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Evolution of Hormone
Signaling Networks in
Plant Defense
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Matthias L. Berens,1 Hannah M. Berry,2 Akira Mine,1

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Cristiana T. Argueso,2 and Kenichi Tsuda1

Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research,
50829 Cologne, Germany; email:
Department of Bioagricultural Sciences and Pest Management, Colorado State University,
Fort Collins, Colorado 80523

Annu. Rev. Phytopathol. 2017. 55:18.118.25 Keywords

The Annual Review of Phytopathology is online at plant defense, phytohormones, hormone cross talk, evolution, trade-off Abstract
Studies with model plants such as Arabidopsis thaliana have revealed that phy-
Copyright  c 2017 by Annual Reviews. tohormones are central regulators of plant defense. The intricate network of
All rights reserved
phytohormone signaling pathways enables plants to activate appropriate and
effective defense responses against pathogens as well as to balance defense
and growth. The timing of the evolution of most phytohormone signaling
pathways seems to coincide with the colonization of land, a likely require-
ment for plant adaptations to the more variable terrestrial environments,
which included the presence of pathogens. In this review, we explore the
evolution of defense hormone signaling networks by combining the model
plant-based knowledge about molecular components mediating phytohor-
mone signaling and cross talk with available genome information of other
plant species. We highlight conserved hubs in hormone cross talk and discuss
evolutionary advantages of defense hormone cross talk. Finally, we examine
possibilities of engineering hormone cross talk for improvement of plant
fitness and crop production.


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In nature, plants are constantly exposed to a vast number of insects and microbes such as viruses,
bacteria, fungi, and oomycetes (76, 81). Some of these are herbivores or pathogens that reduce plant
fitness and crop production (29, 76). Plants recognize microbial or insect signatures to activate in-
nate immune responses. For instance, recognition of conserved pathogen- or microbe-associated
molecular patterns (PAMPs or MAMPs) via cell surfacelocalized pattern-recognition recep-
tors (PRRs) activates pattern-triggered immunity (PTI) (29). Plant-derived damage-associated
molecular patterns (DAMPs) that are released upon infection or herbivore feeding are recognized
similarly to MAMPs and also trigger immune responses (29). Pathogens sometimes overcome
PTI by deploying virulence effectors (81, 151), whereas some hosts sense virulence effectors
mainly through intracellular nucleotide-binding leucine-rich-repeat receptors (NLRs), resulting
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in activation of effector-triggered immunity (ETI) (81). Activated immune responses such as the
production of reactive oxygen species, activation of MAP kinases (MAPKs), and transcriptional
reprogramming occur in both PTI and ETI but with temporal and quantitative differences (30).
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Although receptor repertoires are mostly family specific, PTI signaling downstream of receptors
seems to be conserved in land plants ranging from the moss Physcomitrella patens to angiosperms
(14, 93, 116, 137).
Phytohormones are small molecules produced within plants that govern diverse physiological
processes, including plant defense. Among them, jasmonate ( JA) and salicylic acid (SA) are major
defense-related phytohormones (151). Other phytohormones, such as ethylene (ET), abscisic
acid (ABA), auxin, gibberellins (GAs), cytokinins (CKs), and brassinosteroids (BRs), are also
involved in defense responses (151). Signaling pathways mediated by these phytohormones
intimately interact antagonistically or synergistically (Figure 1). This regulatory logic determines
the outcome of downstream responses activated by phytohormones. Hormonal interactions
collectively form hormone signaling networks, which mediate immunity as well as growth and
abiotic stress responses (134). The importance of hormone signaling networks in defense is
reflected by the fact that many pathogens interfere with hormone signaling or produce hormones
that increase virulence (151, 155).

prioritization Xa Xb Xa Xb Xa Xb Xa Xb

accuracy Xab Xab Xab Xab
Figure 1
Conceptual representation for roles of antagonistic and synergistic cross talk between the two putative
phytohormones A and B. The illustrations show the outcomes in three different stimulus conditions (only A,
only B, both A and B). The antagonistic cross talk can mediate prioritizing the response Xa over Xb , whereas the
synergistic cross talk ensures an accurate induction of the response Xab only when both A and B are activated.

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During the past three decades, extensive knowledge about molecular mechanisms for hormone
signaling and cross talk in plant defense has only been obtained for limited species, such as the
model eudicot plant Arabidopsis thaliana (134, 151). Thus, only fragmented knowledge about the
evolutionary conservation of hormone signaling networks in plants is currently available. Under-
standing conservation or diversification of hormone signaling networks is crucial for translation of
knowledge from model species to crops. Moreover, we comprehend plant adaptations to environ-
ments only when we understand when, why, and how hormone signaling and cross talk evolved.
In this review, we summarize hormone signaling networks in plant defense from an evolutionary
perspective. We also speculate about the evolution of hormone networks by combining molecular
insights gained from studies in model plant species with available genome information for other
plant species. Furthermore, we discuss roles in plant defense for and evolutionary advantages of
hormone cross talk. Finally, we explore possible strategies for engineering hormone cross talk to
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improve crop production.

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In A. thaliana, although there are exceptions, JA is a positive regulator of immunity against
necrotrophic pathogens that actively kill hosts to acquire nutrients and herbivore defense, whereas
SA is a positive regulator of immunity against biotrophic pathogens that feed on living hosts as well
as against hemibiotrophs that show a biotrophic phase in the early stage of infection (56). Other
phytohormones, such as ABA, auxin, BRs, ET, GAs, and CKs, modulate immunity in hormone
signaling networks mainly through interactions with SA and JA (134).

