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. 2025 Aug 27;25:1141. doi: 10.1186/s12870-025-07006-7

Responses of biomass and non-structural carbohydrates to soil moisture gradient of two Carex species in an alpine meadow in Southeast Qinghai-Xizang Plateau

Zhong-kui Li 1, Da-cai Zhang 1,✉
PMCID: PMC12382178  PMID: 40866854

Abstract

Background

Changes in soil moisture content affect the variations in biomass and non-structural carbohydrates (NSC) in plants; different species may have different response strategies. In the alpine meadow of Dongda Mountain in Southeast Qinghai-Xizang Plateau, five quadrats were set up respectively along the soil moisture gradient which evolved from the drought habitat near the alpine screes to the wet habitat in the ravine. According to the natural distribution pattern of the two Carex populations, C. parvula and C. alatauensis are co-dominant species in this region.

Results

Root biomass constituted the greatest proportion of total biomass of two Carex species. The root biomass of C. alatauensis, stem biomass of C. parvula and leaf, above-ground, below-ground and whole plant biomass of two species all increased with the increase of soil moisture content (P < 0.05). The NSC, soluble sugar (SS) and starch concentrations in roots of C. parvula all increased with the increase of soil moisture content (P < 0.05), but those in roots of C. alatauensis reached an optimum, and then declined with the increase of soil moisture content (P < 0.05). The NSC and SS concentrations in stems and leaves of C. parvula reached an optimum, and then declined with the increase of soil moisture content respectively (P < 0.01), but those of C. alatauensis declined first, and then increased with the increase of soil moisture content (P < 0.05). The dry matter (DM) allocation of NSC in leaves of both species was the lowest, and the DMNSC, DMSS and DMstarch in organs and whole plant all increased with the increase of soil moisture content (P < 0.05), except those in roots and leaves of C. alatauensis.

Conclusions

The SS concentration and DMstarch in roots of C. parvula and those in leaves of C. alatauensis were the main contributors of the two species to combat soil moisture changes. Both species kept the highest biomass allocation in roots and increased SS/Starch in leaves to adapt to drought habitat. In conclusion, the asymmetric responses of biomass and NSC in organs were exhibited to adapt to soil moisture changes in an alpine meadow.

Keywords: Soluble sugar, Starch, Dry matter, Carex parvula, C. alatauensis

Highlight

The variations and allocation patterns between two Carex species in an alpine meadow in Southeast Qinghai-Xizang Plateau and soil moisture content differ in biomass and non-structural carbohydrates.

Introduction

Plant growth is closely related to soil moisture content [37], because the changes of soil moisture content can affect the photosynthesis process and efficiency of plants [10], and thereby influence the synthesis [23] and transport [24, 29] of substances, and form the corresponding allocation [41] and storage patterns [33, 49]. For instance, the reduction of soil moisture inhibited the photosynthesis of Quercus macrocarpa and reduced the non-structural carbohydrates (NSC) concentrations of its organs, which has been confirmed in the tracking study of carbon isotope [38], indicating that changes in soil moisture significantly affect the carbon assimilation process of plants. The biomass of plants integrates the effects of soil moisture variations on the growth and adaptation [18], which is the result of all physiological and biological responses of plants in different habitats [8]. For example, the above-ground biomass (AB), below-ground biomass (BB) and whole plant biomass (WP-B) of Medicago sativa were significantly affected by the decrease of soil moisture. The BB/AB of M. sativa increased first and then decreased, and the yield was improved by prompting the below-ground biomass allocation when compared to the proportion of above-ground biomass [16]. It might due to the allocation pattern of biomass which enhanced the water use efficiency [24]. The drought tolerance of Pinus tabulaeformis also significantly improved by increasing BB/AB level [22], which means plants usually promote the below-ground biomass allocation and reduce the above-ground biomass allocation to combat water deficit. Then, different biomass allocation patterns occurred under this kind of biological adjustment.

Non-structural carbohydrates are important energy substances for plant growth and metabolism, of which more than 90% are soluble sugars (SS) and starch [12, 27]. Soil moisture affects the variations of NSC in plants, but the species-specific responses and the underlying physiological mechanisms regulating NSC dynamics under varying soil moisture conditions are still unclear. Thus the relationship between NSC and soil moisture and the response mechanisms of different species still needs to be further studied [44, 50]. The decrease of soil moisture content caused the variations of NSC concentrations and allocations in plants [30] which can affect plant physiological activities [7], such as photosynthesis, substance synthesis and transport [20]. Starch mainly plays a storage role and could be converted into SS when water is reduced [11, 36]. SS concentration in plant tissues increased and directly affected osmotic regulation with the decrease of soil moisture [44]. Thus, the increase of SS concentration in above-ground tissue of a plant can enhance its tolerance under drought conditions [2]. For example, the decrease in soil moisture significantly increased the SS concentrations in the main branches of trees [14]. M. sativa root system had strong drought tolerance but not flood tolerance which was more sensitive to excessive water. Compared with water deficit, excessive soil moisture reduced soil permeability and affected root respiration [16]. Other studies showed that severe or prolonged drought disrupted the carbon balance, and that the reduction of NSC dry matter (DMNSC) led to carbon starvation and plant death [10, 24], which means the total amount of available NSC for conversion in the body is critical for plant growth and death [4]. It can be seen that the production, storage and metabolism of NSC have a great impact on plant growth and environmental responses [23].

