Patterns of nitrogen and phosphorus stoichiometry among leaf, stem and root of desert plants and responses to climate and soil factors in Xinjiang, China

Abstract

Nitrogen (N) and phosphorus (P) play essential roles in plant growth and deserve more attention in desert ecosystems. Nutrients stoichiometry patterns across various plant organs can reflect the plants' trade-offs to obtain resources and their growth strategy. However, it is still unclear how these nutrients are allocated among desert plant organs and how they are related to the arid climate conditions. This study aimed to examine how plant N and P stoichiometry varies among the organs of desert plants, and how they respond to climate and soil factors. Therefore, we analyzed N and P stoichiometry of leaves, stems, and roots collected from 29 desert sites in Xinjiang, China, to achieve this goal. Our studies indicated that the mean N and P concentrations in the stems (17.5 ± 0.2 and 1.0 ± 0.02 mg g⁻¹, respectively) and roots (10.3 ± 0.2 and 0.7 ± 0.01 mg g⁻¹, respectively) were significantly lower than those in leaves (21.4 ± 0.3 and 1.2 ± 0.02 mg g⁻¹, respectively); the N:P ratio in stems (19.1 ± 0.3) was significantly higher than those in roots (17.6 ± 0.4), but N:P in leaves (18.2 ± 0.3) was not significantly different from those in stems and roots. Across plant life forms, N and N:P of both leaves and roots were respectively higher in shrubs than those in trees and herbs, P in three organs were significantly lower in trees than those in shrubs and herbs. Moreover, our results demonstrated that most soil factors had direct influences on N and P stoichiometry among different organs, and climate factors had indirect effect on N and P stoichiometry by affecting soil factors. This study provided the N and P stoichiometric characteristics of desert plant organs and explored their relationships with environmental variables, which can help understand nutrient stoichiometry patterns and utilization strategy of N and P and their potential responses to global climate changes in the desert ecosystems of central Asia.

Full text

Catena 199 (2021) 105100
Available online 26 December 2020
0341-8162/© 2020 Elsevier B.V. All rights reserved.
Patterns of nitrogen and phosphorus stoichiometry among leaf, stem and
root of desert plants and responses to climate and soil factors in
Xinjiang, China
Yan Luo
a
,
b
,
c
,
d
, Qingwen Peng
a
,
b
,
c
,
d
, Kaihui Li
a
,
b
,
d
, Yanming Gong
a
,
b
,
d
, Yanyan Liu
a
,
b
,
d
,
Wenxuan Han
a
,
d
,
*
a
State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
b
Bayinbuluk Grassland Ecosystem Research Station, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Bayinbuluk 841314, China
c
University of the Chinese Academy of Sciences, Beijing 100039, China
d
CAS Research Center for Ecology and Environment of Central Asia, Urumqi 830011, China
ARTICLE INFO
Keywords:
Arid region
Climate factors
Desert ecosystem
Edaphic factors
Nitrogen and phosphorus stoichiometry
Plant organs
ABSTRACT
Nitrogen (N) and phosphorus (P) play essential roles in plant growth and deserve more attention in desert
ecosystems. Nutrients stoichiometry patterns across various plant organs can reect the plants’ trade-offs to
obtain resources and their growth strategy. However, it is still unclear how these nutrients are allocated among
desert plant organs and how they are related to the arid climate conditions. This study aimed to examine how
plant N and P stoichiometry varies among the organs of desert plants, and how they respond to climate and soil
factors. Therefore, we analyzed N and P stoichiometry of leaves, stems, and roots collected from 29 desert sites in
Xinjiang, China, to achieve this goal. Our studies indicated that the mean N and P concentrations in the stems
(17.5 ±0.2 and 1.0 ±0.02 mg g
−1
, respectively) and roots (10.3 ±0.2 and 0.7 ±0.01 mg g
−1
, respectively) were
signicantly lower than those in leaves (21.4 ±0.3 and 1.2 ±0.02 mg g
−1
, respectively); the N:P ratio in stems
(19.1 ±0.3) was signicantly higher than those in roots (17.6 ±0.4), but N:P in leaves (18.2 ±0.3) was not
signicantly different from those in stems and roots. Across plant life forms, N and N:P of both leaves and roots
were respectively higher in shrubs than those in trees and herbs, P in three organs were signicantly lower in
trees than those in shrubs and herbs. Moreover, our results demonstrated that most soil factors had direct in-
uences on N and P stoichiometry among different organs, and climate factors had indirect effect on N and P
stoichiometry by affecting soil factors. This study provided the N and P stoichiometric characteristics of desert
plant organs and explored their relationships with environmental variables, which can help understand nutrient
stoichiometry patterns and utilization strategy of N and P and their potential responses to global climate changes
in the desert ecosystems of central Asia.
