Download Applied Biochemistry and Microbiology

ISSN 00036838, Applied Biochemistry and Microbiology, 2015, Vol. 51, No. 3, pp. 271–277. © Pleiades Publishing, Inc., 2015.
Original Russian Text © V.K. Chebotar, N.V. Malfanova, A.V. Shcherbakov, G.A. Ahtemova, A.Y. Borisov, B. Lugtenberg, I.A. Tikhonovich, 2015, published in Prikladnaya Biokhimiya
i Mikrobiologiya, 2015, Vol. 51, No. 3, pp. 283–289.
Endophytic Bacteria in Microbial Preparations
that Improve Plant Development (Review)
V. K. Chebotara, b, N. V. Malfanovaa, c, A. V. Shcherbakova, b, G. A. Ahtemovaa, A. Y. Borisova,
B. Lugtenbergc, and I. A. Tikhonovicha
a AllRussia
b
Research Institute for Agricultural Microbiology, Pushkin, 196608 Russia
International Research Center “Biotechnology of Third Millennium,” Saint Petersburg National Research University
of Information Technologies, Mechanics and Optics (ITMO University), St. Petersburg, 191002 Russia
c
Institute of Biology, Leiden University, Leiden 2333, BE 8 Netherlands
email: [email protected]
Received August 20, 2014
Abstract—In this review data on the possibility of using endophytic bacteria for improving crop yields and
quality are discussed.
Keywords: endophytic bacteria, plant associations with microorganisms, inoculation of endophytic microor
ganisms
DOI: 10.1134/S0003683815030059
INTRODUCTION
The association of plants with microorganisms that
do not suppress or even stimulate their development
attracts the attention of scientists, not only as the
object of study with respect to the fundamentals of the
coexistence and interaction of different organisms but
also because of their possible use in the practice of an
environmentally oriented production of agricultural
products.
Every microorganism associated with a plant
organism is an evolutionarily verified component of a
complex plant–microbial system beyond the scope of
a single plant [1], and it has a significant impact on the
biological structure and functioning of the entire sys
tem [2]. Microorganisms existing within the plant,
including aboveground and underground parts and
seeds, that positively affect plant development are
defined as endophytic. They use the internal environ
ment of the plant (endosphere) as a unique ecological
niche, protecting them from changes in the environ
ment, and they formed as a result of hundreds of mil
lions of years of evolution [3, 4]. These organisms can
be transmitted through generations, from ancestor to
descendent, as an integral part of the plant organism
endosphere.
Only microorganisms capable of colonizing the
internal tissues of plants without causing disease and
adversely affecting plant development are endophytic
[5, 6]. In the world there are about 300000 species of
plants, and each species may be a host for one or more
species of endophytic microorganisms. However, until
recently only some microorganisms across several
plant species have been sufficiently studied [7, 8]. Cur
rently, the attention of scientists is devoted to endo
phytic fungi [9] and bacteria [10, 11].
In the last decade, a majority of agriculturally ori
ented research has been aimed at studying rhizosphere
microorganisms [12–14]. Among these organisms,
bacteria are the most technologically advanced, both
in terms of production and the use of microbial prep
arations in agriculture. [15] This opens up prospects
for the use of prokaryotic microorganisms beneficial
for plant development under different conditions [10].
Endophytic bacteria colonize the same ecological
niche in the plant as pathogens, and therefore they are
used as a promising biological method to control plant
pathogens, i.e. they are socalled “biocontrol” agents
[14, 16, 17]. It was established that bacterial endo
phytes are capable of inhibiting the development of
phytophagous insects [18] and nematodes [19, 20] via
the synthesis of biologically active compounds with
“antipathogenic” action. The study of the “biochem
ical weapons” of such bacteria will allow the isolation
and purification of those chemical compounds that
can be used for the production of new preparations to
combat plant, animal, and even human diseases [7, 8].
Some strains of endophytic bacteria are used for the
phytoremediation of soils, i.e. the purification of tech
nologically contaminated areas by the production of
special plant–bacterial systems [10, 21–25].
This review discusses the literature data on endo
phytic bacteria and their use in the development of
new microbial preparations that can be used in agri
culture.
271
272
CHEBOTAR et al.
Biodiversity of Endophytic Bacteria
The endophytes’ niche can be occupied only by
those bacteria that are able to colonize different parts
of the intercellular spaces of plants, even seeds. The
classic biodiversity studies of endophytic bacteria are
based on characteristics of isolates obtained from var
ious internal tissues of different plants after steriliza
tion of their surface [26, 27]. Bacterial endophytes
include both Grampositive and Gramnegative spe
cies isolated from a wide range of host plants [28, 29].
