch P50. The Dh (86.3%, p = 0.002) had a significant influence on root Ks, but N (58.5%, p = 0.006) contributed the most to root P50 (Figure 7A). In T. distichum, T (29.1%, p = 0.09) and the Ttob (28.5%, p = 0.10) contributed the most to branch Ks and P50, respectively, whereas N (48.2%, p = 0.024) and Np (33.5%, p = 0.04) had the greatest effect on root Ks and P50, respectively (Figure 7B). In T. distichum var. imbricatum, the Np (30.9%, p = 0.06) explained a large proportion of the branch Ks, but the Dpm contributed the most to branch P50 (51.2%, p = 0.008) and root Ks (65.2%, p = 0.006). The Fa (50.3%, p = 0.01) and the Ttob (21.1%, p = 0.04) also had significant effects on root P50 (Figure 7C).

4. Discussion

Our results indicated that the three taxa exhibited both low efficiency and low safety in xylem, and that there was no safety–efficiency trade-off in branches and roots. The reason behind this is that the structural requirement for safety and efficiency differs. Namely, the structural basis for a safety–efficiency trade-off does not exist, and thus trade-offs cannot be achieved.

4.1. Differences between Branch and Root Hydraulic Functional Traits

The hydraulic conductivity of the roots in the three taxa was higher than that of the branches (Figure 1A). The absorption of water by roots is the key link in the soil–plant–atmosphere continuum [2,44,45]. When absorbed, water is transported toward branches and leaves to meet plant transpiration and photosynthetic requirements [16], which ensure the normal and healthy growth of plants.
Generally, roots are more vulnerable to drought than branches in angiosperms and conifer species [36,46,47]. This was confirmed by our results (Figure 1B). The drought-resistance strategy of a xerophytic tree such as Haloxylon ammodendron (C.A. Mey.), which is widely distributed across the desert regions of Asia and Africa, is to preferentially allocate photoassimilates to roots to develop an efficient root system to supply water [48,49]. The preservation of roots under severe drought improves cavitation recovery after drought [50]. When faced with more severe and frequent droughts, trees in humid regions are potentially at higher risk of hydraulic failure because they have weaker xylem cavitation resistances (especially root resistance) than species that have been growing for a long time in water shortage environments. Therefore, studies on the drought adaptation mechanisms of plants in humid regions are highly desired.

4.2. Efficiency–Safety Trade-Off

The results from this study suggested that there was no safety–efficiency trade-off in the branches and roots of the three taxa (Figure 2A–F). Gleason et al. found many species with both low efficiency and low safety (gymnosperms: 0 < Ks < 2 kg·s−1·m−1·MPa−1; −6 < P50 < 0 MPa, respectively) [27]. The Ks and P50 of the branches from the three taxa have been compared with those for Pinaceae plants (0.02 < Ks < 1.32 kg·s−1·m−1·MPa−1; −5.61 < P50 < −0.60 MPa) [27,51,52]. The results from this study suggested that the three taxa are both low-safety and low-efficiency species.
Previous studies have proposed several mechanisms to explain the phenomenon (low-safety and low-efficiency species). Building redundancy [53] or new xylem [23,27] into the vascular network can maintain water supply to leaves despite accumulation of cavitation. Some species evolve to refill the cavitation conduits [54]. The “fast–slow” plant economics spectrum suggests that “slow” species acquire and use resources slowly, and therefore only need low efficiency and low safety [20,41,55]. Furthermore, a number of studies suggest that low-safety and low-efficiency species have an anatomical basis for high efficiency trade-off against important traits other than safety, e.g., mechanical support in xylem [20,27]. Likewise, our results showed that pattern. In S. sempervirens, branch Ks was significantly negatively correlated with WD (Figure 6A), and root Ks was negatively correlated with Ttob (Figure 6D). The correlation coefficient between Ttob and P50 was −0.51 (Figure 6F) in root of T. distichum var. imbricatum. Moreover, the correlation coefficient between wood density and T. distichum branch P50 was −0.4 (Figure 6B). These results suggested that there was a trade-off between water transport and mechanical support, and they were consistent with the results of Pratt and Jacobsen [20].
Furthermore, the trade-offs for a series of anatomical traits or even single traits are potentially involved in a cause-and-effect explanation for the observed safety–efficiency trade-off. Lens et al. analyzed the trait correlation network between hydraulic function and the anatomical traits from light, scanning, and transmission electron microscopy of seven Acer taxa, and provided a comprehensive perspective for the study of structure–function relations in angiosperms [19]. Almost all measured anatomical traits are the cause-and-effect basis of the safety–efficiency trade-off. In our study, no trade-off was found in both branch and root within the three taxa. In S. sempervirens, Dh, T, Dap, and Fa were positively correlated with branch P50 and branch Ks (Figure 6A). Similarly, there was a significant tendency for root Ks and P50 to rise as Dh and N increased (Figure 6D). The same phenomenon also occurred in the branch and root xylem of T. distichum var. imbricatum and T. distichum (Figure 6B,C,E,F).
Redundancy analysis also indicated that the structural demands for high efficiency in branches and roots within species were different from those for high safety (i.e., the root Ks of S. sempervirens was strongly controlled by Dh, in contrast, the root P50 of S. sempervirens was strongly determined by tracheid density, N). Thus, the xylem anatomy contributed to safety and efficiency independently, rather than in opposition to each other. As structural requirements of hydraulic conductivity and cavitation resistance were different, functional safety–efficiency trade-off hypothesis cannot be achieved. Up till now, this independence of structural requirements has been found only in the Cupressaceae species we studied. However, this independent species-specificity greatly increases our understanding on the evolution of the hydraulic conducting system [56].

