The effects of different disease-resistant cultivars of banana on rhizosphere microbial communities...

R E S EA RCH L E T T E R

The effects of different disease-resistant cultivars of banana onrhizosphere microbial communities and enzyme activities

Jianbo Sun, Ming Peng, Yuguang Wang, Wenbin Li & Qiyu Xia

Key Laboratory of Biology and Genetic Resources of Tropical Crops, Ministry of Agriculture, Institute of Tropical Bioscience and Biotechnology,

Chinese Academy of Tropical Agricultural Sciences, Long hua District, Hai kou, Hai nan Province, China

Correspondence: Ming Peng, Key

Laboratory of Biology and Genetic Resources

of Torpical Crops, Ministry of Agriculture,

Institute of Tropical Bioscience and

Biotechnology, Chinese Academy of Tropical

Agricultural Sciences, No. 4, Xue yuan Road,

Long hua District, Hai kou, Post code

571101, Hai nan Province, China.

Tel.: +86 0898 66890981; fax: +86 0898

66988081; e-mail: [email protected]

Received 23 May 2013; accepted 3 June

2013. Final version published online 8 July

2013.

DOI: 10.1111/1574-6968.12192

Editor: Yaacov Okon

Keywords

banana; rhizosphere; bacterial community;

T-RFLP; real-time PCR; enzyme activity.

Abstract

To understand the mechanism of soil microbial ecosystem and biochemical

properties in suppressing soilborne plant diseases, the relationship between the

soil rhizosphere microbial communities, hydrolase activities, and different dis-

ease-resistant cultivars was investigated. There were statistically significant dif-

ferences in microbial diversity in the rhizosphere soil between the disease-

tolerant cultivar Fj01 and susceptible cultivar Baxi. The rhizosphere soil of Fj01

showed a trend of higher microbial diversity than that of Baxi. At the same

growth stage, the similar trends of variation in microbial community diversity

between the two different cultivars were observed. The bacterial community

abundance in rhizosphere soil from the two banana cultivars was quantified by

real-time PCR assays. The size of the rhizosphere bacterial population from the

Fj01 was significantly larger than that from the Baxi during the growing stage

from July to September. The activities of urease and phosphatase were analyzed

to study the effects of the two banana cultivars to soil ecosystem functioning.

Urease activity was significantly higher in the rhizosphere soil of Fj01 than that

of Baxi in the period from July to September. However, phosphatase activity

showed no significant difference between the two different rhizosphere soils.

Introduction

Fusarium wilt of banana is a serious and destructive dis-

ease worldwide. It is a vascular wilt disease caused by the

soilborne fungus Fusarium oxysporum f.sp. cubense (Peng

et al., 1999). There are no effective chemical control mea-

sures currently, and the resistance breeding is tedious. It

is therefore necessary to find effective and integrated sus-

tainable methods to control Fusarium wilt of banana. Soil

microbial ecosystem and biochemical properties are seen

to be critical to the maintenance of soil health and quality

(Naeem et al., 1994; Garbeva et al., 2004), and good soil

quality may be helpful to improve the capacity of the dis-

ease suppressiveness (Abawi & Widmer, 2000; Peters

et al., 2003). However, little is known about the relation-

ship between the rhizosphere soil microbial ecosystem,

biochemical properties of different disease-resistant culti-

vars, and the suppressing of Fusarium wilt of banana.

The rhizosphere is a special micro-ecosystem, which

includes plant, soil, and microorganism; meanwhile, it is

the gateway through which soilborne pathogens enter the

crop. Plant species and genotype are significant factors

determining the structure and composition of microbial

communities in the rhizosphere (Smalla et al., 2001;

Garbeva et al., 2004; Mazzola, 2004).

Several studies have shown a correlation between the

microbial communities in the rhizosphere and the disease

caused by soilborne pathogens (Workneh & van Bruggen,

1994; Mazzola & Gu, 2002). One possible strategy is the

management of the diversity and the structure of rhizo-

sphere microbial communities and, as a result, enhances

the antagonism to pathogens activity, leading to a

decrease in plant disease caused by soilborne pathogens.

Various approaches have been developed to analyze

microbial ecosystems in soil microbial communities.

