Plant Soil
https://doi.org/10.1007/s11104-024-06709-4
RESEARCH ARTICLE
The interaction between Fusarium oxysporum f. sp. cubense
tropical race 4 and soil properties in banana plantations
in Southwest China
Wenlong Zhang · Tingting Bai · Arslan Jamil · Huacai Fan · Xundong Li ·
Si‑Jun Zheng · Shengtao Xu
Received: 4 March 2024 / Accepted: 28 April 2024
© The Author(s), under exclusive licence to Springer Nature Switzerland AG 2024
Abstract
Aims Banana Fusarium wilt (Fusarium oxysporum
f. sp. cubense tropical race 4) is a typical destruc-
tive soil-borne disease, which was the main limiting
factor for the sustainable development of the banana
industry worldwide. In banana production, soil physi-
ochemical properties and soil microbiome were effec-
tively affected the occurrence and spread of Fusar-
ium wilt. However, there is still a lack of systematic
research, particularly in exploring the correlation
Responsible Editor: Luz E. Bashan.
Wenlong Zhang and Tingting Bai contributed equally to
this work.
Supplementary Information The online version
contains supplementary material available at https://​doi.​
org/​10.​1007/​s11104-​024-​06709-4.
W. Zhang · T. Bai · A. Jamil · H. Fan · X. Li ·
S.-J. Zheng (*) · S. Xu (*)
Yunnan Key Laboratory of Green Prevention and Control
of Agricultural Transboundary Pests, Agricultural
Environment and Resources Institute, Yunnan Academy
of Agricultural Sciences, Kunming, Yunnan 650205,
China
e-mail: sijunzheng63@163.com
S. Xu
e-mail: xushengtao.14@hotmail.com
S.-J. Zheng
Bioversity International, Kunming, Yunnan 650205, China
between the occurrence of banana Fusarium wilt and
soil properties across various climates and soil types.
Methods In this study we investigated the soil phys-
icochemical properties, bacterial and fungal commu-
nity composition, and pathogenic fungal abundance
in 140 banana plantations which were affected by
banana Fusarium wilt in Yunnan Province, China.
Results The results showed that the abundance of
soil-borne pathogenic fungi was positively correlated
with total phosphorus, total nitrogen, organic matter,
urease activity, annual precipitation, and the alpha
diversity of bacterial and fungal communities. In
contrast, it showed a significant negative correlation
with the annual mean temperature. As the abundance
of pathogen increased, numerous potential disease-
suppressive bacterial genera (such as Rhodanobacter,
Gemmatimonas, Novosphingobium) and soil-borne
pathogenic fungal genera (such as Plectosphaerella,
Nigrospora, Cyphellophora) also increased, and the
co-occurrence network showed a higher modulariza-
tion index.
Conclusions The results enhance the understand-
ing of the patterns of soil-borne pathogenic fungal
population dynamics in banana plantations, which
would provide evidence and guidance for reducing
pathogenic fungal abundance and selecting beneficial
microorganisms in banana production. Furthermore,
this would provide a theoretical basis for sustainable
prevention and control of banana wilt disease.
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Keywords Banana Fusarium wilt · Physiochemical
properties · Soil microbial communities · Pathogenic
fungal abundance
Introduction
The relentless onslaught of soil-borne fungal patho-
gens in modern agriculture poses a staggering threat,
causing an estimated 15% annual yield reduction
across crops (Newbery et al. 2016). Concurrently,
modern and intensive farming practices are promot-
ing the proliferation of plant pathogens, particularly
aggressive soil borne fungi (Hartmann and Six 2023).
Current chemical fungicides used to combat these
pathogens have shown limited efficacy and pose sig-
nificant environmental risks (Delgado-Baquerizo
et al. 2020). In addition to traditional epidemiologi-
cal management measures, alternative soil manage-
ment practices are increasingly becoming a focus of
research, such as soil fertility regulation and biologi-
cal control (Katan 2017).
The growth and development of soil-borne patho-
gens are inevitably influenced by the entire soil eco-
system (Bakker et al. 2020). Soil fertility is one of the
key driving factors in the occurrence and develop-
ment of soil-borne diseases (Panth et al. 2020). Addi-
tionally, soil characteristics have a significant impact
in influencing the structure and activity of microbial
communities in the soil, modulating plant defense
mechanisms and thus regulating pathogen popula-
tions (Xiong et al. 2017). The coordinated evolution
of plants and their root microbiota assists plants in
better adapting to their environment, such as nutri-
ent cycling, growth stimulation, and resilience to both
environmental stresses and biological threats (Trivedi
et al. 2020). The microbiome can protect plants from
pathogen invasion through various mechanisms, such
as producing inhibitory substances or occupying eco-
logical niches that directly suppress the growth of
pathogen, and/or inducing plant immune responses
to enhance the plant’s resistance to pathogenic micro-
organisms (Li et al. 2021a, b). Conversely, pathogens
can also exploit soil microorganisms to enhance their
virulence (Snelders et al. 2020). Therefore, this recip-
rocal interaction between soil-borne pathogens and
the plant microbiome is of paramount importance in
understanding the dynamics of soil-borne diseases.
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Plant Soil
Banana (Musa spp.) as the world’s top traded fruit and
the fourth-largest staple crop hold extensive economic
and nutritional values (Evans et al. 2020). However,
Fusarium wilt of Banana (FWB) caused by Fusarium
oxysporum f. sp. cubense (Foc) infection poses a signifi-
cant threat to the sustainable development of the banana
industry (Pegg et al. 2019). Commercial banana varieties
are unable to withstand the infect of Fusarium oxyspo-
rum f. sp. cubense tropical race 4 (Foc TR4), which has
now reached -producing regions globally (Zuo et al.
