Plant Soil

https://doi.org/10.1007/s11104-018-3616-7

REGULAR ARTICLE

Competition between Zea mays genotypes with different root

morphological and physiological traits is dependent
on phosphorus forms and supply patterns
Hongbo Li & Deshan Zhang & Xinxin Wang &
Haigang Li & Zed Rengel & Jianbo Shen

Received: 26 November 2017 / Accepted: 26 February 2018

# Springer International Publishing AG, part of Springer Nature 2018

Abstract Results In homogeneous Pinorg and Porg environ-

Background and aims Each genotype within species
has a particular combination of root morphological
and/or physiological traits to adapt to phosphorus-
limited environments, which can lead to its unique plant
fitness and competitive ability. Yet, how the various
phosphorus environments affect the competition be-
tween genotypes remains obscure.
Methods Two maize (Zea mays L.) genotypes (XY335
and HMY, bred in nutrient-rich and nutrient-poor envi-
ronments, respectively) were grown in monoculture and
mixture in phosphorus-limited soil with homogeneous
or heterogeneous supply patterns and inorganic (Pinorg)
or organic phosphorus (Porg) forms.
ments, XY335 had higher root length and surface
area, but lower mycorrhizal colonization and the
acid phosphatase and phytase activities in the
rhizosphere, than HMY. In heterogeneous phos-
phorus environments, XY335 had higher root pro-
liferation than HMY. The root trait divergence
influenced the competition in mixture: XY335
had a competitive advantage compared to HMY
under heterogeneous phosphorus conditions,
whereas HMY exhibited a stronger competitive
ability in homogeneous phosphorus treatments;
these reverse trends were more significant in the
Porg than Pinorg treatments.

Hongbo Li, Deshan Zhang and Xinxin Wang contributed equally

to this work.

Responsible Editor: Ismail Cakmak

Electronic supplementary material The online version of this

article (https://doi.org/10.1007/s11104-018-3616-7) contains
supplementary material, which is available to authorized users.

H. Li : H. Li : J. Shen (*) X. Wang

College of Resources and Environmental Sciences, Center for Mountain Area Research Institute, Agricultural University of
Resources, Environment and Food Security, Key Laboratory of Hebei, Baoding 071001, China
Plant-Soil Interactions, Ministry of Education, China Agricultural
University, Beijing 100193, People’s Republic of China
e-mail: jbshen@cau.edu.cn

D. Zhang Z. Rengel
Shanghai Academy of Agricultural Sciences No. 1000, Soil Science and Plant Nutrition, UWA School of Agriculture and
Eco-Environmental Protection Research Institute, Jinqi Road, Environment, The University of Western Australia, Perth, WA
Shanghai 201403, China 6009, Australia

Conclusions The results suggested the importance of
root physiological traits in homogeneous phosphorus-
limited soil environments, whereas P acquisition strate-
gy based on root morphological traits favours heteroge-
neous phosphorus supply.
Keywords Nutrient patch . Foraging strategy . Root
trait . Mycorrhizal colonization . Rhizosphere properties .
Plant interaction . Genetic diversity
Introduction
Phosphorus (P) has low availability in soil because it is
easily adsorbed by mineral surfaces and/or precipitated
as poorly-soluble phosphate salts (Hinsinger 2001; Shen
et al. 2011). Moreover, up to 80% of P is present in the
organic forms in a range of soils (Dalal 1997, Turner
et al. 2005); organic P cannot be taken up by plants
directly. Hence, P supply often limits primary produc-
tivity in natural and agricultural systems (Vance et al.
2003). In response, plants can regulate root morpholog-
ical or foraging traits to increase absorption area, such as
increasing (i) density and/or length of root hairs, (ii)
mycorrhizal colonization and (iii) specific root length
(Bates and Lynch 2001; Richardson et al. 2011). In
addition, especially for unavailable P forms (such as
organic P), plant also can employ physiological or P-
mining traits, including the increased root acid phospha-
tase and phytase activity or changing the rhizosphere
pH, to mobilize and absorb P (Lambers et al. 2006). The
multiple root morphological and physiological traits
across species can also underpin their differences in
the ability to access different P forms (Pearse et al.
2006; Shen et al. 2013; Ceulemans et al. 2017). Conse-
quently, these distinct root trait-based morphological
and physiological responses among species may govern
their capacity to draw down a shared limited soil re-
source (Zhang et al. 2016; Lambers et al. 2017), and
lead to different fitness (Chesson 2000; Kraft et al.
2015) and competitive ability (Semchenko et al. 2017).
Trait differences among competing plants can affect
the outcome of competition (Bennett et al. 2016), espe-
cially regarding the root traits that are responsible for
soil resource acquisition. Some studies suggested that
species with the high specific root length could be
superior competitors in both P-limited (Fort et al.
2014) and heterogeneous nutrient environments
(Mommer et al. 2011). However, a specific root trait or
Plant Soil
nutrient acquisition strategy may not result in high fit-
ness (competitive ability) in different environments
(Ceulemans et al. 2017; Li et al. 2017), especially when
the adaptive strategy is context-specific. For example,
roots and mycorrhizal hyphae can capture available
inorganic P in soil directly, whereas hydrolyzing organic
P is dependent on root and hyphae P-mining traits
(Lambers et al. 2008; Wang et al. 2017). However, there
is a balance or complementarity between root morpho-
logical and physiological responses to variable P-limited
environments across plant species (Lyu et al. 2016).
Hence, an outcome of competition between plant spe-
cies with diverse root morphological and physiological
traits can vary in various P environments (Chamberlain
et al. 2014; Mommer et al. 2016).
For the individuals with similar competitive pheno-
types that are expected to compete most strongly
(MacArthur and Levins 1967), such as different geno-
types within species, the competitive outcome still can
vary in diverse environments if genotypes have differ-
ential access to the relevant resource-containing niches
(Zuppinger-Dingley et al. 2014). For instance, genetic
diversity can increase temporal stability of plant produc-
tion under both drought and non-drought conditions
(Prieto et al. 2015), implying the altered competitive
advantage among different genotypes in various envi-
ronments. Thus, how different root traits influence
plant-plant competition depends on their interaction
with the limiting factors in the environment (Mayfield
and Levine 2010). However, empirical evidence on how
variation in root traits influences outcome of competi-
tion among genotypes of the same species subjected to
different environments is scarce (e.g. Abbott and
Stachowicz 2016), especially regarding diverse P chem-
ical forms or supply patterns.
The plant competitive ability can be mediated by the
nutrient supply patterns, resource availability and/or
chemical forms (Adler et al. 2013; Nasto et al. 2017).
In heterogeneous nutrient environments, a successful
competitor can rapidly proliferate roots in a nutrient-
rich patch zone (Li et al. 2016; Chen et al. 2017) to cause
resource pre-emption before competing plants access
the nutrient-rich patch (Grime 1994). Conversely, only
the plants that can efficiently explore unavailable re-
sources survive or succeed in diverse nutrient environ-
ments (Tilman 1982). For example, within species, Liu
et al. (2004) found the P-efficient genotype of maize
with a stronger rhizosphere effect (decreased soil pH
and increased acid phosphatase activity in the
Plant Soil

