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Actinobacteria as Effective Biocontrol Agents against Plant Pathogens, an

Overview on Their Role in Eliciting Plant Defense

Article in Microorganisms · August 2022

DOI: 10.3390/microorganisms10091739

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 microorganisms

Review
Actinobacteria as Effective Biocontrol Agents against
Plant Pathogens, an Overview on Their Role in Eliciting
Plant Defense
Marzieh Ebrahimi-Zarandi 1 , Roohallah Saberi Riseh 2, * and Mika T. Tarkka 3,4, *

1 Department of Plant Protection, Faculty of Agriculture, Shahid Bahonar University of Kerman,

Kerman 7618411764, Iran
2 Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University of Rafsanjan,
Imam Khomeini Square, Rafsanjan 7718897111, Iran
3 UFZ—Helmholtz Centre for Environmental Research, Department of Soil Ecology, Theodor-Lieser-Str. 4,
06120 Halle (Saale), Germany
4 German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-Leipzig Puschstrasse 4,
04103 Leipzig, Germany
* Correspondence: r.saberi@vru.ac.ir (R.S.R.); mika.tarkka@ufz.de (M.T.T.)

Abstract: Pathogen suppression and induced systemic resistance are suitable alternative biocontrol
strategies for integrated plant disease management and potentially comprise a sustainable alternative
to agrochemicals. The use of Actinobacteria as biocontrol agents is accepted in practical sustainable
agriculture, and a short overview on the plant-beneficial members of this phylum and recent updates
on their biocontrol efficacies are the two topics of this review. Actinobacteria include a large portion
of microbial rhizosphere communities and colonizers of plant tissues that not only produce pest-
antagonistic secondary metabolites and enzymes but also stimulate plant growth. Non-pathogenic
Citation: Ebrahimi-Zarandi, M.; Actinobacteria can also induce systemic resistance against pathogens, but the mechanisms are
Saberi Riseh, R.; Tarkka, M.T. still poorly described. In the absence of a pathogen, a mild defense response is elicited under
Actinobacteria as Effective Biocontrol jasmonic acid and salicylic acid signaling that involves pathogenesis-related proteins and secondary
Agents against Plant Pathogens, an plant metabolites. Priming response partly includes the same compounds as the response to a sole
Overview on Their Role in Eliciting actinobacterium, and the additional involvement of ethylene signaling has been suggested. Recent
Plant Defense. Microorganisms 2022, amplicon sequencing studies on bacterial communities suggest that future work may reveal how
10, 1739. https://doi.org/10.3390/
biocontrol active strains of Actinobacteria can be enriched in plant rhizosphere.
microorganisms10091739

Academic Editor: Jean Stéphane Keywords: actinobacteria; biocontrol; induced systemic resistance; plant defense
Venisse

Received: 20 July 2022

Accepted: 25 August 2022
1. Introduction
Published: 29 August 2022
Intensive agricultural practice is accompanied by the leaching of mineral fertilizers
Publisher’s Note: MDPI stays neutral
and combatting emerging phytopathogens with synthetic agrochemicals, and the necessity
with regard to jurisdictional claims in
of developing complementary methods to improve plant nutrition and to control plant
published maps and institutional affil-
pathogens has been recognized [1]. Biological control uses microbial biocontrol agents to
iations.
protect plants against pathogens with direct and indirect mechanisms. Direct mechanisms
include hyperparasitism, predation and antibiosis, as well as competition for nutrients
and space with other microorganisms, but the impacts of single microbial strains on the
Copyright: © 2022 by the authors. microbiome assembly and the induction of host resistance are indirect mechanisms for
Licensee MDPI, Basel, Switzerland. microbial biocontrol agents against pathogens [2]. Damage to plant pathogens and the
This article is an open access article effect of bacterial biocontrol agents have been proven in several field studies [3–9].
distributed under the terms and Members of Actinobacteria are engaged in beneficial interactions with plants, stimu-
conditions of the Creative Commons lating plant growth and disease resistance (Figure 1). Among microbial biocontrol agents,
Attribution (CC BY) license (https:// the members of Actinobacteria are particularly interesting due to their widespread abilities
creativecommons.org/licenses/by/ to inhibit the growth of a wide range of phytopathogens and the prolific production of
4.0/).