2018). Due to the limited banana genetic diversity within
the banana crop, breeding disease-resistant cultivars are
a formidable challenge. In addition to optimizing field
management practices, the use of biological control to
regulate soil microbial communities for reducing the
incidence of wilt disease is emerging as a future develop-
ment trend (Siamak and Zheng 2018).
Improving soil properties had been proven to effec-
tively enhance disease control (Ghorbani et al. 2008).
Despite previous research uncovering an association
between the occurrence of FWB and the soil micro-
biome (Fu et al. 2017; Hong et al. 2020; Kaushal et al.
2020), the specific interactions between soil properties,
Foc TR4, and soil microbiome at different pathogen lev-
els remain elusive. To address this gap in knowledge, we
conducted a comprehensive study involving the collec-
tion of soil samples from 140 banana plantations in Yun-
nan province affected by FWB. Our investigation delves
into assessing the physicochemical properties, enzyme
activity, bacterial and fungal community composition,
and the abundance of Foc TR4. The hypothesis of this
study was that soil Foc TR4 abundance was highly cor-
related with the soil properties, particularly with the soil
community composition. The study aims to unravel the
key drivers of Foc TR4 abundance in banana plantation
soils, explore the impact of pathogen abundance on the
soil microbial community, and identify microbial taxa
associated with the pathogen. Through these efforts, we
aim to contribute valuable insights into managing patho-
genic fungal abundance and promoting beneficial micro-
organisms in banana production.
Materials and methods
Sampling points and soil sampling
Through preliminary on-site inspections in Yun-
nan Province, the following sampling areas were
Plant Soil
identified. The 21 counties and cities were selected
as representatives of different climate and soil types
(Fig. S1). For each county or city, 8–10 sampling
points were established within typical banana orchards
exhibiting symptoms of Fusarium wilt. Soil samples
were collected from the rhizosphere. We obtained cli-
mate data including annual average temperature of all
sampling points from the Worldclim database (https://​
www.​world​clim.​org). The basic information such as
geographical location and climate characteristics of
each sampling point was shown in Table S1.
Soil samples were collected from five parts around
one same plant at a depth of 0–20 cm, and the pro-
tocol was according to Lundberg et al. (2012). After
mixing, the soil samples were placed in sterile, self-
sealing bags and labeled. A portion of the samples
was subjected to -80 °C freeze-drying to remove
moisture, and then stored at -80 °C for subsequent
determination of soil microbial and pathogenic con-
tent. Another portion was air-dried naturally, and
reserved for the analysis of soil physicochemical indi-
cators and enzyme activity after sieving through a
75-mesh sieve.
Determination of soil nutrients and enzyme activity
Soil pH was determined using an acidity meter
(PHSJ-4 F, Shanghai INESA Scientific Instrument
Co., Ltd, Shanghai, China). The soil chemical meas-
urement analyses followed the standard procedures
according to Page et al. (1982) and Klute and Page
(1986). The total soluble salt content was measured
by the conductivity method. Organic matter content
was determined by the potassium dichromate titra-
tion method. Alkaline nitrogen content was deter-
mined using the sodium hydroxide-alkali diffusion
method. Available phosphorus content was meas-
ured by the sodium bicarbonate-molybdenum anti-
mony anti-absorption spectrophotometry method.
Available potassium content was determined by the
ammonium acetate-flame photometry method. Total
nitrogen in the soil were determined using a carbon-
nitrogen elemental analyzer (VARIO MAX C/N, Ger-
many) through dry combustion. Microbial carbon and
nitrogen content were determined using the chloro-
form fumigation extraction method with ­K2SO4. Soil
urease activity was determined by the indophenol
blue colorimetric method. Soil catalase activity was
determined by the potassium permanganate titration
method. Soil sucrase activity was determined using
the 3, 5-dinitrosalicylic acid colorimetric method.
Alkaline phosphatase activity was determined by the
disodium phenylphosphate colorimetric method.
DNA extraction and PCR amplification
Genomic DNA was extracted from soil samples
using the E.Z.N.A.® soil DNA Kit (Omega Bio-tek,
Norcross, GA, U.S.), following the manufacturer’s
protocols. The DNA quality and concentration were
assessed through 1.0% agarose gel electrophoresis
and a NanoDrop2000 spectrophotometer (Thermo
Scientific, United States) and stored at -80 °C until
further use. For bacterial 16 S rRNA gene amplifi-
cation of the V3-V4 hypervariable region, primer
pairs 338 F (5’-ACT​CCT​ACG​GGA​GGC​AGC​AG-3’)
and 806R (5’-GGA​CTA​CHVGGG​TWT​CTAAT-
3’) were employed. Additionally, the ITS1 region of
fungal ITS rRNA genes was targeted using the for-
ward primer ITS5F (5’- GGA​AGT​AAA​AGT​CGT​
AAC​AAGG-3’) and reverse primer ITS1R (5’- GCT​
GCG​TTC​TTC​ATC​GAT​GC-3’) with a T100 Ther-
mal Cycler PCR thermocycler (BIO-RAD, USA).
