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Carex parva and Carex
scabrirostris adopt diverse
response strategies to adapt to
low-light conditions
Wanting Liu, Rong Fan, Siyu Yang, Sibo Chen,
Yulin Huang and Wenli Ji*
College of Landscape Architecture and Art, Northwest A&F University, Xianyang, China
Introduction: In recent years, the visible light intensity of lawns has significantly
decreased due to obstructions caused by urban shading objects. Carex has a
competitive advantage over other turfgrass in low-light conditions and extensive
management. Therefore, exploring their survival strategy in low-light
environments is of great significance.
Methods: This study focuses on two species of Carex,Carex parva and Carex
scabrirostris, and investigates their response to low-light conditions (150 mmol/
m
2
/s) by simulating urban lawn conditions. Biomass allocation characteristics,
leaf anatomical features, biochemical parameters, root morphology and
photosynthetic parameters were measured.
Results: (a) Peroxidase activity, specific leaf area, and relative water content are
key factors influencing the photosynthetic capacity of the two Carex species. (b)
Under low-light conditions, photosynthetic parameters, leaf physiological
indicators, and biomass allocation of the two Carex species were significantly
affected (p<0.05). Both Carex species increased their investment in leaf biomass,
maintained lateral root growth, and cleared reactive oxygen species to maintain
their physiological balance. (c) In the simulated urban low-light environment,
neither C. parva nor C. scabrirostris produced dauciform roots.
Discussion: In terms of response strategies, C. scabrirostris is a high-
photosynthesis investing species with high productivity under low-light
conditions, whereas C. parva exhibits minimal response, indicating a slow
investment. C. scabrirostris has greater potential for application in low-light
environments compared to C. parva. These results provide a theoretical basis
for the cultivation and application of these two Carex species, as well as the
expansion of turfgrass germplasm resources.
KEYWORDS
Carex, low-light environment, photosynthesis, ecological strategy, dauciform root
Frontiers in Plant Science frontiersin.org01
OPEN ACCESS
EDITED BY
Alexander G. Ivanov,
Bulgarian Academy of Sciences, Bulgaria
REVIEWED BY
Georgios Liakopoulos,
Agricultural University of Athens, Greece
Caner Ünlü,
Istanbul Technical University, Türkiye
*CORRESPONDENCE
Wenli Ji
jiwenli@nwafu.edu.cn
RECEIVED 14 May 2024
ACCEPTED 16 September 2024
PUBLISHED 14 October 2024
CITATION
Liu W, Fan R, Yang S, Chen S, Huang Y and
Ji W (2024) Carex parva and Carex
scabrirostris adopt diverse response strategies
to adapt to low-light conditions.
Front. Plant Sci. 15:1432539.
doi: 10.3389/fpls.2024.1432539
COPYRIGHT
©2024Liu,Fan,Yang,Chen,HuangandJi.
This is an open-access article distributed under
the terms of the Creative Commons Attribution
License (CC BY). The use, distribution or
reproduction in other forums is permitted,
provided the original author(s) and the
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original publication in this journal is cited, in
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practice. No use, distribution or reproduction
is permitted which does not comply with
these terms.
TYPE Original Research
PUBLISHED 14 October 2024
DOI 10.3389/fpls.2024.1432539
1 Introduction
In recent years, lawns have played an increasingly significant
role in landscape greening (Thompson and Kao-Kniffin, 2019),
providing not only social benefits and ecosystem services to the
urban environment but also substantial economic and ecological
benefits (Trammell et al., 2019). Currently, urban buildings,
artificial structures, and dense tree canopies have created
numerous shaded areas, resulting in a significant reduction in
visible light intensity within cities (Francini et al., 2023).
However, most types of turfgrass do not adapt well to excessively
shaded environments (Zhang et al., 2016). Given that light
conditions are an important factor restricting turfgrass growth in
urban environments, selecting a shade-tolerant turfgrass species is
imperative (Fu et al., 2020).
Carex, one of the most ecologically diverse genera (Jakovljevic
et al., 2014), is currently being used in urban lawns, and their
growth status is being explored (Shokoya et al., 2022). Compared
with other turfgrasses, the Carex genus has the advantage of
growing in low-light or low-maintenance conditions (Więcław,
2017). It has been found that the Carex genus produces
dauciform roots (Güsewell and Schroth, 2017), which are effective
in absorbing water and nutrients from deeper soils and storing large
amounts of nutrients in infertile soils, providing a stable source of
nutrients for plant growth (Shane et al., 2005). Research has found
that the Carex genus can produce dauciform roots (Güsewell and
Schroth, 2017), which are capable of effectively absorbing water and
nutrients from deep soil layers. As a result, dauciform roots can
store large amounts of nutrients in infertile soils, providing a stable
nutrient source for plant growth. Previous studies have found that
Carex species with dauciform root systems are more likely to occur
in areas with high light intensity and lower phosphorus availability
(Playsted et al., 2006;Brundrett, 2009). However, the formation of
dauciform roots under low-light conditions in urban lawns is
mainly unknown.
Typical responses of plants to low-light environments include an
increase in aboveground biomass, thinner leaves, and a larger specific
leaf area (SLA) (Milla and Matesanz, 2017). Additionally, low-light
conditions reduce the maximum carboxylation capacity (Vc
max
),
maximum electron transport rate (J
max
), light saturation point
(LSP), and net photosynthetic rate (Pn
max
)(Haque et al., 2017;Fu
et al., 2017;Sun et al., 2023). These changes are the result of the long-
term coordination between leaf functional traits and photosynthesis
(Nam et al., 2017;Wright et al., 2004). Leaf anatomical structure
reflects important photosynthetic physiological characteristics
(Maza-Villalobos et al., 2022). Wang et al. (2023) studied factors
influencing plant photosynthetic capacity based on leaf anatomy. It is
important to select Carex species that can efficiently utilize light
energy, considering that Carex species lack palisade tissue in
mesophyll cells (Wang et al., 2023).
