Applied Soil Ecology 119 (2017) 250–259

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Applied Soil Ecology

journal homepage: www.elsevier.com/locate/apsoil

Effect of alternate partial root-zone drip irrigation on soil bacterial MARK

communities and tomato yield
⁎
Jingwei Wanga,c, Wenquan Niua,b, , Mingzhi Zhangd, Yuan Lia
a
Institute of Soil and Water Conservation, Northwest A & F University, Yangling, Shaanxi 712100, China
b
Institute of Soil and Water Conservation, CAS & MWR, Yangling, Shaanxi 712100, China
c
The Center of Ecological Environment Construction of Soil and Water Conservation in Shanxi Province, TaiYuan, Shanxi 030002, China
d
College of Water Resources and Architectural Engineering, Northwest A & F University, Yangling, Shaanxi 712100, China

A R T I C L E I N F O A B S T R A C T

Keywords: The aim of this study was to assess the effect of alternate partial root-zone drip irrigation (ADI) on the soil
Alternate partial root-zone drip irrigation microbial communities in the crop root zone and the relation between the soil microbial community changes and
Tomato crop growth. We investigated the effect of ADI at different lower limits of irrigation (ILLs, 50%, 60%, and 70% of
Root-zone soil the field capacity (FC)) on soil bacterial diversity in the root zone of greenhouse tomato and analyzed the
Bacteria
relation between the soil bacterial community changes and tomato growth. The soil bacterial community
Community diversity
structure was markedly different under ADI compared with SDI (ground drip irrigation). It was closely related to
the soil microenvironment. Among various environmental factors, the tomato root activity, root length, and soil
CO2 flux showed significant effects on the difference in soil bacterial communities. Environmental changes in the
root-zone soil inevitably affected crop growth, and SDI and ADI resulted in significant differences in root growth,
single fruit weight, number of fruits and fruit yield per tomato plant. Our results suggest that an ILL at 70% of the
FC could significantly improve the root-zone soil environment, which was beneficial for the organic matter,
cellulose, nitrogen and sulfur metabolism and increased the oxygen content in the root-zone soil. Therefore, the
root areas, root forks, the fruit number and the yield per plant were better under an ILL at 70% of the FC.

1. Introduction
Alternate partial root-zone drip irrigation (ADI) is a technique that
has been of increasing interest to researchers worldwide in recent years.
The ADI technique artificially controls alternate wetting and drying in
the partial root zone of crops, which can regulate stomatal con-
ductance, reduce transpiration, and improve water use efficiency
through crop root signals (Dodd et al., 2008; Kirda et al., 2007). ADI has
been shown to significantly improve water use efficiency while also
increasing crop photosynthesis (Wang et al., 2011) and preventing yield
loss (Kang and Zhang, 2004). Additionally, alternate wetting and drying
in the crop root-zone soil can stimulate root growth, enhance root ac-
tivity (Yang et al., 2010), regulate assimilation distribution (Shao et al.,
2008), and markedly increase the root-to-shoot ratio (Kang et al., 1998;
Liang et al., 2000). Changes in root growth will inevitably affect nu-
trient use in the root-zone soil. ADI has been found to facilitate root
growth and simultaneously increase leaf nitrogen concentrations in
maize (Wang et al., 2012). Moreover, alternate wetting and drying of
the soil under ADI has been found to promote nitrogen accumulation
from the soil to the root surface and, thereby, enhance the capacity of
the roots and crops for nitrogen uptake, ultimately improving the ni-
trogen-use efficiency (Wang et al., 2013).
However, the cycling and use of soil nutrients are closely associated
with soil microbes (Zhong et al., 2010). The underlying reason for ADI
improvements to soil nutrient use may be that alternate wetting and
drying changes in the root zone alter soil water and heat conditions
among the various environmental factors, thereby changing the struc-
ture of the soil microbial communities and accelerating the rate of soil
nutrient cycling. With the same amount of irrigation, alternate wetting
and drying of the soil under ADI has been found to enhance the activity
and metabolism of soil microbes, accelerate the rate of soil organic
matter mineralization, change the carbon-to-nitrogen ratio in the soil,
and promote nitrogen uptake and use by tomato (Wang et al., 2010).
Moreover, alternate wetting and drying under ADI has been reported to
accelerate the rate of carbon and nitrogen mineralization in the soil,
which can lead to soil carbon and nitrogen loss and is unfavorable to
the health of soil quality (Sun et al., 2013). Therefore, investigating the
effect of ADI on soil microbial community changes is critical for ob-
taining a better understanding of the underlying mechanisms of ADI
and the rational allocation of drip irrigation. However, relevant

⁎
Corresponding author at: Institute of Soil and Water Conservation, Northwest A & F University, No.26 Xinong Road, Yangling, Shanxi Province, 712100, China.
E-mail address: nwq@vip.sina.com (W. Niu).