The PCR reaction mixture included 4 µL 5 × Fast Pfu
buffer, 2 µL 2.5 mM dNTPs, 0.8 µL each primer (5
µM), 0.4 µL Fast Pfu polymerase, 10 ng of template
DNA, and ddH2O to a final volume of 20 µL. PCR
cycling conditions consisted of initial denaturation at
95 °C for 3 min, followed by 27 cycles of denaturing
at 95 °C for 30 s, annealing at 55 °C for 30 s, and
extension at 72 °C for 45 s. A single extension step at
72 °C for 10 min concluded the process, followed by
cooling to 4 °C. The PCR product was purified from a
2% agarose gel using the PCR Clean-Up Kit (YuHua,
Shanghai, China) according to the manufacturer’s
instructions. Quantification was performed using
Qubit 4.0 (Thermo Fisher Scientific, USA).
Quantitative real‑time PCR analyses
Primers FocSc-1(5’-CAG​GGG​ATG​TAT​GAG​GAG​
GCT​AGG​CTA-3’) and FocSc-2(5’-GTG​ACA​GCG​
TCG​TCT​AGT​TCC​TTG​GAG-3’) were used to quan-
tify the abundances of Foc TR4 by quantitative real-
time PCR (qPCR). The qPCR amplification was per-
formed using Takara SYBR Premix Ex TaqTM (Tli
RNaseH Plus) kit (Code No. RR820). The establish-
ment of a standard curve utilized the recombinant
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plasmid pMD18-T-158, containing a 158 bp fragment.
The concentration of the extracted plasmid DNA was
determined and then converted into copy numbers
using the formula: Copy number = (6.02 × ­1023 cop-
ies ­mol−1 × plasmid concentration g µL−1) / MW g
­mol−1. Here, MW (average molecular weight of dou-
ble-stranded DNA) = base pairs × 660 / base pair. Six
concentration gradients ­(108, ­107, ­106, ­105, ­104, ­103
copy number µL−1) were prepared as standard sam-
ples for constructing the standard curve. The standard
curve required R² > 0.99 and 90 < Eff % < 110. The
pathogen content in the tested samples was calculated
based on instrument detection results, the mass of the
sample used for DNA extraction, the total amount of
extracted DNA, and the template amount used in the
qPCR reaction. The pathogen content was expressed
as copy number per gram of soil.
Illumina sequencing and data processing
The purified amplicons, pooled equimolarly, underwent
paired-end sequencing on an Illumina PE250 platform
(Illumina, San Diego, USA) by Majorbio Bio-Pharm
Technology Co. Ltd. (Shanghai, China), following
standard protocols. Raw sequencing reads were submit-
ted to the NCBI Sequence Read Archive (SRA) data-
base (16 S: PRJNA946914, ITS: SRPPRJNA947073).
Raw FASTQ files were demultiplexed using an in-
house Perl script, then quality-filtered with fastp version
0.19.6 (Chen et al. 2018), and merged using FLASH
version 1.2.7 (Magoč and Salzberg 2011) based on
the following criteria: (1) reads with an average qual-
ity score < 20 over a 50 bp sliding window were trun-
cated, and reads shorter than 50 bp were discarded;
reads with ambiguous characters were also removed;
(2) only overlapping sequences longer than 10 bp were
assembled with a maximum mismatch ratio of 0.2 in
the overlap region; unassembled reads were discarded;
(3) samples were differentiated by barcode and prim-
ers, and sequence direction was adjusted with exact
barcode matching and a 2-nucleotide mismatch allow-
ance in primer matching. The optimized sequences
were clustered into operational taxonomic units (OTUs)
at a 97% sequence similarity level using UPARSE 7.1
(Stackebrandt and Goebel 1994; Edgar 2013). The most
abundant sequence in each OTU was selected as a rep-
resentative sequence. The OTU table was manually
filtered, removing chloroplast sequences from all sam-
ples. To minimize sequencing depth effects on alpha
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Plant Soil
and beta diversity measures, the number of 16 S rRNA
gene sequences per sample was rarefied to 20,000. The
taxonomy of each OTU representative sequence was
determined using the RDP Classifier version 2.2 (Wang
et al. 2007) against the 16 S rRNA gene database (e.g.,
Silva v138) with a confidence threshold of 0.7.
Statistical analysis
Correlation between the abundance of Foc TR4 and
soil properties, enzyme activity, and climate calcu-
lated by Spearman. Bioinformatic analysis of the
soil microbiome was carried out using the Majorbio
Cloud platform (https://​cloud.​major​bio.​com) and R
4.2.3. Alpha diversity includes observed OTUs and
Shannon index, and correlation analysis with Foc
TR4 was based on Spearman. The similarity among
the microbial communities in different samples was
determined by principal coordinate analysis (PCoA)
based on Bray-curtis dissimilarity using Vegan v2.5-3
package, and correlation analysis with environmen-
tal factors calculated through Mantel’s test (Dixon
2003). Constructing a core Microbial Evolution Tree
Using NJ Method by MEGA 7 and optimized with
iTOL (https://​itol.​embl.​de/). The co-occurrence net-
work was constructed using vegan, psych (Revelle
and Revelle, 2015), and igraph (Han et al. 2010)
packages and Gephi 0.9.2, and calculated the correla-
tion between each module and the abundance of Foc
TR4. Each node represents an OTU, and each edge
represents a significant correlation between node
(Spearman, R > 0.6, P < 0.05) (De Vries et al. 2018).
Calculating the module index through Gephi 0.9.2
was performed.
