Streptomyces can be an excellent plant growth manager

Abstract

Streptomyces, the most abundant and arguably the most important genus of actinomycetes, is an important source of biologically active compounds such as antibiotics, and extracellular hydrolytic enzymes. Since Streptomyces can have a beneficial symbiotic relationship with plants they can contribute to nutrition, health and fitness of the latter. This review article summarizes recent research contributions on the ability of Streptomyces to promote plant growth and improve plant tolerance to biotic and abiotic stress responses, as well as on the consequences, on plant health, of the enrichment of rhizospheric soils in Streptomyces species. This review summarizes the most recent reports of the contribution of Streptomyces to plant growth, health and fitness and suggests future research directions to promote the use of these bacteria for the development of a cleaner agriculture.

Full text

Vol.:(0123456789)
1 3
World Journal of Microbiology and Biotechnology (2022) 38:193
https://doi.org/10.1007/s11274-022-03380-8
REVIEW
Streptomyces can be anexcellent plant growth manager
FeiPang1· ManojKumarSolanki2· ZhenWang1
Received: 4 July 2022 / Accepted: 7 August 2022
© The Author(s), under exclusive licence to Springer Nature B.V. 2022
Abstract
Streptomyces, the most abundant and arguably the most important genus of actinomycetes, is an important source of biologi-
cally active compounds such as antibiotics, and extracellular hydrolytic enzymes. Since Streptomyces can have a beneficial
symbiotic relationship with plants they can contribute to nutrition, health and fitness of the latter. This review article sum-
marizes recent research contributions on the ability of Streptomyces to promote plant growth and improve plant tolerance
to biotic and abiotic stress responses, as well as on the consequences, on plant health, of the enrichment of rhizospheric
soils in Streptomyces species. This review summarizes the most recent reports of the contribution of Streptomyces to plant
growth, health and fitness and suggests future research directions to promote the use of these bacteria for the development
of a cleaner agriculture.
Keywords Streptomyces· Plant health· Bioremediation· Abiotic factors· Biotic pathogens
Introduction
Chemical fertilizers and pesticides have been increas-
ingly used in conventional agriculture to ensure the grow-
ing global food demands (Kamaei etal. 2019) and this has
also increased environmental pollution. In recent years,
microbes-based products such as biofertilizers and biope-
sticides have been utilized, but still, a significant portion
of agriculture depends on chemical products. Therefore, an
increasing number of researchers have used advanced bio-
technological and microbiological strategies to explore the
links between beneficial microbes and plant growth. Indeed,
micro-organisms play important roles to reduce plant disease
by limiting growth of phytopathogenic agents via competi-
tion for nutrients, production of antimicrobial compounds
and hydrolytic enzymes as well as by the induction of plant
defenses promoting systemic resistance (Ha-Tran et al.
2021).
Plant growth-promoting rhizobacteria (PGPR) is a class
of beneficial microorganisms that positively interact with
the plant. Some PGPR can fix nitrogen and absorb from the
soil nutrients necessary for plant growth such as phosphate,
zinc, iron and potassium (Basu etal. 2021). Plant root exu-
dates and metabolites can regulate microbial functions in
the rhizosphere (Bhardwaj etal. 2014; Canarini etal. 2019;
Korenblum etal. 2022; Maurer etal. 2021; Olanrewaju etal.
2019). For instance, plant growth-promoting Streptomyces
(PGPS) can colonize plant rhizospheres or tissues and form
good symbiotic relationships (Olanrewaju and Babalola
2019). Streptomyces are Gram-positive bacteria that belong
to the Streptomycetaceae family and Actinomycetales order.
Streptomyces, the largest genus of Actinobacteria with more
than 570 distinct species (Law etal. 2018), comprises aero-
bic filamentous bacteria growing as vegetative mycelium
that will eventually form aerial hyphae whose tip ends differ-
entiate into spores. Spores are able to survive under adverse
environmental conditions and their dissemination allows
the bacteria to colonize various environments (Castro etal.
2018). Two-thirds of the 23,000 bioactive secondary metab-
olites produced by microorganisms are produced by Act-
inobacteria, and mainly Streptomyces species. (Ochi 2017;
Quinn etal. 2020) Indeed, approximately three quarter of
* Manoj Kumar Solanki
mkswings321@gmail.com
* Zhen Wang
wang798110510@163.com
1 Guangxi Key Laboratory ofAgricultural Resources
Chemistry andBiotechnology, College ofBiology
andPharmacy, Yulin Normal University, Yulin537000,
China
2 Plant Cytogenetics andMolecular Biology Group, Faculty
ofNatural Sciences, Institute ofBiology, Biotechnology
andEnvironmental Protection, University ofSilesia
inKatowice, 40-701Katowice, Poland

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
193 Page 2 of 12
Streptomyces strains are able to produce antibiotics (Vuru-
konda etal. 2018) and 60% of the new pesticides and her-
bicides described in the past 30years are derived from
Streptomyces species. Furthermore Streptomyces species
secrete numerous hydrolases able to degrade major com-
ponents of the cell wall of the fungi, such as chitin and cel-
lulose limiting growth of the latter (Lv etal. 2021; Meschke
and Schrempf 2010; Schrempf 2001; 2017; Siemieniewicz
and Schrempf 2007). This article reviews comprehensively
how PGPRs promote plant growth and improve plant stress
tolerance.
Streptomyces species provide nutrients
toplants
PGPRs are beneficial microorganisms present in the rhizo-
sphere. PGPRs promote plant growth and development
through various direct or indirect processes, including the
circulation of nutriments or metals and the synthesis of plant
hormones. They also contribute to maintain the rhizospheric
microbial network and thus soil homeostasis and fertility
(Pramanik etal. 2021; Trivedi etal. 2020) and help plants
to resist abiotic and biotic stress.
Most nitrogen presents in gas form in nature that can-
not be absorbed and utilized by plants, as plants can only
directly absorb nitrogen in the form of NO3− or NH4+ and
small amounts of amino acids and oligopeptides. Little
information on nitrogen fixation by Streptomyces species
is available in comparison with other bacteria. Different
bacteria have different nitrogen fixation pathways: da-Silva
etal. (2017) reported that saprophytic rhizobia growth is
regulated through stress response genes such as otsA (tre-
halose-6-phosphate synthase), groEL (heat shock protein),
clpB (chaperone), and rpoH (transcriptional regulator) in the
extreme environments. And perhaps these genes are involved
in symbiosis, for example heat shock proteins (such as
ClpB and GroESL) transcriptomic up-regulation resulted in
Bradyrhizobium japonicum and Sinorhizobium meliloti nod-
ules in stress condition (Oleńska etal. 2020). Pseudomonas
stutzeri core genome NfiS is involved in optimization of
nitrogen fixation by the direct posttranscriptional regulation
of nitrogenase genenifKmRNA (Zhan etal. 2016), but the
nitrogen fixation pathway of Streptomyces remains unclear.
Ribbe etal. (1997) reported that Streptomyces thermoauto-
trophicus has nitrogen fixation ability, but this feature was
questioned by MacKellar etal. (2016). Afterward, Wang
etal. (2017b) and Dahal etal. (2017) successively reported
the nitrogen-fixing ability of Streptomyces. In particular,
sugarcane's nitrogen-fixing ability was shown to increase
by 9.16% after inoculation with Streptomyces chartreusis
WZS021, and the transconjugation system of this strain was
established and optimized to insert marker genes to detect
nitrogen fixation sites of the strain and exogenous gene trans-
fer (Wang etal. 2017a). Moreover, Dahal etal. (2017) also
detected nitrogen-fixing Streptomyces in the South Dakota
moorland arid region.
Plants naturally have low phosphorus absorption and
utilization capacity; thus, most of the phosphorus fertiliz-
ers either precipitated and thus become insoluble or were
adsorbed on soil constituents cannot be efficiently utilized by
the crops. Notably, Streptomyces species can convert insolu-
ble phosphorus of the soil into a soluble form that plants can
assimilate (Alori etal. 2017). Streptomyces played signifi-
cant role in maintaining bioavailability of phosphate in the
form of polyphosphate. Two-component system consisting
controls positively phosphate scavenging (hydrolases) and
uptake (high affinity ABC transporters) in conditions of low
phosphate concentration, during this process PhoR phospho-
rylates its cognate response regulator (PhoB or PhoP) helps
bacteria to adapt phosphate limited condition (Devine 2018;
Romero-Rodríguez etal. 2018).
Bacteria secrete substances such as extracellular enzymes,
organic acids, protons, siderophores to convert insoluble
phosphorus into soluble phosphates and these process play
important role in inhibiting other microorganism (Hamdali
etal. 2021). Among these, the secretion of organic acids is
the primary mechanism of phosphorus solubilization and
extracellular enzymes could be involved in the scavenging
of phosphate present in biological molecules (Zhang etal.
2021). Extracellular enzymes are involved in the scaveng-
ing of phosphate of biological molecules present in the soil.
As for potassium, potassium-dissolving bacteria secrete
inorganic acids, organic acids and extracellular polymers
(primarily proteins and polysaccharides), that can facilitate
the decomposition of potassium-containing minerals, either
indirectly by changing environmental pH or through chela-
tion (Etesami etal. 2017; Wei etal. 2020). The mechanism
by which bacteria dissolve potassium minerals is mainly:
by adjusting pH; acid hydrolysis in the area surrounding the
microorganism; by enhancing chelation of K-bound cations
(Meena etal. 2015).
Iron usually exists in the soil in insoluble forms, such
as carbonates, hydroxides, and oxides; therefore, most of
the iron cannot be absorbed by plants (Carroll and Moore
2018). Siderophores, which are small-molecule iron che-
lators widely distributed in microbial species, including
PGPR, convert unavailable ferric iron to usable ferrous
iron, an essential source of iron for plants (Saha etal. 2016).
Precisely, siderophores capture iron and transport it across
the cell membrane to the cytoplasm (Hesse etal. 2018;
Khan etal. 2018). Lipoproteins involved in iron transport
in Gram-positive Streptomyces and siderophore-binding
proteins (SBPs), are present in the cell membrane. Their
interaction with extracellular siderophores triggers a con-
formational change of the SBP-permease complex, allowing