http://dx.doi.org/10.1016/j.apsoil.2017.06.032
Received 31 October 2016; Received in revised form 25 June 2017; Accepted 28 June 2017
Available online 11 July 2017
0929-1393/ © 2017 Published by Elsevier B.V.
J. Wang et al.
research is lacking, and existing studies have mainly used the conven-
tional microbiological method of pure plate culture (Wang et al., 2006,
2008; Yu et al., 2008) and have found that ADI could improve soil
microorganisms in the root-zone compared to SDI, and water deficits
could improve soil permeability to promote microorganism growth.
However, the culture-based method can only detect a very small pro-
portion (0.1–1%) of the microbes in the soil environment, which does
not truly reflect the soil microbial communities (Cheung et al., 2010). A
popular technique in microbial ecology research is high-throughput
sequencing (Lin et al., 2014), which obtains a large amount of micro-
biological information and involves an automated process that can
compensate for the shortcomings of the conventional culture method.
In the present study, we believe that changes in soil bacterial (the
most important soil microorganisms) communities underlie ADI im-
provements in soil nutrients and promote crop growth. In addition,
obtaining abundant and accurate microbiological information is cen-
tral. Therefore, we used high-throughput sequencing to assess the effect
of ADI with plastic mulch on soil bacterial communities in the root zone
of a greenhouse tomato and further analyzed the relation between the
changes in the soil bacterial communities and the root growth and yield
of tomato, thereby providing evidence to prove the hypotheses. In ad-
dition, this study provides evidence for rationally allocating various
agronomic measures, facilitating crop growth, and improving the soil
and water use efficiency in the production practice of an agriculture
facility.
2. Materials and methods
2.1. Experimental site
The experiment was carried out in a plastic greenhouse in the
Dazhai Village, Dazhai County, Yangling District, Shaanxi Province,
China. The experimental site was located at longitude 108°08′E and
latitude 34°16′N, with an elevation of 521 m. This site belongs to the
warm temperate, semihumid, monsoon zone. The mean annual tem-
perature is approximately 16.3 °C, the mean annual rainfall is
535.6 mm, the mean annual sunshine time is ∼2163 h, and the mean
annual frost-free period is 210 d. The experimental soil had a bulk
density of 1.34 g cm−3 and a field capacity (FC) of 28.17% (by mass
water content). The soil contained 25.4% gravel (2–0.02 mm), 44.1%
silt (0.02–0.002 mm), and 30.5% clay (< 0.002 mm). The soil porosity
was 49.38%.
2.2. Experimental design
The experiment was performed from October 2014 to May 2015
using the tomato cultivar “Haidi” (widely cultivated locally). The
greenhouse was 108-m long in the east-west direction and 8-m wide in
the south-north direction. In the greenhouse, plots were divided from
west to east. Each plot was raised with double ridges and was 6.0 m in
length. The ridge width was 0.6 m, and the furrow width was 0.3 m,
with a height of 0.2 m and an area of 3.4 m2. Thirty-four tomato
seedlings per plot were planted in double rows, with a plant spacing of
0.35 m. Guard rows were set up at both ends of the experimental field.
The experimental design included two treatments: ground drip ir-
rigation (SDI) under plastic mulch and ADI under plastic mulch. The
SDI treatment served as the control: drip tapes were located in the
middle of the row between the tomato plants; the lower limit of irri-
gation (ILL) was set at 70% of the FC, corresponding to an upper limit of
irrigation at 75% of the FC. For the ADI treatments, the ILLs were set at
50%, 60%, and 70% of the FC, corresponding to the upper limits of
irrigation at 55%, 65%, and 75% of the FC, respectively. At both ends of
each plot, a drip tape was laid at a distance of 30 cm from the roots of
the tomato plants. Two drip tapes were used for alternate irrigation
over a period of 15–20 days. Each treatment had three replicates, and
12 plots were included in the experiment. The plastic mulch was a
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Applied Soil Ecology 119 (2017) 250–259
white, translucent, high-pressure, low-density, polyethylene film
(Xinfeng Plastic Factory, Jingjiang, Jiangsum, China), 0.014 mm in
thickness. The embedded flat drip tapes (Dayu Water-Saving Group Co.,
Ltd., Gansu, China) were 16 mm in diameter and 0.3 mm in wall
thickness, with an emitter spacing of 30 cm, working pressure of
0.1 Mpa, and emitter flow rate of 1.2 l/h.
Soil water content was measured and controlled using a Field TDR
200 soil moisture meter (Spectrum, Aurora, IL, USA). A 100-cm deep
probe was installed in the center of each plot. Soil water content was
measured at 10-cm intervals down to a depth of 60 cm. Meanwhile, soil
samples were taken by boring, and the measurements of the soil water
content were calibrated by the oven drying method. When the soil
water content dropped to the lower limit of the soil water, the water
was supplemented according to the depth of the wetting layer at 40 cm.
The irrigation amount was calculated as follows:
M = sρb phθf (q1 − q2)/η ,
where M is the irrigation amount, m3; s is the planned wetting area,
4.6 m2; ρb is the soil bulk density, 1.35 g/m3; p is the wetting propor-
tion, 0.8; h is the depth of wetting layer, 0.4 m; θf is the maximum FC,
31.54%; q1 and q2 are the upper limit of irrigation and measured soil
moisture content, respectively, %FC; and η is the coefficient of water
use, 0.95.
2.3. Analytical methods
2.3.1. Sample collection
There were 3 replicates in each treatment. When the fruit was
nearly ripe, 3 tomato plants per replicate per treatment were randomly
selected, numbered and marked. Fruit was harvested from March
18–May 3, 2015. The fruit was marked with the corresponding plant
number and weighed using a 0.01-g precision electronic balance.
After the harvest of the fruit, plant samples were collected on May 5,
2015, for laboratory analysis. The aboveground part of each plant (3
tomato plants per replicate per treatment) was cut, collected, and
numbered. At the same time, root samples were collected by whole-root
excavation. The roots of each plant (3 tomato plants per replicate per
treatment) were excavated in a rectangular area of 40 cm × 30 cm,
with the midline between adjacent plants as the boundary; the depth of
the excavation was consistent with the actual depth of the tomato roots
(∼50 cm). The overall root sample was taken from the soil, and large
soil clumps between the roots were removed. The soil attached to the
roots was vigorously shaken off onto clean filter paper that had been
sterilized at high temperature, placed in sterile plastic tubes and taken
to the laboratory for soil bacterial community analysis. The root sam-
ples were placed in mesh bags with a mesh diameter of 0.5 mm and
delivered to the laboratory for subsequent tests.
2.3.2. Soil bacterial community analysis
The root-zone soil from 3 replicates per treatment was sequenced to
analyze the bacterial communities using high-throughput sequencing
technique. The specific steps were as follows:
a DNA extraction and analysis: Bacterial DNA was extracted from the
soil samples using an E.Z.N.A.® soil DNA Kit and purified using a
DNA purification kit. The concentration and quality (OD260/OD280
ratio) of the DNA were determined using a NanoDrop 2000 spec-
trophotometer. The DNA integrity was checked by electrophoresis
on 1% agarose gels. After completion of electrophoresis, the gel was
stained with ethidium bromide (0.5 mg/L, Sigma, USA) for 20 min,
rinsed with clean water for 10 min, and then observed under UV
light (Bio-Rad, Gel Doc™ XR+, Hercules, CA, USA). The purified
DNA was stored in a freezer at −20 °C for subsequent polymerase
chain reaction (PCR) and Illumina MiSeq sequencing.
b PCR amplification: The V3-V4 region of the bacterial 16S rRNA was
amplified by PCR using the primers 338F 5′-
J. Wang et al. Applied Soil Ecology 119 (2017) 250–259