5. Conclusions

We compared the differences and the quantitative relationships of hydraulic function and anatomical structure of xylem at organ level. Our results suggest that there is no safety–efficiency trade-off in the xylem of branches and roots. The reason behind this is that the structural basis for a safety–efficiency trade-off does not exist, and thus trade-offs cannot be achieved. Interrelationships in xylem functions are determined by the relationship between traits in the xylem vascular bundle network. The analysis of complex, multivariate relationships in networks is helpful to accurately quantify xylem function and water adaptation mechanisms in plants. The current study was limited to branch and root xylem hydraulic functional traits and their relationship to xylem anatomical structure. More systematic quantitative analyses of this relationship are required at the whole-plant level (including roots, stems, branches, petioles, and leaves) in order to fully understand the hydraulic system. The trade-off and correlations we observed in the Cupressaceae species may not necessarily exist in other groups. Further studies are required in different plant groups.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f13101564/s1, Figure S1: Relationships between Ks and P50 for the branches and roots within Taxa; Table S1: Two-way ANOVA of traits.

Author Contributions

Z.-Y.W. and J.-B.X. planned and designed the research. B.-N.Z. and J.-B.X. conducted field work and performed the experiments. J.-B.X. and Z.-Y.W. analyzed the data and wrote the paper. B.-N.Z. revised the paper. All authors have read and agreed to the published version of the manuscript.

Funding

National Natural Science Foundations of China (31770651, 41730638 and 31901280).

