1 s2.0 S2452219821001294 Main

Rhizosphere 20 (2021) 100433
Contents lists available at ScienceDirect
Rhizosphere
journal homepage: www.elsevier.com/locate/rhisph
Plant growth-promoting root-colonizing bacterial endophytes

Bartholomew Saanu Adeleke a, Olubukola Oluranti Babalola a, *, Bernard R. Glick b
a
Food Security and Safety Niche Area, Faculty of Natural and Agricultural Sciences, North-West University, Private Bag X2046, Mmabatho, 2735, South Africa
b
Department of Biology, University of Waterloo, Waterloo, ON, Canada
A R T I C L E I N F O A B S T R A C T
Keywords: The development of an environmentally friendly agricultural system as opposed to conventional methods using
Bioinoculants chemical fertilizers and pesticides for improved crop productivity is a promising aspect of modern agricultural
Endophytic bacteria biotechnology. Current research has focused on using free-living microbes that can colonize the plant endosphere
Plant growth
as a means of enhancing crop productivity. In the plant rhizosphere, the complex root matrix facilitates microbe-
Phytohormones
Root matrix
microbe, microbe-plant, and soil-microbe interactions in establishing microbial communities, which precede
Sustainable agriculture endophytic colonization of the plant by some of these microbes. Endophytic microbes play an important role in
plant growth promotion, as they employ direct or indirect mechanisms to facilitate plant growth by producing
phytohormones and various secondary metabolites. The roles of endophytic microbes in sustaining plant growth
under biotic and abiotic stresses through these mechanisms can provide insights into their envisaged putative
functions in establishing host plant interactions for maximum use in the agricultural sector as an ecofriendly
alternative tool to improve crop yield. In addition, a better understanding of endophytic bacteria functions in
agriculture, medicine, biotechnology, and industry may enable scientists to unlock several opportunities by
exploring valuable endophytic bioproducts in the recent application as bioinoculants, biostimulants, and envi
ronmental safety in pollution control and phytoremediation. Furthermore, the genomic insights into endosphere
biology can provide detail structural diversity and functional profiling of endophytic microbiome for possible
recommendations in future agriculture as a source of the organic amendment. Hence, this review emphasis on
the root-colonizing endophytic bacteria and their importance in modern agricultural biotechnology.
1. Introduction plant diseases (Cordovez et al., 2019). The symbiotic association that
exists between mycorrhizal and rhizobacteria in the root of leguminous
Agricultural intensification is an important condition for the food plants enables them to establish cooperation with the host plants to
security of the population of the world (Jayne et al., 2019; Adeleke and overcome nutrients (nitrogen, phosphorus, potassium, etc.) deficiency
Babalola, 2020b). However, the use of chemical fertilizers to improve in the soil and reduction of nitrogen fertilizer usage on farmlands
soil fertility and increase crop yields poses a threat to both ecosystems (Oldroyd and Leyser, 2020). Some plant microbes, such as Rhizobium,
and human health. For example, human diseases, in some cases, have Bacillus, Azospirillum, Pantoea, Streptomyces, Flavobacterium, and Pseu
been linked to the consumption of foods grown with chemical fertilizers domonas, fix nitrogen to the soil by forming symbioses with the plant
(Babalola, 2010). Against this background, the use of biofertilizers root, thus enhancing symbiotic efficiency in shaping plant-bacteria in
consisting of bacteria that are naturally associated with plant roots may teractions (Remans et al., 2008). Isolation and identification of endo
be a useful and promising alternative to the widespread application of phytic bacteria associated with bananas in Kenya and their potential use
agricultural chemicals. Biofertilizer application may be utilized in the in developing biofertilizers for sustainable banana production have been
agricultural bioeconomy to maximally ensure food production, and reported (Ngamau et al., 2012). Also, Vargas-Díaz et al. (2019) have
incorporation into the crop-breeding programs (Uzoh and Babalola, evaluated the use of endophytic bacteria from the root nodules of soy
2018; Fasusi et al., 2021). In recent times, the potential of crop micro bean and their potential as biofertilizers. Biofertilizer use in agriculture
biomes for food security has been the focus of many researchers using is considered safe and environmentally friendly and can replace agro
the current state-of-art technology in understanding the biological chemicals (chemical fertilizers and pesticides) without any negative
functions of plant microbiome to enhance plant growth and control of impacts on the ecosystem (Glick, 2020; Fasusi et al., 2021).
* Corresponding author.
E-mail address: [email protected] (O.O. Babalola).
https://doi.org/10.1016/j.rhisph.2021.100433
Received 28 July 2021; Received in revised form 18 September 2021; Accepted 23 September 2021
Available online 24 September 2021
2452-2198/© 2021 North-West University. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
B.S. Adeleke et al. Rhizosphere 20 (2021) 100433
To further create insights into the potential of indigenous crop co-inoculation of plant growth-promoting Bradyrhizobium and Azospir
microbiomes for sustainable agriculture, a new framework for the next illum on soybean germination under drought stress has been investigated
green revolution has been proposed to serve as an ecological model in to enhance soybean yield under greenhouse experiments (Silva et al.,
unifying the principles of endophytic research (Chen et al., 2021b). 2019). Similarly, Dubey et al. (2021) reported bioprospecting the
Adopting this approach can help understand plant-bacteria co-evolve endophytic bacteria Bacillus cereus, Pseudomonas sp., and P. otitidis in
ment with promises for a desirable selection of beneficial microbes to enhancing soybean yield under drought stress. Hence, harnessing these
improved yield under drought stress (Tank and Saraf, 2010). Notably, a bacteria should help circumvent some environmental stressors influ
Raman-Stable Isotope Probing (Raman-SIP) and SynComs framework to encing plant performance.