ACTCCTACGGGAGGCAGCAG-3′ and 806R 5′-GGACT
ACHVGGGTWTCTAAT-3′. The primers for each sample contained a
special barcode of eight sequences. After the completion of the
preliminary experiment, formal PCR amplification was conducted
using TransGen AP221-02: TransStart Fastpfu DNA Polymerase. The
PCR reaction contained 4 μl of 5 × FastPfu Buffer, 2 μl of 2.5 mM
dNTPs, 0.8 μl of Forward Primer (5 μM), 0.8 μl of Reverse Primer
(5 μM), 0.4 μl of FastPfu Polymerase, and a 10-ng sample of DNA,
with double-distilled water added to achieve a total volume of 20 μl.
The PCR program was performed on an ABI GeneAmp® 9700 System
with the following parameters: (a) 1 × (3 min at 95 °C), (b)
27 × (30 s at 95 °C; 30 s at 55 °C; and 45 s at 72 °C), and (c) 10 min
at 72 °C and then held 10 °C until halted by user. Each sample was
amplified in three replicates.
c DNA sequencing by the Illumina MiSeq platform: The PCR products
(3 μl) were checked by electrophoresis on a 2% agarose gel, purified
using a DNA Gel Extraction Kit, and quantified using a
QuantiFluor™-ST Fluorometer. The purified PCR products from the
three replicates were pooled at an equal molar ratio. DNA sequen-
cing results of the samples were obtained by bidirectional paired-
end (PE) sequencing on the Illumina MiSeq platform.
d Sequencing data processing: Miseq sequencing generated the PE
sequence data. First, the PE reads were merged into one sequence
according to the overlap relation. Additionally, the quality of the
reads and the effect of the merge were subjected to quality control
(QC) filtering. Effective sequences were identified, and the sequence
orientation was calibrated according to the barcode and the primer
sequences attached to the ends of the sequence.
e QC filtering of the original DNA sequences using QIIME (version
1.17): The 300 bp reads were truncated at any site receiving an
average quality score < 20 over a 50 bp sliding window, discarding
the truncated reads that were shorter than 50 bp. Next, the PE reads
were merged into one sequence according to the overlap relation-
ship; the minimum length of the overlap was 10 bp. The maximum
mismatch rate allowed in the overlap region of the merged sequence
was 0.2, and sequences that did not meet this criterion were dis-
carded. The samples were identified according to the barcode and
primer sequences at the ends of each sequence, and the sequence
orientation was adjusted. The number of mismatches allowed in the
barcode was 0, and the maximum number of mismatches allowed in
the primers was 2.The operational taxonomic unit (OTU) is a unified
designation of a taxon (e.g., strain, genus, species, and group) that is
artificially set to facilitate analysis in phylogenetics or population
genetics research. DNA sequences were classified at the 97% simi-
larity level, and each group was defined as one OTU. OTUs were
clustered with a 97% similarity cutoff using UPARSE (version 7.1
http://drive5.com/uparse/) and chimeric sequences were identified
and removed using UCHIME. The taxonomy of each 16S rRNA gene
sequence was analyzed using RDP Classifier (http://rdp.cme.msu.
edu/) against the silva (SSU115) 16S rRNA database using a con-
fidence threshold of 70% (Amato et al., 2013).
f Sequence rarefied: The sequence numbers of each sample were
normalized to 17,330 reads (the reads in A60 with the least number
of reads in four treatments). Tags with 97% similarity (Needleman-
Wunsch alignment) were grouped into OTUs to calculate the rar-
efaction curves and diversity indices.
2.3.3. Tomato root analysis
Root samples collected from the greenhouse were soaked in water in
the laboratory and washed with water to separate the soil and roots.
During washes, three layers of gauze spread at the bottom of the wash
tank collected the fine roots. The clean root samples were placed in
Ziploc bags using tweezers. A duplex scanner was used to scan the
roots, and WinRHIZO, an image analysis system, was used to measure
the total root length, root surface area and root forks. A portion of the
root samples was used to measure root activity by the triphenyl tetra-
zolium chloride (TTC) method (Zhang et al., 2013).
2.4. Data analysis
The experimental data were organized with Microsoft Excel. All
statistical analyses were performed using SPSS 22.0. The normality and
homogeneity of the data for each response variable were tested before
the statistical analyses and then analyzed via one-way ANOVA with
different treatments. The indices of bacterial community abundance,
community diversity, and sequencing depth were calculated using
MOTHUR (http://www.mothur.org). The principal component analysis
(PCA), the similarity analysis, the Venn diagrams, and the abundance-
rank curves were all generated using the relative abundance (each OTU
count was divided by the depth sequencing for each sample). A hier-
archical cluster analysis was performed using the beta diversity dis-
tance matrix (Jiang et al., 2013). A tree structure was constructed using
the unweighted pair group method with the arithmetic mean. The re-
dundancy analysis (RDA) was conducted using Canoco software. Tables
and plots were drawn in Excel 2010 and Origin 8.0.
3. Results
3.1. Soil bacterial sequence, abundance, and diversity in the root zone of
tomato under ADI and SDI
As shown in Table 1, the sequencing depth was greater than 0.986
for CK, A50, A60, and A70, indicating that the sequencing results can
truly reflect the real condition of the soil bacterial communities in the
root zone of tomato in all treatments.
Approximately 19,428; 31,167; 17,330 and 31,495 high quality
sequence reads were generated for CK, A50, A60 and A70, respectively.
Furthermore, there were significant differences in the sequence reads
among the bacterial communities for the four treatments; however no
significant difference was observed in OTU numbers. With the in-
creasing ILL, the sequence read numbers initially decreased and then
increased. The sequence reads in A50 and A70 were 1.60 and 1.62
times that in CK, respectively, whereas the sequence reads in A60 were
10.80% smaller than that in CK.
To compare the diversity indices, we normalized the sequence
number of each sample to 17,330 reads. Tags with 97% similarity