Salicylic Acid and Jasmonate as Conserved Positive Regulators of Plant Defense

Salicylic acid. Plants synthesize SA via two pathways: the phenylalanine ammonium lyase (PAL)
pathway and the isochorismate (IC) pathway, both of which utilize chorismate, the end product of
the shikimate pathway, as a precursor (35). The PAL pathway operates in the cytosol, and the IC
pathway operates in chloroplasts. Mutation or silencing of isochorismate synthase 1 (ICS1), which
encodes a key enzyme of the IC pathway in A. thaliana, tomato, tobacco, and soybean, leads to
the loss of pathogen-triggered SA production (19, 152, 174, 187). Interestingly, silencing of PAL
genes also results in the loss of SA induction upon pathogen infection in soybean (152). Decreased
PAL activity only partially compromises SA induction in A. thaliana, tobacco, and cucumber (77,
131, 154). Thus, in eudicots, the IC pathway seems to be the major route for SA biosynthesis in
immunity, but the PAL pathway also contributes. Genes for both pathways are present in the moss
P. patens, which also exhibits pathogen-induced SA accumulation (137); this may suggest conserved
roles of these SA biosynthesis pathways for immunity in the land plants. The importance of these
SA biosynthesis pathways is reflected by the fact that the effector Cmu1 from the fungal pathogen
Ustilago maydis degrades chorismate via the chorismate mutase activity, thereby reducing host SA
production and promoting pathogen virulence (46). Secreted chorismate mutases are widespread
among plant-associated microbes (46).
It is not known when the reliance of eudicots on the IC pathway for SA biosynthesis in immunity
was established. ICS converts chorismate to IC, which is presumably further metabolized into SA
in plants (160). IC is also the precursor of phylloquinone, an essential metabolite for photosynthesis
in plants (60). Thus, conservation of the ICS gene in land plants does not necessarily mean that
it contributes to SA biosynthesis. Interestingly, the fungal pathogen Verticillium dahliae secretes
an isochorismatase, Vdlsc1, that hydrolyzes IC, thereby reducing SA biosynthesis and promoting
virulence (101). V. dahliae has a broad host range (more than 200 plant species) but does not
cause diseases in monocots (78, 101). This, together with the lack of evidence that ICS is essential Evolution of Hormone Signaling Networks in Plant Defense 18.3

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for SA biosynthesis in monocots, suggests that the major contribution of the IC pathway to SA
biosynthesis during immune responses may be restricted to eudicots or even certain orders within
eudicots (198). Importantly, the enzyme that converts IC to SA has not been identified in plants.
Plant genomes do not include genes similar to bacterial IC pyruvate lyases that can convert IC to SA
(35). Thus, SA biosynthesis may be more complex and diversified in plants compared with bacteria.
Further research is required to understand SA biosynthesis and its evolution in the plant lineage.
Pathogen infection causes increased SA accumulation in eudicots such as A. thaliana, strawberry,
pepper, and potato (52, 59, 64, 86, 193), although this does not appear to be the case in monocots.
However, exogenous application of SA or its analog benzothiadiazole (BTH) triggers immune
responses and resistance against biotrophic and hemibiotrophic pathogens in both eudicots and
monocots (59, 162, 172, 193). Reducing endogenous amounts of SA by ICS or PAL suppression or
by introducing the bacterial salicylate hydroxylase gene NahG increases susceptibility to biotrophic
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and hemibiotrophic pathogens in many eudicots and monocots (64, 86, 110, 125, 152). Thus,
regulation of SA biosynthesis during plant immunity may not be conserved, but the positive role
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of SA in resistance against biotrophs and hemibiotrophs is widely conserved in angiosperms.

Interestingly, a fungal elicitor treatment increases SA accumulation in the cell culture of the
gymnosperm Ginkgo biloba (191), although whether SA contributes to immunity in G. biloba is not
known. In P. patens, SA is induced upon infection with the fungal pathogen Botrytis cinerea (137),
and SA application increases resistance against the bacterial pathogen Pectobacterium carotovorum
(formerly Erwinia carotovora) (5). Furthermore, the central regulator of SA signaling, nonexpressor
of pathogenesis-related genes 1 (NPR1), is conserved in land plants but not in algae (168). Because
the loss of SA does not lead to obvious developmental or growth defects in most angiosperms (171),
SA signaling appears to have evolved to regulate plant defense against microbial pathogens after
colonization of the land.

Jasmonate. In A. thaliana, chloroplast membrane lipids are converted to 12-oxophytodienoic

acid (OPDA) via sequential enzymatic reactions of lipoxygenases (LOXs), allene oxide synthase
(AOS), and allene oxide cyclase (185). OPDA is further converted to jasmonic acid via 2-oxo-
phytodienoic acid reductases (OPRs) (185). The isoleucine-conjugate of jasmonic acid ( JA-Ile) is
formed by JA amido synthetase 1 ( JAR1) and is known as the most potent endogenous form of JA
(185). The P. patens genome contains JA biosynthesis genes, including LOX, AOS, and OPR (137).
However, the complete biosynthesis of active JA seems to be absent in P. patens (137), whereas
P. patens produces detectable levels of the JA precursor OPDA (137). However, jasmonic acid and
JA-Ile are detected in several other bryophytes at different levels with no obvious relationship to
phylogeny (201).
In A. thaliana, JA-Ile is perceived by coronatine-insensitive 1 (COI1), which mediates
26S proteasome-dependent degradation of JAZ ( JA ZIM-domain) family proteins that act as
transcriptional repressors in JA signaling (185). This liberates a group of MYC transcription
factors from regulatory suppression, thereby initiating transcriptional reprogramming (185). The
COI1-JAZ-MYC core JA-signaling components are conserved in bryophytes such as P. patens and
lycophytes such as Selaginella moellendorffii but not in algae (168). Thus, JA signaling seems to have
been acquired after the separation of land plants from algae. P. patens responds to not only OPDA
but also methyl JA (137), which is an inactive form of JA that is presumably converted to active
JA in plants (185). Thus, the JA perception system in bryophytes may ambiguously recognize
OPDA and JA. More specifically, the JA and COI1 perception system may have been established
later in evolution, as A. thaliana COI1 does not interact with OPDA (169). Interestingly, in
P. patens and A. thaliana, the lack of OPDA or JA biosynthesis and signaling, respectively, results
in developmental defects (158, 161). It is tempting to ask whether defense or development is the

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ancient role of JA/OPDA signaling. This may be answered by extensive comparative analysis in
JA application triggers immunity against necrotrophic pathogens in A. thaliana, rice, and Med-
icago truncatula (55, 156, 164). Consistently, abundant evidence supports the idea that endogenous
JA biosynthesis is required for immunity against necrotrophic pathogens in many angiosperm
species (16, 192). In addition to necrotrophic pathogens, JA is associated with herbivore defense
in multiple angiosperms, such as A. thaliana, maize, poplar, Picea sitchensis, Nicotiana attenuata, and
M. truncatula (76). Outside of angiosperms, knowledge regarding the roles of JA in plant defense
is scarce. In the gymnosperm G. biloba and the fern Pteridium aquilinum, JA treatment triggers
production of volatile compounds (140, 175) that might attract natural predators of the attacking
herbivores, thereby acting as defense molecules (76). These results suggest that positive roles of
JA in defense exist broadly in vascular plants. However, further research into nonvascular plants
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is required to understand the emergence of JA roles in triggering defense.