Traditional culture-based methods are based on isola-

FEMS Microbiol Lett 345 (2013) 121–126 ª 2013 Federation of European Microbiological SocietiesPublished by John Wiley & Sons Ltd. All rights reserved

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tion–cultivation approaches. However, only a small

fraction of the microbial cells in soil are cultivable. Alter-

native approaches based molecular fingerprinting meth-

ods provide a complex view of the microbial community

without the need for isolation and cultivation. Terminal

restriction fragment length polymorphism (T-RFLP) anal-

ysis is one of the most rapid and powerful methods for

comparing microbial communities. It has been shown to

be an ideal technique for the rapid analysis of microbial

diversity (Bankhead et al., 2004; Ausec et al., 2009). Ter-

minal restriction fragments of T-RFLP analysis are

detected by fluorescence, and the result of scanning can

be compared with the data stored in databases. In this

research, the microbial diversity was determined by

T-RFLP profiles of the 16S rRNA gene obtained from dif-

ferent soil samples.

Real-time PCR has been used for the detection and

quantification of bacteria in various environments (Becker

et al., 2000). In this study, real-time PCR is used for the

quantification of soil bacterial community.

Soil enzyme activities have been considered as indicators

of soil quality (Bastida et al., 2008). Soil microbial commu-

nities are the primary source of soil enzymes. Here, we ana-

lyzed the enzyme activities of urease and phosphatase to

access functional changes in the rhizosphere microbial

community between two cultivars of banana.

The objective of this research was to compare the

bacterial community structure and hydrolase activities in

the rhizosphere of banana between two different disease-

resistant cultivars against Fusarium wilt disease at differ-

ent growth stages.

Materials and methods

Soil sampling

The samples were collected from the experimental field in

Chinese Academy of Tropical Agricultural Sciences,

Hainan Province, China. The soil type is tropical red loam.

The experiments were carried out during the 2010

growing season. Two cultivars of ‘Baxi’ and ‘Fj01’ were

grown in a randomized plot design with three replications

per cultivar, each containing four plants. The ‘Baxi’ and

‘Fj01’ were susceptible and disease-tolerant cultivars,

respectively.

The plantlets of banana were transplanted into the field

in February. After this, soil samples from the rhizosphere

of banana were collected every month until September.

Samples collected from the cultivars of Baxi and Fj01 at

different month were named B1–B7 and F1–F7 in time

order, respectively.

Soil cores were taken at c. 20 cm from the tree and at

30 cm depth. Each sample was collected at five cores per

tree and three plants per plot. Pieces of root from the

composite sample were picked out, and their tightly

adherent soil was collected. The rhizosphere soil was

homogenized and sieved to remove possible root frag-

ments. Soil samples were stored at �20 °C for subsequent

molecular analyses.

Soil DNA extraction and PCR amplification of

16S rRNA genes

Total DNA was extracted from 500 mg of soil sample

using the Fast DNA SPIN kit for soil (Qbiogene). The

purity and concentration of the DNA were determined

using a spectrophotometer (Jasco, Tokyo, Japan).

For the T-RFLP analysis, the 16S rRNA gene was ampli-

fied with the primers 27F (5′-AGAGTTTGATCCTGGCT-CAG-3′) and 1492R (5′-GGTTACCTTGTTACGACTT-3′;Culman et al., 2006). The 5′ end of the 27F primer was

labeled with 6-carboxyfluorescein (6-FAM) for fluorescent

detection.

The PCR mixtures contained 0.1 lM of each primer,

30 ng of template DNA, 19 PCR buffer, 2.0 mM MgCl2,

200 lM dNTP mix, and 2.5 U of Taq DNA polymerase

(Sangon Biotech, China).

DNA amplification was performed in a thermocycler

(Biometra, Germany) under the following conditions:

initial denaturation at 95 °C for 5 min followed by 30

cycles of denaturation at 94 °C for 1 min, annealing at

52 °C for 1 min, and extension at 72 °C for 1.5 min,

with a final extension at 72 °C for 7 min. Three indepen-

dent PCRs were performed, combined for each, and puri-

fied using a Qiagen gel extraction kit (Qiagen, Germany).

Approximately 200 ng of fluorescently labeled PCR

products was digested with the restriction enzyme HaeIII

at 37 °C for 3 h. The reaction mixtures contained 8 lL of

PCR product, 2.0 lL of 109 restriction enzyme buffer,

3 U of HaeIII, and ultrapure water to a final volume of

20 lL. Digestion products were verified on a 1.5% agarose

gel in 1% TBE buffer. The digested DNA was purified

using a gel extraction kit (Omega). The Three replicates of

the digestion product from each sample were mixed.

