Crosstalk between endophytes and a plant host within information-processing networks
Plants are heavily populated by pro- and eukaryotic microorganisms and represent therefore the tremendous complexity as a biological system. This system exists as an information-processing entity with rather complex processes of communication, occurring throughout the individual plant. The plant cel...
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Kozyrovska, N.O. 2019-06-12T12:47:57Z 2019-06-12T12:47:57Z 2013 Crosstalk between endophytes and a plant host within information-processing networks / N.O. Kozyrovska // Вiopolymers and Cell. — 2013. — Т. 29, №. 3. — С. 234-243. — Бібліогр.: 83 назв. — англ. 0233-7657 DOI: http://dx.doi.org/10.7124/bc.00081D https://nasplib.isofts.kiev.ua/handle/123456789/152581 579.26 + 581.5 + 681.518 Plants are heavily populated by pro- and eukaryotic microorganisms and represent therefore the tremendous complexity as a biological system. This system exists as an information-processing entity with rather complex processes of communication, occurring throughout the individual plant. The plant cellular information-processing network constitutes the foundation for processes like growth, defense, and adaptation to the environment. Up to date, the molecular mechanisms, underlying perception, transfer, analysis, and storage of the endogenous and environmental information within the plant, remain to be fully understood. The associated microorganisms and their investment in the information conditioning are often ignored. Endophytes as plant partners are indispensable integrative part of the plant system. Diverse endophytic microorganisms comprise «normal» microbiota that plays a role in plant immunity and helps the plant system to survive in the environment (providing assistance in defense, nutrition, detoxification etc.). The role of endophytic microbiota in the processing of information may be presumed, taking into account a plant-microbial co-evolution and empirical data. Since the literature are beginning to emerge on this topic, in this article, I review key works in the field of plant-endophytes interactions in the context of information processing and represent the opinion on their putative role in plant information web under defense and the adaptation to changed conditions. Рослини густо населені про- та евкаріотними мікроорганізмами і, отже, являють собою біологічну систему надзвичайної складності. Ця система з доволі непростими процесами комунікації, що відбуваються вздовж усієї рослини, існує для обробки інформації. Мережева обробка інформації у рослин є основою для таких процесів, як ріст, захист і пристосування до навколишнього середовища. Молекулярні механізми, що лежать в основі сприйняття, передачі, аналізу та зберігання ендогенної і зовнішньої інформації всередині рослини, ще належить повністю з’ясувати. Асоційовані з рослиною мікроорганізми та їхній внесок в обробку інформації дослідники часто ігнорують. Ендофіти як партнери рослини є необхідною інтегративною частиною її системи. Різноманітні ендофітні мікроорганізми являють собою «нормальну» мікрофлору, яка відіграє важливу роль в імунітеті рослин і допомагає їм вижити у навколишньому середовищі (захист, живлення, детоксикація тощо). Певну роль ендофітної мікробіоти в обробці інформації можна припустити, беручи до уваги ко-еволюцію рослинно-мікробних систем та емпіричні дані. Оскільки в літературі починають з’являтися публікації на цю тему, в представленому огляді розглянуто ключові роботи в галузі взаємодії рослин з ендофітами у контексті обробки інформації і висловлено думку стосовно їхньої прогнозованої ролі в інформаційній мережі рослин за умов захисту та пристосування останніх до змінених умов та налаштування відповідної поведінки рослини. Растения густо населены про- и эукариотическими микроорганизмами и, таким образом, представляют собой биологическую систему чрезвычайной сложности. Эта система с довольно непростыми процессами коммуникации, проходящими в растении, существует для обработки информации. Сетевая обработка информации у растений служит основой для таких процессов, как рост, защита и приспособление к окружающей среде. Молекулярные механизмы, лежащие в основе восприятия, передачи, анализа и сохранения эндогенной и внешней информации внутри растения, еще предстоит выяснить. Ассоциированные с растением микроорганизмы и их вклад в обработку информации исследователи часто игнорируют. Эндофиты как партнеры растений являются необходимой интегративной частью ее системы. Разнообразные эндофитные микроорганизмы – это «нормальная» микрофлора, выполняющая важную роль в иммунитете растений и помогающая им выжить в окружающей среде (защита, питание, детоксикация и др.). Определенную роль эндофитной микробиоты в обработке информацмм можно предположить, приняв во внимание ко-эволюцию растительно-микробных систем, а также эмпирические данные. Поскольку в литературе начинают появляться публикации на эту тему, в представленном обзоре рассмотрены ключевые работы в области взаимодействия растений с эндофитами в контексте обработки информации и изложено мнение об их прогнозируемой роли в информационной сети растений в условиях защиты и проспособления последних к измененным условиям и настройке соответствующего поведения растения. en Інститут молекулярної біології і генетики НАН України Вiopolymers and Cell Reviews Crosstalk between endophytes and a plant host within information-processing networks Перехресні взаємодії між ендофітами та рослиною-хазяїном у мережах інформаційного процесингу Перекрестные взаимодействия между эндофитами и растением-хозяином в сетях информационного процессинга Article published earlier |
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Crosstalk between endophytes and a plant host within information-processing networks |
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Crosstalk between endophytes and a plant host within information-processing networks Kozyrovska, N.O. Reviews |
| title_short |
Crosstalk between endophytes and a plant host within information-processing networks |
| title_full |
Crosstalk between endophytes and a plant host within information-processing networks |
| title_fullStr |
Crosstalk between endophytes and a plant host within information-processing networks |
| title_full_unstemmed |
Crosstalk between endophytes and a plant host within information-processing networks |
| title_sort |
crosstalk between endophytes and a plant host within information-processing networks |
| author |
Kozyrovska, N.O. |
| author_facet |
Kozyrovska, N.O. |
| topic |
Reviews |
| topic_facet |
Reviews |
| publishDate |
2013 |
| language |
English |
| container_title |
Вiopolymers and Cell |
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Інститут молекулярної біології і генетики НАН України |
| format |
Article |
| title_alt |
Перехресні взаємодії між ендофітами та рослиною-хазяїном у мережах інформаційного процесингу Перекрестные взаимодействия между эндофитами и растением-хозяином в сетях информационного процессинга |
| description |
Plants are heavily populated by pro- and eukaryotic microorganisms and represent therefore the tremendous complexity as a biological system. This system exists as an information-processing entity with rather complex processes of communication, occurring throughout the individual plant. The plant cellular information-processing network constitutes the foundation for processes like growth, defense, and adaptation to the environment. Up to date, the molecular mechanisms, underlying perception, transfer, analysis, and storage of the endogenous and environmental information within the plant, remain to be fully understood. The associated microorganisms and their investment in the information conditioning are often ignored. Endophytes as plant partners are indispensable integrative part of the plant system. Diverse endophytic microorganisms comprise «normal» microbiota that plays a role in plant immunity and helps the plant system to survive in the environment (providing assistance in defense, nutrition, detoxification etc.). The role of endophytic microbiota in the processing of information may be presumed, taking into account a plant-microbial co-evolution and empirical data. Since the literature are beginning to emerge on this topic, in this article, I review key works in the field of plant-endophytes interactions in the context of information processing and represent the opinion on their putative role in plant information web under defense and the adaptation to changed conditions.
