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Interactions between arbuscular mycorrhizal fungi
and soil properties jointly influence plant C, N, and
P stoichiometry in West Lake, Hangzhou†
Mengfei Yu,
a
Qinxiang Wang,
b
Weixia Tao,
b
Guihua Liu,
c
Wenzhi Liu,
c
Lai Wang*
de
and Lin Ma*
c
Arbuscular mycorrhizal fungi (AMF) play important roles in terrestrial plants via mutualistic symbiosis.
However, knowledge about the functions of AMF in aquatic plants remains limited. Here, four dominate
emergent plant communities in West Lake, Hangzhou were chosen, the characteristics of AMF, plant
C, N, and P stoichiometry, and soil properties were investigated. The results showed that both AMF
infection rates and the number of AMF spore species increased, suggesting a great mutualism between
AMF and emergent plants. Contents of C, N, and P in aboveground biomass and roots and their ratios
varied greatly among these four emergent plants. Moreover, AMF infection frequency showed
a significant negative correlation with aboveground biomass N (p< 0.05), whereas the rates of
arbuscular mycorrhiza formation and vesicular formation after root infection showed significant negative
correlations with root N and root N/P. Soil total C, soil total N, soil total P, and oxidation–reduction
potential (ORP) were significantly associated with AMF infection characteristics. Our main findings are
that the results of redundancy analysis and path analysis further indicated that soil C, N, and P contents,
and ORP affected plant C, N, and P contents and their stoichiometry directly. Meanwhile, soil properties
can also regulate plant ecological stoichiometry indirectly via altering AMF mycorrhiza. Our findings
highlight that interactions between AMF and soil play crucial roles in regulating plant ecological
stoichiometry and can be treated as a whole in investigating the relationships between plant and soil.
1. Introduction
Arbuscular mycorrhizal fungi (AMF), as a kind of obligate soil
symbiotic microorganism in the phylum Glomeromycota, exist
in the rhizosphere of plants. It is well known that arbuscular
mycorrhizas are capable of establishing the most common
terrestrial mutualistic symbiosis with approximately 80% of
terrestrial plant species.
1,2
Numerous studies have reported that
AMF exhibit large amounts of benecial effects on terrestrial
plants, such as improving uptake of nutrients from the soil,
3
alleviating water stress,
4
and enhancing resistance to salinity,
pH, heavy metals and drought.
5–8
Little attentions have been paid to exploring the roles of AMF
in aquatic plants.
9
This might be partly ascribed that the relative
low concentration of oxygen in the soil of aquatic environments
limited the growth of AMF and their symbiosis with plants.
Meanwhile, it might be also attributed to the fact that the plants
in aquatic ecosystems directly absorb nutrients from water
through their roots and shoots rather than AMF. However, in
the recent years, AMF are widely found in many species of
plants in aquatic ecosystems around the world.
10,11
Thus, there
is a pressing need to better understand the effects of AMF on
aquatic plants.
Ecological stoichiometry focused on the dynamical balance
of several chemical elements such as C, N, and P between
organisms and their environments.
12,13
It successfully inte-
grated into the studies at various levels, from microscopic
molecules to macroscopic ecosystems,
14
and played an impor-
tant role in investigating the functions of ecosystems, compe-
tition among plants, and nutrition limitation.
15,16
The main
focus of ecological stoichiometry were plant C, N, and P stoi-
chiometric ratios, which can be affected by many factors such as
nutrients, diseases, water and AMF, etc.
a
Hubei Provincial Key Laboratory for Protection and Application of Special Plant
Germplasm in Wuling Area of China, College of Life Sciences, South-Central
University for Nationalities, 182 Min Zu Da Dao, Wuhan 430074, Hubei, China
b
Yellow River Conservancy Technical Institute, Kaifeng 475000, Henan, China
c
Hubei Key Laboratory of Wetland Evolution & Ecological Restoration, Wuhan
Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China. E-mail:
malin@wbgcas.cn; Tel: +86-27-87700849
d
State Key Laboratory of Iron and Steel Industry Environmental Protection, Energy
Conservation and Environment Protection Co., Ltd, MCC Group, Xi Tu Cheng 3,
Haidian, Beijing 100088, China
e
State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of
Hydrobiology, Chinese Academy of Sciences, Dong Hu Nan Lu 7, Wuhan 430072,
China. E-mail: yituyimi@139.com; Tel: +86-15623413021
†Electronic supplementary information (ESI) available. See DOI:
10.1039/d0ra08185j
Cite this: RSC Adv., 2020, 10, 39943
Received 24th September 2020
Accepted 28th October 2020
DOI: 10.1039/d0ra08185j
rsc.li/rsc-advances
This journal is © The Royal Society of Chemistry 2020 RSC Adv.,2020,10,39943–39953 | 39943
RSC Advances
PAPER
AMF can forms symbiotic relationship with plants and
improves plant N and P uptake.