1. Introduction
Nitrogen (N) and phosphorus (P) are the two most vital elements for
plant growth, metabolism, photosynthesis and stress resistance (Aerts
and Chapin, 1999; Elser et al., 2007). The N:P ratio is a critical indicator
of nutrient limitation (N vs P) in the terrestrial ecosystem (Drenovsky
and Richards, 2004; Güsewell, 2004; Koerselman and Meuleman, 1996;
Schreeg et al., 2014). In desert ecosystems, scarce rainfall and high
evaporation induce slow biogeochemical cycling of plant N and P,
resulting in infertile soil conditions (low soil nutrients and high
salinization) (Charley and West, 1975; Hartley et al., 2007; Noy-Meir,
1973). Under water and nutrient co-limiting conditions, many physio-
logical processes related to desert plant N and P can be constrained, such
as N-xation and nutrient mineralization (Huang et al., 2018). N uptake
and xation, and availability of P of desert plants are strongly inuenced
by soil water (Huang et al., 2018), temperature (He et al., 2014), and soil
pH and salinity (Gong et al., 2017; He et al., 2016a). Therefore, studying
the N and P stoichiometry of desert plants can help better predict
biogeochemical cycles in desert ecosystems with consideration of global
climate change.
* Corresponding author at: 818 South Beijing Road, Urumqi 830011, China.
E-mail address: hanwenxuan@ms.xjb.ac.cn (W. Han).
Contents lists available at ScienceDirect
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journal homepage: www.elsevier.com/locate/catena
https://doi.org/10.1016/j.catena.2020.105100
Received 8 June 2020; Received in revised form 1 October 2020; Accepted 11 December 2020

Catena 199 (2021) 105100
2
Nutrients stoichiometry and allocation patterns in different plant
organs (e.g., leaves, stems and roots) reect the trade-offs a plant faces
to draw aboveground and belowground resources (Elser et al., 2010;
Fortunel et al., 2012). Nutrients stoichiometry patterns largely depend
on the ability of plants to acquire, transport, and store nutrients in the
shoot and root systems (Schreeg et al., 2014). The shoot system is
composed of leaves and stems. Leaves are the main photosynthetic or-
gans that capture light and carbon dioxide, and accumulate nutrients;
stems support the leaves and are responsible for transporting water and
nutrients between the root and shoot systems, and storing water and
nutrients (Fortunel et al., 2012). The root system xes plants in the soil,
absorbs water and nutrients from the soil and transports them to the
shoot system, and often stores water and nutrients (Jackson et al., 1996).
Therefore, leaves, stems and roots play key roles in regulating the sur-
vival, growth and reproduction of plants (Poorter et al., 2012; Reich
et al., 2008). However, due to sampling difculties and labor costs,
previous studies have primarily focused on the nutrient stoichiometry of
leaves; few studies have investigated the nutrient stoichiometry of stems
and roots. Some studies have found that stems and roots are structural
and transport organs as well as play a role in nutrient acquisition and
storage (Minden et al., 2014). For example, in woody plants, approxi-
mately one-third of the proteins are stored in the structural organs and
roots. Under drought conditions, these stored nutrients play a vital role
in supporting plant growth (Lambers et al., 2008).
In desert ecosystem, desert plants can survive in an environment
with limited water and nutrition only through reasonable allocation of
limited resources among organs (Eziz et al., 2017; Gusewell, 2002;
Khasanova et al., 2013; Sardans et al., 2017; West and Skujins, 1978).
According to the concept of functional equilibrium, plants will increase
the biomass ratio of the roots compared to the shoots (leaves and stems)
if the limiting factors derive from belowground (e.g., nutrients, water)
(Bloom et al., 1985; Eziz et al., 2017), whereas the biomass of the leaves
and stems will be increased if the limiting factors come from above-
ground (e.g., light, CO
2
) (Bloom et al., 1985). Compared to stems or
roots, leaves are more susceptible to environmental stresses (Fortunel
et al., 2012). To maintain normal physiological activities of leaves in
water and nutrient limited habitats, desert plants absorb enough water
and nutrients by increasing root proliferation or depth, reducing levels
of nutrient concentrations in tissue, and having low stomatal conduc-
tance and high nutrient resorption efciency (He et al., 2016b; Poorter
et al., 2012). Under the arid environment, desert plants need to make
full use of water, use the light efciently during the short growing sea-
son, and maximize the photosynthetic activity of leaves, so as to
distribute more nutrients to the leaves (Yan et al., 2016). The long-term
adaptation to drought and the low nutrient environment has led to the
coordinated diversity of different organs of desert plants in the use or
acquisition of nutrients (He et al., 2015; Yang et al., 2018). Although the
relationship between specic physiological functions and resources of
different organs have been recognized, few studies have comprehen-
sively analyzed the changes of nutrient levels among different organs of
desert plants.