Plants also adapt to low-light conditions by altering their
physiological and metabolic processes (Zhang et al., 2022;
Kittipornkul et al., 2023). Specifically, the chlorophyll content
decreases while osmoregulatory substances accumulate, and
antioxidant enzyme activity increases (Wu, 2016;Wu et al., 2021).
In the absence of light, plants secrete many osmoregulatory
substances to maintain normal osmotic pressure in the cytoplasm
(Huang et al., 2022). Lower light will imbalance the internal
scavenging system of reactive oxygen species, leading to membrane
lipid peroxidation (Liang et al., 2009;Zhang et al., 2022). Antioxidant
enzymes, such as peroxidase (POD), can eliminate reactive oxygen
species, maintaining redox homeostasis (Liu et al., 2021).
As a significant concept in ecology, the leaf economics spectrum
reveals the coordination and trade-offs among various plant traits
(Wright et al., 2004). Plants adopt different investment strategies in
low-light environments (Wright et al., 2004). Plants that prioritize
rapid return on investment often have larger and thinner leaves,
whereas plants employing resource-storage strategies exhibit
contrasting characteristics (Jiang et al., 2023). These traits result
from the ongoing interactions between plants and their
environments over time (Violle et al., 2007). Similarly, the same
species may exhibit different structural characteristics in different
environments (Hu et al., 2022). Studying the variability and
plasticity of plant traits also contributes to understanding their
growth strategies under different environmental conditions
(Fajardo and Siefert, 2016;Lafont Rapnouil et al., 2023).
Additionally, plant functional traits can be categorized into soft
traits and hard traits. In order to obtain certain key physiological
traits that are difficult to measure in real time in the field, such as
indicators related to photosynthesis, other easily observable soft
traits can be used as proxies (Cornelissen et al., 2003). Since
different plant organs and tissues respond differently to
environmental changes (Funk and Cornwell, 2013), it is of
significant importance to identify functional trait indicators in
Carex species that are associated with the efficient utilization of
light energy.
C. parva is a perennial herb of the genus Carex in the family
Cyperaceae. It has high resistance to drought and shaded
conditions, making it suitable for extensive management. It is also
a turfgrass species with excellent potential for urban areas (Dai
et al., 2010). C. scabrirostris, an endemic species of high research
value in China, commonly grows alongside C. parva (Dai et al.,
2010). Currently, there are limited studies on the environmental
adaptability and survival strategies of these two Carex species
(Wang et al., 2023). Out of 865 species of sedge plants in China,
only three, including C. parva, have been observed to develop
dauciform roots in their natural habitats (Gao and Yang, 2016).
Further exploring the excellent potential and application value of
Carex species in low-light environments and providing parental
materials for domesticating and introducing urban lawns in China.
This study aims to investigate the response changes of C. parva
and C. scabrirostris under low-light environments, as well as their
different growth strategies in heterogeneous environments.
Specifically, we propose and explore the following questions: (a)
Can we identify the key factors influencing the photosynthetic
capacity of these two species of Carex? (b) How do the responses
of these two Carex species change in simulated low-light urban
environments, and how do they adapt to low-light environments?
(c) Do these two species of Carex have different growth strategies
under two different light environments, and which Carex has a
broader range of potential applications in low-light environments?
This study further explores the excellent potential and application
Liu et al. 10.3389/fpls.2024.1432539
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value of Carex species in low-light environments, providing parental
material and preliminary theoretical support for the introduction and
domestication of these species in urban lawns in China.
2 Materials and methods
2.1 Study area
The plant materials used in this experiment were C. parva and
C. scabrirostris, which belong to the genus Carex in the family
Cyperaceae. They were collected from the Taibai Mountains (34°
10’N, 107°58’E), a predominantly high-altitude grassland situated at
an elevation of 3,620 m (Dai et al., 2010). The area experiences an
annual precipitation of 751.8 mm, with a yearly relative humidity of
70% and an average annual temperature of 11°C (Cao et al., 2016).
We selected three sample areas in the Taibai Mountains, with a
distance of 20 m between each sample area. Each area was dug up to
form three sample clusters measuring 20 cm × 20 cm × 20 cm
(length, width, and depth) (Falcioni et al., 2017). Soil samples were
taken at the four corners and the central area of the sample plot
using the plum 5-point method (Falcioni et al., 2017).
The plant materials were stored in the climate chamber of
Northwest A&F University (34°26’N, 108°06’E). The chamber was
established under the following conditions: light duration of 14 h
day/10 h night, day/night temperature of 25/18°C, light intensity of
150 mmol/m²/s, air relative humidity controlled at 65%–75%, and
soil moisture maintained consistent with the original habitat. The
parameters were chosen based on the shaded lawn environments in
Shaanxi as the main reason (Wang et al., 2023). The experiment was
conducted during the optimal growth season for the selected plants,
which was late July.
2.2 Sampling and measurements
After being collected from the field, some plants were
immediately processed upon arrival at the laboratory, while the
remaining plants were kept in a growth chamber to simulate a low-
light environment for 80 days before processing. Five randomly
selected samples of each species were harvested for analysis. During
the harvesting process, plant photosynthesis was measured,
including the light response curve and the CO
2
response curve,
using the LI-6400XT (LI-COR, Lincoln, NE, USA).
Photosynthetically active radiation (PAR) levels were set at 2000,
1500, 1200, 1000, 750, 500, 250, 200, 150, 100, 50, 25, and 0 mmol
m
−2
s
−1
, with a CO
2
concentration of 400 mmol mol
−1
. The CO
2
concentration in the sample chamber was varied between 400, 300,
200, 150, 100, and 50 mmol mol
−1
, and then set back to 400, 600,
800, 1000, 1200, 1500, and 2000 mmol mol
−1
, with a constant PAR
of 1000 mmol mol
−1
. The hyperbolic tangent model was used to fit
indices such as the LSP, light compensation point (LCP), dark
respiration rate (RD), maximum carboxylation rate (Vc
max
), and
maximum electron transport rate (J
max
)(Wang et al., 2023).