15
It appeared to be closely
related with plant C, N, and P stoichiometry, but this mutual-
istic symbiosis relationship were likely to be inuenced by
a series of environmental factors, especially soil properties such
as total N, pH, Zn
2+
concentration
17
and nutrients.
10
A previous
study reported that C, N, and P contents in soils regulated C, N,
and P ecological stoichiometry of aboveground biomass via root
uptake of organic matters and different types of nutrients.
18
Similarly, leaf N and P contents in trees, shrubs, and herbs
species could be affected by soil C/N ratio and pH.
19
Moreover,
soil N concentration and Mn
2+
jointly affected AMF diversity
and colonization in Boehmeria nivea root.
20
Additionally, Collins
& Foster (2009) found that AMF played a vital role for mediating
plant community diversity at lower soil P level.
21
Thus, a better
comprehensive knowledge of interaction between AMF and soil
will be conductive to uncover the effects of AMF on aquatic
plants.
In the last four decades of twenty century, the quality of West
Lake water, located in Hangzhou of China as a China-
internationally renowned tourist and cultural base, was
affected by the activities related to the fast economic develop-
ment. The deterioration of water quality was mainly due to the
relative high ratio of heavy fraction organic matter (HFOM)/
light fraction organic matter (LFOM) rather than zinc, boron
or manganese in the lake sediments.
22
In the current study, we
conducted four kinds of emergent plants and rhizosphere soil
samples from four different sites in the West Lake. The AMF
infection characteristics, C, N, and P contents and their stoi-
chiometric ratios in emergent plants, and soil properties were
investigated. We expected that arbuscular mycorrhizal fungi,
soil properties, and their interactions jointly regulated C, N, and
P stoichiometry in emergent plants. The objectives of this study
were as following: (1) to investigate the AMF infection charac-
teristics in emergent plants; (2) to evaluate the correlations
among AMF infection characteristics, plant C, N, and P stoi-
chiometry, and soil properties; (3) to elucidate potential path-
ways of the effect of AMF infection characteristics on plant C, N,
and P stoichiometry when soil properties was considered.
2. Materials and methods
2.1 Study site description
West Lake located in the west region of urban area of Hang-
zhou, China, with a lake area of 6.38 km
2
. It is surrounded by
mountains except the east side. The nearly oval lake owns a at
and shallow bottom with an average depth of 2.27 m. For the
west Lake, its average annual total solar radiation ranged from
100 to 110 kcal cm
1
,
2
whereas its average annual sunshine
hours ranged from 1800 to 2100 hours. From the 1950s to the
1980s, due to the rapid economic development and the
increasing pressure of the West Lake tourism load, water quality
for West Lake was worsening. The eutrophication of the water
body frequently occurred, cyanobacteria multiplied, the aquatic
vegetation system collapsed, and the water environment dete-
riorated. Although water quality of West Lake has been
improved as a result of ecological restoration projects in the
past four decades, further studies were still needed to remediate
the water quality and elucidate the underlying mechanisms.
2.2 Field sampling
Four articial emergent plants restoration sites Jin Sha Gang
(S1), Mao Jia Bu (S2), Wu Gui Tan (S3), Yu Hu Wan (S4) were
chosen (Fig. 1). The dominated emergent plants Phragmites
Fig. 1 Locations of four sampling sites along the West Lake, Hangzhou, China.
39944 |RSC Adv.,2020,10, 39943–39953 This journal is © The Royal Society of Chemistry 2020
RSC Advances Paper
australis,Zizania latifolia,Scirpus validus, and Lythrum salicaria
and corresponding surface soil samples (0–10 cm depth) were
collected from four sites S1–S4, respectively. In each site, three
plots of 2 m 2 m (length width) following similar envi-
ronmental characteristics and vegetation were established.
Plants derived from three 0.25 m
2
quadrats at random locations
within every sampling sites were selected and divided into two
different parts: aboveground biomass (including the leaf and
stem) and root. Root systems with adherent soils were carefully
collected to protect the feeder roots, sealed in polyethylene bags
and brought back to the lab at 4 C for further analysis.