The NSC in plants had different variations and allocation patterns among species and organs [30, 44]. For example, the concentrations and allocation patterns of NSC and its components in three temperate tree species were found to have inter-specific variations and significant differences among tree species and tissues [51]. The study on the variations of NSC in seven warm temperate deciduous broad-leaved trees showed that the species type had significant effects on the NSC concentrations in branches and leaves [44]. The concentrations of SS and starch in the roots, branches and leaves of Picea meyeri increased with decreasing soil moisture, except starch in the leaves [50]. At the whole plant level, the decrease of soil moisture significantly decreased the whole plant NSC, SS and starch concentrations of Pinus radiata, but there was no significant change in the whole plant NSC concentration of Eucalyptus globulus and E. smithii, while the starch concentration decreased significantly [25]. Besides, the growth of Q. mongolica was slow but the concentration of NSC in roots was very high in arid habitat [44], and the high stress resistance of Carex alatauensis was directly related to the high concentration of NSC in the root collar [55]. Generally speaking, plants tend to invest SS in the above-ground part, while starch is mainly stored in the trunk, and this kind of distribution pattern leads to a balanced distribution of NSC among different organs [51].

The alpine meadow ecosystem in Qinghai-Xizang Plateau can be an indicator of climate change, because it actively responds to global change by influencing energy-water exchanges and modulating carbon cycle dynamics [40]. Carex in the Cyperaceae family are cold-mesophilic, wet-mesophilic and dry-mesophilic subterranean budding herbaceous plants with short rhizomes, adapt to different climatic types [45]. C. alatauensis and C. parvula both highly resistant species, are the establishment species of Carex meadow [19]. C. alatauensis usually grows in habitat with moderate soil moisture [6], it has a weak ability to adapt to arid habitat. Meanwhile, C. parvula is a dry-mesophilic and drought-tolerant plant with a strong ability to adapt to arid habitat [45]. This paper aims to study the dynamics of biomass and NSC of two Carex species with soil moisture content change, and attempt to answer the following scientific issues: (i) What are the variations and allocation patterns of biomass in these two Carex species with soil moisture content changes? (ii) Are NSC concentration variations and dry matter allocation patterns of two Carex species affected by soil moisture content changes? (iii) Is there any inter-specific difference in the main contribution indexes of NSC in the two Carex species in response to soil moisture content changes? Here we also formulated a hypothesis that the biomass, NSC concentration and dry matter will be decreased significantly with the decrease of soil moisture content and these two Carex species may have different ecological response strategies.

Materials and methods

Study sites and experimental design

The research site was located in the alpine meadow near Dongda Mountain bealock, southeast Qinghai-Xizang Plateau, with the geographical coordinates of 29°71′38″−29°71′92″N, 98°04′59″−98°04′66″E, and the altitude of the bealock is 5008 m. The terrain of the study site is concave, the terrain of ravine is flat, the stream runs through it, and the habitat is wet; sloping elevation on both sides and habitat tends to be drought [48, 52]. The seasonal distribution of precipitation in this area throughout the year is uneven. The evaporation is large while the relative humidity is relatively low. The annual average precipitation is 400–600 mm, mainly concentrated from May to October, accounting for about 80% of the annual precipitation [35]. C. parvula and C. alatauensis were the dominant species in the phytocoenosium. According to the natural distribution zone of the two Carex populations, five 5 × 5 m2 quadrats were set up respectively, from the droughty habitat near the alpine screes to the wet habitat in the ravine. The Cp4 and Cp5 quadrats of C. parvula are overlap with Ca1 and Ca2 quadrats of C. alatauensis, respectively, and the two Carex species are co-dominant species in this region (Table 1). In dry season (October), the TS-TW soil temperature and humidity rapid measuring instrument was used to measure the soil volumetric water content among 5 sample points in each quadrat, and the average value was taken as the soil moisture content of the quadrat.

Table 1.

Quadrats information

No. of quadrats Soil moisture content (%) Altitude (m) Longitude and latitude Dominant species
Cp1 10.17 4868.6 29°71′38″N, 98°04′64″E C. parvula
Cp2 15.60 4816.5 29°71′58″N, 98°04′60″E C. parvula
Cp3 20.63 4801.5 29°71′66″N, 98°04′64″E C. parvula
Cp4, Ca1 25.00, 23.12 4798.1, 4816.7 29°71′68″N, 98°04′62″E, 29°71′58″N, 98°04′60″E

C. parvula,

C. alatauensis
Cp5, Ca2 30.37, 32.64 4802.1, 4803.6 29°71′66″N, 98°04′61″E, 29°71′64″N, 98°04′59″E

C. parvula,

C. alatauensis
Ca3 42.62 4800.9 29°71′65″N, 98°04′59″E C. alatauensis
Ca4 52.56 4793.0 29°71′92″N, 98°04′66″E C. alatauensis
Ca5 63.04 4797.1 29°71′69″N, 98°04′62″E C. alatauensis
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Plant sample collection and processing