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Abscisic Acid, Auxin, Ethylene, Cytokinins, Gibberellins, and Brassinosteroids

as Modulators of Plant Defense
Abscisic acid. ABA has a major function in abiotic stress response, which explains the high degree
of conservation of its signaling pathway within all land plants (31, 111). ABA biosynthesis from
carotenoid precursors involves the zeaxanthin epoxidase ABA deficient 1 (ABA1) that contributes to
stress-induced ABA accumulation in P. patens and angiosperms (166). Similarly, genes for the core
ABA signaling pathway, consisting of pyrabactin resistance 1/PYR1-like regulatory component of
ABA receptor (PYR/PYL/RCAR), clade A phosphatase 2Cs (PP2Cs), and Snf1-related kinases 2
(SnRK2s), show high functional conservation within all land plants. Because no homologs of the
ABA receptors have been identified in algal genomes (180), ABA signaling most likely evolved
during colonization of the land to promote survival in stressful environments (31).
ABA triggers the closure of stomata, which are a major route for invasion into plant tissues by
many foliar microbial pathogens (99, 113). In angiosperms, pathogen entry is deterred by stomatal
closure, a plant defense mechanism, triggered via recognition of MAMPs such as flagellin and
chitin (113). In A. thaliana, both ABA and SA biosynthesis and signaling are required for full
MAMP-triggered stomatal closure, although the detailed mechanism of how these two hormones
cooperate is obscure (114, 209). ABA also plays an important role in MAMP-induced stomatal
closure in tomato (48). In P. patens, ABA triggers stomatal closure, and the downstream signaling
pathway seems to be conserved (20, 99). However, this response is absent in ferns and lycophytes,
suggesting that ABA-triggered stomatal closure arose by convergent evolution in some bryophytes
and seed plants or that extant ferns and lycophytes have lost the mechanism previously evolved
in bryophytes (111). Although the MAMP chitin is recognized and triggers immune responses in
P. patens (14), it is not known whether chitin triggers stomatal closure in P. patens. Comparative
analysis of MAMP- and ABA-triggered stomatal closure across the plant lineage contributes to
our understanding of the evolution of stomatal closure in response to biotic and abiotic stresses.
In contrast to its positive role in stomata immunity, ABA application induces disease suscep-
tibility in A. thaliana, tomato, soybean, barley, and rice independent of the pathogen lifestyle
(9, 89, 173, 184). Consistently, lowering host ABA biosynthesis increases pathogen resistance in
A. thaliana, tomato, rice, and barley (9, 89, 173). However, ABA promotes postinvasive immunity
in some cases (41, 73). Complex immune modulations by ABA are likely explained by interactions
with other hormone signaling pathways (134).
In postinvasive immunity, ABA antagonistically interacts with SA. In A. thaliana, ABA appli-
cation suppresses SA accumulation concomitantly with reduced expression of ICS1 (196). ABA Evolution of Hormone Signaling Networks in Plant Defense 18.5

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treatment also blocks chemically induced SA accumulation in tobacco (92). In tomato, impaired
ABA biosynthesis leads to increased PAL activity (9), and ABA suppresses enzymatic PAL activity
in soybean (184). In rice, ABA suppresses SA-mediated defense response through inactivation
of a MAPK, an important SA signaling component in rice (172). Thus, SA suppression by ABA
is widespread in angiosperms, although distinct mechanisms seem to have evolved in different
species. This idea is supported by the fact that many pathogens produce ABA or hijack host ABA
production to suppress SA-mediated immunity in a wide range of plant species (7, 57).

Auxin. Auxin regulates plant growth and development (200). In angiosperms, the tryptophan
aminotransferase of Arabidopsis (TAA) and YUCCA flavin monooxygenase (YUC) pathway is the
major auxin biosynthesis pathway in which Trp is the precursor (200). This route seems to be an
innovation of land plants, although there is some debate as to whether it previously evolved in
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charophytes, a group of green algae (200). In A. thaliana, auxin is perceived by transport inhibitor
response 1 (TIR1) and the auxin signaling F-box (AFB) proteins, which mediate degradation
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of auxin/indole-3-acetic acid (Aux/IAA) transcriptional repressors through the 26S proteasome

(180). Degradation of Aux/IAA liberates the transcription factors auxin response factors (ARFs),
allowing for the expression of auxin-response genes (180). These core auxin signaling components
are conserved in angiosperms, bryophytes such as P. patens, and the lycophyte S. moellendorffii
(95, 180, 200). Consistently, the growth-promoting effect of auxin is observed across land plants
(95). Thus, auxin signaling was likely established during land colonization, although certain auxin
signaling components were already present in some charophytes (180).
In angiosperms, activation of auxin signaling is often associated with disease susceptibility. For
instance, application of an auxin such as indole-3-acetic acid (IAA) increases susceptibility against
hemibiotrophic pathogens in rice (52). In A. thaliana, Brassica rapa, soybean, and wheat, auxin-
deficient plants show resistant phenotypes (79, 120, 183, 197). In P. patens, treatment with high
levels of auxin leads to disease susceptibility to Pythium debaryanum, whereas low concentrations
promote resistance (116), pointing to complex immune modulation by auxin. This dose depen-
dency may explain the context-dependent effects of auxin on immunity (53). In A. thaliana, auxin
signaling interacts with other phytohormone signaling pathways, including SA, JA, and ET (134).
For example, auxin suppresses immunity against the bacterial pathogen Pseudomonas syringae via
SA suppression (144, 181), whereas SA application stabilizes auxin resistant 2 (AXR2), a repressor
of auxin-mediated transcription, thereby suppressing auxin signaling (181). In P. patens, elicitor-
induced accumulation of IAA is associated with decreases in SA (3), suggesting that immune
suppression by IAA through interaction with other phytohormone signaling processes emerged
before bryophytes and other land plants diverged. Consistent with the modulator roles of auxin in
plant immunity, many plant-associated bacteria and fungi produce auxin or manipulate host auxin
accumulation (7, 57, 155, 197). These include both mutualistic and pathogenic microbes.