2.3 AMF infection in roots of emergent plants
To determine the characteristics of AMF infection in the roots of
emergent plants, the rates of AMF infection were calculated as
previously reported.
23
Briey, the roots were cut into 1.0 cm
segments, xed in 3% glutaraldehyde at 4 C for 24 h, washed
thrice in 0.1 M sodium cacodylate buffer followed by a dehy-
dration in a graded series of acetone. The stained root segments
suspended in lactoglycerol was randomly chosen, spread in
a 60 mm Petri dish, and observed under a stereomicroscope
Nikon Eclipse 80i (Nikon, Tokyo, Japan). The different coloni-
zation patterns such as the structures of arbuscular, vesicular,
and hyphae were investigated. The different colonization
patterns such as the frequency of infection (F), the rate of
infection (R), the rate of arbuscular formation (AR), and the rate
of vesicular formation (VR) were performed using the magnied
intersection method.
24
2.4 Isolation and identication of AMF spore in soils
The isolation of AMF spores were performed using wet-sieving
and sucrose density gradient centrifugation methods.
25
Briey, AMF spores were picked up using a micropipetter under
a stereomicroscope from 10 g soil. The isolated spores were
identied morphologically based on their sizes, colors, surface
ornamentation, spore contents and wall structure.
26
2.5 Chemical analysis of plants
The plants were washed thrice with deionized water, dried at
105 C for 15 min and 80 C until reaching constant weight.
27
Then, the dried plant samples were grounded, sieved, and ali-
quoted for further analysis. Aer digestion in sulfuric acid, total
C (TC) and total N (TN) in the plants were analyzed using a high
sensitivity elemental analyzer system (Vario TOC cube, Hanau,
Germany), whereas total P (TP) contents were digested by
sulfuric acid and analyzed via a spectrophotometer using the
molybdenum blue method (UV-1900, SHIMADZU, Japan).
28
Plant TC, TN, and TP contents were presented as mg TC/TN/TP
per g plant dry weight.
2.6 Chemical analysis of soils
The soils were air dried for 30 days, ground, and sieved. Soil
total C (STC), soil total N (SCN), and soil total P (STP) were
determined as above mentioned. In order to measure the
contents of STP, the soils were heated at 450 C for 3 h, digested
in muriatic acid for 16 h, and determined by the ascorbic acid
method.
29
Soil STC, STN, and STP contents were presented
as mg STC/STN/STP per g soil dry weight. Oxidation–reduction
potential (ORP) were determined using an Orion 5-Star Portable
Multimeter. Soil pH was determined using a pH/conductivity
meter using a soil-to-water solution diluted in 1 : 5.
2.7 Statistics
The normality of data distribution was rstly assessed using the
Shapiro–Wilk test. When necessary, data were logarithmically
or Box-Cox transformed to achieve normality. One-way ANOVAs
were performed to analyze the differences among AMF infection
characteristics, plant C, N, and P contents and their stoichio-
metric ratios in four types of emergent plants, followed by
a Tukey post-hoc tests. Pearson correlation coefficient's r, with p
< 0.05, were utilized to determine the correlations between AMF
infection characteristics and plant stoichiometric ratios or soil
properties. Then, redundancy analysis (RDA) were employed to
determine relative contributions of soil properties to the
composition of plant communities using the Canoco for
Windows 4.5 package. Statistical procedures were performed
using the SPSS 20.0 soware. Differences were declared signif-
icant at P< 0.05 unless otherwise stated.
To further investigate potential direct and/or indirect effects
of crucial explanatory variables on AMF infections in the roots
of emergent plants, we have performed path analysis using full
information maximum likelihood estimation method.
30
Firstly,
a conceptual path model has been built on the basis of the
literature and the author's experience of wetland restoration
(Fig. S1†). Secondly, potential explanatory variables were chosen
Table 1 AMF infection characteristics of emerged plant in lakeshore wet zone
a
Plants Types
AMF
FRAR VR
Phragmites australis Intermediate 85.67 3.05
a
67.49 2.40
b
62.56 2.23
a
55.04 1.96
b
Phalaris arundinacea Intermediate 87.79 4.88
a
39.01 2.17
a
70.93 3.94
a
79.19 4.40
c
Scirpus validus Arum 97.93 3.58
b
76.53 3.41
c
65.85 2.93
a
44.22 1.97
a
Lythrum salicaria Arum 97.53 4.27
b
87.38 5.00
d
82.84 4.74
b
73.19 4.18
c
a
F: infection frequency (%); R: infection rate (%); AR: rate of arbuscular mycorrhiza formation aer root infection (%); FR: rate of vesicle formation
aer root infection (%). The different lowercase letters indicated signicant differences (p< 0.05) among different plant communities.