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
Page 3 of 12 193
the translocation of iron-siderophore complex into the
cytoplasm (Wilson etal. 2016). There are as many as ten
types of siderophores in Streptomyces species: enterobactin
(Streptomyces tendae), fradiamine A (Streptomyces fradie),
pyochelin (Streptomyces scabies), ferrithiocin (Streptomy-
ces antibioticus), streptobactin and benarthin (Streptomy-
ces sp. YM5-799), coelichelin (Streptomyces coelicolor),
desferrioxamine B (Streptomyces coelicolor and Strepto-
myces pilosus), quinichelin (Streptomyces sp. MBT76),
and foroxymithine (Streptomyces nitrosporeus) (Terra etal.
2021). In addition, siderophores have broad potential appli-
cations in different research areas like agriculture and medi-
cal research. Streptomyces species are an essential source of
siderophores that can be utilized efficiently in other sectors.
Regulate plant hormone levels
Auxin can induce plant cell elongation and division and
plays an essential role in plant growth and development.
Interestingly, various microorganisms present in the rhizo-
sphere or in plants tissues can produce indole-3-acetic acid
(IAA), the most common auxin (Park etal. 2017). IAA is
mainly synthesized via five intermediates such as indole-
3-pyruvate (IPy), indole-3-acetamide (IAM), indole-3-ace-
tonitrile (IAN), tryptamine (TAM), and tryptophan side
chain oxidaze (TSO) (Patten etal. 2013; Rodrigues etal.
2016; Spaepen and Vanderleyden 2011). However, some
PGPR can oxidizes L-tryptophan to produce IPy, a reac-
tion catalyzed by proteins of the L-amino acid oxidase gene
cluster (Kudoyarova etal. 2019; Spaepen etal. 2007). Some
PGPR can also produce other kinds of auxins such as indole-
3-butyric acid and indole-3-acetaldehyde, that were shown to
affect plant growth (Oleńska etal. 2020). Auxins secreted by
bacteria stimulate the elongation of primary roots of plants
and at high concentrations promotes the formation of lateral
roots and adventitious roots and thus enhance the ability of
the plant to absorb minerals (Verbon and Liberman 2016).
Furthermore, IAA relaxes the cell walls of plant roots facili-
tating the secretion of root exudates that benefit to PGPR
growth (Massoud etal. 2018). The ability of Streptomyces to
secrete phytohormones stimulates its plant growth-promot-
ing activity. Streptomyces sp. CLV45 that was isolated from
Fabaceae rhizosphere is able to produce 398.53mg IAA per
gram cell and was shown to have a positive effect on soy-
bean growth (Horstmann etal. 2020). Streptomyces alfalfae
11F produces IAA and siderophore that effectively promote
the germination and growth of switchgrass seeds (Niu etal.
2022b). Some PGPR can also produce other phytohormones,
such as gibberellic acid and abscisic acid, and other hor-
mones that can promote plant growth through the stimula-
tion of natural plant defenses (Barka etal. 2016; Goudjal
etal. 2016; Olanrewaju and Babalola 2019). The processes
by which Streptomyces species promote plant growth are
diverse and their synergistic impacts are highly beneficial
for the plant (Fig.1).
Streptomyces species enhance plant
tolerance tobiotic stress
Induced systemic resistance (ISR) is a PGPR-mediated
stimulation of plants systemic resistance that reduces dam-
age caused by biotic stressors, such as fungal and bacte-
rial pathogens, nematodes, and insects (Pieterse etal. 2014;
Tonelli etal. 2020). This mechanism relies on the generation
of ISR-specific signals such as jasmonic acid or ethylene.
PGPR and actinobacteria can promote the upregulation of
the expression of ISR-related genes in plants to alter host
plant vulnerability and improve plant resistance against
the pathogenic elements (Ansari etal. 2020; Samaras etal.
2021).
For instance, Wang etal. (2021) isolated 58 actinomy-
cetes from the sugarcane rhizosphere, among which Strepto-
myces griseorubiginosus BTU6 that significantly enhanced
sugarcane smut resistance via the up-regulation of the
expression of the defense enzymes of the plant. However,
most Streptomyces enhance plants tolerance to pests and
diseases through the production of antibiotics (Han etal.
2021), volatile compounds (VOCs) (Jones and Elliot 2017)
or siderophores (Vijayabharathi etal. 2015).
Antibiotic andsecondary metabolites
Streptomyces isolated from various ecosystems around the
world have played a key role in the discovery of important
bioactive compounds, including antibiotics, antifungal
drugs and antiparasitic drugs useful to agriculture as well
as anticancer/antitumoral drugs and other bioactive second-
ary metabolites (Pham etal. 2019). Streptomyces contain
abundant secondary metabolic biosynthetic gene clusters.
With the development of genome sequencing methods and
bioinformatics technology, many analytical tools including
antiSMASH and PRISM have been used to predict biosyn-
thetic gene clusters and chemical structure of encoded prod-
ucts (Kalkreuter etal. 2020). A large number of genome
sequencing analysis showed that: most Streptomyces contain
dozens of secondary metabolite biosynthesis gene clusters,
the number of which far exceeds the types of compounds
currently isolated from Streptomyces (Pan etal. 2017; Ren
etal. 2020). This indicates that Streptomyces has a great
potential to synthesize new natural compounds. The explo-
ration and development of marine Streptomyces, especially
deep-sea Streptomyces resources, has not only expanded
the knowledge of marine Streptomyces diversity, but also
provided the possibility to obtain new metabolites and new