T-RFLP analysis

Terminal restriction fragments (T-RFs) were separated on

an ABI 373 sequencer (Applied Biosystems). The peak

results were analyzed using GENEMAPPER software 4.0

(Applied Biosystem). In each sample, only peaks over a

threshold of 100 fluorescence units were considered for

further analysis. The relative abundance of each T-RF was

calculated as a relative percentage by calculating the ratio

of a given peak area to the total peak area within one

sample. T-RFs with relative abundance below 2% were

ª 2013 Federation of European Microbiological Societies FEMS Microbiol Lett 345 (2013) 121–126Published by John Wiley & Sons Ltd. All rights reserved

122 J.B. Sun et al.

regarded as background noise and excluded from analysis.

T-RFs smaller than 50 bp or larger than 600 bp were

excluded from the analysis.

Quantification of bacteria by real-time PCR

Soil samples from the rhizosphere were collected every

2 months from March to September. Total soil DNA was

extracted in the same way as described in Quantification

of bacteria by real-time PCR and using 1 lL of 50-fold

diluted extracted DNA (1–7 ng) as template.

Abundances of bacteria were determined by quantita-

tive real-time PCR analysis of 16S rRNA gene. Each reac-

tion was performed in a 25-lL volume containing

12.5 lL of SYBR� Green PCR Master Mix, 1 lL sample

DNA, and 20 lmol of each primer. The primers used for

the amplification were as follows: 338F: 5′-CCT ACG

GGA GGC AGC AG-3′ and 518R: 5′-ATT ACC GCG

GCT GCT GG-3′ (Seghers et al., 2003).Real-time PCR was performed on a MX3000P real-time

PCR machine (Stratagene, Cedar Creek, TX). Quantitative

PCR were performed under the following conditions:

95 °C for 3 min and 40 cycles of 95 °C for 30 s, 53 °Cfor 40 s, and 72 °C for 1 min. Three independent quanti-

tative PCRs were performed for each soil sample.

The bacterial 16S rRNA gene standard was amplified

with the primers 27F: 5′-AGA GTT TGA TCC TGG CTC

AG-3′ and 1492R: 5′-GGT TAC CTT GTT ACG ACT T-3′(Ahn et al., 2009). The amplified product was then cloned

into the pGEM-T Easy Vector (Promega). Standard curves

were generated with serial dilution series of quantified

plasmid DNA.

Soil enzyme activities in rhizosphere soil

Soil samples from the rhizosphere were collected as the

methods described in Quantification of bacteria by real-

time PCR. Phosphatase activity was determined using p-ni-

trophenyl phosphate disodium (0.115 M) as substrate, and

the released p-nitrophenol (PNP) by phosphatase was mea-

sured spectrophotometrically at 410 nm (Ros et al., 2006).

Urease activity was determined using phenol–sodiumhypochlorite colorimetry (Wang et al., 2009). The released

NHþ4 was measured at a wavelength of 578 nm.

Data analysis

To evaluate the diversity indices of each community, each

different OTU was treated as a different species, and the

peak area for individual T-RFs was normalized to percent

of the total fingerprint area as a relative abundance.

The Shannon–Wiener and Shannon evenness index

were used to evaluate the richness and evenness of each

sample. The Shannon–Wiener index was calculated from

(H′) = �∑pi ln pi, where pi is the proportion of the peak

area for each T-RF out of the total peak area for all

T-RFs. The evenness index was calculated from (E′) = H/

Hmax, where S is the number of T-RFs within a given

profile, Hmax = ln S.

ANOVA was used to analyze the statistical significance of

the data, and multiple comparisons of significant differ-

ences were calculated using Tukey’s t-test at the 5% level

with SPSS 11.5 (SPSS for Windows, version 11.5).

Results

T-RFLP profiles

Bacterial community profiles of the rhizosphere microbial

communities in two different cultivars were analyzed

using the T-RFLP fingerprints of the 16S rRNA genes.

T-RFs with a relative abundance of more than 2% were

considered. For this analysis, a similar trend in diversity

between samples from the disease-tolerant (Fj01) and sus-

ceptible cultivars (Baxi) was observed. Two months after

transplantation, both of the diversities in the rhizosphere

of the two different cultivars were all increased. After this,

the diversities decreased for both cultivars up to

5 months after transplantation and then increased slowly

(Fig. 1). During the tested growing stage, the diversity of

samples in Fj01 was significantly (P < 0.05) higher than

that in the cultivar of Baxi (Table 1).

In the period from March to June, differences in diver-

sities of the T-RF profiles in the two cultivars were also

compared. Some T-RFs were present only at one specific

cultivar. For example, the T-RFs of 73, 208, and 291 bp

were present only in the samples of Fj01. In contrast, the

T-RFs of 196 and 307 bp were only observed in the sam-

ples of Baxi.