This journal is © The Royal Society of Chemistry 2020 RSC Adv.,2020,10,39943–39953 | 39945
Paper RSC Advances
and used in the path analysis on the basis of Pearson's analysis
and RDA. Correspondence analysis (CA) was performed to
reduce variable numbers of AMF infection characteristics, soil
properties, plant stoichiometry (Table S1†). The rst principal
component for each CA analysis was assigned into the next path
analysis. Thirdly, the path coefficients, direct and indirect
effects, and the model t parameters were analyzed using AMOS
version 20.0 soware packages. The path model nally
conrmed was considered as acceptable t to the data when the
value for the comparative t index was greater than 0.9 and root
square error of approximation was less than 0.1, respectively.
3. Results
3.1 Determination of AMF infection characteristics and the
diversity of AMF spores
Infection characteristics of AMF in roots of emergent plants
were shown in Table 1. The infection frequencies (F) of AMF in
Phragmites australis (85.67%) and Phalaris arudicacea (87.79%)
were signicantly lower than those in Scirpus validus (97.73%)
and Lythrum salicaria groups (97.53%) (p< 0.05). Meanwhile,
the highest infection rate (R) and the rate of arbuscular
mycorrhiza formation (AR) of four emergent plants were
detected in Lythrum salicaria (87.38% and 82.24%). For the rate
of vesicle formation (VF), the values in Phragmites australis and
Scirpus validus were 55.04% and 44.22%, which were consider-
ably lower than those in Phalaris arundinacea (79.19%) and
Lythrum salicaria (73.19%) (p< 0.05).
AMF spores was isolated and identied from the rhizosphere
soil of the plants (Fig. 2). There were 24 types of known species
of AMF spores. Among them, the most abundant spore species
was Glomus melanosporum, which was 24.58 in 100 g dry soil and
accounted for 25.10% in the whole spores. Meanwhile, there
were ve other types of spore species, Scutellospora nigra,
Glomus mosseae,Scutellospora calospora,Acaulospora dilatata,
and Glomus aureum, whose ratios were 13.77%, 12.78%, 3.93%,
3.34%, and 3.05%, respectively.
3.2 Measurement of soil properties
The concentrations of STC and STN in root rhizosphere soils
ranged from 38.29 g kg
1
to 130.33 g kg
1
, and 1.12 g kg
1
to
5.07 g kg
1
, respectively, and the highest contents were detected
in Lythrum salicaria (Table 2). Meanwhile, the contents of STP in
root rhizosphere soils varied from 0.67 g kg
1
to 2.11 g kg
1
,
while the value in Phragmites australis was signicantly higher
compared with those in the other three emergent plants. Soil
ORP and pH covered the range from 35.19 to 34.32, and 6.19
to 7.16, respectively. Phragmites australis had the lowest soil
ORP, while there was no signicant differences in pH among
the four emergent plants.
3.3 C, N, and P contents and their stoichiometric ratios in
emergent plants
For the aboveground biomass of emergent plants, their average
contents of C, N, and P elements were 439.88 g kg
1
, 16.06 g
kg
1
, and 2.20 g kg
1
, respectively. Meanwhile, for the roots of
emergent plants, their contents of C, N, and P elements aver-
aged at 405.82 g kg
1
, 11.60 g kg
1
, and 2.03 g kg
1
, respectively
(Fig. 3). For the C content, the value of Phragmites australis in
aboveground biomass was higher compared with those in the
other three emergent plants, while the highest C content in root
has been observed in Lythrum salicaria. The N content in
aboveground biomass of Phragmites australis was signicantly
higher compared with those of the other three emergent plants,
and Scirpus validus the highest value in root. Besides, the P
Fig. 2 Infection characteristics of AMF in emerged aquatic plants in
West Lake. (A) Representative microscopic images of typical AMF
infection in emerged aquatic plants Phragmites australis and Lythrum
salicaria. Solid arrow: dark septate hyphae; dotted arrow: vesicle.
Magnifications: 400; (B) representative images of AMF spores
observed in the roots of emerged aquatic plants. Magnifications:
400; (C) biodiversity and relative ratios of AMF spore species in
emerged plants.
39946 |RSC Adv.,2020,10, 39943–39953 This journal is © The Royal Society of Chemistry 2020
RSC Advances Paper
values of Zizania latifolia in aboveground biomass and root were
remarkably higher compared with those of the other three
groups.