Results
Correlation between soil characteristics and Foc TR4
abundance
In 140 soil samples collected from diseased banana
plantations, the average Foc TR4 gene copy number
was 3.35 × ­106 copies ­g−1, ranging from 1.53 × ­107
to 1.32 × ­105 copies ­g−1. The average pH was 5.38,
with 111 samples having a pH lower than 6, indicat-
ing an overall acidic nature. Organic matter content
was 26.50 g ­kg−1. Total nitrogen was 1.48 g ­kg−1,
while available nitrogen was 115.91 mg ­kg−1. Total
Plant Soil
phosphorus measured 4.04 g k­g−1, and available
phosphorus was 91.14 mg ­kg−1. Total potassium was
34.39 g ­kg−1, and available potassium was 493.87 mg
­kg−1. Enzyme activity measurements revealed cata-
lase at 44.63 ­g−1 soil 24 ­h−1, phosphatase at 14.83 ­g−1
soil 24 ­h−1, invertase at 29.86 ­g−1 soil 24 ­h−1, and
urease at 273.56 ­g−1 soil 24 ­h−1. The abundance of
Foc TR4 showed a significant positive correlation
with total phosphorus (R = 0.32, P < 0.01), total nitro-
gen (R = 0.30, P < 0.05), organic matter (R = 0.18,
P < 0.05), urease (R = 0.18, P < 0.05), and annual pre-
cipitation (R = 0.34, P < 0.01). In contrast, it exhibited
a significant negative correlation with mean annual
temperature (R = − 0.25, P < 0.01) (Fig. 1).
Fig. 1  The correlation between environmental factors and Foc
TR4 abundance based on Spearman (**P < 0.01, *P < 0.05).
TP: total phosphorus; APR: annual precipitation; TN: total
nitrogen; AMT: annual mean temperature; SOM: soil organic
matter; URE: urease. Green represents positive correlation, red
represents negative correlation
Fig. 2  Correlation between Shannon index (a) and observed OTUs index (b) of bacterial and fungal communities and abundance of
Foc TR4 based on Spearman
Community diversity and composition and Foc TR4
correlations
The abundance of Foc TR4 was significantly posi-
tively correlated with the diversity (R = 0.18, p < 0.05)
and richness (R = 0.22, p < 0.01) of bacterial com-
munity, but for fungal communities, only richness
shows a significant positive correlation (R = 0.21,
p < 0.05) (Fig. 2). Furthermore, both bacterial com-
munity diversity and richness are significantly associ-
ated with the composition of bacterial (Shannon: R =
-0.72, Obs: R = 0.48, p < 0.001) and fungal (Shannon:
R = 0.42, Obs: R = 0.22, p < 0.01) communities, while
fungal community species richness was significantly
associated with the composition of both bacterial
(R = 0.28, p < 0.001) and fungal (R = 0.24, p < 0 0.01)
communities (Fig S2).
The OTU level, The mental’s test indicated that
the composition of bacterial and fungal communi-
ties was significantly correlated with pH (R = 0.32,
p < 0.001 for bacteria, R = 0.34, p < 0.001 for fungi),
CAT (R = 0.25, p < 0.001, R = 0.26, p < 0.001), INV
(R = 0.13, p < 0.01, R = 0.14, p < 0.01), AN (R = 0.13,
p < 0.01, R = 0.10, p < 0.01), and AP (R = 0.13,
p < 0.01, R = 0.17, p < 0.01). The composition of
bacterial communities at the order level was signifi-
cantly correlated with the abundance of pathogenic
bacteria (R = 0.06, p < 0.05). At the phylum level, the
composition of fungal communities was significantly
correlated with the abundance of pathogenic fungal
(R = 0.17, p < 0.001), while at other taxonomic levels,
there was no correlation between the composition of
bacterial and fungal communities and the abundance
of pathogenic bacteria (Table 1).
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Microbial taxa associated with pathogen
At the phylum level, Proteobacteria, Bacteroidota,
Cyanobacteria, Rozellomycota, and Glomeromycota
are significantly positively correlated with the abun-
dance of Foc TR4, while Firmicutes and WPS-2 are
significantly negatively correlated with pathogenic
bacteria abundance (Table 2). At the genus level,
Rhodanobacter, Gemmatimonas, Novosphingobium,
Allorhizobium-Neorhizobium-Pararhizobium-Rhizo-
bium, Solirubrobacter, Ilumatobacter, Reyranella,
Mucilaginibacter, Hyphomicrobium, Actinoplanes,
Rhodoplanes, SWB02, Flavobacterium, Devosia,
Dokdonella, Trichoderma, Purpureocillium and
Metarhiziu was positively correlated with the abun-
dance of FocTR4, and Bacillus is negatively cor-
related with the abundance of pathogenic bacteria.
These genera are known to possess high biocontrol
potential (Table 3).
