Journal of Plant Nutrition

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Crop rhizospheric microbial community structure

and functional diversity as affected by maize and
potato intercropping

Xiao Min Qin, Yi Zheng, Li Tang & Guang Qiang Long

To cite this article: Xiao Min Qin, Yi Zheng, Li Tang & Guang Qiang Long (2017) Crop
rhizospheric microbial community structure and functional diversity as affected by maize and potato
intercropping, Journal of Plant Nutrition, 40:17, 2402-2412, DOI: 10.1080/01904167.2017.1346674

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JOURNAL OF PLANT NUTRITION
2017, VOL. 40, NO. 17, 2402–2412
https://doi.org/10.1080/01904167.2017.1346674

Crop rhizospheric microbial community structure and functional

diversity as affected by maize and potato intercropping
Xiao Min Qina,b, Yi Zhenga,c, Li Tanga, and Guang Qiang Longa
a
College of Resources and Environment, Yunnan Agricultural University, Kunming, China; bPlant Nutrition and
Fertilization Department, Guangxi South Subtropical Agricultural Science Research Institute, Chongzuo, China; cCollege
of Environment science and Engineering, Southwest Forestry University, Kunming, China

ABSTRACT ARTICLE HISTORY

Field trials were conducted to evaluate the effects of different cropping Received 31 January 2016
patterns (maize monocropping, maize and potato intercropping, potato Accepted 8 June 2016
monocropping) on microbial abundance, community structure, and microbial KEYWORDS
functional diversity using plate culture and Biolog technique. Results showed intercropping; maize;
that compared with monocropping, intercropping increased the abundance microbial community;
of soil bacteria, fungi, and actinomyces in rhizosphere surrounding maize microbial functional diversity;
and potato. The average well color development (AWCD) and Shannon index potato
(H) were higher in intercropping soil than that found in monocropping soil.
The ability of rhizospheric soil microorganisms in utilizing six types of carbon
sources had definite differences, and the most dominant community
structure was the carbohydrates metabolic groups. Principal component
analysis demonstrated that intercropping changed significantly soil microbial
community functional diversity depending mainly on carbohydrates and
carboxylic acids. Our findings suggested that maize–potato intercropping has
positive effects on the improvement of soil microbial abundances, activity,
and functional diversity.

Introduction
Soil microorganisms are the most dynamic components in soil ecosystem, play critical roles in nutrient
cycling and soil structure maintenance (Doran and Zeiss 2000), and their diversity is a sensitive indica-
tor that could reflect changes in soil quality and closely relate to plant productivity (Mader et al. 2002),
especially the functional diversity is closely related to the biochemical processes of circulation and
transformation of the elements such as carbon (C), nitrogen (N), and phosphorus (P) (Giller et al.
1997). However, soil microbial diversity is affected by a range of factors, such as planting patternssoil
type and climatic conditions, and the planting patterns as one of the most important factors.
Numbers studies have demonstrated that long-term continuous cropping will reduce the diversity of
soil microbial species, and cause the imbalance of soil microbial community structure and function
(Yusuf et al. 2009; Wang et al. 2015). Rotation could change the soil micro-ecological environment,
improve soil microbial diversity, ease continuous cropping obstacle compared to continuous cropping
(Wu et al. 2013; Trabelsi et al. 2012; Larkin 2008). Intercropping, as the most representative planting
model, has been widely spread and applied in agricultural production. Previous studies also have
shown that compared with monocropping, intercropping could increase nutrient utilization efficiency
while reduce fertilizer consumption (Ayisi et al. 1997; Li et al. 2007; Wang, Zhu, and Xia 2012), boost

CONTACT Yi Zheng zhengyi–[email protected] College of Resources and Environment, Yunnan Agricultural University, Kunming
650201, China.
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/lpla.
© 2017 Taylor & Francis Group, LLC
 JOURNAL OF PLANT NUTRITION 2403

crop yield (Nataraj et al. 2010; Mao et al. 2012), and lower disease, insect, and weed pressures (Hummel
et al. 2009; Workayehu and Wortmann 2011), and enhance rhizospheric microbial community diver-
sity (Hinsinger et al. 2011; He et al. 2013).
As a representative intercropping system, maize (Zea mays L.) with long-stalked and deep roots,
intercrop with potato (Solanum tuberosum L.) with a low light saturation point that could result in
complementary effect is greater than the competition, play an important role in increasing crop yield
(Ebwongu, Adipala, and Ssekabembe 2001), lowering disease (Sharaiha, Haddad, and Abu Blan 1989),
and have been widely spread and applied in agricultural production in the world. Previous studies con-
centrated primarily on the yield, field configuration, and group optimization (Zheng et al. 2010), but
changes in soil microbial community were not well understood in the maize and potato intercropping
system. Therefore, exploring changes in microbial abundances, community structure, and microbial
functional diversity could provide a further theoretical basis for the intercropping system.