Plant morphological indices were measured next. Leaf area was
measured using the LI-3000C portable leaf area meter. Three
mature leaves were randomly selected, and their length, average
width, maximum width, and leaf area were measured. Using a
caliper (De Antonio et al., 2023), the thickness of the leaf on the
same side as the main vein was measured, and the fresh weight and
dry weight of these leaves were recorded. Additionally, the
anatomical and structural characteristics of leaf sections were
observed using a MoticBA410 microscope (Jiang et al., 2023).
Images were captured, and parameters such as upper epidermis
thickness, lower epidermis (LET) thickness, and cuticle thickness
(CUT) were documented. Root morphology, including root length,
root volume, and root surface area, was measured using the
Winrhizo software. Among the 175 specimens of C. parva and 76
specimens of C. scabrirostris collected in the field, 0 and 64 plants
with dauciform roots (lateral roots with swollen axes) were
observed, respectively. The aboveground parts of the plants were
separated on a quartz surface, and their fresh weight and dry weight
were measured individually using an electronic balance.
Last, physiological indices of the plants were measured.
Chlorophyll a and b were extracted from fresh leaves using 95%
(v/v) ethanol according to Lichtenthaler and Wellburn (1983).
Malondialdehyde (MDA) content was determined using the
thiobarbituric acid method, proline mass fraction using the
sulfosalicylic acid extraction ninhydrin colorimetric method, Soluble
protein (SP) content using the Coomassie Brilliant Blue method, and
POD content using the guaiacol method (Weng et al., 2015).
2.3 Statistical analysis
Data analysis for this study was conducted using SPSS 19.0, and
graphs were generated using Origin 22. The normality of all data
was assessed using the Shapiro–Wilk test, and the homogeneity of
variances was assessed using Levene’s test. In case the results did not
follow a normal distribution, a square root transformation was
applied to achieve normality. Fisher’s LSD analysis was used to
determine the statistical significance of differences between
treatments (p< 0.05). To assess the variability of plant functional
traits between species, the coefficient of variation (CV) was
calculated using the formula CV = (SD ÷ M) × 100%, where SD
is the standard deviation and M is the mean. Traits with a CV
exceeding 50% were considered ecologically adaptive traits, while
traits with a lower CV served as indicators of systematic evolution,
reflecting species’adaptive potential (Zhang et al., 2021).
Additionally, the plasticity index (PI) was used to characterize the
response of two Carex species to different environments. It was
calculated as PI = (max −min)/max, where max and min represent
the maximum and minimum values of a certain trait. Traits with PI
> 0.6 were defined as sensitive indicators of habitat response, while
traits with PI < 0.2 were considered inert indicators of habitat
response. Spearman correlation analysis was used to examine the
relationships among plant functional traits. To further screen
relevant indicators for the efficient utilization of light in two types
of Carex, redundancy analysis (RDA) was performed on nine
functional trait indicators. Detrended correspondence analysis
(DCA) was conducted on RDA data (Grinn-Gofronet al., 2018).
Indicators were selected based on causality and correlation analysis,
Liu et al. 10.3389/fpls.2024.1432539
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excluding those with poor response and indicators directly derived
from basic indicators (Flexas et al., 2022). RDA was used to explore
the associations between photosynthetic traits and plant
physiological ecology, ranking the contribution values for each
indicator (Liu et al., 2021). Finally, the RDA results were
compared and validated with the corresponding correlation
analysis to ensure the accuracy of the findings (Dong et al., 2022).
3 Result
3.1 Changes in photosynthetic parameters
The light response curves of C. parva and C. scabrirostris
exhibited similar variations (Figure 1A). Overall, regardless of the
environment, C. scabrirostris displayed greater photosynthetic
capacity than C. parva (Figure 1A;Table 1). Under low-light
conditions, the LSP of C. parva increased significantly, while that
of C. scabrirostris decreased significantly (p< 0.05) (Table 1). Both
C. parva and C. scabrirostris exhibited significant reductions in RD
under low-light conditions. Compared to their natural habitats,
both Carex species showed increased stomatal conductance (Gs)
and transpiration rates (Tr) under low-light conditions (Figures 1C,
E). However, in low-light conditions, the intercellular CO
2
concentration (Ci) decreased in C. parva, while C. scabrirostris
exhibited higher Ci levels at PAR < 800 (Figure 1D). Additionally,
under PAR < 500, C. scabrirostris showed the highest light use
efficiency (LUE) among the Carex species under low-light
conditions (Figure 1F).
Additionally, akin to the changes observed in the light response
curve, C. scabrirostris demonstrated a higher responsiveness to CO
2
compared to C. parva (Figure 1B;Table 1). An
max
, CSP, VC
max
, and
J
max
showed significant reductions in C. scabrirostris, while CCP
and RP exhibited significant increases. Conversely, in C. parva,
CCP, and VCmax experienced significant decreases, while the other
variables exhibited minimal or no response (Table 1).
3.2 Changes of plant morphology
Both Carex species significantly increased their aboveground
biomass and decreased their belowground biomass under low-light
conditions, leading to a reduced root-shoot ratio (Figures 2A,B).
Morphologically, the leaves of both Carex species significantly
elongate in response to low-light conditions (Figure 3C). In this
setting, the leaf area of C. parva significantly increased, whereas the
SLA remained relatively unchanged. Conversely, the leaf area of C.
scabrirostris decreased significantly, accompanied by a notable
increase in SLA (Figures 3A,B).
Concerning leaf relative water content (LRWC), the two Carex
species exhibited distinct trends. LRWC decreased significantly in
C. parva, whereas it significantly increased in C. scabrirostris
(Figure 3D). Leaf tissue density (LTD) significantly increased in
both C. parva and C. scabrirostris under low-light conditions
(Figure 3E). Figure 4 illustrates that under low-light conditions,
the LET of C. scabrirostris increased significantly, while the CUT of
both Carex species decreased significantly to varying degrees (p<
0.05). No significant changes were observed in the leaf dissection of
C. parva (Figures 4A–C). Both C. parva and C. scabrirostris
exhibited significantly thinner leaf thickness (LT) under low-light
conditions (Figure 4D).
In terms of root morphology, the specific root length (SRL) of C.
scabrirostris significantly increased under low-light conditions,
while there was no significant change in C. parva (Figure 3G).