rhizosphere) developed better than the P-inefficient ge-

notype in P-limited conditions. Based on the distinct
nutrient foraging strategies in soils with heterogeneous- 20 cm
ly supplied and limited nutrients, there are important 1.5 cm

gaps in our understanding of how the diverse root traits

contribute to the competitive advantage in various P-
limited environments.
Here, we used two maize genotypes Huangmaya
(HMY) and Xianyu335 (XY335) that had been selected
in low and high soil fertility environments, respectively.
Due to the distinct selection environments, the two

Phosphorus patch
genotypes may have contrasting P-capture strategies

35 cm
(Barot et al. 2016): species from nutrient-rich habitats
have high root proliferation capacity, especially in the P-
patch zones (Grime 1994), whereas species from
nutrient-poor habitats may have the capacity to adapt
to the P-limited conditions with functional root traits
(such as enhanced rhizosphere processes). The two
maize genotypes were grown in monoculture and mix-
ture, with homogeneous or heterogeneous P supply as
inorganic or organic forms. The total P was limited for
maize growth in either type of supply. We measured a
variety of root morphological and physiological traits
related to P capture in soils. 3 cm

The objectives of the experiment were to character-
ize: (i) whether the genotype bred in the nutrient-rich
habitats would exhibit differences in the root morpho-
logical and physiological responses to P-limited envi-
ronments compared to genotype selected in the nutrient-
poor habitats; and if so (ii) how the P chemical forms
and supply patterns regulated the outcome of the com-
petition when the two genotypes grew together.
Materials and methods
Soil and microcosms
A calcareous loamy soil was collected from the
Changping Long-Term Fertilizer Station (40°08′12″N,
116°10′45″E) of China Agricultural University in Bei-
jing. The soil contained (per kg) 12.8 g organic C, 0.72 g
total N, 2.6 mg Olsen-P, 8.5 mg available N, 32 mg
available K, and had pH value 8.3 (the ratio of soil:
0.01 M CaCl2 solution was 1:2.5). The soil was air-dried
and passed through a 2-mm sieve. Microcosm PVC-
rhizoboxes (20 × 1.5 × 35 cm, Fig. 1) were constructed
as described by Zhang et al. (2016). Every rhizobox was
filled with 1.4 kg air-dried soil.
Fig. 1 Design of the rhizobox for maize growth. In the heteroge-
neous P supply treatments in experiment II, phosphorus was
localized in the middle of the rhizobox (grey rectangle)
Experiment I: Root trait responses to limiting P supply
Two maize (Zea mays L.) genotypes were used to test
the root morphological and physiological differences in
response to low-P supply: HMY, an open-pollinated,
early senescing genotype bred in the 1950s (Wang
et al. 2017), when barely any P fertilizer was used in
China (Li et al. 2015); and XY335 (patent number: 10/
271,942; Pioneer Hi-Bred International), a modern hy-
brid bred in the 2000s, when excessive amounts of P
fertilizer were applied in agriculture (Jiao et al. 2016).
Each maize genotype was tested at homogeneous P
supply of 50 mg P kg−1 soil as the inorganic (Pinorg, as
KH2PO4) or organic phosphorus treatments (Porg, as
sodium phytate, Sigma, USA). This supply of P was
relatively low (in contrast, optimum P supply under
these conditions would be 200 mg P/kg soil, Zhang et al.
2016). The other nutrients were uniformly added to soil
at the following rates (mg kg−1 soil): 200 N (KNO3),
200 K (KNO3 and K2SO4), 39 Mg (MgSO4·7H2O), 5.5
Fe (EDTA-Fe), 6.7 Mn (MnSO 4 ·H 2 O), 10 Zn