Materials and methods

Study site
Field experiments were conducted on the farm of Yunnan Agricultural University at Xundian, north-
east Kunming, Yunnan province, China (23
320 N103
130 E). This region has a subtropical monsoon
climate with an average annual precipitation of 1040 mm, an average annual temperature of 14.7
C,
and an altitude of 1953.5 m. The initial basic properties of the soil are shown in Table 1, these differen-
ces were due to the field experiment sites were not different in 2013 and 2014, we changed an experi-
ment site because the farm land reformation in 2014, the soil was poor relatively compared to that in
2013, but all did not affect our results that we wanted to study in intercropping system.
The Xundan-7 maize (Z. mays L.) and Hui-2 potato (S. tuberosum L.) were chosen for the field study.

Experiment design
Field experiments were conducted with three planting treatments which consisted of maize monocrop-
ping, maize and potato intercropping, potato monocropping and three replications, a total of nine plots
in a random block design, the plot area was 32.50 m2 (5 m £ 6.5 m). For intercropping, the planting
ratios of maize and potato was 2:2, i.e. every two rows maize intercropped with two rows potato at one
strip and three replicated strips in per plot. The maize were planted with a row width of 0.5 m and a
plant spacing of 0.25 m, and potato with a row spacing of 0.5 m and a plant spacing of 0.35 m. The
planting density in intercropping plot was same as monocropping.
Urea, super phosphate and potassium sulfate were applied as nitrogen (N), phosphorus (P), and
potassium (K) fertilizers for experiments. For maize, nitrogen fertilizers rates were applied three times,
namely 40%, 25%,and 35%, and potato were applied two times: 60% and 40%. Phosphorus fertilizer
phosphorus pentoxide (P2O5) of 75 kg ha¡1 and potassium fertilizer potassium oxide (K2O) of 125 kg
ha¡1 were applied as the form of basal fertilizer, and the fertilizer rates were same inper plot.

Soilsampling
Sampling took place at jointing stage/squaring stage and maturing stage in 2013 and 2014, first took
theplant roots from the soil, shook loose soil off, and then brushed off the soil that was strongly

Table 1. Physicochemical properties of the soil in 2013 and 2014.

Organic C (g kg¡1) AvailableN (mg kg¡1) AvailableP (mg kg¡1) AvailableK (mg kg¡1) pH

2013 25.06 87.37 23.31 207.82 6.79

2014 18.44 36.61 2.5 117.83 7.28
2404 X. M. QIN ET AL.

adhered to the roots as rhizosphere soil. Choose randomly four plants in per monocropping plot and
four plants respectively in per intercropping plot, and then the rhizosphere soils of four plants were
mixed as one sample. Part of the soil was stored at 4
C until being used for the microcosm experiment
as described below, another part was air-dried, ground, and passed through 1-mm and 2-mm mesh
sieves for chemical analysis.

Measurements
Abundance measurements of culturable microorganisms
According to the methods conducted by Lin (2010), the total numbers of cultured bacteria, fungi, and
actinomycetes were determined as the number of colony forming units (CFUs) on agar plates using
the dilution plate methods.

Biolog ecoplates analyses

Biolog Ecoplates (Biolog Inc., Hayward, CA, USA) were used to determine the soil microbial functional
diversity based on the utilization of 31 carbon substrates (Garland and Mills 1991). Fresh soils (10 g)
were extracted by shaking for 30 min at 200 rpm with 90 ml 0.85% NaCl. This suspension was allowed
to settle for 15–30 min. Ten-fold dilutions were performed until the desired (10¡3) dilution was
reached. An aliquot (150 ml) of the diluted suspension was placed in each well of the Biolog Ecoplate
using a multi-channel repetitive-dispensing pipette. The plates were incubated at 28
C, and the absor-
bance at 590 nm was recorded at 24 hr intervals for 10 days using the reader incorporated into the
Biolog GEN III Micro Station TM (USA). Three replicates per treatment and sampling time were
performed. The readings at 120 hr were used for the statistical analysis.
The overall rate of substrate utilization by microorganisms was measured by calculating the Average
Well Color Development (AWCD) for each plate:
X
AWCD D ðCi ¡ Ri Þ=31