For the C/N, the ratio of Scirpus validus in aboveground
biomass was signicantly higher compared with those in the
other three groups, while the highest C/N ratio in root has been
observed in Lythrum salicaria (Fig. 4). Meanwhile, the C/P ratio
in aboveground biomass of Lythrum salicaria was remarkably
higher than those of the other three groups, and Phragmites
australis had the highest value in root. Besides, the N/P ratios of
Phragmites australis in both aboveground biomass and root
were considerably higher than those of the other three groups.
3.4 Relationships among AMF infection characteristics,
plant C, N, P stoichiometry, and soil properties
AMF infection frequency exhibited a signicant and negative
correlation with the content of N in aboveground biomass
Table 2 Soil properties in the rhizosphere of emerged plants in lakeshore wet zone
a
Plants STC (g kg
1
) STN (g kg
1
) STP (g kg
1
) OPR pH
Phragmites australis 38.29 4.29
a
1.12 0.21
a
2.11 0.27
c
35.19 3.07
a
6.19 0.65
Phalaris arundinacea 57.84 11.87
ab
1.77 0.35
a
1.62 0.09
b
26.65 10.18
b
6.89 0.30
Scirpus validus 83.30 6.30
b
3.21 0.76
b
1.27 0.08
b
34.32 2.76
b
7.06 0.33
Lythrum salicaria 130.33 28.08
c
5.07 0.69
c
0.67 0.20
a
32.49 8.37
b
7.16 0.39
a
The different lowercase letters indicated signicant differences (p< 0.05) among different plant communities.
Fig. 3 C, N, and P contents of the emerged plants in West Lake. (A) C contents of the aboveground biomass (left panel) and roots (right panel) of
the emerged plants, Phragmites australis,Zizania latifolia,Scirpus validus, and Lythrum salicaria; (B) the N contents of the aboveground biomass
(left panel) and roots (right panel) of the emerged plants, Phragmites australis,Zizania latifolia,Scirpus validus, and Lythrum salicaria; (C) the P
contents of the aboveground biomass (left panel) and roots (right panel) of the emerged plants, Phragmites australis,Zizania latifolia,Scirpus
validus, and Lythrum salicaria.
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Paper RSC Advances
Fig. 4 C, N, and P stoichiometry of the emerged plants in West Lake. (A) The C/N ratios of the aboveground biomass (left panel) and roots (right
panel) of the emerged plants, Phragmites australis,Zizania latifolia,Scirpus validus, and Lythrum salicaria, respectively; (B) the C/P ratios of the
aboveground biomass (left panel) and roots (right panel) of the emerged plants, Phragmites australis,Zizania latifolia,Scirpus validus, and Lythrum
salicaria, respectively; (C) the N/P contents of the aboveground biomass (left panel) and roots (right panel) of the emerged plants, Phragmites
australis,Zizania latifolia,Scirpus validus, and Lythrum salicaria, respectively.
Table 3 Pearson correlation coefficients between AMF infection characteristics and C, N, and P contents and their stoichiometric ratios of plant
communities
c
Items
AMF infection characteristics
F(%) R(%) AR (%) FR (%)
Aboveground biomass C (g kg
1
)0.049 0.528 0.194 0.445
Root C (g kg
1
)0.002 0.326 0.573 0.478
Aboveground biomass N (g kg
1
)0.607
a
0.237 0.223 0.189
Root N (g kg
1
)0.205 0.183 0.864
b
0.768
b
Aboveground biomass P (g kg
1
) 0.324 0.873
b
0.198 0.357
Root P (g kg
1
) 0.228 0.389 0.103 0.174
Aboveground biomass C/N 0.566 0.344 0.054 0.401
Root C/N 0.209 0.246 0.868
b
0.739
b
Aboveground biomass C/P 0.275 0.858
b
0.146 0.383
Root C/P 0.417 0.251 0.212 0.144
Aboveground biomass N/P 0.364 0.222 0.082 0.002
Root N/P 0.487 0.029 0.810
b
0.634
a
a
p< 0.05.
b
p< 0.01.
c
F: infection frequency (%); R: infection rate (%); AR: rate of arbuscular mycorrhiza formation aer root infection (%); FR: rate
of vesicular formation aer root infection (%).
39948 |RSC Adv.,2020,10, 39943–39953 This journal is © The Royal Society of Chemistry 2020
RSC Advances Paper
(Table 3). The rate of infection was signicantly positive asso-
ciated with the aboveground biomass P and aboveground
biomass C/P (p< 0.01). Meanwhile, both AR and FR exhibited
signicant and negative relationships with root N, and root N/P,
respectively (p< 0.01). Besides, root C/N was positively related to
AR, and negatively correlated with FR (p< 0.01).