(ZnSO4·7H2O), 2 Cu (CuSO4·5H2O), 0.68 B (H3BO3)
and 0.12 Mo (Na2MoO4·2H2O). All the nutrients were
uniformly mixed with the soil before filling the
rhizoboxes. There were four factorial treatment combi-
nations (2 genotypes × 2 P forms) in experiment I, with
five replicates per treatment. All the rhizoboxes were
arranged in a completely randomized design.
Maize seeds were surface-sterilized in 30% v/v H2O2
for 20 min, washed with deionized water, soaked in
saturated CaSO4 solution for 12 h and then germinated
on wet filter paper with de-ionized water in dark for 36 h
at 28 °C. Two uniform maize seeds were selected and
sown per rhizobox. Soil moisture was kept at 18–20%
(w/w) as determined gravimetrically by weighing each
rhizobox every 2 days during the experiment.
The rhizobox experiment was conducted in a green-
house at the China Agricultural University (40°01′41″
N, 116°16′49″E) in May. The glasshouse temperature
range was 23–28 °C with 12–14 h daytime throughout
the growth period.
Plants were harvested 30 days after sowing (DAS)
and separated into shoots and roots. The shoots were
oven-dried at 72 °C for 72 h. Dry samples were weighed
and then crushed and homogenized. Phosphorus con-
centration in shoots was determined according to John-
son and Ulrich (1959): 0.3–0.5 g shoot dry sample was
weighed and digested with a mixture of 5 mL of con-
centrated sulfuric acid and 8 mL of 30% v/v H2O2. The
solution was then to a 50 mL volumetric flask,
diluted with deionized water to volume, and
mixed; a 5 mL subsample was analyzed by the
molybdo-vanadophosphate method at 440 nm by
spectrophotometry.
All roots were carefully picked up from soil. Follow-
ing root excavation, the soil adhering to roots was de-
fined as rhizosphere soil and was sub-sampled for the
pH and the acid phosphatase (phosphomonoesterase)
and phytase activity measurements. Roots were washed
in deionized water and then scanned with an EPSON
root scanner at 400 dots per inch (Epson Expression
1600 pro, Model EU-35, Tokyo, Japan). The total root
length, root surface area and average root diameter were
analyzed using software Win-RHIZO (WinRhizo
Pro2004b, version5.0, Regent Instruments Inc., Quebec,
QC, Canada). Afterwards, fine roots were cut to 1 cm
segments and thoroughly mixed. A subsample (approx-
imately 0.5 g) was cleared with 10% (w:v) KOH at
90 °C for 2 h and stained with trypan blue, followed
by measuring mycorrhizal colonization using the grid-
Plant Soil
line intersect method (Trouvelot et al. 1986). After-
wards, all the roots were collected and dried at 75 °C
for 72 h and weighed to calculate the specific root
length.
Acid phosphatase (phosphomonoesterase) activity in
the rhizosphere soil was analyzed according to Neu-
mann (2006): 0.5 mL soil suspension (0.5 g rhizosphere
soil mixed with 2 mL deionized water) was transferred
into 2-mL Eppendorf vials, and then 0.4 mL acetate
buffer (pH 5.2) and 0.1 mL substrate [pNPP (p-
nitrophenylphosphate); Sigma St. Louis, MO, USA]
were added. The mixed solution was incubated for
30 min at 30 °C. The reaction was terminated with
0.5 mL 0.5 M NaOH, and the mixture was centrifuged
for 10 min at 12,000×g. In controls, NaOH was added
before incubation. The concentration of pNP (p-nitro-
phenol) in the supernatant was measured spectrophoto-
metrically at 405 nm.
Phytase activity in the rhizosphere soil was analyzed
as follows (Richardson et al. 2000): 0.5 mL soil suspen-
sion (prepared by mixing 0.5 g rhizosphere soil with
2 mL deionized water) was supplemented with 2 mL
30 mM MES [2-(N-morpholino)ethanesulfonic acid]
buffer (pH 5.5), 0.5 mL 2 mM EDTA and 0.5 mL
20 mM Na-phytate (Sigma, St. Louis, MO, USA). The
mixture was incubated for 1 h at 37 °C and the reaction
terminated with 1 mL 25% v/v trichloroacetic acid
(TCA). Suspensions were subsequently centrifuged at
12,000×g for 10 min. In controls, TCA was added prior
to incubation. The orthophosphate concentration in the
supernatant was determined by measuring absorbance at
882 nm using the molybdenum-blue reaction.
Experiment II: Nutrient supply × planting patterns
To address the question of how soil P heterogeneity
affects root interactions between HMY and XY335, we
set up a rhizobox experiment comprising four phospho-
rus supply treatments (Porg or Pinorg supplied either
heterogeneously or homogeneously) and three planting
patterns: two monocultures (HMY/HMY or XY335/
XY335) and mixed culture (HMY/XY335). Therefore,
12 treatments with five replicates per treatment were set
up in Experiment II.
For the homogeneous P treatment, 50 mg total P kg−1
was spread uniformly throughout the soil. For the het-