Five months after transplantation, the lowest diversities

of samples in two different cultivars were all observed.

During this period, seven of the T-RF profiles were

common to all the samples of Fj01 (64, 73, 193, 208, 231,

Fig. 1. Comparison of the soil diversity in rhizosphere of Baxi and

Fj01. The numbers 1–7 in x-axis indicate the different soil samples

from the rhizosphere collected every month.


Effect of banana cultivar on rhizosphere soil 123

258, and 291 bp). However, only three T-RFs (72, 196,

and 232 bp) were present in all the samples of Baxi.

In addition, the first five T-RFs and their relative

abundance of each sample were analyzed according to the

T-RF profile (Table 2). In the samples collected from the

Fj01, the T-RFs of 73, 291, 193, 233, 64, 231, and 217 bp

were detected as the dominant components with the

relative abundance of 12.7%, 14.1%, 12.4%, 11.7%,

11.6%, 16.3%, and 14.6% in the different months, respec-

tively. In contrast, samples collected from the susceptible

cultivar in the different months were dominated by 231,

231, 231, 230, 72, 206, and 217 bp and with the relative

abundance of 14.0%, 10.9%, 14.3%, 21.8%, 15.0%,

16.1%, and 25.3%, respectively.

Abundance of bacteria in rhizosphere soil

Rhizosphere soil bacterial community abundance was

detected by real-time PCR assays. The sizes were expressed

as 16S rRNA gene copy numbers. Rhizosphere soil bacte-

rial abundance of Fj01 was higher during the tested grow-

ing stage than that of Baxi. Especially in the period from

July to September, The size of the rhizosphere bacterial

population from the cultivar Fj01 was significantly larger

than that from the cultivar Baxi (Fig. 2).

Soil enzyme activities

The activities of enzymes in the rhizosphere soil are shown

in Table 3. From May to September, the activity of urease

in the rhizosphere soil of Fj01 was higher than that of Baxi;

furthermore, there were significant differences between

Table 1. Diversity indices of the bacterial communities in the

rhizosphere soil based on the data from T-RFLP analysis

Samples Shannon index Evenness

Soil samples from the cultivar

of BaxiaB1 2.63 0.97

B2 2.67 0.99

B3 2.50 0.98

B4 2.47 0.94

B5 2.28 0.99

B6 2.32 0.93

B7 2.35 0.91

Soil samples from the

cultivar of Fj01bF1 2.58 0.98

F2 2.75 0.97

F3 2.64 0.97

F4 2.55 0.97

F5 2.35 0.95

F6 2.49 0.97

F7 2.52 0.98

Different superscript lowercase letters indicate significant (P < 0.05)

differences (univariate analysis of variance). B1–B7 and F1–F7: samples

collected from the cultivars of Baxi and Fj01 at different month,

respectively.

Table 2. Distribution and relative abundance of the first five dominant T-RFs after restriction with HaeIII

Samples T-RF size (bp) [relative abundance (%)]

B1 231 (14.0) 196 (10.7) 307 (8.9) 328 (8.9) 216 (7.8)

B2 231 (10.9) 196 (8.4) 329 (8.2) 216 (8.1) 291(8.1)

B3 231 (14.3) 196 (11.7) 307 (9.8) 232 (8.9) 291 (8.8)

B4 230 (21.8) 330 (12.4) 216 (8.8) 196 (8.3) 307 (7.2)

B5 72 (15.0) 188 (12.4) 66 (11.7) 90 (10.3) 231 (10.3)

B6 206 (16.1) 201 (14.3) 205 (14.0) 233 (13.5) 193 (7.9)

B7 217 (25.3) 231 (8.9) 216 (8.5) 291 (7.6) 307 (7.5)

F1 73 (12.7) 208 (10.8) 296 (10.0) 231 (8.9) 167 (8.0)

F2 291 (14.1) 231 (9.9) 216 (7.5) 64 (7.3) 234 (6.9)

F3 193 (12.4) 73 (11.7) 217 (8.7) 208 (8.0) 168 (7.6) 296 (7.6)

F4 233 (11.7) 193 (10.5) 216 (10.5) 73 (9.8) 208 (9.3)

F5 64 (11.6) 182 (10.5) 146 (10.2) 219 (9.7) 138 (9.6)

F6 231 (16.3) 197 (12.6) 72 (8.4) 74 (8.1) 193 (7.9)

F7 217 (14.6) 90 (10.1) 221 (9.8) 174 (8.5) 170 (8.0)

The relative abundance is the ratio of a given peak area to the sum of all the peak areas in one sample. B1–B7 and F1–F7: samples collected

from the cultivars of Baxi and Fj01 at different month, respectively.