where Ci is the OD in each carbon source well and Ri is the OD of control well. The microbial commu-
nity diversity was calculated by the Shannon index:
X
HD ¡ Pi ðlnPi Þ

where Pi is calculated by subtracting the control from each substrate absorbance

P and then dividing this
value by the total color change recorded for all 31 substrates, PiD (Ci¡Ri)/ (Ci¡Ri). The evenness
was calculated as E D H/ln (richness), where richness referred to the number of substrates utilized.

Statistical analysis
The data for the different treatments were analyzed by Fisher’s least significant difference (LSD) test at
a significance level of 0.05 after verifying the significance by analysis of variance (ANOVA) and the car-
bon sources utilization data were also subjected to Principal Component Analysis (PCA) and ANOVA
was then performed to analyze the computed data using SPSS 19.0 software and Microsoft Excel 2010.

Results
Cultured microbial abundances affected by intercropping
Bacteria
Soil bacteria are the main components of soil microorganisms, can decompose all kinds of organic
matter. In 2013 and 2014 (Table 2), intercropping significantly increased the soil bacteria abundances
 JOURNAL OF PLANT NUTRITION 2405

Table 2. Effects of maize and potato intercropping on abundances of rhizospheric soil microorganisms.

2013 2014
Growth
Item Crops stages M I M I

Bacteria quantity Maize Jointing stage 141.00 § 1.69 b 162.25 § 1.89 a 138.22 § 2.24 b 166.50 § 3.58 a
(£ 106CFU¢g¡1) Maturing stage 112.65 § 3.71 b 157.54 § 2.71 a 79.81 § 3.19 b 97.81 § 2.93 a
Potato Squaring stage 74.72 § 1.02 b 101.71 § 2.61 a 132.12 § 3.29 b 171.58 § 3.36 a
Maturing stage 65.50 § 4.57 b 106.28 § 3.47 a 70.64 § 2.67 b 109.58 § 1.41 a
Fungi quantity Maize Jointing stage 10.85 § 1.53 a 11.72 § 1.02 a 23.62 § 3.41 a 28.95 § 2.87 a
(£ 104 CFUg¡1) Maturing stage 5.75 § 0.66 b 14.22 § 1.30 a 39.03 § 2.66 b 43.17 § 2.55 a
Potato Squaring stage 12.60 § 0.86 b 17.76 § 0.37 a 68.18 § 2.70 b 116.73 § 3.87 a
Maturing stage 7.36 § 0.65 b 13.58 § 1.59 a 27.33 § 3.09 b 56.27 § 2.18 a
Actinomyces quantity Maize Jointing stage 24.32 § 0.87 a 25.70 § 0.83 a 21.63 § 1.82 b 27.26 § 0.29 a
(£ 105 CFUg¡1) Maturing stage 39.98 § 0.99 b 46.95 § 2.02 a 13.35 § 2.06 a 16.42 § 2.40 a
Potato Squaring stage 33.68 § 0.36 b 35.26 § 0.25 a 25.05 § 2.49 b 34.89 § 2.49 a
Maturing stage 28.56 § 0.68 b 35.16 § 1.85 a 18.62 § 2.10 a 19.08 § 3.28 a

M: Monocropping; I: Intercropping. Different small letters meant significant difference between monocropping and intercropping pat-
tern at 0.05 leve1. The same below.

in the rhizosphere surrounding maize and potatoin comparison with that observed in monocropping.
Furthermore, the maize rhizospheric soil bacteria abundances were higher than that found in potato at
two growth periods, which was caused by exudates of the different types and quantities which were
released by different phyletic orgenotypic plants (Hu et al. 2006).

Fungi
Fungi in soil are less than the abundance of bacteria, but the biomass of fungiin soilis larger, and the
role can not be ignored. In 2013 and 2014 (Table 2), the potato rhizospheric soil fungi abundances at
squaring stage were greater than that found at mature stage, while the maize rhizospheric soil fungi
abundances had different changes.At the maturing stage, the fungi abundances of intercropped maize
significantly increased by 147.30% and 10.61%, respectively, in comparison with that found in mono-
cropped maize. Furthermore, the fungi abundances of intercropped potato at two growth stages also
were significantly higher than that observed in monocropped potato.