erogeneous P treatment, the same amount of P as in the
homogeneous treatment was placed at the centre of the
rhizobox in a 3-cm P-rich column [in cm, 3 (width) ×
Plant Soil
1.5 (thickness) × 35 (length), Fig. 1], referred to as the P-
rich patch (about 333 mg P/kg soil). Two phosphorus
forms (Porg and Pinorg) were tested as in Experiment I.
Experiment II was conducted in the same greenhouse
as experiment I in June. The temperature range was 28–
31 °C with 14–17 h daytime throughout the growth
period. Plants were harvested 30 DAS and separated
into shoots and roots. To ensure the maize roots were
unbroken (and separated from the neighbouring maize
in the mixture treatments), we put individual rhizoboxes
into a water-filled container (150 × 50 × 15 cm), washed
away all soil with running tap water, and then carefully
separated the roots of neighbouring plants. The roots
were analyzed with a scanner and software to measure
the root morphology parameters as in Expt I. Both the
shoots and roots (after scanning) were dried at 75 °C for
72 h and weighed. The shoot P content was determined
as described above.
Statistics
To determine how root morphology and physiology of
two maize genotypes responded to the low-P supply, we
used the 2-way ANOVA to test the effects of maize
genotypes, P forms and their interaction on the shoot
biomass and root traits (Expt I).
In experiment II, 2-way ANOVA was performed to
test the effects of P forms, nutrient supply patterns
(heterogeneous and homogeneous) and their interaction
on the total root length, root biomass, shoot biomass and
shoot P content of the two genotypes under monoculture
or mixture condition; when appropriate, the post-hoc
means comparisons were done using the Tukey’s test
at 5% probability level (P ≤ 0.05) in SPSS 21.0 (SPSS
Inc., Chicago, IL, USA).
To test the root morphological plasticity of the two
genotypes, the root response ratio (RRS) to nutrient
patch was calculated. The RRS was defined as the extent
of total root proliferation under heterogeneous vs. ho-
mogeneous nutrient supply (Li et al. 2014). The formula
was:
h
0 0 
0 0 i
RRS ¼ ∑ Ra b −Rab = Ra b þ Rab =n
where Ra′b′ and Rab are the total root length in, respec-
tively, the heterogeneous and homogeneous P environ-
ments in a given planting pattern. The a′ and a represent
the heterogeneous and homogeneous P supply treat-
ments, and the b′ and b are two randomly selected
individuals from five replicates of the same maize ge-
notype in the heterogeneous and homogeneous P supply
treatments, respectively. The n is the number of Ra′b′ −
Rab values. Three-way analysis of variance (ANOVA)
was adopted to test the influence of genotypes, P forms
and planting patterns on the RRS.
To test the competitive advantage of XY335 and
HMY in the mixture treatments under different P envi-
ronments, the competitive ratio was calculated by the
formula ∑[(Xmix/Xmono)/(Hmix/Hmono)]/n (adapted
from Morris and Garrity 1993). The Xmix and Xmono
are biomass or nutrient content of two randomly select-
ed individuals (in each of five replicates) of XY335 in
mixture and monoculture treatments, respectively; the
same applies to HMY genotype (Hmix and Hmono).
The n is the number of the (Xmix/Xmono)/(Hmix/
Hmono) values. The value greater than 1 indicates com-
petitive advantage of XY335 in the mixture. Two-way
ANOVA was used to test the competitive ratio regarding
root biomass, shoot biomass and shoot P content in the
mixture.
Results
Different root responses to P-limited environments
between genotypes (Expt I)
There was a significant effect of genotypes on total root
length, root surface area and mycorrhizal colonization
(Table 1). Compared to HMY, the total root length of
XY335 was 26–33% higher, and the root surface area
was 47–81% larger, but mycorrhizal colonization was
lower 16–19% regardless of the P forms (Table 2).
There was a significant positive relationship between
total root length and shoot P concentration in XY335
(r2 = 0.60, P = 0.008), but no significance was noted for
HMY (P = 0.997) in P-limited environments, especially
in the Porg treatments (Fig. S1), hinting XY335, but not
HMY, could rely more on increasing root length to
increase P capture.
Specific root length (SRL) and average root diameter
were significantly influenced by the interaction of maize
genotypes and P forms (Table 1). The SRL of HMY was
similar between the Porg and Pinorg treatments, whereas
SRL of XY335 was much higher in the Porg, but lower
in the Pinorg treatment, compared with HMY (Table 2).
The average root diameter of XY335 was lower in the
 Plant Soil