validate the functions of plant microbiome under different conditions for The abundance of rhizobacteria below ground shares some functions
sustainable agriculture with novel insights for future studies have with the root endophytic bacteria. There is direct infiltration of some
recently been documented on beneficial biome (Chen et al., 2021b). rhizosphere bacteria from the external root zone into the internal tissue
To this above premise, three-step have been suggested, which to become endophytes (Nwachukwu et al., 2021). Endophytic bacteria
include; (i) labeling the wild-relative-crop-associated microbes with can be linked to signal networking models and secretion of plant
15
N2 and using Raman-SIP to probe N2-fixing bacteria based on the 15N2- metabolic compounds which facilitate microbial communication in and
induced Raman shifts in carbon-nitrogen (C–N) bonds of cytochrome c out of the root tissues (Soldan et al., 2019). Bacterial endophytes pri
(cyt c), which suggest how nitrogen fixation activity of endophytic marily penetrate plant roots vertically or horizontally by seed inocula
bacteria based on C–N shifts can be determined (Cui et al., 2018), (ii) tion, cell injury, or cracks (Banhara et al., 2015). Many bacteria
sorting, purification, and inoculation of endophytic bacteria represen regarded as root endophytes have been reported to originate from the
tative based on their diversity and N2 fixation. Consequently, there is a rhizosphere (Aloo et al., 2019).
need to take into consideration, the priority effects on crops when An insight into the functioning of a few endophytic bacteria has been
inoculating with SynComs in combined form (Carlström et al., 2019). elaborated using a metagenomics approach (Akinsanya et al., 2015;
Also, growing crops in a clay-based medium that contain soluble organic Mashiane et al., 2017; Fadiji et al., 2020). According to Akinsanya et al.
nitrogen ammonium, or nitrate amended with or without SynComs is (2015), a total of 175 bacterial species from the leaf, 211 from the root,
fundamental. In step 3, the selection of most copious or combined strains and 148 from the stem were reported, revealing diverse endophytic
can further be tested under field conditions. bacteria in the plant root compared to the stem and leaf. A study by
Despite the prospect of these frameworks in plant beneficial biome Fadiji et al. (2020), reported major endophytic bacterial phyla, such as
studies, several limitations surrounding their use have been highlighted Firmicutes, Bacteroidetes, Actinobacteria, Proteobacteria, Acid
in the previous study by Chen et al. (2021b), thus suggesting a future obacteria, Chloroflexi, Verrucomicrobia, Tenericutes, Planctomycetes,
solution to improve the developed Raman hardware and software to Cyanobacteria, and Chlorobi in maize cultivated on organic fertilizer,
facilitate the detection of endophytic bacterial cells of interest from the inorganic and non-fertilizer soils. Furthermore, a diverse bacteria com
downstream procedures. The use of Raman-SIP to unraveled endosphere munity structure in the tissues of Pseudowintera colorata (Mountain
processes in bridging the gap between single-strain and horopito or pepper tree) growing in sub-alpine regions of New Zealand
community-level plant-microbe interactions has been documented has been reported to influence plant growth upon inoculating P. colorata
(O’Banion et al., 2020). Authors proposed that through biotechnological seedlings and antagonism against four different phytopathogenic fungi
advancement, Raman-SIP will be a powerful tool to unravel the poten (Purushotham et al., 2020). Maropola et al. (2015) documented the
tial of endophytic microbiome in agriculture sustainably. relative abundance of major bacterial lineages recovered from com
Endophytic microbes are often referred to as endosphere colonizers posite samples of sorghum root and stem tissues subsequently showing
that complete their life cycle within the tissues of plants without causing their role in enhancing sorghum yield. Several other studies have
harm to the host plants (Santoyo et al., 2016; Adeleke and Babalola, identified agriculturally important endophytic bacteria from the leaves
2020a, 2020b). The functioning of bacteria within plant tissues relies on and seeds of plants (Bilal et al., 2018; Rahman et al., 2018). Seed en
their ability to colonize a complex root matrix and adapt to different dophytes have been reported to exert beneficial effects on the next
environmental conditions (Banik et al., 2019). Plant adaptation to harsh generation of the host plant, for example, plant protection against
environments can increase microbial survival in the endosphere. To this pathogens, releasing seeds from dormancy, seedling growth promotion,
premise, the positive influence of endophytic bacteria in boosting the and enhanced seed germination (Khalaf and Raizada, 2018; Rahman
stress response in plants to environmental stressors can underlie their et al., 2018). These attributes can be the reason why beneficial seed
potential role in formulating bioinoculants (Orozco-Mosqueda et al., endophytes are often transferred from one generation to the other
2021). Based on the prediction of oxidative and nitrosative stress genes (Frank et al., 2017). Diverse seed endophytic bacteria phyla and genera
in diverse endophytic bacteria, such as Stenotrophomonas indicatrix, have been reported (Truyens et al., 2015; Frank et al., 2017). Conse
Bradyrhizobium diazoefficiens, Leifonia sp., and Enterobacter cloacae, it quently, the identification of major endophytic bacterial phyla, Pro
has been recommended that these microbes can stimulate the induction teobacteria, and Firmicutes and genera, Bacillus, Pantoea, Pseudomonas,
of resistance in plants to environmental stressors (Battu and Ulagana Stenotrophomonas, etc. with varied ecological functions, ranging from
than, 2020; Li et al., 2020; Shastry et al., 2020; Adeleke et al., 2021b). beneficial plant-microbe cooperation to antibiosis activity against plant
Factors, such as drought, salinity, humidity, temperature, pathogen, and pathogens have been reported in maize (Mashiane et al., 2018). Addi
soil type have all been shown to influence the microbial population and tionally, Bulgari et al. (2014) reported an endophytic bacterial com
functioning in plants (Adeleke and Babalola, 2020a; Igiehon et al., munity in grapevine leaves with identifiable genera, Sphingomonas,
2021). Also, the influence of plant type, genotype, developmental stage, Burkholderia, Pantoea, and Methylobacterium. According to Lopez-Ve
geographical location, and soil type on bacterial diversity and survival lasco et al. (2013), the abundance of the bacterial phyla Proteobacteria
has been reported (Chen et al., 2019b). Wemheuer et al. (2017) exam was discovered in the seed and leaf endophytes of spinach (Spinacia
ined the influence of agricultural practices on the diversity of endo oleracea).