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
193 Page 4 of 12
biofunctional active substances (Yang etal. 2020). Indeed
macrocyclic tetralactones, such as avermectins, milbemycin,
piericidins, nanchangmycin, dianemycin, and meilingmycin,
biosynthesized by Streptomyces are highly effective to kill
worms, mites, and insects and are widely used in agricul-
ture (Amelia-Yap etal. 2022). Suárez-Moreno etal. (2019)
found that Streptomyces A20 can produce streptomycin D,
E, F to protect rice from bacterial pathogens. Actinomycin
D, isolated from Streptomyces sp. NEAU-HV9, has strong
antagonistic activity against Ralstonia solanacearum of
tomato (Ling etal. 2020).
Volatile organic compounds (VOCs)
In addition to antibiotics and hydrolases, Streptomyces
species produce several VOCs that directly or indirectly
stimulate plant growth. VOCs are low-molecular-weight
compounds that evaporate at room temperature and pres-
sure and can quickly diffuse through the atmosphere and
soil (Schulz-Bohm etal. 2017). VOCs released by micro-
organisms are complex and diverse, belonging to different
classes, including alkanes, hydrocarbons, alcohols, alde-
hydes, ketones, esters, phenols, heterocyclic compounds,
and benzene derivatives (Tilocca etal. 2020). Microbial
VOCs have multiple functions: they can inhibit the growth
of bacteria and fungi, promote or inhibit plant growth, trig-
ger ISR in plants, and attract other microorganisms, plants,
and animals (Liu and Brettell 2019). Abiotic soil conditions,
such as temperature, pH, moisture content, and soil texture,
can have significant effects on the production, composition,
and function of microbial VOCs (Han etal. 2018; Som etal.
2017). In addition, VOCs of Streptomyces play an important
role in the life cycle. For example, geosmin and 2-methyl-
isoborneol attract springtails to help Streptomyces spread
spores (Becher etal. 2020; York 2020). Geosmin can inter-
fere with Caenorhabditis elegans and avoid predation by
them (Zaroubi etal. 2022).
Siderophores
Bacteria with strong siderophore synthesis capacity are able
to survive under limited iron conditions (Khan etal. 2018;
Wang etal. 2020) and the ability of these bacteria to effi-
ciently capture trace amount of iron, limits the availability of
this indispensable element for the growth and reproduction
of plant pathogenic microorganisms limiting their detrimen-
tal impact on plant health.
Fig. 1 Systematic representation of Plant and actinobacteria (Strepto-
myces) interaction towards plant growth regulation below and above
grounds. Actinobacteria colonize in the rhizosphere, endosphere, and
phyllosphere and enhance soil fertility via nutrient stabilization and
transport. The antimicrobial property (antibiosis and mycoparasitism)
of actinobacteria protects plants from pathogens andupregulated the
plant defense against both abiotic and biotic stresses. Actinobacteria
application (via spray or soil inoculation) improves the metal uptake,
hydrolytic enzymes, phytohormones, osmolytes, and antioxidants.
SOD superoxide dismutase, CAT catalase (CAT), APX ascorbate per-
oxidase, MDA malondialdehyde, DHAR dehydroascorbate reductase,
GR glutathione reductase, GPX guaiacol peroxidase; Fe iron, Zn zinc,
P phosphorus, K potassium, VOC volatile organic compounds, HCN
hydrogen cyanide

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
Page 5 of 12 193
Recent studies on the improvement of plant tolerance to
biotic stress by Streptomyces are summarized in Table1.
Streptomyces species improve plant
tolerance toabiotic stress
PGPR can also induce systemic resistance to abiotic stress
by stimulating phytohormone and VOCs production, cal-
lose deposition and Ca2+ influx (Yu etal. 2022). For
instance, phytohormone production alters plant physiology
in response to abiotic stressors, such as drought and salt
stress (Sadiq etal. 2020). In contrast, VOCs produced by
PGPS species regulate genes involved in Na+ homeostasis
and protect plants from salt stress (Numan etal. 2018). In
addition, the production cytokinin and growth hormone or
of reactive oxygen species bursts or antioxidant enzymes can
mitigate abiotic stressors in plants (Kumar and Verma 2018).
Recent studies on the mitigation of plant abiotic stress by
Streptomyces are summarized in Table2.
Drought andsalinity stress
Drought and salinity are important ecological factors that
affect crop yield. They cause plant tissue damage by alter-
ing the water balance, interfering with ion homeostasis and
metabolism, and producing reactive oxygen species (ROS).
Under stressfull conditions, PGPRs stimulate plant hormone
synthesis, inhibit the growth of plant pathogens, and induce
systemic plant tolerance (Sathya etal. 2017). The activity
of endogenous plant hormones regulating plant metabolism
changes accordingly during induced systemic tolerance by
different environmental factors. Plant metabolic pathways
are upregulated or downregulated at different developmental
stages to adapt to water and salinity conditions that affect
plant growth (Kumar and Verma 2018). Similarly, endog-
enous phytohormones regulate plant growth to adapt to
environmental changes in a complex way. A single phyto-
hormone can regulate multiple developmental processes,
whereas a single process may require the synergistic action
of various proteins or enzymes (Großkinsky etal. 2016;
Verbon and Liberman 2016). In drought, salt stress, high
temperature, and other causes of plant endostasis disorders,
Streptomyces can secrete extracellular polysaccharides and
osmoregulators to alleviate osmotic disorders and water loss
to maintain the stability of the internal environment (Niu
etal. 2022a). For instance, the induction of stomatal regula-
tion to regulate plant water content is of crucial importance
in these conditions (Yu etal. 2022). Hence, PGPRs can ben-
efit host plants by mitigating abiotic stressors, such as heat,
cold, drought, and nutrient deficiencies, thereby reducing
their adverse effects on plant health and fitness (Atkinson
and Urwin 2012; Wang etal. 2019).
An important mechanism by which Streptomyces spe-
cies improve plant tolerance to abiotic stress is their abil-
ity to hydrolyze 1-aminocyclopropane-1-carboxylic acid
(ACC), the precursor of ethylene in plants, to ammonia and
α-ketobutyric acid by a specific deaminase (Glick 2014).
This enzyme reduces the level of plant endogenous ACC
in response to stress and thus ethylene generation, improv-
ing plant adaptation to the environment (Vejan etal. 2016).
Ethylene is widely involved in plant growth and develop-
ment, and plays an important role in leaf senescence and
abscission, as well as in plant response to stress (Arraes etal.
2015). Streptomyces can also promote the growth of wheat,
maize, chickpeas, and soybeans under salt stress (Akbari
etal. 2020; Gao etal. 2022; Nozari etal. 2021).
Metal stress
In recent years, phytoremediation technology has become
a hot topic in overcoming soil heavy metal contamination
because of its low cost and need for environmental safety.
However, application of these technologies is limited due
to small biomass yields due to limited tolerance of plants to
metals (Behera etal. 2022).
As a new and effective remediation method,
plant–microbe remediation compensates for many short-
comings of single phytoremediation approaches. Microor-
ganisms can not only enhance the heavy metal tolerance of
plants, promote growth of plant root systems leading to an
increase of the absorption of soil nutrients including metals
and thus increasing biomass. They thus effectively cooper-
ate with plants to remove heavy metal ions from the soil,
thereby achieving rapid soil restoration (Ahsan etal. 2017;
Vaid etal. 2022). Furthermore, PGPRs species enhance
plant tolerance to metal stress by regulating the expression
of antioxidant enzymes and osmotic regulators and doing
so enhances their phytoremediation capacity (Bhanse etal.
2022). In addition, Streptomyces strains have great applica-
tion potential for the degradation of pesticide residues in soil
(Briceño etal. 2018).
Pathogenicity ofStreptomyces
Most Streptomyces are soil-dwelling saprophytic bacteria
with rich diversity. Only a few species are plant pathogens,
among which more than 20 species cause potato scab and
are widely distributed in the main potato-producing areas,
and that can also infect other crops such as carrots, radishes,
sugar beets, peanuts, and sweet potatoes (Ismail etal. 2020;
Mora-Romero etal. 2022). The production of various phy-
totoxins medicates Streptomyces-induced potato scabs. In
addition to the most common thaxtomins (Deflandre etal.
2022), other pathogenic toxins and toxic metabolites have

