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Nitrogen acquisition strategy and
its effects on invasiveness of a
subtropical invasive plant
Ming Guan
1,2
†
, Xiao-Cui Pan
2
†
, Jian-Kun Sun
1
, Ji-Xin Chen
1
,
De-Liang Kong
3
and Yu-Long Feng
1
*
1
Liaoning Key Laboratory for Biological Invasions and Global Changes, College of Bioscience and
Biotechnology, Shenyang Agricultural University, Shenyang, Liaoning, China,
2
Zhejiang Provincial Key
Laboratory of Plant Evolutionary Ecology and Conservation, School of Life Sciences, Taizhou
University, Taizhou, Zhejiang, China,
3
College of Forestry, Henan Agricultural University, Zhengzhou,
Henan, China
Introduction: Preference and plasticity in nitrogen (N) form uptake are the main
strategies with which plants absorb soil N. However, little effort has been made to
explore effects of N form acquisition strategies, especially the plasticity, on
invasiveness of exotic plants, although many studies have determined the
effects of N levels (e.g. N deposition).
Methods: To address this problem, we studied the differences in N form
acquisition strategies between the invasive plant Solidago canadensis and its
co-occurring native plant Artemisia lavandulaefolia, effects of so il N
environments, and the relationship between N form acquisition strategy of S.
canadensis and its invasiveness using a
15
N-labeling technique in three habitats at
four field sites.
Results: Total biomass, root biomass, and the uptakes of soil dissolved inorganic
N (DIN) per quadrat were higher for the invasive relative to the native species in all
three habitats. The invader always preferred dominant soil N forms: NH
4+
in
habitats with NH
4+
as the dominant DIN and NO
3-
in habitats with NO
3-
as the
dominant DIN, while A. lavandulaefolia consistently preferred NO
3-
in all habitats.
Plasticity in N form uptake was higher in the invasive relative to the native species,
especially in the farmland. Plant N form acquisition strategy was influenced by
both DIN levels and the proportions of different N forms (NO
3-
/NH
4+
) as judged
by their negative effects on the proportional contributions of NH
4+
to plant N
(f
NH4+
) and the preference for NH
4+
(b
NH4+
). In addition, total biomass was
positively associated with f
NH4+
or b
NH4+
for S. canadensis, while negatively for A.
lavandulaefolia. Interestingly, the species may prefer to absorb NH
4+
when soil
DIN and/or NO
3-
/NH
4+
ratio were low, and root to shoot ratio may be affected by
plant nutrient status per se, rather than by soil nutrient availability.
Discussion: Our results indicate that the superior N form acquisition strategy of
the invader contributes to its higher N uptake, and therefore to its invasiveness in
different habitats, improving our understanding of invasiveness of exotic plants in
diverse habitats in terms of utilization of different N forms.
KEYWORDS
exotic plant invasion, nitrogen form preference, nitrogen levels,
15
N labeling, plant
nitrogen form acquisition strategy, plasticity in nitrogen form uptake
Frontiers in Plant Science frontiersin.org01
OPEN ACCESS
EDITED BY
Shen Shicai,
Yunnan Academy of Agricultural Sciences,
China
REVIEWED BY
Bo Liu,
Chinese Academy of Agricultural Sciences,
China
Xiao Guo,
Qingdao Agricultural University, China
Yulong Zheng,
Chinese Academy of Sciences (CAS), China
*CORRESPONDENCE
Yu-Long Feng
fyl@syau.edu.cn
†
These authors have contributed equally to
this work
RECEIVED 21 June 2023
ACCEPTED 03 August 2023
PUBLISHED 21 August 2023
CITATION
Guan M, Pan X-C, Sun J-K, Chen J-X,
Kong D-L and Feng Y-L (2023) Nitrogen
acquisition strategy and its effects on
invasiveness of a subtropical invasive plant.
Front. Plant Sci. 14:1243849.
doi: 10.3389/fpls.2023.1243849
COPYRIGHT
© 2023 Guan, Pan, Sun, Chen, Kong and
Feng. 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 copyright owner(s) are
credited and that the original publication in
this journal is cited, in accordance with
accepted academic practice. No use,
distribution or reproduction is permitted
which does not comply with these terms.
TYPE Original Research
PUBLISHED 21 August 2023
DOI 10.3389/fpls.2023.1243849
1 Introduction
Invasions by exotic plant species can not only severely affect
species composition, structure, and function of invaded ecosystems,
but also pose a serious threat to the social economy (Chen et al.,
2016;Kerr et al., 2016;Iqbal et al., 2020;Kumar Rai and Singh, 2020;
Zhao et al., 2020). Many studies have focused on understanding
how exotic plants successfully invade new environments, and how
to predict and prevent exotic plant invasions (Catford et al., 2009;
Lau and Schultheis, 2015;Enders et al., 2020;Huang et al., 2020;Liu
et al., 2022). It is generally believed that high competitiveness and
adaptability to new environments contribute to successful invasion
of exotic plants (Blossey and Notzold, 1995;Feng et al., 2009;Liao
et al., 2020;Zheng et al., 2020). The efficient absorption and
utilization of soil nitrogen (N) is one of the key functional traits
that endow invasive plants with competitive advantages (Castro-
Dı
ez et al., 2014;Parepa et al., 2019;Huang et al., 2020;Liu et al.,
2022;Luo et al., 2022;Guo et al., 2023). Thus, understanding how
invasive plants gain advantages in soil N uptake over natives can
provide an important scientific basis for the effective prediction and
prevention of exotic plant invasions.
Plants can directly absorb nitrate (NO
3-
), ammonium (NH
4+
)
and N-containing organic micromolecules such as amino acids
from soils (McKane et al., 2002;Houle et al., 2014;Sun et al., 2021).
However, different plant species have different abilities to absorb
these N forms due to many reasons, for example their contents and
proportions in soils, differences in their mobility in soils (Brady and
Weil, 1999) and energy consumption when assimilated in cells
(Salsac et al., 1987), and the interspecific differences in expressions
of various N transport genes for absorbing different N forms (Luo
et al., 2022;Zhang et al., 2022a), sensitivities to NH
4+
toxicity
(Britto and Kronzucker, 2002;Zhang et al., 2022b), and associations
with symbiotic microorganisms. Some plants show preferences for a
particular form of soil N, regardless of the availability of alternative
N forms (Huangfu et al., 2016;Chen and Chen, 2018;Tang et al.,
2020;Luo et al., 2022;Zhang et al., 2022a). For example, Rice (Oryza
sativa), Xanthium sibiricum and invasive plant Flaveria bidentis
prefer to absorb NH
4+
,whilewheat(Triticum aestivum), the
invasive plant X. strumarium and Ipomoea cairica prefer to
absorb NO
3-
(Li et al., 2013;Huangfu et al., 2016;Chen and
Chen, 2018;Luo et al., 2022). Some plants can adjust their uptake
of different N forms according to their proportions in soil, i.e.,
showing plasticity in N form uptake (Andersen and Turner, 2013;
Russo et al., 2013;Sun et al., 2021). It has been found that plants
have different absorption capacities and preferences for different
soil N forms in different habitats (Averill and Finzi, 2011;Wang and
Macko, 2011;Boczulak et al., 2014). Compared with the plants that
always prefer a specific N form in different habitats, plants with
plasticity in N form uptake may have advantage in N acquisition,
contributing to increasing their competitiveness and making them
superior competitors. Numerous studies have demonstrated that
the main soil N form (Its content is higher than those of others)
varies in different habitats (Wilson et al., 2005;Zhang et al., 2013).