Microorganisms 2022, 10, 1739. https://doi.org/10.3390/microorganisms10091739 https://www.mdpi.com/journal/microorganisms

Microorganisms 2022, 10, 1739 2 of 16

abilities to inhibit the growth of a wide range of phytopathogens and the prolific produc-
Microorganisms 2022, 10, 1739 2 of 15
tion of antimicrobial compounds [10,11]. Though most studies on biocontrol have in-
volved Streptomyces species, reports also exist on, e.g., isolates from the genera Actino-
planes, Arthrobacter, Microbacterium, Micromonospora and Rhodococcus. Since the members
antimicrobial compounds [10,11]. Though most studies on biocontrol have involved Strep-
of Actinobacteria are generally
tomyces species, reports also existversatile in theirfrom
on, e.g., isolates metabolism
the generaand thus competitive
Actinoplanes, Arthrobacter,for both
root
Microbacterium, Micromonospora and Rhodococcus. Since the members of Actinobacteria are and
exudates and plant litter, they form intimate associations with plant materials
comprise
generally frequent
versatilecolonizers of rhizospheres
in their metabolism and thus and plant tissues
competitive [12].root
for both Plant growthand
exudates promo-
tion by Actinobacteria
plant litter, they formtakesintimateplace through the
associations withsecretion of plantand
plant materials growth regulators
comprise frequent [13,14],
colonizers of rhizospheres and plant tissues [12]. Plant growth promotion
nitrogen fixation, phosphate solubilization, and iron acquisition [15–19]. Such traits are by Actinobacteria
takes place
expressed by,through the secretion
for instance, membersof plant
of growth regulators
the genera [13,14],
Frankia, nitrogen fixation,
Streptomyces, phos- Mi-
Micrococcus,
phate solubilization, and iron acquisition [15–19]. Such traits are expressed by, for instance,
cromonospora, Kitasatospora and Thermobifidia. Actinobacteria may also influence symbiosis
members of the genera Frankia, Streptomyces, Micrococcus, Micromonospora, Kitasatospora
formation between host plants and their mutualists, nitrogen-fixing bacteria [20] and my-
and Thermobifidia. Actinobacteria may also influence symbiosis formation between host
corrhizal
plants andfungi
their[21]. Investigations
mutualists, on plant
nitrogen-fixing growth
bacteria [20]promotion
and mycorrhizalhavefungi
revealed that the in
[21]. Inves-
vitro antagonistic
tigations on plantactivity against pathogens
growth promotion by Actinobacteria
have revealed that the in vitrodoes not necessarily
antagonistic activity cor-
relate with
against their biocontrol
pathogens activity [22].
by Actinobacteria doesInstead, plant growth
not necessarily correlatepromotion has been asso-
with their biocontrol
ciated with
activity biocontrol
[22]. activity,
Instead, plant growthandpromotion
this has two important
has been implications.
associated First,activity,
with biocontrol the screen-
ingand
forthis has two important
biocontrol strains shouldimplications. First, thetoscreening
not be limited the resultsfor of
biocontrol
in vitro strains should
bioactivity assays;
not be limited to the results of in vitro bioactivity assays; second, the
second, the Actinobacteria may protect host plants in vivo by not only inhibiting the path-Actinobacteria may
protect host plants in vivo by not only inhibiting the pathogen but also by eliciting plant
ogen but also by eliciting plant disease resistance [23].
disease resistance [23].

Figure
Figure 1. 1. Beneficialinteractions
Beneficial interactions of
of Actinobacteria
Actinobacteria with
withplants.
plants.
Indeed, rhizobacteria can mediate induced systemic resistance (ISR) in plants by
Indeed, rhizobacteria can mediate induced systemic resistance (ISR) in plants by
priming for plant defense, first revealed with Pseudomonas and Bacillus strains [24–26].
priming
Primingfor plantthe
brings defense,
plants tofirst revealed
an altered with
state thatPseudomonas
enables them and Bacillus
to more strains
quickly [24–26].
and/or
Priming brings the plants to an altered state that enables them to more
strongly respond to a subsequent pathogen infection [27,28]. The traditional ISR pathwaysquickly and/or
strongly respond
in plants duringto a subsequent
Pseudomonas- and pathogen infectionISR
Bacillus-mediated [27,28]. The
lead to thetraditional
faster and ISR pathways
stronger
in expression
plants during Pseudomonas-
of marker genes forand Bacillus-mediated
the salicylic ISRacid,
acid, jasmonic leadandto the fastersignaling
ethylene and stronger
pathways of
expression upon subsequent
marker genes pathogen infection.
for the salicylic ISR by
acid, Actinobacteria
jasmonic acid, andwasethylene
identifiedsignaling
by
Conn et al.
pathways [29] subsequent
upon Micromonospora
as a result of pathogen or Streptomyces
infection. strain inoculations.
ISR by Actinobacteria was identified by
In this review, we focus on recent developments in the area of Actinobacteria-based
Conn et al. [29] as a result of Micromonospora or Streptomyces strain inoculations.
biocontrol, starting with the compound production against the pests and then moving to
In this review, we focus on recent developments in the area of Actinobacteria-based
biocontrol, starting with the compound production against the pests and then moving to
the elicitation of plant defenses. We close the review by evaluating the community studies
Microorganisms 2022, 10, 1739 3 of 15

the elicitation of plant defenses. We close the review by evaluating the community studies
of plant-associated Actinobacteria and discussing the potential to enrich stress releasing
members of this phylum by specific treatments. We expect that the appreciation of these
thematic areas will be crucial for the development of novel Actinobacteria-based biocontrol
approaches.