Endophytic bacteria were isolated from both mono
cots and dicots; woody plants, such as oak (Quercus L.)
and pear (Pyrus L.); and herbaceous plants, such as
sugar beet (Beta vulgaris L.) and maize (Zea mays L.)
[30]. Thus, analysis of the tissues of the aboveground
parts of spring crocus (Crocus vernus (L.) Hill) demon
strated the presence of a previously known bacterial
endophyte community, as well as those that had not yet
been identified [31].
A study of microbial endophyte communities that
inhabit the stems, roots, and tubers of agricultural
crops with an analysis of 16S RNA sequences and fatty
acids compositions, as well as the utilization of various
carbon sources, revealed that they are represented by
the genera Cellulomonas, Clavibacter, Curtobacterium,
Pseudomonas, and Microbacterium [32].
The high density of cultured endophytic bacteria
was detected in seedlings of poplar (Populus L.),
spruce (Picea A. Dietr.), and larch (Larix Mill.) grown
from tissue cultures [33]. Based on the analysis of
16S RNA sequences, most of these isolates were
assigned to the genus Paenibacillus, to a species close
to P. humicus, which were accumulated in tissues in
vitro without any apparent adverse effect on plants.
Endophytic bacteria of the genera Methylobacterium,
Stenotrophomonas, and Bacillus were also found.
Sequence analysis of the 16S RNA gene from the
endophytic bacteria of rice (Oryza sativa L.) showed
that they belong to different Proteobacteria subclasses
(including the genera Cytophaga and Flexibacter), as
well as the groups DeinococcusThermus, Acidobacte
ria, and Archea. The most numerous were the Betapro
teobacteria group (27% of all isolates), in which the
genus Stenotrophomonas dominated. About 15% of all
isolates belonged to uncultivated bacterial species [34].
A study of endophytic bacteria in the stem of maize
grown in Indian tropics [35] showed that the bacteria
are present for the whole growing period and the bac
terial count is 1.36–6.12 × 105 CFU/g raw biomass
(CFU is the colonyforming unit, e. g. the number of
cells capable of growth on artificial media). The fact
that Bacillus pumilus, B. subtilis, Pseudomonas aerugi
nosa, and P. fluorescens dominated in bacterial isolates
was established based on a chromatographic analysis
of fatty acids [35].
As the result of the study of maize (Zea mays L.),
sorghum (Sorghum vulgare Moench), soybean (Gly
cine max (L.) Merr.), wheat (Triticum vulgare L.), and
a number of wild plants (grasses and leguminous
grasses), 853 bacterial endophytes strains were iso
lated; about half of these strains were Grampositive,
and the rest were Gramnegative bacteria. An analysis
of the fatty acid composition made it possible to assign
the endophyte isolates to 15 genera: Agrobacterium,
Bacillus, Bradyrhizobium, Cellulomonas, Clavibacter,
Corynebacterium, Enterobacter, Erwinia, Escherichia,
Klebsiella, Microbacterium, Micrococcus, Pseudomo
nas, Rothia and Xanthomonas. Bacillus, Corynebacte
rium, and Microbacterium were dominant [36]. Endo
phytic bacteria of the genera Cellulomonas, Clavi
bacter, Curtobacterium, and Microbacterium, which
were isolated from both cultivated and wild plants,
colonized mainly maize and sorghum [36].
Thus, the data presented above make it possible to
evaluate the extent of the diversity of bacterial endo
phytic microbial flora existing in complex mutually
beneficial plant–microbe systems and the number of
isolates capable of growth on artificial media.
Artificial Inoculation of Endophytic Bacteria
and Colonization of Plant Endosphere
The study of artificial inoculation of plants with
bacterial endophytes previously isolated as a culture is
the basis for the selection of the most promising
strains for technological applications. Special meth
ods were developed to analyze the ability of endo
phytic bacteria to colonize the endosphere after the
inoculation of leaf surfaces and the fruit cocoa tree
(Theobroma cacao L.) [37].
It turned out that, after the inoculation of maize with
the dominant bacterial endophyte strains (B. pumilus,
B. subtilis, P. aeruginosa and P. fluorescens), the total
bacterial count in seedlings grown in the greenhouse
was lower (1.6–3.1 × 105 CFU/g raw stem biomass)
than in seedlings grown under field conditions (1.8–
3.6 × 105 CFU/g). The highest density of endophytic
bacteria (3.1 × 105 CF /g) was observed 28 days after
inoculation with B. subtilis [35]. This finding indicates
the regulation of interactions with certain endophytic
bacteria by plants and the existence of specific pairs of
bacteria host plants.