phytic bacterial communities in the aerial parts of Dactylis glomerata, Despite the advancement of metagenomics in identifying some non-
Festuca rubra, and Lolium perenne over two consecutive years using 16 S culturable microbes, there remains a need for further study of these
rRNA gene amplicon sequencing. microorganisms for possible use in agriculture. Therefore, this review is
The application of plant growth-promoting endophytic bacteria focused on bacterial endophytes associated with plant roots and en
(PGPEB) to improve plant growth in drought-prone regions and deavors to provide up-to-date information on their diversity and agri
nutrient-limiting soils have been investigated under greenhouse and cultural importance. In the sections below, the following shall be
field experimental trials (Banik et al., 2019). For example, the effect of discussed (i) root-colonizing potential of endophytic bacteria and their
2
mechanism of action (ii) plant-endophyte interactions (iii) endophytic 3. Plant-endophyte interactions in promoting plant growth
bacteria as a source of bioinoculants, and (iv) genomic insights into root
endophytic bacteria communities. Plants harbor diverse bacterial communities and their cooperation
contributes to the physiological functions of the host plants (Adeleke
2. Overview of plant root-colonizing endophytic bacteria and and Babalola, 2021). In a natural environment, the interdependent
their mechanism of action cooperation between endophytic bacteria and host plants depends on
the nutrient bioavailability and colonization potential within the plant
Endophytic bacteria colonizing plant roots can be isolated directly tissues. Some examples of identifiable endophytic bacteria genera
from surface-sterilized tissues. The mechanisms used by endophytic include Pseudomonas brenneri, Ewingella Americana, Pantoea agglomerans,
bacteria in plant growth promotion include nitrogen fixation, plant Bacillus cereus, and Pseudomonas otitidis (Babalola et al., 2021; Dubey
growth stimulation via phytohormone synthesis and modulation, side et al., 2021; Rana et al., 2021).
rophore production, induction of systemic resistance, and synthesis of Many PGPEB has been identified and their application in improving
bioactive compounds against phytopathogens (Ngoma et al., 2014). The crop yields has been aimed at ensuring agricultural sustainability
plant growth-promoting potential of endophytic bacteria, for example, (Babalola et al., 2007; Adedeji et al., 2020). For example, Rhizobacter
to produce IAA, has contributed to the growth regulation and develop spp. and other nitrogen fixers have been employed in agricultural
mental processes in plants, which include tissue differentiation, cell management (Etesami, 2018). PGPEB colonizes the root endosphere and
division, and elongation, apical dominance, and responses to light, may benefit plants either by direct or indirect means (Glick, 2012).
gravity, and pathogens (Babalola and Glick, 2012). Also, ACC deaminase Directly, endophytic bacteria enhance plant growth by nitrogen fixation,
production by endophytic bacteria plays a major role in lowering plant modulation of plant hormone levels (auxin, cytokinin, ethylene, and
ethylene levels, thus stimulating plant growth (Glick et al., 2007). The gibberellin), phosphate, iron and potassium solubilization, secondary
highlights of various PGPEB inhabiting the roots of different plants, metabolite synthesis, antibiosis activities against plant pathogens, and
mechanisms used by these bacteria, and the effects of these relationships boosting plant responses to abiotic stresses (Rajini et al., 2020). Some
are presented in Table 1. The presence of special organelles, such as examples of phosphate solubilizing bacterial genera, such as Pseudo
fimbriae or pili in bacteria cells can enhance their attachment to the root monas, Burkholderia, Paraburkholderia, Novosphingobium, and Ochrobac
matrix and subsequently the absorption of soil nutrients for plant use trum have been reported to enhance the biomass yield of Chinese
(Kandel et al., 2017). seedlings based on their multifunctional attributes (Chen et al., 2021a).
Because of the high accumulation of nutrient and exudate secretions The use of root endophytic bacteria in developing bioinoculants has
in the endo-rhizosphere compartments, the root zone is a hotspot pre shown success and their application in modern agricultural practices is
dominated by large numbers of endophytic microbes and other plant promising (Afzal et al., 2019). Several plant growth-promoting bacteria
growth-promoting bacteria (Tsunoda and van Dam, 2017; Glick, 2020). have been studied (Santoyo et al., 2016; Mamphogoro et al., 2020;
High bacterial diversity in the root endosphere compared to the stems Imade and Babalola, 2021; Orozco-Mosqueda et al., 2021). Therefore,
and leaves of plants has been documented (Zhang et al., 2017). Organic harnessing these bacteria in organic farming to enhance agricultural
compounds, such as amino acids, vitamins, and carbohydrates released productivity can help avert future food challenges. Also, the application
from plant roots can act as signaling molecules for root-associated mi of these bacteria in the bioremediation process of environmental pol
crobes to attach to the root surfaces in forming biofilms (Muzzamal lutants, heavy metals, xenobiotics as well as in the production of anti
et al., 2012). The colonization strategies employed by endophytic bac biotics, siderophores, enzymes, and induction of systemic resistance
teria and root nodule bacteria are presented in Fig. 1. Elucidation of the against pathogens has been documented (Glick, 2003, 2010; Glick and
bacterial community across plant organs has revealed their structural Stearns, 2011; Kong and Glick, 2017b; Etesami and Maheshwari, 2018).