Ammonium is the main N form in infertile or acidic (especially
hypoxic) soils (Wilson et al., 2005;Zhang et al., 2013), while NO
3-
in
fertile aerated or alkaline (including neutral) soils (Wilson et al.,
2005). However, few studies have investigated the main soil N
forms, N form acquisition strategies, and their relationship for a
given plant in different habitats.
Like superior competitors in alpine tundra (Ashton et al., 2010),
alpine meadow (Song et al., 2015), and subalpine coniferous forest
(Zhang et al., 2018), invasive plants may have higher plasticity in N
form uptake than co-occurring natives, or preferentially utilize the
main soil N form in different habitats. If so, the invaders will be
better adapted to the variations in N sources within and across
various habitats, and will be able to acquire more quantities of soil
N. Such N uptake strategies can give invasive plants a competitive
advantage over natives, promoting their successful invasion.
However, few studies have focused on the plasticity in N form
uptake of invasive plants. The habitats of invasive plants are diverse,
and the contents and relative proportions of NH
4+
and NO
3-
in soils
exhibit a high degree of spatial and temporal heterogeneity
(Andersen and Turner, 2013). The heterogeneity in soil N forms
and the differences in plant N form acquisition strategies may
inevitably affect the distribution of invasive plants, and the
expression of their invasiveness (Yu and He, 2021a;Yu and He,
2021b). However, very few studies have explored the impacts of the
contents and proportions of different soil N forms on N form
acquisition strategies of invasive plants, and their relationships with
their successful invasion.
Solidago canadensis, native to North America, is a highly
invasive and destructive weed in many countries. It is now widely
distributed throughout the eastern and southern provinces of
China. S. canadensis has caused serious damage to native
ecosystems and economic development (Lu et al., 2005;Li et al.,
2016b). A previous study has shown that S. canadensis grows larger
and has greater chlorophyll content, higher root biomass allocation
and stronger low-N tolerance than its congeneric native species
under different NO
3-
/NH
4+
ratios and levels (Yu and He, 2021a).
However, it is unclear whether or how the N form acquisition
strategy of S. canadensis changes with varying soil N levels and the
proportions of different N forms, and how these characteristics
affect its invasiveness.
In this study, we measured the contents and the proportions of
different N forms in rhizosphere soils of S. canadensis and its co-
occurring native plant Artemisia lavandulaefolia, and their N form
acquisition strategies using
15
N-labelling technique. In order to
increase the variations in soil N contents and the proportions of
different N forms, this study was conducted in three habitats
(farmland, wasteland, and roadside) at four sites, where S.
canadensis invades seriously. The main purposes of this study
were to explore: (1) the differences in N form acquisition
strategies between S. canadensis and A. lavandulaefolia in
different habitats; (2) the effects of the variations in soil N
contents and the proportions of different N forms on N form
acquisition strategies of the invasive and native plants; and (3) the
effects of N form acquisition strategy of S. canadensis on its
invasiveness. We hypothesize that compared with the native plant
the invader may have higher ability to adjust their absorption of
different N forms according to their availability in soils, i.e., showing
higher plasticity in N form uptake, and thus absorb more N in each
habitat, contributing to its invasiveness. This study is significant for
Guan et al. 10.3389/fpls.2023.1243849
Frontiers in Plant Science frontiersin.org02
understanding the effects of N acquisition strategies on invasion
success of exotic plants, and also provides a theoretical basis for
predicting future spread of invasive plants, and making strategies to
manage them.
2 Materials and methods
2.1 Study sites
Our study was conducted in August of 2020 at four sites in
Zhejiang Province, east China: Ningbo (29°54′N, 121°26′E; 4 m
asl), Xiangshan (29°22′N, 121°45′E; 135 m asl), Taizhou (28°52′N,
120°55′E; 211 m asl), and Wenzhou (27°56′N, 120°42′E; 5 m asl).
These sites were all heavily invaded by S. canadensis. There is a
typical subtropical monsoon climate in these sites, with a mean
annual temperature (MAT) of 16°C –19°C, and a mean annual
precipitation (MAP) of 1200 –1900 mm. In each site, farmland,
wasteland, and roadside were chosen as study habitats, where soil N
contents and the proportions of different N forms may be different
(Li et al., 2014;Zhou et al., 2015;Zhao et al., 2017). The farmlands
in our study sites were planted with Ipomoea batatas or Brassica
napus, and all were invaded by S. canadensis. At the wasteland and
roadside habitats in the four sites, we selected herbaceous
communities with less human interference, in which the
dominant native plants mainly included A. lavandulaefolia,
Setaria viridis,Paspalum thunbergii,Humulus scandens,
Geranium carolinianum, and Ranunculus cantoniensis. We found
numerous patches of coexisting S. canadensis and A.
lavandulaefolia in the three habitats of the four study sites during
afield survey. We selected A. lavandulaefolia as the native plant to
compare with S. canadensis for the following reasons: (1) Both
belong to the Asteraceae family, sharing similar evolutionary
history; (2) more importantly, they commonly co-occur in the
wild in southern China (EBFC, 1985). According to the local
residents, S. canadensis began to invade in the four areas in 2005.
The characteristics of rhizosphere soils of S. canadensis and A.
lavandulaefolia in the three habitats of the four sites are
summarized in Table S1.
At each habitat in each study site, three 1.0 m × 1.0 m quadrats
(> 5 m apart from one another) were randomly established, where
the coverage of S. canadensis was greater than 90%. Nearby each S.
canadensis quadrat, we established a 1.0 m × 1.0 m quadrat with
more than 90% coverage of A. lavandulaefolia. The paired quadrats
of S. canadensis and A. lavandulaefolia within each habitat were less
than 5 m apart from each other in order to ensure similar soil
physico-chemical properties.