2. Actinobacteria as Successful Biocontrol Agents

Numerous studies have proven that Actinobacteria are successful biocontrol agents
against plant pathogens (Table 1). Biological activity against pathogens has been estab-
lished for several actinobacterial secondary metabolites. For instance, Cheng et al. [30]
reported that azalomycin produced by Streptomyces malaysiensis MJM1968 exhibited antifun-
gal activity on Fusarium oxysporum, Rhizoctonia solani, Cladosporium cladosporioides, Fusarium
chlamydosporum, Colletotrichum gloeosporioides, Pestalotia spp. and Alternaria mali. Addition-
ally, prodiginines from S. lividans caused the inhibition of Verticillium dahliae growth [31].
Siderophores are other bioactive compounds produced by Actinobacteria that can promote
plant growth and induce resistance in plants against pathogens [32,33]. Siderophores are
small molecules with a high affinity for Fe3+ . Sadeghi et al. [34] reported that a siderophore-
producer Streptomyces strain improved iron acquisition and wheat growth promotion under
salinity stress conditions. Actinobacteria isolated from Achillea fragrantissima that produced
both chitinases and siderophores showed antimicrobial activity against pathogenic mi-
croorganisms [35]. Dimkpa et al. [36] reported that hydroxamate siderophores produced
by Streptomyces tendae F4 promoted the growth and improved the cadmium uptake of
sunflower plants.
Actinobacteria are also well-known for the release of enzymes that are active against
phytopathogens, including chitinases, glucanases, amylases, cellulases, lipases and pro-
teases [37]. Chitinase- and glucanase-producing S. cavourensis SY224 controlled anthracnose
disease in pepper [38]. S. halstedii and S. griseus produced highly active antifungal chitinases
and are effective biological agents for the protection of crops [39,40]. Glucanase-producing
Actinoplanes campanulatus and Micromonospora chalcea protected cucumber from Pythium
aphanidermatum under greenhouse conditions [41]. Streptomyces sp. MT7, as a chitinolytic
strain, showed antagonistic activity against several wood-rotting fungi including Phane-
rochaete chrysosporium, Coriolus versicolor, Polystictus versicolor, and Schizophyllum commune,
the causal agents of white rot, as well as Gloeophyllum trabeum, Postia placenta, Polyporus agar-
icans and Polyporus friabilis, the causal agents of brown rot [42]. Gopalakrishnan et al. [43]
reported that Streptomyces strains reduced Fusarium wilt in chickpea via the production of
several metabolites in concert including not only the enzymes cellulase and protease but
also hydrogen cyanide. Dieback caused by the fungus Lasiodiplodia theobromae is an impor-
tant disease on mango plantations, and the antifungal action of Micromonospora tulbaghiae
UAE1 against the fungus was associated with both antibiotic and chitinase production [44].
The quenching of quorum-sensing molecules may also lead to biocontrol by Actinobacteria.
The biocontrol agent of soft rot disease in various host plants, Rhodococcus pyridinivorans
XN-36, degrades a wide range of N-acyl homoserine lactones and prevents quorum-sensing
among plant-pathogenic bacteria [45]. Additionally, in co-cultures between Arthrobacter sp.
IBN110 and the plant pathogen Erwinia carotovora, the N-acyl homoserine lactone levels
and pectate lyase activity, both important for rot induction, were shown to be significantly
reduced in relation to a single culture of E. carotovora [46].
Volatile organic compounds (VOCs) are bioactive molecules produced by many plant-
associated Actinobacteria, e.g., Streptomyces strains possessing antifungal activity [47–49].
Volatile substances produced by S. platensis F-1 caused resistance in rice, oilseed rape, and
strawberry against Rhizoctonia solani, Sclerotinia sclerotiorum, and Botrytis cinerea, respec-
tively [50]. S. angustmyceticus NR8-2 was shown to emit volatile antifungal compounds
including alcohols, aldehydes, carboxylic acids and fatty acids. This species also produced
β-1,3-glucanase, and controlled Colletotrichum sp. and Curvularia lunata leaf spot on Tokyo
Bekana cabbage [51].
Microorganisms 2022, 10, 1739 4 of 15

Table 1. The examples of biocontrol activity of the actinobacterial strains against some phytopathogens.