Actinomyces
The abundance of soil actinomyces is between bacteria and fungi. In 2013, the intercropped maize rhi-
zospheric soil actinomyces abundances were 17.43% higher than that observed in monocropped at the
mature stage, while that significantly increased by 36.03% at jointing stage in 2014 (Table 2). Further-
more, the actinomycetes abundances of intercropped potato at two growth stages were 1.39, 1.05 and
1.23,1.02 fold higher than that observed in monocropped, respectively.

Microbial functional diversity

Effects of intercropping on average well color development (AWCD)
The AWCD is a good indicator for the metabolic activity of microbial community and closely corre-
lates with the functional diversity (Zabinski and Gannon 1997; Benizri and Amiaud 2005). The
AWCD of the soil was almost zero after the first 24 hr incubation period but gradually increased with
an increase in the incubation time. Furthermore, the AWCD values were higher in intercropping soil
than that found in monocropping soil (Figure 1A).
As shown in Figure 1B, on the culture time of 120 hr, intercropped potato presented the highest
AWCD, and the monocropped exhibited the lowest AWCD. In addition, the AWCD values of inter-
cropping soil was 17.36% higher than that observed in monocropping soilfor maize, as well as the
AWCD values of intercropping soil increased by 3.76% compared with those found in monocropping
soil for potato. Moreover, the AWCD values of potato rhizospheric soil were greater than those found
2406 X. M. QIN ET AL.

Figure 1. Effects of maize and potato intercropping on average well color development (AWCD) of 31 carbon sources. Note: MM:
Monocropping maize; IM: Intercropping maize; MP: Monocropping potato; IP: Intercropping potato.

in maize.The above analysis showed that maize and potato intercropping can promote the ability of soil
microorganisms in utilizing carbon sources and increase microbial metabolic activity.

The differences in utilizing six types of carbon source by rhizospheric microorganisms

The ability of soil microorganisms in utilizing different carbon sources reflects the metabolic functional
groups of soil microorganisms. As shown in Figure 2, different cropping patterns had significant effect
on utilization ability of different carbon sources by soil microorganisms. The dominant microbial com-
munity structures were the metabolic groups of carbohydrates, amino acids and amine in monocrop-
ping soil, while that were the carbohydrates metabolic groups, amino acids metabolic groups,
carboxylic acid metabolic groups in intercropping soil.
Different cropping patterns had significant differences on ability of soil microorganisms in utilizing
carbohydrates, amino acids, carboxylic acids, polymers, phenolic acids, and amines are given in Table 3.
When compared with monocropping, intercropping increased respectively the ability of maize rhizo-
spheric soil microorganisms to utilize amino acids, carboxylic acids, polymers, and phenolic amine by
5.47%, 70.92%, 89.76%, 23.42%, and 156.85%, while decreased the utilization of carbohydrates. Also,
intercropping increased the potato rhizospheric soil microbial utilization of carboxylic acids, polymers,
and phenolic acid scompared with monocropping, but decreased the microbial utilization of carbohy-
drates, amino acids, and amine. Furthermore, the ability of potato rhizospheric soil microorganisms in
utilizing six types of carbon sources was higher than that observed in maize.

Analysis of rhizospheric soil microbial physiological carbonmetabolic fingerprint

Theability of soil microorganisms to utilize different carbon resources on the micro-plate is
defined as Biologmetabolic fingerprinting. As shown in Figure 3, intercropping increased the abil-
ity in utilizing D-xylose, L-a-glycerol phosphate, a-D-lactose, b-methyl-D-glucoside, i-Erythritol,
D-mannitol, L-phenylalanine, L-arginine, pyruvic acid methyl ester, D-Glucosaminic acid, D-Gal-
acturonic acid, D-malic acid, Tween-40, Cyclodextrin, Putrescine, and 2-hydroxybenzoic acid by

Figure 2. Percentage of utilized substrates by rhizospheric soil microorganisms. Note: CH: Carbohydrates; AA: Amino acids; CA:
Carboxylic acids; PM: Polymers; AM: Amines; PA: Phenolic acids.
 JOURNAL OF PLANT NUTRITION 2407

Table 3. Effect of intercropping on the ability to utilize six types of carbon sources by rhizospheric microorganisms.