Table 1
Bacteria sequences, abundances and diversity indices of tomato root zone soil under the different treatments, CK, A50, A60 and A70.

Treatments DNA sequence Operational Taxonomic Units Abundance-based coverage estimators Coverage Diversity index

Reads OTU Ace Chao Shannon diversity Simpson diversity

CK 19428 ± 301b 1217 ± 19a 1375 ± 21b 1390 ± 30ab 0.989 ± 0.0036a 5.96 ± 0.013a 0.007 ± 0.00019a
A50 31167 ± 328a 1253 ± 14a 1458 ± 15a 1467 ± 21a 0.995 ± 0.0023a 6.00 ± 0.010a 0.006 ± 0.00011a
A60 17330 ± 306c 1199 ± 21a 1356 ± 24b 1363 ± 32b 0.986 ± 0.0012a 5.90 ± 0.013a 0.0073 ± 0.00018a
A70 31495 ± 476a 1243 ± 19a 1422 ± 21ab 1433 ± 29ab 0.993 ± 0.0032a 5.82 ± 0.010a 0.0074 ± 0.00012a

Note: The data were analyzed by one-way ANOVA with different treatments; the different lowercase letters indicate significant differences (p < 0.05) among the different test processes;
the same is true for the tables below.

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J. Wang et al.
Fig. 1. Rarefaction curves for the OTUs.
(Needleman-Wunsch alignment) were then grouped into OTUs to cal-
culate the rarefaction curves and diversity indices. There was no sig-
nificant difference in OTU numbers among the bacterial communities of
the four treatments. The rarefaction curves for the four treatments
tended to be flat, with the read numbers increasing (Fig. 1); therefore,
the amount of sequencing data was reasonable as shown by the cov-
erage in Table 1.
There were no significant differences in the bacterial community
diversity index values among the four treatments (Table 1), although
the values were higher in A50 and lower in A60 and A70 compared
with CK. Additionally, there were significant differences in the bacterial
community abundance index values among the four treatments. The
bacterial community abundance index values were higher in A50 and
A70 but lower in A60 compared with CK; the highest abundance index
values were found in A50.
Fig. 2 also shows that the species evenness of the bacterial com-
munities was similar in the four treatments (CK, S10, S20, and S30);
however, the bacterial communities in A50 and A70 showed higher
species richness than CK and A60.
3.2. Soil bacterial community composition in the root zone of tomato under
ADI and SDI
We analyzed bacteria with relative abundances accounting for more
than 1% of the soil bacterial community in the root zone of tomato for
the CK, A50, A60, and A70 treatments at the phylum classification
level. Bacteria that accounted for less than 1% of the soil bacterial
community were defined as others. As shown in Fig. 3, the bacterial
communities primarily comprised 11 groups, including Proteobacteria,
Chloroflexi, Actinobacteria, Bacteroidetes, Acidobacteria, Gemmati-
monadetes, Candidate¬_division_TM7, Firmicutes, Deinococcus-
Themus, Planctomycetes and Candidate¬_division_QD1, which ac-
counted for more than 98% of the bacterial communities in the four
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Applied Soil Ecology 119 (2017) 250–259
treatments.
With an increase in the ILL, the relative abundance of
Proteobacteria showed an increasing trend in the bacterial communities
of A50, A60, and A70; however, the three treatments remained lower
than CK by approximately 12%, 11%, and 5%, respectively. Chloroflexi
showed a decreasing trend in A50, A60, and A70 (21.05%, 19.24%, and
15.69%, respectively), all of which were higher than CK (14.68%).
Actinobacteria initially decreased before increasing in the three ADI
treatments (12.40%, 11.48%, and 12.69%, respectively), which were
lower than CK (14.24%). Bacteroidetes tended to increase in the three
ADI treatments (7.52%, 8.23%, and 11.04%, respectively), but the
abundance observed in CK (7.54%) was consistent with that observed
in A50. The abundances of Acidobacteria were 7.50%, 7.14%, and
3.98% in A50, A60, and A70, respectively; CK (4.97%) was higher than
A70 but lower than A50 and A60. Similar to the abundances of
Acidobacteria, the Gemmatimonadetes abundance in CK (5.21%) was
higher than that of A70 (4.78%) but lower than those of A50 (6.75%)
and A60 (6.58%). Candidate_division_TM7, Firmicutes and
Deinococcus-Themus showed higher relative abundances in the bac-
terial communities of A50, A60, and A70 compared with CK. As the ILL
increased, Candidate_division_TM7 showed an increasing trend,
Firmicutes initially increased before decreasing, whereas Deinococcus-
Themus increased after a decrease. The relative abundance of
Planctomycetes in the bacterial community of CK was 21.49% and
18.26% lower than that in A50 and A60, respectively, and 3.61 times
that in A70. The relative abundance of Candidate_division_OD1 in the
bacterial community of CK was 54.32% and 73.42% lower than that in
A50 and A60, respectively, and 1.58 times that in A70.
Some bacteria were present with a relative abundance less than 1%,
which accounted for less than 2% of the total bacterial community.
Next, we analyzed these trace bacteria in different treatments (Fig. 4).
Fig. 4 shows that the relative abundance of Nitrospirae was highest
among the bacteria phyla with a relative abundance less than 1% in the
J. Wang et al. Applied Soil Ecology 119 (2017) 250–259

Fig 2. The rank-abundance distribution curve of the OTUs under alternate root-zone irrigation and ground drip irrigation with plastic.

Fig. 3. The bacterial community structure at the phylum

classification level under different soil treatments, i.e., alter-
nate partial root-zone irrigation and ground drip irrigation
with plastic mulch.

four treatments. Nitrospirae decreased with increasing ILL and ac- which was significantly higher than that in the other treatments,
counted for 29.10% 19.88%, and 14.07% of the trace bacteria in A50, namely, 3.82, 2.82, and 27.68 times that in CK, A50, and A70, re-
A60, and A70, respectively, all of which were lower than that in CK, spectively. Elusimicrobia showed a higher relative abundance in CK,
31.51%. Verrucomicrobia had a relative abundance of 19.10% in A60, which was 2.58, 17.19, and 19.34 times that in A50, A60, and A70,