Numerous studies have shown that the variation of plant nutrient
stoichiometry is inuenced by many environmental factors (e.g. climate
and soil properties). Reich and Oleksyn (2004) (over the globe) and Han
et al. (2005) (across China) certied that leaf N and P concentrations
decreased and N:P ratio increased with increasing mean annual tem-
perature (MAT) and mean annual precipitation (MAP). Hong et al.
(2014) has reported that leaf P was negatively correlated with MAT and
MAP, and root P and N:P were negatively and positively correlated with
MAT, respectively. He et al. (2015) found that MAT, MAP and the aridity
index (AI) in the desert ecosystem had signicant effects on leaf P, but
no effects on stems and roots. In addition to climate factors, soil attri-
butes are critical to plant growth and therefore affect plant nutrient
stoichiometry. Research has found that leaf N and P concentrations are
positively correlated with soil nutrients (Han et al., 2011); N and P
concentrations of stems and roots are affected by soil P and pH (He et al.,
2015). Both climate and soil have direct and indirect effects on the
distribution and composition of vegetation; a plants’ responses to the
environment may result in different nutrients stoichiometry patterns
among different plant life forms (Han et al., 2011; Li et al., 2010a; Yang
et al., 2014). According to the aforementioned studies, we know that
climate, soil factors and plant types all inuence the N and P stoichi-
ometry among organs in a complex way.
Desert plants are sensitive to global change. Increasing drought
conditions and unpredictable rainfall events will change soil nutrient
availability, thus affecting the nutrient stoichiometry among plant or-
gans (Sardans et al., 2017; Tian et al., 2019). However, the nutrient
stoichiometry among different organs of desert plants and their rela-
tionship with environmental factors remain unclear. Due to their
drought resistance, desert plants play a vital role in maintaining the
structure and function of desert ecosystems. In this study, we will
explore the patterns of N and P stoichiometry among plant organs and
across different life forms of desert plants; we will also determine their
responses to environmental factors in Xinjiang. Specically, we hy-
pothesized that (1) under drought and barren desert conditions, leaves
have higher N and P concentrations than roots and stems in desert
ecosystem; and (2) due to different physiological functions among or-
gans, N and P stoichiometry in different organs may show varying re-
sponses to climate and soil factors.
2. Materials and methods
2.1. Study area
This study was conducted in 29 eld sites in Xinjiang, China (Fig. 1),
with elevations ranging from 270 to 1451 m. The environment of the
study area is extremely dry and soil has a highly saline content. MAP
ranges between 45 and 169 mm, and MAT ranges between 5.85 and
11.87 ◦C. The mean potential evapotranspiration was 1104.37 mm, and
the mean solar radiation was 3478.16 kJ m
2
day
−1
(Fig. S1). The soils at
these sites were primarily brown desert soil and gray desert soil ac-
cording to the USDA soil classication (Soil Survey Staff, 2014). The
dominant plant species include Tamarix romosissima, Haloxylon ammo-
dendron, Reaumuria soongarica, Krascheninnikovia ceratoides, Nitraria
tangutorum, Poacynum hendersonii, Salsola foliosa, and Leymus secalinus
(Table S1).
2.2. Climate and soil data
We selected eight environmental variables: MAT (◦C), MAP (mm), AI
(unitless) (AI, dened as the ratio of precipitation to potential evapo-
transpiration); soil pH, soil electrical conductivity (EC, mS cm
−1
), soil
water stress coefcient (K
soil
, %, ratio of actual evapotranspiration to
potential evapotranspiration), soil total nitrogen (STN, mg g
−1
), and soil
total phosphorus (STP, mg g
−1
). MAT and MAP were obtained from
WorldClim version 2.0 (http://worldclim.org/version 2); AI and K
soil
were extracted from the CGIAR-CSI database (http://www.cgiar-csi.
org). Soil pH, soil EC, STN, and STP were measured during the
growing season.
2.3. Sampling and measurement
Field investigation and sample collection of plants and soil were
executed in July 2018. Sampling sites were selected according to the
distribution patterns of desert vegetation types. The sampling sites were
selected in locations distant from anthropogenic disturbances. At each of
the 29 sites, three 10 ×10 m plots were established randomly and
marked. Within each plot, the plant information of species composition,
life forms, height, coverage and base diameter were measured. Overall,
we divided organs into leaves, stems, and roots, and classied species
into trees, shrubs, and herbs. We analyzed the N and P concentrations in
different plant organs (including 510 leaves, 510 stems and 510 roots)
Y. Luo et al.

Catena 199 (2021) 105100
3
from 1530 samples; our database consisted of 30 species from 12 fam-
ilies, including 2 tree species (125 individuals, 375 leaf/stem/root
samples), 18 shrub species (295 individuals, 885 leaf/stem/root sam-
ples), 10 herb species (90 individual, 270 leaf/stem/root samples)
(Table S1). In addition, the spatial geographical coordinates and altitude
of each plot were recorded with a GPS (GPSMAP®60CSx, Garmin,
American).
