Extracellular ATP is a central signaling moleculein plant stress responsesYangrong Cao1, Kiwamu Tanaka1, Cuong T Nguyen and Gary Stacey2
Available online at www.sciencedirect.com
ScienceDirect
Because of their sessile nature, plants have developed a
number of sophisticated signaling systems to adapt to
environmental changes. Previous research has shown that
extracellular ATP is an important signaling molecule used by
plants and functions in a variety of processes, including growth,
development, and stress responses. Recently, DORN1 was
identified as the first plant purinoceptor, essential for the plant
response to ATP. The identification of the receptor is a
milestone for our overall understanding of various physiological
events regulated by extracellular ATP. In this review, we will
discuss the possible roles of DORN1 providing future direction
for research into the role of extracellular ATP in plants.
Addresses
Divisions of Plant Sciences and Biochemistry, National Center for
Soybean Biotechnology, C.S. Bond Life Sciences Center, University of
Missouri, Columbia, MO 65211, USA
Corresponding author: Stacey, Gary ([email protected])1 These authors contributed equally to this work.2 Permanent address: 217E C.S. Bond Life Sciences Center, 1201
Rollins Street, University of Missouri, Columbia, MO 65211, USA.
Current Opinion in Plant Biology 2014, 20:82–87
This review comes from a themed issue on Biotic interactions
Edited by Makoto Hayashi and Martin Parniske
http://dx.doi.org/10.1016/j.pbi.2014.04.009
1369-5266X/Elsevier Ltd
IntroductionAdenosine 50-triphosphate (ATP) serves as a universal
energy source for all organisms. ATP is maintained at a
very high concentration (�mM) inside of the cell [1].
However, wounding (e.g. due to herbivory) or stimulation
of the cell with the appropriate stimuli (e.g. touch) can
cause the release of ATP into the extracellular matrix
where it can be recognized by plasma membrane loca-
lized purinoceptors. Animals have two general classes of
purinoceptors: P2X ligand-gated ion channels and P2Y G
protein-coupled receptors [2]. Extracellular ATP has
been shown to play a variety of roles in animals, including
muscle contraction, inflammation, neurotransmission, cell
growth and death [3].
In contrast to animals, the role of extracellular ATP as a
signal in plants has received considerably less attention.
Current Opinion in Plant Biology 2014, 20:82–87
Several reviews have been published in last few years [4–7] surveying evidence that extracellular ATP is a signal in
plants. However, relatively few laboratories have focused
on extracellular ATP reflecting the skepticism that exists
about its function in plants. A similar situation was pre-
sent in the animal research community for many years.
This lasted from the initial reports on extracellular ATP
to the first identification of specific purinoceptors [8,9],
which seemed to convince people that this signaling
pathway did indeed exist in animals [10,11]. Therefore,
the hope is that the recent identification of the first plant
purinoceptor DORN1 [12��] will stimulate greater in-
terest in the role of extracellular signaling in plants.
DORN1 unveils an extracellular ATP signalingpathway in plantsSequence based searches failed to identify animal-like
P2X and P2Y receptors in plants [4]. Therefore, Choi
et al. [12��] utilized a forward genetic screen to identify
Arabidopsis thaliana mutants that failed to show an intra-
cellular calcium response upon the addition of ATP. This
led to the identification of several mutants defective in the
DORN1 gene, which encodes LecRK-I.9 (At5g60300), a L-
type lectin receptor-like kinase. A variety of assays were
used to show that dorn1 mutant plants are insensitive to
ATP, as well as other nucleotides, with the exception of
pyrimidine nucleotides (such as CTP). The extracellular
lectin domain of DORN1 directly binds to ATP with high
affinity (Kd = 45.7 nM) and with the same relative selectiv-
ity as shown by the plant to nucleotides. For example, as
expected, dorn1 mutant plants still respond to CTP [12��].
Therefore, it is likely that Arabidopsis has a separate re-
ceptor for CTP. This is not surprising given that animals
also possess several purinoceptors that can vary with regard
to the ligand specificity. For example, some animal P2Y
receptors recognize other nucleotides (e.g. ADP and UTP)
in addition to ATP [3,13].