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
193 Page 6 of 12
Table 1 Role and underlying mechanism of Streptomyces in plants under different biotic stressors
Strain Plant Disease Pathogen or insect References
Streptomyces sp. A20, 5.1,
7.1
Rice Bacterial panicle blight Burkholderia glumae Suárez-Moreno etal. (2019)
Streptomyces sp. N2 Wheat Wheat take-all Gaeumannomyces graminis
var. tritici Worsley etal. (2020)
Streptomyces sp. MR14 Tomato Fusarium wilt in tomato Fusarium oxysporum f.sp.
lycopersici Kaur etal. (2019)
Streptomyces cellulosae
Actino 48
Tobacco Tobacco mosaic virus Tobamovirus Abo-Zaid etal. (2020)
Streptomyces sp. NEAU-
S7GS2
Soybean Sclerotinia stem rot disease Sclerotinia sclerotiorum Liu etal. (2019)
Streptomyces sp. 5–10 Curculigo capitulata Fusarium wilt of banana Fusarium oxysporum f. sp.
cubense Yun etal. (2021)
Streptomyces griseus CAI-24,
CAI-121, CAI-127
Streptomyces africanus
KAI-32
Streptomyces coelicolor
KAI-90
Chickpea Fusarium wilt Fusarium oxysporum f. sp.
ciceri Ankati etal. (2021)
Streptomyces ovatisporus
LC597360
Tomato Tomato mosaic disease Tomato mosaic virus Taha etal. (2021)
Streptomyces morookaensis
Sm4-1986
Banana Fusarium wilt of banana Fusarium oxysporum f. sp.
cubense Zhu etal. (2021)
Streptomyces shenzhenesis
TKSC3
Streptomyces sp. SS8
Rice Bacterial leaf streak disease Xanthomonas oryzae pv.
oryzicola Hata etal. (2021)
Streptomyces griseorubigino-
sus BTU6
Sugarcane Sugarcane smut Sporisorium scitamineum Wang etal. (2021)
Streptomyces albus CAI-17,
KAI-27
Streptomyces griseus KAI-26,
MMA-32
Streptomyces cavourensis
SAI-13
Sorghum Charcoal rot disease Macrophomina phaseolina Gopalakrishnan etal. (2021)
Streptomyces avermitillis
PAN Act2
Streptomyces cinnamonesis
PAN Act3
Streptomyces canus PAN
Act5
Pomegranate Wilt disease Cerotocystis fimbriata,
Fusarium oxysporum,
Macrophomina sp., and
Sclerotium sp.
Panneerselvam etal. (2021)
Streptomyces sp. SP5 Tomato Early blight Alternaria solani Devi etal. (2021)
Streptomyces panaciradicis
ARK 13,
Streptomyces tritolerans
ARK 17
Streptomyces recifensis ARK
63
Streptomyces tendae ARK 91
Streptomyces manipurensis
ARK 94
Soybean Root rot disease Fusarium oxysporum Sari etal. (2021)
Streptomyces strain H2, H3 Tomato Root rot Pythium aphanidermatum Hassanisaadi etal. (2021)
Streptomyces griseocarneus
R132
Pepper Anthracnose Colletotrichum gloeospori-
oides Liotti etal. (2019)
Streptomyces globisporus
Act7 and Act28
Cotton Verticillium wilt in cotton Verticillium dahliae Chen etal. (2021)

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
Page 7 of 12 193
Table 2 Role and underlying mechanism of Streptomyces in plants under different abiotic stressors
MDA malondialdehyde, APX ascorbate peroxidase, SOD superoxide dismutase, Na+ sodium ion, H2O2 hydrogen peroxide, RuBisCO ribulose-1,5-bisphosphate carboxylase/oxygenase
Strain Plant Mechanism Stressor References
Streptomyces sp. KLBMP5084 Tomato Effectively increase antioxidant enzyme activity, soluble
sugar, and proline content in leaves and stems, and
reduce MDA content
Salt Gong etal. (2020)
Streptomyces variabilis 4NC
Streptomyces fradiae 8PK
Stevia Accumulation of RuBisCO large subunit protein Salt Tolba etal. (2019)
Streptomyces sp. C-2012 Wheat Increases chlorophyll and carotenoids and reduces Na+
concentration, affects APX and SOD activity
Salt Akbari etal. (2020)
Streptomyces sp. CLV97, CLV179 Maize Significantly promotes the growth of corn plants Salt Nozari etal. (2021)
Streptomyces sp. X52 Maize Regulation of inter-root bacterial communities to improve
plant growth in saline soils
Salt Peng etal. (2021)
Streptomyces pactum Act12 Wheat Induction of abscisic acid accumulation and upregulation
of drought resistance-related gene expression to enhance
plant osmoregulation and antioxidant capacity
Drought Li etal. (2020)
Streptomyces pseudovenezuelae MG547870 Maize Promotes plant growth and reduces the effects of drought
stress
Drought Chukwuneme etal. (2020)
Streptomyces laurentii EU-LWT3-69 Great millet Increases accumulation of glycine betaine, proline, sugars,
chlorophyll content and reduces lipid peroxidation
Drought Kour etal. (2020)
Streptomyces sp. Ac3 Maize Significantly alleviated drought stress-induced increases in
H2O2, lipid peroxidation and protein oxidation (protein
carbonyls). It also increased antioxidants (total ascor-
bate, glutathione, and tocopherols)
Drought Warrad etal. (2020)
Streptomyces albidoflavus OsiLf-2 Rice Enhancement of rice osmoregulation by increasing proline
content (250.3% and 49.4%, respectively) and soluble
sugar (20.9% and 49.4%, respectively) in rice under
drought and salinity conditions
Drought, salt Niu etal. (2022a)
Streptomyces pactum Act12 Potherb mustard Shoot fresh weight, chlorophyll a and chlorophyll b
decrease
Cadmium and zinc Guo etal. (2019)
Streptomyces pactum Act 12 Wheat Decreased peroxidase, catalase, superoxide dismutase, and
lipid peroxidation
Contaminated mining soils Ali etal. (2021)
Streptomyces sp. NRC21696 Maize Significant increases in the germination, plant fresh and
dry weights, lengths of leaf; root and cob, and photosyn-
thetic pigments
Chromium and arsenic AL-Huqail and El-Bondkly (2021)
Streptomyces sp. Hlh1 Maize Degradation of phenanthrene, pyrene, and anthracene Petroleum hydrocarbons Baoune etal. (2019)
Streptomyces sp. Z38 Maize Improved lindane dissipation, decreased MDA concentra-
tion, and increased SOD
Cadmium, lindane Solá etal. (2021)
Streptomyces rapamycinicus K5PN1 Strep-
tomyces cyaneus 11-10SHTh
Chlorophytum
comosum (Thunb.)
Jacques
Stimulates plant growth and uptake of cadmium Cadmium Junpradit etal. (2021)