Plant identification was confirmed, and voucher specimens were deposited in the Southwest Forestry University herbarium, which is publicly available. Compared with C. parvula, C. alatauensis has larger individual plant, thus, a larger sampling area is required. Considering the differences in morphological characteristics between these two Carex species, we improved the sampling tool and customized the cutting ring (d = 10 cm, h = 26 cm). Soil boring auger (d = 3.5 cm) was used to extract 15 cm soil column of C. parvula; customized cutting ring (d = 10 cm) was used to extract 10 cm soil column of C. alatauensis, and 5 soil columns were extracted from each quadrat. When taking NSC assay materials, one 20 × 20 × 15 cm3 soil block was randomly excavated in each soil moisture gradient quadrat to obtain healthy plants by total harvest method. After litters and other impurities are removed out, materials are cleaned up in 80 mesh nylon net and separated into roots, stems and leaves with scissors. All materials are dried with a unit heater and stored in a ziplock bag containing discolored silicone. Take all materials back to the laboratory and kiln dry at 80 ℃ to constant weight in drying oven (at least 72 h). The biomass was weighed with an analytical balance with the accuracy of 0.0001 g, and the NSC assay materials were pulverized and then stored in a ziplock bag containing discolored silicone for later experiments.

Measurement of NSC concentration

The SS and starch concentrations were determined by modified phenol concentrated sulfuric acid method [1]. Extraction and concentration determination of SS: Weighing 50 mg powder sample with analytical balance, ground and homogenized in mortar with distilled water (add a small amount of SiO2), and then rinse and pour into centrifuge tube (10 ml) to make the sample liquid up to 8 ml. Boiled in a water bath kettle for 30 min and centrifuged at 4000 r/min for 10 min. After centrifugation, pour the extracting solution into a volumetric flask and metered the volume to 100 ml. Adding 1 ml distilled water, 1 ml 9% phenol and 5 ml concentrated sulfuric acid in turn to a glass test tube, shake well, and wait for color reaction at room temperature for 30 min. Using blank space as reference, the optical density was measured at the wavelength of 485 nm by ultraviolet–visible spectrophotometer (preheating 30 min), and the SS concentration was calculated from the standard curve. Extraction and concentration determination of starch: Distilled water was added to the SS residue to make the sample liquid in centrifuge tube up to 8 ml. After boiling for 15 min, 1 ml 9.2 mol/L HCIO4 was added and wait for static settlement for 15 min. Subsequent centrifugation, constant volume and determination procedure were consistent with SS concentration determination method.

Data processing

According to the morphological characteristics of the two Carex species [45], the below-ground biomass (BB) is the sum of root and stem biomass, the above-ground biomass (AB) is the leaf biomass, and the whole plant biomass (WP-B) is the sum of root, stem and leaf biomass. The biomass of different organs were got from the area of the cutting ring and samples obtained, then the biological biomass per unit area was extrapolated into g/cm2. The linear weighted sum method (LWSM) was used to calculate the NSC concentration of the whole plant based on the biomass allocation and NSC concentration differences among different organs. Taking the proportion of the biomass of each organ in the whole plant biomass as the corresponding weight, the NSC concentration of each organ was multiplied by the corresponding weight and summed to obtain the NSC concentration of the whole plant [25], and the calculation of SS and starch concentration of the whole plant can be deduced by analogy. The specific calculation process is in accordance with the following Eq. (1):

graphic file with name d33e701.gif 1

where CWP and COrgan represent the NSC, SS and starch concentrations (mg/g) of the whole plant and different organs respectively. BWP and BOrgan represent the biomass (g/cm2) of the whole plant and different organs respectively. When analyzing the allocation patterns of NSC among organs, the dry matter (DM) of NSC was calculated by combining the NSC concentration and biomass data of each organ. The NSC DM of the whole plant can be deduced by analogy. The specific calculation process is in accordance with the following Eq. (2):

graphic file with name d33e738.gif 2

where NSC DMWP represents the NSC, SS and starch DM (mg/cm2) of the whole plant, COrgan represents the NSC, SS and starch concentrations (mg/g) of different organs, BOrgan represents the biomass (g/cm2) of different organs.

Data analysis

The variations of biomass, NSC, SS and starch concentrations and DM among soil moisture content were analyzed by One-way ANOVA, all the indicators conform to the normal distribution, statistical significance was assessed at P < 0.05. Two-way ANOVA was used to analyze whether soil moisture content and different organs and their interactions have significant interaction on NSC concentration and dry matter accumulation of two Carex species, statistical significance was assessed at P < 0.05. The correlation strength and response characteristics of biomass and NSC to soil moisture content were demonstrated by scatter plot and analyzed by regression analysis. When selecting the NSC indexes of two Carex species that contributed the most to adapt to soil moisture content changes, the eigenvalue, variance contribution rate and loading were obtained through principal component analysis (PCA). The number of principal components was determined by extracting factors with eigenvalue > 1 according to the degree of variation. The greater the variance contribution rate, the more information about the original variable is included, and the cumulative contribution rate is required to be more than 80%. With the eigenvalue of each principal component as the weight and the variance contribution rate as the coefficient λ, the comprehensive evaluation model F was calculated following Eq. (3):

graphic file with name d33e788.gif 3

and then ranking according to F value [48]. In this ranking analysis, the larger F value of the index indicates the greater contribution of the index to adapt to the changes of soil moisture content. Analyzing data and drawing plots with IBM SPSS Statistics 27 and Origin Pro 2024.