Methods of in vivo analysis of biological material
are required for research on the structural changes of
plant endospheres and the spatial distribution of
microorganisms in the course of development and
operation of plant–microbe systems. One such marker
system includes labeling with green fluorescent protein
(GFP), which allows the detection and counting of
microbial organisms in situ on the surface and inside
plants in various laboratory, field, and environmental
studies [38–41]. GFPtagged bacterial cells can be eas
ily identified by epifluorescent microscopy with a con
focal laser scanning microscope [23, 42]. This system
proved to be very informative for monitoring the colo
nization of internal plant tissues with pseudomonads
[39, 40].
APPLIED BIOCHEMISTRY AND MICROBIOLOGY
Vol. 51
No. 3
2015
ENDOPHYTIC BACTERIA IN MICROBIAL PREPARATIONS
Endophytic bacteria cells colonizing internal plant
tissues can also be visualized with the βglucuronidase
(GUS) reporter system. The GUStagged strain
Herbaspirillum seropedicae Z61 was used for artificial
inoculation of rice seedlings. The most intensive
GUSstaining was observed in coleoptiles, lateral
roots, and lateral root connections to the main root.
This H. seropedicae strain colonized intercellular
spaces, aerenchyma, and cortical cells, and some
microbial cells penetrated to the stele and further into
the vascular tissue [43].
The most successful colonization of the plant by
endophytic bacteria requires a corresponding (“the
most complementary”) host plant. Thus, it was shown
that the obligate nitrogenfixing endophyte Azoarcus sp.
BH72 strain induces the defense mechanisms of the
host plant and complicates the colonization of rice by
other endophytic bacteria [44]. In other words, the
system endophyteplant acquires new adaptive fea
tures not typical for organisms outside the system.
Influence of Bacterial Endophytes
on Plant Growth and Development
An investigation of the influence of endophytic
bacteria on plant development [10] showed that endo
phytes are different from biocontrol strains of rhizo
sphere bacteria, since they not only inhibit the growth
of pathogenic microorganisms but also stimulate the
growth of plants. Endophytic bacteria are able to
improve the nitrogen and phosphorus nutrition of
plants [45–48], produce auxins [49], and synthesize
vitamins [50] and siderophores [51]. Furthermore, it
was shown that endophytic bacteria can regulate
osmotic pressure and operation of the stomata or
modify plant root development [33, 47], improving
the general condition of the plants. Therefore, it is
advisable to develop economically viable methods of
exploiting this ability of endophytes in various fields of
human activity associated with the cultivation of
plants, such as crop production, forestry, landscaping,
and others.
The Ability of Endophytic Bacteria
to Control the Development of Plant Diseases
(“Biocontrol Activity”)
The “biocontrol activity” of microorganisms is
defined as their ability to reduce populations of target
species of antagonistorganisms via a variety of eco
logical mechanisms, including pathogenesis, compe
tition within the ecological niche, and the production
of various compounds that slow their growth and
development [52].
Endophytic bacteria are capable of reducing or
preventing adverse effects of phytopathogens on plants
[33, 53]; therefore, the artificial inoculation of plants
with endophytic bacteria can significantly reduce the
effect of pathogenic fungi, bacteria, viruses, insects,
APPLIED BIOCHEMISTRY AND MICROBIOLOGY
273
and nematodes [29, 54–56]. It was suggested that cer
tain types of endophytic bacteria activate plant defense
mechanisms, which ensure their overall resistance to
microorganisms and parasites [10, 57].
It was shown that 9 out of 137 isolates of bacterial
endophytes isolated from the tissues of stems, roots, and
nodules of soybean in vitro inhibited the growth of
pathogenic fungi Rhizoctonia bataticola, Macrophomina
phaseolina, Fusarium udum and Sclerotium rolfsii [58].
Other studies have shown that 36 out of 60 bacterial
endophytes isolated from nodules of the wood legume
Sophora alopecuroides L. inhibited the growth of the
fungal pathogen Verticillium dahlia on artificial media
[59]. It was also demonstrated that both living cultures
and the thermostable components of the culture fluids
of 4 endophyte isolates of B. subtilis and one isolate of
Burkholderia sp. inhibited the development of F. circi
natum, inducing cancer of the pine (Pinus taeda L.)
[60]. During the development of the biological control
methods of the nematode Meloidogyne incognita, it was
found that 4 out of 19 bacterial strains of endophytes
(genera Bacillus, Pseudomonas and Methylobacterium)
isolated from various agricultural crops had a negative
effect on its development. Even filtrates of their culture
supernatant reduced the quantity of “adult females”
and egg weight [61].
However, the search for endophytic bacteria of
coffee plants (Coffea arabica L. and Coffea robusta L.)
that suppress the development of the leaf pathogen
fungus Hemileia vastatrix Berk. Br. revealed that iso
lates can suppress or enhance the development of the
disease [62].