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
193 Page 8 of 12
been identified, including concanamycins, COR-like phyto-
toxins, borrelidin, and unidentified toxic metabolites (Bown
etal. 2017; Cheng etal. 2019; Lapaz etal. 2019). In recent
years, with the increase in human demand for potatoes, their
cultivation area has gradually expanded, and continuous
cropping for many years in the main production areas has
led to a yearly increase in the degree of potato scab damage.
Therefore, research on the diversity, pathogenic toxins, and
control of disease-causing Streptomyces deserves attention.
Conclusion andprospect
Streptomyces activate plant defense mechanisms to reduce
oxidative stress and other stresses caused by various environ-
mental biotic or abiotic stresses (Wang etal. 2019). Strep-
tomyces also secrete antibiotics and siderophores to limit
growth of soil-born phytopathogens and preserve plant
health. They also synthetize phytohormones to promote
nutrient cycling to remedy nutrient imbalance occurring in
stressful conditions. Numerous studies indicate that Strep-
tomyces strains can contribute significantly to plant abiotic
stress alleviation but the nature of the cellular mechanisms
involved in these processes remains to be elucidated. Even
if PGPRs species have various functions and good applica-
tion prospects, there are few commercial products available
based on Streptomyces strains and their biologically active
molecules. Indeed, most studies remain at a research stage
and few studies have been conducted in field experiments.
Moreover, the plant-promoting effects of Streptomyces are
likely to be multi-factorial and a comprehensive under-
standing of the underlying mechanisms are far reached yet.
Indeed, in soil, Streptomyces are part of an interactive micro-
biome network and it is essential to understand the contribu-
tion of the interaction of Streptomyces with the rhizospheric
microbiome to relieve plant stress.
Author contributions PF and WZ wrote the main manuscript text and
MKS prepared figures1. WZ and MKS reviewed the manuscript.
Funding The present study was supported by the National Natural Sci-
ence Foundation of China (32101836), Guangxi Natural Science Foun-
dation (CN) (2022GXNSFBA035542), the Scientific Startup Founda-
tion for Doctors of Yulin Normal University (CN) (G2020ZK13).
Declarations
Conflict of interest The authors declare no competing interests.
References
Abo-Zaid GA, Matar SM, Abdelkhalek A (2020) Induction of plant
resistance against tobacco mosaic virus using the biocontrol
agent Streptomyces cellulosae isolate Actino 48. Agronomy
10:1620
Ahsan MT, Najam-ul-Haq M, Idrees M, Ullah I, Afzal M (2017) Bacte-
rial endophytes enhance phytostabilization in soils contaminated
with uranium and lead. Int J Phytorem 19:937–946
Akbari A, Gharanjik S, Koobaz P, Sadeghi A (2020) Plant growth pro-
moting Streptomyces strains are selectively interacting with the
wheat cultivars especially in saline conditions. Heliyon 6:e03675
AL-Huqail A, El-Bondkly A (2021) Improvement of Zea mays L.
growth parameters under chromium and arsenic stress by the
heavy metal-resistant Streptomyces sp. NRC21696. Int J Environ
Sci Technol 19:5301–5322
Ali A, Guo D, Li Y, Shaheen SM, Wahid F, Antoniadis V, Abdelrah-
man H, Al-Solaimani SG, Li R, Tsang DC (2021) Streptomyces
pactum addition to contaminated mining soils improved soil
quality and enhanced metals phytoextraction by wheat in a green
remediation trial. Chemosphere 273:129692
Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubi-
lization and its potential for use in sustainable agriculture. Front
Microbiol 8:971
Amelia-Yap ZH, Azman AS, AbuBakar S, Low VL (2022) Strepto-
myces derivatives as an insecticide: current perspectives, chal-
lenges and future research needs for mosquito control. Acta Trop
229:106381
Ankati S, Srinivas V, Pratyusha S, Gopalakrishnan S (2021) Streptomy-
ces consortia-mediated plant defense against Fusarium wilt and
plant growth-promotion in chickpea. Microb Pathog 157:104961
Ansari WA, Krishna R, Zeyad MT, Singh S, Yadav A (2020) Endo-
phytic actinomycetes-mediated modulation of defense and sys-
temic resistance confers host plant fitness under biotic stress
conditions. In: Singh R, Manchanda G, Maurya I, Wei Y (eds)
Microbial versatility in varied environments. Springer, Singapore
Arraes FBM, Beneventi MA, Lisei de Sa ME, Paixao JFR, Albuquer-
que EVS, Marin SRR, Purgatto E, Nepomuceno AL, Grossi-de-
Sa MF (2015) Implications of ethylene biosynthesis and signal-
ing in soybean drought stress tolerance. BMC Plant Biol 15:213
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abi-
otic stresses: from genes to the field. J Exp Bot 63:3523–3543
Baoune H, Aparicio JD, Pucci G, Ould El Hadj-Khelil A, Polti MA
(2019) Bioremediation of petroleum-contaminated soils using
Streptomyces sp. Hlh1. J Soils Sediments 19:2222–2230
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk
H-P, Clément C, Ouhdouch Y, van Wezel GP (2016) Taxonomy,
physiology, and natural products of Actinobacteria. Microbiol
Mol Biol Rev 80:1–43
Basu A, Prasad P, Das SN, Kalam S, Sayyed R, Reddy M, El Enshasy
H (2021) Plant growth promoting rhizobacteria (PGPR) as green
bioinoculants: recent developments, constraints, and prospects.
Sustainability 13:1140
Becher PG, Verschut V, Bibb MJ, Bush MJ, Molnár BP, Barane E,
Al-Bassam MM, Chandra G, Song L, Challis GL (2020) Devel-
opmentally regulated volatiles geosmin and 2-methylisoborneol
attract a soil arthropod to Streptomyces bacteria promoting spore
dispersal. Nat Microbiol 5:821–829
Behera HT, Mojumdar A, Ray L (2022) Biology, genetic aspects
and oxidative stress response of actinobacteria and strategies
for bioremediation of toxic metals. In: S Das, HR Dash (eds)
Microbial Biodegradation and Bioremediation (Second Edition).
Elsevier
Bhanse P, Kumar M, Singh L, Awasthi MK, Qureshi A (2022)
Role of plant growth-promoting rhizobacteria in boosting the