Рослини густо населені про- та евкаріотними мікроорганізмами і, отже, являють собою біологічну систему надзвичайної складності. Ця система з доволі непростими процесами комунікації, що відбуваються вздовж усієї рослини, існує для обробки інформації. Мережева обробка інформації у рослин є основою для таких процесів, як ріст, захист і пристосування до навколишнього середовища. Молекулярні механізми, що лежать в основі сприйняття, передачі, аналізу та зберігання ендогенної і зовнішньої інформації всередині рослини, ще належить повністю з’ясувати. Асоційовані з рослиною мікроорганізми та їхній внесок в обробку інформації дослідники часто ігнорують. Ендофіти як партнери рослини є необхідною інтегративною частиною її системи. Різноманітні ендофітні мікроорганізми являють собою «нормальну» мікрофлору, яка відіграє важливу роль в імунітеті рослин і допомагає їм вижити у навколишньому середовищі (захист, живлення, детоксикація тощо). Певну роль ендофітної мікробіоти в обробці інформації можна припустити, беручи до уваги ко-еволюцію рослинно-мікробних систем та емпіричні дані. Оскільки в літературі починають з’являтися публікації на цю тему, в представленому огляді розглянуто ключові роботи в галузі взаємодії рослин з ендофітами у контексті обробки інформації і висловлено думку стосовно їхньої прогнозованої ролі в інформаційній мережі рослин за умов захисту та пристосування останніх до змінених умов та налаштування відповідної поведінки рослини.
Растения густо населены про- и эукариотическими микроорганизмами и, таким образом, представляют собой биологическую систему чрезвычайной сложности. Эта система с довольно непростыми процессами коммуникации, проходящими в растении, существует для обработки информации. Сетевая обработка информации у растений служит основой для таких процессов, как рост, защита и приспособление к окружающей среде. Молекулярные механизмы, лежащие в основе восприятия, передачи, анализа и сохранения эндогенной и внешней информации внутри растения, еще предстоит выяснить. Ассоциированные с растением микроорганизмы и их вклад в обработку информации исследователи часто игнорируют. Эндофиты как партнеры растений являются необходимой интегративной частью ее системы. Разнообразные эндофитные микроорганизмы – это «нормальная» микрофлора, выполняющая важную роль в иммунитете растений и помогающая им выжить в окружающей среде (защита, питание, детоксикация и др.). Определенную роль эндофитной микробиоты в обработке информацмм можно предположить, приняв во внимание ко-эволюцию растительно-микробных систем, а также эмпирические данные. Поскольку в литературе начинают появляться публикации на эту тему, в представленном обзоре рассмотрены ключевые работы в области взаимодействия растений с эндофитами в контексте обработки информации и изложено мнение об их прогнозируемой роли в информационной сети растений в условиях защиты и проспособления последних к измененным условиям и настройке соответствующего поведения растения.
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Crosstalk between endophytes and a plant host within information-processing networks / N.O. Kozyrovska // Вiopolymers and Cell. — 2013. — Т. 29, №. 3. — С. 234-243. — Бібліогр.: 83 назв. — англ. |
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UDC 579.26 + 581.5 + 681.518
Crosstalk between endophytes and a plant host
within information processing networks
N. O. Kozyrovska
Institute of Molecular Biology and Genetics, NAS of Ukraine
150, Akademika Zabolotnogo Str., Kyiv, Ukraine, 03680
kozyrna@ukr.net
Plants are heavily populated by pro- and eukaryotic microorganisms and represent therefore the tremendous
complexity as a biological system. This system exists as an information processing entity with rather complex
processes of communication, occurring throughout the individual plant. The plant cellular information proces-
sing network constitutes the foundation for processes like growth, defense, and adaptation to the environment. Up
to date, the molecular mechanisms, underlying perception, transfer, analysis, and storage of the endogenous and
environmental information within the plant, remain to be fully understood. The associated microorganisms and
their investment in the information conditioning are often ignored. Endophytes as plant partners are indispen-
sable integrative part of the plant system. Diverse endophytic microorganisms comprise «normal» microbiota that
plays a role in plant immunity and helps the plant system to survive in the environment (providing assistance in
defense, nutrition, detoxification etc.). The role of endophytic microbiota in the processing of information may
be presumed, taking into account a plant-microbial co-evolution and empirical data. Since the literature are be-
ginning to emerge on this topic, in this article, I review key works in the field of plant-endophytes interactions in
the context of information processing and represent the opinion on their putative role in plant information web
under defense and the adaptation to changed conditions.
Keywords: a plant system, endophytes, information processing, plant defense, adaptation.
Plant is a complex ecosystem with a versatile com-
munal life. The plant as all existing living entities is
systemically inhabited by diverse microorganisms [1–
3], and so far it constitutes a hierarchically complex sys-
tem, displaying different genetic landscapes, interacto-
mes, and information processing networks. The plant
controls its interactions with beneficial and pathogenic
microbes in the context of environmental influences,
and the outcome of such interactions depends on the in-
teracting partners and their surrounding. Individual
plants have unique microbiomes, and differences in plant-
associated microbiome structures occur mainly due to
host genetic control. However, vertically-transferred core
microbial species follow the plant host species during
its evolution [4, 5]. Micro-inhabitants interact with the
plant partner in a metabolically-based manner, using own
«talents» of making relationships. On the first view, the
interactions between partners can be described in terms
of classical relationships: from obligatory symbiosis
through loyal mutualism and unobtrusive commensa-
lism to obligatory parasitism; however, plant-microbial
relationships may be more specialized or variable and
often depend on the phase in microbial life-time and en-
vironmental factors. Moreover, mutualists are able to
short-circuit plant defense responses to enable succes-
sful colonization of the plant host, demonstrating that
the boundaries between mutualists and pathogens are
factitious.