STC and STN showed signicantly positive correlations with
AMF infection frequency (p< 0.01), infection rate (p< 0.05), and
AR (p< 0.01), respectively (Table 4). Similarly, STP was signi-
cantly negatively correlated with AMF infection frequency,
infection rate, and AR (p< 0.01), respectively. Besides, ORP had
signicant positive association with AMF infection frequency
and AR, respectively. No signicant correlation was detected
between pH and infection frequency, infection rate, AR, and FR,
respectively.
RDA analysis results in Fig. 5 demonstrated that axis 1 and
axis 2 accounted for 42.37% and 29.42% of the total variation,
respectively. Soil properties explained 72.9% of the total varia-
tion in the contents of C, N, and P elements and their stoi-
chiometric ratios in emergent plants. The results of Monte
Carlo permutation test demonstrated that all axes were signif-
icant (F-ratio ¼3.2, P-value ¼0.006). According to the centroid
principle and distance rule, the contents of P in soils showed
positive correlations with N contents of aboveground biomass,
root N contents and root N : P ratios. Meanwhile, there were
positive associations between soil C and N contents, and root
C : N ratios and C contents, respectively. Additionally, the
aboveground biomass C : N ratios and P contents, and root P
contents, showed positive correlations with soil ORP and pH,
respectively, whereas C content, N/P ratio of aboveground
biomass, and root C/P showed signicantly negative relation-
ships with soil ORP and pH, respectively (Fig. 5).
3.5 Direct and indirect effects of explanatory variables on
plant C, N, P stoichiometry
To further elucidate the interaction between AMF and soil
properties jointly inuences plant C, N, and P stoichiometry,
pathway analysis was performed and shown in Fig. 6. In the
path model, soil C, N, and P contents and ORP could regulate
plant C, N, and P stoichiometry both directly and indirectly. Soil
C, N, and P contents had signicant direct inuences on plant
C, N, and P contents and AMF infection characteristics. Simi-
larly, ORP showed strong and signicant negative effects on
both plant C, N, and P contents and their stoichiometric ratios.
Besides, AMF infection characteristics had relatively large but
nonsignicant effects on both plant C, N, and P contents and
their stoichiometric ratios.
Table 4 Pearson correlation coefficients between AMF infection
characteristics and soil properties
c
Items
AMF infection characteristics
F(%) R(%) AR (%) FR (%)
STC (g kg
1
) 0.721
b
0.641
a
0.810
b
0.226
STN (g kg
1
) 0.739
b
0.688
a
0.770
b
0.246
STP (g kg
1
)0.780
b
0.578
a
0.820
b
0.147
ORP 0.686
a
0.106 0.592
a
0.226
pH 0.347 0.326 0.221 0.135
a
p< 0.05.
b
p< 0.01.
c
F: infection frequency (%); R: infection rate (%);
AR: rate of arbuscular mycorrhiza formation aer root infection (%); FR:
rate of vesicle formation aer root infection (%).
Fig. 5 RDA ordination plots of C, N, and P contents and their stoi-
chiometric ratios of different plants and soil properties in West Lake.
Abbreviations: Above C, aboveground biomass C; Above N, above-
ground biomass N; Above P, aboveground biomass P; Above C : N,
aboveground biomass C : N; Above C : P, aboveground biomass C : P;
Above N : P, aboveground biomass N : P.
Fig. 6 Path diagrams estimating the effects of soil environmental
factors, and AMF infection characteristics on plant C, N, and P contents
and their stoichiometric ratios in emerged plants. Solid lines indicate
significant effects (p< 0.05), while dashed lines demonstrate insig-
nificant effects. The values for standard path coefficients were marked
adjacent to the arrows.
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Paper RSC Advances
4. Discussion
4.1 AMF infection characteristics, spore count, and diversity
Our results demonstrated that both AMF infection frequencies
(>85.67%) and infection rates (39.01–87.38%) in four emergent
plants were relative high (Table 1), suggesting a potential good
mutualistic symbiosis between AMF and emergent plants. A
total of 28 AMF spore species observed in emergent plants in the
present study was nearly the same as that (29 species) reported
in soils from three plantation sites in Meghalaya, northeast
India.
31
Compared with approximately 240 recognized AMF
species,
32
the number of AMF spores observed in the current
study were relative high due to the lack of host specicity.