Fig. 2. Quantification of 16S rRNA gene copy numbers in samples

from cultivars Fj01 and Baxi at different growth stages. Different

letters in the same column indicate significant differences at P < 0.05

(Tukey’s test).


124 J.B. Sun et al.

Fj01 and Baxi during the growing stage from July to Sep-

tember. However, there were no statistically significant dif-

ferences in the activities of phosphatase in rhizosphere soil

between Fj01 and Baxi (Table 3).

Discussion

Rhizosphere is a special micro-ecosystem of plant–microorganism interactions. Rhizosphere bacterial com-

munities play an important role in suppressing soilborne

plant diseases and promoting plant growth.

Plant roots release a broad range of compounds into

the surrounding soil. The composition of root exudates is

affected by the plant species and developmental stage (Di

Cello et al., 1997; Siciliano et al., 1998; Yang & Crowle,

2000; Dunfield & Germida, 2001). These root exudates

create unique environments for the microorganisms living

in the rhizosphere. There are differences in utilization of

different compositions of root exudates by the microor-

ganisms, and thus, different rhizosphere communities

were formed (Rumberger et al., 2004; Orlando et al.,

2007).

In this study, significant differences in rhizosphere bac-

terial community structure and diversity of banana in

relation to different disease-resistant cultivars were

observed. One possible explanation for the result might be

due to the difference in root exudates released by the dif-

ferent cultivars. These compounds provided potential car-

bon source to promote microbial growth, thus leading to

different composition and diversity in their rhizosphere.

Seasonal shifts in microbial diversity in the rhizosphere

have also been observed in some studies. Rumberger et al.

(2007) revealed that in the rhizosphere of apple trees, the

composition of bacterial communities was highly variable

in different seasons. In this study, the impact of different

growth stage on bacterial diversity in the rhizosphere was

also observed. With the development of growth stage, the

diversities of the two cultivars in rhizosphere were

decreased.

Several studies have also indicated the relationship

between the plant diseases and the diversity of soil micro-

bial communities. For example, P�erez-Piqueres et al.

(2006) showed that differences in soil suppressiveness to

Rhizoctonia solani disease were related to differences in

microbial composition. Using the T-RFLP fingerprints,

Rotenberg et al. (2007) revealed that the incorporating of

paper mill residuals into soil may improve the bacterial

communities in soil and thus increase the soil’s ability to

suppress root rot disease. In this study, the disease-

tolerant cultivar (Fj01) showed a higher bacterial diversity

in the rhizosphere than that of the susceptible cultivar

(Baxi) during the tested growing stage in general. The

results indicated the relationship between bacterial diver-

sity and the suppressiveness to soilborne diseases in rhi-

zosphere of banana.

Urease and phosphatase play important roles in soil

organic nutrient cycling and are important indicators of

soil quality (Dick et al., 2000). Soil enzyme activities are

greatly affected by root secretion and soil microorganisms

(Ros et al., 2006). In the present study, the difference of

soil urease activity between the two banana cultivars

could be attributed to the changes in soil microbial group

composition and root secretion. The higher activity of

urease increased the ability of organic nutrient cycling in

soil and thus provided a better nutrition environment for

banana growth.

The mechanisms of plant diseases caused by soilborne

pathogens are multiple and complex. A higher biodiver-

sity and good biochemical property have been associated

with better soil quality and thus a greater capacity in

suppressing soilborne diseases. In this study, the disease-

tolerant cultivar (Fj01) showed a significant higher micro-

bial diversity and urease activity compared with the

susceptible cultivar (Baxi). This may be one of the impor-

tant reasons why the fungus is more difficult to infect the

disease-tolerant cultivar compared with the susceptible

cultivar of banana.

Acknowledgement

This work was financially supported by the grant no.

200903049-2 and ITBB110305.

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Table 3. Enzyme activities in rhizosphere soil from Fj01 and Baxi at different growth stages

Cultivar March May July September

Urease activity (NH4–N mg g�1 soil 24 h�1) Fj01 2.13 � 0.049a 2.26 � 0.012a 2.35 � 0.015a 2.31 � 0.009a

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The effects of different disease-resistant cultivars of banana on rhizosphere microbial communities...

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