A wide range of co-inhabitants create a spectrum of
impacts on the plant biology. Accidentally incoming
microorganisms may play a simple role of additional or-
ganic food processed by plant into valuable nutrients
for heterotrophic feeding, but co-evolved inhabitants
cooperate with the plant, affecting its fitness. Recrui-
234
ISSN 0233–7657. Biopolymers and Cell. 2013. Vol. 29. N 3. P. 234–243 doi: 10.7124/bc.00081D
� Institute of Molecular Biology and Genetics, NAS of Ukraine, 2013
235
CROSSTALK BETWEEN ENDOPHYTES AND A PLANT WITHIN INFORMATION-PROCESSING NETWORKS
ting of the soil and rhizosphere microbes by plant sys-
tem is fully reasonable, relying on cooperative tenden-
cies in the world of living organisms [6] and a poor plas-
ticity in the plant as a multi-cellular entity under adapta-
tion to the changed environment in comparison with as-
sociated microbes; genetic exchange and phenotypic
variation are important drivers of microbial plasticity,
which are critical for microbial persistence in fluctua-
ting environments. It is exploited by the plant, permanent-
ly selecting dual microbial partners for its programs
(fighting the enemies, adaptation to the changed envi-
ronment etc.). In evolution, the plant as a sessile orga-
nism has got practically additional instrument repre-
sented by microbial organisms for a tuning its behavior.
Microbes are self-sufficient unicellular organisms,
however, they are united in multi-cellular populations
within a species and exhibit inter-conversion between
phenotypically distinct sub-populations. The latter for-
mation depends on the surrounding, a nutrient availabi-
lity, specialization etc. Cells of both heterogeneous bac-
terial single populations or well-organized communities
of mixed populations interact for coordinated activi-
ties, i. e. populations behave as multi-cellular organisms
and exhibit signs of a social entity [7]. To govern the
unity of a cell population and to manipulate the sub-
structures within species, the well balanced regulatory
systems evolved, which are based on the perception and
processing of information, e. g. cell-to-cell communi-
cation via regulatory molecules or physical signals. Due
to coordination and synchronization, microbial orga-
nisms exhibit cooperative social behaviors, such as bio-
film or persister phenotype formation, chemical defense,
etc. In the plant system, the activity of associated mic-
robiota expressed in providing bioactive compounds,
which plant cannot produce, in fine-tuning plant beha-
vior under adaptation to changed conditions, detoxica-
tion of the plant super-organism etc.
When we focus on information processing in the
plant system, we cannot ignore microbial constituents,
which may either serve or regulate some plant physiolo-
gical processes and so far participate in its information
processing networks. Especially, this may concern en-
dophytic microorganisms, which comprise indigenous
residents within the plant interior and represent a diver-
se part of plant-associated microbiome (reviewed in [1,
8, 9]. There are certain peculiarities in the endophy-
te-plant partner co-existence: (i) endophytes are a cate-
gory of microbes, that capable to cheat plant immune
system in order to form populations in the plant interior
without causing any harm; (ii) relaying on small-size
populations restricted by a set of factors (e. g. a short-
age of signaling molecules, nurients, a control by the
macro-organism etc.), endophytes seem to be metabo-
lically less active than microbes, colonizing the plant
outside; (iii) the spatial structure of endophytic micro-
biome can strongly affect their social interactions; en-
dophytic bacteria frequently grow in dense, multi-cellular
communities in biofilms [10], however, more often a dis-
tance between their cells/populations is longer than e.
g. in epiphyte microbiome.
Endophytic populations are constituted by both ge-
notype-associated core species, which often pass through
plant generations, and incoming recruited microbes.
Metagenomic analysis of DNA derived from the inner
tissues of healthy plants showed a great diversity of mic-
robial organisms within the plant host [2, 3, 6, 11]; even
grown aseptically in laboratory plants exhibit systemic
colonization of the endosphere. Endophytic communi-
ty members directly or distantly communicate between
themselves and with the plant host, using physico-che-
mical signals, and are doomed to be either integrated
into the plant information web or at least to interplay
with it. There are several indirect lines of evidence to
believe that endophytes are acceptors and enhancers of
environmental signals, as well as they are creators and
mediators of intrinsic information.
First, endophytic microorganisms have multiple
impacts on a plant micro-ecosystem functioning and
may affect plant responses to various environmental
changes, including climate (see rev. [1, 9]). Second,
both plants and microorganisms produce a wide array
of similar metabolites, which have common precursors.
For example, the universal precursors for isoprenoids
(carotenoids, quinones, hormones and secondary meta-
bolites, that serve in plant defense and communication)
may be produced in two ways, and both of them are wi-
despread in eubacteria and archaea [13]. The hypo-
thesis of xenohormesis proposed by Howitz and Sin-
clair [14] states that stress-induced molecules from
plants can be sensed by microorganisms, which obvi-
ously are capable to produce similar secondary me-
tabolites. According to this hypothesis, plants and mic-
roorganisms possess homologous gene clusters (pro-
bably, being horizontally transferred between do-
mains) and thus might be cross-activated by plant hosts
or endophytes under some emergency (e. g. pathogen
attack). It is a well known example of the same bioac-
tive compounds synthesis by medicinal plants and en-
dophytic bacteria or fungi, residing in these plants (ta-
xol, for instance, producing by fungi [15]). Third, en-
dophytes possess certain instruments of interaction with
plant hosts similar to another plant-associated micro-
organisms. Commonalities in endophytes and pathogens
seen, e. g. in availability of type III or IV protein secre-
tion systems [16, 17], which they may use for adaptation
in the plant host. However, the question remains, con-
cerning the functionality of these systems. The hori-
zontal acquisition of type IV secretion system is known
in the nature and presumably may occur in the endophy-
tosphere. For example, in the endophytic Klebsiella pneu-
monia, genetic determinants for such secretion system
are located within integrated mobile element and could
be acquired via a gene transfer mechanism [16]. Final-
ly, it was documented in many laboratories, that the in-
digenous endophytic microbial communities sense ex-
ternal cues, modulating a community structure under
the impact of biotic or abiotic factors on the plant sys-
tem [12, 18–24].