33
Meanwhile, the number of AMF spore species observed here
was also higher than the numbers of those (21–23) reported in
the Tibet Plateau.
34,35
This difference on the AMF spore diversity
may be due to the altitude, which was negatively related to the
diversities of AMF.
36–38
Moreover, the AMF infection rates
observed in the present study were much higher than those
reported in acidic soils (21–43.67%).
39,40
This discrepancy may
be ascribed to the differences in pH, which may negatively affect
root colonization in the acidic range.
41
The pH values of plant
rhizosphere soils in this study were all close to 7.0, which was
benecial for the growth of AMF and plants. However, it should
be noted that many other factors such as temperature,
42,43
light,
44
plant competitors
45
and pathogens
46
may also be
involved in determining the mutualism between AMF and
emergent plants.
4.2 Correlations between AMF and plant C, N, and P
contents and their stoichiometry
C, N, and P contents and their stoichiometric ratios were
powerful indicators of multiple ecological processes, which
played important roles in physiological traits
47
and the evalua-
tion of nutrient limitation for plant growth.
48
For example, an
N : P ratio >16 might suggest a limitation of P element, while
the value <14 meant a limitation of N element.
49,50
In the current
study, all values of plant N : P ratios were <12, suggesting the
presence of N limitation in these plants. This revealed that
limited supply of N may be a possible explanation of high
infection rates of AMF observed in the present study, which
promote the uptake of N element and plant growth.
51
Our
results supported the conclusion of Vries et al. (2011), who re-
ported that a higher AMF biomass was probably the result of
low N concentration rather than the direct cause of higher N
retention in two grassland soils.
52
Moreover, AMF infection
rates (R) exhibited a signicant positive relationship with P
contents in aboveground biomass, suggesting that mycorrhizal
growth response in plants was mainly due to increased photo-
synthesis and P allocation in the aboveground biomass (Table
3). Additionally, high AMF infection rates increased uptake of
other growth-limiting nutrients such as K
+
, and then enhanced
the uptake of P and plant growth.
39
The negative correlations between AR/FR rates and root N/
root N/P shown in Table 3, indicated that high AR/FR rates of
AMF reduced the allocation of N element in the plant roots. This
reduced N allocation was consistent with the observation that
AMF negatively affects nitrogen acquisition and grain yield of
maize in a N-decient soil.
53
Meanwhile, N limitation in soils
can impair plant control over the AMF-plant symbiosis and
result in the a shiof symbiosis to commensalism even para-
sitism.
54
Therefore, homeostatic regulation of C : N : P ratio
rather than simple N supply in the soil of West Lake is necessary
to improve the interaction between AMF and plants. This was
because that a reduction of N content below the minimum
requirement for maintaining cell functions resulted in the
senescence of tissues,
55
whereas excessive N supply will lead to
toxic effects in plants, especially those adapted to nutrient-poor
soils.
56
In addition, it's also generally acknowledged that the
magnitude of the effect of AMF on the performance of plant
species was species specic.
57
Therefore, the exact relationship
between AMF infection characteristics and plant C, N, and P
contents and stoichiometric ratios in emergent plants still
needs further investigations.
4.3 Relationship between AMF biodiversity and soil
properties
The relationship between AMF and soil properties was interde-
pendent. On the one hand, AMF can provide multiple benets for
the soils. A previous study reported that AMF can enhance the
health conditions of soil by regulating soil food web and main-
taining soil structure through their external hyphae.
58
Similarly,
AMF can regulate soil respiration and its response to precipita-
tion changes a semiarid steppe.
59
Moreover, the presence of AMF
in soil can induce shis in soil microbial communities, such as
N-cycling related denitrication organisms,
60
which also partici-
pated in the reduction of N loss. On the other hand, based on the
trade balance model hypothesized by Johnson, the functions of
AMF symbiosis mainly depended on N, P availability and their
stoichiometric ratios.
61
According to Johnson's theory, the
mutualistic benets were mostly expected when the contents ofN
and P were high and low, respectively, in the rhizosphere soils.
However, the contents of both N and P in the soils were low, both
the frequencies and rates of AMF infection were very high in
three of four sampled plants in the present study. The content of
P<3gkg
1
observed in the current study was higher than that in
Lythrum salicaria L., where it was colonized by AMF only when the
content of P in hydroponic sand culture was below 1 g L
1
.
62
The
discrepancy on the AMF infection rates between our experiment
and White's may be ascribed to the limited levels of P availability
in Lythrum salicaria L., which were only set at 0, 0.1, 1, 10, and
47.5 g PO
4
per L, respectively.