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
Page 9 of 12 193
phytoremediation of stressed soils: opportunities, challenges, and
prospects. Chemosphere 303:134954
Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers
function as key player in sustainable agriculture by improving
soil fertility, plant tolerance and crop productivity. Microb Cell
Fact 13:66
Bown L, Li Y, Berrué F, Verhoeven JT, Dufour SC, Bignell DR (2017)
Coronafacoyl phytotoxin biosynthesis and evolution in the com-
mon scab pathogen Streptomyces scabiei. Appl Environ Micro-
biol 83:e01169-e1117
Briceño G, Fuentes MS, Saez JM, Diez MC, Benimeli CS (2018) Strep-
tomyces genus as biotechnological tool for pesticide degradation
in polluted systems. Crit Rev Environ Sci Technol 48:773–805
Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root
exudation of primary metabolites: mechanisms and their roles in
plant responses to environmental stimuli. Front Plant Sci 10:157
Carroll CS, Moore MM (2018) Ironing out siderophore biosynthesis: a
review of non-ribosomal peptide synthetase (NRPS)-independent
siderophore synthetases. Crit Rev Biochem Mol Biol 53:356–381
Castro JF, Razmilic V, Gomez-Escribano JP, Andrews B, Asenjo J,
Bibb M (2018) The ‘gifted’ actinomycete Streptomyces leeuwen-
hoekii. Antonie Van Leeuwenhoek 111:1433–1448
Chen Q, Bai S, Zhang T, Duan C, Zhao J, Xue Q, Li Y (2021) Effects of
seed-coating preparations of living Streptomyces globisporus on
plant growth promotion and disease control against Verticillium
wilt in cotton. Sustainability 13:6001
Cheng Z, Bown L, Piercey B, Bignell DR (2019) Positive and negative
regulation of the virulence-associated coronafacoyl phytotoxin
in the potato common scab pathogen Streptomyces scabies. Mol
Plant-Microbe Interact 32:1348–1359
Chukwuneme CF, Babalola OO, Kutu FR, Ojuederie OB (2020) Char-
acterization of actinomycetes isolates for plant growth promoting
traits and their effects on drought tolerance in maize. J Plant
Interact 15:93–105
da-Silva JR, Alexandre A, Brígido C, Oliveira S (2017) Can stress
response genes be used to improve the symbiotic performance
of rhizobia? AIMS Microbiol 3:365–382
Dahal B, NandaKafle G, Perkins L, Brözel VS (2017) Diversity of
free-living nitrogen fixing Streptomyces in soils of the badlands
of South Dakota. Microbiol Res 195:31–39
Deflandre B, Stulanovic N, Planckaert S, Anderssen S, Bonometti B,
Karim L, Coppieters W, Devreese B, Rigali S (2022) The viru-
lome of Streptomyces scabiei in response to cello-oligosaccha-
ride elicitors. Microbial Genomics 8:000760
Devi S, Sharma M, kumari Manhas R (2021) Investigating the plant
growth promoting and biocontrol potentiality of endophytic
Streptomyces sp. SP5 against early blight in tomato seedling.
Research Square: PPR356488
Devine KM (2018) Activation of the PhoPR-mediated response to
phosphate limitation is regulated by wall teichoic acid metabo-
lism in Bacillus subtilis. Front Microbiol 9:2678
Etesami H, Emami S, Alikhani HA (2017) Potassium solubilizing bac-
teria (KSB): mechanisms, promotion of plant growth, and future
prospects - a review. J Soil Sci Plant Nut 17:897–911
Gao Y, Han Y, Li X, Li M, Wang C, Li Z, Wang Y, Wang W (2022)
A salt-tolerant Streptomyces paradoxus D2–8 from rhizosphere
soil of Phragmites communis augments soybean tolerance to soda
saline-alkali stress. Pol J Microbiol 71:43–53
Glick BR (2014) Bacteria with ACC deaminase can promote plant
growth and help to feed the world. Microbiol Res 169:30–39
Gong Y, Chen L-J, Pan S-Y, Li X-W, Xu M-J, Zhang C-M, Xing K, Qin
S (2020) Antifungal potential evaluation and alleviation of salt
stress in tomato seedlings by a halotolerant plant growth-promot-
ing actinomycete Streptomyces sp. KLBMP5084. Rhizosphere 16
Gopalakrishnan S, Srinivas V, Naresh N, Pratyusha S, Ankati S,
Madhuprakash J, Govindaraj M, Sharma R (2021) Deciphering
the antagonistic effect of Streptomyces spp and host-plant
resistance induction against charcoal rot of sorghum. Planta
253:57
Goudjal Y, Zamoum M, Meklat A, Sabaou N, Mathieu F, Zitouni
A (2016) Plant-growth-promoting potential of endosymbiotic
actinobacteria isolated from sand truffles (Terfezia leonis Tul.)
of the Algerian Sahara. Ann Microbiol 66:91–100
Großkinsky DK, Tafner R, Moreno MV, Stenglein SA, García de
Salamone IE, Nelson LM, Novák O, Strnad M, van der Graaff
E, Roitsch T (2016) Cytokinin production by Pseudomonas
fluorescens G20–18 determines biocontrol activity against
Pseudomonas syringae in Arabidopsis. Sci Rep 6:23310
Guo D, Ren C, Ali A, Du J, Zhang Z, Li R, Zhang Z (2019) Strepto-
myces pactum and sulfur mediated the antioxidant enzymes in
plant and phytoextraction of potentially toxic elements from a
smelter-contaminated soils. Environ Pollut 251:37–44
Hamdali H, Lebrihi A, Monje MC, Benharref A, Hafidi M, Ouh-
douch Y, Virolle MJ (2021) A molecule of the viridomycin
family originating from a Streptomyces griseus-related strain
has the ability to solubilize rock phosphate and to inhibit
microbial growth. Antibiotics 10:72
Han D, Yan D, Wang Q, Fang W, Wang X, Li J, Wang D, Li Y, Ouy-
ang C, Cao A (2018) Effects of soil type, temperature, mois-
ture, application dose, fertilizer, and organic amendments on
chemical properties and biodegradation of dimethyl disulfide
in soil. Land Degrad Dev 29:4282–4290
Han X, Wang J, Liu L, Shen F, Meng Q, Li X, Li Y, Liu D (2021)
Identification and predictions regarding the biosynthesis
pathway of polyene macrolides produced by Streptomy-
ces roseoflavus Men-myco-93-63. Appl Environ Microbiol
87:e03157-e3120
Hassanisaadi M, Shahidi Bonjar GH, Hosseinipour A, Abdolshahi R,
Ait Barka E, Saadoun I (2021) Biological control of Pythium
aphanidermatum, the causal agent of tomato root rot by two
Streptomyces root symbionts. Agronomy 11:846
Ha-Tran DM, Nguyen TTM, Hung S-H, Huang E, Huang C-C (2021)
Roles of plant growth-promoting rhizobacteria (PGPR) in stimu-
lating salinity stress defense in plants: a review. Int J Mol Sci
22:3154
Hata EM, Yusof MT, Zulperi D (2021) Induction of systemic resistance
against bacterial leaf streak disease and growth promotion in rice
plant by Streptomyces shenzhenesis TKSC3 and Streptomyces sp.
SS8. Plant Pathol J 37:173–181
Hesse E, O’Brien S, Tromas N, Bayer F, Luján AM, van Veen EM,
Hodgson DJ, Buckling A (2018) Ecological selection of sidero-
phore-producing microbial taxa in response to heavy metal con-
tamination. Ecol Lett 21:117–127
Horstmann JL, Dias MP, Ortolan F, Medina-Silva R, Astarita LV,
Santarém ER (2020) Streptomyces sp. CLV45 from Fabaceae
rhizosphere benefits growth of soybean plants. Braz J Microbiol
51:1861–1871
Ismail S, Jiang B, Nasimi Z, Inam-ul-Haq M, Yamamoto N, Danso
Ofori A, Khan N, Arshad M, Abbas K, Zheng A (2020) Inves-
tigation of Streptomyces scabies causing potato scab by various
detection techniques, its pathogenicity and determination of host-
disease resistance in potato germplasm. Pathogens 9:760
Jones SE, Elliot MA (2017) Streptomyces exploration: competition,
volatile communication and new bacterial behaviours. Trends
Microbiol 25:522–531
Junpradit C, Thooppeng P, Duangmal K, Prapagdee B (2021) Influ-
ence of cadmium-resistant Streptomycetes on plant growth and
cadmium uptake by Chlorophytum comosum (Thunb.) Jacques.
Environ Sci Pollut R 28:39398–39408
Kalkreuter E, Pan G, Cepeda AJ, Shen B (2020) Targeting bacterial
genomes for natural product discovery. Trends Pharmacol Sci
41:13–26