We constructed a phylogenetic tree of the core
bacterial OTUs found in all samples and correlated
them with environmental factors. Among the core
microbiota, there were 14 Actinobacteria, 13 Proteo-
bacteria, 3 Firmicutes, and 1 each of Nitrospirota,
Acidobacteriota, and Myxococcota. Specifically,
OTU23598 (Pedomicrobium, R = 0.257), OTU23485
(Sphingomonas, R = 0.175), OTU24018 (Devosia,
R = 0.255), and OTU507 (Mycobacterium, R = 0.257)

Table 1  The correlation Community Factor Phylum Class Order Family Genus OTU
between environmental
factors and microbial Bacterial CAT​ 0.073 0.299*** 0.295*** 0.32*** 0.311*** 0.251***
community composition
PHO 0.078* 0.06 0.063 0.077* 0.08* 0.065
based on Mental’s test
INV 0.007 0.175*** 0.182*** 0.196*** 0.189*** 0.132**
URE 0.006 0.076 0.085* 0.089* 0.085* 0.048
pH 0.076 0.374*** 0.394*** 0.424*** 0.411*** 0.317***
SOM 0.051 0.172** 0.176** 0.187** 0.182** 0.16**
TN 0.027 0.133* 0.127** 0.134** 0.126* 0.087
AN 0.055 0.097* 0.109** 0.119*** 0.128** 0.132**
TP -0.007 0.037 0.04 0.046 0.07 0.089
AP -0.026 0.13* 0.146** 0.162** 0.159** 0.133**
TK -0.029 -0.029 -0.025 -0.012 0.004 0.028
AK 0.078 -0.027 -0.009 -0.002 0.001 -0.025
FocTR4 0.034 0.059* 0.032 0.021 0.012 0.016
AMT -0.043 0.007 0.004 0.01 0.006 0.03
APR 0.043 -0.056 -0.076 -0.081 -0.089 -0.087
Fungal CAT​ 0.061 0.066 0.101* 0.099* 0.112** 0.262***
CAT​Catalase, PHO PHO 0.045 -0.06 -0.078 -0.069 -0.069 0.089*
Phosphatase, INV INV 0.03 -0.021 -0.008 -0.002 0.008 0.137**
Invertase, URE Urease,
URE -0.006 0.093* 0.085* 0.069 0.063 0.055
SOM soil organic matter,
TN total nitrogen, AN pH 0.078* 0.04 0.044 0.055 0.066 0.339***
available nitrogen, TP total SOM 0.034 -0.012 0.001 0.019 -0.004 0.142*
phosphorus, AP available TN 0.042 -0.05 -0.038 -0.032 -0.05 0.076
phosphorus, TK total
AN 0.064* 0.101** 0.109** 0.132*** 0.125** 0.103**
potassium, AK available
potassium, Foc TR4 the TP 0.047 0.154** 0.15** 0.177** 0.192** 0.088
abundance of Foc TR4 AP 0.006 0.056 0.092 0.108* 0.109* 0.165**
*Significant at the 0.05 TK 0.019 0.175** 0.201*** 0.238*** 0.257*** 0.053
probability level AK 0.004 -0.056 -0.055 -0.044 -0.051 0.011
**Significant at the 0.01 FocTR4 0.171*** -0.019 0.009 0.016 0.016 0.008
probability level AMT 0.095* -0.057 -0.062 -0.053 -0.06 0.018
***Significant at the 0.001 APR 0.061* -0.088 -0.054 -0.035 -0.037 -0.107
probability level

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Table 2  The correlation between microbial taxa and Foc TR4 Table 3  The correlation between microbial taxa and Foc TR4
in the level of phylum by Spearman in the level of genus by Spearman
Phylum R RA Phylum Genus R RA

Proteobacteria 0.27** 31.90% Proteobacteria Rhodanobacter 0.17* 4.88%

Bacteroidota 0.39*** 4.19% Proteobacteria Dongia 0.17** 4.23%
Firmicutes -0.27** 2.52% Gemmatimonadota Gemmatimonas 0.17** 3.99%
WPS-2 -0.18* 0.92% Actinobacteriota Nakamurella 0.18** 3.85%
Cyanobacteria 0.21* 0.52% Actinobacteriota Galbitalea 0.18** 3.80%
Rozellomycota 0.22** 0.41% Bacteroidota Puia 0.18** 3.51%
Glomeromycota 0.17* 0.19% Proteobacteria Novosphingobium 0.19** 2.62%
Proteobacteria Allorhizobium- 0.20** 2.05%
*Significant at the 0.05 probability level
Neorhizobium-Para-
**Significant at the 0.01 probability level rhizobium-Rhizobium
***Significant at the 0.001 probability level Actinobacteriota Solirubrobacter 0.20** 2.01%
R correlation coefficient with Foc TR4, RA Relative abundance Actinobacteriota Ilumatobacter 0.20** 1.81%
of Foc TR4 Proteobacteria Reyranella 0.20** 1.71%
Bacteroidota Mucilaginibacter 0.21** 1.12%
Proteobacteria Hyphomicrobium 0.22** 0.82%
were significantly (P < 0.05) positively correlated with Actinobacteriota Actinoplanes 0.23** 0.64%
the abundance of pathogenic bacteria. OTU23514 Proteobacteria Ellin6067 0.23** 0.54%
(Unclass_Xanthobacteraceae, R = − 0.175), OTU23930 Proteobacteria Rhodoplanes 0.24** 0.49%
(Bacillus, R = − 0.216), OTU14931 (Candidatus_Soli- Proteobacteria SWB02 0.24** 0.43%
bacter, R = − 0.197), OTU23396 (unclass_Streptomyc- Bacteroidota Flavobacterium 0.24** 0.41%
etaceae, R = − 0.177), and OTU14049 (Mycobacterium, Bacteroidota Edaphobaculum 0.24** 0.38%
R = − 0.225) were significantly (P < 0.05) negatively Acidobacteriota Candidatus_Koribacter -0.25** 0.29%
correlated with the abundance of FocTR4. Among Proteobacteria Devosia 0.26** 0.17%
the core fungal OTUs, only OTU11728 (Fusarium) Firmicutes Bacillus -0.26* 0.17%
and OTU12062 (Trichoderma) were identified, and Proteobacteria Dokdonella 0.26** 0.16%
OTU12062 showed a significant negative correlation Proteobacteria Castellaniella 0.26** 0.16%
with the abundance of pathogenic bacteria (R = − 0.270, Ascomycota Trichoderma 0.21* 5.71%
P < 0.01) (Fig. 3). Ascomycota Plectosphaerella 0.23** 1.43%
Ascomycota Nigrospora 0.29*** 0.74%
Network analysis Ascomycota Cyphellophora 0.19* 0.51%
Ascomycota Codinaea 0.18* 0.29%
We constructed cross - kingdoms networks for bac- Ascomycota Microascus 0.22** 0.27%
teria and fungi (Fig. 4a), in which the module 5 was Ascomycota Purpureocillium 0.28*** 0.20%
significantly positively correlated with the abun- Ascomycota Dactylonectria 0.19* 0.18%
dance of Foc TR4 (Fig. 4b, Table S2). Exception Ascomycota Scytalidium 0.22** 0.16%
OUT23378 (unclass_Chloroplast), all other members Ascomycota Metarhizium 0.20* 0.14%
in this module were fungi. We constructed correlation Ascomycota Pyrenochaetopsis 0.25** 0.14%