dynamic in natural environments (Brijesh Singh et al., 2019). Different Based on the multifaceted roles of endophytic bacteria toward agricul
vascular plants growing in different climatic zones, such as tropical, tural sustainability, additional research would help maximize their po
temperate, cold, and polar harbor one or more bacterial endophytes, but tential in sustainable plant health for improved crop yield.
are less explored (Acuña-Rodríguez et al., 2020). Nevertheless, focusing The use of Bradyrhizobium diazoefficiens and Azospirillum spp. as in
on endosphere research will make information available on PGPEB oculants to enhance crop yield and productivity on a commercial scale
across different climatic regions. For example, findings on endophytic by farmers growing soybean, corn, and wheat in Argentina and Mexico
bacteria from plant species growing in the glacier forefront, rock sides, has been documented (Cassán et al., 2020). Rhizobium-based-biofertil
stream banks, and snow patch communities have been documented and izers via seed inoculation are widely used in organic farming (Wolde-
suggested to have promise for use in sustainable agriculture (Zheng meskel et al., 2018). The cooperation of PGPEB with plant roots can be
et al., 2016). Furthermore, the predominance of bacterial communities achieved naturally or by inoculation. However, to confirm the efficacy
in the roots of different Mediterranean wild legumes growing in tropical of microorganisms on plant growth, it is necessary to re-isolate them
regions has been reported (Muresu et al., 2019). Some of the identifiable after inoculation from the same inoculated plants. Interestingly, endo
PGBEB include Hedysarum carnosum, H. spinosissimum, Ornithopus com phytic bacteria can be engineered in developing biopesticides as
pressus, Rhizobium sullae, Pseudomonas sp., Microbacterium sp., Micro biocontrol agents against plant pathogens (Fadiji and Babalola, 2020b).
bacterium sp., and Pantoea agglomerans (Muresu et al., 2019). Endosphere engineering can further be achieved through the informa
Based on the conservative biodiversity of the endophytic community, tion gained from metagenomics studies.
many hypotheses have been proposed for further investigation into the The mechanisms displayed by microbial endophytes vary, based on
bacterial community structure of vascular plants in tropical, temperate, their type and source. Understanding the mechanisms used by endo
and other regions (Nandini et al., 2018). Many authors have reported phytes is important, as differences in their ability to modulate plant
endophytic bacterial phyla, for example, Actinobacteria, Bacteroidetes, hormone levels and other metabolites can be measured under laboratory
Firmicutes, Acidobacteria, and Proteobacteria from plants growing in conditions (Ambreetha et al., 2018). The bioinoculant application and
the Arctic, cold, tropical, polar, temperate, tropics, and cold regions effect of endophyte application on root development for nutrient ab
(Nissinen et al., 2012; Park et al., 2013; Miguel et al., 2016; Firrincieli sorption in tomato, corn, cotton, and sorghum have been documented
et al., 2020). To this end, additional research studying bacterial diversity (Lin et al., 2018).
across different climatic conditions would help elaborate their potential The mechanisms employed by endophytic bacteria in enhancing
for various agricultural and industrial applications. agricultural productivity are summarized in Fig. 2. The direct mecha
nisms employed by PGPEB, include nitrogen fixation, synthesis of the
phytohormones auxin, cytokinin, gibberellin, and abscisic acid
3
B.S. Adeleke et al.
Table 1
Some plant-associated bacterial endophytes and their mechanisms of action.
Host plant Endophytic bacteria Mechanisms Effects References
Soybean Bradyrhizobium japonicum IAA production, nitrogen fixation Increased root and shoot dry weight, and nitrogen Subramanian et al.
content (2015)
Serratia proteamaculans IAA synthesis, ACC deaminase, acetoin, 2,3-butanediol synthesis Improved root and shoot development Taghavi et al. (2009)
Arabidopsis Paraburkholderia phytofirmans IAA production, induction of salt tolerance Enhanced tolerance to stress, increase root and (Zúñiga et al., 2013;
shoot weight, chlorophyll content Ledger et al., 2016)
Tomato Pseudomonas fluorescens and P. migulae Induction of heat stress response; ACC deaminase, IAA production Enhanced stress tolerance (Ali et al., 2014a; Issa
et al., 2018)
Bacillus pumilis, B. licheniformis, B. megateruim, B. IAA production, secondary metabolite synthesis, antibiosis, siderophore Increase root and shoot length, weight, and the Amaresan et al. (2012)
cereus, Serratia marcescens production, phosphate solubilization, number of secondary roots
Wheat Paraburkholderia phytofirmans Solubilization and recovery of nitrogen, phosphorus, and potassium Enhanced root biomass, plant height, and Aziz et al. (2020)
chlorophyll content
Bacillus cabrialessi Biocontrol activity Phytopathogen control de los Santos Villalobos
et al. (2019)
Bacillus subtilis, Bacillus megaterium Biocontrol activity Suppressed fungal pathogen mycelial growth Pan et al. (2015)