At each sampling site, plant samples were collected with branch
shears, and divided into leaves, stems and roots, and stored separately in
labeled paper bags. For herb species, at least ten fully-mature, entire
individuals were dug up with roots to a soil depth of 20 cm. For trees and
shrubs, fully-matured and sun-exposed leaves and stems were collected
from ve individuals. To sample the roots of trees and shrubs, we rst
loosened the soil on one side of the target tree within a distance of 2 m
from the trunk of the target tree. Then, we nd the root branches (roots
with depths of 50–100 cm) and followed them to conrm that they were
from the same plant individuals. Subsequently, sections were cut from
the lateral root or taproot (diameters >2 mm) of the woody species. The
soils around these root sections were sampled. Plant samples (including
leaves, stems and roots) were cleared carefully to remove soil particles
and other materials. Samples were then brought to the laboratory and
rinsed with deionized water and dried for 30 min at 105 ◦C to avoid
losses due to respiration and decomposition. Samples were then dried to
constant weight at 65 ◦C, following which plant samples were milled and
stored in sample bags for chemical analysis.
In each plot, soil samples (0–20 cm) were collected using a hand
auger. Five samples were collected from each site and then mixed evenly
after removing organic debris and stones. After being sieved (2-mm
meshes), ve sub-samples were separated and stored in sample bags at
4 ◦C. The soil samples were brought back to the laboratory, air-dried,
ground to ne powder using a ball mill, and stored separately in bags
for nutrients analysis.
The N concentration of plant and soil samples was measured through
a CHNS/O Elemental Analyzer (Pekin-Elmer, USA), P concentration was
analyzed colorimetrically after H
2
SO
4
-H
2
O
2
-HF digestion (John, 1970).
Soil pH and EC were determined using a pH meter and a conductivity
meter (SevenExcellence-S470, USA), respectively, after water extraction
(extracted with 1: 2.5 and 1: 5 of soil: deionized water ratio,
respectively) (Bao, 2000).
2.4. Data analysis
Kolmogorov-Smirnov and Levene’s tests were used to verify the
normality of the data and the equality of error variance, respectively. We
performed a one-way ANOVA to test the differences of N and P stoi-
chiometry among organs and among life forms. Tukey’s HSD post hoc
test was used to compare the signicant difference of means (p <0.05).
All calculation results were showed using mean ±standard error (SE).
All statistical tests were conducted using R 3.6.1 and IBM-SPSS Statistics
25.0.
An aggregated boosted tree (ABT) model was conducted to quanti-
tatively assess the relative effects of environmental variables on the N
and P stoichiometry among organs of trees, shrubs, and herbs. The
model is a statistical learning method that can obtain both accurate
prediction and explanation (De’ath, 2007). The model was carried out
using the ‘lattice’ and ‘gbm’ packages in R 3.6.1 (R Development Core
Team, 2019).
Structural equation modeling (SEM) was applied to evaluate and
quantify the effects of plant life forms, climate factors, and edaphic
factors on N and P stoichiometry in organs. We performed the structural
equation modeling analyses based on the hierarchical pathways of prior
knowledge and conceptual models (Table S2). Prior to SEMs, some
environmental variables were excluded for this analysis due to insig-
nicant effects or collinearity according to the results of correlation
analyses. For leaf N, we excluded AI because of its collinearity with MAP
(r =0.78, p <0.01, Fig. S2) and MAT (r =0.78, p <0.01, Fig. S2). Before
modeling, we checked the distributions of all variables and tested their
normality. In order to satisfy the assumptions of normal distribution, the
specic values of climate and soil factors and N and P stoichiometry
among organs were ln-transformed to improve normality. Since some of
the introduced variables were not normally distributed after conversion,
we conrmed the t of the model using Pearson correlation analysis.
After data manipulation, we used a dataset to parameterize the model
and tested the overall goodness of t. The model was considered to be a
good t if the data included an insignicant (p >0.05) chi-square test
statistic, RMSEA <0.05, p >0.05, and both GFI and AGIF >0.90
Fig. 1. Locations of the 24 sampling sites in Xinjiang, China. The gure was drawn based on the map of Xinjiang at a scale of 1:5,500,000 (Xinjiang Bureau of
Surveying Mapping and Geoinformation, No. Xin S (2016) 250).