Table 1 Expt I: the results of 2-way ANOVA for the effects of maize genotypes (G) and P forms (PF, organic or inorganic) on shoot biomass
and the root morphological and physiological (enzymatic activities and pH in the rhizosphere) traits

Variables d.f. G PF G*PF

Shoot biomass (g plant−1) 1, 16 0.33 ns 5.5* 17***

Total root length (m plant−1) 1, 16 9.0** 0.04 ns 0.15 ns
2 −1
Root surface area (cm plant ) 1, 16 42*** 2.4 ns 2.9 ns
Specific root length (m g−1 root dry weight) 1, 16 0.65 ns 5.4* 13**
Average root diameter (mm) 1, 16 3.0 ns 2.5 ns 40***
Mycorrhizal colonization (%) 1,16 29*** 1.8 ns 0.41 ns
Acid phosphatase in rhizosphere (μg pNP g−1 soil min−1) 1, 16 19*** 17*** 0.11 ns
−1 −1
Phytase in rhizosphere (μg P g soil h ) 1, 16 41*** 6.7* 1.5 ns
Rhizosphere pH 1, 16 0.41 ns 0.06 ns 0.07 ns

pNP = para-nitrophenol
Significance levels are shown as: ns non-significant at P = 0.05, * P ≤ 0.05, ** P < 0.01, *** P < 0.001

Porg than the Pinorg treatment, but the opposite applied to
HMY (Table 2).
The acid phosphatase and phytase activities differed
between the two maize genotypes and P forms (Table 1):
acid phosphatase and phytase activities were higher in
the rhizosphere of HMY than XY335 (31–50% higher
in the Pinorg and 65–83% in the Porg treatment, Table 2)
and higher in the Porg than Pinorg treatment (27–30% in
HMY and 18–45% in XY335). The rhizosphere pH did
not differ among the treatments (Table 2).
There was a significant interaction of maize geno-
types and P forms on shoot biomass (Table 1). Organic
and inorganic P had a contrasting effect on shoot growth
of HMY and XY335: the shoot biomass of HMY was
higher, and that of XY335 lower, in the Porg than Pinorg
treatment (Table 2).
Root proliferation in different P supply patterns (Expt II)
For HMY, only heterogeneous Porg supply in monocul-
ture significantly improved the total root proliferation
(Table S1; Fig. 2a). For XY335, P supply patterns had a
significant effect on total root length in monoculture
(Table S1), particularly in the heterogeneous Porg envi-
ronment (Fig. 2c). Moreover, there was a significant 2-
way interaction effect of P forms and P supply patterns
on total root length of XY335 in mixture: total root
length under heterogeneous Porg was about 2.7-fold

Table 2 Expt I: shoot biomass and the root morphological and physiological (enzymatic activities and pH in the rhizosphere) traits of two
maize genotypes (HMY and XY335) in the homogeneous organic phosphorus (Porg) and inorganic phosphorus (Pinorg) environments

Variables HMY XY335

Porg Pinorg Porg Pinorg

Shoot biomass (g plant−1) 0.94 ± 0.04a 0.82 ± 0.04b 0.70 ± 0.06b 1.1 ± 0.1a
Total root length (m plant−1) 20.5 ± 2.6b 19.3 ± 1.3b 25.9 ± 1.6a 25.6 ± 2.0a
Root surface area (cm2 plant−1) 340 ± 34b 345 ± 29b 616 ± 46a 507 ± 21a
Specific root length (m g−1) 87 ± 9b 86 ± 8b 100 ± 7a 61 ± 3c
Average root diameter (mm) 0.36 ± 0.01b 0.32 ± 0.01c 0.32 ± 0.01c 0.38 ± 0.01a
Mycorrhizal colonization (%) 54 ± 3a 51 ± 2a 44 ± 1b 43 ± 1b
Acid phosphatase in rhizosphere (μg pNP g−1 soil min−1) 3.8 ± 0.3a 3.0 ± 0.2b 2.9 ± 0.1b 2.0 ± 0.1c
Phytase in rhizosphere (μg P g−1 soil h−1) 8.6 ± 0.5a 6.6 ± 0.7b 4.7 ± 0.4c 4.0 ± 0.4d
Rhizosphere pH 8.0 ± 0.1a 8.1 ± 0.1a 8.1 ± 0.1a 8.0 ± 0.1a

Each value is the mean of five replicates (±SE). Different letters denote significant difference (P ≤ 0.05) among treatments in a row
Plant Soil

Monoculture Mixture
80
(a) HMY (b) HMY
Total root length (m plant-1) PF: 4.5 * PF: 2.7 ns
Nutri.: 1.7 ns Nutri.: 0.59 ns
60 PF x Nutri.: 2.9 ns PF x Nutri.: 0.52 ns

40 a'
a
b a' a'
a' a a
20

0
80
(c) XY335 (d) XY335
a
PF: 1.4 ns
Total root length (m plant-1)

PF: 0.87 ns
Nutri.: 6.6 *
Nutri.: 6.9 *
60 PF x Nutri.: 0.20 ns
PF x Nutri.: 6.5 *