Onion Burkholderia phytofirmans ACC deaminase synthesis, IAA production Enhanced plant vigor and resistance to biotic and Weilharter et al. (2011)
abiotic stresses
Sunflower Stentotrophomonas indicatrix IAA synthesis, phosphate solubilization, siderophore production, secondary Enhanced root number, root length, seed number, Adeleke et al. (2021b)
metabolite synthesis shoot length
Groundnut Chryseobacterium indologenes, Enterobacter cloacae, Nitrogen fixation, IAA and ACC deaminase production, siderophore production, Increased root and shoot length and weight Dhole et al. (2016)
Klebsiella pneumoniae, Pseudomonas aeruginosa, phosphate solubilization
4
Enterobacter ludwigii
Millet Bacillus amyloliquefaciens, B. subtilis, B. cereus Zinc, potassium and phosphate solubilization, siderophore production, antibiosis Enhance root length, weight, percent disease index, Kushwaha et al. (2020)
against Fusarium solani, Rhizoctonia solani, and Sclerotium rolfsii, protease, and disease over control
amylase, lipase, chitinase, pectinase production
Cotton Pantoea spp, Empedobacter spp, Enterobacter spp, Biocontrol activity, siderophore and IAA production, protease, chitinase, Enhanced shoot and root length, germination, and (Li et al., 2010, 2012)
Rhizobium spp, Klebsiella spp. cellulose, pectinase production vigor index
Potato Klebsiella oxytoca, Pseudomonas marginalis, P. Amylase, cellulase, protease, and phosphatase production, biocontrol against Suppressed fungal pathogen mycelial growth Boiu-sicuia et al. (2017)
viridilivida, Bacillus endophyticus, B. atrophaeus/subtilis plant fungal pathogens
Burkholderia vietnamiensis Nitrogen fixation Enhanced yield biomass Shinjo et al. (2018)
Hopbush Streptomyces alboniger, Bacillus idriensis, Pseudomonas Ammonia production, hydrogen cyanide, and siderophore production, phosphate Enhanced root length Afzal et al. (2017)
taiwanensis, P. geniculate solubilization, ACC deaminase, IAA production, cellulase, protease, pectinase,
chitinase
Peanut Bacillus velesensis Siderophore production, phosphate solubilization Inhibition of fungal pathogen mycelial growth, Chen et al. (2019a)
seedling height, seedling dry weight, root length,
and root dry weight
Sugarcane Gluconacetobacter diazotrophicus IAA synthesis, nitrogen fixation Enhanced biomass yield Bertalan et al. (2009)
Kosakonia radicincitans Nitrogen fixation, secondary metabolite synthesis, siderophore production, IAA Enhanced root length and plant weight Beracochea et al. (2019)
biosynthesis
Rice Pantoea ananatis IAA and siderophore production Increased plant growth and crop yield Megías et al. (2016)
Poplar Stenotrophomonas maltophilia, Pseudomonas putida ACC deaminase, IAA synthesis Improved root and shoot development Taghavi et al. (2009)
Rhizosphere 20 (2021) 100433

Cape Achromobacter xylosoxidans ACC deaminase Increased germination percentage and root weight (Karthikeyan et al.,
periwinkle under saline conditions 2012; Wu et al., 2021)
Fig. 1. Bacterial dynamics and root nodules containing endophytes. Key: RNE – root-nodule endophytes.
Fig. 2. Mechanisms used by PGPEB and agricultural importance. a - plant immunity/survival, b - plant growth promotion, c - agricultural importance.
(Maheshwari et al., 2019). Also, lowering of ethylene by the enzyme promote plant growth indirectly (Santoyo et al., 2016). The enzyme ACC
1-aminocyclopropane-1-carboxylate (ACC) deaminase and the solubili deaminase is one of the key attributes of endophytic bacteria in stimu
zation of minerals (zinc, iron, phosphorus, sulfur, and potassium) and lating plant growth under high concentrations of toxic metals (Gamalero
the increased survival under stress conditions, such as drought and soil and Glick, 2012; Kong and Glick, 2017b; Pandey and Gupta, 2019).
salinity (Dubey et al., 2021). Also, the ability of PGPEB to produce These abiotic stressors are of particular agricultural importance in less
organic acids, enzymes, antimicrobial compounds such as antibiotics than favorable soils or climate conditions. Some endophytic bacteria can
and cyanide, induce systemic resistance and produce siderophores all modulate root-bacteria and bacteria-bacteria interactions due to their
5
ability to fix nitrogen in the soil and the major group of bacteria found in functions but are different in terms of abundance and diversity (Bergna
this category are rhizobia inhabiting the nodules of plants (See Fig. 1). et al., 2018). The plant growth-promoting bacteria found in the root
The α- and β-rhizobia, such as Rhizobium tropici and Cupriavidus taiwa nodules of leguminous plants can function in fixing atmospheric nitro
nensis colonizing root nodules of Phaseolus vulgaris and Mimosa pudica gen for plant use (Naik et al., 2019).
have been identified as nitrogen-fixing bacteria (Bomfeti et al., 2011). Many bacterial endophytes can be cultured and can be directly
1-aminocyclopropane-1-carboxylic acid (ACC) deaminase-producing applied to crops either by spraying, seed, or root inoculation. Also,
endophytic bacterium, Pseudomonas fluorescens, however, can lower endophytic microbes can be used to combat phytopathogens as an
ethylene levels in plants and this has been shown to play an important alternative to pesticides and insecticides (Fadiji and Babalola, 2020a).