Thus, when using hightechnological endophytic
bacteria from different plant species for biological
control, we should remember that pathogens are evo
lutionarily verified components of complex plant
microbe systems, and not all endophytes are their
antagonists.
In recent years, a number of papers were published
that describe the isolation of bacterial endophytes and
the characterization of their biocontrol activity [10, 11].
Some of them contain analyses of the biocontrol activ
ity of various combinations of endophytic fungi and
bacteria [63]. However, the possibility of using micro
bial preparations based on such organisms in agricul
ture, forestry, and landscaping and the technology of
their production currently remain understudied.
Endophytic Bacteria—Producers
of “Secondary Metabolites”
Many endophytes represent soil bacteria of the
genera Pseudomonas, Burkholderia, and Bacillus [27],
which are well known as producers of “secondary
metabolites” such as antibiotics, anticancer drugs,
volatile organic compounds, and fungicidal, insecti
cidal, and immunosuppressive agents.
An investigation of the “secondary metabolites” of
the endophytic bacteria of medicinal plants [64], based
Vol. 51
No. 3
2015
274
CHEBOTAR et al.
on the hypothesis that endophytes determine their
healing properties, may open up new possibilities for
“biochemical” pharmacology.
The chemical nature of the biologically active sub
stances produced by bacterial endophytes is very
diverse, and a discussion of the whole spectrum within
this review, which is dedicated to the use of endophytic
bacteria in drugs improving plant growth, is not possi
ble. More details of this aspect are discussed in other
reviews [10, 11, 65].
It should be noted that the term “secondary metab
olites,” e.g., “organic compounds not involved directly
in the normal growth, development, and reproduction
of organisms,” [66] should be used, since there is noth
ing that is “nonfunctional” or secondary in nature. The
possibility of biosynthesis of the substance in the body
indicates that this substance is necessary for the body
under conditions that are “normal” and evolutionarily
determined. Otherwise, the biochemical synthesis of
such substances would not be supported by this organ
ism in the course of the evolution of the biosphere [65].
Microorganismproducers of “secondary metabo
lites” in cell cultures are used in biotechnological pro
duction [67]. However, until now endophytic bacteria
forming biologically active substances were not suffi
ciently used as producers of chemical compounds [10].
This review is devoted to a discussion of microbial
agents based on endophytic bacteria, i.e. biological
preparations containing live forms of microorganisms
that are effective preparation agents [33, 45–51,52].
Taking into account the multifaceted relationship of
a bacterial endophyte with plants, other endophytes,
and the environment, including the plant endosphere,
one can imagine how difficult it is for the metabolism
to be adjusted. Even the use of tap water instead of dis
tilled water for the preparation of the nutrient medium
for cultivation of microorganisms causes the appear
ance of new “secondary metabolites” [68].
Prospects for the Use of Endophytic Bacteria
in Microbial Preparations that Improve Plant Growth
At the beginning of the development of a new prep
aration based on microbial endophytic bacteria, which
could be used to stimulate plant development and pro
tect plants from diseases, it is necessary to define both
the targeted agricultural plants and pathogens con
trolled by this preparation. The biodiversity of bacterial
endophytes and host plants makes it possible to obtain
endophytic bacteria with desired properties, which may
be determined based on a biocontrol activity test in vitro
[10, 11, 14, 27, 47, 48]. Such a task—“to find the
organism with the desired properties in nature, multi
ply, and return it back”—is an alternative to the inten
sification of plant production that is based on a wide
variety of agricultural chemicals and the genetic modi
fication of organisms.
The development of such a biological preparation
includes the selection of the desired microorganism
and the confirmation of its positive impact on the tar
geted and/or model plants after artificial inoculation.
Afterwards, certification/registration of the prepara
tion is necessary: (1) to determine the chemical struc
ture of the produced biologically active substances
determining the desired properties of microorganism,
(2) to perform taxonomic identification through DNA
technology [69], and (3) to discover the methods of
colonization of the endosphere. These three tasks are
performed in parallel with the aim of creating eco
nomically feasible technologies for the production and
application of microbial preparations. Thus, the fol
lowing characteristics are extremely important for
production: simple composition of the nutrient
media, the possibility of obtaining liquid bacterial cul
tures with high density (109 CFU/mL), and informa
tion about the cultivation parameters for the produc
tion of maximally active bacterial cells with the desired
properties. For the use of microbial preparations, the
following characteristics should also be considered:
shelf life (at least six months) without loss of properties
(bacteria with a resting stage is preferable), prepara
tion form (liquid/dry) and ease of integration into
existing technologies for plants cultivation, the cost of
the preparation market form (delivery costs), and the
presence of aftereffects [70].