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J. Wang et al.
respectively. The relative abundance of cyanobacteria in A70 was 5.88,
3.02, and 9.42 times that in CK, A50, and A60, respectively. Chlorobi
had a higher relative abundance in A60, which was 2.95, 2.94, and 2.03
times that in CK, A50, and A70, respectively. Synergistetes was not
detected in the CK; the highest relative abundance was found in A50,
which was 5.10 and 1.66 times that in A60 and A70, respectively. Ar-
matimonadetes showed a significantly higher relative abundance in CK,
which was 6.25, 3.21, and 1.45 times that in A50, A60, and A70, re-
spectively. Both Thermotogae and Fibrobacteres showed significantly
higher relative abundances in A60 and A70, compared with CK and
A50.
Among the trace bacteria with relatively less abundance than 1%,
some unclassified bacteria showed a significantly different distribution
in the four treatments. The relative abundances of
Candidate_division_WS6 in A50, A60, and A70 were 2.91, 2.91, and
1.65 times that in CK. WCHB1-60 showed a relative abundance of
16.48% in A70, in contrast to 0.59% and 0.78% in A50 and A60, re-
spectively, and 0 in CK. JL-ETNP-Z39 had a significantly higher relative
abundance in A50 (13.55%), whereas TA06 had a significantly higher
relative abundance in A60 (2.34%), compared with other treatments.
3.3. PCA and RDA of soil bacterial communities in the root zone of tomato
Fig. 5 shows that the first three principal components, PC1, PC2,
and PC3 contributed 56.33%, 31.07%, and 12.6%, respectively, of the
variance in the bacterial communities of CK, A50, A60, and A70. Three
replicate samples of each treatment clustered together; however, four
treatments were separated under PC1, PC2, and PC3. In terms of PC1,
CK, A50, A60, and A70 were clearly separated, and the bacterial
communities were significantly different. In terms of PC2, the four
treatments were clearly separated, and A70 was closest to CK. In terms
of PC3, the four treatments were clearly separated, and A50 was closest
to CK.
Further analysis of the relation between the bacterial community
and the soil environmental factors revealed different degrees of corre-
lation. Here, we only showed the highest correlation (Fig. 6). Fig. 6
reveals that the tomato root activity, root length, and soil CO2 flux
showed the highest correlation with the bacterial communities of CK,
A50, A60, and A70. CK was positively correlated with the root activity
and negatively correlated with the root length and soil CO2 flux; A50
and A60 were negatively correlated with the root activity and positively
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Applied Soil Ecology 119 (2017) 250–259
Fig. 4. The trace bacterial community structure at the
phylum classification level in soils under different treatments,
i.e., alternate partial root-zone irrigation and ground drip
irrigation with plastic mulch.
correlated with the root length and soil CO2 flux; and A70 was posi-
tively correlated with the root activity and negatively correlated with
the soil CO2 flux and root length. The soil CO2 flux and root length
significantly separated CK, A50, A60, and A70, and their effects on the
four treatments were substantially different. Root activity also sig-
nificantly separated the four treatments, but the effects on CK and A60
were similar.
3.4. Root growth and yield of the tomato under ADI and SDI
The root growth and yield were determined, and some significant
difference indicators were analyzed (Table 2). The results showed that
the root areas of A50, A60, and A70 were significantly greater than the
root areas of CK, with A50 and A70 presenting significantly greater root
forks than the other two treatments. There were significant differences
in the single fruit weight, the number of fruits per plant, and the fruit
yield per plant between treatments. A50, A60, and A70 resulted in a
significantly higher number of fruits per plant than CK. CK and A70
were significantly higher than A50 in terms of the single fruit weight,
whereas no significant difference was found between A60 and A50. The
fruit yield per plant was 24.22% and 21.03% higher with A70, com-
pared to CK and A50, respectively.
4. Discussion