role in facilitating the nodulation process of α- and β-rhizobia (Nasci Bacterial root colonization is determined by bacteria strain, host geno
mento et al., 2019). Furthermore, endophytic bacteria can indirectly type, soil pH, soil type, drought, salinity, root architecture, soil nutri
enhance plant growth by stimulating plant responses or producing sec ents, etc. The pattern of bacterial colonization in the root endosphere
ondary metabolites against phytopathogens (Santoyo et al., 2012). One differs from one bacterium to another. Endophytic bacteria may enter
such indirect technique is the induction of systemic responses (ISR) plant tissue via roots, stems, leaves, flowers, and cotyledons (Ambele
which can be achieved through specific plant response pathways e.g., et al., 2020). Findings have shown different entry modes and coloniza
the jasmonic acid (JA) pathway (van Loon and Glick, 2004; Asghari tion patterns of different endophytic strains (Omomowo and Babalola,
et al., 2020). Stimulation of plant defense responses through signaling 2019; Fouda et al., 2021). The secretion of lytic enzymes, cell wall
pathways in endophytic bacteria has been reported by Montejano-R degrading enzymes, and cellulases by endophytic bacterial strains can
amírez et al. (2020). The authors investigated the antifungal compound facilitate the entry of a bacterial strain by hydrolyzing the external
(N, N-dimethyl hexadecyl amine) produced by the facultative endo covering of plant cells (Toghueo and Boyom, 2021). A study by Rein
phytic bacterium Arthrobacter agilis. This compound modulates the hold-Hurek et al. (2006) revealed the colonization potential of the
expression of genes involved in low-response, defense, and iron con endophytic bacterium Azoarcus sp. in the root endosphere was due to
centrations in Medicago truncatula infected with phytopathogens, such as endoglucanase biosynthesis and the presence of the eglA gene. Similar
Botrytis cinerea, and Pseudomonas syringae without involving the JA reports have been documented by Suzuki et al. (2005) on the biosyn
pathway. thesis of a nonspecific wax-degrading enzyme by Streptomyces galbus,
Additionally, the compound IAA produced by endophytic bacteria which enhances the colonization of the Rhododendron endosphere by
can directly contribute to plant physiological functions, such as growth this bacterium. The colonization pattern of endophytic bacteria, such as
promotion, lateral root formation, increase in biomass yield in terms of Paraburkholderia phytofirmans, and Ralstonia solanacearum by attach
below and aboveground parameters, and chlorophyll pigmentation ment, and invasion of the root regions through the exodermis layer have
(Santoyo et al., 2016). Subsequently, to further discuss the direct and been reported to facilitate subsequent bacterial entry and survival, and
indirect mechanisms of PGPEB and their bioprospecting in agricultural use of plant nutrients as a source of carbon (Afzal et al., 2019). In
biotechnology, we recommend a few recently published review articles addition, all of the mechanisms for the successful establishment of
and books (Adeleke and Babalola, 2021; Eid et al., 2021; Wu et al., bacteria as endophytes rely on their ability to utilize certain metabolites
2021). These mechanisms help in understanding the coexistence be secreted from plants.
tween endosphere bacterial communities and host plants. Biofertilization in agriculture is considered safe and environmentally
friendly. The use of bacterial endophytes as bioinoculant has the po
4. Plant root endophytes and bioinoculant synthesis tential to immensely contribute to crop production since these organ
isms exhibit a strong affinity for their host plants (Mahanty et al., 2017).
Roots are specialized organs that provide mechanical support to Intensive agriculture using chemical fertilizer in large amounts has no
plants in the uptake of nutrients from the soil (Ahkami et al., 2017). The doubt resulted in a manifold increase in the productivity of farm com
plant supporting tissue (xylem and phloem) in the roots can facilitate the modities, but the adverse effect of these chemicals are visible to soil
absorption and movement of nutrients and water directly from the soil structure, endo-rhizosphere biodiversity, water bodies, persistent in the
to the stem and other parts of the plant (Feng et al., 2019). The ability of food chain, and human health (Ngwira et al., 2013). Hence, organic
root-associated endophytic bacteria to produce IAA can enhance root farming using organic fertilizer in enhancing biodiversity can be
development, thus contributing to plant nutrition in absorbing nutrients instrumental in enhancing biodiversity as the best substitute for chem
from the soil (Adedeji and Babalola, 2020). Injury to plant roots allows ical fertilizer. To successfully achieve this, the real potential of organic
free release of root exudates containing fixed carbon in the form of agriculture on biodiversity requires a stronger shift to a systems
polysaccharide mucilage to the soil environment and these compounds approach, based on an improved understanding of ecosystem functions
can serve as a chemoattractant and source of energy to the microor (Akanmu et al., 2021). Therefore, incorporation of organic fertilizer,
ganisms around the root (Adeleke and Babalola, 2021). Like soils, plant such as compost, manure, animal waste, and biofertilizers into the soil
roots harbor a consortium of bacteria in the endosphere compartments can play a major role in improving soil fertility by supplying micro-and-
(Wang et al., 2019). The root architectural system and rhizodeposition macro-nutrients as major plant nutrients, which favor healthy root
of nutrients can modulate the activities of root endophytic bacteria in growth (Fasusi et al., 2021). In addition, organic fertilizers increase
the endo-rhizosphere regions. Regardless of the plant regions colonized microbial activity in the endo-rhizosphere region, which helps free up
by endophytes, they may exhibit similar functions in crop breeding other nutrients in addition to those provided by the fertilizer. Subse
(Hashem et al., 2019). quently, soil amended with biofertilizers can enhance nutrient avail
The root systems serve as an excellent source of nutrients for endo ability to crop plants and boost plant and soil health for higher crop
phytic bacteria and form an interface for plant-bacterial interactions in a yields sustainably (Mahanty et al., 2017).
given econiche. Excessive rhizodeposition of root exudates containing Furthermore, for effective production of bioinoculants on a com
metabolite compounds, such as terpenoid, phenol, alkaloids, proteins, mercial scale, selection of appropriate carrier and bacterial strains is
and peptides have been reported to influence belowground bacterial required. In addition, bacteria in the plant endosphere can be difficult to
diversity (Imade and Babalola, 2021). Apart from the roots of plants, isolate due to the complex environment in which they are found.