Given the accepted nomenclature for purinoceptors in
animals (i.e. P2Y, P2X), Choi et al. [12��] proposed
that DORN1 be considered the founding member in a
new family of purinoceptors, P2K (where K refers to
kinase). Computer based homology searches indicate that
lectin-receptor kinases are only found in plants [14] and,
therefore, the P2K family appears to be plant-specific.
Within the plant kingdom, L-type LecRKs are found in
primitive plants (e.g. moss) through higher plants, but not
in algae [12��]. Indeed, a P2X receptor-like receptor was
previously identified in green algae but appears to act in
the cytoplasm, not as a plasma membrane receptor [15].
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Extracellular ATP in plant stress responses Cao et al. 83
In Arabidopsis, there are 45 genes encoding L-type
LecRK [16], some of which have been implicated in
plant innate immunity [17��,18�,19�,20], response to
wounding [21], salt stress [22,23], osmotic stress
[23,24], and hormone signaling [23–25], suggesting that
the L-type LecRK gene family plays an important role in
mediating plant response to diverse stresses. It is con-
ceivable that some LecRKs function as P2K purinocep-
tors, functionally redundant to DORN1 in specific tissues
and/or growth or developmental stages. Given that dorn1mutant plants still respond normally to pyrimidine
nucleotides, it is also possible that other LecRKs are
pyrimidine receptors.
Extracellular ATP plays a fundamental role inmediating plant environmental responsesExogenous application of ATP can rapidly trigger
elevation of cellular Ca2+ concentration, production of
nitric oxide (NO), reactive oxygen species (ROS), and
phosphatidic acid, and activation of mitogen-activated
protein kinase (MPK) phosphorylation [26�,27–29,30�,31–33]. Many of these same responses (e.g.
Ca2+, NO, and ROS) also exemplify the response of
Figure 1
Defence response(GO:0006952)
Response to stress(GO:0006950)
N-terminmodi(GO:0
Protein(GO:0
Regula-tion of
defenseresponse(GO:0031
347)Protein lipida
(GO:00064
Salt stressresponse(GO:00096
51) Lipoprotemetabolis
(GO:00421
Response to chitin
(GO:0010200)
Immune response(GO:0006955)
Otherorganismsresponse
(GO:0051707)
Biotic stimuliresponse
(GO:0009607)
Signaltransduction(GO:0007165)
Functional categorization of ATP-upregulated genes using GO term enrichmen
322 ATP-upregulated genes by AgriGO (http://bioinfo.cau.edu.cn/agriGO/). The
rectangle represents a cluster of related terms labeled according to representa
Size of the rectangle reflects the p-value. Rectangles are grouped in superclus
immune response (green), protein modification (red), and programmed cell dea
Expression Omnibus.
www.sciencedirect.com
animal cells to extracellular ATP. These responses ulti-
mately lead to the induction of gene expression. For
example, Choi et al. [12��] showed that the expression
of �600 genes in Arabidopsis responded to the addition of
ATP but none of these genes responded in dorn1 mutant
plants. A total of 322 genes were upregulated by ATP
addition [12��]. A comparison of this list of ATP-induced
genes to those responding to a variety of other stresses
showed a significant overlap. Examples are shown in
Figure 1. Many ATP-induced genes are classified into
categories known to respond to biotic or abiotic stresses.
Consistent with this result, various biotic and abiotic
stimuli induce ATP release [30�,34–39]. Therefore, an
obvious hypothesis is that ATP, released from plants as a
result of stresses, acts as an intermediate signal to activate
stress–responsive pathways.
Role of extracellular ATP in plant response towoundingMany stimuli including chemical, heat, pathogen attack,
and other stresses can trigger ATP release from cells, but
the levels of ATP released are usually very low (as
summarized in [4,5]). For example, nM levels of ATP
al proteinfication031365)
acylation043543)
Programmedcell death
(GO:0012501)
Death(GO:0016267)
Immune systemprocess
(GO:0002376)
Photo-synthesis(GO:0015
979)
Carbohy-drate
biosyn-thesis
(GO:0016051)
Response tostimuli
(GO:0050896)
Plastidorgani-zation
(GO:0009657)
tion97) Peptide
modifi-cation
(GO:0018193)in
m57)
Current Opinion in Plant Biology
t test based on Biological Processes. A list of GO terms was generated for
list was summarized and visualized by REVIGO (http://revigo.irb.hr/). Each
tive GO terms and accession number categories shown in the rectangles.