40 a' b bc
a
a'
b c
20

0
Hetero Homo Hetero Homo Hetero Homo Hetero Homo
Organic phosphorus Inorganic phosphorus Organic phosphorus Inorganic phosphorus
Fig. 2 Expt II: total root length of maize genotypes HMY and Different letters in each graph denote significant difference be-
XY335 in four P supply patterns (homogenous or heterogeneous tween nutrient supply treatments within the P form (P ≤ 0.05). PF:
with inorganic or organic P) and two planting patterns (monocul- organic or inorganic; Nutri: nutrient supply treatments; Homo:
ture vs mixture). Each value is the mean of five replicates (±SE). homogeneous P supply; Hetero: heterogeneous P supply

greater than homogeneous Porg and 75% greater com- supply. The RRS was significantly influenced by the
pared with the two Pinorg treatments (Fig. 2d). interaction of P forms, planting patterns and genotypes
The changes in root growth could also be reflected in (F1, 192 = 23; P < 0.001). However, the trends were dif-
the root response ratio (RRS) to the heterogeneous P ferent between HMY and XY335 (Fig. 3): for HMY, the

Fig. 3 Expt II: root response ratio 0.6 G: 40 ***

(RRS) of two maize genotypes (G) M: 0.00 ns a
Response ratio of total root length

to heterogeneous supply of inor- 0.5 PF: 24***

G x M x PF: 23***
ganic (Pinorg) or organic P (Porg)
form (PF) under monoculture and 0.4
mixture (M). The RRS is calculat-
ed as the ratio of the total root 0.3
length in the heterogeneous vs. b
b
homogeneous P supply treatments. 0.2 b
The positive RRS value means
heterogeneous P improved root 0.1 b
growth compared to homogeneous
P supply in monoculture or mix- 0.0
ture. Different letters denote sig-
nificant difference among treat- -0.1 c
ments (P ≤ 0.05) c c
-0.2 HMY XY335 HMY XY335 HMY XY335 HMY XY335
Mono-Porg Mono-Pinorg Mix-Porg Mix-Pinorg
 Plant Soil

only RRS value higher than zero was in the heteroge-
neous Porg treatment in monoculture; in contrast, all the
RRS values of XY335 were positive regardless of the
treatment, with the highest value recorded in the hetero-
geneous Porg supply in the mixture.
Plant growth and outcome of competition
In both monoculture and mixture, P supply pattern
had a significant effect on shoot biomass of HMY
(Table S1). In monoculture, the heterogeneous Porg
and Pinorg supply significantly improved shoot bio-
mass of HMY compared with the homogeneous P
supply (Fig. 4a); in contrast, shoot biomass of HMY
was higher in the homogeneous than heterogeneous
Porg supply in the mixture, and a similar but non-
significant trend was present between the homoge-
neous and heterogeneous Pinorg treatments (Fig. 4c).
Compared with the homogeneous P supply, the
heterogeneous Porg supply improved root biomass of
HMY only in monoculture (Fig. S2). In mixture, het-
erogeneous P supply had a negative effect on shoot P
content of HMY, regardless of phosphorus forms (Fig.
S3b); in contrast, there were no significant differences
among treatments in monoculture (Fig. S3a).
For XY335, there was a significant 2-way interactive
effect of P forms and P supply patterns on root and shoot
biomass in both monoculture and mixture (Table S1).
Among the four treatments in each planting pattern,
XY335 had the highest shoot biomass in heterogeneous
Porg supply and the lowest in homogeneous Porg treat-
ments, especially in mixture conditions (Fig. 4c, d).
Compared with the homogeneous Pinorg treatments, het-
erogeneous Pinorg supply also exhibited trends of im-
proving XY335 shoot growth, but the positive effects
were not significant in the two planting patterns (Fig. 4c,
d). Heterogeneous Porg and Pinorg improved XY335 root
biomass in monoculture (Fig. S2c), but only

Monoculture Mixture
2.5
(a) HMY (b) HMY PF: 2.0 ns
PF: 0.31 ns Nutri.: 7.8 *
2.0 Nutri.: 21 *** PF x Nutri.: 0.06 ns
Shoot biomass (g plant-1)

PF x Nutri.: 1.6 ns
a'
1.5 a' a
a
b a'
1.0 b'
b

0.5

0.0
2.5
(c) XY335 (d) XY335
PF: 3.4 ns PF: 0.004 ns
Nutri.: 35 *** a Nutri.: 39 ***
2.0
Shoot biomass (g plant )

PF x Nutri.: 14 **
-1

PF x Nutri.: 8.7 **

a b
1.5 ab
b
bc
1.0
c
c
0.5

0.0
Hetero Homo Hetero Homo Hetero Homo Hetero Homo
Organic phosphorus Inorganic phosphorus Organic phosphorus Inorganic phosphorus
Fig. 4 Expt II: shoot biomass of maize genotypes HMY and replicates (±SE). Different letters in each graph denote significant
XY335 as influenced by the P form (organic and inorganic, PF) difference among treatments (P ≤ 0.05). Homo: homogeneous P
and P supply patterns (heterogeneous and homogeneous, Nutri.) in supply; Hetero: heterogeneous P supply
different planting patterns. Each value is the mean of five
Plant Soil