Y. Luo et al.

Catena 199 (2021) 105100
4
(Schermelleh-Engel et al., 2003). We choose the model with the lowest
AICs as our nal model among acceptable models. Through reasonable
model t, we explained the path coefcients of the model. Additionally,
we calculated the standardized total effects of plant life forms (com-
posite variable including trees, shrubs, and herbs), MAT, MAP, AI, STN,
STP, pH, EC and K
soil
on organs (leaves, stems and roots). All SEM an-
alyses were performed using AMOS 23.0 (AMOS IBM USA).
3. Results
3.1. Patterns of N and P concentrations and N:P of leaves, stems, and
roots
Across all plants, the mean (±SE) of the leaf N and P concentration
and N:P were 21.4 ±0.3 mg g
−1
, 1.2 ±0.02 mg g
−1
, and 18.2 ±0.3,
respectively (Table 1). The mean concentration of stem N and P was
17.5 ±0.2 mg g
−1
and 1.0 ±0.02 mg g
−1
, respectively, while N:P was
19.1 ±0.3. The corresponding stoichiometry in the root was 10.3 ±0.2
mg g
−1
and 0.7 ±0.01 mg g
−1
for N and P, respectively. The N:P ratio
was 17.6 ±0.4 (Table 1). The mean N and P concentration were
signicantly lower in stems and roots than in leaves (p <0.001), and the
mean N:P was signicantly higher in stems than in roots (p <0.001)
(Table 1).
The N and P concentrations among different life forms were all
greater in leaves than in stem and root (Fig. 2). The N concentration in
leaves and roots of shrubs was higher than that in trees and herbs, while
the N concentration in stem of trees was lower than in shrubs and herbs
(p <0.05). The P concentration in three organs of trees was signicantly
lower than in shrubs and herbs (p <0.05). The N:P ratio in three organs
was signicantly different among different life forms (p <0.05).
3.2. Inuences of climate and soil factors on N and P concentrations and
N:P ratio among leaves, stems, and roots
ABT analysis indicated that N and P stoichiometry in organs were
more greatly inuenced by soil than climate (Fig. 3a, e and i). For trees
(Fig. 3b–d), MAT was the major factor affected N concentrations of
leaves and stems, and EC was an important factor impacting P concen-
trations and N:P in leaves and stems; STN, MAP, and STP were the major
factors impacting root N and P stoichiometry. For shrubs (Fig. 3f–h), EC
was the most important factor for N concentrations in three organs;
while MAP, AI, and STP were the major factors impacting P concen-
trations in three organs; MAT, STP, and EC were the major factors for N:
P in three organs, respectively. For herbs (Fig. 3j–l), MAT was the most
important factor for leaf N and P stoichiometry, AI was the major factor
impacting the N concentrations and N:P of the stems, and the EC was a
major factor impacting the N and N:P of the root. In stems and roots, the
major factor impacting the P was K
soil
.
The structural equation modeling analysis showed that life form, EC,
and K
soil
had direct effects on leaf N concentration, and MAP had indi-
rect impact on leaf N (Fig. 4a and Fig. S3). Life form, EC, pH, and STN
had direct effects on leaf P concentration. MAT showed indirect inu-
ence on leaf P (Fig. 4b). pH, STN, and K
soil
had direct effects on leaf N:P
ratios. MAP and MAT had indirect impact on leaf N:P (Fig. 4c).
Furthermore, Life form and pH had direct effects on stem N. MAP and
MAT had indirect impact on stem N (Fig. 4d). Life form, EC, K
soil
, and
STP had direct effects on stem P concentration. MAP had indirect impact
on leaf P (Fig. 4e). STP had direct effects on stem N:P ratios. MAT had
indirect impact on stem N:P through (Fig. 4f). MAP, K
soil
, and pH
directly impacted root N concentration (Fig. 4g). Root P was mainly
impacted by life form, K
soil
, and STP. MAP had indirect impact on root P
(Fig. 4h). Life form, STP, and EC had direct effects on root N:P (Fig. 4i).
4. Discussion
4.1. Patterns of N and P stoichiometry among leaves, stems, and roots
Our rst hypotheses that desert plants allocate more N and P into
leaves than stems and roots was supported by our ndings (Table 1).