2.2
15
N labeling and sample collection
Three individuals of S. canadensis or A. lavandulaefolia (> 15 cm
apart from one another) with similar size were selected for
15
N
labeling in each quadrat, and one for each of the three N treatments:
15
NH
4+
,
15
NO
3-
, and control. The
15
N-labeled ammonium chloride
(NH
4
Cl,
15
N 99.12 atom%) and sodium nitrate (NaNO
3
,
15
N 99.21
atom%) were purchased from Shanghai Engineering Research Center
for Stable Isotopes (Shanghai, China). Each plant for the control
treatment was treated with 48 mL deionized water with no N
addition. A given mass of
15
NH
4
Cl and
15
NaNO
3
(containing
360 mg
15
N) was weighed, dissolved in 48 mL deionized water (0.5
mmol
15
NL
-1
), and applied for each individual plant. The
nitrification inhibitor dicyandiamide (DCD) was added to each
sampled plant (75 mg plant
-1
; corresponding to ≈50 μg g
-1
soil) in
order to prevent potential ammonium oxidation (Zhu et al., 2019).
To ensure homogeneous distribution of the labeling solutions in the
soil around each labeled plant, we used the Rhizon Cera soil solution
sampler (Rhizosphere Research Products, Wageningen, Netherlands)
instead of a traditional sterile syringe needle to inject the
isotopic solution.
The front of the sampler is a 10-cm long porous polyester tube,
with a diameter of 5 mm and many uniform pores of 0.15 mm. This
sampler could release the labeling solution or deionized water
evenly into different parts of the soil when pressure is carefully
applied to the syringe. The effectiveness of the sampler had been
confirmed in our preliminary experiments using trypan blue dye.
We further determined the minimal number of the samplers
needed, the volume of the solution needed to add into each
sampler, and its insertion depth into soil in order to achieve a
homogeneous distribution of the solution in the soil around each
labeled plant. Based on these preliminary experiments, the labeling
method was as follows: carefully removing plant litter from soil
surface around each target plant, and putting a circular injection
template on the ground with the plant as the center (Figure S1). The
injection template was a hardboard circle (11 cm in diameter),
which matches the outside diameter of the Luoyang shovel. On the
template, a circle with a radius of 2.5 cm was drawn and six holes
(0.5 bore diameter) were made evenly along the circumference.
Then we drilled six holes into the soil up to 10 cm depth around the
target plant, inserted the sampler with 8 mL labeling solution into
each hole to the depth of 10 cm, and finally injected the solution
into soil. Using this method, the solution was evenly dispersed in
the soil inside a cylinder with a height of 15 cm and a radius of 5 cm
centered around the plant.
Forty-eight hours after
15
N labeling, plant material and
rhizosphere soil were collected for each labeled or control plant.
We first clipped each plant at 1 cm above ground, then dug out the
soil (including roots; not necessary to collect all roots of the plant,
just the roots within the range of
15
N labeling) around the plant
with a radius of 5 cm and to a depth of 15 cm using a specialized soil
auger (Luoyang shovel, 10 cm in internal diameter). The shoot and
soil of each plant were immediately put into plastic self-sealing bags,
respectively, which were stored in an ice box. The plant and soil
samples collected every day were transported back to our laboratory
on the same day. Rhizosphere soil for each soil sample was collected
using a hand-shaking method in the laboratory (Zhao et al., 2020),
passed through a 2-mm sieve, and separated into two portions.
One portion (≈10 g) was air-dried at room temperature for
determination of total N and C contents, while the other portion
was stored at 4°C for determination of NH
4+
and NO
3-
contents.
The roots in each soil sample were collected, rinsed immediately
with water, soaked in 0.5 mmol L
-1
CaCl
2
solution for 5 min, and
Guan et al. 10.3389/fpls.2023.1243849
Frontiers in Plant Science frontiersin.org03
then rinsed thoroughly with deionized water to remove the
15
N
adsorbed on the root surface (Cui et al., 2017). The roots and the
shoot from each sample plant were oven-dried at 60°C to constant
weight, and then ground to a fine powder for determination of total
N and d
15
N contents using a ball mill (GT200, Grinder, China) with
1400 r min
-1
for 30 s.
2.3 Measurements
2.3.1 Plant biomass and root to shoot ratio
In the mono-dominant community of S. canadensis or A.
lavandulaefolia at each habitat in each study site, three quadrats
(0.5 m × 0.5 m) were randomly established for biomass
measurement. The above-ground plant tissues (stems and leaves)
in each quadrat were clipped above ground surface, and put into a
kraft paper bag. Roots were carefully dug out with a shovel (to a
depth of 15 cm; more than 95% of the total roots), shaken to remove
soil, rinsed with water, and then put into a kraft paper bag. Shoots
and roots were transported to our laboratory, oven-dried to
constant weight at 60°C, and weighed using an analytical balance,
respectively for each quadrat. Total above- and belowground
biomass (g m
-2
) were calculated per square meter, and root to
shoot ratio was calculated for each quadrat.
2.3.2 Total plant N concentration and d
15
N
Total N concentration and d
15
N in the whole plant powder were
measured using an element analyzer-stable isotopic mass
spectrometer (Flash EA 1112 HT-Delta V Advantage, Thermo
Fisher Scientific, Waltham, MA, USA). The measurement was
conducted by the Third Institute of Oceanography, Ministry of
Natural Resources, Xiamen, China. Three compounds were used as
references: DL-alanine (d
15
N = -1.7‰), glycine (d
15
N=10‰), and
histidine (d
15
N=-8‰). The analytical precision for d
15
N
was 0.2‰.
2.3.3 Soil dissolved inorganic N content
Ten gram of each rhizosphere soil sample was weighed
accurately, extracted in 50 mL 2 mol L
-1
KCl using a reciprocal
shaker (200 r min
-1
for 1 h), and then filtered through Whatman #1
filter paper. The concentrations of NH
4+
and NO
3-
was determined
using an Auto Analyzer III instrument (AA3, SEAL Analytical,
Norderstedt, Germany).
