horticulturae

Review
Significance of Soil Siderophore-Producing Bacteria
in Evaluation and Elevation of Crop Yield
Siwen Zhang 1,2 , Zishi Deng 2 , Ali Borham 1,3 , Yao Ma 1 , Yi Wang 4 , Jiawei Hu 1 , Juanjuan Wang 1,5, *
and Tsing Bohu 6,7, *

1 Department of Resources and Environmental Science, College of Environmental Science and Engineering,
Yangzhou University, Yangzhou 225127, China
2 National Observation and Research Station of Coastal Ecological Environments in Macao,
Macao Environmental Research Institute, Macau University of Science and Technology,
Macao SAR 999078, China
3 Agricultural Botany Department, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt
4 College of Natural and Environment, Northwest A&F University, Yangling 712100, China
5 Key Laboratory of Arable Land Quality Monitoring and Evaluation (Yangzhou University),
Ministry of Agriculture and Rural Affairs, Yangzhou 225127, China
6 State Key Laboratory of Lunar and Planetary Sciences, Macau University of Science and Technology, Taipa,
Macao SAR 999078, China
7 Xiong’an Institute of Innovation, Baoding 071700, China
* Correspondence: [email protected] (J.W.); [email protected] (T.B.)

Abstract: Iron is a vital element for plant and microbial growth; yet, the major portion of iron in soils
is in the form of (oxi-)hydroxides with limited bioavailability, resulting in decreased crop yield quality.
In response to iron deficiency, soil microorganisms produce siderophores that transform insoluble
iron into a soluble form that plants and microorganisms can use. The abundance and activity of
siderophore-producing bacteria (SPB) might be used as a biological assessment index for the fertility
status of cultivated land. In order to achieve this goal, it is critical to investigate the influences of SPB
on plant growth and soil quality. In this study, we performed a mixed-effect model meta-analysis on
342 research studies that compared plant growth with and without SPB. The findings revealed that
SPB increased plant growth significantly (up to 30%). The stimulating effects on plants followed the
Citation: Zhang, S.; Deng, Z.;
sequences of pant weight, plant height, and germination rate.
Borham, A.; Ma, Y.; Wang, Y.; Hu, J.;
Wang, J.; Bohu, T. Significance of Soil
Keywords: siderophore-producing bacteria; meta-analysis; plant growth; growth-promoting effect
Siderophore-Producing Bacteria in
Evaluation and Elevation of Crop
Yield. Horticulturae 2023, 9, 370.
https://doi.org/10.3390/
horticulturae9030370 1. Introduction

Academic Editor: Giovanni Bubici

Iron, a vital element for almost all life, is essential for numerous biological activities, in-
cluding electron transport, oxygen metabolism, nitrogen fixation, DNA and RNA synthesis,
Received: 30 November 2022 etc. [1,2]. Although it is the fourth most abundant metal in the earth’s crust, the bioavailabil-
Revised: 5 March 2023 ity of iron is very low [3]. The content of soluble iron in the soil is insufficient for the proper
Accepted: 10 March 2023 development of plants (10− 9 –10− 4 mol/L) [4] and microorganisms (10− 7 –10− 5 mol/L).
Published: 12 March 2023
The soluble iron content in the majority of soils (particularly alkaline soils) is only pico-
molar (10− 9 –10− 18 mol/L) [5–7]. In a highly aerobic alkaline environment, Fe2+ is readily
oxidized in soils and forms iron oxides or hydroxides varied in compositions, degrees of
Copyright: © 2023 by the authors.
crystallization, and solubility [1]. The solubility of Fe3+ (oxi-)hydroxides in soil decreases
Licensee MDPI, Basel, Switzerland. by a factor of 1000 for every unit increase in pH. Soluble iron is at its lowest concentration
This article is an open access article when the pH is between 7.5 and 8.5 [8]. Because soluble iron is scarce and largely found
distributed under the terms and in poorly soluble Fe compounds in neutral or alkaline soils, crops suffer from severe iron
conditions of the Creative Commons deficiency [9]. In China, the soil is alkaline in the north, where iron deficiency is more
Attribution (CC BY) license (https:// severe, and acid in the southern region. Iron is an essential trace element for plant growth,
creativecommons.org/licenses/by/ and the amount of soluble iron has an impact on the health of plants. Plant leaves turn
4.0/). yellow from the veins due to a drop in chlorophyll content brought on by an iron deficit.