Strain Host Pathogen Reference

Streptomyces halstedii AJ-7 Red pepper Phytophthora capsici [52]
Streptomyces sp. CA2, AA2 Tomato Rhizoctonia solani [22]
S. griseus Tomato Fusarium sp. [53]
Streptomyces sp. S2,C Sugar beet Rhizoctonia solani [54]
Streptomyces sp. MBCu-56 Cucurbit Colletotrichum orbiculare [55]
S. aurantiogriseus
Rice Rhizoctonia solani [56]
VSMGT1014
Streptomyces sp. J-2 Sugar beet Sclerotium rolfsii [57]
Streptomyces spp. Sugar beet Fusarium spp. [58]
Actinoplanes campanulatus #2
Micromonospora chalcea #8 Cucumber Pythium aphanidermatum [41]
S. spiralis #17
Streptomyces sp. strain g10 [59]
Banana Fusarium oxysporum f.sp. cubense
S. malaysiensis 8ZJF-21 [60]
Streptomyces sp. S160 Chickpea Macrophomina phaseolina [61]
Amycolatopsis sp. 521 Apple Colletotrichum gloeosporioides [62]
Alternaria solani, A. alternata, Colletotrichum
S. albidoflavus Tomato gloeosporioides, Fusarium oxysporum, Fusarium [63]
solani, Rhizoctonia solani, and Botrytis cinerea
Pepper,
Streptomyces sp. A1022 Colletotrichum gloeosporioides [64]
Cherry Tomato
S. misionensis BH4-1,BH4-3 Pistachio Paecilomycesformosus [65]
S. globisporus JK-1 Rice Magnaporthe oryzae [66]
Streptomyces sp. MT7 - Wood-rotting fungi [42]
S. mutabilis IA1 Wheat Fusarium culmorum [67]
Micromonospora sp.
Tomato Botrytis cinerea [68]
ALFpr18c, ALFb5
S. globosus UAE1 Date Palm Thielaviopsis punctulata [69]
Streptomyces spp. A20, 5.1, 7.1 Rice Burkholderia glumae [70]
S. angustmyceticus Colletotrichum sp. and
Cabbage [51]
NR8-2 Curvularia lunata
Streptomyces sp. HAAG3-15 Cucumber F. oxysporum f.sp. cucumerinum [71]
Streptomyces spp. R7,F8 Tomato R. solani [72]
S. laydicus M01 Cucumber A. alternata [73]
Cucumber Pythium aphanidermatum and [74]
S. fulvissimus Uts22
Wheat Gaeumannomyces graminis var. tritici [75]
Pectobacterium carotovorum subsp. Carotovorum,
Streptomyces sp. TP199 Potato [76]
and Pectobacterium atrosepticum
S. violaceusniger AC12AB Potato Streptomyces scabies [77]
Tomato Ralstonia solanacearum,
Streptomyces sp. AN090126 Red Pepper Xanthomonas euvesicatoria, and [78]
Creeping bentgrass Sclerotinia homoeocarpa
Microorganisms 2022, 10, 1739 5 of 15

Several commercial products derived from Actinobacteria are available for use in
crop protection. Table 2 shows the Streptomyces spp.-based products and active substances
derived from them registered as commercial products for the control of plant pathogens.
Mycostop was the first actinobacterial commercial product derived from S. griseoviridis K61
that is used against some soilborne fungal pathogens [79].

Table 2. List of Streptomyces spp.-based products and active substances derived from them registered
as commercial products to control of plant pathogens (data collected and modified into a table
from [80–83]).