Ethylene. ET plays diverse physiological roles in plant growth and development and in
stress responses in land plants (82). ET is synthesized from the enzymatic conversion of S-
adenosylmethionine to 1-amino-cyclopropane-1-carboxylic acid (ACC) by ACC synthase (ACS)
and subsequently to ET by ACC oxidase (82). ET is perceived by multiple receptors that include
ethylene response 1 (ETR1) in the endoplasmic reticulum membrane, which activates the key
component ethylene insensitive 2 (EIN2) (151). Upon activation, the C-terminal part of EIN2 is
cleaved and moves into the nucleus, where it activates the transcription factor ethylene insensi-
tive 3 (EIN3) (151). This core ET signaling pathway was likely assembled during the course of
evolution of the charophyte lineage that gave rise to land plants (82), although further fine-tuning
mechanisms evolved later (180).

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ET contributes positively and negatively to immunity depending on the pathogen, environ-

mental conditions, and plant species. For instance, in soybean, ET insensitivity increases severity
of disease caused by the necrotrophic fungus Rhizoctonia solani (71), whereas enhanced ACS2
expression promotes resistance against R. solani in rice (69). Thus, as reported in A. thaliana, pos-
itive roles of ET in resistance against necrotrophs seem widespread in angiosperms (56). ET also
contributes to resistance against biotrophic and hemibiotrophic pathogens in A. thaliana, soy-
bean, tobacco, and rice (69, 71, 150, 170). In A. thaliana, perception of bacterial flagellin triggers
ET production through increased expression of ACS and stabilization of ACS (36, 102). How-
ever, there are many examples in which ET promotes disease susceptibility against biotrophs and
hemibiotrophs (21, 23, 100, 107, 149). This dichotomy can be explained by complex modulation
of SA and JA signaling by ET interaction (134). For instance, cooperation between ET and SA is
evident in transcriptional reprogramming in response to MAMPs in A. thaliana (170). In contrast,
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EIN3 binds to the promoter of ICS1 to repress its expression (21). Furthermore, ET signaling
represents an inhibitory signaling sector for both JA and SA in the PTI signaling network (171).
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Because ET signaling precedes JA and SA signaling (180), ET signaling could have been co-opted
by later-emerging JA and SA signaling pathways as a core modulator.

Cytokinins. CKs regulate multiple physiological processes, including regulation of cell division
in land plants (151). CK signaling employs a two-component phosphor-relay system similar to
those widely used in microbial systems. In A. thaliana, upon binding to CK, histidine kinase
is activated via autophosphorylation and phosphorylates the downstream components, histidine
phosphotransfer proteins, which then phosphorylate response regulator proteins (ARRs) in the
nucleus (151). ARRs are divided into at least two major groups, type-A and type-B ARRs (151).
Type-B ARRs are positive regulators and can function as DNA-binding transcription factors,
whereas type-A ARRs lack DNA binding domains and act as negative regulators of CK signaling
(151). This core CK signaling pathway was likely assembled in charophytes (180).
Exogenous CK treatments increase resistance against biotrophic and hemibiotrophic pathogens
in rice, barley, tobacco, and potato (10, 61, 63, 80, 103, 148). The effects of CK on immunity are
dependent on the concentration in some species: high CK levels lead to resistance, whereas low
CK levels result in susceptibility (6, 63, 80, 103, 148). In A. thaliana, CK enhances SA responses,
thereby positively contributing to resistance against biotrophic pathogens. This is partly explained
by a physical interaction between a type-B ARR, ARR2, and an NPR1-interacting transcription
factor, TGA3 (6, 26). The cooperation of CK with SA has also been observed in tobacco and rice
(61, 80), suggesting that this is a conserved cross talk in angiosperms. However, it is not known
whether the same molecular mechanism operates in different species. Although SA signaling in
plant immunity likely evolved after the CK pathway, the charophyte lineage seems to have the
TGA class of bZIP transcription factors (180). Thus, it is possible that this ARR-TGA cross
talk emerged to mediate immunity or other processes before SA signaling evolved. This question
deserves further investigation.

Gibberellins. GAs regulate various developmental processes such as stem elongation in an-
giosperms. GA is perceived by gibberellin insensitive dwarf 1 (GID1) in the nucleus (151). GA-
bound GID1 interacts with and triggers proteasome-mediated degradation of DELLA proteins,
which are negative regulators of GA signaling (151). GID1 and DELLAs exist in land plants (180);
however, active GA is barely detectable in P. patens (65). P. patens GID1 and DELLA lack the
protein-protein interaction domains that are present in angiosperms (180) and do not interact
(70). Furthermore, P. patens GID1 is unable to complement A. thaliana gid1 mutants (37). These Evolution of Hormone Signaling Networks in Plant Defense 18.7

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PY55CH18-Tsuda ARI 15 June 2017 8:49

findings suggest that GA signaling evolved in a stepwise acquisition (37) and the full GA signaling
pathway likely originated after the evolutionary split of bryophytes in the land plant lineage (180).
Like other modulator hormones, GA also influences immunity in angiosperms (39, 44, 98, 122).
Involvement of GA in immunity is, for example, mediated by the interaction between DELLAs
and JAZs (75, 122), negative regulators of GA and JA signaling, respectively (151). Considering
that P. patens DELLA lacks the domain required to interact with GID1 and JAZs (75, 180), the
GA-JA cross talk through DELLA-JAZ interaction likely evolved after the evolutionary split of
P. patens from the lineage that led to the vascular plants.