Data Availability Statement

The data that support this study will be shared upon reasonable request to the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Species-specific sapwood conductivity (Ks), (A) and water potential at 50% loss of hydraulic conductivity (P50), (B) in the branches and roots. P50 values were converted from negatives to positives. Different letters indicate a significant difference between means at p < 0.05 (multiple comparisons of treatments by means of a Tukey test).
Figure 1. Species-specific sapwood conductivity (Ks), (A) and water potential at 50% loss of hydraulic conductivity (P50), (B) in the branches and roots. P50 values were converted from negatives to positives. Different letters indicate a significant difference between means at p < 0.05 (multiple comparisons of treatments by means of a Tukey test).
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Figure 2. Tracheid and pit photographs of the branch and root xylem in the three taxa (×400). Scale: 100 μm. (A): S. sempervirens branch tracheids; (B): S. sempervirens branch pits; (C): S. sempervirens root tracheids; (D): S. sempervirens root pits; (E): T. distichum branch tracheids; (F): T. distichum branch pits; (G): T. distichum root tracheids; (H): T. distichum root pits; (I): T. distichum var. imbricatum branch tracheids; (J): T. distichum var. imbricatum branch pits; (K): T. distichum var. imbricatum root tracheids; (L): T. distichum var. imbricatum root pits.
Figure 2. Tracheid and pit photographs of the branch and root xylem in the three taxa (×400). Scale: 100 μm. (A): S. sempervirens branch tracheids; (B): S. sempervirens branch pits; (C): S. sempervirens root tracheids; (D): S. sempervirens root pits; (E): T. distichum branch tracheids; (F): T. distichum branch pits; (G): T. distichum root tracheids; (H): T. distichum root pits; (I): T. distichum var. imbricatum branch tracheids; (J): T. distichum var. imbricatum branch pits; (K): T. distichum var. imbricatum root tracheids; (L): T. distichum var. imbricatum root pits.
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Figure 3. Hydraulic diameters (Dh), (A), tracheid wall thickness (T), (B), and tracheid density (N), (C) of the branches and roots in the three taxa. Different letters indicate a significant difference between means at p < 0.05 (multiple comparisons of treatments by means of a Tukey test).
Figure 3. Hydraulic diameters (Dh), (A), tracheid wall thickness (T), (B), and tracheid density (N), (C) of the branches and roots in the three taxa. Different letters indicate a significant difference between means at p < 0.05 (multiple comparisons of treatments by means of a Tukey test).
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Figure 4. Pit aperture diameters (Dpa), (A), pit membrane diameters (Dpm), (B), aperture opening ratio (Fa), (C), and pit density (Np), (D) of the branches and roots the in three taxa. Different letters indicate a significant difference between means at p < 0.05 (multiple comparisons of treatments by means of a Tukey test).
Figure 4. Pit aperture diameters (Dpa), (A), pit membrane diameters (Dpm), (B), aperture opening ratio (Fa), (C), and pit density (Np), (D) of the branches and roots the in three taxa. Different letters indicate a significant difference between means at p < 0.05 (multiple comparisons of treatments by means of a Tukey test).
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Figure 5. Wood density (WD), (A) and thickness-to-span ratio (Ttob), (B) of the branches and roots in the three taxa. Different letters indicate a significant difference between means at p < 0.05 (multiple comparisons of treatments by means of a Tukey test).
Figure 5. Wood density (WD), (A) and thickness-to-span ratio (Ttob), (B) of the branches and roots in the three taxa. Different letters indicate a significant difference between means at p < 0.05 (multiple comparisons of treatments by means of a Tukey test).
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Figure 6. Correlations between the xylem structural and functional traits (Ks and P50) in the branches and roots within taxa. (A): Branch of S. sempervirens; (B): Branch of T. distichum; (C): Branch of T. distichum var. imbricatum; (D): Root of S. sempervirens; (E): Root of T. distichum; (F): Root of T. distichum var. imbricatum. Ks: Specific conductivity; P50: Water potential in the xylem of branches and roots corresponding to a loss in water conductivity of 50%; Dh: Hydraulic diameter; T: Tracheid wall thickness; N: Tracheid density; Dpa: Pit aperture diameter; Dpm: Pit membrane diameter; Fa: Aperture opening ratio; Np: Pit density; WD: Wood density; and Ttob: Thickness-to-span ratio. *, 0.01 < p < 0.05; **, p < 0.01.