ters with the same color based on the SimRel semantic similarity measure:
th (dark blue). The accession number of the gene list is GSE52610 in Gene
Current Opinion in Plant Biology 2014, 20:82–87
84 Biotic interactions
were released into the surrounding medium when the
Arabidopsis root was mechanically stimulated [38]. How-
ever, given the high affinity of DORN1 for ATP, these
levels of extracellular ATP may be sufficient to trigger
receptor activation. In contrast, ATP levels released at the
site of wounding can reach �40 mM [30�]. Indeed, Choi
et al. [12��] found that �60% of the genes induced by ATP
addition to Arabidopsis were also induced by wounding.
The majority (90%) of these overlapping genes
responded very early to wounding [12��]. Transgenic
lines ectopically expressing DORN1 at a high level
showed a much stronger gene induction in response to
both ATP and wound treatments; whereas expression was
markedly reduced in the dorn1 mutant plants. These data
suggest that extracellular ATP is released during wound-
ing as a damage associated molecular pattern (DAMP)
signal, which is then recognized by the DORN1 receptor
(Figure 2). ATP is well known as a DAMP signal in
animals where it contributes to the wound-induced
inflammatory response which is an important defense
against short-term pathogen infection [40,41]. Although
comparable data is lacking for other biotic and abiotic
stresses, it seems likely that extracellular ATP signaling,
mediated through DORN1, is also important in the plant
response to a variety of stresses.
Role of extracellular ATP signaling in plantinnate immunityIn addition to the response to wounding, there is also
some evidence to suggest that extracellular ATP plays an
important role in plant immune responses. The function
Figure 2
[ATP]e
[ATP]i(mM level)
Wound Exocytosis Transport
An overview of ATP signaling pathway in plants. Cytosolic ATP is discharge
transport. The released ATP binds to the extracellular lectin domain of the D
domain. Receptor activation ultimately leads to a variety of cellular respons
expression.
Current Opinion in Plant Biology 2014, 20:82–87
of extracellular ATP in regulating plant immune
responses seems to be dose-dependent and time-depend-
ent. Short-term treatment (minutes to several hours) with
ATP induced defense-related gene expression and respir-
atory burst oxidase homolog D and F (RBOHD and
RBOHF)-dependent ROS production in Arabidopsis[30�]. Exposure to high levels of ATP (�mM) was shown
to trigger programmed cell death in Populus euphratica[42�]. Similar treatments also led to stomatal closure in
Arabidopsis [43]. Both program cell death and stomatal
closing are viewed as positive indicators of a plant innate
immunity response. Recently, ATP addition was reported
to trigger calcium increase in endoplasmic reticulum [44]
and mitochondria [45], which might link to the induction
of apoptosis [46]. Suppression of apyrases (AtAPY1 and
AtAPY2), which leads to a slight increase of extracellular
ATP levels, induced the expression of several genes, most
of which are involved in biotic stress responses [47��].These data suggest that short-term treatment with ATP
or exposure to higher levels of ATP can enhance plant
defense. However, other conflicting data are available,
perhaps reflecting differences in experimental design.
For example, Clark et al. [43] reported that treatment
with low levels of ATP resulted in stomatal opening
[43,48], which, although not tested, would allow more
efficient pathogen invasion. Prolonged exposure (�days)
to exogenous ATP was shown to suppress hypersensitive
cell death induced by a pathogen-derived mycotoxin [49]
and decrease salicylic acid production, pathogenesis-
related (PR) gene expression, and resistance to bacterial
pathogens and tobacco mosaic virus [50,51], suggesting
[Ca2+ ]i
LectinAPY
Kinase
MPKKK?MPKK?MPK3/6
Ca2+
Ca2+
Binds to ATP receptor
DORN1Limit [ATP]e
Current Opinion in Plant Biology
d outside the cell via cell lysis (i.e. wounding), exocytosis, or active
ORN1 receptor, which in turn activates the intracellular DORN1 kinase
es, including increased cytosolic Ca2+, MAPK activation, and gene
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Extracellular ATP in plant stress responses Cao et al. 85
that prolonged ATP treatment or exposure to low levels
of ATP can suppress plant immune responses.