Brassinosteroids. BRs are phytohormones regulating growth in angiosperms (25, 27). The
P. patens and S. moellendorffii genomes lack orthologous genes for BR biosynthesis in A. thaliana
(145). However, BRs were detected in plants ranging from algae and bryophytes to gymnosperms
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and angiosperms, suggesting that different BR synthesis pathways have evolved in plants (145).
Sequence comparisons of BR receptors orthologous to the A. thaliana brassinosteroid insensitive 1
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(BRI1) suggest that the BR perception system observed in A. thaliana was established no earlier
than the divergence of lycophytes from the seed plant lineage (37, 179). Another study suggests
that the canonical BR pathway emerged after the split between gymnosperms and angiosperms
(180). In any case, the BRI1-mediated BR signaling seems to be a relatively recent innovation
compared to other phytohormones (82). S. moellendorffii responds to BR for growth regulation,
suggesting that BR signaling exists in lycophytes, although the signaling mechanism seems to be
different from the one found in angiosperms (25).
BRs modulate immunity positively or negatively in a context-dependent manner. It is known
that BR signaling interacts with multiple other hormone signaling pathways, although only a few
molecular insights have been described (32). For instance, in rice, BR recognition leads to DELLA
stabilization that consequently blocks GA signaling (40). Consistently, BR and GA treatments have
opposite effects on resistance against the oomycete pathogen Pythium graminicola (40). Another
interesting aspect of BR in immunity is that MAMP and BR perception share the coreceptor
BRI1-associated receptor kinase 1 (BAK1), also known as somatic embryogenesis receptor kinase 3
(SERK3), and other SERK family members in A. thaliana (32, 109). Involvement of BAK1 in the
cross talk between PTI and BR signaling is under debate (32). Although BAK1 was originally
isolated as a gene required for BR signaling in A. thaliana (32), BAK1 might have been functional
in PTI signaling before it was integrated into BR signaling, as functional BAK1 is present in
P. patens, whereas BRI1 seems to have emerged no earlier than the divergence of lycophytes from
the seed plant lineage (11, 182).


Studies with the model plant A. thaliana have significantly advanced our understanding of molecu-
lar components that mediate hormone cross talk (134, 151). Here, we highlight several hub compo-
nents that are central in hormone signaling networks from an evolutionary perspective (Figure 2).

Figure 2
(a) Schematic overview of the conservation of hormone signaling components. The tree illustrates representative species in plant
evolution and was copied and modified from phytozome v11.0 (58). Conservation of signaling components (colored bars) is based on
Wang et al. (180). (be) Schematic representation of potentially conserved hormone cross talks: (b) abscisic acid (ABA)salicylic acid
(SA)-immunity cross talk, (c) auxin-immunity cross talk, (d) gibberellin (GA) and jasmonate ( JA) cross talk via DELLA-JAZ interaction,
and (e) ABA, JA, GA, and ethylene (ET) cross talk via the hub MYC2. The color code facilitates analysis of conservation of components
based on panel a.

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, IC



l. D














Medicago truncatula
a Fabidae
Glycine max
Arabidopsis thaliana
Arabidopsis lyrata
Brassicaceae Capsella rubella
Eutrema salsugineum
Carica papaya
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Gossypium raimondii
Rosid Citrus sinensis
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Pentapetalae Linum usitatissimum

Eucalyptus grandis
Vitis vinifera
Kalanchoe laxiflora
Solanum tuberosum
Solanum lycopersicum
Angiosperm Aquilegia coerulea
Zea mays
Oryza sativa
Brachypodium distachyon
Embryophyte Amborella trichopoda
Selaginella moellendorffii
Viridiplantae Bryophytes
Physcomitrella patens ?
Chlorophyte ?
Chlamydomonas reinhardtii
Conserved Not conserved ? Not identified

b Abiotic stress Pathogens c IAA GH3.X GH3.X Immunity


PALs TIR1 miR393

SA NPR1 Immunity AUX/IAA

closure ARFs IAA response Immunity

d GA JA-Ile e ABA JA-Ile ANACs

DELLA JAZs response SA
DELLA Immunity
response MYCs JA/ET
response GA EIN3
(and others) response

Activation Inhibition Protein degradation Transcription Evolution of Hormone Signaling Networks in Plant Defense 18.9

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In A. thaliana, the major mode of SA perception is explained by functions of NPR1 and its ho-
mologs, NPR3 and NPR4 (147). NPR1 binds SA through Cys521/529 via the transition of the metal
copper, which triggers a conformational change of NPR1, allowing transcriptional regulation,
for example, through interactions with TGA-type transcription factors (189). However, these Cys
residues are not conserved among other plant species, suggesting either that the function of NPR1
as an SA receptor might have evolved relatively recently or that distinct amino acids harboring
electronegative elements are involved in copper binding in other plants (189). Another study re-
ports that NPR3 and NPR4 perceive SA, thereby regulating NPR1 protein turnover (54). In this
model, NPR3 and NPR4 provide stable NPR1 in a specific range of SA concentrations (147).
Thus, this SA perception mode requires all three NPR proteins. NPR1, NPR3, and NPR4 are
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broadly divided into two subclasses in angiosperms: NPR1 or NPR3/4. Although angiosperms
generally contain an NPR1 and two genes for NPR3 and NPR4, P. patens has only two NPR genes,
which are not diverged into the two subclasses (180). As mentioned earlier, P. patens responds to
Annu. Rev. Phytopathol. 2017.55. Downloaded from

SA (5). NPR1 is conserved in angiosperms, lycophytes, and bryophytes but not in algae (168, 180),
suggesting that NPR1-dependent SA signaling was assembled in plants during land colonization.
Nevertheless, SA perception mechanisms may be distinct in different plant species.
In A. thaliana, NPR1 mediates SA-regulated suppression of JA and ABA signaling (146, 156,
196). WRKY70, a transcription factor that acts downstream of NPR1, has been identified as a me-
diator of suppression of JA and ABA responses by SA (96, 97). Similar to NPR1, WRKY70 shows
conservation in land plants, including bryophytes and lycophytes (168). Importantly, rice NPR1
and WRKY13 (orthologous to A. thaliana WRKY70) also mediate suppression of JA response by
SA (139, 199). NPR1 is also a target of other phytohormones. For example, in A. thaliana, ABA
treatment induces proteasome-mediated NPR1 degradation, which correlates with a suppression
of SA-mediated responses by ABA (45). The suppressive effect of ABA on SA responses has also
been observed in tobacco and rice (92, 172). Thus, NPR1 is likely an important conserved hub in
the interconnection between SA and other hormone signaling pathways.