Isolated strains of endophytic bacteria can be used
directly to inoculate seeds and seedlings. This will
allow a reduction of the negative impact of stress biotic
and abiotic factors on the plant as a result of the active
colonization of internal tissues of plants and the subse
quent positive biochemical and physiological impact
on them. The endosphere provides endophytes with a
significant advantage over organisms in the plant rhizo
sphere and phyllosphere, including stable pH levels
and moisture, as well as the flow of nutrients and the
lack of competition from a large number of microor
ganisms [71]. The endophytes colonizing a plant’s
endosphere niche are evolutionarily verified microsym
bionts selected by the plant. Assimilates and other
organic compounds used by plants for the production
of endophytic bacteria biomass are adequately com
pensated by stimulating the development and physio
logical state of the host plant [72].
Artificial inoculation of a plant with endophytic
bacteria should not require large amounts of inoculum
because of the specificity of plant–microbe systems
and the competitiveness of endophytic bacteria. This
property is crucial to a certain extent for economically
justified biotechnological production, and it makes it
possible to replace traditional chemical pesticides.
The presence of the vertical (from ancestors to
decedents) transmission of endophytic bacteria
through the seed endosphere and the high potential of
the biodiversity of seed endophytes [73] allow the clas
sification of biotechnology based on endophytic bac
teria, which is ideal. Indeed, after the isolation of bac
APPLIED BIOCHEMISTRY AND MICROBIOLOGY
Vol. 51
No. 3
2015
ENDOPHYTIC BACTERIA IN MICROBIAL PREPARATIONS
terial endophyte of seeds with desirable properties
from one variety/genetic line/plant species and the
inoculation of target varieties/species of agricultural
plants, these bacteria will be transferred from genera
tion to generation through the endosphere and will
ensure the presence of endophytes in the seeds.
The application of combinations of endophytes
with commercial pesticides used for the treatment of
seeds or seedlings can result in a synergistic effect
against one or several pathogens. While chemical pes
ticides have a shortterm inhibitory effect on phyto
pathogenic microorganisms, biological agents can
have an adverse effects on phytopathogens throughout
the growing season [71].
The fact that the application of endophytic bacteria
preparation in agricultural agrocenoses can insignifi
cantly adjust plant–microbe systems formed in the
course of evolution should be considered. The total
elimination of plant diseases and increasing crop
yields by orders of magnitude should not be expected.
Since the plant plays an active role in interactions
with endophytes, not only the selection of bacteria from
plant endospheres but also the selection/breeding of
highly complementary (susceptible) species/varieties of
agricultural plants should be performed for maximal
effect of microbial preparations based on endophytes.
Even 20 years ago, the data on the endophytic
microflora of plants were fragmentary, while today
there are university courses based on the isolation and
characterization of primary endophytes of plants [74].
This review focuses on bacterial endophytes as the
most technologically advanced microorganisms of the
endosphere, although the variety of plant endophytes
impress with their enormous potential [9, 11]. Unfor
tunately, among the bacteria associated with plants,
there are groups of bacteria associated with human
diseases, the socalled “risk groups” [14, 75].
Endophytic microorganisms with the desired prop
erties that are isolated from plants and capable of
growth on artificial media can be currently used to
develop new microbial preparations. The presence of
uncultured endophytic bacteria [34, 76] provides a task
for researchers to identify opportunities for the use of
these microorganisms in crop production in the future.
The goal of future research will be to study the control
of plant microbial communities of endospheres by
optimizing the conditions for the functioning of plant–
microbe systems in phytocenoses. Such studies will
undoubtedly be of great importance for the further
development of microbiology, biology, plant–microbe
systems, and ecology, and will provide a strong eco
nomic effect from the application of endophytic bacte
ria–based microbial preparations for the improvement
of the plant development for different purposes.
APPLIED BIOCHEMISTRY AND MICROBIOLOGY
275
ACKNOWLEGMENTS
This work was supported by the Russian Science
Foundation (project no. 141600146) and state sup
port for the leading universities of the Russian Feder
ation (grant 074U01).
REFERENCES
1. Clay, K. and Holah, J., Science, 1999, vol. 285, no. 5434,
pp. 1742–1745.
2. Omacini, M., Chaneton, E.J., Ghersa, C.M., and
Muller, C.B., Nature, 2001, vol. 409, pp. 78–81.
3. Redecker, D., Kodner, R., and Graham, L.E., Science,
2000, vol. 289.
4. Krings, M., Taylor, T.N., Hass, H., Kerp, H.,
Dotzler, N., and Hermsen, E.J., New Phytol., 2007,
vol. 174, pp. 648–657.