How adaptive social interactions evolve in the endo-
phytosphere? What are the parameters, governing the
success of cooperative traits? How microbial organisms
mount own information web within authentic plant in-
formation continuum? Is there the cross-talk between
endophytes and the plant host within information pro-
cessing networks? To address these questions, we first
need to outline briefly the authentic information proces-
sing system in plant host and then to provide some care-
ful prognosis about a cross-talk between endophytes
and the plant partner, as the role of endophytes in the
plant information processing networks has no yet a so-
lid foundation. Nevertheless, important insights may
be obtained from the analysis of the impact of other
plant-associated bacteria on information processing in
the plant system, mainly pathogens and their non-patho-
genic mutants.
Information processing system in plants as alter-
native to neuronal network. Information is encoded
signals, incoming to the living organism from outside
or being induced inside and spreading over signaling
cascades to a target cell. The plant information network
is hierarchically organized due to sub-systems at each
organizational level, which allow to process signals in
the plant interior and re-distribute there in some other
form [25]. Plants permanently meet the environmental
challenges, which cannot avoid (the gravitational force,
the influence of the Moon, vibrations, irradiations, tem-
perature, pathogens etc.) and need to adapt itself to per-
manent challenges. While they don’t have a real neuro-
nal network, individual plants have sensory receptors,
ion channels, vessels, which have certain features of a
«nervous» system [24] and may represent specific kind
of a proto-nervous system in plants [26]. It can perform
subsequent transformation of accepted signals in the form
of plant-specific information, using the regulatory mo-
lecules, such as plant hormones, receptor kinases,
transcription factors, small non-coding RNAs, etc. (re-
viewed in [27]). Another class of intrinsic modulators
of signals is the bioelectric impulses being derived
from ionic exchanges across membranes and channeled
within a phytoneural system [25]. There might be a «de-
cision-making» process, prioritizing one type of respon-
se above others; recognized and encoded information is
transferred to the nucleus, where plant response is regu-
lated at the levels of transcription, translation and post-
translational events. In addition to processes, occurring
in nuclea, the apo- and aloplastic information proces-
sing play a critical role in regulating integrative func-
tions in plants.
Some acquired valuable information is stored by
plants in order to update their behavior and survive
future challenges; in other words, plants induce a
«memory» via epigenetic mechanisms (reviewed in
[28]).
Individual plant cells have acquired highly autono-
mous capabilities in sense of information processing.
The question rises, how molecular networks at the sing-
le-cell level ultimately define collective cell behaviors?
The understanding, how interaction among cells pro-
ceeds, enabling the spread of signals within informa-
tion processing networks, is a fundamental problem in
biology. The closely related question is, how this auto-
nomous cell system mediates the regulation of func-
tions across the plant, including growth, defense, and
adaptation to the environment, and how this system
236
KOZYROVSKA N. O.
cross-talk with information processing networks of as-
sociated microbes?
Endophytes as putative components of the infor-
mation processing network in a plant system. Signal
perception and transmission. In a hierarchy of the plant
information-processing system, the sub-systems, which
recognize, percept, and transmit signals, take a central
place. In plant systems, perception and transmission of
biochemical signals occur mostly through two mecha-
nisms: (i) protein-protein interactions and enzymatic re-
actions such as protein phosphorylation and dephospho-
rylation or (ii) protein degradation or production of in-
tra-cellular messengers. There are two stages in protein-
protein interactions: (i) a cell surface receptor should
be activated by an extracellular signaling molecule; (ii)
this receptor alters a second messenger, mounting a res-
ponse. One of the systems, sensing and responding to
environmental cues, is a histidine kinase-based signa-
ling system, which plants use to relay signals [29]. Au-
tophosphorylating histidine protein kinases provide
phosphoryl groups for response regulator proteins, and
phosphorylation induces so far a conformational chan-
ge in the regulatory domain that results in the activation
of an associated domain and a switch on of the response
or further signal transmission. The ectodomain of plant
receptor kinase functions in different signaling path-
ways, including symbiosis and defense [30]. In apo-
plast, environmental signals, e. g. chitin, peptidogly-
can etc. (MAMPs) (see on-line glossary at www.biopo
lymers.org.ua doi: 10.7124/bc.00081D) are being re-
cognized, accepted and transported across a cell wall
and membrane to tissues/organ, so far the apoplast is
involved in a cell-to-cell communication. Here, hormo-
nes interact with cell-surface recep-tors, and microorga-
nisms trigger a local or systemic acquired resistance, i. e.
this is a place, where intensive information recognition
and decoding-encoding events take place. Both apo- and
aloplasts are occupied by endophytes [31, 32], which
might be involved in plant programs, and in these set-
tings, a cross-talk with the authentic plant information
processing network may occur.
In bacteria, in analogy to plants, there is the auto-
phosphorylation of histidine residue on the ectodomain
and a phosphor-transfer from there to an aspartate resi-
due on the response regulator. It was shown, that histi-
dine kinase modules are evolutionarily conserved bet-
ween plants and bacteria. Phylogenetic analysis indica-
ted that two-component systems (TCSs) originated in
domain Bacteria and were radiated to domains Archaea
and Eukarya via multiple lateral transfer events. This
observation is also supported by greater abundance and
wider distribution of TCS in Bacteria, in comparison to
Archaea and Eukarya (reviewed in [33]). One such
feature is the integration of TCS signaling pathways
with other signaling systems of eukaryotes: bacterial
histidine kinase components have been shown to be
functional in plants and vice versa [34]. This may mean
that in some cases, bacterial TCSs can be integrated into
plant information processing events, when some sig-
nals in endophytosphere can be captured by bacteria or
when indigenous bacteria amplify plant hormonal
signals by own resources, being involved in some event
of joint interest (e. g. defense).