2.4 Calculations
2.4.1 Plant uptake of different N forms
The
15
N atom% excess of the labeled plant compared with that
of the control plant (APE
labeled
, %) was calculated according to
McKane et al. (2002) and Cui et al. (2017) as follows:
APElabeled = AT % excesslabeled −AT % excesscontrol
= AT %labeled −AT %control (1)
where AT% excess
labeled
or AT% excess
control
indicates the
difference in the
15
N atom% between the labeled (AT%
labeled
,
15
N/
(
15
N+
14
N) × 100) or the control plant (AT%
control
) and the
atmosphere (
15
N AT%
atm
). Uptake of
15
N by the labeled plant
(
15
N
uptake
,mg) was calculated as follows:
15Nuptake = APElabeled totalbiomass Ncontent 1000
=½(AT %labeled −AT %control )=100
(totalbiomass Ncontent)labeled 1000 (2)
where, total biomass is the sum of above- and underground
biomass of the labeled plant (g), and N
content
is the N content of the
labeled plant (%). The
15
N uptake rate of the plant (
15
N
uptake
rate,
mgNg
-1
root h
-1
) was calculated as follows:
15Nuptake rate =15 Nuptake =(rootbiomass time) (3)
where time is the duration of labeling treatment (h), and root
biomass was in gram. The uptake for the existing N (either
14
Nor
15
N) in soil by the labeled plant (Actual N uptake) was calculated
according to McKane et al. (2002) and Zhang et al. (2019) as
follows:
ActualNuptake =15 Nuptake Cavailable=C15 Nadded (4)
where C
available
is the content of the existing NO
3-
or NH
4+
in
the soil (mg N kg
-1
dw soil), and C
15
N
added
is the content of the
15
N-
NO
3-
or
15
N-NH
4+
added into the soil (mg N kg
-1
dw soil). The
uptake rate of the labeled plant for the existing NO
3-
or NH
4+
in the
soil (Actual N uptake rate, mgNg
-1
root h
-1
) was calculated as
follows:
ActualNuptakerate
=½15Nuptake Cavailable=C15Nadded=½rootbiomass time
=15 Nuptakerate Cavailable=C15Nadded (5)
The uptake for the NO
3-
or NH
4+
that already presented in the
soil before N labeling treatment by the plants in each quadrat (N
Uptake per quadrat, mgm
-2
) was calculated as follows:
Uptakeperquadrat
= ActualNuptakerate rootbiomassquadrat time (6)
where root biomass
quadrat
is the sum of root biomass in each
quadrat (g m
-2
).
The proportional contribution of NO
3-
(f
NO3-
)orNH
4+
(f
NH4+
)
to plant N was calculated as the fraction of the actual uptake rate of
NO
3-
or NH
4+
in the total actual uptake rate of NO
3-
and NH
4+
(Guo et al., 2021).
2.4.2 Plant N form preference
Plant preferences (b) for different inorganic N forms were
calculated according to Liu et al. (2013) and Zhang et al. (2018)
as follows:
bNF =fNF −½NF=½DIN: (7)
Guan et al. 10.3389/fpls.2023.1243849
Frontiers in Plant Science frontiersin.org04
Where b
NF
,f
NF
, [NF]/[DIN] were the preference for a certain
inorganic N form, the proportional contribution of this N form to
plant N, and the proportional contribution of this N form to DIN
(NH
4+
and NO
3-
) of the soil, respectively. b
NF
> 0 indicates a
preference for this N form; b
NF
< 0 indicates no preference for this
inorganic N form, but a preference for the other inorganic N form;
and b
NF
= 0 indicates no preference.
2.4.3 Plasticity in plant N form uptake
Based on McKane et al. (2002);Kahmen et al. (2006), and Gao
et al. (2020), the percentage similarity between plant uptake of
different N forms and the availability of those N forms in
rhizosphere soil (PS or percentage similarity) was used to
estimate the plasticity of plant N form uptake, which was
calculated as follows:
PS( % ) = 100 –0:5
½(jfþ
NH4–½NHþ
4=½DIN)+(
jj
f−
NO3–½NO−
3=½DINj)
100
(8)
The higher the value of the percentage similarity, the greater the
plant plasticity in the inorganic N form uptake. The value of the
percentage similarity = 100% indicates that the plant absorbs the
two N forms strictly according to their proportions in rhizosphere
soil, i.e., that the plant absorbs soil inorganic N absolutely using the
plastic strategy. The lower the value of the percentage similarity, the
lower the plant plasticity in the inorganic N form uptake, indicating
a preference or negative preference for specific N form.
2.5 Statistical analysis
Linear mixed-effects model was conducted to test the effects of
habitats, species, and their interactions on each variable. Habitats,
species, and their interactions were used as fixed factors, and quadrats
nested within study sites as random factors. The models were
performed in R (version 4.2.2) using the ‘lme’and ‘anova.lme’
functions of the ‘nlme’package (Pinheiro et al., 2016). One-way
analysis of variance (ANOVA) was conducted to detect the
difference in each variable for the same species (S. canadensis or A.
lavandulaefolia) among different habitats. Independent samples t-test
was used to detect the difference in each variable between S. canadensis
and A. lavandulaefolia in the same habitat, and the difference between
b
NF
and 0. These analyses were carried out using SPSS (version 2018;
SPSS Inc., Chicago, IL, USA). The relationships between the values of
f
NH4+
or b
NH4+
versus soil DIN contents or the ratios of NO
3-
to NH
4+
,
and those between total biomass or root to shoot ratios versus the
values of f
NH4+
or b
NH4+
were analyzed for each species with
standardized major axis (SMA) regression, using the ‘smatr’package
in R (Warton et al., 2012). We first tested whether the slopes of SMA
regressions were significantly different between S. canadensis and A.
lavandulaefolia; if not, we further tested the interspecific differences in
intercepts and the shift along the common slope. Before all above-
mentioned analyses, the preferences for different soil N forms were
quantile-transformed, and the other variables were log-transformed in
order to meet the assumptions of normality (Shapiro-Wilk tests) and
homoscedasticity (Levene’s test). Linear regression analysis was used
to examine the significance of the correlations between root to shoot
ratios versus total biomass, and those between the contents of total
dissolved inorganic nitrogen, NO
3-
and NH
4+
versus root to shoot
ratios for each species.
3 Results
3.1 Total biomass, root biomass, and root
to shoot ratio
Total biomass, root biomass, and root to shoot ratio were
significantly affected by habitats, species, and their interactions
(P< 0.05; Table S2). Total biomass of S. canadensis was the
highest in the farmland, and the lowest in the roadside (P< 0.05;
Figure 1A). In contrast, total biomass of A. lavandulaefolia was the
highest in the roadside, and the lowest in the wasteland (P< 0.05).
Total biomass were significantly higher for the invasive relative to
the native species in all three habitats (P< 0.05).
For both species, root biomass was similar in the farmland and
wasteland, both significantly lower than that in the roadside (P<
0.05; Figure 1B). Root biomass was significantly higher for the
invasive relative to the native species in all three habitats (P< 0.05).
For both species, root to shoot ratios were the highest in the
roadside, and the lowest in the farmland (P< 0.05; Figure 1C). Root
to shoot ratios were significantly lower for the invasive relative to
the native species in all three habitats (P< 0.05).
3.2 Contents of different N forms in
rhizosphere soils
The contents of NO
3-
,NH
4+
and DIN in rhizosphere soil, and
the ratio of NO
3-
to NH
4+
were all significantly influenced by
habitats, species, and their interactions (P< 0.05; Table S3). For both
the invasive and native species, soil NO
3-
contents were similar in
the farmland and wasteland, both significantly lower than that in
the roadside (P< 0.05; Figure 2A). The invader was significantly
higher in soil NO
3-
content than A. lavandulaefolia in the farmland
(P< 0.05), but similar in the wasteland and roadside.