Horticulturae 2023, 9, 370. https://doi.org/10.3390/horticulturae9030370 https://www.mdpi.com/journal/horticulturae

Horticulturae 2023, 9, 370 2 of 10

Severe iron deficiency may cause plant death at the seedling stage, which would reduce
agricultural productivity [10]. High iron intake, however, may also result in the release of
reactive oxygen species and iron poisoning. Iron concentration needs to be maintained at a
steady level for plants to grow properly. In recent years, iron deficiency in plants has been
highlighted as one of the greatest agricultural challenges internationally [11].
To provide iron nutrition for themselves or their hosts, TonB-dependent transporters
help transfer iron into cells [12]. The siderophore cell membrane’s transport mechanism is
shown in Figure 1.

Figure 1. Process of transferring metal ions into cells by siderophores in soil. Metal ions combine
with the siderophore produced by bacteria near a plant’s root in dirt. Some complex compounds
enter the cell membrane, whereas metal ions remain in the periplasm, and siderophores are released
for cyclic usage. Others enter the cytoplasm via the cell membrane with the aid of TonB machinery.

For siderophores, there are more than 500 different chemical structures [13]. Siderophores
can be divided into three broad categories [14] based on the functional groups that bind
to Fe3+ and the varied topologies of siderophores: hydroxamate siderophores, catecholate
siderophores, and carboxylate siderophores. Hydroxamate siderophores are the most
frequently produced siderophores by both bacteria and fungi. The bacterial hydroxamic
type is composed of hydroxylated and acylated alkylamines, as opposed to the fungal
hydroxamic type, which is composed of hydroxylated and acylated ornithine groups [15].
Catechol is made by bacteria. This siderophore is lipophilic, has a strong affinity for iron,
and can withstand environmental pH changes. In addition, catecholate siderophores may
be utilized as a potent reducing agent to compete with pathogenic fungi for iron more
efficiently. Few bacteria can create carboxylate siderophores. Different siderophores chelate
Fe3+ in different ways. The most efficient chelators of Fe3+ are the carboxylate, hydroxamate,
and catecholate types [13]. The iron-chelating ability of fungal siderophores is slightly
less than that of bacterial siderophores among the siderophores of the same functional
group [16]. The synthesis of siderophores is greatly influenced by metal ions in the soil.
The main determinant of siderophores’ formation is the concentration of soluble iron. For
example, the ability of Acinetobacter calcoaceticus to secrete is inhibited when the amount
of soluble iron in the environment approaches 20 uM [17]. In the presence of iron, the
cytoplasmic Fur protein of Pseudomonas aeruginosa inhibits siderophore production [18].
Fur regulates siderophore secretion by controlling gene expression in response to changes
in iron concentration [19]. Additionally, research has demonstrated that some plants may
produce chemicals such as furanone in the absence of iron to specifically encourage or
hinder the development of siderophores [20]. Other metal ions, such as Cd2+ , Hg2+ , and
Co2+ , can similarly stimulate or inhibit the production of siderophores by bacteria [21,22].
For instance, Trichoderma produces siderophores when iron is scarce, and its production is
boosted by high Zn2+ concentrations. The synthesis of siderophores also heavily depends
on sources of carbon and nitrogen [23]. It has been shown that the synthesis of siderophores
can be greatly increased by cultivating SPB in the lab using mannitol and sucrose as carbon
Horticulturae 2023, 9, 370 3 of 10