Scaffolding: is there commonality in pathogens and
endophytes? Environmental cues are perceived and trans-
mitted by a myriad of plant signal transduction pathways;
by turning on specific transcription factors in the nuc-
leus this leads to the activation of genes, encoding pro-
teins, that enable plant adaptation to environmental chal-
lenges. Many of these genes are more often regulated
by the modulation of scaffold protein properties than by
the activities of integral components in the signaling
cascades. This strategy enables signal transmission to be
turned on or off rapidly or to be tuned to the cues via the
assembly or disassembly of the complexes of plant scaf-
fold protein with bacterial effector molecule. Actually,
the manipulation of scaffolding represents the intimate
type of plant-microbial interactions. Some bacterial fac-
tors use plant scaffold proteins to become active, while
others target the host scaffold proteins to suppress its ac-
tivity. For example, the interaction between the HopQ1
effector secreted by Pseudomonas syringae pv. phaseo-
licola and a specific plant protein is needed for modu-
lating the properties of this bacterial effector in planta
and spreading through the plant [35]. The outcome of the
scaffolding depends on the competition between pro-
cesses mediated by the plant and bacteria. When HopQ1
enters plant cells, it is recognized by the immune system,
which prevents infection. However, being phosphoryla-
ted, the effector suppresses plant defense, and a sprea-
ding across the plant depends on the speed of phospho-
rylation-dephosphorylation processes. Transcription fact-
237
CROSSTALK BETWEEN ENDOPHYTES AND A PLANT WITHIN INFORMATION-PROCESSING NETWORKS
ors, which are used in the plant system to coordinate
gene expression, might be imitated by bacteria to indu-
ce developmental gene reprogramming on their benefit
[35]. In this relation, plants are not complete losers and
also use such a strategy, secreting compounds that mimic
the bacterial signals and thereby may confuse bacterial
activity [37].
Role of bacterial bioactive molecules in the regula-
tion of biological processes in plants. The metabolo-
mes of plants include thousands of bioactive compounds,
which significantly exceed those of prokaryotes or ani-
mals. However, there is a room for microbially produ-
ced biologicals in the plant information web. The me-
tabolome of bacterial cells consist of thousands metabo-
lites, referring to genome-based metabolic network mo-
dels [38]. Microbes utilize this great variety of metabo-
lites to perform fundamental processes (population main-
tenance, defense, intra- and interspecies communica-
tion etc.). Small bacterial bioactive molecules such as
hormones, autoinducers, volatiles etc. act as signals to
recognize the environment and coordinate physiolo-
gical processes in the contact with surrounding. Some
of these molecules could be used by microbial orga-
nisms to manipulate the plant physiology, silencing hor-
mone-mediated signaling or amplifying plant signals
by own hormones.
Plant hormones have a designation to collectively
regulate every aspect of plant life, from pattern forma-
tion during development to responses to biotic and abio-
tic stressors [39]. These low-molecular-weight com-
pounds abscisic acid (ABA), auxins, brassinosteroids,
cytokinin, gibberellic acid, ethylene, jasmonic acid
(JA), salicylic acid, several peptide hormones act as
systemic signals, transmitting information over large
distances. Hormonal signaling pathways are known to
interact at the level of gene expression. Studies show
that there is overlap between phytohormones, as well
as between hormones originated from plants and mic-
roorganisms.
Bacteria manipulate plant development by interfe-
ring with the plant’s own growth hormones, in particu-
lar, with auxins. For example, rhizobia reduce the au-
xin transport, exploiting flavonoids, which have been
suggested as potential auxin transport inhibitors [40].
Another intriguing example illustrates, how a bacterial
component of flagella positively contributes to MAMP-
triggered immunity by silencing auxin receptors and
subsequently suppressing auxin signaling [41]. Bacte-
ria manipulate also the components of another plant
hormone signaling pathways (ABA and JA) and do this
via miRNAs [42].
Quorum sensing and communications within endo-
phytosphere. The produced by the plant host hormones
can cross-signal with quorum sensing (QS) signals to
modulate bacterial or fungal gene expression. QS-sig-
naling may represent an example of the integrative net-
work of signal processing in plants and takes important
position in the global information processing network.
Plants can recognize, uptake, degrade or quench micro-
bial signaling molecules – autoinducers [43]. Microbes
produce and detect the latter in order to recognize self
and non-self, as well as to synchronize cells for the exe-
cution of specific functions like production of enzymes,
conjugation, biofilm formation etc. under a threshold
concentration of autoinducers [44]. In the endophyto-
sphere, the benefits from secreted substances such as
QS molecules seem to be much lower because autoin-
ducers commonly diffuse not so far away from produ-
cers. Endophytes utilize AI-1 or AI-2 systems [45, 46]
or unknown yet QS [47] and, theoretically, may increa-
se a pool of signaling molecules by incoming endophy-
tes or activated (re-awaken) resident populations. QS re-
gulates cell–cell communications within a single popu-
lation, as well as inter-species and inter-kingdom inter-
actions between bacteria, fungi, and plants [43]. Recent
results show that QS has a prominent role in interrela-
tionships between the plant and endophytes [48, 49].
The composition and abundance of autoinducers may
modulate cultivar-specific plant responses, e. g. a bacte-
rial strain with quenched QS signal had a great impact
on gene expression in the host plant, as compared to a
wild strain [48].
In the plant endosphere, synergism among different
bacterial species in the interspecies signaling is a highly
probable [19, 49]. With certain presumption, we may
speculate about synergistic effects in endophytic micro-
biome between community members, producing the sa-
me type signaling molecules, or the donation them to
species, which have no a quorum of autoinducers in
small endophytic populations. In theory, QS signal mo-
lecules may provoke resuscitation from dormant state in
endophytes, gaining signs of emergency from the envi-
238
KOZYROVSKA N. O.
ronment. The question rises again, how endophytes sen-
se external signals?
Resuscitation of endophytic persisters: an interplay
with plant information processing? The metagenomic
approach to a study of microbial communities has ope-
ned an unprecedented variety of uncultivable endophy-
tes. It was shown, in particular, that their diversity ex-
ceeds that of the cultivable bacteria isolated from plant
tissues on Petri plates [50–54]. In general, the unculti-
vable bacteria originated from environmental samples
fall in either a category for which appropriate labora-
tory conditions necessary for growth are not identified
yet, or a category that requires the removal or addition
of certain factors to re-initiate growth [55]. Many bac-
terial species are able to enter into a state of dormancy,
in which cells can persist for extended periods without
division. Persisters resist acids, multi-drug action, os-
motic stress, oxidation etc. [56] and reach this without
any genetic change. The reversibility of this state enab-
les dormant organisms to «re-awaken» or resuscitate
under conditions permissive to re-growth.