networks based on different Foc TR4 abundances. Ascomycota Sodiomyces 0.22* 0.13%
The results indicate that as the Foc TR4 abundance in Ascomycota Acrocalymma 0.2* 0.13%
the soil increases, the modularity index of the cross - Ascomycota Immersiella 0.30*** 0.13%
kingdoms network significantly increases (R = 0.758, Ascomycota Apiosordaria 0.18* 0.12%
P < 0.05), suggesting an improvement in network sta-
bility (Fig. 4c). There was no significant correlation *Significant at the 0.05 probability level
**Significant at the 0.01 probability level
observed between the average degree and the abun-
***Significant at the 0.001 probability level
dance of Foc TR4, and there was no correlation with R correlation coefficient with Foc TR4, RA Relative abundance
the complexity of the cross-domain network. of Foc TR4

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Fig. 3  The phylogenetic distribution of the bacterial core
OTUs (present in all soil samples) and their primary driving
factors were investigated. A phylogenetic tree was constructed
using the NJ method. A heatmap was generated to illustrate
the correlation between environmental factors and core OTUs
using the Spearman correlation coefficient. CAT: Catalase;
Discussion
In this study, we attempted to investigate the abun-
dance of Foc TR4 in banana plantations and their
relationship with soil and environmental factors, as
well as the microbial communities. By characteriz-
ing the bacterial and fungal communities at 140 soil
samples were collected from 140 sampling points
in banana plantations through amplicon sequenc-
ing and analyzing soil physicochemical properties,
we found that the abundance of pathogens was sig-
nificantly positively correlated with total phosphorus,
total nitrogen, organic matterin the soil and annual
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Plant Soil
PHO: Phosphatase; INV: Invertase; URE: UreaseSOM: soil
organic matter; TN: total nitrogen; AN: available nitrogen; TP:
total phosphorus; AP: available phosphorus; TK: total potas-
sium; AK: available potassium. FocTR4: the abundance of Foc
TR4
precipitation, while it was negatively correlated with
temperature. Pathogen abundance was positively cor-
related with bacterial diversity and fungal richness,
but it was not related to the composition of bacterial
and fungal communities. However, within different
taxonomic groups, many microorganisms were still
found to be correlated with Foc TR4, with the asso-
ciated bacteria often having high biocontrol poten-
tial and the fungi mainly being soil-borne pathogens.
Additionally, our network analysis revealed that as the
pathogen abundance increased, the modularity index
of the network also increased. These results deepen
our understanding of the patterns of soil pathogen
Plant Soil
Fig. 4  Inter-kingdoms co-occurrence networks for bacteria
and fungi. Different colors represent different modules, and
each node represents an OTU (a). Correlation between Mod-
population changes in banana plantations and provide
evidence and guidance on how to reduce pathogen
abundance and select beneficial microorganisms in
banana production.
The impact of soil properties and environmental
factors on the abundance of pathogen
Revealing the influence of soil properties on the
abundance of soil-borne pathogenic fungi is cru-
cial for helping banana plantations reduce patho-
gen abundance in the soil (Löbmann et al. 2016;
Van Agtmaal et al. 2018). Our study indicates that
total phosphorus, total nitrogen, and organic mat-
ter in the soil are significantly positively correlated
with the abundance of pathogens. In the case of
interactions between under conditions of high phos-
phorus, more fungi tend to exhibit plant-damaging
effects (Mesny et al. 2021). A research shows that
higher phosphorus application rates increase the
severity of peanut wilt disease (Li et al. 2021a, b).
High nitrogen content and low pH could accelerate
the infect of FocTR4 and hinder plant development
(Segura-Mena et al. 2021) in the soil. A study also
suggests that increasing soil nitrogen levels could
ule 5 and abundance of Foc TR4 by Spearman (b). Correlation
between the module index of different Foc TR4 and abundance
of pathogen by Spearman (c)
increase the incidence of banana wilt disease by Foc
1 and the losses of biomass (Segura et al. 2022). It
is generally believed that the application of organic
fertilizers reduces the number of pathogens (Zhang
et al. 2014; Tao et al. 2020), which may be related
to adding organic fertilizers with a high diversity
of carbon sources can enhance microbial diver-
sity, thereby reducing pathogen numbers (Shen
et al. 2013). Excessive organic matter can also
increase the number of pathogenic fungi in the soil,
a research shows that the application of crop straw
and fresh livestock manure significantly increases
the proportion of plant pathogenic fungi, which is
associated with increased soil organic carbon (Du
et al. 2022). In this study, the positive correlations
between Foc TR4 and these nutrients may be related
to excessive fertilizer application in banana planta-
tions. Exceeding the threshold of nutrients required
for plant growth can increase the nutrients available
to pathogens in the soil and increase the plant pre-
disposition, making it easier for pathogens to infect
(Walters and Bingham 2007; Zhang et al. 2022).