Experimental results and analysis

Relationship between biomass and soil moisture content of two Carex species

Soil moisture content, different organs and their interactions had significant interaction effects on biomass of the two Carex species (Table 2).

Table 2.

Two-way ANOVA on the effects of soil moisture content and organ on Biomass of two Carex species

Source of variations The biomass of C. Parvula The biomass of C. alatauensis
F value P F value P
SMC 11.98 P < 0.01 28.33 P < 0.01
Organ 665.63 P < 0.01 65.02 P < 0.01
SMC × Organ 6.14 P < 0.01 4.32 P < 0.01
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The acronyms in the table represent: SMC Soil moisture content. The same as below

The root biomass of C. alatauensis, stem biomass of C. parvula and leaf, above-ground, below-ground and whole plant biomass of two Carex species all increased with the increase of soil moisture content (R2 = 0.17–0.68, P < 0.05; Fig. 1a, b). The root biomass of C. parvula reached an optimum, and then declined with the increase of soil moisture content (R2 = 0.49, P < 0.01; Fig. 1a). The stem biomass of C. alatauensis declined first, and then increased with the increase of soil moisture content (R2 = 0.45, P < 0.01; Fig. 1b). The BB/AB of C. parvula declined with the increase of soil moisture content (R2 = 0.45, P < 0.01; Fig. 1c). The BB/AB of C. alatauensis declined first, and then increased with the increase of soil moisture content (R2 = 0.35, P < 0.01; Fig. 1d). Root was the largest part in the biomass allocation of two Carex species, and root biomass of C. parvula was significantly larger than stem and leaf biomass (P < 0.05, Fig. 2a, b).

Fig. 1.

Fig. 1

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The relationship between biomass of two Carex species and soil moisture content. (a-b), the relationship between root biomass (R-B), stem biomass (S-B), leaf biomass (L-B), above-ground biomass (AB), below-ground biomass (BB) and whole plant biomass (WP-B) of two Carex species and soil moisture content (n = 5). (a), C. parvula (b), C. alatauensis. (c-d), The relationship between BB/AB of two Carex species and soil moisture content (n = 5). (c), C. parvula (d), C. alatauensis

Fig. 2.

Fig. 2

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The biomass allocation patterns of two Carex species with soil moisture content. (a-b), the biomass allocation patterns among different organs (leaf, stem and root) of two Carex species with soil moisture content (n = 5). (a), C. parvula (b), C. alatauensis

Relationship between NSC concentration, DMNSC and soil moisture content of two Carex species

Soil moisture content, different organs and their interactions had significant interaction effects on NSC, SS and starch concentrations, dry matter accumulation and SS/Starch ratio of the two Carex species (Table 3).

Table 3.

Two-way ANOVA on the effects of soil moisture content and organ on NSC of two Carex species

Source of variations C. Parvula (F value) C. alatauensis (F value)
SMC Organ SMC × Organ SMC Organ SMC × Organ
Concentration NSC 319.28* 959.83* 113.45* 325.03* 17705.15* 213.01*
SS 281.36* 1873.84* 141.85* 446.09* 19645.97* 317.99*
Starch 92.93* 261.71* 21.56* 47.23* 3937.67* 54.79*
SS/Starch 26.45* 355.63* 19.31* 84.44* 1588.26* 93.1*
DM NSC 16.59* 665.58* 6.93* 18* 54.19* 5.29*
SS 17.48* 608.68* 6.8* 16.89* 48.88* 5.06*
Starch 14.78* 778.88* 7.37* 20.54* 71.92* 6.24*
SS/Starch 10.01* 113.75* 6.28* 10.85* 198.54* 12.74*
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NSC Non-structural carbohydrates, SS Soluble sugar, DM Dry matter

*represents significant difference at P < 0.01. The same as below

The NSC, SS and starch concentrations in whole plant and roots of C. parvula all increased with the increase of soil moisture content (R2 = 0.17–0.48, P < 0.05; Fig. 3a-c). The NSC and SS concentrations in stems and leaves of C. parvula reached an optimum, and then declined with the increase of soil moisture content respectively (R2 = 0.68–0.88, P < 0.01; Fig. 3a, b), but those of C. alatauensis declined first, and then increased with the increase of soil moisture content (R2 = 0.28–0.75, P < 0.05; Fig. 3d, e). The concentrations of NSC, SS and starch in roots of C. alatauensis reached an optimum, and then declined with the increase of soil moisture content, but those in whole plant of C. alatauensis declined first, and then increased with the increase of soil moisture content (R2 = 0.32–0.64, P < 0.05; Fig. 3d-f). The starch concentration in leaves of C. parvula reached an optimum, and then declined with the increase of soil moisture content (R2 = 0.40, P < 0.01; Fig. 3c), the starch concentration in leaves of C. alatauensis increased with the increase of soil moisture content (R2 = 0.60, P < 0.01; Fig. 3f). The starch concentration in stems of C. alatauensis declined first, and then increased with the increase of soil moisture content (R2 = 0.73, P < 0.01; Fig. 3f). The concentrations of NSC, SS and starch in stems of C. alatauensis were higher than those in roots and leaves (P < 0.05, Fig. 3d-f).