Our results show that compared with SDI, ADI resulted in sig-
nificantly different soil bacterial communities in the root zone of to-
mato. Little difference was observed in the bacterial community di-
versity indices; however, significant differences in the bacterial
community abundance index values were observed among the four
treatments. Wang found that ADI could improve soil microorganisms in
the maize root zone (Wang et al., 2006, 2008; Yu et al., 2008), but her
studies used conventional microbiological methods, and the results
were limited. Our use of high-throughput sequencing technology in this
study strengthens the reliability of the results. In addition, we also
found that the ILL exhibited little effect on the composition of the soil
bacterial communities and significant effects on the relative abun-
dances of the various bacteria within the community in the root zone of
the tomato under ADI. This is because ADI increases the inhomogeneity
of the soil moisture distribution (Selim et al., 2012), and the soil dry
and wet zones alternate frequently in the root zone (Sanchez-Martin
J. Wang et al.
Fig. 5. Principal component analysis of the different soil microbial communities under alternate partial root-zone irrigation and ground drip irrigation with plastic. The points with the
same color and shape indicate the replicate samples of each treatment.
et al., 2008), thereby enhancing soil nutrient mineralization to improve
bacterial growth.
When classified at the phylum level, soil bacterial communities in
the root zone of tomato under ADI and SDI mainly comprised 11 bac-
terial groups. These bacterial groups had a relative abundance greater
than 1% each and accounted for more than 98% of the bacterial com-
munity. In the soil bacterial communities under ADI, Proteobacteria
showed a greatly lower relative abundance, whereas Actinobacteria
showed a slightly lower relative abundance compared with the results
from SDI. Nitrosomonas belonging to Proteobacteria can oxidize am-
monia to nitrite (Arp et al., 2002). Actinobacteria are important de-
composers of organic matter in the soil, while they also play a role in
nitrogen cycling (Ningthoujam et al., 2009; Ventura et al., 2007).
Therefore, compared with SDI, ADI could reduce the accumulation of
nitrites in the soil and prevent their damage to the crop root zone.
With increasing ILL, the relative abundance of Proteobacteria
showed an increasing trend, whereas Actinobacteria initially decreased
before increasing under ADI. The ILL at 70% of the FC was more con-
ducive to reducing the accumulation of nitrite in the root zone,
256
Applied Soil Ecology 119 (2017) 250–259
compared with 50% and 60% of the FC; ILL at 70% of the FC could also
improve organic matter metabolism and nitrogen fixation in the root
zone (Ningthoujam et al., 2009; Ventura et al., 2007).
On the whole, the ILL at 50% and 60% of the FC could improve the
growth of Chloroflexi, Bacteroidetes, Acidobacteria,
Gemmatimonadetes and Planctomycetes, and the ILL at 70% of the FC
could significantly facilitate the growth of Bacteroidetes but inhibit the
growth of Acidobacteria, Gemmatimonadetes and Planctomycetes.
Chloroflexi can perform photosynthesis to synthesize organic substances
(Bryant et al., 2011); Bacteroidetes can degrade cellulose among var-
ious recalcitrant carbohydrates in the soil (Fernández-Gómez et al.,
2013); Acidobacteria are closely associated with the metabolism of soil
organic matter (Ward et al., 2009); Gemmatimonadetes are related to
phosphorus metabolism (Takaichi et al., 2010); and ammonia-oxidizing
bacteria belonging to Planctomycetes can acquire energy from the
oxidation of NH4+ to nitrogen with NO2− in anoxic environment (Xu
et al., 2010), which has great significance for nitrogen cycling. There-
fore, the ILL at 50% and 60% of the FC could significantly improve the
organic matter, phosphorus, and nitrogen metabolism in the root-zone
Fig. 6. Redundancy analysis (RDA) of the soil microbial
communities under alternate partial root-zone irrigation and
ground drip irrigation with plastic mulch.
J. Wang et al. Applied Soil Ecology 119 (2017) 250–259

Table 2
Root areas, root forks and yield of tomatoes under the different treatments, CK, A50, A60 and A70.