Element concentrations (especially N and P) are closely related to organ
functions (Drenovsky et al., 2010; Yan et al., 2016). Higher leaf nutrient
concentrations are important for plant photosynthesis, metabolic ac-
tivity, and water and nutrient utilization, therefore, they are crucial for
the survival of desert plants, especially under drought and high salinity
conditions (Drenovsky et al., 2010; Marschner et al., 1997). Plants adapt
to the nutrient constraints in the environment by regulating the nutri-
ents in their organs (Kerkhoff et al., 2006; Marschner et al., 1997). From
the perspective of ecology and evolution, the pattern of nutrient distri-
bution among different organs of plants is closely related to their cor-
responding functional traits (Broadley et al., 2004; Kay et al., 2005).
Compared with leaves, stems and roots have relatively low N and P
concentrations because their main functions are to absorb and transport
water and nutrients to leaves (Yang et al., 2014). In general, desert
plants allocated more biomass to roots and stems for water and nutrient
acquisition (Zhang et al., 2017). However, the amount of biomass can
also be a diluting factor, which leads to lower nutrient concentrations in
roots and stems (Kerkhoff et al., 2006). Therefore, the stems and roots do
not store too much N and P. Our results are consistent with those He
et al. (2016b) and Yang et al. (2014), which indicated that desert species
had higher N and P concentrations in photosynthetic organs (leaves)
than in non-photosynthetic organs (stems and roots).
The N (21.4 mg g
−1
) and P (1.2 mg g
−1
) concentrations of desert
plants in leaf were higher than stems and roots, but are lower than some
studies about desert plants (e.g., 25.9 and 1.5 mg g
−1
, (Castellanos et al.,
2018); 24.4 and 1.7 mg g
−1
(Li et al., 2010b); 28.1 and 1.9 mg g
−1
(Wang et al., 2015); 34.1 and 2.5 mg g
−1
(Zhang et al., 2016))
(Table S3). Leaf N:P is regarded as an indicator of soil nutrient limitation
for plants (Drenovsky and Richards, 2004; Koerselman and Meuleman,
1996), where N:P <14 means N limitation, N:P >16 signies P limi-
tation and 14 <N:P <16 N and P colimitation (Aerts and Chapin, 1999;
Koerselman and Meuleman, 1996). The higher leaf N:P (18.2) in our
study might suggest that desert plants are relatively limited by P (Elser
et al., 2000; Han et al., 2005; Li et al., 2010b) (Table S3), which could be
due to several situations. Specically, the extremely low soil water and
nutrient concentrations in our study area may have resulted in low
nutrient supply for the desert species. Secondly, under water and
nutrient limited conditions, desert plants may have had a limited ability
to assimilate P, which decreased the nutrient cycle and metabolic ac-
tivity (He et al., 2016a), ultimately causing a reduced nutrient feedback
mechanism between plants and soil. Moreover, the desert plants in our
study were limited by P, owing to the low precipitation and high
evaporation (Yang et al., 2014). Therefore, plant nutrient concentrations
Table 1
Concentrations and ratios of analyzed N, P and N:P in organs of desert plants. Different letters in the row indicate signicant differences among organs (Turkey’s HSD
test, ANOVA; p <0.05). SE, standard error; CV, coefcient of variation; n, sample size.
Leaf Stem Root
Nutrient Mean ±SE CV(%) Mean ±SE CV(%) Mean ±SE CV(%) n F p
N (mg g
−1
) 21.4
a
±0.3 32.9 17.5
b
±0.2 28.9 10.3
c
±0.2 37.9 510 605.8 <0.001
P (mg g
−1
) 1.2
a
±0.02 24.9 1.0
b
±0.02 37.3 0.7
c
±0.01 39.3 510 433.5 <0.001
N:P 18.2
ab
±0.3 34.2 19.1
a
±0.3 32.3 17.6
b
±0.4 50.0 510 4.7 <0.001
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Catena 199 (2021) 105100
5
Fig. 2. N (a), P (b) and N:P (c) stoichiometry in organs (leaf, stem and root) of different plant life forms. Different uppercase letters above bars indicate signicant
differences between organs for the same plant life form; different lowercase letters above bars indicate signicant differences between plant life forms for the same
organ (Turkey’s HSD test, ANOVA; p <0.05). The dashed lines in subplot (c) represent the threshold of P limitation (above the black dashed line N:P =16) vs. P and
N co-limitation (between the dashed lines N:P =14 and 16) vs N limitation (below the gray line N:P =14) (Koerselmas and Meuleman, 1996).
Fig. 3. Relative variable importance plot (%) of N, P and N:P stoichiometry for tree (a-d), shrub (e-h) and herb (i-l) in organs (leaf, stem and root) by aggregated
boosted tree models. AI, aridity index; EC, electrical conductivity; K
soil
, soil water stress coefcient; MAT, mean annual temperature; MAP, mean annual precipi-
tation; pH, soil pH; STN, soil total nitrogen; STP, soil total phosphorus; L-N, Leaf total nitrogen; L-P, Leaf total phosphorus; L-N:P, the ratio of leaf nitrogen :
phosphorus; S-N, Stem total nitrogen; S-P, Stem total phosphorus; S-N:P, the ratio of stem nitrogen : phosphorus; R-N, Root total nitrogen; R-P, Root total phosphorus;
R-N:P, the ratio of root nitrogen : phosphorus.