Signaling molecules such as cyclic adenosine mo-
nophosphate and N-acyl-homoserine lactones were
shown to be responsible for resuscitation from a dor-
mant state; in addition, the resuscitation-promoting fac-
tors (Rpf) can stimulate growth after exiting the VBNC
state (reviewed in [57]). Rpfs are the member of a fami-
ly of secreted proteins found throughout the Actino-
bacteria and in Firmicutes species, which produce pep-
tidoglycans from the cell wall that could exert bacterial
signaling [58, 59]. Growth factors used for the resusci-
tation of non-dividing cells are not limited to the des-
cribed species and obviously can be associated with re-
suscitation of plant-associated microbiota. The high le-
vel of persistence is favored by great competition for re-
sources, and it may be predicted in the endophytosphe-
re. Persistence provides a direct benefit for populations
by producing a sub-population that reduces local compe-
tition for resources and preventing therefore the spread of
strains with a poor fitness. Certain (dormant) endophy-
tic populations of microbes may sense a lack of signals
needed to perform any physiological functions in the
endophytosphere, in contrast to active sub-populations,
which are more plant-«devoted» and capable to fulfill
beneficial functions, e. g. nitrogen fixation [60–62]. On
the other hand, the host may keep endophytic microbial
populations small, preventing their proliferation with spe-
cific regulators, destroying or quenching microbial regu-
lators [49]. The maintenance of dormant sub-popula-
tions may be a hidden strategy in the plant system survi-
val, and a mechanism of re-growth of dormant popula-
tion may serve a plantmicrobial cooperation under stress-
ful conditions. Actually, the formation of persister cells
is not reported for endophytes yet. In line with this, in
the pathogenic bacterium Xanthomonas fastidiosa, the
formation of persister phenotype under stressful condi-
tions is recently discovered [63].
The expression of toxin–antitoxin (TA) systems di-
rectly correlates with the persistence phenotype, indu-
cing in microbes under unfavorable conditions [64].
Stress conditions result in the degradation or depletion
of the antitoxin and the disturbance of the TA balance,
leading to the delay of main cellular processes and
dormancy. TA loci are highly abundant in free-living,
but lost from host-associated prokaryotes [65]. Never-
theless, the TA systems were detected in complete geno-
mes of endophytic bacteria [66, 67], including obligate
endophyte Herbaspirillum seropedicae, and presumab-
ly TA systems exist in all endophytic species, but re-
main uncovered yet. Relaying on a big body of eviden-
ce, which exhibit the modulation of endophytic micro-
biome under impact of different external cues [12, 18,
19, 21–23, 51, 67], it can be presumed that both known
and uncovered yet (bio)physical and (bio)chemical sig-
nals are involved in «awakening» and synchronization
of microbes in endophytosphere.
Epigenetic manipulations by bacteria in the plant
system. Epigenetic mechanisms include DNA methyla-
tion and post-translational modifications of histones and
serve the regulation of gene expression during plant de-
velopment, defense, and exposure to stresses (reviewed
in [68]). Plants perceive both abiotic and biotic stresses
within a life-time, «memorize» them via epigenetic me-
chanisms, and save this «memory» for next generations
[69–71]. In bacteria, epigenetic mechanisms control
DNA replication and gene expression, the packaging of
bacteriophage genomes, transposase activity, a stress-
induced variability of bacteria [72].
The role of epigenetic mechanisms in shaping host–
microbial interactions has received not enough atten-
tion, except interactions between hosts and pathogens
(see rev. [73]). The latter involve a recombination bet-
239
CROSSTALK BETWEEN ENDOPHYTES AND A PLANT WITHIN INFORMATION-PROCESSING NETWORKS
ween transposon elements and sequence repeats, enco-
ding resistance proteins; via recombination events mic-
robes involved in the extensive reprogramming of plant
transcription and formation of trans-generation «me-
mory», which fixes interaction with microbes for des-
cendants [74]. Another mechanism of a plant-microbial
interrelationship is DNA methylation-demethylation,
potentially acting to prime transcriptional activation of
some resistance genes linked to transposable elements
[75]. Exposed to bacterial plants pathogen or avirulent
bacteria reveal numerous stress-induced differentially
demethylated regions associated with differentially ex-
pressed defense-related genes [76]. The epigenetic chan-
ges suggest that the epigenome may help organisms to
develop resistance to pathogens [80] and to other envi-
ronmental stressors [78]. In a similar way, endophytic
bacteria induce DNA methylation-demethylation in
plant hosts. Recently, Da et al. [79] reported the first
evidence exhibited cytosine methylation polymor-
phisms in potato plant DNA as a response to the bac-
terial endophyte Burkholderia phytofirmans PsJN. The
DNA methylation levels in different potato varieties dif-
fered and depended on their responsiveness to endo-
phyte: a highly responsive to the bacterium variety exhi-
bited a little change in the overall cytosine methylation
pattern, but a poorly-responsive variety exhibited signi-
ficantly higher levels of overall cytosine methylation
and a decrease in the number of non-methylated sites in
the bacterized plants compared to controls. In this case,
the DNA methylation level correlated with bacterial
effects on the plant host.
In plant endosphere, bacteria-fungal interactions
may be relevant to epigenetic events. Fungi use the me-
chanism of histone post-translational modification to
modulate the transcription of genes involved in seconda-
ry metabolite production [80]. External epigenetic mo-
difiers may re-program biosynthetic pathways and activa-
te secondary metabolite genes resulted in the enhanced
production of secondary metabolites. In the study [81],
bacteria were shown to perform a role of epigenetic mo-
difiers in interactions with eukaryotic partners: histone
acetylation occurred during the interaction of the fun-
gus Aspergillus nidulans and the bacterium Streptomyces
rapamycinicus. In the result, the fungus activated sup-
pressed genes and produced secondary metabolites,
orsellinic acid and its derivatives, known as radical sca-
vengers. The nature of the compound, promoting his-
tone modification, is unknown yet; however, it was pro-
ven that for this action a physical contact of fungal hy-
phae with bacterial cells was obligatory.