FIGURE 1
Light use efficiency of C.parva and C.scabrirostris with different photosynthetically active radiation. (A) Light response curves; (B) carbon dioxide
response curves; (C) stomatal conductance; (D) transpiration rate; (E) intercellular CO
2
concentration; (F) PN, net photosynthetic rate; PAR,
photosynthetically active radiation; CA, air carbon dioxide concentration; Gs, Stomatal conductance; Tr, Transpiration rate; Ci, Intercellular CO
2
concentration; LUE, light use efficiency.
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However, both species of Carex showed a significant reduction in
root tissue density (RTD) and branching intensity (BI) to varying
degrees (Figures 2F,3H). It is worth noting that C. scabrirostris was
found to have dauciform roots with an average density of 50.5
(number·g-1DW) in the field habitat, whereas the original
dauciform roots disappeared after a period of growth in a low-
light environment (Table 2).
3.3 Changes of leaf
biochemical parameters
The proline content in the leaves of both Carex species
decreased significantly under low-light conditions (Figure 4A). SP
levels significantly decreased in C. scabrirostris, whereas C. parva
did not respond to SP (Figure 4B). Additionally, the MDA content
in both Carex species significantly increased, with increases of
35.7% for C. parva and 80.9% for C. scabrirostris (Figure 4C).
POD activity significantly increased by 62.5% in C. scabrirostris,
(Supplementary Table), whereas no significant change was observed
in C. parva (Figure 4D). Furthermore, under low-light conditions,
both Carex species exhibited significant decreases in chlorophyll a
and chlorophyll a/b (Figures 4E,H). Total chlorophyll content
significantly decreased in C. parva, whereas no significant change
was observed in C. scabrirostris (Figure 4G).
3.4 Plant plasticity, variability, and
correlation between traits
Plants in field habitats exhibit high sensitivity (PI ≥0.6) in terms
of LT, net photosynthetic rate (Pn
max
), LET, POD, RD, and LCP
response from the perspective of plant plasticity (Figures 5A,C). In
termsofCUT,SRL,andchlorophylla+b,theyexhibitlow
sensitivity (PI < 0.2). In low-light environments, plants
demonstrate high sensitivity (PI ≥0.6) in terms of LT, leaf dry
matter content (LDWC), CUT, RD, Pn
max
, leaf area (LA), LCP, and
POD. However, they exhibit low sensitivity (PI < 0.2) in terms of
RTD, SP, and chlorophyll a/b.
From the perspective of plant variability (Figures 5B,D), plants
in field habitats exhibit greater variability (CV > 50%) in terms of
CUT, LET, RD, and LCP. In terms of LA, SRL, RTD, and
chlorophyll a + b, they demonstrate smaller variability (CV
<20%). However, in low-light environments, plants demonstrate
greater variability (CV >50%) in terms of POD, LDWC, LA, and
LCP. On the other hand, they show smaller variability (CV <20%)
in terms of SP, chlorophyll a/b, SRL, LET, chlorophyll a + b, and
RTD. The ranking of plant plasticity and variability remains
consistent across different environments.
In terms of morphological indicators, morphologically, SLA
shows a positive correlation with LRWC and a negative correlation
with LET, irrespective of the environment (Figures 4D,6C).
Regarding intraspecificcorrelationsofC. scabrirostris across
different environments, dauciform root density (DRD) shows
significant positive correlations with Pn
max
and SP, and
significant negative correlations with VC
max
,J
max
, POD, and SLA
(Figure 6B). In the natural habitat promoting dauciform root
growth, the indicators that are significantly positively correlated
with DRD remain consistent, while they show significant negative
correlationswithLCP,RD,chlorophylla/b,CUT,andLET
(Figure 6C). Regarding photosynthetic parameters, in natural
habitats, Pn
max
exhibits positive correlations with SRL, DRD, and
SP, while significantly negatively correlated with LDMC and
chlorophyll a/b (Figure 6C). In low-light environments, Pn
max
shows a significant positive correlation with POD (Figure 6D).
Regarding physiological characteristics, in natural habitats, POD
exhibits significant positive correlations with SLA and LRWC, while
significantly negatively correlated with LDMC and chlorophyll a/b.
TABLE 1 Light response curve parameters, CO
2
response curve parameters of Carex parva and Carex scabrirostris.
Specie Carex parva Carex scabrirostris
Environments Field habitat Low-light habitat Field habitat Low-light habitat
Photo response parameters
a0.02 ± 0.01c 0.04 ± 0.01bc 0.07 ± 0.01b 0.12 ± 0.03a
Pn
max
8.08 ± 0.82c 5.54 ± 1.97c 16.66 ± 2.23a 11.87 ± 2.33b
LSP 1012.26 ± 25.31c 1212.67 ± 122.30b 1356.25 ± 3.63a 847.65 ± 41.29d
LCP 54.32 ± 9.35a 32.92 ± 3.41b 14.66 ± 1.90c 11.31 ± 0.94c
RD 3.95 ± 0.11a 1.12 ± 0.06b 1.12 ± 0.18b 0.67 ± 0.26c
CO
2
response parameters
An
max
14.46 ± 2.49bc 18.13 ± 0.70b 25.88 ± 3.38a 12.13 ± 1.60c
CSP 1891.45 ± 34.60a 1808.10 ± 132.63a 1733.80 ± 122.80a 1440.34 ± 70.47b
CCP 148.48 ± 3.56ab 130.75 ± 25.17c 99.78 ± 12.97b 176.11 ± 5.01a
RP 3.95 ± 0.56a 4.66 ± 0.36a 2.24 ± 0.21b 4.02 ± 0.53a
Vc
max
36.33 ± 2.57a 30.61 ± 0.42b 36.47 ± 1.09ab 23.42 ± 2.10c
J
max
27.67 ± 2.52a 26.50 ± 2.02a 18.95 ± 1.84b 15.20 ± 0.53c
a, apparent quantum efficiency; Pn
max
, maximum net photosynthetic rate in light curve; LSP, light saturation point; LCP, light compensation point; RD, dark breathing rate; An
max
, maximum
net photosynthetic rate in CO
2
response curve; CSP, CO
2
saturation point; CCP, CO
2
compensation point; RP, photorespiration rate; VC
max
, maximum carboxylation rate; J
max
, maximum
electron conductivity. Different letters following each value within a row indicate significant differences at p < 0.05. The same letter means no significant difference.