endophytic bacteria also colonize other parts of the plants. For example, Nevertheless, findings into diverse bacterial community structures in the
the identification of endophytic bacteria colonizing the leaves and stem roots of soybean, corn, sorghum, tomatoes, millet, wheat, and cherry
of plants has been reported (Cao et al., 2004; Akinsanya et al., 2015; have been reported using 16 S rRNA gene amplicon sequencing (Berg
Mahlangu and Serepa-Dlamini, 2018; Zakaria and Aziz, 2018). The et al., 2015). Furthermore, employing metagenomics techniques in
bacterial populations found in various plant organs often share similar evaluating unculturable endophytic bacteria should provide additional
6
opportunities to harness PGPEB for use in agriculture and further surface sterilization, DNA extraction from the sterilized plant tissues,
studies. and, finally, sequencing either the 16 S rRNA gene amplicon or shotgun
metagenome to determine bacteria taxonomy. The metagenomics and
5. Genomic insights into root endophytic bacteria communities functional profiling of diverse bacterial endophytes in plants, such as
maize, rice, sorghum, and cowpea have been investigated by several
Genomic insights into endosphere biology have significantly researchers (Maropola et al., 2015; Kunda et al., 2018; de Araujo et al.,
increased our understanding of root endophytic bacteria and their 2019; Fadiji et al., 2020). The specific functions of maize inhabiting
functioning in plant growth promotion and crop protection (Adeleke endophytes, which include nitrogen metabolism, stress response, po
et al., 2021b). Diverse approaches in assessing endophytic bacterial tassium, and phosphorus metabolism, iron acquisition, and metabolism
communities have been documented in the literature. Hence, it is have been reported by Fadiji et al. (2020). Based on the putative func
important to adopt appropriate techniques in studying bacterial endo tions of these bacteria, the authors have recommended the use of
phytes inhabiting the root endosphere. In this regard, the two ap culture-dependent methods in identifying these bacteria for further
proaches widely adopted include culture-dependent and exploration in sustainable agricultural systems.
culture-independent techniques. Culture-dependent approaches Metagenomic techniques are promising without bias compared to
include direct culturing of relevant bacteria while culture-independent culture-dependent methods in culturing prokaryotes, but with limita
approaches include shotgun metagenomics, proteomics, metabolomics, tions, among which are, the extra cost of depleting host DNA for
and meta-transcriptomics (Maropola et al., 2015; Selvin et al., 2019). sequencing, the presence of plant DNA, the low efficiency of endophytic
The section below provides a brief overview of the metagenomics of DNA extraction or amplification of the 16 S rRNA. Small amounts of
endophytes. To isolate endophytic bacteria from plant organs such as bacterial DNA sometimes result after DNA extraction (Bulgarelli et al.,
leaves, roots, and stems, surface sterilization of the plant tissue is 2013). These limitations might be the reasons why limited success has
important before plating on appropriate media. Culture-dependent been recorded using shotgun metagenome sequencing to investigate
methods have been widely employed due to their low cost, ease of endosphere bacterial communities in plants. Hong et al. (2019) per
performance, and effectiveness in obtaining pure bacterial cultures for formed a metagenomic analysis of the bacterial endophyte community
further characterization of bacteria morphology, phylogeny, physiology, structure and functions in Panax ginseng at different ages and identified
and biochemistry (Pei et al., 2017). important putative genes involved in iron acquisition and metabolism,
It is often difficult to assess diverse bacteria communities in the plant metabolite metabolism, stress response, nitrogen fixation, and side
endosphere due to the varied growth parameters required for culturing rophore production which might contribute to bacterial functions in
them. For instance, the growth of oligotrophic endophytic bacteria on plants. Similarly, Tian et al. (2015) employed a metagenomics approach
solid media is often outcompeted by the copiotrophic endophytes due to in studying endophytic bacterial communities and functions in tomatoes
their ability to utilize nutrients in synthesizing antibiotics (Okunishi and found that they possess secondary metabolite genes which suggest
et al., 2005). To successfully isolate endophytic bacteria from the plant that they may suppress nematode infection in tomato roots.
endosphere, the procedures involved are (i) surface sterilization of plant The genetic composition of bacteria in the root endosphere may
tissue using disinfectants such as 3% hypochlorite, 70% ethanol, a differ from the bacterial genetic composition in the whole plant, but
combination of mercury chloride and ethanol. These disinfectants are with similar structural diversity and metabolic activities (Stefan et al.,
used to remove unwanted or contaminating microbes from the plant 2018). Genetic analysis of many plant-associated microbes has revealed
surfaces. The efficient use of Tween 20 or Tween 80 to reduce the surface the structural composition and functions of the bacterial community in
tension of solvents has also been used (Romero et al., 2014). Depending the endo-rhizosphere compartments (Beckers et al., 2017). The use of
on the plant material, sterilization time with ethanol and hypochlorite is next-generation sequencing in the identification of bacteria genera
usually from 30 s to 10 min. Furthermore, the samples are typically associated with the roots of plants have been reported, which include
rinsed several times with distilled water to remove the chlorinated maize (Potshangbam et al., 2017), sorghum (Correa-Galeote et al.,
compounds that may later induce mutagenesis and cell death. Alterna 2018), millet (Manjunatha et al., 2019), and soybean (Yang et al., 2018).