62
Meanwhile, Pearson's analysis in
Table 4 demonstrated that ORP showed signicant and positive
correlations with AMF infection frequency and rate of AR,
respectively (p< 0.05). This positive correlation may be due to that
a higher ORP means relative sufficient oxygen, which will
promote the growth of eutrophic fungi AMF.
4.4 Interactions between AMF and soil properties altering
plant C, N, and P stoichiometry
Our results of RDA analysis in Fig. 5 demonstrated that the soil
properties explained 72.9% of the total variation in the contents
39950 |RSC Adv.,2020,10, 39943–39953 This journal is © The Royal Society of Chemistry 2020
RSC Advances Paper
of C, N, and P and their stoichiometric ratios in plants. These
data suggest that soil properties affect the plant C, N, and P
contents and their stoichiometric ratios. This conclusion was
consistent with the ndings in plants, where C, N, and P
ecological stoichiometric ratios of plant aboveground biomass
were regulated by STC, STN and STP.
18,27
Meanwhile, the result
of path analysis in Fig. 6 demonstrated that soil ORP also
exerted signicant and negative effect on plant C, N, and P
contents (1.307) and their stoichiometry (1.197), respec-
tively. This could be attributed to that a lower ORP would be
benecial for the metabolism of the plant, which in turn
promoted the uptake of soil nutrient especially C, N, and P.
63
These data revealed that soil properties can alter plant ecolog-
ical stoichiometry directly.
The West Lake as an urban lake with a long history, was
mainly polluted by high organic matter pollution load with
a high degree of sediment humication.
22
Meanwhile, the
contents of N, P in the sediments of the West Lake were also
very high and exerts important impact on the release of
endogenous nitrogen and phosphorus.
22
These characteristics
of West Lake sediments increased the difficulty of lake water
restoration. Moreover, we found that the pH of rhizosphere soil
of emergent plants mainly ranged from 6.89 to 7.16, which
showed no signicant correlation with the C, N, and P stoichi-
ometry or AMF infection characteristics in this study (Table 2).
Based on these information, the control of endogenous
nitrogen and phosphorus release need to be take into consid-
eration during the future of West Lake water restoration.
The result of path analysis in Fig. 6 demonstrated that STC,
STN, and STP (0.981) had positive and signicant effects on
AMF. Meanwhile, the effects of AMF on plant C, N, and P
contents (0.375) and stoichiometry (0.348) was marginally
signicant. These data suggested that soil properties could also
affect plant ecological stoichiometry via AMF indirectly, which
may be a possible explanation for the unexplained variations in
plant C, N, and P contents and their stoichiometry. Meanwhile,
our results were in consist with that of Battini et al., who re-
ported that AMF and their associated bacteria could enhance
the growth and P uptake in maize.
64
Together, soil properties can affect the plant ecological
stoichiometry directly and indirectly via the AMF mycorrhizal.
Interactions between soil properties and AMF also play a crucial
role in regulating plant ecological stoichiometry, which may be
a possible explanation for the uncertain roles of AMF in
different ecological systems. Based on the tight relation
between soil and AMF, we propose that soil and AMF can be
treated as a whole in exploring their effects on plant ecological
stoichiometry and/or performances when necessary.
5. Conclusions
In summary, our data demonstrated that the frequencies and
rates of AMF infection in emergent plants in West Lake,
Hangzhou, China were relatively high. Both AMF infection rates
and AMF spore species showed a high diversity, suggesting
a good mutualism between AMF and plant. The limitation of N
element in the rhizosphere soil reduced the N/P ratio to
promote the growth of aboveground biomass. Soil properties
can affect the plant ecological stoichiometry directly and indi-
rectly via the AMF mycorrhizal pathway. Therefore, AMF and
plant root rhizosphere soil should be considered as a whole in
exploring the factors, which affected the growth and tness of
plants. This new perspective will be helpful in clarifying the
relationships among AMF, plants and soils and providing
theoretical support for the restoration and reconstruction of
lake aquatic vegetation. Further investigations are needed to the
elucidate the possible relations between C : N : P stoichiometry
and compounds/biomolecules, which could be considered as
possible biomarkers of the infection process of emergent plants
by the AMF.
Conflicts of interest
There are no conicts to declare.
Acknowledgements
This work was supported by the National Natural Science
Foundation of China [Grant number 51709255]; the CRSRI
Open Research Program [grant number CKWV2019769/KY]; and
Key Laboratory Construction of Hubei Province [grant number
2018BFC360].
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