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In low-light environments, POD shows a negative correlation with
chlorophyll a/b.
3.5 Redundancy analysis
The explanatory variables of the first and second axes were
39.83% and 34.13%, respectively, indicating that the first and
second axes accounted for 73.96% of the variation in the
photosynthetic characteristics of the two Carex species (Figure 7).
Among the explanatory variables, POD had the longest arrow and
the largest projected area, explaining 37.8% of the variation with a
significant p-value of 0.002. This indicates a strong correlation with
photosynthetic characteristics, significantly affecting them (p<
0.05). Additionally, POD had the highest contribution value of
39.2% and showed a positive correlation (acute angle) with aand
FIGURE 2
The effect of different environments on the aboveground and underground biomass changes in C. parva and C. scabrirostris. Different letters
indicate significant differences in means between treatments based on ANOVA. Bars represent Means ± SE (standard errors). (A) is the aboveground
and underground fresh biomass, (B) is the aboveground and underground dry biomass.
FIGURE 3
Effects of different environments on the morphological changes and leaf anatomical indices of C. parva and C. scabrirostris. Different letters indicate
significant differences in means between treatments based on ANOVA. Bars represent Means ± SE (standard errors). (A) is the specific leaf area, (B) is
the single leaf area, (C) is the leaf length, (D) is the relative leaf water content, (E) is the leaf tissue density, (F) is the specific root length, (G) is the
root tissue density, (H) is the branching intensity, (I) is the upper epidermis thickness, (J) is the lower epidermis thickness, (K) is the thickness of
cuticle, (L) is the leaf thickness.
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Pn
max
, while exhibiting a negative correlation (obtuse angle) with
LCP and RD. DRD explained 31.10% of the variation with a p-value
of 0.010, significantly affecting photosynthetic characteristics,
positively correlating with Pn
max
,An
max
, and LSP, and negatively
correlating with RP. SLA accounted for 15.5% of the variation with
ap-value of 0.004, significantly affecting photosynthetic
characteristics and positively correlating with Pn
max
and J
max
.
Among these variables, SLA and ashowed the smallest angle.
LRWC explained 3.80% of the variation with a p-value of 0.042,
significantly affecting photosynthetic characteristics, positively
correlating with aand Vc
max
, and negatively correlating with
CSP. The results of RDA were consistent with the correlation
values obtained from Pearson analysis.
4 Discussion
4.1 Key factors affecting the
photosynthetic capacity of two
Carex species
In this experiment, immediately after sampling the field habitat
plants, we simulated the native environments of C. parva and C.
scabrirostris in an artificial climate chamber in order to obtain
plants acclimated in low-light conditions. By controlling
environmental factors, we minimized phenological differences
among the two groups (Rosbakh et al., 2021) and reduced growth
differences to the lowest possible level. We used the same soil
substrate as in their field habitats, maintained humidity and soil
moisture according to their native conditions, and strictly regulated
the diurnal temperature variations in the climate chamber. This
approach ensured that light intensity was the major variable,
allowing us to investigate the acclimation changes and key factors
influencing the photosynthetic capacity of the two Carex species
under low-light conditions.
This study found that the POD activity, SLA, DRD, and LRWC
of the two Carex species contributed 88.2% to their photosynthetic
capacity (Table 3) and were significantly correlated with
photosynthesisrelated indicators (p< 0.05). Among these, POD
activity made the largest contribution to the photosynthesis-related
indicators of the two Carex species. Under low-light stress
conditions, the two Carex species produce reactive oxygen species
that damage chloroplasts, resulting in decreased photosynthetic
capacity. In order to maintain the redox balance and preserve the
photosynthetic function of chloroplasts, both Carex species
exhibited high POD activity to eliminate reactive oxygen species,
stabilizing cell membranes and the photosystem (Liang et al., 2009;
Zhang et al., 2022). Further analysis reveals that the plasticity and
variability of POD activity showed strong regulatory potential
under different environmental conditions, reinforcing the role of
POD as a key factor in the response of plants to environmental
variation. Therefore, they are key indicators influencing the habitat
adaptability of Carex species. This also confirms that POD will
change accordingly with environmental changes to help plants cope
with adverse environments. Shading increased the POD activity of
Cedrela fissilis, consistent with the findings of this study (Barbosa
et al., 2022).
TABLE 2 Dauciform root (DR) density, length and width of Carex
scabrirostris in the field habitat.
Specie DR density
(number·g
−1
DW)
DR
length
(mm)
DR
width
(mm)
Carex scabrirostris
(field habitat)
50.50 774.51 124.79
FIGURE 4
Effects of different environments on biochemical parameters of C. parva and C. scabrirostris leaves. Different letters indicate significant differences in
means between treatments based on ANOVA. Bars represent Means ± SE (standard errors). (A) is the proline content, (B) is the soluble protein
content, (C) is the malondialdehyde content, (D) is the peroxidase activity, (E) is the chorophylla content, (F) is the chorophyllb content, (G) is the
total chorophyll content, (H) is the chorophya/b.
Liu et al. 10.3389/fpls.2024.1432539
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SLA and LRWC are essential indicators of leaf structure and
morphology in plants. SLA is closely related to plant growth and
survival strategies, associated with light capture and photosynthetic
capacity. A larger leaf area facilitates capturing more light energy
and enables faster plant growth potential. Plants with effective
photosynthesis maintain high LRWC, preserving chloroplast
structure and function. Both Carex species exhibited low SLA in
fully illuminated environments, indicating that excessive
FIGURE 6
Spearman correlation analysis showed the relationship between functional traits of C. parva and C. scabrirostris.(A) is the relationship between the
functional traits of C. parva;(B) is the relationship between the functional traits of C. scabrirostris;(C) is the relationship between the functional traits
of two Carex species in the field environment; (D) is the relationship between the functional traits of two Carex species in the low-light environment.