Y. Luo et al.

Catena 199 (2021) 105100
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are also expected to decrease in drought conditions. In addition, desert
plants acclimatize through morphological and physiological adjust-
ments, such as slowing the growth of plants to reduce the rate of
metabolism and reducing the demand for resource (He et al., 2016a; Niu
et al., 2019) to cope with the barren environment (Chapin, 1991;
Peaucelle et al., 2012).
4.2. Variations of N and P stoichiometry in leaves, stems, and roots
among different desert plant life forms
Nutrient variations and allocations among plant organs are inu-
enced by various factors such as evolutionary history, environmental
controls and plant functional groups (Han et al., 2011; He et al., 2016b;
Li et al., 2010a; Yang et al., 2018). Although the metabolic (leaves) and
structural (roots and stems) organs have different functions, the N and P
concentrations showed a consistent relationship in different plant life
forms. The N concentrations of leaves, stems and roots were signicantly
higher in shrubs (22.8 mg g
−1
, 18.0 mg g
−1
and 11.3 mg g
−1
) than trees
and herbs, and the P concentrations were signicantly lower in trees
(1.1 mg g
−1
, 0.8 mg g
−1
and 0.6 mg g
−1
) than herbs and shrubs, which
partially supported the opinions that short-lived and fast-growing spe-
cies have higher N and P concentrations than long-lived, slow-growing
species (Gusewell, 2002; Han et al., 2011; Thompson et al., 1997).
Higher N concentration in shrubs may primarily result from water
deciency and lower fertility conditions because shrubs need additional
non-protein nitrogen with osmotic adjustment under drought and
nutrient stress; this reects that the characteristics of desert plants
contribute to resource acquisition (Brouillette et al., 2014; Zhang et al.,
2016). Shrubs had more root branches and more complex structures
than herbs for building symbiotic relationships with microorganisms,
allowing for increased absorption of nutrient and water utilization ef-
ciency under drought conditions (He and Dijkstra, 2014; Jackson et al.,
1996; Zhou et al., 2010). Another possible reason for the higher N
concentrations in shrubs may be because the majority of species in our
study are deciduous; therefore, they have higher nutrient concentrations
than other species (Killingbeck and Whitford, 1996). Higher P concen-
trations in herbs may be due to the fact that fast-growing plants need
sufcient P-rich RNA for protein synthesis to meet the requirements for
rapid growth (Han et al., 2005; Matzek and Vitousek, 2009). Addition-
ally, previous studies have found that in P-poor systems, slow-growing
shrubs move P from deeper soil layers to shallow soil, which helps
meet the demand for high leaf P for fast-growing herbs (He et al., 2014).
Signicantly differences were apparent in the N:P of stems and roots
of trees (19.9 and 18.1), shrubs (18.4 and 18.4), and herbs (17.5 and
14.2) compared with leaves, showing that the sensitivity of different
organs to soil nutrients is signicantly different, and the N:P of most
stems and roots were mainly restricted by P for different life forms.
Sterner and Elser (2002) suggested that leaf N:P ratio indicates soil
nutrient should be based on the optional N:P ratio, but this ratio can be
affected by the surrounding environment. Schreeg et al. (2014) pro-
posed that the N:P ratios of stems and roots plant tissues might be better
indicators than fresh leaves for determining soil nutrient effectiveness
because stems and roots showed less reliance on maintaining an optimal
ratio. Due to the higher metabolically activity of root, large amounts of
N and P were required to synthesize carrier enzymes to actively absorb
nutrients from soil solutions (Garrish et al., 2010; Olsen and Bell, 1990).
Fig. 4. Structural equation models for N, P and N:P of leaf (a-c), stem (d-f) and root (g-i), based 58on the effects of life form, climate and soil factors. Single-headed
arrows represent causal relationships. Red and black arrows indicate positive and negative relationships, respectively. Dotted arrows represent nonsignicant paths
(p >0.05). Numbers adjacent to arrows are standardized path coefcients. The path widths are scaled proportionally to the path coefcient. Continuous and dashed
arrow indicate positive and negative relationship. *, **, and *** represent correlation that is signicant at the 0.05, 0.01 and 0.001 level (2-tailed), respectively. The
meaning of the abbreviations is the same as Fig. 3. (For interpretation of the references to colour in this gure legend, the reader is referred to the web version of
this article.)