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
193 Page 10 of 12
Kamaei R, Faramarzi F, Parsa M, Jahan M (2019) The effects of biolog-
ical, chemical, and organic fertilizers application on root growth
features and grain yield of Sorghum. J Plant Nutr 42:2221–2233
Kaur T, Rani R, Manhas RK (2019) Biocontrol and plant growth pro-
moting potential of phylogenetically new Streptomyces sp. MR14
of rhizospheric origin. AMB Express 9:125
Khan A, Singh P, Srivastava A (2018) Synthesis, nature and utility of
universal iron chelator—Siderophore: a review. Microbiol Res
212:103–111
Korenblum E, Massalha H, Aharoni A (2022) Plant–microbe interac-
tions in the rhizosphere via a circular metabolic economy. Plant
Cell 163
Kour D, Rana KL, Kaur T, Sheikh I, Yadav AN, Kumar V, Dhaliwal
HS, Saxena AK (2020) Microbe-mediated alleviation of drought
stress and acquisition of phosphorus in great millet (Sorghum
bicolour L.) by drought-adaptive and phosphorus-solubilizing
microbes. Biocatal Agric Biotechnol 23:101–501
Kudoyarova G, Arkhipova T, Korshunova T, Bakaeva M, Loginov
O, Dodd IC (2019) Phytohormone mediation of interactions
between plants and non-symbiotic growth promoting bacteria
under edaphic stresses. Front Plant Sci 10:1368
Kumar A, Verma JP (2018) Does plant-microbe interaction confer
stress tolerance in plants: a review? Microbiol Res 207:41–52
Lapaz MI, López A, Huguet-Tapia JC, Pérez-Baldassari MF, Igle-
sias C, Loria R, Moyna G, Pianzzola MJ (2019) Isolation and
structural characterization of a non-diketopiperazine phytotoxin
from a potato pathogenic Streptomyces strain. Nat Prod Res
33:2951–2957
Law JW-F, Tan K-X, Wong SH, Ab Mutalib N-S, Lee L-H (2018)
Taxonomic and characterization methods of Streptomyces: a
review. Prog Microbes Mol Biol 1:a0000009
Li H, Guo Q, Jing Y, Liu Z, Zheng Z, Sun Y, Xue Q, Lai H (2020)
Application of Streptomyces pactum Act12 enhances drought
resistance in wheat. J Plant Growth Regul 39:122–132
Ling L, Han X, Li X, Zhang X, Wang H, Zhang L, Cao P, Wu Y, Wang
X, Zhao J (2020) A Streptomyces sp. NEAU-HV9: Isolation,
identification, and potential as a biocontrol agent against Ral-
stonia solanacearum of tomato plants. Microorganisms 8:351
Liotti RG, da Silva Figueiredo MI, Soares MA (2019) Streptomyces
griseocarneus R132 controls phytopathogens and promotes
growth of pepper (Capsicum annuum). Biol Control 138:104065
Liu H, Brettell LE (2019) Plant defense by VOC-induced microbial
priming. Trends Plant Sci 24:187–189
Liu D, Yan R, Fu Y, Wang X, Zhang J, Xiang W (2019) Antifungal,
plant growth-promoting, and genomic properties of an endo-
phytic actinobacterium Streptomyces sp. NEAU-S7GS2. Front
Microbiol 10:2077
Lv C, Gu T, Ma R, Yao W, Huang Y, Gu J, Zhao G (2021) Biochemical
characterization of a GH19 chitinase from Streptomyces alfalfae
and its applications in crystalline chitin conversion and biocon-
trol. Int J Biol Macromol 167:193–201
MacKellar D, Lieber L, Norman JS, Bolger A, Tobin C, Murray JW,
Oksaksin M, Chang RL, Ford TJ, Nguyen PQ (2016) Streptomy-
ces thermoautotrophicus does not fix nitrogen. Sci Rep 6:1–12
Massoud MB, Sakouhi L, Karmous I, Zhu Y, El Ferjani E, Sheehan D,
Chaoui A (2018) Protective role of exogenous phytohormones on
redox status in pea seedlings under copper stress. J Plant Physiol
221:51–61
Maurer D, Malique F, Alfarraj S, Albasher G, Horn MA, Butterbach-
Bahl K, Dannenmann M, Rennenberg H (2021) Interactive regu-
lation of root exudation and rhizosphere denitrification by plant
metabolite content and soil properties. Plant Soil 467:107–127
Meena VS, Maurya BR, Verma JP, Aeron A, Kumar A, Kim K, Bajpai
VK (2015) Potassium solubilizing rhizobacteria (KSR): isola-
tion, identification, and K-release dynamics from waste mica.
Ecol Eng 81:340–347
Meschke H, Schrempf H (2010) Streptomyces lividans inhibits the pro-
liferation of the fungus Verticillium dahliae on seeds and roots of
Arabidopsis thaliana. Microb Biotechnol 3:428–443
Mora-Romero GA, Félix-Gastélum R, Bomberger RA, Romero-Urías
C, Tanaka K (2022) Common potato disease symptoms: ambi-
guity of symptom-based identification of causal pathogens
and value of on-site molecular diagnostics. J Gen Plant Pathol
88:89–104
Niu S, Gao Y, Zi H, Liu Y, Liu X, Xiong X, Yao Q, Qin Z, Chen N,
Guo L (2022a) The osmolyte-producing endophyte Streptomyces
albidoflavus OsiLf-2 induces drought and salt tolerance in rice
via a multi-level mechanism. Crop J 10:375–386
Niu Z, Yue Y, Su D, Ma S, Hu L, Hou X, Zhang T, Dong D, Zhang D,
Lu C (2022b) The characterization of Streptomyces alfalfae strain
11F and its effect on seed germination and growth promotion in
switchgrass. Biomass Bioenerg 158:106360
Nozari RM, Ortolan F, Astarita LV, Santarém ER (2021) Streptomy-
ces spp. enhance vegetative growth of maize plants under saline
stress. Braz J Microbiol 52:1371–1383
Numan M, Bashir S, Khan Y, Mumtaz R, Shinwari ZK, Khan AL,
Khan A, Ahmed A-H (2018) Plant growth promoting bacteria
as an alternative strategy for salt tolerance in plants: a review.
Microbiol Res 209:21–32
Ochi K (2017) Insights into microbial cryptic gene activation and strain
improvement: principle, application and technical aspects. J
Antibiot 70:25–40
Olanrewaju OS, Babalola OO (2019) Streptomyces: implications and
interactions in plant growth promotion. Appl Microbiol Biot
103:1179–1188
Olanrewaju OS, Ayangbenro AS, Glick BR, Babalola OO (2019) Plant
health: feedback effect of root exudates-rhizobiome interactions.
Appl Microbiol Biot 103:1155–1166
Oleńska E, Małek W, Wójcik M, Swiecicka I, Thijs S, Vangronsveld
J (2020) Beneficial features of plant growth-promoting rhizo-
bacteria for improving plant growth and health in challenging
conditions: a methodical review. Sci Total Environ 743:140682
Pan G, Xu Z, Guo Z, Hindra MM, Yang D, Zhou H, Gansemans Y,
Zhu X, Huang Y (2017) Discovery of the leinamycin family of
natural products by mining actinobacterial genomes. Proc Natl
Acad Sci USA 114:E11131–E11140
Panneerselvam P, Selvakumar G, Ganeshamurthy A, Mitra D, Senapati
A (2021) Enhancing pomegranate (Punica granatum L.) plant
health through the intervention of a Streptomyces consortium.
Biocontrol Sci Technol 31:430–442
Park S-H, Elhiti M, Wang H, Xu A, Brown D, Wang A (2017) Adventi-
tious root formation of invitro peach shoots is regulated by auxin
and ethylene. Sci Hortic 226:250–260
Patten CL, Blakney AJ, Coulson TJ (2013) Activity, distribution and
function of indole-3-acetic acid biosynthetic pathways in bacte-
ria. Crit Rev Microbiol 39:395–415
Peng J, Ma J, Wei X, Zhang C, Jia N, Wang X, Wang ET, Hu D, Wang
Z (2021) Accumulation of beneficial bacteria in the rhizosphere
of maize (Zea mays L.) grown in a saline soil in responding
to a consortium of plant growth promoting rhizobacteria. Ann
Microbiol 71:1–12
Pham JV, Yilma MA, Feliz A, Majid MT, Maffetone N, Walker JR,
Kim E, Cho HJ, Reynolds JM, Song MC (2019) A review of the
microbial production of bioactive natural products and biologics.
Front Microbiol 10:1404
Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC,
Bakker PA (2014) Induced systemic resistance by beneficial
microbes. Annu Rev Phytopathol 52:347–375
Pramanik K, Mandal S, Banerjee S, Ghosh A, Maiti TK, Mandal NC
(2021) Unraveling the heavy metal resistance and biocontrol
potential of Pseudomonas sp. K32 strain facilitating rice seedling
growth under Cd stress. Chemosphere 274