Fig. 3.

Fig. 3

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The relationship between NSC concentration of two Carex species and soil moisture content. (a-f), the relationship between non-structural carbohydrates (NSC), soluble sugar (SS) and starch concentrations in different organs (leaf, stem and root) and whole plant of two Carex species and soil moisture content (n = 5). (a-c), the relationship between NSC, SS and starch concentrations of C. parvula and soil moisture content (n = 5). (a), NSC concentration (b), SS concentration (c), starch concentration. (d-f), the relationship between NSC, SS and starch concentrations of C. alatauensis and soil moisture content (n = 5). (d), NSC concentration (e), SS concentration (f), starch concentration. Whole plant NSC, SS and starch represent a weighted quantity (linear weighted sum method, LWSM) for plant organ (based on the contribution of each organ to whole plant biomass)

The DMNSC, DMSS and DMstarch in whole plant, roots, stems and leaves of C. parvula and those in roots and leaves of C. alatauensis all increased with the increase of soil moisture content (R2 = 0.18–0.64, P < 0.05; Fig. 4). The DMNSC, DMSS and DMstarch in whole plant and stems of C. alatauensis all declined first, and then increased with the increase of soil moisture content (R2 = 0.53–64, P < 0.01; Fig. 4d-f). The DMNSC, DMSS and DMstarch in roots of C. parvula were higher than those in stems and leaves respectively (P < 0.05, Fig. 5a-c), and there was no significant difference between stems and leaves (P > 0.05). The DMNSC, DMSS and DMstarch of C. alatauensis were basically showed as stems > root > leaves (Fig. 5d-f).

Fig. 4.

Fig. 4

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The relationship between DMNSC of two Carex species and soil moisture content. (a-f), the relationship between dry matter (DM) of non-structural carbohydrates (NSC), soluble sugar (SS) and starch in different organs (leaf, stem and root) and whole plant of two Carex species and soil moisture content (n = 5). (a-c), the relationship between DMNSC, DMSS and DMstarch in different organs of C. parvula and soil moisture content (n = 5). (a), DMNSC (b), DMSS (c), DMstarch. (d-f), the relationship between DMNSC, DMSS and DMstarch in different organs of C. alatauensis and soil moisture content (n = 5). (d), DMNSC (e), DMSS (f), DMstarch

Fig. 5.

Fig. 5

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The allocation patterns of DMNSC of two Carex species with soil moisture content. (a-f), dry matter (DM) of non-structural carbohydrates (NSC), soluble sugar (SS) and starch allocation patterns among different organs (leaf, stem and root) of two Carex species with soil moisture content (n = 5). (a-c), DMNSC, DMSS and DMstarch allocation patterns among different organs of C. parvula with soil moisture content (n = 5). (a), DMNSC (b), DMSS (c), DMstarch. (d-f), DMNSC, DMSS and DMstarch allocation patterns among different organs of C. alatauensis with soil moisture content (n = 5). (d), DMNSC (e), DMSS (f), DMstarch

Relationship between SS/Starch and soil moisture content of two Carex species

The SS/Starch in whole plant, roots, stems and leaves of two species was the highest in the leaves of the most arid habitat (Fig. 6). With the increase of soil moisture content, the SS/Starch in whole plant increased constantly (R2 = 0.33, P < 0.05; Fig. 6a, b), that in stems of C. parvula declined (R2 = 0.22–0.27, P < 0.05; Fig. 6a, b); that in leaves declined first, and then increased (R2 = 0.32, P < 0.05; Fig. 6a, b); and that in roots did not change in a linear way (P > 0.05, Fig. 6a, b). With the increase of soil moisture content, the SS/Starch in whole plant and leaves of C. alatauensis declined constantly (R2 = 0.16–0.58, P < 0.05; Fig. 6c, d), and that in roots and stems did not change in a linear way (P > 0.05, Fig. 6c, d).

Fig. 6.

Fig. 6

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SS/Starch changes of two Carex species with soil moisture content. (a-d), SS/Starch changes in different organs (leaf, stem and root) and whole plant of two Carex species with soil moisture content (n = 5). (a, c), the SS and starch concentration ratio of two Carex species with soil moisture content (n = 5). (a), C. parvula (c), C. alatauensis. (b, d), the DMSS and DMstarch ratio of two Carex species with soil moisture content (n = 5). (b), C. parvula (d), C. alatauensis

Screening of main NSC indexes contribute to the adaptation to soil moisture changes

The results of principal component analysis showed that NSC concentration indexes of two Carex species had different contribution values in response to soil moisture changes. The PC1 of C. parvula mainly included S-starch and L-starch, PC2 mainly included R-SS and R-starch, the cumulative variance contribution rate reached 84.75%, and R-SS was the largest contributor to adapt to soil moisture changes. The PC1 of C. alatauensis mainly included L-SS and S-starch, PC2 mainly included L-starch, the cumulative variance contribution rate reached 84.46%, and L-SS was the largest contributor to adapt to soil moisture changes (Table 4).