Urease activity is an important indicator of soil
nitrogen availability, and its enzyme-catalyzed
products are a nitrogen source available to plants.
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Its activity can indicate soil nitrogen-supplying
capacity and is often positively correlated with
organic matter content, total nitrogen, and read-
ily available nitrogen content (Zantua et al. 1977;
Dharmakeerthi and Thenabadu 1996). The positive
correlation with FocTR4 in this study reflects the
increased pathogen abundance in soils with high
nitrogen content.
Despite large-scale studies suggesting an increase
in soil-borne pathogens with climate warming (Del-
gado-Baquerizo et al. 2020), this study reveals that
the soil content of FocTR4 is significantly nega-
tively correlated with the annual average tempera-
ture and positively correlated with precipitation.
The possible reason for this is that more overcast
and cooler days can increase plant predisposition
and accelerate the spread of pathogens (Pegg et al.
2019). Additionally, studies by Buddenhagen (2009)
proposed Foc TR4 as a genetically diverse fungal
species with various geographic lineages and patho-
types. Some of these, such as the South American
lineage, are likely more adapted to cooler climates,
exhibiting optimal growth and reproduction at tem-
peratures below 20 °C (Dita et al. 2017; Ploetz
2006). In contrast, the globally prevalent Tropical
Race 4 (TR4) lineage thrives in warmer conditions
(25–35 °C) (García-Bastidas et al. 2014; Molina
et al. 2009). Other lineages like Foc TR4, found in
Southeast Asia, may demonstrate wider tempera-
ture tolerance or even a preference for cooler condi-
tions (Maryani et al. 2019). Therefore, in the future,
banana plantations in Yunnan Province should aim
to select locations with higher annual average tem-
peratures and lower precipitation. Additionally,
they should reduce fertilizer application, especially
nitrogen and phosphorus, and find the appropriate
fertilizer amounts. This may help slow down the
accumulation of pathogens, thus reducing the inci-
dence of diseases.
The interaction between pathogen abundance and soil
bacterial and fungal communities
Higher soil microbial diversity is considered to be
associated with soil disease suppression (Garbeva
et al. 2004). In this study, the soil bacterial com-
munity species diversity and fungal community
species richness in banana plantations were sig-
nificantly positively correlated with the abundance
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Plant Soil
of pathogens. While this contradicts the traditional
paradigm, it aligns with other studies suggesting
that the relationship between diversity and dis-
ease can be more complex, context-dependent, and
driven by specific functional groups rather than
overall diversity indices (Liu et al. 2023). Previ-
ous studies have shown that disease-suppressive
soils in banana plantations have more stable bac-
terial and fungal community diversity and exhibit
higher diversity in response to Foc TR4 invasion
compared to disease-conducive soils (Ou et al.
2019). One potential explanation for our findings
might lie in the specific interactions within the
banana soil microbiome. Network analysis revealed
that stronger competition among microbial species
indeed reduced pathogen dominance, implying the
presence of antagonistic or resource-limiting mech-
anisms acting against Foc TR4 (Coyte et al. 2015).
Higher microbial diversity hinders the establish-
ment of pathogens in the soil (Gao et al. 2021).
The Mantel’s test results in this study show that
the composition of both bacterial and fungal com-
munities is significantly correlated with pH, avail-
able nitrogen, and available phosphorus. Notably, the
abundance of pathogens did not exhibit a significant
correlation with the composition of the microbial
community. The possible reason was that the soil
samples originated from diverse regions and climates,
which might reduce the correlation between Foc TR4
and microbiome composition. The primary drivers of
soil microbial communities are abiotic factors such
as climate and soil properties, with pH being particu-
larly significant (Islam et al. 2020). The relationship
between soil properties and microorganisms is recip-
rocal. Microorganisms regulated by the environment
simultaneously drive changes in the environment, and
the subsequent changes in soil properties driven by
microorganisms subsequently alter the composition
and function of microbial communities (Hartmann
and Six 2023).
These factors can serve as broad targets for the
regulation of soil microorganisms. However, vari-
ous microbial taxonomic groups remained signifi-
cantly associated with pathogen abundance. With
increasing pathogen abundance, there was a signifi-
cant enrichment of bacteria that are known to sup-
press pathogen abundance. For example, Rhodano-
bacter, the application of salicylic acid led to the
enrichment of Rhodanobacter in the root system of
Plant Soil
watermelons, assisting in resisting the infection of
a specialized watermelon sickle fungus (Zhu et al.
2022). High-abundance Gemmatimonas has been
identified as a potential biomarker for soil health
in Central American banana plantations (Shen
et al. 2014), and numerous studies have revealed its
(potential) functions in suppressing disease occur-
rence (Franke-Whittle et al. 2015; Rangjaroen
et al. 2017; Pang et al. 2022), including Candida-
tus_Koribacter (Xu et al. 2022) and Bacillus (He
et al. 2021), which are negatively correlated with
pathogen abundance. Conversely, as the abundance
of soil-borne pathogenic fungi gradually increased,
beneficial microorganisms such as Trichoderma
(Zin and Badaluddin 2020), Purpureocillium, and
Metarhizium (Baron et al. 2020), which have the
potential to suppress diseases, were identified.
These fungi have been reported as potential biocon-
trol fungi for various crop disease.