Y. Luo et al.

Catena 199 (2021) 105100
7
Therefore, roots may be a more accurate indicator of soil nutrient status
(Schreeg et al., 2014). However, this requires further study for
verication.
4.3. Resoponses of N and P stoichiometry among organs to environmental
factors
In this arid region, insufcient rainfall events and high evaporation
also limit N and P from leaching into the soil, whereas salt crust can
develop in high saline habitats (Zhang et al., 2018). Drought and salinity
cause the most serious constraints on the uptake and cycling of plant
nutrients; the changing moisture content and salt concentrations may
change the nutrient cycles of desert plants through their effects on soil
properties (Gong et al., 2017). We identied the specic environmental
factors that affect nutrient stoichiometry among organs, and clarify the
causal relationship among the environmental factors (Fig. 4 and Fig. S2).
The climate can directly or indirectly affect soil factors via improved
plant-soil feedback responses (Sardans and Pe˜
nuelas, 2012) and further
regulate the variations in plant nutrient concentrations and ratios
among organs.
Our results conrmed that the variation of N and P stoichiometry
among organs are more attributed to plant life form and soil nutrient
conditions, rather than climate conditions. These results indicated that
most variations in N and P concentrations related to photosynthetic
capacity and osmoregulation can be explained by taxonomy, high-
lighting the importance of genetics in the control over N and P.
Furthermore, patterns of nutrient stoichiometry of the organs of desert
plants indicated the environmental status and stability of the desert
ecosystem (Gutterman, 1994; Yang et al., 2014). The nutrient stoichi-
ometry and allocation among plant organs can be affected by many
factors, such as soil water and nutrient conditions, and plant functional
groups (He et al., 2014; Sardans et al., 2017).
Among the environmental factors, K
soil
was the stronger regulator in
driving leaf and root N, and stem and root P; EC was the stronger
regulator in driving leaf and root N, and leaf and stem P; pH was the
stronger regulator in driving leaf P. K
soil
, EC and pH represented
drought, alkalinity and salinity, respectively, which explained a large
fraction of the variances of N and P concentrations among three organs.
The availability of N and P largely affected by soil water and salinization
conditions. Long-term drought and infrequent precipitation may
decrease the soil nutrient availabilities and constrain soil weathering,
leading to a slow release of P and an increase in the loss of N (Belnap,
2011). Moreover, our results found that STP had a highly relative in-
uence on the nutrients of stems and roots. Stems and roots played key
roles in the nutrient cycle in desert habitats, although most studies
showed that stems and roots had lower nutrient levels than leaves (He
et al., 2014; He et al., 2016a; Zhou et al., 2010).
Previous researches indicated that MAT and MAP can directly or
indirectly inuence plant organs nutrient concentrations and ratios via
changing soil biogeographical processes and vegetation composition
(Chapin et al., 1987; Han et al., 2011; He et al., 2016a; Li et al., 2010a;
Liu et al., 2019). Climate factors (MAP and MAT) had indirect effects on
organs N and P concentrations by affecting soil properties. Through
long-term adaptation to drought and high salt conditions, desert plants
have developed special survival strategies. The ranges of MAP (from 45
to 169 mm) and MAT (5.85–11.87 ◦C) (Fig. S1) in the studied region
were very narrow, which does not explain the strong uctuations with
plant nutrients.
5. Conclusions
Overall, this study comprehensively analyzed the variation patterns
of nutrient stoichiometry among different organs of desert plants, and
their responses to climate and soil factors. Our results showed that the
desert plants had higher N and P concentrations in leaves than in stems
and roots. Nutrients stoichiometry patterns among plant organs are
affected by many environmental factors; soil properties showed a larger
impact on plant organ N and P stoichiometry than climates. These re-
sults provided an important reference basis for understanding nutrient
stoichiometry patterns, utilization strategy, and plant-environment re-
lationships in desert ecosystems.
Declaration of Competing Interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Acknowledgments
This work was funded by the Light of West China Program of the
Chinese Academy of Sciences, and the Special Project of Introducing
High-level Talents to Xinjiang Uygur Autonomous Region, China. K.L.
was also supported by the Strategic Priority Research Program of Chi-
nese Academy of Sciences (XDA20050103) and the opening project
(2017D04012) of Key Laboratory of Science & Technology Department
of Xinjiang Uygur Autonomous Region; Y.G. and Y.L. were also sup-
ported by the National Natural Science Foundation of China
(31700460). We also thank Xinwen Zhu, Maosong He, Yuan Su and
Jiajia Le for assistance with eld sampling and laboratory work and
International Science Editing (http://www.internationalscienceediting.
com) for help editing and proofreading this manuscript.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.catena.2020.105100.
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