MYC2 is a core transcriptional activator of JA signaling and is conserved in land plants (13, 17,
83, 153, 203). MYC2 regulates JA-mediated suppression of ICS1 and induction of genes for SA
metabolism through transcriptional regulation of SNAC-A transcription factors in A. thaliana (165,
209). A similar mechanism involving SNAC-A transcription factors seems to operate in tomato for
JA-mediated suppression of SA accumulation (48). Because SNAC transcription factors are found
in genomes of land plants, including P. patens and S. moellendorffii (121, 124, 129, 133, 135, 165), it
is interesting to test whether the function of SNAC in SA suppression is conserved in other plants.
During PTI in A. thaliana, MYC2 and its homologs MYC3 and MYC4 negatively regulate
expression of phytoalexin deficient 4 (PAD4), which contributes to SA accumulation (115). This
transcriptional regulation also occurs in other Brassicaceae species. Interestingly, MYC2 activates
expression of a gene essential for SA accumulation, enhanced disease susceptibility 5 (EDS5), through
direct binding to its promoter (115). This transcriptional regulation ensures resilient SA accumu-
lation at high temperature when PAD4 cannot fulfill its function. Apparently, EDS5 orthologs are
restricted to the family Brassicaceae. EDS5 is inducible by JA in Brassicaceae species that contain the
MYC2 binding motif (CACGTG) in the EDS5 promoter (115). Thus, transcriptional regulation
of EDS5 by JA seems to be an innovation of the Brassicaceae family.
In A. thaliana, application of egg extracts from the cabbage butterfly Pieris brassicae triggers
proteasome-mediated degradation of MYC2 in an SA-dependent manner, which correlates with
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reduced defense against this herbivore (146). Interestingly, in tomato, herbivore-induced JA sup-
pression via SA activation is mediated by bacterial symbionts in the herbivore, suggesting that
herbivores exploit SA-mediated suppression of JA (28, 42). Because MYC2 and SA responses are
conserved in land plants, SA-mediated MYC2 degradation can be tested in different plant species
to unravel the evolutionary origin of this cross talk.
MYC2 suppresses ET-mediated responses through transcriptional suppression of the con-
served transcription factor ORA59, which represents the core component in ET-mediated immu-
nity in A. thaliana (202). In addition, MYC2 antagonizes the transcription factor EIN3, regulating
ORA59 expression through physical interaction (205). Interestingly, MYC2 was initially described
as a mediator of ABA responses (85). Thus, the negative effects of ABA on ET response observed in
A. thaliana can be explained by the EIN3 and ORA59 regulation by MYC2 (4). MYC2 interacts with
the ABA receptor PYL6, thereby modulating JA-ABA cross talk (2). However, PYL6 homologs
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seem to be restricted to the Brassicaceae (58), suggesting that this cross talk evolved only recently.
MYC2 function is suppressed by not only JAZs but also DELLAs through physical interaction
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(74). Therefore, MYC2-regulated processes are fully activated only when both JA and GA are
present (74). In A. thaliana, this JA-GA synergy mediates the production of sesquiterpenes involved
in plant-insect interactions (74, 76).


In the absence of GA, DELLAs interact with JAZs in A. thaliana (75). This mediates a GA-JA
antagonism as opposed to the GA-JA synergy described above (Figure 2d). DELLA degrada-
tion upon GA perception releases JAZs that in turn suppress JA-mediated responses, resulting
in attenuation of immunity against necrotrophic pathogens and promotion of immunity against
biotrophic and hemibiotrophic pathogens (122). Consequently, loss of DELLAs increases SA
accumulation and enhances immunity against biotrophic and hemibiotrophic pathogens (122).
The release of JAZ suppression by DELLAs increases resistance against herbivores (18) but re-
duces immunity against biotrophic and hemibiotrophic pathogens (38). The GA-JA antagonism
mediated by DELLA-JAZ interactions seems to be conserved in rice (39). As described above,
the domain in DELLAs required for the interaction with JAZs is absent in bryophytes (75, 180).
Thus, DELLA and JAZ interaction likely evolved after the divergence of bryophytes in the plant
lineage. Furthermore, GA promotes but JA suppresses plant growth in many angiosperms, includ-
ing maize, rice, wheat, N. attenuata, Hylobius abietis, sun flower, and others (33, 6668, 72, 104,
112, 143, 192). Therefore, GA-JA antagonism likely represents an evolutionarily conserved hub
in the hormone network that controls defense and growth, at least in angiosperms. Consistently,
in N. attenuata, GA application antagonizes growth retardation caused by JA overaccumulation
(68). Genomes of rice, tomato, and barley only encode a single gene for the DELLA protein (104),
simplifying the application of genetic analysis to understand the significance and conservation of
GA-JA cross talk in defense and growth.

Auxin suppression often increases resistance against biotrophic and hemibiotrophic pathogens.
In A. thaliana, bacterial flagellin perception leads to suppression of auxin signaling through
reduction of the auxin receptor transcript TIR1, which is mediated by the microRNA miR393
(123). miR393 is induced in response to flagellin, and its overexpression results in increased
resistance (123). Interestingly, the mature A. thaliana miR393 sequence perfectly matches some
miRNAs in other angiosperms such as rice, Lotus japonicus, and M. truncatula (123), and such
miRNAs have been detected widely in RNAseq data from a wide range of vascular plants (117). In Evolution of Hormone Signaling Networks in Plant Defense 18.11

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addition, complementary sites of miR393 targets are conserved in monocots (163). Consistently,
in cassava and rice, miR393-mediated suppression of TIR genes leads to pathogen resistance (136,
208), pointing to a conserved role in immunity-mediated suppression of auxin signaling through
miR393, at least in angiosperms.