sources and yeast extract and urea as nitrogen sources [20]. With a 13.3% increase in iron
carrier synthesis in the presence of 5 g/L glucose in a PDA medium, strain RL1 had the
highest rate [24]. The production of siderophores is also influenced by temperature, pH,
C/N ratio, and medium type [15–25].
At present, SPB has been found to promote the growth of many plants. For example,
it has been found that Bacillus subtilis Bs-15 has a good effect on the prevention and
control of pepper Fusarium wilt and growth promotion [26]. Moreover, SPB can raise the
amount of nutrients in the soil to the point where wheat plant growth has been seen even
under drought-like situations. [27]. The inoculation of SPB in lettuce increased nitrogen,
phosphorus, and potassium nutrients under drought stress and promoted its growth [28].
Therefore, the use of SPB to promote crop growth to produce microbial iron fertilizer will
be expected to replace some chemical fertilizers. At the same time, the antibacterial effect
of SPB can also be applied in biological control.
However, there is little research on the variables that affect SPB from the perspective
of a plant. We conducted a global study involving 342 comparative data points from
30 studies in the literature over the course of the preceding five years in order to carefully
assess the effects of adding SPB to soil on plant development and the factors influencing
the growth-promoting influence of SPB on plants. Our goals are to (1) quantify the changes
in plant growth caused by the addition of SPB and (2) examine the effects of different plant
family and genus classifications and measurement techniques on these changes. As a result,
we will be able to use SPB as rhizobacteria that promote growth more successfully.

2. Materials and Methods

2.1. Date Sources
To locate the relevant literature for our meta-analysis, we searched the Web of Science
and China National Knowledge Infrastructure (CNKI) for articles investigating the growth-
promoting impact of siderophore-producing bacteria published between 2018 and 2022.
The literature search was performed following guidelines from Preferred Reporting Items
for Systematic Reviews and Meta-Analyses (PRISMA) [29] (Table S1). The search terms
were “siderophore and growth-promoting” or “siderophore and plant”. In addition, the
following criteria were used to evaluate the publications’ integrity, relevance, and scientific
merit: (1) We ensured that each research was independent and based on real measurement
data; (2) each study was required to disclose the effects of SPB on plant development with
or without the substance; (3) the research must include the kinds and development of
plants; (4) the statistical information, including mean values of root length and root dry
weight, standard deviation (SD), and sample size, was collected directly from the tables of
the published articles or from the graphs using GetData 2.20.
The selected studies provided information on (1) the names and families of tested
plants; and (2) germination rate, plant height, root length, leaf fresh weight, leaf dry
weight, root fresh weight, root dry weight, total fresh weight, and total dry weight. As a
consequence, we narrowed down the findings to 30 scientific journal papers containing 342
observations (Table S1).

2.2. Date Analysis

We employed the natural logarithmic response ratio (ln RR) to evaluate the effect size
of SPB on plant growth. !
Ye
ln RR = ln (1)
Yc

where Ye and Yc are the mean value of the variable with (treatment) or without (control)
the addition of SPB.
The variance of each observation was calculated as follows:

Se 2 Sc 2
vi = + (2)
Ne Ye 2 Nc Yc 2
Horticulturae 2023, 9, 370 4 of 10

where Se and Sc are the SD of each observation, while Ne and Nc are the sample size of
each variable in treatment and control groups. If we can only extract the standard error
(SE) from a study, the SD should be recalculated.
This meta-analysis was performed using the cumulative effect size. We used the
random-effect model to perform the following calculation: For the within-case variance (τ2),
we use the restricted maximum likelihood (REML). The weight (Wi ) of each observation
and the total variance between observations in the model (I 2 ) were calculated as follows:

1
Wi = (3)
Vi + τ 2

( k − 1) ∑ wi
S2 = (4)
( ∑ wi )2 − ∑ wi 2
τ2
I2 = (5)
τ 2 + S2
where k is the sample size of the study.
The statistical tests were deemed significant at a p-value of less than 0.05. All meta-
analysis processes were performed using Openmee, and all figures were created with
GraphPad Prism.