5. Holliday, P., in A Dictionary of Plant Pathology, Holli
day, P., Ed., Cambridge: Cambridge University Press,
1989.
6. Schulz, B. and Boyle, C., in What Are Endophytes?
Microbial Root Endophytes, Boyle, C.J.C. and
Sieber, T.N., Eds., Berlin: SpringerVerlag, 2006,
pp. 191–206.
7. Strobel, G. and Daisy, B., Microbiol. Mol. Biol. Rev.,
2003, vol. 67, no. 4, pp. 491–502.
8. Strobel, G., Daisy, B., Castillo, U., and Harper, J.,
J. Nat. Prod., 2004, vol. 67, pp. 257–268.
9. Rodriguez, R.J., White, Jr.J.F., Arnold, A.E., and Red
man, R.S., New Phytol., 2009, vol. 182, pp. 314–330.
10. Ryan, R.P., Germaine, K., Franks, A., Ryan, D.J., and
Dowling, D.N., FEMS Microbiol. Letts., 2008, vol. 278,
no. 1, pp. 1–9.
11. Ruby, E.J. and Raghunath, T.M., J. Pharm. Res., 2011,
vol. 4, no. 3, pp. 795–799.
12. Lindow, S.E. and Brandl, M.T., Appl. Environ. Micro
biol., 2003, vol. 69, pp. 1875–1883.
13. Kuiper, I., Lagendijk, E.L., Bloemberg, G.V., and
Lugtenberg, B.J., Mol. Plant Microbe Interact., 2004,
vol. 17, no. 1, pp. 6–15.
14. Berg, G., Eberl, L., and Hartmann, A., Environ. Micro
biol., 2005, vol. 7, pp. 1673–1685.
15. Chebotar’, V.K., Makarova, N.M., Shaposhnikov, A.I.,
and Kravchenko, L.V., Prikl. Biokhim. Mikrobiol.,
2009, vol. 45, no. 4, pp. 465–469.
16. Lima, A.C.F., Pizauro, J.M., Macari, M., and Mal
heiros, E.B., Rev. Bras. Zootec., 2003, vol. 32, pp. 200–
207.
17. Koumoutsi, A., Chen, XH., Henne, A., Liesegang, H.,
Hitzeroth, G., Franke, P., Vater, J., and Borriss, R.,
J. Bacteriol., 2004, vol. 186, no. 4, pp. 1084–1096.
18. Azevedo, J.L., Maccheroni, J.Jr., Pereira, O., and
Ara, W.L., Electr. J. Biotec., 2000, vol. 3, pp. 40–65.
19. Hallmann, J., QuadtHallmann, A., Mahaffee, W.F.,
and Kloepper, J.W., Can. J. Microbiol., 1997, vol. 43,
pp. 895–914.
Vol. 51
No. 3
2015
276
CHEBOTAR et al.
20. Hallmann, J., QuadtHallmann, A., Rodriguez
Kabana, R., and Kloepper, J.W., Soil Biol. Biochem.,
1998, vol. 30, pp. 925–937.
21. Siciliano, S., Fortin, N., and Himoc, N., Appl. Environ.
Microbiol., 2001, vol. 67, pp. 2469–2475.
22. Barac, T., Taghavi, S., Borremans, B., Provoost, A.,
Oeyen, L., Colpaert, J.V., Vangronsveld, J., and
van der Lelie, D., Nat. Biotechnol., 2004, vol. 22,
pp. 583–588.
23. Germaine, K., Keogh, E., GarciaCabellos, G., Borre
mans, B., Lelie, D., Barac, T., Oeyen, L., Vangrons
veld, J., Moore, F.P., Moore, E.R., Campbell, C.D.,
Ryan, D., and Dowling, D.N., FEMS Microbiol. Ecol.,
2004, vol. 48, pp. 109–118.
24. Germaine, K., Liu, X., Cabellos, G., Hogan, J.,
Ryan, D., and Dowling, D.N., FEMS Microbiol.
Ecol., 2006, vol. 57, pp. 302–310.
25. PorteousMoore, F., Barac, T., Borremans, B.,
Oeyen, L., Vangronsveld, J., van der Lelie, D., Camp
bell, D., and Moore, E.R.B., Syst. Appl. Microbiol.,
2006, vol. 29, pp. 539–556.
26. Miche, L. and Balandreau, J., Appl. Environ. Micro
biol., 2001, vol. 67, pp. 3046–3052.
27. Lodewyckx, C., Vangronsveld, J., Porteous, F.,
Moore, E.R.B., Taghavi, S., Mezgeay, M., and
van der Lelie, D., Crit. Rev. Plant Sci., 2002, vol. 21,
pp. 583–60.