Table 4.

Factor loading and rank of principal components in NSC concentration indexes of two Carex species

Indexes C. parvula Indexes C. alatauensis
Factor loading F Rank Factor loading F Rank
F1 F2 F1 F2
R-SS 0.365 0.553 0.429 1 L-SS 0.469 0.099 0.386 1
R-starch 0.362 0.553 0.427 2 S-starch 0.464 0.028 0.366 2
S-starch 0.491 −0.099 0.291 3 L-starch 0.005 0.884 0.203 3
L-starch 0.448 −0.058 0.276 4 S-SS 0.360 −0.433 0.181 4
L-SS 0.413 −0.401 0.136 5 R-SS −0.465 −0.081 −0.379 5
S-SS 0.350 −0.462 0.074 6 R-starch −0.467 −0.117 −0.388 6
Eigenvalues 3.356 1.729 3.924 1.144
Percentage of Variance (%) 55.931 28.820 65.393 19.068
Cumulative (%) 55.931 84.751 65.393 84.460
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The acronyms in the table represent: R-SS Root soluble sugar, R-starch Root starch, S-SS Stem soluble sugar, S-starch Stem starch, L-SS Leaf soluble sugar, L-starch Leaf starch. The same as below

The results of principal component analysis showed that DMNSC indexes of two Carex species had different contribution values in response to soil moisture changes. The PC1 of C. parvula mainly included DML-SS and DML-starch, PC2 mainly included DMR-starch and DMR-SS, the cumulative variance contribution rate reached 82.40%, and DMR-starch was the largest contributor to adapt to soil moisture changes. The PC1 of C. alatauensis mainly included DMR-SS and DMS-starch, PC2 mainly included DML-SS and DML-starch, the cumulative variance contribution rate reached 83.08%, and DML-starch was the largest contributor to adapt to soil moisture changes (Table 5).

Table 5.

Factor loading and rank of principal components in DMNSC indexes of two Carex species

Indexes C. parvula Indexes C. alatauensis
Factor loading F Rank Factor loading F Rank
F1 F2 F1 F2
DMR-starch 0.285 0.592 0.376 1 DML-starch 0.406 0.538 0.435 1
DML-starch 0.483 0.104 0.372 2 DML-SS 0.363 0.522 0.398 2
DML-SS 0.487 0.087 0.369 3 DMR-starch 0.395 0.080 0.327 3
DMR-SS 0.336 0.394 0.353 4 DMR-SS 0.430 −0.123 0.310 4
DMS-starch 0.435 −0.439 0.178 5 DMS-starch 0.431 −0.415 0.248 5
DMS-SS 0.383 −0.531 0.114 6 DMS-SS 0.420 −0.495 0.222 6
Eigenvalues 3.491 1.453 3.906 1.079
Percentage of Variance (%) 58.184 24.215 65.102 17.980
Cumulative (%) 58.184 82.399 65.102 83.082
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Discussion

Asymmetric response of biomass to changes in soil moisture content

With the decrease of soil moisture content, the root biomass of C. alatauensis, stem biomass of C. parvula and leaf, above-ground, below-ground and whole plant biomass of two Carex species all decreased (P < 0.05, Fig. 1a, b), which indicates that the decrease of soil moisture content significantly limited the accumulation of biomass in these two Carex species. This kind of adaptation strategy coincides with the patterns that above-ground and below-ground biomass of C. moorcroftii [39] and above-ground biomass of C. tibetikobresia [6] all decreased with soil moisture content decreased. The root biomass of C. parvula and the stem biomass of C. alatauensis had opposite response pattern when facing with the changes in soil moisture content (P < 0.05, Fig. 1a, b). The variation characteristic of C. parvula supports the conclusion of previous study that the biomass of C. parvula increased first and then decreased with the decrease of soil moisture [6], but the stem biomass of C. alatauensis showed an opposite pattern of response, which indicates that different organs of plants might have different response strategies in biomass accumulation.

Among various plant organs, biomass allocation was highest in roots (P < 0.05, Fig. 2a, b), which reflects the trade-off and allocation strategy of two Carex species to improve below-ground and inhibit above-ground biomass accumulation [21] in response to the droughty alpine meadow habitat. The BB/AB of C. parvula declined with the increase of soil moisture content (P < 0.05, Fig. 1c), which is similar to the BB/AB of Buchloe dactyloides in droughty habitat [21], and the BB/AB of Pinus koraiensis and Fraxinus mandsurica in arid habitat [46] were significantly higher than those in moist habitat, while the BB/AB of Juglans mandshurica and Tilia amurensis [46] were decreased than those in moist habitat. The BB/AB of C. alatauensis declined first, and then increased with the increase of soil moisture content (P < 0.05, Fig. 1d), which is consistent with the trend of BB/AB in C. moorcroftii decreased first and then increased with habitat drying [39]. It indicated that both excessive and low moisture content promoted the growth of the below-ground tissues of C. alatauensis. Both Carex species took the allocation strategy by increasing root and stem biomass and reducing leaf biomass to avoid over-consumption of limited water in the above-ground tissue, and this was related to the asymmetric response of morphological characteristics of plant organs, the sensitivity and trade-off strategy of each organ to water changes were shown also [39]. It demonstrated that soil moisture content significantly affected the growth and development of two Carex species [6], which is further manifested as biomass accumulation and distribution.