heterogeneous Porg increased root growth of XY335 in
mixture (Fig. S2d).
Compared with the homogeneous P treatments, only
the heterogeneous Porg treatment improved shoot P con-
tent of XY335 in either monoculture or mixture condi-
tions (Fig. S3c, S3d). In contrast, compared with het-
erogeneous P supply, homogeneous Porg or Pinorg supply
increased shoot P content in HMY grown in mixture
(Fig. S3b).
In all the mixture treatments, the competitive ratios
regarding root biomass, shoot biomass and shoot P
content were significantly influenced by the interaction
of P forms and P supply patterns (all P < 0.001;
Table S2). For shoot biomass and shoot P content, all
the competitive ratios were greater than 1 in the hetero-
geneous and lower than 1 in the homogeneous P supply
(Fig. 5), suggesting that genotype XY335 could have a
competitive advantage over HMY when grown in mix-
ture in heterogeneous P environments, whereas the re-
verse was true in homogeneous P environments. How-
ever, root biomass exhibited different patterns; the
values were greater than 1 in organic P environments,
especially in heterogeneous Porg supply, and were lower
than 1 in both homogeneous and heterogeneous Pinorg
environments (Fig. 5). Interestingly, all the competition
ratios regarding root and shoot biomass and shoot P
content were higher in heterogeneous Porg than hetero-
geneous Pinorg environments (Fig. 5). Overall, the com-
petitive ratio regarding root biomass was more likely to
be affected by P forms, whereas competitive ratios
regarding shoot biomass and shoot P content were
strongly influenced by P supply patterns (Fig. S5).
Discussion
We compared two maize genotypes varying widely in
their root traits to examine their competitive ability
under various P-limited environments (different P forms
and supply patterns). There were three key findings.
Firstly, genotype HMY (bred in nutrient-poor habitats)
had a stronger root physiological and a weaker root
morphological response to P-limited environments than
genotype XY335 (bred in nutrient-rich habitats). Sec-
ondly, XY335 had greater root proliferation than HMY
in heterogeneous P supply. Thirdly, when in mixture
with HMY, XY335 had a competitive advantage in
heterogeneous P environments, but was disadvantaged

Fig. 5 Expt II: the competitive

Shoot biomass

ratio of XY335 and HMY in a Hetero-Porg

mixture in the heterogeneous Homo-Porg
c
(Hetero) and homogeneous
Hetero-Pinorg
(Homo) P environments [inor- b
ganic phosphorus (Pinorg) and or- Homo-Pinorg
c
ganic phosphorus (Porg)]. Values
greater than 1 indicate XY335
had greater competitive ability
than HMY in mixture. Different
Shoot P content

letters for each variable denote a

significant difference among c
treatments (P ≤ 0.05)
b
bc

a
Root biomass

b
c
b

0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0

Competitive ratio (XY335/HMY)