Gretchen Hagen 3 Family

Members of the Gretchen Hagen 3 (GH3) family of acyl acid amido synthetases modulate immu-
nity and growth through changing the balance of active hormones (127). They conjugate amino
acid residues to several phytohormones (157). For instance, A. thaliana JAR1 (GH3.11) conjugates
isoleucine to jasmonic acid (151). In A. thaliana, WES1 (GH3.5) inactivates auxin by conjugating
it to aspartic acid (186). Interestingly, WES1 also converts SA to SA-Asp (186), which weakens SA
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activity (24). Consequently, WES1 overexpression results in contrasting phenotypes for resistance
against P. syringae (132, 206), probably due to its action on both SA and auxin. Overexpression of
Annu. Rev. Phytopathol. 2017.55. Downloaded from

rice GH3.8 decreases free IAA levels by converting it to IAA-Asp and increases resistance against
Xanthomonas oryzae (43). Mutants deficient in AvrPphB susceptible 3 (PBS3, also GH3.12) show
reduced SA accumulation and resistance against P. syringae in A. thaliana (35). However, the mode
of action of PBS3 remains unknown, as it does not directly act on SA for amino acid conjugation
(126). Interestingly, expression of WES1 is influenced by auxin, SA, ABA, and abiotic and biotic
stress (132). Expression of other GH3 genes is also influenced by pathogen infection and hor-
mone treatment in many angiosperms (43, 51, 91, 94, 130, 132, 195, 204). In pea, SA treatment
increases IAA-Asp accumulation (130), suggesting that SA lowers active free auxin levels via the
GH3 activity to increase resistance. Genes encoding GH3 family members are present in land
plants (127, 167). In P. patens, two GH3 proteins have been shown to conjugate amino acids to
IAA (106). Thus, GH3 family members are conserved hubs for hormone networks that modulate
various phytohormone levels in immunity and growth.


Colonization of land by plants represents one of the most important steps in evolutionary history.
Land colonization likely required an enhanced ability to respond to the more variable terrestrial
environments, including the presence of pathogens (31, 34). Hormone cross talk is an effective way
to integrate multiple stimuli to coordinate sophisticated physiological responses. In the section
below, we discuss fitness advantages of hormone cross talk in harsh terrestrial environments.

Hormone Cross Talk in Combined Stress

The existence and conservation of hormone cross talk are assumed to bring fitness advantages
to plants simultaneously exposed to multiple stresses (134, 178). Experiments in A. thaliana have
shown that when attacked by herbivores and pathogens of different lifestyles, plants indeed expe-
rience hormone cross talk, as measured by changes in hormone-regulated gene expression (178).
The absence of any observed fitness reduction (i.e., growth alterations) under these conditions can
be interpreted as a consequence of hormone cross talk, allowing plants to activate specific rather
than general defense responses, thus conserving resources that can be used for growth (178).
In the particular case of abiotic stress, ABA lowers plant immunity through cross talk with
immune-related hormonal pathways (138, 172, 196). Such cross talk likely evolved to modulate
the activation of immune responses during adverse abiotic conditions encountered by plants upon

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land colonization. For example, conditions of drought are likely to signal a lower probability of
pathogen attack, as increased humidity is necessary for sporulation and spore germination in most
biotrophic and necrotrophic fungi and oomycetes and is essential for bacterial survival and spread
(190). Thus, the mostly negative cross talk of ABA on SA- and JA-regulated defense responses is
likely a response to lower defense activation when a pathogen attack is not imminent. In addition,
because activated immunity lowers abiotic stress responses, negative ABA effects on JA and SA
signaling can enhance abiotic stress responses, which may be necessary to increase survival of
certain plant species in severe abiotic stress conditions (118, 196).

Hormone Cross Talk in Plant Growth and Defense Trade-Offs

Plant diseases caused by pathogens influence plant metabolism and physiology, often resulting in
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plant growth defects (159). Mutants expressing constitutive resistance often display dwarf pheno-
types as well as elevated levels of defense hormones and pathogen-related gene expression. Some
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develop areas of spontaneous cell death and are known as lesion-mimic mutants (177). Naturally
occurring and chemically induced lesion mimic mutants have been identified in a variety of plants,
including A. thaliana, rice, barley, maize, and wheat, with many of them also displaying reduced
vegetative growth (15). For example, loss-of-function mutations in constitutive pathogenesis-related 5
(CPR5) result in dwarf plants displaying spontaneous cell death, accompanied by increased levels of
SA and resistance to biotrophic pathogens (62). Genes encoding CPR5 proteins have been found
in the genomes of plants as early in the plant lineage as P. patens (62), suggesting conservation of
regulatory mechanisms for defense and growth trade-offs in bryophytes.
Hormone cross talk participates in defense and growth trade-offs. In rice and A. thaliana,
upregulation of GA signaling by mutation in phytochrome B (PHYB) impairs JA, leading to
increased plant growth and herbivore susceptibility (18). In contrast, constitutively activating JA
responses increases defense against herbivores but reduces plant growth through repression of
GA signaling (18).
Trade-offs between growth and defense also occur at the level of brassinazole-resistant 1 (BZR1)
(105), a transcription factor mediating BR-induced transcription. BZR1 interacts with the bHLH
factor HBI1, which not only regulates growth-associated processes but also functions as a negative
regulator of immunity, pointing to a role for this factor as a switch between BR-mediated growth
and immunity (50). Growth and defense trade-offs mediated by hormone cross talk also enable
precise defense activation and regulation in certain tissues or at certain developmental stages. For
example, barley Mlo mutants show increased callose deposition and cell death phenotypes in older
plants, which are absent in young seedlings (188).
Auxin and CKs are two classic growth hormones, acting mostly antagonistically to each other.
During plant immunity, auxin functions mostly by increasing susceptibility to pathogens, whereas
high levels of CKs have the opposite effect and enhance pathogen resistance. A function for these
two hormones in growth changes during defense activation has not been demonstrated, but given
their role in plant growth, their participation is probable (1).
A potential role for hormone cross talk linking defense activation and growth suppression is
control of plant speciation. During hybrid necrosis, the F1 progeny derived from a cross between
certain incompatible species/genotypes display severely stunted growth accompanied by high
levels of SA-mediated immunity. A similar phenotype is also seen during hybrid breakdown,
which is commonly expressed in the F2 progeny. Such phenotypes are predicted by the Bateson-
Dobzhansky-Muller model of incompatibility (47, 119) and are believed to operate as a mechanism
of postzygotic incompatibility that contributes to the maintenance of gene barriers among species
(12). Evolution of Hormone Signaling Networks in Plant Defense 18.13