In the area in the lower left corner, the number represents the correlation coefficient. In the upper right corner, blue indicates a negative correlation,
red indicates a positive correlation, and * indicates a significant correlation. a, apparent quantum efficiency; Pn
max
, maximum net photosynthetic
rate in the light curve; LSP, light saturation point; LCP, light compensation point; RD, rate of dark respiration; An
max
, maximum net photosynthetic
rate (CO
2
—response curves); CSP, CO
2
saturation point; CCP, CO
2
compensation point; RP, photorespiration rate; J
max
maximum electron
conductivity; SP, soluble protein; Pro, proline content; MDA, malondialdehyde content; POD, peroxidase activity; Chla/b, Chlorophyll a/b; SLA,
specific leaf area; LT, leaf thickness; LDWC, leaf dry weight/fresh weight; LRWC leaf relative water content; SRL, specific root length; CUT, cuticle
thickness; LET, lower epidermal thickness.
FIGURE 5
Plasticity index and coefficient of variation ranking of physiological and ecological indicators of C. parva and C. scabrirostris in different
environments. LA, leaf area; LRWC, leaf relative water content; SRL, specific root length; RTD, root tissue density; CUT, cuticle thickness; LET, lower
epidermal thickness; LT, leaf thickness; SP, soluble protein concentration; POD, peroxidase activity; Chla/b, chlorophyll a/b; Chla+b, total chlorophyll
content; Pn
max
, maximum net photosynthetic rate in the light curve; LCP, light compensation point; RD, rate of dark respiration. (A) is the plasticity
indicators in field environment, (B) is the coeffcient of variation index in field environment, (C) is the plasticity indicators in low-light environment,
(D) is the coeffcient of variation index in low-light environment.
Liu et al. 10.3389/fpls.2024.1432539
Frontiers in Plant Science frontiersin.org08
investment in leaf morphology for efficient light absorption was
unnecessary. In low-light conditions, C. scabrirostris actively
increases its leaf area ratio to maximize light capture, maintaining
relatively high LRWC, effectively preserving chloroplast structure
and photosystem II function, enabling efficient photosynthesis. In
this environment, C. parva showed a non-significant increase in
SLA and a decrease in LRWC. This may be due to C. parva’s weaker
ability to adapt to low light or the different ways in which the leaf
morphology of the two Carex species adapts to light intensity.
Meanwhile, both SLA and LRWC showed strong plasticity and
variability under low light, serving as sensitive indicators of habitat
response. This is also supporting evidence that the two species of
Carex adapted to different light environments by regulating these
indicators. In summary, plants adapt to different light environments
by adjusting the morphological structure and physiological changes
in their leaves.
As not all Carex species produce dauciform roots, this study
finds that POD activity and LRWC as the most crucial physiological
indicators affecting the photosynthetic capacity of the two Carex
species during the transition from full light to low-light
environments. Additionally, SLA is considered one of the most
important indicators from a morphological perspective affecting the
photosynthetic characteristics of these two Carex species.
Valladares et al. (2006) considers the PI and CV to be relatively
simple and effective methods, noting a strong correlation between
each method. In this study, the rankings of the PI and CV are
generally consistent, reflecting the sensitivity of each index to
habitat responses. In summary, POD significantly influences the
photosynthetic characteristics of both Carex. Under low-light
conditions, the POD, SLA, and LRWC of C. scabrirostris are all
significantly greater than those of C. parva, indicating that C.
scabrirostris possesses higher photosynthetic efficiency and greater
light energy utilization.
4.2 Responses of two Carex species to
low-light environment
In this experiment, both C. parva and C. scabrirostris showed
increased stomatal conductance, transpiration rate, and
aboveground dry matter content under low-light conditions (PAR
= 150). These results suggest that in such an environment, the water
vapor exchange between the leaves of both Carex species and the
external environment is promoted, thereby enabling the
accumulation of photosynthetic products. C. parva reduces its
LCP under low-light conditions but accumulates organic matter
by increasing its LSP. Under low-light conditions, both the Pn
max
and LSP of C. scabrirostris significantly decreased, indicating a
reduction in its photosynthetic capacity. This reduction, in turn,
enhances its adaptability to low-light environments (Fu et al., 2017).
The Pn
max
of both Carex species under low-light conditions is lower
than in the field environment, possibly indicating acclimation to
low light. Furthermore, regardless of the light environment, Pn
max
of C. scabrirostris is significantly higher than that of C. parva,
demonstrating its superior photosynthetic ability. Further analysis
of LUE indicates that C. scabrirostris exhibits the highest LUE under
low-light conditions, suggesting strong adaptability and survival
capabilities in such environments. Both Vc
max
and J
max
limit plant
photosynthesis, and under low-light conditions compared to their
natural environments, both Carex species exhibited varying degrees
of reduction in Vc
max
and J
max
. This could be one of the reasons for
the weakened photosynthetic capacity, consistent with the findings
of this study (Choi et al., 2021).
Plants have been shown to adapt to low-light conditions by
increasing their chlorophyll content and reducing the a/b ratio
under shaded conditions (Yao et al., 2016;Hirano et al., 2019). In
low-light environments, the chlorophyll a/b ratio significantly
decreases in both Carex species. C. scabrirostris displayed no
significant alterations in total chlorophyll content, while C. parva
significantly decreased. This also confirms that C. scabrirostris is
more shade tolerant. Additionally, the SP content of both Carex
species is positively correlated with Pn
max
and An
max
.Pn
max
and
An
max
decrease significantly under low-light conditions. This
indicates that photosynthesis in both Carex species is hindered
compared to their native habitat in such low-light conditions,
potentially reducing the photosynthetic yield of plants, thus
limiting their ability to produce more proteins (Miao et al., 2023).