tively, sodium thiosulfate has been reported to decrease the damaging Similarly, several methods have been employed in the identification of
effects of hypochlorite on bacterial cells, suggesting its suitability in novel genes from bacteria colonizing the root endosphere and a few of
preparing gnotobiotic models (Miché and Balandreau, 2001). Following the specific functional genes have been revealed in field experimental
an appropriate sterilization procedure helps to prevent the penetration studies (Afzal et al., 2019). For example, the identification of multiple
of the disinfectant into the plant endosphere and the removal of genes responsible for plant growth promotion in endophytic Bacillus
epiphytic microbes. A sterility check is usually performed by plating the toyonensis COPE52 and B. thuringiensis CR71 which upon inoculation
last rinse of water on appropriate bacteriological solid media, such as under greenhouse conditions has been reported to enhance the yield of
nutrient agar. blueberry (Vaccinium spp.) and cucumber (Cucumis sativus) (Con
Copiotrophic endophytic are a group of endophytes that require a treras-Pérez et al., 2019; Flores et al., 2020). Also, a bioinformatics study
nutrient-rich medium for growth. This notwithstanding, endophytic by Ali et al. (2014b) reported a set of functional genes involved in
bacteria are often referred to as oligotrophs that require specific media determining the endophytic behavior of Burkholderia spp. Hence, pre
for growth. For example, the use of nutrient agar for culturing endo diction of plant growth-promoting genes involved in the synthesis of IAA
phytic bacteria from Aloe vera has been reported (Youssef et al., 2016). (dha and trp), enzyme production (lon, amy, and pul), phosphate solu
Growing bacterial endophytes in a rich and minimal medium may be bilization (ppx and pho), bacterial attachment (flg, flh, fli, and mot),
influenced by the media nutrient composition. Hence, devising inno biological control by secreting volatile compounds (i.e., acetoin, 2,3
vative culture approaches will help obtain sufficient data from unculti -butanediol (ilv), biofilms (efp, hfq, bcs, yhj, and crp), plant protection
vable endophytic microbes in future research. against oxidative and nitrosative stress (sod, kat, bsa, and grx), side
Recent research is focused on the metagenomics approach in rophores (fbp fiu, and fet), cytokinin biosynthesis (mia), and ammonia
studying bacterial communities of the root endosphere. Employing production (nad) in the bacterial genome can be inferred to confirm the
metagenomics is promising because it helps to identify the role of bac activities of these bacteria through inoculation experiments (Zaferanloo
terial endophytes in various plant biological processes, including nitri et al., 2013; Adeleke et al., 2021a; Singh et al., 2021). Furthermore,
fication, phytoremediation, biodegradation, plant growth promotion, molecular analysis of endophytic bacteria from plant roots can enable
and suppression of phytopathogens (Li et al., 2018). scientists to determine genomic sequences that reveal important func
Culture-independent techniques first begin with the collection of tions of these microbes via online analytical software.
healthy plant materials, washing these tissues with distilled water, Research into diverse bacterial communities in some plants using
7
culture-dependent methods has been reported (Puri et al., 2018), how combined nanoscale secondary ion mass spectrometry techniques
ever, only a very small portion (1%) of the microbial population in these (NanoSIMS) combined with advanced Raman spectroscopy-based single
samples has been identified. The use of a metagenomics approach in cell-based methods can be employed in the study of plant-endophyte-
studying endophytic bacteria is relatively new and has not yet been fully interactions in situ, and biological functions in the removal of complex
explored. Several hypotheses exist regarding the use of metagenomic pollutants from the contaminated soil. Hence, the concept of this
analysis of root-associated endophytic bacteria. A metagenomic study of biotechnological advancement in establishing a strong plant-microbial
a transgenic Bacillus thuringiensis (Bt) cry maize cultivar and its isogenic framework may create insights for future endosphere research with
parental line (i.e., a non-Bt maize cultivar) revealed that the most promises in solving agricultural problems.
dominant Proteobacteria in the Bt maize endosphere were similar to
those in the non-Bt maize cultivar (Mashiane et al., 2017). While this Authors’ contributions
phenomenon appears universal, the challenges associated with the use
of culture-independent techniques in culturing endophytic bacteria have B.S.A and O.O.B had the idea for the article and suggested the review
caused some technical difficulties. Therefore, employing a meta topic; B.S.A. performed the literature search and wrote the first draft; O.
genomics approach in studying diverse endophytic bacterial commu O.B and B.R.G made substantial technical and intellectual contributions
nities would help scientists to develop bioinoculants that can be applied to the structure of the various drafts of the manuscript. All authors
in the field for improved crop production. For instance, based on the approved the article for publication.
functional traits of some identifiable bacteria endophytes, a field
experiment performed by Hungria et al. (2010) using singularly or Declaration of competing interest
combined applied endophytic Azospirillum brasilense and A. lipoferum as
bioinoculants found that these strains contributed significantly to the The authors declare that they have no known competing financial
yield of maize and wheat in Brazil. interests or personal relationships that could have appeared to influence
the work reported in this paper.
6. Conclusion and future prospects
Acknowledgment
Endospheric communities are groups of microorganisms colonizing
the internal tissues of plants without causing any deleterious effects to B.S.A. thanked the National Research Foundation of South Africa and
the host plants. Understanding the mechanisms employed by PGPEB in The World Academy of Science (TWAS) for the NRF-TWAS African Re
plant growth promotion is fundamentally important and this can be naissance Doctoral scholarship (UID: 116100). O.O.B. acknowledges the
conventionally investigated in vitro. Endophyte interdependence with National Research Foundation of South Africa for the grants (Grant
their host plants contributes to their effectiveness under different envi numbers: 123634; 132595), supporting research in her laboratory.
ronmental conditions. On a commercial scale, harnessing endophytic
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Rhizosphere 20 (2021) 100433

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Plant growth-promoting root-colonizing bacterial endophytes

Rhizosphere 20 (2021) 100433

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