For S. canadensis,NH
4+
contents in rhizosphere soils were similar
in the farmland and wasteland, both significantly higher than that in
the roadside (P<0.05;Figure 2B). For A. lavandulaefolia,soilNH
4+
content was significantly higher in the wasteland than in the farmland
(P< 0.05), which were not significantly different with that in the
roadside (P>0.05).Theinvaderwassignificantly higher in soil NH
4+
content than A. lavandulaefolia in the farmland, while lower in the
wasteland and roadside (P<0.05).
For S. canadensis, DIN contents in rhizosphere soils were
similar in all three habitats (P> 0.05; Figure 2C). For A.
lavandulaefolia, soil DIN contents were similar in the roadside
and wasteland, both significantly higher than that in the farmland
Guan et al. 10.3389/fpls.2023.1243849
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(P< 0.05). Similarly as in soil NH
4+
content, the invader was
significantly higher in soil DIN content than A. lavandulaefolia in
the farmland, while lower in the wasteland and roadside (P< 0.05).
For S. canadensis, the ratios of NO
3-
to NH
4+
in rhizosphere
soils were similar in the farmland and wasteland, both significantly
lower than that in the roadside (P<0.05;Figure 2D). For A.
lavandulaefolia, the ratio of NO
3-
to NH
4+
was the highest in the
roadside, followed by the farmland and wasteland, respectively (P<
0.05). Compared with A. lavandulaefolia,S. canadensis showed a
significantly higher ratio of NO
3-
to NH
4+
in the wasteland and
roadside (P< 0.05), but not in the farmland (P> 0.05).
3.3 Uptakes for different N forms in
rhizosphere soils
The uptakes of soil NO
3-
,NH
4+
and DIN per quadrat, and the
uptake ratio of NO
3-
to NH
4+
were all significantly influenced by
habitats, species, and their interactions (P< 0.05; Table S4). For S.
canadensis, the uptake of soil NO
3-
per quadrat was the highest in
the roadside, followed by the farmland and wasteland, respectively
(P< 0.05; Figure 3A). For A. lavandulaefolia, the uptakes of soil
NO
3-
per quadrat were similar in the farmland and wasteland, both
significantly lower than that in the roadside (P< 0.05). The uptakes
of soil NO
3-
per quadrat were significantly higher for the invasive
relative to the native species in all three habitats (P< 0.05).
In the farmland and wasteland compared with the roadside, the
uptake of soil NH
4+
per quadrat were significantly higher for S.
canadensis, while significantly lower for A. lavandulaefolia (P< 0.05;
Figure 3B). Compared with A. lavandulaefolia,S. canadensis showed
significantly higher NH
4+
uptake per quadrat in the farmland and
wasteland (P< 0.05), but not in the roadside (P> 0.05).
For S. canadensis, the uptakes of soil DIN per quadrat were
similar in the farmland and roadside, both significantly higher than
that in the wasteland (P< 0.05; Figure 3C). For A. lavandulaefolia,
the uptakes of soil DIN per quadrat were similar in the farmland
and wasteland, both significantly lower than that in the roadside
(P< 0.05). The uptakes of soil DIN per quadrat were significantly
higher for the invasive relative to the native species in all three
habitats (P< 0.05).
For S. canadensis, the uptake ratios of soil NO
3-
to NH
4+
was
highest in the roadside, followed by the farmland and wasteland,
respectively (P< 0.05; Figure 3D). For A. lavandulaefolia, the uptake
ratios of NO
3-
to NH
4+
were similar in the farmland and wasteland,
both significantly lower than that in the roadside (P<0.05).
Compared with A. lavandulaefolia,S. canadensis showed
significantly lower uptake ratios of NO
3-
to NH
4+
in the farmland
and wasteland (P< 0.05), but not in the roadside (P> 0.05).
A
C
B
FIGURE 1
Total biomass (A), root biomass (B), and root to shoot ratio (C) of Solidago canadensis (closed bars) and Artemisia lavanduiaefolia (open bars) in
different habitats. Mean ± SE (n= 12). Different upper- and lowercase letters indicate significant differences among habitats for S. canadensis and
A.lavanduiaefolia, respectively (P< 0.05; one-way ANOVA); * indicates significant differences between the two species in the same habitat (P< 0.05;
independent sample t-test).
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3.4 Proportional contribution of different N
forms to plant N
The values of f
NO3-
and f
NH4+
were significantly influenced by
habitats, species, and their interactions (P< 0.05; Table S6). For S.
canadensis, the value of f
NO3-
was the highest in the roadside,
followed by the farmland and wasteland, respectively (P< 0.05;
Figure 4A). For A. lavandulaefolia, the values of f
NO3-
were similar
in the farmland and wasteland, both significantly lower than that in
the roadside (P< 0.05). Compared with A. lavandulaefolia,S.
canadensis showed significantly lower f
NO3-
values in the farmland
and wasteland (P< 0.05), but not in the roadside (P> 0.05).
For S. canadensis, the value of f
NH4+
was the highest in the
wasteland, followed by the farmland and roadside, respectively (P<
0.05; Figure 4B). For A. lavandulaefolia, the values of f
NH4+
were
similar in the farmland and wasteland, both significantly higher
than that in the roadside (P< 0.05). Compared with A.
lavandulaefolia,S. canadensis showed significantly higher f
NH4+
values in the farmland and wasteland (P< 0.05), but not in the
roadside (P< 0.05).
3.5 Preference for different N forms
For S. canadensis, there was no significant difference between
b
NO3-
or b
NH4+
versus zero in the farmland (P> 0.05), indicating no
significant preference for N forms; in the wasteland the value of
b
NO3-
was significantly lower than zero and the value of b
NH4+
was
significantly higher than zero, indicating a preference for NH
4+
; and
in the roadside the value of b
NO3-
was significantly higher than zero
and the value of b
NH4+
was significantly lower than zero, showing a
preference for NO
3-
. For A. lavandulaefolia, the values of b
NO3-
were significantly higher than zero in all three habitats, while the
values of b
NH4+
were significantly lower than zero, indicating a
consistent preference for NO
3-
.
The values of b
NO3-
and b
NH4+
were significantly influenced by
habitats, species, and their interactions (P< 0.05; Table S7). For both
species, the values of b
NO3-
were similar in the farmland and
wasteland, both significantly lower than that in the roadside (P<
0.05; Figure 5A). For the values of b
NH4+
, however, both species
were significantly lower in the roadside than in the farmland and
wasteland (P< 0.05; Figure 5B).
Compared with A. lavandulaefolia,S. canadensis showed
significantly lower values of b
NO3-
and significantly higher values
of b
NH4+
in the farmland and wasteland (P< 0.05). There was no
significant difference in the values of b
NO3-
and b
NH4+
between the
two species in the roadside (P> 0.05).