2.3. Model Diagnostic and Influencing Factor Analysis

Using a linear mixed-effect model, we looked into how the plant family and mea-
surement mode affected these impacts. The funnel plot analysis and fail-safe number
test were used with the Openmee software and a 95% confidence interval to examine the
model’s diagnostics.

3. Results
3.1. Variation in Plant Family Growth under SPB
Plant growth increased by 30.00% on SPB based on 342 observations. Our paired
observations reported 10 plant families: Pailionaceae (30 studies), Rosaceae (12 studies), Lil-
iaceae (2 studies), Leguminosae (28 studies), Compositae (14 studies), Musaceae (3 studies),
Solanaceae (49 studies), Cucurbitaceae (21 studies), Cruciferae (52 studies), and Gramineae
(131 studies). The way SPB affected plant growth was different for each plant family
(Figure 2, Table S2). Compared with the control, our results showed that adding SPB had a
significant effect on plants from different families, especially the Compositae and Cucur-
bitaceae, which were helped by 49.1% and 50.8%, respectively. Gramineae, Rosaceae, and
Musaceae, on the other hand, were only helped by 15.60%, 17.20%, and 22.30%, respectively.
At the same time, the different numbers of paired observations showed that the results of
the meta-analysis did not change much when the number of observations was decreased.
This showed that our analysis was accurate.
SPB had different encouraging effects on plants belonging to different families. The
majority of current research is focused on graminaceous plants, with little attention paid to
other plant families. Although SPB had the least effect on graminaceous plants, it had the
lowest error rate (Figure 2).
Horticulturae 2023, 9, 370 5 of 10

Figure 2. The size of the effect of SPB on different plant families. The error bars in the circles display
the 95% confidence intervals (CIs) for the overall mean. The answer is deemed significant if the CI
does not overlap with zero. The number in parentheses indicates the number of observations.

3.2. Growth Changes under SPB for Various Measurement Modes

Different measurement methods could produce different results (Figure 3, Table S3).
When compared to the control group, the plant’s overall dry weight increased by 83.00%.
Additionally, there was a 23.70% rise in root length and a 26.80% increase in plant height,
while the germination rate has just increased by 5.60%.

Figure 3. The effect size of measurement methods under SPB. The error bars in the circles display the
95% confidence intervals (CIs) for the overall mean. The answer is deemed significant if the CI does
not overlap with zero. The number in parentheses indicates the number of observations.

The effects of SPB were primarily reported in terms of changes in biomass, with
weight increase preferred over plant length increase (Figure 3). This might be because iron
supplementation promotes plant photosynthesis and the accumulation of organic materials.

3.3. Potential Bias in Publications

The funnel plot analysis proved that our research was less susceptible to publication
bias and that our finding was trustworthy (Figure 4), and the fail-safe number test showed
that 22,332,149 trials with opposing results would be required to overturn our conclusions.
Horticulturae 2023, 9, 370 6 of 10

Figure 4. The funnel plot analysis of all paired data. The 95% confidence interval (CI) is indicated
by the white area in the center. Every single black dot stands for a distinct pair of observations. The
result is reliable and less prone to publication bias if the black dot is symmetrical with regard to the
solid line in the center.