Product Name Organism Targeted Pathogen/Disease

Mycostop,
Damping off caused by Alternaria and R. solani and
Verdera Oy, S. griseoviridis K61
Fusarium, Phytophthora, and Pythium wilt and root diseases
Finland
Soilborne pathogens, viz. Pythium, Fusarium, Phytophthora,
Actinovate,
Rhizoctonia, and Verticillium; foliar diseases such as
Novozymes S. lydicus WYEC 108
powdery and downy mildew, Botrytis, Alternaria, Postia,
BioAg Inc., USA
Geotrichum, and Sclerotinia
Mykocide KIBC Co., Ltd.
S. colombiensis Powdery mildews, grey mold, and brown patch
South Korea
Safegrow KIBC Co., Ltd.
S. kasugaensis Sheath blight and large patch
South Korea
Bactophil S. albus Seed germination diseases
Blasticidin-S
S. griseochromogenes Pyricularia oryzae
BLA-S
Leaf spot in sugar beet and celery (Cercospora spp.), scab in
Kasugamycin
S. kasugaensis pears and apples (Venturia spp.), and soybean root rot
Kasumin, Kasurab
(Phytophthora sojae)
Streptomycin Bacterial rots, canker, and other bacterial diseases;
Agrimycin, Paushak, Xanthomonas oryzae, Xanthomonas citri, and Pseudomonas
S. griseus
Cuprimicin 17, AAstrepto 17, tabaci of pome fruit, stone fruit, citrus, olives, vegetables,
AS-50, Dustret, Cuprimic 100 and 500 potatoes, tobacco, cotton, and ornamentals
Phytomycin Fire blight (Erwinia amylovora) and diseases caused by
Mycoshield, Cuprimic 100 and 500, S. rimosus Pseudomonas sp., Xanthomonas sp. and
Mycoject mycoplasma-like organisms
Validamycin
Validacin, Valimun, R. solani and other Rhizoctonia in rice, potatoes, vegetables,
S. hygroscopicus
Dantotsupadanvalida, Mycin strawberries, tobacco, ginger, cotton, sugar beet, etc.
Hustler, Valida, Sheathmar
Plant-pathogenic fungi, Sphaerotheca spp. and other
powdery mildews; Botrytis cinerea, Sclerotinia sclerotiorum,
Polyoxorim
Corynespora melonis, Cochliobolus miyabeanus, Alternaria
Endorse, PolyoxinZ, Stopit, Polyoxin S. cacaoi var. asoensis
alternata and other species in vines, apples, pears,
AL and Z, Polybelin
vegetables, and ornamentals; rice sheath blight (R. solani),
apple, pear canker, and Helminthosporium in rice
Natamycin S. natalensis and Basal rots on daffodils and ornamentals caused by
Delvolan S. chattanoogensis Fusarium oxysporum
Bold names in the first column indicate biocontrol metabolites as active substances.

Although biocontrol activities by Actinobacteria have been recognized as potentially

useful for sustainable agriculture, only few products are currently commercialized [84]. The
establishment of suitable and rapid screening for appropriate biocontrol candidates is one
of the critical steps towards the development of novel commercial biocontrol products [85].
Additionally, formulation methods and procedures of inoculations play an important role
in obtaining satisfactory results of the application of the certain commercial product in
Microorganisms 2022, 10, 1739 6 of 15

the field conditions [86], and their further development is crucial in order to obtain robust
actinobacterial formulations.

3. The Potential of Actinobacteria to Induce Systemic Resistance in Plants

3.1. General Mechanisms of Induced Systemic Resistance (ISR)
ISR exerts a broad-spectrum response against pathogens, and it can be comparably
effective in different plant species [87]. The elicitors of ISR that are produced by or derived
from bacteria include lipopolysaccharides (LPS), flagella, siderophores, biosurfactants,
volatile organic compounds (VOCs), quorum-sensing molecules and antibiotics [88–90].
The perception of some of the beneficial microorganisms involves early responses such
as ion fluxes, MAP kinase cascade activation, extracellular medium alkalization, and
the production of reactive oxygen species (ROS) followed by the activation of various
molecular and cellular host defense responses [91–93]. Jasmonic acid (JA) and ethylene
(ET) are central players in the priming of plant resistance by bacteria [26,87]. Figure 2 sums
up the molecular components and mechanisms involved in ISR by beneficial microbes.
Although beneficial microorganisms often trigger ISR through the JA/ET pathway, several
plant growth-promoting rhizobacteria and fungi have been shown to trigger ISR through
salicylic acid (SA)-dependent mechanisms. For example, Paenibacillus alvei K-165 and
P. fluorescens SS101 were found to induce an SA-dependent pathway in Arabidopsis [94,95],
Microorganisms 2022, 10, 1739 and an SA-producing mutant of Pseudomonas aeruginosa 7NSK2 did not induce resistance 7 of 16 to
Botrytis cinerea in wild-type tomatoes [96].

Figure 2. Induced systemic resistance (ISR) by beneficial microorganisms. JA and ET are central
Figure 2. Induced systemic resistance (ISR) by beneficial microorganisms. JA and ET are central
regulators phytohormones of ISR, and transcription factors (e.g., MYC2) mediate the increased re-
regulators phytohormones
sponsiveness of ISR,
of this pathway and transcription
to stimulation, known asfactors (e.g.,
priming. MYC2) mediate
Transcription the increased
factor MYB72, as a
responsiveness of this pathway to stimulation, known as priming. Transcription factor
root-specific transcription factor and early signaling factor, functions as a node of convergence MYB72,in as
a root-specific transcription
ISR elicited by factor and
beneficial microbes. early
(ET, signaling
ethylene; factor, functions
JA, jasmonic as a NONEXPRESSOR
acid; NPR1, node of convergenceOF in
ISRPRelicited
GENES1; MAMPs, microbes.
by beneficial microbe-associated molecular
(ET, ethylene; patterns;acid;
JA, jasmonic PRRs, plantNONEXPRESSOR
NPR1, recognition receptors;
OF PR
PTI, PAMP-triggered immunity; TFs, transcription factors).
GENES1; MAMPs, microbe-associated molecular patterns; PRRs, plant recognition receptors; PTI,
PAMP-triggered immunity; TFs, transcription factors).
3.2. Actinobacteria Priming Plant Defense
In a pioneering paper, Conn et al. [29] reported priming by wheat endophytic Ac-
tinobacteria belonging to Micromonospora and Streptomyces. The priming by these Actino-
bacteria was associated with upregulating genes in either the SAR and/or JA/ET path-
ways, depending on the infecting pathogen, and the ISR also occurred after the applica-
tion of bacterial culture filtrates. Priming by a culture filtrate was also proven with the
Microorganisms 2022, 10, 1739 7 of 15