Summarizing, I would like to refer a reader to Figu-
re, where putative scenarios of the endophytic microbio-
me involvement in the plant information processing
network is schematically displayed. It is obvious, that the
scenarios are based on scarce information available and
do not fully reflect a reality. To know more, this review
emphasizes the need to invest efforts in the study of the
processing of information under assistance of microbial
organisms as this will lead not only to intriguing disco-
veries on the level of molecular biology, quantum phy-
sics etc., but to a design of new green technologies of
plant protection and other technological breakthroughs.
240
KOZYROVSKA N. O.
Sensing of intrinsic or extrinsic cues
Recruits
Epigenetic events
Indigenous
microbes
Activity
Signaling small
organic molecules
Defensive
or other effects
Population & Resources
saving
Scaffolding?
Persistence
Sensing of intrinsic or extrinsic cues
Integration with a plant
Information processing
network or independent
signaling
???
Signal transmisson
Hormone/QS
interplay
Physical signals
Putative scenarios of the en-
dophytic microbiome invol-
vement in plant information
processing networks
Í. O. Êîçèðîâñüêà
Ïåðåõðåñí³ âçàºìî䳿 ì³æ åíäîô³òàìè òà ðîñëèíîþ-õàçÿ¿íîì
ó ìåðåæàõ ³íôîðìàö³éíîãî ïðîöåñèíãó
Ðåçþìå
Ðîñëèíè ãóñòî íàñåëåí³ ïðî- òà åâêàð³îòíèìè ì³êðîîðãàí³çìàìè ³,
îòæå, ÿâëÿþòü ñîáîþ á³îëîã³÷íó ñèñòåìó íàäçâè÷àéíî¿ ñêëàäíî-
ñò³. Öÿ ñèñòåìà ç äîâîë³ íåïðîñòèìè ïðîöåñàìè êîìóí³êàö³¿, ùî
â³äáóâàþòüñÿ âçäîâæ óñ³º¿ ðîñëèíè, ³ñíóº äëÿ îáðîáêè ³íôîðìàö³¿.
Ìåðåæåâà îáðîáêà ³íôîðìàö³¿ ó ðîñëèí º îñíîâîþ äëÿ òàêèõ ïðî-
öåñ³â, ÿê ð³ñò, çàõèñò ³ ïðèñòîñóâàííÿ äî íàâêîëèøíüîãî ñåðåäî-
âèùà. Ìîëåêóëÿðí³ ìåõàí³çìè, ùî ëåæàòü â îñíîâ³ ñïðèéíÿòòÿ,
ïåðåäà÷³, àíàë³çó òà çáåð³ãàííÿ åíäîãåííî¿ ³ çîâí³øíüî¿ ³íôîðìà-
ö³¿ âñåðåäèí³ ðîñëèíè, ùå íàëåæèòü ïîâí³ñòþ ç’ÿñóâàòè. Àñîö³-
éîâàí³ ç ðîñëèíîþ ì³êðîîðãàí³çìè òà ¿õí³é âíåñîê â îáðîáêó ³íôîð-
ìàö³¿ äîñë³äíèêè ÷àñòî ³ãíîðóþòü. Åíäîô³òè ÿê ïàðòíåðè ðîñëè-
íè º íåîáõ³äíîþ ³íòåãðàòèâíîþ ÷àñòèíîþ ¿¿ ñèñòåìè. гçíîìà-
í³òí³ åíäîô³òí³ ì³êðîîðãàí³çìè ÿâëÿþòü ñîáîþ «íîðìàëüíó» ì³ê-
ðîôëîðó, ÿêà â³ä³ãðຠâàæëèâó ðîëü â ³ìóí³òåò³ ðîñëèí ³ äîïîìàãàº
¿ì âèæèòè ó íàâêîëèøíüîìó ñåðåäîâèù³ (çàõèñò, æèâëåííÿ, äå-
òîêñèêàö³ÿ òîùî). Ïåâíó ðîëü åíäîô³òíî¿ ì³êðîá³îòè â îáðîáö³
³íôîðìàö³¿ ìîæíà ïðèïóñòèòè, áåðó÷è äî óâàãè êî-åâîëþö³þ ðîñ-
ëèííî-ì³êðîáíèõ ñèñòåì òà åìï³ðè÷í³ äàí³. Îñê³ëüêè â ë³òåðàòóð³
ïî÷èíàþòü ç’ÿâëÿòèñÿ ïóáë³êàö³¿ íà öþ òåìó, â ïðåäñòàâëåíîìó
îãëÿä³ ðîçãëÿíóòî êëþ÷îâ³ ðîáîòè â ãàëóç³ âçàºìî䳿 ðîñëèí ç åí-
äîô³òàìè ó êîíòåêñò³ îáðîáêè ³íôîðìàö³¿ ³ âèñëîâëåíî äóìêó
ñòîñîâíî ¿õíüî¿ ïðîãíîçîâàíî¿ ðîë³ â ³íôîðìàö³éí³é ìåðåæ³ ðîñ-
ëèí çà óìîâ çàõèñòó òà ïðèñòîñóâàííÿ îñòàíí³õ äî çì³íåíèõ óìîâ
òà íàëàøòóâàííÿ â³äïîâ³äíî¿ ïîâåä³íêè ðîñëèíè.
Êëþ÷îâ³ ñëîâà: ðîñëèíà ÿê ñèñòåìà, åíäîô³òè, îáðîáêà ³íôîð-
ìàö³¿, çàõèñò ðîñëèí, ïðèñòîñóâàííÿ.