This finding is important for understanding the growth strategies
and physiological mechanisms of Carex species in low-light
environments. C. scabrirostris exhibits the highest levels of SP and
Pn
max
in its habitat, providing nutrients for plant growth and aiding
FIGURE 7
RDA analysis between photosynthetic and ecophysiological
properties of two Carex species. a, apparent quantum efficiency;
Pn
max
, maximum net photosynthetic rate in light curve; LSP, light
saturation point; LCP, light compensation point; RD, dark respiration
rate; An
max
, maximum net photosynthetic rate in CO
2
response
curve; CSP, CO
2
saturation point; CCP, CO
2
compensation point;
RP, photorespiration rate; VC
max
, maximum carboxylation rate; J
max
,
maximum electronic conductivity; POD, peroxidase activity; DRD,
dauciform root density; SLA, specific leaf area; LRWC, leaf relative
water content; Chla/b, chlorophylla/b; SP, soluble protein; LET,
lower epidermal thickness; CUT, cuticle thickness; SRL, specific
root length.
Liu et al. 10.3389/fpls.2024.1432539
Frontiers in Plant Science frontiersin.org09
in better acclimation to the environment (Wang et al., 2021).
Additionally, the excessive accumulation of lipid peroxidation
products, measured as MDA, in both Carex species under low-
light environments can cause damage to chloroplasts through the
generation of reactive oxygen species, leading to a decline in plant
photosynthetic capacity. To maintain internal redox homeostasis
and sustain chloroplast function, both Carex species demonstrate
higher POD activity to scavenge reactive oxygen species and
maintain intracellular redox balance, thus keeping the cell
membrane and the photosystem stable (Smirnoff and
Arnaud, 2019).
Plants can maximize their photosynthetic efficiency and
capacity by adjusting leaf area, and the increase in leaf area
determines the light interception capacity (Weraduwage et al.,
2015;Yao et al., 2016). Under full sunlight, two species of Carex
actively regulate leaf area and aboveground biomass, exhibiting the
lowest SLA and aboveground biomass. This acclimation avoids
excessive light absorption and inhibition (Yao et al., 2016). In low-
light environments, C. parva increases its individual leaf area to
obtain more light energy. On the contrary, leaf thickness is
significantly negatively correlated with individual leaf area. These
morphological changes can optimize the leaf’s ability to capture
light and alleviate potential light inhibition effects in C. parva. Leaf
thickness and SLA of C. scabrirostris show a similar trend to C.
parva. However, the individual leaf area of C. scabrirostris decreases
significantly, although this decrease may be indicative of the plant’s
capability to transport resources from aboveground to
underground. This may explain why C. scabrirostris has decreased
underground biomass while increasing aboveground biomass. The
biomass of aboveground organisms is inversely proportional to leaf
area, further indicating that the allocation of aboveground and
belowground biomass is influenced by leaf area. Upper epidermal
cell thickness in two Carex species is found to display a significant
negative correlation with SLA while demonstrating a noteworthy
positive correlation with the chlorophyll a/b ratio. Thinning of the
epidermis thickness of two Carex species increases the light-
exposed surface area, enhancing the light capture capacity of the
leaves. It facilitates light penetration through the leaf surface,
promotes photochemical reactions within leaf cells, and ultimately
improves photosynthetic efficiency (Rocas et al., 2001).
In low-light environments, the RTD and BI of both C. parva and C.
scabrirostris are significantly reduced, which decreases their
competitiveness in the underground (Cheng et al., 2009). The SRL of
C. scabrirostris significantly increases in low-light environments,
indicating an active enhancement of root absorption for water and
nutrients, thereby improving its adaptability to low-light conditions
(Bordron et al., 2021). Consequently, C. scabrirostris exhibits a high level
of competitiveness in terms of nutrient and water resources, promoting
rapid growth even in low-light conditions (Birouste et al., 2014).
4.3 Growth strategies of two Carex species
in two different environments
In addressing the third research question, it is possible to
answer from both the perspective of trait variation, plasticity, and
the leaf economic spectrum. Analyzing CV and PI is necessary to
accurately reflect a species’response to environmental changes and
resource competition during community assembly (Donovan et al.,
2011;Navarro and Hidalgo-Triana, 2021). Compared with roots,
leaves exhibit greater plasticity and variability (Figure 4). This
suggests that the root systems of the two Carex species remain
relatively stable in heterogeneous environments. Meanwhile, plants
trade-off various traits and make corresponding changes with
environmental variations (Römermann et al., 2016). The different
sensitivities of morphology, leaf anatomical structures, and
photosynthetic parameters in this study to environmental changes
indicate that plants also trade-off among different morphologies,
leaf anatomical structures, and photosynthetic capacities to achieve
optimal survival strategies, which benefit individual survival and
population development. On the other hand, plants face the
combined influences of various habitat factors, and a positive
response of a certain trait to one environmental factor may be a
negative response to another environmental factor (Langley et al.,
2022). Plants also balance their responses to different habitat
factors. In low-light environments, light is the main
environmental factor limiting the growth of both Carex species.
After weighing the pros and cons, both Carex species prioritize
increasing leaf area and accumulating aboveground biomass to cope
with the stressful conditions of low light. In field habitats, the CV
values of LCP, LET, CUT, and RD are all above 50%, indicating that
plants maintain internal leaf moisture through thicker cuticles and
epidermal layers (Guo et al., 2023) and increase their
photosynthetic capacity with higher LCP and faster RDs. Under
low-light conditions, the CV values of LA, LRWC, and POD are all
above 50%, which is related to the reduction in photosynthetic
capacity. Plants strategically increase leaf area and utilize POD to
eliminate reactive oxygen species, thereby optimizing light
absorption and addressing limitations under low-light conditions.
Theoretical analysis of leaf economics spectra reveals that the
investment strategies of both Carex species remain unchanged,
whether in field habitats or low-light environments. C. parva,with
TABLE 3 Contribution value of each index to photosynthesis.