Treatments Root area/cm2 Root forks Fruit numbers per strain Single fruit weight/g Yield per plant/kg

CK 727.66 ± 46.46b 3979.00 ± 91.79c 13.83 ± 0.36b 164.24 ± 4.81a 2.27 ± 0.047b
A50 1047.88 ± 18.93a 10340 ± 24.24ab 15.79 ± 0.34a 141.26 ± 1.64b 2.33 ± 0.058b
A60 965.98 ± 26.98a 9012 ± 55.06b 16.08 ± 0.35a 160.12 ± 9.12ab 2.56 ± 0.16ab
A70 933.81 ± 54.90a 11404 ± 25.69a 16.64 ± 0.58a 175.40 ± 9.96a 2.82 ± 0.028a

Fig. 7. The relative abundance of some important metabolic bacteria in bacterial community structures at the genus classification level in soils under different treatments, i.e., alternate
partial root-zone irrigation and ground drip irrigation with plastic mulch.

Table 3
Soil porosity, CO2 flux, root activity and root length under the different treatments, CK, A50, A60 and A70.

Treatments 0–30 cm soil porosity/% CO2 flux/mg m−2 min−1 Root activity/(mg TTC g−1 h−1) Root length/cm

CK 41.37 ± 2.11ab 3.36 ± 0.17a 12.62 ± 0.71a 1473.69 ± 10.17c

A50 37.82 ± 3.23b 4.56 ± 0.49a 13.22 ± 0.25a 2524.88 ± 11.58a
A60 47.88 ± 2.80ab 4.36 ± 0.61a 14.21 ± 0.78a 2080.02 ± 16.81b
A70 50.57 ± 1.70a 4.11 ± 0.13a 16.12 ± 0.76a 1869.25 ± 10.21b

soil, as well as enhance anaerobic denitrification, thereby leading to soil
nitrogen loss. The ILL at 70% of the FC could also significantly improve
the metabolism of the soil organic matter, but might reduce the meta-
bolism of soil phosphorous. The possible reason is that when the ILL is
relatively low, the frequently alternating wet and dry conditions are
beneficial to soil respiration and promote the growth of bacteria related
to nutrient metabolism, thereby accelerating the transformation of soil
nutrients. When the ILL is relatively high, the frequency of alternate
wetting and drying is lowered, and soil respiration is depressed, thereby
inhibiting the growth of some soil nutrient-metabolizing bacteria.
Additionally, Candidate_division_TM7, Firmicutes and Deinococcus-
Themus also showed a higher relative abundance in the soil bacterial
communities under ADI compared with SDI. Candidate_division_TM7
can degrade toluene, among other organic substances (Luo et al., 2009),
Firmicutes can reduce the incidence of crop blight (Mowlick et al.,
2014), and Deinococcus-Themus prefer a warm soil environment
(Griffiths and Gupta, 2007). Therefore, ADI can alter the bacterial
community composition and reduce the incidence of plant diseases by
improving the soil environment of the root zone.
Moreover, our results show that the effects of SDI and ADI were
more significant for trace bacteria with a relative abundance less than
1% of the soil bacterial community. Elusimicrobia, Armatimonadetes
and Nitrospirae were the dominant bacteria under SDI. Synergistetes
were the dominant bacteria under ADI with an ILL at 50% FC.
Verrucomicrobia, Chlorobi, Thermotogae and Fibrobacteres were the
dominant bacteria under ADI with an ILL at 60% FC. Cyanobacteria,
Thermotogae, Fibrobacteres and Chlorobi were the dominant bacteria
under ADI with an ILL at 70% FC. With respect to the metabolic
function, Elusimicrobia and Armatimonadetes can break up sugars
(Herlemann et al., 2009; Lee et al., 2014); Nitrospirae oxidize nitrites to
nitrates; Synergistetes are able to catabolize proteins (Bhandari and
Gupta, 2012; Militon et al., 2015); some species of Verrucomicrobia
oxidize methane (Op den Camp et al., 2009); Chlorobi perform an-
oxygenic photosynthesis using sulfides (Imhoff, 2003); Cyanobacteria
are capable of photosynthesis to release oxygen (Kumar et al., 2011);
Thermotogae preferentially inhabit warm soil environments and cata-
bolize carbohydrates, including sugars (Bhandari and Gupta, 2014);
and Fibrobacteres can break down and metabolize cellulose (Ransom-
Jones et al., 2012). As seen, different treatments altered the composi-
tion of the soil nutrient-metabolizing bacteria. The ILL at 50% of the FC
could significantly improve the degradation of proteins in the root-zone
soil. The ILLs at 60% and 70% of the FC were conducive to sulfur
metabolism in the root-zone soil. The ILL at 70% of the FC markedly
promoted the growth and reproduction of cyanobacteria in the root-
zone soil, which was beneficial to increase oxygen content in the root-
zone soil and provide organic substances for root growth and other