3.2. Actinobacteria Priming Plant Defense

In a pioneering paper, Conn et al. [29] reported priming by wheat endophytic Acti-
nobacteria belonging to Micromonospora and Streptomyces. The priming by these Actinobac-
teria was associated with upregulating genes in either the SAR and/or JA/ET pathways,
depending on the infecting pathogen, and the ISR also occurred after the application of
bacterial culture filtrates. Priming by a culture filtrate was also proven with the culture
filtrate of S. bikiniensis HD-087. Its application induced resistance in cucumber against
Fusarium oxysporum f.sp. cucumerinum and was associated with highly increased activities
of peroxidase, β-1,3-glucanase, and phenylalanine ammonia lyase [97]. The induction
of cytosolic Ca2+ and biphasic oxidative burst by Streptomyces sp. OE7 in tobacco cells
was demonstrated by Baz et al. [98], suggesting that this strain elicits ISR in a similar
manner to the Pseudomonas and Bacillus strains. The ability of Streptomyces strains S.
toxytricini vh22, S. avidinii vh32, S. tricolor vh85, S. toxytricini vh6 and S. flavotricini vh8
to protect tomato against Rhizoctonia solani under greenhouse conditions was reported by
Patil et al. [99]. Phenylalanine ammonia lyase (PAL) activity and total phenolic contents in
tomato increased following the inoculation of these four strains compared to an untreated
control [99], and they were further enhanced by the presence of the plant pathogen, though
Streptomyces strain-specific differences were observed. Whereas the isolates vh6 and vh8
offered the most extensive disease reductions, the highest PAL activities and levels of
total phenolic compounds were observed for the strain vh32, suggesting that protection
against R. solani involves further determinants of plant phenolics induction [99]. Simi-
larly, biochemical experiments revealed that actinomycetes isolated from vermicompost
enhanced defense-related enzyme activities, including those of peroxidase, polyphenol
oxidase, and phenylalanine ammonia lyase, in tomato plants challenged by R. solani [100].
Streptomyces sp. strain AcH 505 induced resistance in oak against Microsphaera alphitoides,
the causal agent of powdery mildew. RNA-Seq analysis revealed that not only JA but also
the ET, SA, and (in part) ABA pathways may play roles in Streptomyces AcH 505-mediated
priming in oaks. The study also revealed that Streptomyces sp. strain AcH 505 was able to
activate plant defense responses in the absence of pathogen challenge [101]. Furthermore,
in accordance with reports discussed earlier, the authors of the study demonstrated the
priming-like accumulation of transcripts related to phenylpropanoid biosynthesis and
reported enhanced phenylalanine ammonia lyase activity, suggesting that plant secondary
metabolism may be involved.
Martinez-Hidalgo et al. [68] demonstrated that Micromonospora strains ALFpr18c and
ALFb5 stimulated defense responses of different tomato cultivars upon Botrytis cinerea
attack. Their study revealed that the induced systemic resistance in tomato was long
lasting and that jasmonates played a key role in the defense priming effect [68]. Singh
and Gaur [102] reported that endophytic Streptomyces spp. triggered systemic resistance
against Sclerotium rolfsii in chickpeas and mitigated the oxidative stress generated by this
pathogen. Their biochemical experiments indicated that S. griseus in challenge with the
pathogen caused increases in the amount of defense-related enzymes such as PAL and PPO
along with the accumulation of total phenolics and flavonoids. Furthermore, real-time PCR
analysis revealed significant enhancements of genes encoding superoxide dismutase (SOD),
PAL, peroxidase (PO), ascorbate peroxidase (APX), catalase (CAT), chitinase (CHI), and
β-glucanase (GLU) after priming with S. griseus, which corroborated the above-mentioned
findings [102].
The grapevine rhizosphere inhabitant Streptomyces anulatus S37 promotes grapevine
growth and induces resistance against phytopathogens, including B. cinerea. The lo-
cal defense events induced in grapevine suspension cells were investigated by Vatsa-
Portugal et al. [103]; S. anulatus S37 induced early defense responses including oxidative
burst, extracellular alkalization, protein kinase activation, the induction of defense gene
expression, and phytoalexin accumulation [103]. Additionally, an early interaction between
Streptomyces sp. UPMRS4 and rice plant under Pyricularia oryzae stress [104] has demon-
strated increases in chitinase (Cht-1), glucanase (Gns1), pathogenesis-related gene (OsPR1a),
Microorganisms 2022, 10, 1739 8 of 15

and salicylic acid-responsive gene (Oswrky45) transcript abundancies. The ability of S.