Plant innate immunity is composed of two successive
layers. The initial plant response is often mediated by
recognition of microbe-associated molecular patterns
(MAMP); that is, conserved molecular signatures on
the microbe that plants have evolved to recognize. This
recognition results in MAMP-triggered immunity (MTI).
However, pathogens adapted to their host by synthesizing
and secreting into the host cell specific proteins, termed
effectors, which actively suppress innate immunity.
Plants can counter this suppression through the pro-
duction of resistance proteins (R proteins) that, either
directly or indirectly, recognize specific effectors. This R
protein mediated immunity is termed effector-triggered
immunity (ETI).
There is considerable overlap between genes induced by
ATP and those also induced by a variety of pathogens
(Figure 1), which might reflect an overlap between the
plant DAMP response (to ATP) and MTI. Indeed, the
addition of chitin mixture or yeast extract is known to
induce ATP release in the root tissues of Medicago trun-catula and Salvia miltiorrhiza [35,39]. Previously, LecRK-
I.9 (DORN1) was shown to be a potential target of IPI-O
[52], a RXLR-dEER effector protein secreted by the
pathogen Phytophthora. Indeed, mutant plants defective
in LecRK-I.9 showed enhanced susceptibility to the
oomycete pathogen P. brassicae [17��]. Strong ectopic
expression of LecRK-I.9 in Arabidopsis, potato, and Nicoti-ana benthamiana plants resulted in increased resistance to
Phytophthora [17��,53�], suggesting the possibility of using
DORN1 to improve disease resistance in crop plants.
Therefore, the data suggest a central role for ATP in
mediating the plant innate immunity response, as well as
the DORN1 receptor, which pathogens have evolved to
target with effector proteins, presumably to suppress
disease resistance.
A model for ATP actionThe identification of the first plant purinoceptor should
encourage greater attention to the role of ATP as an
important signal in plants [12��]. A possible model for
the action of ATP is shown in Figure 2. In this model,
cytosolic ATP is released by physical wounding or other
stresses. Since brefeldin A, an inhibitor of vesicular
transport, blocks ATP release upon chitin treatment,
it is likely that vesicle fusion with the plasma mem-
brane is one mode of ATP release [39]. Such a path for
ATP release has been well documented in animal
systems [54]. Recently plasma membrane-located
ATP transporters were identified, which could transport
ATP into the plant apoplast [55]. The released ATP
directly binds to DORN1 which causes intracellular
signaling by activating DORN1’s kinase activity. Sub-
sequent signaling steps, undefined at this point, would
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lead to induction of calcium influx, ROS and NO
production, MPK phosphorylation, and gene expres-
sion. This pathway would activate those plant processes
necessary to protect the plant against detrimental
environmental change.
Conclusion and future directionsA wealth of published data strongly supports the existence
of extracellular ATP in plants and it role as a vital extra-
cellular signal. The identification of the DORN1 purino-
ceptor and studies of plants lacking this receptor indicate
that extracellular ATP is a central signal involved in the
plant response to a variety of stresses. It seems likely that
these stresses induce the release of ATP and responses,
previously attributed strictly to the stress, are actually in
direct response to extracellular ATP. Therefore, in order to
fully understand the mechanisms by which plants recog-
nize and respond to stress, it is essential that we understand
the critical and central role of extracellular ATP. Many,
many questions remain to be answered. For example, work
on the structure and function of DORN1 is just beginning.
Similar to other receptors, it is likely that DORN1 acts in
conjunction with other proteins, which likely facilitate
downstream signaling. Examples would include those
proteins that are targets of DORN1 kinase activity.
Animals possess a number of P2X and P2Y receptors
and, therefore, one would expect that other P2K receptors
will be found in plants. Choi et al. [12��] found that
mutations in DORN1 eliminated all of the responses that
they could measure in response to extracellular ATP
addition. Therefore, other Arabidopsis P2K receptors likely
act in specific tissues or during specific growth or devel-
opmental stages. However, the Arabidopsis receptor that
mediates the response to CTP remains to be identified and
may be a P2K family member.
AcknowledgementsThis work was supported by the Division of Chemical Sciences,Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S.Department of Energy (grant no. DE-FG02-08ER15309) and the Next-Generation BioGreen 21 Program Systems and Synthetic AgrobiotechCenter, Rural Development Administration, Republic of Korea (grant no.PJ009068).
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53.�
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Current Opinion in Plant Biology 2014, 20:82–87
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