257
J. Wang et al.
microbial growth; it also enhanced the ability of the soil to break down
recalcitrant sugars.
To further clarify the effect of ADI on bacteria related to soil nu-
trient metabolism, our study deeply analyzed bacteria at the genus level
(Fig. 7), and the results showed that the relative abundance of soil
organic metabolism bacteria was significantly lower in ADI than in SDI;
however, the relative abundances of nitrogen-fixing bacteria and de-
nitrifying bacteria were significantly higher in ADI than in SDI. Ni-
trogen-fixing bacteria increase the N content of the soil (Taylor et al.,
2010); however, denitrifying bacteria should increase the loss of N from
the soil (Ma et al., 2015). Therefore, ADI should enhance nitrogen
metabolism in the root-zone soil. Additionally, different ILLs in ADI
could regulate root-zone soil metabolism. When the ILLs were set at
70% of the FC, the relative abundance of soil organic metabolism
bacteria was significantly higher than that of the ILLs at 50% and 60%
of the FC, but the relative abundance of nitrosation bacteria was sig-
nificantly lower than that of the other three treatments. Therefore, ni-
trite accumulation might be reduced (Ma et al., 2015), and soil organic
metabolism could be maintained at a relatively higher level in the root
soil at ILLs of 70% of the FC than under the other treatments.
Some studies have found that different ILLs in ADI could create
distribution inhomogeneity of root-zone soil environmental factors,
such as temperature, pH, and soil porosity (Raine et al., 2007; Sasal
et al., 2006; Shao et al., 2008) and could directly affect root growth
(North and Nobel, 1991). Differences in root-zone soil environmental
factors can change the bacterial community composition and structure
in the root-zone soil. The results of the PCA show that PC1, PC2, and
PC3 contributed 56.33%, 31.07%, and 12.6% to the difference in the
soil bacterial communities, respectively. The results of RDA show that
the environmental factors, including tomato root activity, root length,
and soil CO2 flux, posed significant effects on the variance in bacterial
communities. Additionally, we measured the soil porosity (the% air-
filled pore space), root activity, root length, and soil CO2 flux in the 0 to
30-cm layer of the root-zone soil of tomato in the different treatments
(Table 3). Soil porosity and tomato root length were significantly dif-
ferent between treatments. Specifically, soil porosity was significantly
higher with the ILL at 60% and 70% of the FC compared with 50% of
the FC. The tomato root length under the ADI treatments was sig-
nificantly greater than that under SDI; the ILL at 50% of the FC
markedly increased tomato root length compared with the treatments
at 60% and 70% of the FC. A previous study has indicated that a re-
latively high ILL can inhibit root growth, whereas a low ILL has the
opposite effect on root growth; this occurs because a water deficit
promotes root growth and increases root depth (Yan et al., 2009).
Different root growth will form various microenvironments of the root
zone, thereby affecting the growth of various bacteria in the bacterial
communities, especially trace bacteria that are strongly influenced by
the microenvironment.
Environmental changes in the root-zone soil will inevitably affect
crop growth and development. In the present study, we also found that
SDI and ADI resulted in significant differences in single fruit weight,
number of fruit per plant, and fruit yield per plant of tomato. Fruit
number per plant was significantly higher under ADI with the ILLs at
50% and 60% of the FC compared with SDI; however, single fruit
weight was significantly lower under ADI with the ILL at 50% of the FC
compared with SDI. It is possible that compared with SDI, ADI with the
ILL at 50% of the FC can markedly improve the bacterial community
structure in root-zone soil and contribute to soil nutrient uptake and
use; however, this ILL is 20% lower than used in SDI, and water
shortage may result in a lower single fruit weight of the tomato. The
single fruit weight was slightly lower, whereas the fruit yield per plant
was slightly higher, under ADI with the ILL at 60% of the FC, compared
with SDI; however, this ILL is 10% lower than that used in SDI. When
ADI was performed with the ILL 10% higher than the ILL used in SDI,
namely, at 70% of the FC, both the fruit numbers per strain and the fruit
yield per tomato plant were significantly higher than those under SDI,
258
Applied Soil Ecology 119 (2017) 250–259
whereas in the soil bacterial structure, various bacteria related to soil
nutrient cycling also showed significantly higher relative abundances
than under SDI. Therefore, we inferred that ADI significantly promoted
tomato growth by altering the bacterial community composition in the
root-zone soil, which was constrained by the ILL. ADI with the ILL at
60% of the FC could achieve the same tomato yield as SDI with the ILL
at 70% of the FC.
In addition, under the ILLs at 70% of the FC, the root length value
was lower and the root area was not significantly different from that of
the other 3 treatments, but the root area value was significantly higher.
This finding would be more conducive for root systems to absorb nu-
trients and distribute more material to the fruits to increase production.
5. Conclusions
The bacterial abundance was higher in the root-zone soil of the
tomato under ADI than that under SDI, whereas the bacterial commu-
nity structure was markedly different from that under SDI. Different
ILLs significantly affected the various bacteria under ADI. The ILL at
70% of the FC was more conducive to soil organic metabolism bacteria
than the ILLs at 50% and 60% of the FC but exhibited a significantly
lower relative abundance of nitrosation bacteria. Different ILLs in ADI
also showed significant effects on tomato growth. The ILL at 70% of the
FC not only exhibited greater root areas and root forks but also ex-
hibited higher numbers of fruits per plant and fruit yields per plant.
Acknowledgments
This study is supported jointly by the Chinese 863 Plan
(2011AA100507), theNational 111 Project in China (No. B12007). the
National Key Research Project of China “13th Five Year Plan
”（2016YFC0400202）and Natural Science Foundation of China (No.
51679205)
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