rochei A-1 in inducing resistance against Botryosphaeria dothidea in apple fruit during storage
was reported by Zhang et al. [105], including enhanced POD, CAT, SOD, PAL, GLU and
CHI activities and H2 O2 generation but decreased lipid peroxidation.
Streptomyces sp. strain NSP3 triggered tomato defense responses against F. oxysporum
f.sp. lycopersici [106]. The effects of seed treatment or soil application with the Streptomyces
sp. strain NSP3 and the combination of two methods were compared under pathogen
challenge. The combination of two above-described methods was more effective for the
induction of PR genes including PR-1a, Chi3, Chi9, and CEVI-1 than either alone [106]. In
another study, Abbasi et al. [107] demonstrated how Streptomyces strains induced systemic
resistance to F. oxysporum f.sp. lycopersici in tomato, and in cucumber, Streptomyces sp.
LH4 was shown to mediate JA and SA defenses in response to Sclerotinia sclerotiorum [108].
Inoculations of S. fimicarius and S. laurentii to rice rhizosphere led to resistance against rice
bacterial blight, as reported by Saikia and Bora [109]. The application of S. lydicus M01 to
rhizospheres promoted cucumber growth via its phosphate solubilization, IAA secretion,
siderophore and ACC deaminase production activities and led to higher numbers of po-
tentially plant-beneficial bacteria in cucumber rhizosphere [73]. It alleviated foliar disease
caused by Alternaria alternata on cucumber, reduced reactive oxygen species accumulation,
and enhanced the activities of antioxidant enfzymes related to ROS scavenging under
A. alternata stress [73]. Tomato-root-colonizing Streptomyces strains R7 and F8 inhibited
R. solani infection under greenhouse conditions and enhanced the expression of PAL1
and LOXB genes of tomatoes, especially upon pathogen inoculation [72]. Lee et al. [110]
showed how plant protection by Streptomyces sp. JCK-6131 takes place via two mecha-
nisms: antibiosis with antimicrobial compounds, streptothricins, and priming. JCK-6131
treatment induced the expression of pathogenesis-related protein genes, suggesting the
simultaneous activation of the salicylate and jasmonate signaling pathways. The induction
of plant resistance against tobacco mosaic virus infection by S. cellulosae was indicated by
the work of Abo-Zaid et al. [111], with a significant increase in the phenylalanine ammonia
lyase, chalcone synthase, and pathogenesis-related protein transcripts. Again, the simul-
taneous activation of the salicylate and jasmonate signaling pathways took place. Finally,
Vergnes et al. [112] inoculated Streptomyces sp. AgN23 on Arabidopsis leaves, which resulted
in resistance against the Alternaria brassicicola infection of the leaves. The activation of
Arabidopsis defense responses by AgN23-induced resistance was partially compromised in
salicylate, jasmonate, and ethylene mutants. In conclusion, these insights into the mecha-
nisms of priming by Actinobacteria suggest a capacity to activate plant defense responses
in the absence of a pathogen. The common determinants of priming seem to be eliciting
both JA/ET- and SA-related signaling, commonly associated with enhanced PR protein
and plant secondary metabolism levels. One interesting open question is whether the plant-
associated microbiomes modulate the priming process, as their community compositions
do change upon the introduction of Actinobacteria to the rhizosphere [73]. According to
the studies mentioned above, Actinobacteria can trigger both the SA and JA/ET pathways
in plants. That the plant response to the biocontrol agents so commonly leads to the partial
elicitation of defense pathways in the absence of the pathogen is intriguing and calls for
further investigations into the mechanisms behind Actinobacteria-based priming.