NSC dynamics and inter-specific variations in response to soil moisture changes

The NSC and SS concentrations in stems and leaves of C. parvula and the NSC, SS and starch concentrations in roots of C. alatauensis all reached an optimum, then declined with the increase of soil moisture content respectively (P < 0.05, Fig. 3). The results are consistent with the previous researches that the concentrations of NSC and SS in leaves of Ulmus pumila, Musa AA Pisang Mas and M. ABB Pisang awak increased first, then decreased with the decrease of soil moisture [41, 42]. It indicated that moderate drought might promote NSC concentration in plants. The NSC, SS and starch concentrations in roots and whole plant of C. parvula all increased with the increase of soil moisture content (P < 0.05, Fig. 3a-c), which are similar to the trends that SS concentration in fine roots of Juglans mandshurica increased with the increase of soil moisture content [15]. It demonstrated that severe water deficit significantly decreased the NSC concentration in C. parvula and whole plant. But it was opposite to that water deficit increased NSC concentration in roots [4, 17] and the whole plant [25]. The concentrations of NSC and SS in stems, leaves and whole plant of C. alatauensis remained at very high levels in extremely arid habitat, which is contrary to the change pattern of C. parvula. Moreover, drought significantly increased the NSC and SS concentrations in non-grass functional groups [34] and severe drought promoted the NSC concentrations in various organs of Reaumuria soongorica [32], indicating that different plant species have different response characteristics of NSC indexes when facing with water content changes in habitat. Furthermore, there are significant differences between species and even opposite adaptation strategies.

In this study, the NSC concentrations in these two Carex species were primarily driven by SS concentration (Fig. 3), which are consistent with previous findings showed that an increase in SS concentration was the major contributor to an increase in plant NSC [44]. This is a kind of regulatory mechanism that plants mainly enhance their osmotic ability by increasing SS concentration [7]. The SS of each organ of the two Carex species was higher than that of starch (P < 0.05), and the SS/Starch ratio was the highest (6.31 times) in the most dry habitat (Fig. 6). Plants can adjust cell osmotic potential according to soil moisture changes, and maintain turgor by maintaining high SS concentration in leaves and cell water content, so as to ensure various physiological activities [13]. SS/Starch can be used as the conversion index of SS and starch, and the higher ratio means the greater demand for SS [11]. For example, the decrease of soil moisture significantly increased SS/Starch in roots, stems and leaves of Caryopteris mongolica [31], and drought treatment enhanced SS/Starch by increasing the conversion from starch to SS in sapwood of Dalbergia odorifera [5]. Dry habitat induced a decrease in leaf osmotic potential, impeded the transport of photosynthetic products, and actively hydrolyzes [11] sugars, thus leading to an increase of SS in leaves [32], this mechanism may be related to the very low organ biomass but still very high SS/Starch level of two Carex species in extremely dry habitat. The SS/Starch in stems of C. parvula and that in leaves and whole plant of C. alatauensis declined constantly with the increase of soil moisture content (Fig. 6), which are similar to SS concentration in the roots and shoots of Juglans regia was higher and starch concentration was lower under drought conditions [26], indicating that SS, as an intracellular solute in plants, has an important drought-resistant effect [47]. And the increase of SS/Starch can help plants regulate osmotic potential to maintain water transport efficiency between leaves and roots [29]. However, the SS/Starch in whole plant of C. parvula increased constantly with the increase of soil moisture content (P < 0.05, Fig. 6a, b), which is contrary to the change pattern of C. alatauensis, it might be related to the different patterns in DMNSC of two Carex species with soil moisture content changes, and the accumulation of DMNSC between different species affects the transformation mechanism of SS and starch.

The variations of NSC reflect the carbon balance of plants under environmental changes such as water deficit [50]. When the newly synthesized NSC is insufficient, the stored NSC can play a regulating and buffering role. If the consumption demand is still not met, the carbon budget balance will be broken, resulting in insufficient supply of NSC and carbon starvation [3, 10, 24]. It is inferred that the sharp decrease of NSC concentration and DMNSC in the stems, leaves and whole plant of the C. parvula in the extremely dry habitat is related to the breakdown of carbon balance. With the increase of soil moisture content, the DMNSC, DMSS and DMstarch in different organs and whole plant of C. parvula and in roots and leaves of C. alatauensis all increased constantly (P < 0.05, Fig. 4). This is consistent with the conclusion that the decrease of soil moisture content reduced the total amount of SS and starch in fine roots, stems and leaves of Robinia pseudoacacia [43], which proves that the decrease of soil moisture content can reduce the accumulation of DMNSC. The different NSC concentration and DMNSC responses of two Carex species reflect that different species adapt to soil moisture change through a multi-channel comprehensive regulation. It was screened by PCA comprehensive sorting model that the main contribution indexes of C. parvula in response to soil moisture content changes were SS concentration and DMstarch in roots, while those of C. alatauensis were SS concentration and DMstarch in leaves (Tables 4, and 5). It indicated that the comprehensive regulation of SS concentration and DMstarch in roots of C. parvula can enhance its tolerance to changes in soil moisture content. On the other hand, the SS concentration and DMstarch in leaves of C. alatauensis were extremely sensitive to soil moisture content changes [17] and played major roles of adaptive regulation.