Name Explains % Contribution % pseudo-
FP
POD 37.8 39.2 6.1 0.002
DRD 31.1 32.2 9.0 0.010
SLA 15.5 16.0 7.9 0.004
LRWC 3.8 4.0 2.3 0.042
Chla/b 2.6 2.7 1.7 0.086
LET 1.7 1.8 1.2 0.458
SP 1.5 1.5 1.0 0.642
CUT 1.2 1.3 0.8 0.130
SRL 1.3 1.3 0.8 0.602
POD, peroxidase activity; DRD, dauciform root density; SLA, specific leaf area; LRWC, leaf
relative water content; Chla/b, chlorophylla/b; SP, soluble protein; LET, lower epidermal
thickness; CUT, cuticle thickness; SRL, specific root length; F: square of dispersion/degree of
freedom within and between groups; p, p-value.
Liu et al. 10.3389/fpls.2024.1432539
Frontiers in Plant Science frontiersin.org10
weaker photosynthetic ability, a smaller SLA, and higher leaf dry
matter accumulation, is categorized as a “slow-investment-high-
return”species. In contrast, C. scabrirostris is a “fast-investment-
low-return”species due to its larger SLA, higher photosynthetic
capacity, and lower leaf dry matter accumulation (Stearns, 1998). C.
scabrirostris employs a rapid investment strategy, enabling it to quickly
occupy space and resources, though it may be less stable in long-term
competition compared to species with slower investment strategies
(Wright and Grier, 2012). Notably, C. scabrirostris shows significant
variation in its investment strategy depending on the environment. In
natural habitats, it allocates more resources underground, enhancing
root expansion and nutrient absorption to address nutrient
limitations. This strategy likely reduces leaf maintenance costs and
increases resource-use efficiency, helping the species cope with the
potential stress of high light intensity. Conversely, under low-light
conditions, C. scabrirostris prioritizes aboveground growth, such as
leaf development and optimization of photosynthetic structures, to
maximize the capture of limited light resources. This flexible
investment strategy underscores C. scabrirostris’s high adaptability
to environmental changes and the diversity of its survival strategies. C.
parva maintains consistent investment strategies in both
environments,possiblyduetoitsslowerinvestmentstrategyorlack
of response within a short time frame. Through in-depth analysis, this
study further reveals that these species employ different response
strategies in their aboveground parts when facing low-light conditions.
C. parva enhances light capture efficiency by increasing leaf area, while
C. scabrirostris reduces individual leaf area and leaf mass but
significantly increases aboveground biomass, potentially due to an
increased number of blades. This illustrates the resource allocation and
compromise strategies employed by plant species in environments
with limited resources, aligning with their trait adaptations and
functional demands (Westoby and Wright, 2006;Heberling and
Fridley, 2012). Under low-light conditions, C. scabrirostris allocates
more resources to aboveground growth, altering its growth strategy,
while C. parva remains unchanged in this experiment. These different
responses reflect the long-term coexistence strategies of the two Carex
species in relation to environmental conditions and
resource competition.
From the perspective of the root economics spectrum, the two
Carex species adopted a rapid investment strategy in a simulated
urban low-light environment, whereas a conservative investment
strategy was observed in their natural habitat (Martín-Robles et al.,
2019). This finding is consistent with the conclusions drawn from
the leaf economics spectrum. Notably, under simulated urban low-
light conditions, C. scabrirostris was unable to produce dauciform
roots. RDA and correlation analysis revealed a significant
association between the presence of dauciform roots and the
plant’s photosynthetic capacity. In low-light conditions, although
the investment strategy for roots and leaves is rapid investment, C.
scabrirostris prioritizes resources to the leaves to optimize light
capture and improve photosynthetic efficiency. As a result, this
leads to reduced investment in the belowground components,
including the formation and maintenance of dauciform roots.
Consequently, after growing in the same soil environment for a
period of time, the dauciform roots of C. scabrirostris
gradually disappeared.
5 Conclusion
This experiment significantly advanced our understanding
of the response mechanisms of C. parva and C. scabrirostris to low-
light conditions. First, indicators such as POD activity, SLA, and
relative water content significantly influenced the photosynthetic
capacity of the two Carex species. Secondly, under low-light
conditions, C. parva exhibited a slow investment-return response
strategy, while C. scabrirostris adopted a fast investment-return
response strategy. Both Carex scabrirostris and Carex parva
allocate more resources to aboveground growth in low-light
environments to better adapt to the reduced light conditions.
Third, in the simulated urban low-light environment, neither C.
parva nor C. scabrirostris produced dauciform roots. The study found
a strong correlation between dauciform root formation in Carex
species and light intensity. Within the scope and conditions of these
experiments, POD activity emerged as a key player in maintaining
plant growth and photosynthetic capacity under low-light conditions.
Delving deeper into the regulatory mechanisms of POD to light will
provide valuable insights for optimizing plant light-use efficiency and
enhancing adaptability to stressful environments.
Furthermore, both species showcased superior shade tolerance
under simulated low-light urban environments, particularly C.
scabrirostris. These findings hold promise for their potential as
excellent turfgrass varieties for low-light environments in cities,
laying a solid research foundation for their future cultivation and
domestication. To safeguard species diversity in lawn grass and
bolster the stability of urban lawns, this study advocates for further
research focusing on the developmental potential of Carex species
and their tolerance to high shade conditions.
Data availability statement
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
Author contributions
WL: Conceptualization, Data curation, Formal analysis,
Investigation, Methodology, Writing –original draft, Writing –
review & editing. RF: Investigation, Methodology, Writing –review
& editing. SY: Formal analysis, Investigation, Writing –review &
editing. SC: Software, Writing –review & editing. YH: Investigation,
Writing –review & editing. WJ: Conceptualization, Funding
acquisition, Investigation, Project administration, Resources,
Writing –review & editing.
Funding
The author(s) declare financial support was received for the
research, authorship, and/or publication of this article. This work was
supported by the Natural Science Foundation of China (32071859),
China’s Ministry of Science and Technology’s Basic Science Resources
Liu et al. 10.3389/fpls.2024.1432539
Frontiers in Plant Science frontiersin.org11
Survey Special Project (2019FY101604) and Shaanxi Academy of
Forestry Technology Innovation Plan (SXLK2021-0203).
Acknowledgments
Wewouldliketothankthereviewersfortheirvaluable
suggestions on our study.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online
at: https://www.frontiersin.org/articles/10.3389/fpls.2024.1432539/
full#supplementary-material
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