4. Discussion
Siderophores are among the phytohormones produced by microbes. Insoluble Fe3+
may be used more easily in the environment when siderophores are present, enhancing
the bioavailability of Fe3+ [30]. Under different iron concentrations, the growth-promoting
effect of SPB was different [31]. Plants may directly absorb and utilize the complex produced
by siderophores and Fe3+ , enhancing their iron nutritional status. Previous studies have
shown that siderophores during the germination and emergence phases [32] increase
the germination rate and seedling activity of popular crops such as tomatoes [33,34],
cucumbers [35], wheat [36–38], etc. In addition, siderophores may deliver nutrients to plants
in heavy-metal-polluted soils to reduce stress toxicity and enhance plant development [39].
For instance, the addition of a suspension of the siderophore fungus led to a progressive
increase in the fresh weight of Shanghaiqing and the amount of photosynthetic pigment in
the leaves [25]. When the highest concentration of spore solution (3.2*108 CFU/mL) was
used, the fresh weight of stems and leaves increased by 74.0%, while the fresh weight of
the plants as a whole increased by 75.0% [25].

4.1. The Inhibitory Effect of SPB on Plant Pathogens

The production of siderophores is one of the most effective techniques for reducing
plant diseases [40]. PGPR may restrict the amount of plant inter-root pathogens by secreting
siderophores, which compete with ambient trace iron to deprive pathogenic bacteria of
iron [32]. For instance, growth-promoting rhizosphere-produced siderophores effectively
ward off fungal infections such as Phytophthora, Pythium, and Sclerotinia plant diseases [41].
Additionally, some research has indicated that siderophores have an impact on the growth
of fungi. The siderophore produced by Pseudomonas aeruginosa FP6 may greatly reduce
Colletotrichum gloeosporioides growth during the growth of peppers [21]. Seven of the
siderophore-producing strains tested by Vijay Karuppiah et al. against Fusarium oxysporum
f. sp., lycopersici MTCC10270 (Fol), Fusarium equiseti MFol, and Sarocladium sp. SWL showed
in vitro antifungal activity [42]. Neofusicoccum kwambonambiense XKD-1, the pathogen
that causes strawberry root rot, was completely inhibited by Penicilium asturianum XK-12
siderophore fermentation broth when 20% (volume fraction) of Penicilium asturianum was
added [43].
The majority of SPB are PGPR, which provides another explanation for the inhibitory
effect of siderophores on harmful bacteria. Unlike pathogens, SPB is indigenous bacteria.
Horticulturae 2023, 9, 370 7 of 10

When the chelating ability and generation of siderophores produced by pathogens and
PGPR in soil are identical, SPB can prioritize controlling iron atoms in soil [44].