3.6 Plasticity in plant uptake for
different N form
The percentage similarity between plant uptake patterns of
different N forms and their pattern of availability in rhizosphere
soil was significantly influenced by habitats and species (P< 0.05;
A
CD
B
FIGURE 2
Contents of NO
3-
(A),NH
4+
(B) and total dissolved inorganic nitrogen (C), and the ratio of NO
3-
to NH
4+
(D) in the rhizosphere soils of Solidago
canadensis (closed bars) and Artemisia lavanduiaefolia (open bars) in different habitats. NN, nitrate nitrogen; AN, ammonium nitrogen; DIN, dissolved
inorganic nitrogen. Mean ± SE (n= 12). Different upper- and lowercase letters indicate significant differences among habitats for S. canadensis and
A.lavanduiaefolia, respectively (P< 0.05; one-way ANOVA); * indicates significant differences between the two species in the same habitat (P< 0.05;
independent sample t-test).
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Table S8), while the effect of the interaction of these factors was not
significant (P= 0.798).
For both species, the vales of percentage similarity were similar in
the farmland and wasteland, both significantly higher than that in the
roadside (P< 0.05; Figure 6). Compared with A. lavandulaefolia,S.
canadensis showed significantly higher value of percentage similarity in
the farmland (P<0.05),butnotinthewastelandandroadside(P>0.05).
3.7 Effects of soil DIN contents and NO
3-
/
NH
4+
ratios on f
NH4+
and b
NH4+
For both the invasive and native species, the values of f
NH4+
or
b
NH4+
decreased significantly with increasing soil DIN contents or
the ratios of NO
3-
to NH
4+
except the values of f
NH4+
with soil DIN
contents for A. lavandulaefolia (marginally significant) (P< 0.05;
AB
FIGURE 4
Proportional contributions (%) of soil NO
3-
(A) and NH
4+
(B) to plant N of Solidago canadensis (closed bars) and Artemisia lavanduiaefolia (open bars)
in different habitats. Mean ± SE (n= 12). Different upper- and lowercase letters indicate significant differences among habitats for S. canadensis and
A. lavanduiaefolia, respectively (P< 0.05; one-way ANOVA); * indicates significant differences between the two species in the same habitat (P< 0.05;
independent sample t-test).
A
CD
B
FIGURE 3
Uptakes of NO
3-
(A),NH
4+
(B) and total dissolved inorganic nitrogen (C) existing in soil, and the ratio of NO
3-
to NH
4+
(D) absorbed by Solidago
canadensis (closed bars) and Artemisia lavanduiaefolia (open bars) in different habitats. NN, nitrate nitrogen; AN, ammonium nitrogen; DIN, dissolved
inorganic nitrogen. Mean ± SE (n= 12). Different upper- and lowercase letters indicate significant differences among habitats for S. canadensis and
A. lavanduiaefolia, respectively (P< 0.05; one-way ANOVA); * indicates significant differences between the two species in the same habitat (P< 0.05;
independent sample t-test).
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Figure 7). The SMA slope of the relationship between the values of
b
NH4+
and soil DIN contents was significantly lower for S.
canadensis than for A. lavandulaefolia (P< 0.05), indicating that
the values of b
NH4+
was more strongly influenced by change in soil
DIN contents for the invasive relative to the native species. The
SMA slopes of the relationship between the values of f
NH4+
or b
NH4+
and the ratios of NO
3-
to NH
4+
were also significantly lower for S.
canadensis than for A. lavandulaefolia (P< 0.05), indicating that the
values of f
NH4+
and b
NH4+
were more strongly influenced by change
in the ratios of NO
3-
to NH
4+
for the invasive relative to the
native species.
3.8 Effects of f
NH4+
and b
NH4+
on total
biomass and root/shoot ratios
Total biomass increased significantly with the increase of the
values of f
NH4+
or b
NH4+
for S. canadensis (P< 0.001; Figure 8A,B),
while decreased significantly for A. lavandulaefolia. The absolute
values of the SMA slope of the relationship were significantly lower
for S. canadensis than for A. lavandulaefolia.
For both species, the root to shoot ratios significantly decreased
withtheincreaseofthevaluesoff
NH4+
or b
NH4+
(P<0.01;Figure 8C,
D). The SMA slopes of the relationships between root to shoot ratios
and the values of f
NH4+
were not significantly different between the two
species (P> 0.05). The value of the y-intercept of the relationship was
significantly higher for A. lavandulaefolia than for S. canadensis (P<
0.05), indicating that root to shoot ratio was significantly lower in S.
canadensis than in A. lavandulaefolia under the same value of f
NH4+
.
The shift along the common slope of the relationship was also
significantly different between the two plants (P< 0.05), with S.
canadensis showing higher values of f
NH4+
but lower root to shoot
ratios, and A. lavandulaefolia showing lower values of f
NH4+
but higher
root to shoot ratios. The SMA slope of the relationship between root to
shoot ratios and the values of b
NH4+
was significantly higher for S.
canadensis than for A. lavandulaefolia (P< 0.05), indicating that root to
shoot ratios were less influencedbythechangeinthevaluesofb
NH4+
for the invasive relative to the native species.
4 Discussion
Consistent with our hypothesis, the invasive plant S. canadensis
absorbed more N than the native plant A. lavandulaefolia in all
three habitats, contributing to its invasion success as judged by its
significantly higher total biomass. Numerous studies have
demonstrated that N is one of the vital factors that influences
invasion success of exotic plants (Lee et al., 2012;Castro-Dı
ez et al.,
FIGURE 6
Percentage similarity between plant uptake pattern of different N
forms and their pattern of availability in rhizosphere soil of Solidago
canadensis (closed bars) and Artemisia lavanduiaefolia (open bars) in
different habitats. Mean ± SE (n= 12). Different upper- and
lowercase letters indicate significant differences among habitats for
S. canadensis and A. lavanduiaefolia, respectively (P< 0.05; one-way
ANOVA); * indicates significant differences between the two species
in the same habitat (P< 0.05; independent sample t-test).
AB
FIGURE 5
Preference for NO
3-
(A) and NH
4+
(B) for Solidago canadensis (closed bars) and Artemisia lavanduiaefolia (open bars) in different habitats. Mean ± SE
(n= 12). s and n indicate significant and non-significant differences with 0, respectively (P< 0.05; independent sample t-test). Different upper- and
lowercase letters indicate significant differences among habitats for S. canadensis and A. lavanduiaefolia, respectively (P< 0.05; one-way ANOVA);
* indicates significant differences between the two species in the same habitat (P< 0.05; independent sample t-test).