In conclusion, while beta diversity did not exhibit
a correlation with pathogens, there was still a signifi-
cant enrichment of beneficial bacteria and soil-borne
pathogenic fungi associated with increasing pathogen
abundance. This reflects the complex species interac-
tions that affect soil microbial community composi-
tion, and this process is likely primarily influenced
by host involvement since most of these microorgan-
isms have been shown to be preferentially recruited
by hosts through the release of corresponding car-
bon sources into the soil. A study showed that com-
pared to healthy chili peppers, plants infected with
Fusarium wilt disease are more susceptible to infec-
tion by other pathogenic fungi, but their roots, stems,
and fruit niches all accumulate potential beneficial
bacteria (Gao et al. 2021). Additionally, core micro-
organisms related to pathogens were identified to be
present in all regions, making them excellent targets
for soil biological regulation (Toju et al. 2018). Such
as, Sphingobium, A type of plant growth promoting
rhizobacteria (Asaf et al. 2020) and a large number
of reported healthy soil biomarkers (Innerebner et al.
2011; Fu et al. 2017; Ding et al. 2021).
The infection of pathogen increases competition
within the soil microbiome
The infection of pathogens intensifies competition
within the soil microbiome, as revealed by our co-
occurrence network analysis. We identified a module
of closely associated microbial taxa, predominantly
fungi, linked to pathogen presence. Interestingly,
this module included both beneficial and pathogenic
players. One prominent member is Mortierella, an
agricultural inoculant known for its cellulose, hemi-
cellulose, and chitinase-degrading enzymes (Li et al.
2020; Ozimek and Hanaka 2020). Studies have shown
that M. alpina inoculation significantly suppresses
ginseng root rot caused by Fusarium while promot-
ing plant growth-promoting bacteria and fostering a
more stable network (Wang et al. 2022). This high-
lights the multifaceted roles some microbes play
within the community, potentially acting as com-
petitors against pathogens while benefiting the host.
However, the module also harbors Plectosphaerella,
a soil-borne fungal pathogen known to induce wilt
disease (Carlucci et al. 2012; Raimondo and Carlucci
2018). This underscores the complexity of soil micro-
bial interactions, where beneficial and detrimental
actors can coexist and potentially influence each oth-
er’s niches and activities (Ray et al. 2020). Building
synthetic communities with carefully chosen players,
like cross-feeding communities, may offer promising
strategies for manipulating these interactions and pro-
moting disease suppression (Vorholt et al. 2017; Ke
et al. 2021). Our findings further suggest that patho-
gen abundance intensifies community modularity,
hinting at heightened competition within the micro-
biome. This aligns with existing research demonstrat-
ing that increased competition can hinder pathogen
invasion and establishment (Wei et al. 2015). Inter-
estingly, while healthy banana plants exhibit a more
stable community as expected (Fu et al. 2019), higher
pathogen abundance seems to trigger the recruit-
ment of specific beneficial bacteria. This suggests a
dynamic response by the host and microbiome, poten-
tially favoring competitive microbes against the path-
ogen. However, the recruitment of beneficial fungi
appears more selective, with an increased presence
of soil-borne fungi alongside pathogens. This raises
intriguing questions about the specific mechanisms
underlying host-microbe interactions and niche differ-
entiation within the soil community under pathogen
pressure. Unraveling these complexities through fur-
ther research is crucial for developing effective strat-
egies to manipulate the microbiome towards sustain-
able disease management.
Through this research, we gain valuable insights
into the intricate relationship between soil properties,
Vol.: (0123456789)
13

microorganisms, and soil-borne pathogens. By appre-
ciating the complexities and dynamics within the soil
microbiome, we can unlock promising avenues for
promoting soil health and mitigating soil-borne dis-
eases in banana plantations and beyond.
Conclusions
Our findings highlight the importance of understand-
ing Fusarium banana wilt pathogens and the environ-
mental factors that influence them. We suggested the
pathogen infection significantly impact the planta-
tions and its native microbial communities. In addi-
tion, we observed a positive correlation among the
pathogen abundance, soil factors, and diversity of
microbial communities. Conversely, a negative cor-
relation was observed with the annual mean tem-
perature. As Foc TR4 accumulate, beneficial bacteria
(such as Rhodanobacter, Gemmatimonas, Novosphin-
gobium) and soil borne fungi (such as Plectosphaere-
lla, Nigrospora, Cyphellophora) were recruited, and
network was more stable. This study contributes
valuable information for mitigating pathogenic fungal
abundance and promoting beneficial microorganisms
in banana production.
Acknowledgements We thank all staff members in the
Yunnan Key Laboratory of Green Prevention and Control of
Agricultural Transboundary Pests for their considerable help
with samples collection. The research leading to these results
received funding from Yunnan Provincial Agricultural Joint
Special Project (202101BD070001-001), Yunnan Provincial
Xingdian Talent Program “Young talent” Project (YNWR-
QNBJ-2019-246; YNWR-QNBJ-2020-298), Natural Science
Foundation of China (31600349), Yunnan Science and Tech-
nology Mission (202204BI090019) and the earmarked fund for
CARS (CARS-31-22). Special thank you is also given to the
reviewers.
Authors’ contributions Wenlong Zhang: Methodology,
Software, Visualization, Writing - review & editing. Tingting
Bai: Conceptualization, Supervision, Funding acquisi-
tion. Arslan Jamil: Writing - review & editing. Huacai Fan:
Resources, Investigation. Xundong Li: Supervision, Funding
acquisition. Si-Jun Zheng: Conceptualization, Supervision,
Funding acquisition. Shengtao Xu: Conceptualization, Super-
vision, Funding acquisition, Writing - review & editing.
Declarations
Conflict of interest The authors declare no conflicts of inter-
est.
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13
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