4.2. The Effect of SPB on Other Metal Ions

In the soil, siderophores might increase the bioavailability of heavy metals. The
siderophore can chelate other metal ions in addition to Fe3+ ions, such as cadmium, lead,
nickel, arsenic, aluminum, magnesium, zinc, copper, cobalt, strontium, and iron [45,46].
Rhodococcus strains that can produce siderophores have been found to be able to extract
the metal ions V (III), Ga (III), and In (III) from mixed metal solutions [24]. The chelation
of heavy metals and siderophores not only reduces the toxicity of heavy metal ions but
also increases the activity of heavy metals in the rhizosphere of plants, increases the
uptake and accumulation of heavy metals by plants, and improves phytoremediation
effectiveness. Following inoculation with P. aeruginosa, Armelle Braud observed that
the absorption of Cr and Pb in the above-ground region of maize increased by 5.4 and
3.8 times, respectively [47]. Peat moss and iron-producing bacteria combined, according
to Hanna Virpiranta’s research, have a 96% nickel adsorption capability [48]. Free heavy
metal ions can easily enter cells through the cell membrane of bacteria through active
or passive absorption. However, due to the increase in molecular weight caused by the
presence of siderophores, some heavy metal ions that have been chelated with them
are unable to enter bacteria via porin. This may reduce the toxicity of heavy metals
to bacteria. Several arsenic-tolerant bacteria will produce siderophores in an arsenic-
contaminated environment. When siderophores chelate with ferrihydrite, realgar, etc., iron
ore is dissolved. Furthermore, siderophores may indirectly affect the way microbes reduce
arsenic by using other substances [49]. When heavy metals bind to free siderophores, they
prevent iron ions from being chelated, which reduces the amount of accessible iron and
encourages the synthesis of more siderophores, which can help bacteria or plants thrive and
partially shield them from the toxicity of heavy metals [50]. The YQ9 is a high-siderophore
of B. vietnamiensis, and investigations have shown that it can withstand high concentrations
of Pb2+ , Zn2+ , Cu2+ , and Cd2+ with minimal inhibitory values of 3000, 5000, 4500, and
1000 mol/L, respectively [51,52]. Additionally, it has been found that siderophore bacteria
may increase their siderophore–pyoverdine production in response to Cd2+ , enhancing the
strains’ resistance to the metal [53]. Carmen Tamariz-Angeles et al. found that the survival
rate of alfalfa seedlings rose after inoculation with the SPB BEP17-Dm, BEP18-Dm, or BRU16
when the environment’s Cd2+ , Pb2+ , or Al+ concentrations were 0.5–1.0 mM, 0.5–1.0 mM,
and 2.5–5.0 mM, respectively [54]. When Cd2+ is given, SPB takes part in siderophore
formation, whereas cell Cd2+ accumulation declines [55]. The influence of siderophores
will, however, decrease as the level of heavy metals increases, as demonstrated by the
fact that the effect of the cadmium-resistant siderophore bacteria LY02 was significantly
reduced at a Cd2+ concentration of 1.3 mM [56].
Therefore, due to their high tolerance for heavy metals, SPB may live and proliferate
in large numbers in contaminated areas if they are introduced into the rhizomes of heavy
metal hyperaccumulator plants. In areas with heavy metal pollution, it may chelate Fe3+
and other metal ions. It might promote the growth of super-enriched plants, enabling
them to take up more metal ions. Moreover, studies have found that microorganisms with
growth-promoting siderophores and growth-inhibiting siderophores have the opposite
effect on pathogenic bacteria [57], which means an incorrect application of siderophores
may have a negative impact on agricultural production. Therefore, the effects of different
types of siderophores need to be further studied.

5. Conclusions
The addition of SPB to varied plant families may increase plant yield to a certain extent.
The most significant effect of SPB on plant root, leaf, and germination rates was on root
dry weight. Nevertheless, more attention should be paid to plant families and variations in
biomass, as the economic value of diverse plant families differs, including ornamental and
Horticulturae 2023, 9, 370 8 of 10

edible varieties. The appropriate use of SPB may increase agricultural yield, whereas a bad
application may increase the heavy metal content of food.

Supplementary Materials: The following supporting information can be downloaded at: https:
//www.mdpi.com/article/10.3390/horticulturae9030370/s1, Table S1: The data extracted from the
literature; Table S2: The size of the effect of SPB on different plant families; Table S3: The effect size of
measurement methods under SPB.
Author Contributions: Conceptualization, J.W., T.B. and S.Z.; methodology, S.Z., T.B. and J.W.;
software, S.Z., J.W. and J.H.; validation, J.W., S.Z. and Z.D.; formal analysis, S.Z., Y.W. and Z.D.;
investigation, S.Z., A.B. and Z.D.; resources, S.Z., J.W. and Y.W.; data curation, S.Z., J.H. and Z.D.;
writing—original draft preparation, S.Z., J.W., Y.M. and Y.W.; writing—review and editing, S.Z., A.B.,
J.W. and Y.W.; visualization, S.Z., J.W. and A.B.; supervision, J.W. and T.B.; project administration,
J.W. and T.B.; funding acquisition, S.Z. and J.W. All authors have read and agreed to the published
version of the manuscript.
Funding: This work was supported by the Postgraduate Research and Practice Innovation Program
of Jiangsu Province (Yangzhou University), grant number KYCX21_3254; and the Key research and
development projects (social development) of Yangzhou, grant number YZ2022060.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.

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