Guan et al. 10.3389/fpls.2023.1243849
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2014;Sun et al., 2021). Compared with native plants, invasive plants
not only have stronger abilities to absorb soil N, and higher leaf N
contents (Huang et al., 2020;Liu et al., 2022), but also utilize leaf N
more efficiently (Feng et al, 2009;Feng et al, 2011). Feng et al. (2009)
found that the invasive relative to native populations of Ageratina
adenophora allocate lower leaf N to cell walls but higher to
photosynthetic organs, resulting in higher photosynthetic rates
and N-use efficiencies. In addition, we further found that N form
acquisition strategies of the invasive and native species were
influenced by both soil N levels and the proportions of different
N forms (Figure 7). More importantly, our results provided robust
evidence for the association between N form acquisition strategy of
S. canadensis and its invasiveness.
4.1 N form acquisition strategy and exotic
plant invasiveness
In the farmland and wasteland, the invader had both higher DIN
uptake rates (Figure S2C) and total root biomass per quadrat
(Figure 1B), both contributing to its higher N uptake. James et al.
(2009) also found that N uptake rates were significantly higher in
three invasive perennial forbs than in six native perennial grasses and
forbs in both heterogeneous and homogeneous nutrient soils. In the
roadside, however, the higher total root biomass per quadrat was the
main reason for the higher N uptake of the invader, where its DIN
uptake rate was lower than that of A. lavandulaefolia (Figure S2C). Of
course, we do not know whether the invader could absorb more
organic N than A. lavandulaefolia in the roadside, which warrants
further study. A recent study showed that S. canadensis could absorb
organic N, particularly in habitats rich in free amino acids (Yu et al.,
2016). Similarly, for S. canadensis, total biomass was the lowest in the
roadside among the habitats (Figure 1A), while the uptake of soil DIN
in the roadside was similar with that in the farmland, and higher than
that in the wasteland. These results indicate that the invader may also
absorb organic N in the wasteland and farmland. In general, the
organic N content in the farmland is higher than that in the wasteland
and roadside (Lv et al., 2011;Quan et al., 2022). Specific root
morphology, high carbon allocation to roots, and a flexible N
uptake strategy may all contribute to the high N uptake rates of
invasive plants (James et al., 2009;Hewins and Hyatt, 2010;Mozdzer
et al., 2010;Hu et al., 2019). In our study, the higher plasticity in soil
N form uptake and the preference for the dominant soil N form
contributed to the higher N uptake rate of S. canadensis (see below).
In addition, the invasive relative to the native species also showed
more stable N uptake rates across all three habitats (Figure S2C). The
stabilityof DIN uptakemay contribute to adaptationof the invader to
temporal and spatial fluctuations in soil N availability, and thus to
invasion success of the invader in the different habitats.
The higher total root biomass of the invasive relative to the native
species was due to its faster growth (i.e., higher total biomass), rather
than to the interspecific difference in root to shoot ratio. The invader
A
CD
B
FIGURE 7
Relationships between f
NH4+
(A, B) and b
NH4+
(C, D) versus total soil dissolved inorganic nitrogen contents and the ratios of NO
3-
to NH
4+
for
Solidago canadensis and Artemisia lavanduiaefolia, respectively. Only significant SMA lines are shown (R
2
> 0.1, P< 0.05). DIN, dissolved inorganic
nitrogen. SL, slope; *, significant differences.
Guan et al. 10.3389/fpls.2023.1243849
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had significantly lower root to shoot ratios in all three habitats. Lower
root to shoot ratios were also found in other invasive species relative to
their co-occurring natives (Zou et al., 2007;teBeestetal.,2009;Liao
et al., 2013;Liao et al., 2019). The low root to shoot ratios may
contribute to invasiveness of exotic species in fertile habitats, by
leaving more biomass for allocation to shoot and thus increasing
utilization of aboveground resources. Negative relationship between
total biomass and root to shoot ratios was indeed found for the
invader (Figure S3A). This result also indicates that the invader had
allometric growth relationship between root and shoot.
Root to shoot ratio was not influenced by soil nutrient levels
(DIN contents) for S. canadensis (Figure S4), which is different with
the results of many other studies (Liao et al., 2013;Guo et al., 2019;
Yan et al., 2019;Li et al., 2020). Liao et al. (2013) found that root to
shoot ratio of the invasive plant Chromolaena odarata decreased
significantly with increasing soil nutrient in both mono- and mixed
cultures. Addition of N also decreases root to shoot ratio of
Arabidopsis thaliana (Yan et al., 2019). However, root to shoot
ratio of the invader decreased significantly with increasing soil
NH
4+
content, while increased with increasing soil NO
3-
content
(Figure S4). The invader can better absorb NH
4+
compared with
NO
3-
(see below), and thus increasing soil NH
4+
can better improve
its N status. These results indicate that root to shoot ratio of the
invader may be influenced by its nutrient status, rather than by soil
nutrient levels per se. Root to shoot ratios were negatively correlated
with f
NH4+
or b
NH4+
for both the invasive and native species
(Figure 8C,D). Along the common SMA slope of the two species,
S. canadensis was located at the end with low root to shoot ratios and
high f
NH4+
values. This result indicates that the higher f
NH4+
was at
least one of the reasons for the lower root to shoot ratio for the
invasive species. Consistently, the values of f
NH4+
were significantly
higher (Figure 4), while root to shoot ratios lower for the invader in
the farmland and wasteland than in the roadside (Figure 1).
Consistent with our hypothesis, the invasive relative to the
native species had higher plasticity in uptake of different soil N
forms, contributing to its more DIN uptake. In the farmland and
wasteland, where NH
4+
was the dominant DIN in rhizosphere soils
for both species, the invasive and native species absorbed NH
4+
relative to NO
3-
more quickly, and thus NH
4+
contributed more
greatly to plant N. In the roadside, where NO
3-
was the dominant
DIN in rhizosphere soils for the two species, both species absorbed
NO
3-
relative to NH
4+
more quickly, and thus NO
3-
contributed
more greatly to plant N. These results indicate that the invasive and
native species had plasticity in N form uptake. This plasticity could
ensure that the two species always utilized the dominant soil N
form, and thus contributed to their adaptation to the changes in soil
N forms. The higher plasticity in N form uptake for the invasive
relative to the native species (especially in the farmland) could help
the invader to adapt to the changes in soil N forms. Plasticity in N
form uptake have also been found in other plants (Andersen and
Turner, 2013;Russo et al., 2013). For example, some plants switch
their N source from NO
3-
to NH
4+
when their habitats change from
A
CD
B
FIGURE 8
Relationships between total biomass (A, B) and root to shoot ratios (C, D) versus f
NH4+
and b
NH4+
for Solidago canadensis and Artemisia
lavanduiaefolia, respectively. Only significant SMA lines are shown (R
2
> 0.1, P< 0.05). TB, total biomass; RS, root to shoot ratio; SL, slope; EL,
elevation or intercept; SH, shift along common slope. *, significant differences; ns, not significant differences.
Guan et al. 10.3389/fpls.2023.1243849
Frontiers in Plant Science frontiersin.org11
dry to wet (Houlton et al., 2007;Wang and Macko, 2011). Plasticity
in N form uptake may be a basic strategy for plants to adapt to the
changes in soil N forms (Ashton et al., 2010), and an important
factor determining plant dominances and diversity patterns (Craine
and Dybzinski, 2013). Until now, however, very few references have
studied the roles of plasticity in N form uptake in exotic plant
invasions, especially using a quantitative estimator.