Crops Cropping patterns Carbohydrates Amino acids Carboxylic acids Polymers Phenolic acids Amines

Maize M 1.367 aA 1.151 aB 0.612 bC 0.381 bD 0.292 bD 0.619 bC

I 1.257 aA 1.214 aA 1.046 aA 0.723 aB 0.750 aB 0.764 aB
Potato M 1.664 aA 1.761 aA 0.995 aB 0.801 aB 0.785 aB 1.388 aA
I 1.404 aA 1.464 aA 1.172 aB 1.047 aB 0.999 aB 1.041 aB

Different capital letters in the same row mean significantly different (p < 0.05).

Figure 3. Effect of intercropping on the utilization of 31 sole carbon sources by rhizospheric soil microorganisms.
2408 X. M. QIN ET AL.

maize rhizospheric soil microorganisms compared with the values obtained in the monocropping.
For potato, the microbial utilization of D-xylose, i-Erythritol, L-phenylalanine, L-serine, pyruvic
acid methyl ester, D-Glucosaminic acid, D-Galacturonic acid, Itaconic acid, D-malic acid, Tween-
40, Cyclodextrin, Glycogen, Putrescine, and 2-hydroxybenzoic acid were higher than those found
in the monocropping. Furthermore, the microbial utilization of D-xylose, i-Erythritol, L-a-glyc-
erol phosphate, L-threonine, itaconic acid, a-ketobutyric acid, and 2-hydroxybenzoic acid all
were weaker than other carbon resources.
Carbohydrates (Cell: D-Cellobiose, Lac: a-D-lactose, MteGlu: b-methyl-D-glucoside, Xyl: D-xylose,
Ery: i-Erythritol, Man: D-mannitol, AceGluc: N-acetyl-D-glucosamine, GluPho: glucose-1-phosphate,
GlyPho: L-a-glycerol phosphate, GalLac: D-Galactonic acid g-lactone).

Principal component analysis of rhizospheric soil microbial diversity

To provide a more straight forward interpretation of the utilization patterns for the 31 carbon
resources of all treatments, we analyzed the utilization data with a PCA. As shown in Figure 4,
the totalvariance ofthe first 11 in 31 principal components was 100%,thefirst and second principal
components explained 26.75% and 19.61% of the variance, respectively (Figure 5), were selected
to analyze the carbon substrate utilization pattern because the variance of 3 to 11 principal com-
ponent was smaller.
As shown in Figure 5, there was a significant separation between monocropping and intercropping
treatments on PC1, intercropping treatment distributed mainly on the positive direction of PC1 and
monocropping treatment distributed mainly on the negative direction of PC1, but no obvious differ-
ence on PC2, which suggested that the carbon substrate utilization pattern of soil microbial community
was significantly affected by intercropping.
As shown in Figure 6 and Table 4, the eigenvector of carbon sources with loadings greater
than 0.50 grouped numbers for PC1 had 15, four types of carbohydrates and carboxylic acids,
two types of amino acids, amines and polymers, and one type of phenolic acid. The eigenvector
of carbon sources with loadings greater than 0.50 grouped numbers for PC2 had 10, including
two types of carbohydrates and polymers, one type of carboxylic acids, phenolic acid and
amine, and three types ofamino acids. These revealed that carbohydrates, carboxylic acids were
sensitive carbon sources that distinguished difference between monocropping and intercropping
treatments.

Figure 4. Variance percentage of 31 principal components.

 JOURNAL OF PLANT NUTRITION 2409

Figure 5. Principal component analysis of carbon utilization profiles in rhizospheric microbial community of monocropping and
intercropping treatments.

Microbial functional diversity index

The microbial diversity assessed by Shannon diversity index (H) and Shannon evenness index are given
in Figure 7. For maize and potato, the Shannon diversity index and Shannon evenness index of rhizo-
spheric soil microbial community in intercropping were higher than that found in monocropping, but
there was no significant difference.