Different NSC allocation patterns of two Carex species

Two-way ANOVA analysis showed that soil moisture content, different organs and their interactions had significant interaction effects on NSC, SS and starch concentrations, dry matter accumulation and SS/Starch ratio of the two Carex species (Table 3). The results indicated that the changes in soil moisture content influenced the variations and distributions of NSC in the organs of two Carex species, and then affected the distribution patterns of NSC in different species. Soil moisture content changes affected NSC allocations among different organs, and the allocation patterns vary among different species. The DMNSC, DMSS and DMstarch in roots of C. parvula were higher than those in stems and leaves (P < 0.05, Fig. 5a-c), which is similar to the studies on Fraxinus excelsior and M. sativa that roots are the main repositories of NSC [54]. The allocation of NSC was related to the carbon source, sink and the intensity that leaves (source organ) are the NSC sources [10, 23] of the whole plant, while the roots (sink organ) are important NSC sinks [10, 54] with large demands of carbon [51]. For example, in dry habitat, plants often transfer newly synthesized carbohydrates to the roots to enhance the absorption of water and mineral ions [31, 53] and accumulate NSC in the roots [30, 44]. U. pumila allocated more nutrient resources to roots with increasing drought intensity [41], indicating that roots are important carbon sinks which are conducive to plant growth in dry habitat. The allocation patterns of DMNSC, DMSS and DMstarch in C. alatauensis showed that stem took the largest part among different organs (Fig. 5d-f). Plants often store photosynthetic products in roots and stems to adapt to unfavorable environments [9, 33], it is generally believed that a large amount of carbohydrates stored in stems of plant played a buffering role in source-sink coordination [28], and NSC in stem enhanced the resistances of plants to drought and other stresses [9]. When the growth of a reservoir organ of a plant is sensitive to water content change, the photosynthetic products will be preferentially allocated to the organs (roots or stems) with strong capacity for utilizing or storage [49]. The accumulations of DMNSC, DMSS and DMstarch in the stems of C. alatauensis might be related to the role and mechanism of the stems mentioned in the above studies. It can be seen that source-sink coordination and NSC differential allocation patterns are important ecological adaptation strategies to enhance stress resistance and maintain growth, development and reproductive evolution of the two Carex species in high altitude and arid environment.

Conclusions

Soil moisture content, different organs and their interactions had significant interaction effects on biomass, NSC concentrations and dry matter accumulation of two Carex species. Under each soil moisture content, the two Carex species both invested the most resources in roots and reduced the growth of above-ground part to enhance water use efficiency and drought tolerance. Both two Carex species maintained a high concentration of NSC in stems to ensure that the source-sink coordination function was played in the process of NSC production (leaves) and consumption (stems or roots) in the shortest distance and the fastest time. It indicated that the asymmetric responses of biomass and NSC in organs of two species were performed to resist soil moisture changes. Beyond that, the main contributors to combat soil moisture changes were SS concentration and DMstarch in the roots of C. parvula which is a drought-tolerant plant, while C. alatauensis as a wet-mesophilic plant were those in leaves. The multi-regulatory mechanisms of biomass allocation, NSC concentration variations and DMNSC accumulation correspond to that two Carex species belong to different water-dependent types and demonstrated strong capacity to adapt to the drought habitat of alpine meadow.

Acknowledgements

We would like to express our gratitude to all those who provided assistance during the sampling and experimentation process. And we thank the anonymous reviewers for their constructive and helpful comments that improved this paper.

Authors’ contributions

Z.L. performed the experiments and other laboratory work, analyzed data and wrote the manuscript. D.Z. conceptualized the study and designed experiments. All the authors conducted field sampling, discussed and edited the results and contributed valuable comments to the final manuscript. And all authors reviewed the manuscript.

Funding

This study was funded by the National Natural Science Foundation of China (Response to arid habitats for bud bank and growth dynamics of roots and stems underground in an alpine meadow, grant number: 31960340).

Data availability

All the raw data generated during current study are not publicly available for the moment because the authors of the study wish to keep them for further analyses. Then data will be made public on an online repository. Nonetheless, further inquiries can be directed to the corresponding author.

Declarations

Ethics approval and consent to participate

Experimental research on the collection of plant material, all methods were carried out in compliance with local and national regulations.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Data Availability Statement

All the raw data generated during current study are not publicly available for the moment because the authors of the study wish to keep them for further analyses. Then data will be made public on an online repository. Nonetheless, further inquiries can be directed to the corresponding author.

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