Preferential uptake of N forms also contributed to the more N
uptake of the invasive relative to the native species. In the farmland
and wasteland, the invader preferred NH
4+
, especially in the
wasteland, and the N (DIN) uptake rates of the invader were
significantly higher than those of the native species (Figure S2C).
The higher DIN uptake rates were mainly associated with its higher
NH
4+
uptake rates, while its NO
3-
uptake rate was not significantly
higher than that of A. lavandulaefolia in the wasteland. In the
roadside, where NO
3-
was the dominant soil N, the invader
preferred NO
3-
. however, A. lavandulaefolia always preferred
NO
3-
in three habitats. These results indicate that the invader
could adjust its preference for N form according to the dominant
soil N form, while A. lavandulaefolia could not. The invader always
preferred to absorb the dominant soil N form, contributing to its
higher N uptake, and therefore to its invasiveness.
We indeed found that total biomass was positively associated
with f
NH4+
or b
NH4+
for the invader, while the relationships were
negative for A. lavandulaefolia (Figure 8). This result indicates that
increasing preference for NH
4+
and its proportional contribution to
plant N increased invasiveness of the invader. A previous study also
found that S. canadensis grows better in soils with a higher ratio of
NH
4+
to NO
3-
soils, indicating its preference for NH
4+
(Lu et al.,
2005). Preferential uptake of N forms was also found in other plants
(Huangfu et al., 2016;Chen and Chen, 2018;Tang et al., 2020;Luo
et al., 2022;Zhang et al., 2022a). Luo et al. (2022) found that
preference for NO
3-
relative to NH
4+
may help the invasive plant X.
strumarium to invade NO
3
–
enriched disturbed habitats. However,
the reasons for the difference in the preference for soil N forms
between invasive and native species are still poorly understood.
4.2 Factors affecting plant N form
acquisition strategy
Our results showed that plant N form acquisition strategy was
influenced by both soil N levels and the proportions of different N
forms (Figure 7). Numerous studies have shown that the habitats
invaded by exotic plants are diverse, and the levels and the
proportions of NO
3-
and NH
4+
in these habitats are different
greatly (Peng et al., 2011;Andersen and Turner, 2013;Li et al.,
2014;Li et al., 2016a;Wang et al., 2020). However, few studies have
investigated the effects of these factors on plant N form uptake
strategy for invasive plants. We found that S. canadensis and A.
lavandulaefolia increased their preferences for NH
4+
and the
proportional contributions of NH
4+
to plant N with decreasing
soil DIN contents and the ratios of NO
3-
to NH
4+
. These results
indicate that plants are more likely to prefer NH
4+
and NH
4+
is the
main N source for plants in barren relative to fertile habitats or in
habitats with low relative to high ratios of NO
3-
to NH
4+
. However,
the values of f
NH4+
and b
NH4+
were more susceptible to the changes
in soil DIN contents and the ratios of NO
3-
to NH
4+
for the invasive
relative to the native species, indicating that the invader responded
more sensitively to the changes in soil contents of NO
3-
to NH
4+
and their ratios (Figure 7). In addition, the values of f
NH4+
and
b
NH4+
were significantly higher for the invasive relative to the native
species in habitats with low DIN contents or low ratios of NO
3-
to NH
4+
.
Plants absorb NH
4+
and NO
3-
using different N transporters,
and the differences in the expressions of the genes of these
transporters may explain interspecificdifferenceinNform
preference (genetic basis). For example, many NO
3-
and NH
4+
transporter genes are significantly different in sequences, or
differentially expressed between the invasive plant X. strumarium
(preference for NO
3-
) and its native congener X. sibiricum
(preference for NH
4+
)(Luo et al., 2022;Zhang et al., 2022a).
The differences in sensitivities to NH
4+
toxicity may also
contribute to the interspecific differences in N form preference
(Britto and Kronzucker, 2002;Niinemets, 2010). Zhang et al.
(2022b) found that X. strumarium is more sensitive to NH
4+
, and
always preferred NO
3-
, contributing to alleviating NH
4+
toxicity at
high levels (Lambers et al., 1998). We do not know whether A.
lavandulaefolia is more sensitive to NH
4+
than the invader, and
whether this is the reason for that pattern A. lavandulaefolia
preferred NO
3-
in the farmland and wasteland, where NH
4+
was
the dominant soil N form. Further studies are needed.
Other factors such as mycorrhizal type, mycorrhizal taxa and
the extent of their infection may also affect interspecific differences
in N form preference between invasive and native plants. A better
understanding of the degree to which mycorrhizal fungi affect plant
N form preferences could significantly improve our understanding
of how invasive plant N acquisition strategies will respond to
environmental changes.
5 Conclusions
The invasive plant S. canadensis could adjust preference for N
forms according to the variations in the dominant soil N forms,
always preferring the dominant soil N form, while the native plant
A. lavandulaefolia consistently preferred NO
3-
in all habitats. The
higher plasticity in N form uptake and the preference for the
dominant soil N form make the invader to better absorb the
dominant soil N forms, contributing to its more stable and more
N uptake, and thus to its invasiveness in the different habitats. With
increasing the uptake and preference for soil NH
4+
, total biomass
increased and root to shoot ratio decreased for the invader. Our
study provides robust evidence that invasiveness of exotic plants is
associated with their N form acquisition strategy, which is
influenced by soil N conditions. These results improve our
understanding of invasion success of exotic plants in diverse
habitats in terms of utilization of different N forms, especially the
role of plasticity in N form uptake.
Guan et al. 10.3389/fpls.2023.1243849
Frontiers in Plant Science frontiersin.org12
Data availability statement
The original contributions presented in the study are included
in the article/Supplementary Material. Further inquiries can be
directed to the corresponding author.
Author contributions
Y-LF, MG and D-LK conceived the ideal and designed
methodology. MG and X-CP conducted the experiments,
analyzed the data and drafted the manuscript. J-KS and J-XC
assisted with soil dissolved inorganic nitrogen analysis. Y-LF and
MG critically reviewed and edited the manuscript. All authors
contributed to the article and approved the submitted version.
Funding
This work was supported by Zhejiang Provincial Natural
Science Foundation of China (LQ20C030004), the National
Natural Sciences Foundation of China (32001238, 32171666 and
32271741), and the National Key R & D Program of China
(2021YFD1400300).
Acknowledgments
We are grateful to Zhenhua Qiu, Huihui Wen, Weihang Chen,
Yitao Xin, Mengmeng Ren and Jinliang Li for their help during the
experimental period and thank Liwen Bianji (Edanz) for the English
language editing.
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.2023.1243849/
full#supplementary-material
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