Discussion
Effects on microbial community structure
The soil microbial community structure refers to the abundances and relative proportions of the main
microflora in soil. Although the culturable microorganisms represent only less than 1% of the total
microbial community depending on the composition of the growth medium, the culturable fraction
still shows differences between monocropping and intercropping treatments. In our study, the abun-
dance of soil bacteria,actinomycetes, and fungi was higher in the rhizosphere surrounding maize and
potato under intercropping than those obtained in monocropping, which were consistent with the

Figure 6. Eigenvector of C sources with loadings for PC1 and PC2. A2–H4 mean 31 C sources of ECO.
2410 X. M. QIN ET AL.

Table 4. C sources with loadings 0.50 grouped numbers.

C sources PC1 PC2

Carbohydrates 4 2
Amino acids 2 3
Carboxylic acids 4 1
Polymers 2 2
Amines 2 1
Phenolic acids 1 1
Total 15 10

3.400 0.980 a
Shannon diversityindex

0.960

Shannon Evenness index

3.300 a a
a 0.940 a
3.200
b 0.920
3.100 a
-

a 0.900
3.000 0.880
2.900 0.860
2.800 0.840
MM IM A MP IP MM IM B MP IP

Figure 7. Effects of maize and potato intercropping on diversity index of rhizospheric soil microbial community.

results of previous studies that found that mulberry and soybean intercropping, wheat and cotton
intercropping, corn and soybean intercropping, and cassava and peanut intercropping (Hu et al. 2013;
Zhang et al. 2011; Li et al. 2013; Tang et al. 2015) could increase the soil bacteria, actinomycetes, and
fungi abundances, these results explained crops intercropping could promote the reproduction of soil
microorganisms, which might be caused byintercropping system where twoor more than two kinds of
crop were planted on the same land, so theroot exudates andplant residue swere more abundant than
monocropping that might provide more energy sources for the reproduction of microorganisms that
result in increasing abundance of soil microorganisms.

Effects on microbial metabolic functional diversity

Numerous studies have demonstrated that intercropping is conducive to maintain soil microbial commu-
nity diversity (Kihara et al. 2012; Yang et al. 2014; Li et al. 2012), and it can improve soil rhizosphere
micro environment (Suman et al. 2006; Xu, Liu, and Tao 2013) and increase microbial activity (Dong
et al. 2013) and crop yield (Nataraj et al. 2010). In this study, the metabolic activity of rhizosphere micro-
bial community was higher in intercropping soil than that found in monocropping soil for maize and
potato, and the intercropped potato presented the highest metabolic activity. The Shannon and evenness
indices for intercropping soil also were increased compared with those obtained with monocropping soil,
these indicated that intercropping could improve the microbial community functional diversity, which
may be due to different crops intercropping will release different specific root exudates lead to form the
corresponding rhizosphere microbial community, and expand crop roots interlaced to produce a rich
variety of rhizospheric exudates that could provide more nutrients for soil microorganism that result in
more obvious rhizospheric effect (He, Shen, and Zhu 2006; Hao and Lao 2001) than monocropping.
Numerous studies have indicated intercropping changed the composition of carbohydrates, amino acids,
and phenolic acids in root exudates and increased rhizosphere microbial diversity (Hao et al. 2010) and sig-
nificantly changed rhizospheric microbial community structure (Song et al. 2007; Peng et al. 2014). In this
study, PCA revealed that there was a significant difference between monocropping and intercropping treat-
ments, and the significant difference between monocropping and intercropping treatments mainly
 JOURNAL OF PLANT NUTRITION 2411

depended on carbohydrates,carboxylic acids, which indicated thatmaize andpotato intercropping changed

significantly carbon sources utilization and metabolic properties of soil microbial community.

Conclusions
Maize and potato intercropping is a one of the important practices of multiple cropping and stereo cul-
tivation in Yunnan Province and across China. The effects of such an intercropping system on the soil
microbial properties remain unclear. In this study, the abundances of soil bacteria, fungi, actinomyces,
and microbial community functional diversity in the rhizosphere surrounding maize and potato under
intercropping were increased compared with those found under monocropping. PCA demonstrated
that intercropping changed significantly metabolic activities and functional diversity of rhizospheric
microbial community depending mainly on carbohydrates and carboxylic acids. Therefore, future
research should focus on efforts to gain in-depth knowledge about the maize–potato intercropping sys-
tem underlying the changes in soil microbial properties, particularly diversity properties.

Funding
We thank to the National Key R&D Program of China (2017YFD0200200) and the National Natural Science Foundation
of China (NSFC) (31460551, 31260504, 41361065, 31210103906 and 41201289) for financial support.

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