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
Page 11 of 12 193
Quinn GA, Banat AM, Abdelhameed AM, Banat IM (2020) Strepto-
myces from traditional medicine: sources of new innovations in
antibiotic discovery. J Med Microbiol 69:1040–1048
Ren H, Shi C, Zhao H (2020) Computational tools for discovering
and engineering natural product biosynthetic pathways. iScience
23:100795
Ribbe M, Gadkari D, Meyer O (1997) N2 fixation by Streptomyces
thermoautotrophicus involves a molybdenum-Dinitrogenase
and a manganese-Superoxide oxidoreductase that couple N2Re-
duction to the oxidation of superoxide produced from O2 by a
molybdenum-CO dehydrogenase. J Biol Chem 272:26627–26633
Rodrigues EP, Soares CdP, Galvão PG, Imada EL, Simões-Araújo JL,
Rouws LF, Oliveira ALd, Vidal MS, Baldani JI (2016) Identifi-
cation of genes involved in indole-3-acetic acid biosynthesis by
Gluconacetobacter diazotrophicus PAL5 strain using transposon
mutagenesis. Front Microbiol 7:1572
Romero-Rodríguez A, Maldonado-Carmona N, Ruiz-Villafán B, Koi-
rala N, Rocha D, Sánchez S (2018) Interplay between carbon,
nitrogen and phosphate utilization in the control of secondary
metabolite production in Streptomyces. Antonie Van Leeuwen-
hoek 111:761–781
Sadiq Y, Zaid A, Khan MMA (2020) Adaptive Physiological Responses
of Plants under Abiotic Stresses: Role of Phytohormones. In: M
Hasanuzzaman (ed) Plant ecophysiology and adaptation under
climate change: mechanisms and perspectives I: general conse-
quences and plant responses. Springer, Singapore
Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P
(2016) Microbial siderophores and their potential applications:
a review. Environ Sci Pollut R 23:3984–3999
Samaras A, Roumeliotis E, Ntasiou P, Karaoglanidis G (2021) Bacillus
subtilis MBI600 promotes growth of tomato plants and induces
systemic resistance contributing to the control of soilborne path-
ogens. Plants 10:1113
Sari M, Nawangsih AA, Wahyudi AT (2021) Rhizosphere Streptomyces
formulas as the biological control agent of phytopathogenic fungi
Fusarium oxysporum and plant growth promoter of soybean. Bio-
diversitas J Biol Divers 22:3015–3023
Sathya A, Vijayabharathi R, Gopalakrishnan S (2017) Plant growth-
promoting actinobacteria: a new strategy for enhancing sustaina-
ble production and protection of grain legumes. 3. Biotech 7:102
Schrempf H (2001) Recognition and degradation of chitin by strepto-
mycetes. Antonie Van Leeuwenhoek 79:285–289
Schrempf H (2017) Elucidating biochemical features and biological
roles of Streptomyces proteins recognizing crystalline chitin-
and cellulose-types and their soluble derivatives. Carbohyd Res
448:220–226
Schulz-Bohm K, Martín-Sánchez L, Garbeva P (2017) Microbial vola-
tiles: small molecules with an important role in intra-and inter-
kingdom interactions. Front Microbiol 8:2484
Siemieniewicz KW, Schrempf H (2007) Concerted responses between
the chitin-binding protein secreting Streptomyces olivaceoviridis
and Aspergillus proliferans. Microbiology 153:593–600
Solá MZS, Prado C, Rosa M, Aráoz MVC, Benimeli CS, Polti MA,
Alvarez A (2021) Assessment of the Streptomyces-plant system
to mitigate the impact of Cr (VI) and lindane in experimental
soils. Environ Sci Pollut R 28:51217–51231
Som S, Willett DS, Alborn HT (2017) Dynamics of belowground vola-
tile diffusion and degradation. Rhizosphere 4:70–74
Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interac-
tions. Cold Spring Harb Perspect Biol 3:a001438
Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in
microbial and microorganism-plant signaling. FEMS Microbiol
Rev 31:425–448
Suárez-Moreno ZR, Vinchira-Villarraga DM, Vergara-Morales DI,
Castellanos L, Ramos FA, Guarnaccia C, Degrassi G, Venturi
V, Moreno-Sarmiento N (2019) Plant-growth promotion and
biocontrol properties of three Streptomyces spp. isolates to con-
trol bacterial rice pathogens. Front Microbiol 10:290
Taha M, Ghaly M, Atwa H, Askoura M (2021) Evaluation of the
effectiveness of soil Streptomyces isolates for induction of plant
resistance against Tomato mosaic virus (ToMV). Curr Microbiol
78:3032–3043
Terra L, Ratcliffe N, Castro HC, Vicente AC, Dyson P (2021) Biotech-
nological potential of streptomyces siderophores as new antibiot-
ics. Curr Med Chem 28:1407–1421
Tilocca B, Cao A, Migheli Q (2020) Scent of a killer: microbial vola-
tilome and its role in the biological control of plant pathogens.
Front Microbiol 11:41
Tolba S, Ibrahim M, Amer EA, Ahmed DA (2019) First insights into
salt tolerance improvement of Stevia by plant growth-promoting
Streptomyces species. Arch Microbiol 201:1295–1306
Tonelli ML, Figueredo MS, Rodríguez J, Fabra A, Ibañez F (2020)
Induced systemic resistance-like responses elicited by rhizobia.
Plant Soil 448:1–14
Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant–micro-
biome interactions: from community assembly to plant health.
Nat Rev Microbiol 18:607–621
Vaid N, Sudan J, Dave S, Mangla H, Pathak H (2022) Insight into
microbes and plants ability for bioremediation of heavy metals.
Curr Microbiol 79:141
Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016)
Role of plant growth promoting rhizobacteria in agricultural
sustainability-a review. Molecules 21:573
Verbon EH, Liberman LM (2016) Beneficial microbes affect endog-
enous mechanisms controlling root development. Trends Plant
Sci 21:218–229
Vijayabharathi R, Sathya A, Gopalakrishnan S (2015) Plant growth-
promoting microbes from herbal vermicompost. In: D Egam-
berdieva, S Shrivastava, A Varma (eds) Plant-growth-promoting
rhizobacteria (PGPR) and medicinal plants. Springer, Cham
Vurukonda SSKP, Giovanardi D, Stefani E (2018) Plant growth pro-
moting and biocontrol activity of Streptomyces spp. as endo-
phytes. Int J Mol Sci 19:952
Wang Z, Pang F, Gu C, Wang L, Xing Y, Yang L, Li Y (2017a) Estab-
lishment and optimization of Streptomyces chartreusi WZS021
transconjugation system. J South Agric 48:581–586
Wang Z, Solanki MK, Pang F, Singh RK, Yang L-T, Li Y-R, Li H-B,
Zhu K, Xing Y-X (2017b) Identification and efficiency of a
nitrogen-fixing endophytic actinobacterial strain from sugarcane.
Sugar Tech 19:492–500
Wang Z, Solanki MK, Yu Z-X, Yang L-T, An Q-L, Dong D-F, Li Y-R
(2019) Draft genome analysis offers insights into the mechanism
by which Streptomyces chartreusis WZS021 increases drought
tolerance in sugarcane. Front Microbiol 9:3262
Wang Z, Yu ZX, Solanki M, Yang LT, Xing YX, Dong DF, Li YR
(2020) Diversity of sugarcane root-associated endophytic Bacil-
lus and their activities in enhancing plant growth. J Appl Micro-
biol 128:814–827
Wang Z, Solanki MK, Yu Z-X, Anas M, Dong D-F, Xing Y-X, Malviya
MK, Pang F, Li Y-R (2021) Genome characteristics reveal the
biocontrol potential of actinobacteria isolated from sugarcane
rhizosphere. Front Microbiol 12:797889
Warrad M, Hassan YM, Mohamed MS, Hagagy N, Al-Maghrabi OA,
Selim S, Saleh AM, AbdElgawad H (2020) A bioactive fraction
from Streptomyces sp. enhances maize tolerance against drought
stress. J Microbiol Biotechn 30:1156–1168
Wei M, Liu X, He Y, Xu X, Wu Z, Yu K, Zheng X (2020) Biochar
inoculated with Pseudomonas putida improves grape (Vitis vinif-
era L.) fruit quality and alters bacterial diversity. Rhizosphere 16
Wilson BR, Bogdan AR, Miyazawa M, Hashimoto K, Tsuji Y (2016)
Siderophores in iron metabolism: from mechanism to therapy
potential. Trends Mol Med 22:1077–1090

World Journal of Microbiology and Biotechnology (2022) 38:193
1 3
193 Page 12 of 12
Worsley SF, Newitt J, Rassbach J, Batey SF, Holmes NA, Murrell JC,
Wilkinson B, Hutchings MI (2020) Streptomyces endophytes
promote host health and enhance growth across plant species.
Appl Environ Microbiol 86:e01053-e1020
Yang Z, He J, Wei X, Ju J, Ma J (2020) Exploration and genome mining
of natural products from marine Streptomyces. Appl Microbiol
Biot 104:67–76
York A (2020) Attracting a ride. Nat Rev Microbiol 18:316–317
Yu Y, Gui Y, Li Z, Jiang C, Guo J, Niu D (2022) Induced systemic
resistance for improving plant immunity by beneficial microbes.
Plants 11:386
Yun T, Zhang M, Zhou D, Jing T, Zang X, Qi D, Chen Y, Li K, Zhao Y,
Tang W (2021) Anti-foc RT4 activity of a newly isolated Strep-
tomyces sp. 5–10 from a medicinal plant (Curculigo capitulata).
Front Microbiol 11:3544
Zaroubi L, Ozugergin I, Mastronardi K, Imfeld A, Law C, Gélinas
Y, Piekny A, Findlay BL (2022) The ubiquitous soil terpene
geosmin acts as a warning chemical. Appl Environ Microbiol
88:e00093-e22
Zhan Y, Yan Y, Deng Z, Chen M, Lu W, Lu C, Shang L, Yang Z,
Zhang W, Wang W (2016) The novel regulatory ncRNA, NfiS,
optimizes nitrogen fixation via base pairing with the nitrogenase
gene nifK mRNA in Pseudomonas stutzeri A1501. Proc Natl
Acad Sci USA 113:E4348–E4356
Zhang H, Han L, Jiang B, Long C (2021) Identification of a phos-
phorus-solubilizing Tsukamurella tyrosinosolvens strain and its
effect on the bacterial diversity of the rhizosphere soil of peanuts
growth-promoting. World J Microb Biot 37:109
Zhu Z, Tian Z, Li J (2021) A Streptomyces morookaensis strain pro-
motes plant growth and suppresses Fusarium wilt of banana.
Trop Plant Pathol 46:175–185
Publisher's Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
Springer Nature or its licensor holds exclusive rights to this article under
a publishing agreement with the author(s) or other rightsholder(s);
author self-archiving of the accepted manuscript version of this article
is solely governed by the terms of such publishing agreement and
applicable law.