28. Rosenblueth, M. and MartinezRomero, E., Mol. Plant
Microbe Interact., 2006, vol. 19, pp. 827–837.
29. Berg, G. and Hallmann, J., in Microbial Root Endo
phytes, Schulz, B.J.E., Boyle, C.J.C., and Sieber, T.N.,
Eds., Berlin: SpringerVerlag, 2006, pp. 53–69.
30. Posada, F. and Vega, F.E., Mycologia, 2005, vol. 97,
pp. 1195–1200.
31. Reiter, B. and Sessitsch, A., Can. J. Microbiol., 2006,
vol. 52, pp. 140–149.
32. Franks, A., Ryan, P.R., Abbas, A., Mark, G.L., and
O’Gara, F., The Molecular Approaches to Soil, Rhizo
sphere and Plant Microorganisms, Cooper, J.E. and
Rao, J.R., Eds., UK: CABI Publishing, 2006, pp. 116–
131.
33. Ulrich, K., Stauber, T., and Ewald, D., Plant Cell Tiss.
Organ. Cult., 2008, vol. 93, pp. 347–351.
34. Sun, L., Qiu, F., Zhang, X., Dai, X., Dong, X., and
Song, W., Microb. Ecol., 2008, vol. 55, pp. 415–424.
35. Rai, R., Prasanta, K., Dash, P.K., Prasanna, B.M., and
Singh, A., J. Microbiol. Biotechnol., 2007, vol. 23,
pp. 853–858.
36. Zinniel, D.K., Lambrecht, P., and Harris, B.N., Appl.
Environ. Microbiol., 2002, vol. 68, pp. 2198–2208.
37. Kurian, P.S., Abraham, K., and Kumar, P.S., Curr. Sci.,
2012, vol. 103, no. 6, pp. 626–628.
38. Gage, D.J., Bobo, T., and Long, S.R., J. Bacteriol.,
1996, vol. 178, pp. 7159–7166.
39. Tombolini, R., Unge, A., Davey, M.E., de Bruijn, F.J.,
and Jansson, J.K., FEMS Microbiol. Ecol., 1997,
vol. 22, pp. 17–28.
40. Tombolini, R. and Jansson, J.K., Methods in Molecular
Biology: Bioluminescence Methods and Protocols,
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
LaRossa, R.A., Ed., N.J.: Humana Press Inc., 1998,
pp. 285–298.
Larrainzar, E., O’Gara, F., and Morrissey, J.P., Annu.
Rev. Microbiol., 2005, vol. 59, pp. 257–277.
Villacieros, M., Power, B., SánchezContreras, M.,
Lloret, J., Oruezabal, R., Martín, M., Fernández
Piñas, F., Bonilla, I., Whelan, C., Dowling, D.N., and
Rivilla, R., Plant Soil, 2003, vol. 251, pp. 47–54.
James, E.K., Gyaneshwar, P., Mathan, N.,
Barraquio, W.L., Reddy, P.M., Iannetta, P.P., Oli
vares, F.L., and Ladha, J.K., Mol. Plant Microbe.
Interact., 2002, vol. 15, no. 9, pp. 894–906.
Miche, L., Battistoni, F., Gemmer, S., Belghazi, M.,
and ReinholdHurek, B., Mol. Plant. Microbe Interact,
2006, vol. 1, pp. 502–511.
Verma, S.C., Ladha, J.K., and Tripathi, A.K., J. Bio
technol., 2001, vol. 91, pp. 127–141.
Wakelin, S., Warren, R., Harvey, P., and Ryder, M.,
Biol. Fert. Soils, 2004, vol. 40, pp. 36–43.
Compant, S., Duffy, B., Nowak, J., Clement, C., and
Barka, E.A., Appl. Environ. Microbiol., 2005, vol. 71,
pp. 4951–4959.
Compant, S., Reiter, B., Sessitsch, A., Nowak, J.,
Clement, C., and Barka, E.A., Appl. Environ. Micro
biol., 2005, vol. 71, pp. 1685–1693.
Lee, S., FloresEncarnacion, M., ContrerasZen
tella, M., GarciaFlores, L., Escamilla, J.E., and
Kennedy, C., J. Bacteriol., 2004, vol. 186, pp. 5384–
5391.
Pirttila, A., Joensuu, P., Pospiech, H., Jalonen, J., and
Hohtola, A., Physiol. Plant., 2004, vol. 121, pp. 305–
312.
Costa, J.M. and Loper, J.E., Mol. Plant Microbe Inter
act., 1994, vol. 7, pp. 440–448.
Whipps, J.M., J. Exp. Bot., 2001, vol. 52 (Spec. Issue),
pp. 487511.