Í. À. Êîçûðîâñêàÿ
Ïåðåêðåñòíûå âçàèìîäåéñòâèÿ ìåæäó ýíäîôèòàìè è
ðàñòåíèåì-õîçÿèíîì â ñåòÿõ èíôîðìàöèîííîãî ïðîöåññèíãà
Ðåçþìå
Ðàñòåíèÿ ãóñòî íàñåëåíû ïðî- è ýóêàðèîòíûìè ìèêðîîðãàíèç-
ìàìè è, òàêèì îáðàçîì, ïðåäñòàâëÿþò ñîáîé áèîëîãè÷åñêóþ ñèñ-
òåìó ÷ðåçâû÷àéíîé ñëîæíîñòè. Ýòà ñèñòåìà ñ äîâîëüíî
íåïðîñòûìè ïðîöåññàìè êîììóíèêàöèè, ïðîõîäÿùèìè â ðàñòåíèè,
ñóùåñòâóåò äëÿ îáðàáîòêè èíôîðìàöèè. Ñåòåâàÿ îáðàáîòêà èí-
ôîðìàöèè ó ðàñòåíèé ñëóæèò îñíîâîé äëÿ òàêèõ ïðîöåññîâ, êàê
ðîñò, çàùèòà è ïðèñïîñîáëåíèå ê îêðóæàþùåé ñðåäå. Ìîëåêóëÿð-
íûå ìåõàíèçìû, ëåæàùèå â îñíîâå âîñïðèÿòèÿ, ïåðåäà÷è, àíàëèçà
è ñîõðàíåíèÿ ýíäîãåííîé è âíåøíåé èíôîðìàöèè âíóòðè ðàñòåíèÿ,
åùå ïðåäñòîèò âûÿñíèòü. Àññîöèèðîâàííûå ñ ðàñòåíèåì ìèêðî-
îðãàíèçìû è èõ âêëàä â îáðàáîòêó èíôîðìàöèè èññëåäîâàòåëè ÷àñ-
òî èãíîðèðóþò. Ýíäîôèòû êàê ïàðòíåðû ðàñòåíèé ÿâëÿþòñÿ
íåîáõîäèìîé èíòåãðàòèâíîé ÷àñòüþ åå ñèñòåìû. Ðàçíîîáðàçíûå
ýíäîôèòíûå ìèêðîîðãàíèçìû – ýòî «íîðìàëüíàÿ» ìèêðîôëîðà,
âûïîëíÿþùàÿ âàæíóþ ðîëü â èììóíèòåòå ðàñòåíèé è ïîìîãàþ-
ùàÿ èì âûæèòü â îêðóæàþùåé ñðåäå (çàùèòà, ïèòàíèå, äåòîêñè-
êàöèÿ è äð.). Îïðåäåëåííóþ ðîëü ýíäîôèòíîé ìèêðîáèîòû â îáðà-
áîòêå èíôîðìàöìì ìîæíî ïðåäïîëîæèòü, ïðèíÿâ âî âíèìàíèå
êî-ýâîëþöèþ ðàñòèòåëüíî-ìèêðîáíûõ ñèñòåì, à òàêæå ýìïèðè-
÷åñêèå äàííûå. Ïîñêîëüêó â ëèòåðàòóðå íà÷èíàþò ïîÿâëÿòüñÿ ïóá-
ëèêàöèè íà ýòó òåìó, â ïðåäñòàâëåííîì îáçîðå ðàññìîòðåíû êëþ-
÷åâûå ðàáîòû â îáëàñòè âçàèìîäåéñòâèÿ ðàñòåíèé ñ ýíäîôèòà-
ìè â êîíòåêñòå îáðàáîòêè èíôîðìàöèè è èçëîæåíî ìíåíèå îá èõ
ïðîãíîçèðóåìîé ðîëè â èíôîðìàöèîííîé ñåòè ðàñòåíèé â óñëîâè-
ÿõ çàùèòû è ïðîñïîñîáëåíèÿ ïîñëåäíèõ ê èçìåíåííûì óñëîâèÿì è
íàñòðîéêå ñîîòâåòñòâóþùåãî ïîâåäåíèÿ ðàñòåíèÿ.
Êëþ÷åâûå ñëîâà: ðàñòåíèå êàê ñèñòåìà, ýíäîôèòû, îáðàáîò-
êà èíôîðìàöèè, çàùèòà ðàñòåíèé, ïðèñïîñîáëåíèå.
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Received 07.04.13
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CROSSTALK BETWEEN ENDOPHYTES AND A PLANT WITHIN INFORMATION-PROCESSING NETWORKS
Glossary of Terms
Endophytosphere – a plant interior.
Epigenetic processes – heritable changes in gene expression that occur without
changes in the DNA sequence.
Interactome – in molecular biology, the whole molecular interactions that take
place in an organism; in microbial ecology, the system of interactions between
microbial organisms within the microbiome, as well as between the microbiome
and the environment.
Metabolome – the pool of small-molecule metabolites present in a biological cell,
tissue, organ or organism as the end-products of cellular processes under
specific physiological state.
Metagenomic analysis – access to the genetic blueprint of communities of
organisms via an array of genomic and bioinformatics tools.
Microbe-associated molecular pattern (MAMP) – structurally conserved patterns
that are specific for a taxonomic group of microbes and initiate immune
responses in a counterpart (lipopolysaccharides, nucleic acids, flagellin,
peptidoglucans etc.). In plants, MAMPs are usually perceived by cell surface
pattern-recognition receptors.
Microbiome – the totality of microbial organisms, occupying certain econiche.
Pattern recognition receptor – host proteins that recognize MAMPs. These
receptors are membrane-bound proteins, typically represented by two
component receptor kinases.
Persistence – a phenomenon of saving a species under unfavorable conditions by
forming non-dividing cell sub-populations.
Persisters – a small fraction of microbial cells in a dormant state that
phenotypically differ from other cells in the population. Persisters have VBNC
characteristics.
Quorum sensing – a mechanism that regulates gene expression in response to
cell density in microbial populations. Small diffusible molecules (N-acyl-
homoserine lactones, – quinolones and unsaturated fatty acids, linear and cyclic
pep- tides etc.) play a role of regulators in QS (see rev. [82]).
Synchronization – a characteristics of material objects to establish integrated
rhythm of joint action in the specific network of signals, and so far this may
coordinate events to operate a system in unison (I. Blekhman, [83]).
The aloplast – the space outside cells within plant tissue.
The apoplast – the extracellular compartment within plant wall.
Toxin-antitoxin systems – small genetic elements found on plasmids or
chromosomes of bacteria, archaea, and unicellular fungi. Typically, TA consists
of two genes in one operon, encoding a stable toxin that disrupts an essential
cellular process, and a labile antitoxin that neutralizes toxicity by binding to the
protein or to the mRNA of the toxin under normal growth conditions.
Two-component system, TCS – a sensor kinase that responds to specific signals
and a cognate response regulator.
VBNC (viable but not culturable) – resting, non-dividing microorganisms
(bacteria, fungi) that require the removal or addition of certain factors to
renitiate growth; they are not detectable by cultural methods.
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