in homogeneous P conditions, especially in the Porg
treatments.
Root traits variation in maize genotypes
Plants can adapt to P-impoverished soils by changing
morphological and/or physiological root features (Lyu
et al. 2016; Wen et al. 2017). Here, old genotype HMY
showed stronger root physiological but weaker root
morphological responses than modern genotype
XY335 to adapt to low-P environments (Table 2). These
differences might have arisen from differential nutrient
availability in the environments in which these two
genotypes were selected and bred. HMY was selected
in poorly-fertile soils in which a relatively large propor-
tion of scarce P was in the organic form in 1950s, given
that only small amounts of manure and no chemical
fertilizer were used as soil inputs in China before 1960
(Li et al. 2015). However, the modern genotypes, such
as XY335, were selected in soils rich in inorganic
nutrients (Schmidt et al. 2016).
Plants from infertile environments differ from those
that were selected in more productive sites with respect
to traits functionally linked to efficient acquisition and
use of nutrients (Milla et al. 2014). In the present study
in low-P environments, we found the specific root
length of HMY was the same in the Porg and Pinorg
treatments (Table 2), but shoot biomass was higher with
Porg than Pinorg, potentially because of high activity of
phytase in the rhizosphere soil of HMY (particularly in
the Porg treatment). Compared with HMY, genotype
XY335 had lower phytase activity in the rhizosphere
soil as well as lower shoot biomass in the Porg treatments
(Table 2). Therefore, genotype XY335 had a lower
capacity to use Porg compared with genotype HMY.
Our findings hinted that selection of modern geno-
types in mineral nutrient-rich environments may have
resulted in diminishing some root traits associated with
stress resistance (see also Wissuwa et al. 2009). Indeed,
Chu et al. (2013) found that HMY had a higher mycor-
rhizal colonization and mycorrhizal responsiveness
compared to modern genotypes under low-P conditions.
This is consistent with our results on mycorrhizal colo-
nization (Table 1), and may be another reason why
HMY did not respond by altering root length to increase
P capture from low-P soils because the function of root
length can be augmented by mycorrhizal fungi (Liu
et al. 2015; Chen et al. 2016; Li et al. 2017). Conse-
quently, the root traits diversification arising from crop
Plant Soil
selection in specific nutritional environments may lead
to differential fitness between genotypes in nutritionally
variable environments.
Diversity of foraging strategy and competitive
advantage between genotypes
In monoculture, root response ratio of HMY was higher
to the Porg than Pinorg patch (Fig. 3). Porg cannot be taken
up by plants directly, which may result in low P con-
centration in shoot and thus the strong P demand, gen-
erating systemic signals to promote root proliferation
(Forde 2002; de Kroon et al. 2009) to meet the plant
nutritional requirements (Figs. S3 and S4). Root prolif-
eration (Fig. 2a) as well as the relatively high phytase
and APase activities in rhizosphere (Table 2) could
effectively contribute to capturing P in the heteroge-
neous Porg treatment to improve shoot growth of HMY
under monoculture (Fig. 4). In the inorganic P-patch,
increasing uptake capacity of roots can play an impor-
tant role in nutrient acquisition (Hodge 2004), especially
for plant species from nutrient-poor habitats (Fransen
et al. 1998). That may be why the total root length (Fig.
2) and root biomass of HMY were similar, whereas the
shoot biomass was significantly higher, in the heteroge-
neous compared with the homogenous Pinorg treatment
under monoculture. Unlike HMY, heterogeneity in ei-
ther Porg or Pinorg can stimulate root growth of XY335
under monoculture (Figs. 3 and S2), suggesting that
plants from the nutrient-rich environments may enhance
root morphological plasticity in response to nutrient-rich
patches (Grime et al. 1986).
The contrasting root trait-based foraging strategies
can confer differential competitive capacity to plants
grown in varied nutritional environments (Fransen and
de Kroon 2001). In the mixtures, the response ratio of
total root length in HMY was negative under heteroge-
neous supply of either Porg or Pinorg, whereas XY335
had positive values, especially in the heterogeneous Porg
treatment (Fig. 3). The higher root morphological plas-
ticity conferred the competitive advantage to XY335 in
the mixture with HMY under heterogeneous P condi-
tions (Fig. 5) because plants with greater root prolifera-
tion could exploit nutrient patches faster, leading to
resource pre-emption (Craine and Dybzinski 2013).
This competitive advantage of XY335 was most re-
markable in the heterogeneous Porg environments (Fig.
5). This may be attributed to the long root length of
XY335 capturing a large proportion of available P
Plant Soil
arising from hydrolysis of Porg by the strong phytase and
acid phosphatase activity in the rhizosphere of HMY, as
in the maize/faba bean intercropping systems (Zhang
et al. 2016). In contrast, a reversed trend of competitive
outcome appeared in the homogeneous environments
(Fig. 5), with shoot growth of XY335 being significant-
ly lower than HMY, especially in the homogeneous Porg
treatment. In homogeneous low-P environments, the
relatively high acid phosphatase and phytase activities
in rhizosphere represent a highly effective P-acquisition
strategy that may give HMY competitive advantage in
mixture, particularly when P is present mostly in the
unavailable organic form. Together, these findings em-
phasized that competitive advantage between
neighbouring plants can be governed by their distinct
root traits arising from specific nutrient environments in
which they evolved.
A recent study by McNickle et al. (2016) proposed
that if plant growth was suppressed by competitor, the
suppression effect would be stronger in patchy than
patch-free soil because root proliferation into nutrient-
rich patches would increase the intensity of competition
(Day et al. 2003). However, this consideration implies
the competitors with similar nutrient foraging strategies,
especially the root morphological responses to patchy
nutrients. In the study presented here we explored for-
aging strategies based on a range of root traits (morpho-
logical as well as physiological); the winners in com-
petitive situations used contrasting nutrient-acquisition
strategies in the homogeneous and heterogeneous P-
limited environments. Ignoring different trait-based for-
aging strategies may be a reason for failing to reach
definitive conclusions, i.e. only one in four species
was found to competitively suppress root growth of a
neighbour in the nutrient-patch conditions (McNickle
et al. 2016). The diversity of root traits among species
could lead to few consistent predictors of competition
belowground (Cahill 2013). Future studies are needed to
test whether these inverse competitive outcomes could
be extended to other plant genera and families to fully
understand how trait-based foraging strategies influence
inter- and intra-species interactions in natural and agri-
cultural ecosystems.
Collectively, these findings can also underlie a po-
tential P management approach in sustainable agricul-
ture systems with low input but high genetic heteroge-
neity (Wood et al. 2015). For example, the mixture of
different maize genotypes with diverse root traits may
increase the stability of maize production in various P
environments, just like in the sown grasslands (Prieto
et al. 2015). In addition, the present study also sheds
light on the differential optimal P supply patterns or P
forms for different maize genotypes to improve P
efficiency.
Conclusions
The contrasting root trait-based P-foraging strategies
were found in two maize genotypes: HMY, an old
genotype, favoured root physiological plasticity to ac-
quire P, whereas XY335, a modern genotype, relied
more on root morphological plasticity. The diversity of
root traits and P environments governed the competitive
outcome: HMY dominated and suppressed XY335
growth in the homogeneous P treatments, whereas the
competitive ability was reversed under P supply hetero-
geneity; the Porg form strengthened the difference in
competitive outcomes. These findings emphasize the
importance of considering root traits and specific nutri-
tional environments together to predict the outcome of
plant-plant interaction. This work may shed new light
on how to manipulate competition between crop species
or genotypes to enhance productivity or improve yield
stability in sustainable agriculture.
Acknowledgements This study was supported by the National
Natural Science Foundation of China (31772402, 31330070),
National Key Research and Development Program of China
(2016YFE0101100, 2017YFD0200200) and the Innovative
Group Grant of the National Science Foundation of China
(31421092). ZR is supported by Australian Research Council
(DP160104434).
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