Gray, E.J. and Smith, D.L., Soil Biol. Biochem., 2005,
vol. 37, pp. 395–412.
Kerry, B.R., Ann. Rev. Phytopath., 2000, vol. 38,
pp. 423–441.
Sturz, A.V., Christie, B.R., and Nowak, J., Crit. Rev.
Plant Sci., 2000, vol. 19, pp. 1–30.
Ping, L. and Boland, W., Trends Plant Sci., 2004, vol. 9,
pp. 263–266.
Kloepper, J.W. and Ryu, C.M., in Microbial Root Endo
phytes, Schulz, B.J.E., Boyle, C.J.C., and Sieber, T.N.,
Eds., Berlin: SpringerVerlag, 2006, pp. 33–52.
Senthilkumar,
M.,
Swarnalakshmi,
K.,
Govindasamy, V., Lee, Y.K., and Annapurna, K., Cur
rent Microbiol., 2009, vol. 58, no. 4, pp. 288–293.
Lin, T., Zhao, L., Yang, Y., Guan, Q., and Gong, M.,
Austr. J. Crop Sci., 2013, vol. 7, no. 1, pp. 139–146.
Soria, S., Alonso, R., and Bettucci, L., Chil. J. Agric.
Res., 2012, vol. 72, no. 2, pp. 281–284.
Vetrivelkalai, P., Sivakumar, M., and Jonathan, E.I.,
J. Biopest., 2012, vol. 3, no. 2, pp. 452–457.
Shiomi, H.F., Alves Silva, H.S., Soares de Melo, I.,
Vieira Nunes, F., and Bettiol, W., Sci. Agric., 2006,
vol. 63, no. 1, pp. 32–39.
APPLIED BIOCHEMISTRY AND MICROBIOLOGY
Vol. 51
No. 3
2015
ENDOPHYTIC BACTERIA IN MICROBIAL PREPARATIONS
63. Chaves, N.P., Pocasangre, L.E., Elango, F.,
Rosales, F.E., and Sikora, R., Sci. Horticult., 2009,
vol. 122, no. 3, pp. 472–478.
64. Paranagama, P.A., Wijeratne, E.M.K., and Gunati
laka, A.A.L., J. Nat. Prod., 2007, vol. 70, pp. 1939–
1945.
65. Soil Biology, Vol. 14: Secondary Metabolites in Soil Ecol
ogy, Karlovsky, P., Ed., Berlin: SpringerVerlag, 2008.
66. Fraenkel, G.S., Science, 1959, vol. 129, no. 3361,
pp. 1466–1470.
67. Products of Secondary Metabolism, Rehm, H.J. and
Reed, G., Eds., Germany, Weinheim: WileyVCH Ver
lag GmbH, 2008, vol. 7, p. 728.
68. Kaaria, P., Matiru, V., and Ndungu, M., Afr. J. Micro
biol. Res, 2012, vol. 6, no. 45, pp. 7253–7258. doi:
10.1002/9783527620890.ch2
69. AlKhaldi, S.F., Mossoba, M.M., Allard, M.M.,
Lienau, E.K., and Brown, E.D., Meth. Mol. Biol., 2012,
vol. 881, pp. 7395.
APPLIED BIOCHEMISTRY AND MICROBIOLOGY
277
70. Laktionov, Yu.V., Popova, T.A., Andreev, O.A., Ibatul
lina, R.P., and Kozhemyakov, A.P., Sel’skokhoz. Biol.,
2011, no. 3, pp. 116118.
71. Backman, P.A. and Sikora, R.A., Biolog. Control, 2008,
vol. 46, pp. 1–3.
72. Lugtenberg, B., Malfanova, N., Kamilova, F., and
Berg, G., Molecular Microbial Ecology of the Rhizo
sphere, de Bruijn, F.J., Ed., Hoboken, NJ, USA: Wiley
Blackwell, 2013, vol. 2, pp. 561–573.
73. Coombs, J.T. and Franco, C.M.M., Appl. Environ.
Microbiol., 2003, vol. 69, pp. 4260–4262.
74. BascomSlack, C.A., Arnold, A.E., and Strobel, S.A.,
Science, 2012, vol. 338, pp. 485–486.
75. Ponka, A., Andersson, Y., Siitonen, A., de Jong, B.,
Jahkola, M., Haikala, O., Kuhmonen, A., and
Pakkala, P., Lancet, 1995, vol. 345, pp. 462–463.
76. Preston, G.M., Haubold, B., and Rainey, P.B., Current
Opin. Microbiol., 1998, vol. 1, pp. 589–597.
Vol. 51
Translated by V. Mittova
No. 3
2015