Figure 6. Correlations between the xylem structural and functional traits (Ks and P50) in the branches and roots within taxa. (A): Branch of S. sempervirens; (B): Branch of T. distichum; (C): Branch of T. distichum var. imbricatum; (D): Root of S. sempervirens; (E): Root of T. distichum; (F): Root of T. distichum var. imbricatum. Ks: Specific conductivity; P50: Water potential in the xylem of branches and roots corresponding to a loss in water conductivity of 50%; Dh: Hydraulic diameter; T: Tracheid wall thickness; N: Tracheid density; Dpa: Pit aperture diameter; Dpm: Pit membrane diameter; Fa: Aperture opening ratio; Np: Pit density; WD: Wood density; and Ttob: Thickness-to-span ratio. *, 0.01 < p < 0.05; **, p < 0.01.
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Figure 7. Interpretation of the relationships between structural traits and functional traits (Ks on P50) in the xylem of the branches and roots within taxa after the redundancy analysis. (A): S. sempervirens; (B): T. distichum; (C): T. distichum var. imbricatum. *, 0.01 < p < 0.05; **, p < 0.01.
Figure 7. Interpretation of the relationships between structural traits and functional traits (Ks on P50) in the xylem of the branches and roots within taxa after the redundancy analysis. (A): S. sempervirens; (B): T. distichum; (C): T. distichum var. imbricatum. *, 0.01 < p < 0.05; **, p < 0.01.
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Table
Table 1. Habitat and structural or densitometric characteristics of the target Cupressaceae taxa.
Table 1. Habitat and structural or densitometric characteristics of the target Cupressaceae taxa.
TaxaAgeHeight (m)DBH (cm)Canopy (m)AgrotypepHElevation (m)Slope (°)
S. sempervirens20.79 ± 0.6417.21 ± 0.4618.14 ± 0.312.70 ± 0.09Red soil5.45 ± 0.1340.43 ± 0.140.62 ± 0.07
T. distichum16.89 ± 0.3123.26 ± 0.4816.73 ± 0.472.45 ± 0.09Red soil5.25 ± 0.1040.42 ± 0.120.48 ± 0.03
T. distichum var. imbricatum17.28 ± 0.5423.78 ± 0.3417.44 ± 0.462.61 ± 0.09Red soil5.35 ± 0.1242.33 ± 0.511.83 ± 0.06
Table
Table 2. Summary of xylem functional traits and anatomical structure of the target Cupressaceae taxa.
Table 2. Summary of xylem functional traits and anatomical structure of the target Cupressaceae taxa.
TaxaOrganKs
(kg·s−1·m−1·Mpa−1)		P50
(-Mpa)		Dh
(μm)		T
(μm)		N
(103·mm−2)		Dpa
(μm)		Dpm
(μm)		FaNp
(103·mm−2)		WD
(g·cm−3)
S. sempervirensBranch0.52 ± 0.046.97 ± 0.7728.60 ± 3.563.44 ± 0.103006.42 ± 73.383.92 ± 0.1110.69 ± 0.240.37 ± 0.013149.25 ± 102.710.39 ± 0.01
Root8.25 ± 0.190.60 ± 0.0229.23 ± 1.093.95 ± 0.161462.34 ± 46.203.77 ± 0.1112.69 ± 0.400.11 ± 0.002583.25 ± 50.640.38 ± 0.01
T. distichumBranch0.78 ± 0.021.73 ± 0.1619.51 ± 0.392.28 ± 0.092114.44 ± 71.544.04 ± 0.149.96 ± 0.260.40 ± 0.013512.81 ± 139.010.36 ± 0.01
Root1.19 ± 0.111.14 ± 0.0934.50 ± 0.882.16 ± 0.111056.49 ± 21.564.15 ± 0.0910.39 ± 0.310.16 ± 0.003436.32 ± 103.600.32 ± 0.01
T. distichum var.
imbricatum		Branch1.23 ± 0.061.66 ± 0.1717.15 ± 0.682.34 ± 0.112648.80 ± 80.723.82 ± 0.119.71 ± 0.220.39 ± 0.014479.59 ± 151.750.41 ± 0.01
Root1.36 ± 0.130.59 ± 0.0733.80 ± 0.702.38 ± 0.081000.62 ± 30.124.32 ± 0.1411.02 ± 0.280.17 ± 0.013373.53 ± 73.850.25 ± 0.01
Ks: Species-specific sapwood conductivity; P50: Water potential at 50% loss of hydraulic conductivity; Dh: Hydraulic diameters; T: Tracheid wall thickness; N: Tracheid density; Dpa: Pit aperture diameters; Dpm: Pit membrane diameters; Fa: Aperture opening ratio; Np: Pit density; WD: Wood density (WD).
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Xie, J.-B.; Zhang, B.-N.; Wang, Z.-Y. Relationships between Xylem Transport, Anatomical, and Mechanical Traits at Organ Level of Two Cupressaceae Species. Forests 2022, 13, 1564. https://doi.org/10.3390/f13101564

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Xie J-B, Zhang B-N, Wang Z-Y. Relationships between Xylem Transport, Anatomical, and Mechanical Traits at Organ Level of Two Cupressaceae Species. Forests. 2022; 13(10):1564. https://doi.org/10.3390/f13101564

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Xie, Jiang-Bo, Bo-Na Zhang, and Zhong-Yuan Wang. 2022. "Relationships between Xylem Transport, Anatomical, and Mechanical Traits at Organ Level of Two Cupressaceae Species" Forests 13, no. 10: 1564. https://doi.org/10.3390/f13101564

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