4. Enrichment of Actinobacteria during the Establishment of Suppressive Soils,

Pathogen Attacks and Abiotic Stress: A Sign of Their Central Role in Plant Protection?
Amplicon sequencing studies have repeatedly indicated that Actinobacteria in soil and
plant microbiomes are associated with the suppression of plant disease and the induction
of abiotic stress tolerance. We expect that a greater understanding of the mechanisms that
lead to higher abundances of plant-protective Actinobacteria can be used to support plant
production [23,110]. There is potential for this idea, since, as described in previous parts
of this review, basic knowledge of disease suppression by Actinobacteria is established
and plants are capable of building up beneficial rhizosphere communities and inducing
Microorganisms 2022, 10, 1739 9 of 15

disease-suppressive soils [113,114]. Plants accomplish these tasks by modulating their

root exudation patterns to support the recruitment of beneficial microorganisms [115,116].
Increasing evidence from amplicon sequencing studies suggests that Actinobacteria form
an important part of disease-suppressive microbial consortia [117,118]. For instance, the
relative abundance of members of Streptomyces, Gaiella, and Microbacterium increase in
suppressive soils [118,119], implying their potential beneficial effects on disease control.
Other studies have shown that disease-induced changes in plant microbiome assembly
also include the enrichment of, e.g., Streptomyces and Microbacterium species [120], that
serve as so-called network hubs with strong interactions with several other taxa in co-
occurrence analyses. This suggests that the recruitment of Actinobacteria by plants is one
means to ensure the survival of the plant until the next generation [118]. Interestingly,
bacterial community analyses also suggest an important role for Actinobacteria as a central
phylum of bacteria in plant rhizospheres and endospheres that support plant drought
tolerance [121]. Studies on bacterial community responses to drought indicate a central role
for Actinobacteria, especially Streptomycetes, in the abiotic stress resistance of plants [122].
A study of the root bacteria of sorghum [123], as well as a survey of thirty different plant
species [124], revealed an increase in the relative abundance of sequences affiliated with
Actinobacteria in root endosphere communities upon drought. An important mechanism
how streptomycetes support the growth of plants during stress is by suppressing ethy-
lene emissions with ACC deaminase activity [125], and Gebauer et al. [126] showed that
Actinobacteria strongly contribute to the ACC-deaminase-carrying bacterial community,
in particular during water deficits. Thus, although the community composition research
on suppressive soil, plant disease and drought tolerance-associated microbiomes does not
prove that the enriched Actinobacterial genera are responsible for plant-beneficial activities,
they have been largely implicated as the agents responsible for these traits. Community
sequencing has strongly contributed to the existing knowledge on Actinobacteria in the
rhizospheres and endospheres of plants, as well as their relations in plant microbiomes.
We think that reconstructions of soil microbial structures by pathogen pressure or abiotic
stress are promising means of how biocontrol and plant-stress-attenuating Actinobacteria
can be enriched in future applications. In this context, omics techniques such as meta-
transcriptomics could be used to tackle their potential activities, e.g., if they may produce
antagonistic compounds against pathogens, elicit plant immunity responses, or synthesize
plant growth stimulators.

5. Conclusions
The application of microbial biocontrol agents for disease control through the induc-
tion of resistance or priming relies on complex consecutive events including the successful
establishment of biocontrol agent on the host, the release of specific elicitors that are recog-
nized by the specific receptors of plants, and signaling. Defense priming by Actinobacteria
has great potential as a successful strategy for modern plant protection, and the mecha-
nisms behind it involve JA/ET- and SA-mediated signaling. The production of defense
compounds often already occurs in the absence of a pathogen, but it is enhanced by its
presence. Optimally, antibiosis and the production of lytic enzymes of an Actinobacteria
biocontrol strain should be combined with the priming activity of the same strain or another
member of a synthetic community. According to plant microbiome studies, the application
of stress, the enrichment of plant-protective actinobacterial consortia, and higher numbers
of potentially plant-beneficial bacteria may constitute novel and promising avenues for
improving plant disease resistance. Amplicon and metagenome and metatranscriptome
sequencing will increase the existing knowledge on Actinobacteria during rhizosphere
colonization and interactions between these bacteria and other microbial communities in
the rhizosphere, as well as create new information on their potential for the production
of antagonistic secondary metabolites and priming effectors. As another important issue,
further studies are needed on actinobacterial bioinoculant formulation using different
additives, carriers, and various methods of inoculation in the field conditions to develop
Microorganisms 2022, 10, 1739 10 of 15

effective commercial products. Ideally, bioinoculants will also promote plant growth in
the absence of pathogen pressure, and to reach this goal, future work should combine
biocontrol and biofertilizer activity analyses.

Author Contributions: Conceptualization, M.E.-Z., R.S.R. and M.T.T.; writing—original draft prepa-
ration, M.E.-Z. and R.S.R.; writing—review and editing, M.T.T. All authors have read and agreed to
the published version of the manuscript.
Funding: Current grants 403641192 and 466312020 of the German Science Foundation (M.T.T.).
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Acknowledgments: The authors would like to thank their current and earlier laboratory members.
Conflicts of Interest: The authors declare no conflict of interest.

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