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PY55CH18-Tsuda ARI 15 June 2017 8:49


The increased knowledge acquired in the past few decades about hormone signaling and cross talk
has allowed scientists to envision the possibility of engineering hormone cross talk to maximize
plant fitness and crop production under a variety of environmental conditions, including pathogen
attack. However, we lack the knowledge of what state of hormone cross talk in a plant is desired in
a certain environmental condition. In addition, the high level of underlying complexity observed
in hormone cross talk during plant immunity makes engineering hormone cross talk an especially
daunting task. In the section below, we discuss the challenges and opportunities for engineering
hormone cross talk in plants.

Challenges in Hormone Cross Talk Engineering

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The complexity of cross talk among different hormone pathways that is beneficial for plant re-
sponses in changing environments greatly complicates any efforts to manipulate cross talk. Fur-
Annu. Rev. Phytopathol. 2017.55. Downloaded from

thermore, much of what has been learned about hormone networks has resulted from studies of
one single stress or from studies on the hormone cross talk between a few plant hormones. How-
ever, under field conditions, plants are exposed to numerous stresses at the same time. At least
at the level of transcription, the response of plants to multiple stresses cannot be predicted from
the responses to individual stresses (8, 142). Recent advances have exploited naturally occurring
genetic diversity to address tolerance to concomitant biotic and abiotic stress using quantitative
trait locus (QTL) approaches (87, 128). Not surprisingly, genetic variation for simultaneous stress
is more limited compared to resistance to single stresses (87), underscoring the challenges of si-
multaneous stress studies. Therefore, an improved understanding of hormone networks and cross
talk will be essential to any efforts of hormone cross talk engineering for enhanced environmental
stress tolerance in natural or managed ecosystems.

Opportunities in Hormone Cross Talk Engineering

Efforts to engineer hormone cross talk in plants rely on the existence of genetic diversity in
hormone relationships. In A. thaliana, genetic diversity has been demonstrated for responses to
SA or JA alone (88, 141, 176), whereas the cross talk between these two hormones appears to be
mostly conserved in different accessions (90). Activation of the SA-dependent pathway leading
to ETI by recognition of avirulent strains of P. syringae pv. tomato DC3000 has been shown to
have little effect on the SA-JA cross talk, with no negative effect on the JA pathway (156). This
surprising finding indicates a mechanism by which plants can counteract the activation of the
negative SA-JA cross talk, likely to avoid enhanced susceptibility to necrotrophs (156).
Other sources of diversity in hormone cross talk come from studying hormone networks in
different plant species. Tomato plants of the cultivar Rio Grande require both SA and JA for
Pto-based resistance against P. syringae pv. tomato T1 expressing AvrPto (49). However, tomato
plants from the variety MicroTom, which does not contain the Pto gene, display enhanced
resistance when the JA pathway is suppressed by mutations in the JA receptor COI1 (207). Thus,
two genetic backgrounds in the same plant species may present different hormone signaling
requirements for resistance.
Further studies on inter- and intraspecies genetic variation of hormone networks may provide
insights into possible points of manipulation for cross talk engineering using genome-editing
technologies. Similarly, adapted pathogens have evolved effector proteins to manipulate plant
physiology, including hormone signaling networks. Several effectors have been identified that
function to increase or decrease the activity of hormone signaling (84, 108, 151). Such strategies

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PY55CH18-Tsuda ARI 15 June 2017 8:49

can be copied in plant cells using the tools of synthetic biology to achieve desired outcomes in
hormone cross talk.
Possible hubs for hormone cross talk engineering have been recently identified (Figure 2).
A phosphomimic version of NPR1 mutated in conserved amino acids known to be targets of
phosphorylation is less prone to ABA-mediated degradation (45), therefore providing a strategy
to repress the negative effect of ABA on SA signaling. In rice, phosphorylation of the SA signal-
ing regulator OsWRKY45 by OsMAPK6 is essential for activation of SA-dependent responses.
Dephosphorylation of OsMAPK6 by ABA-regulated Tyr-specific phosphatases (OsPTP1/2) pre-
vents OsWRKY45 activation by OsMAPK6, and knockouts of OsPTP1/2 allow for activation of
simultaneous abiotic and biotic stress (172). In A. thaliana, the Mediator subunit MED25 reg-
ulates hormone signaling by direct interaction with MYC2, ABI5, and EIN3, which constitute
key regulators in JA, ABA, and ET signaling, respectively (22, 194). Thus, it may be possible
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to manipulate the affinity of interaction between MED25 and other proteins to allow simulta-
neous responses to both biotic and abiotic stress. Finally, an A. thaliana quintuple mutant of the
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JAZ proteins ( jazQ) displays constitutive activation of JA-mediated defense against herbivores but
also displays growth trade-offs characterized by decreased root and shoot biomass (18). A mutant
screen in the jazQ background for plants with increased biomass identified phyB as a mediator
of growth trade-offs. A mutation in PHYB restores the growth of jazQ plants, without affecting
the increased resistance phenotype. The decreased growth phenotype of jazQ plants is also sup-
pressed by overexpression of phytochrome interaction factor 4 (PIF4) encoding a transcription factor
in GA signaling. Furthermore, jazQ phyB displays transcriptional activation of several PIF targets,
suggesting that the restored growth in jazQ phyB plants is mediated by activation of GA signaling
through the derepression of PIF transcription factors, which are repressed in defense-activated
genotypes. Although defense and growth trade-offs may be important to increase plant survival
under multiple stress conditions, this work illustrates that growth and defense can be genetically
unlinked, paving the way for the generation of plants with increased resistance without negative
fitness costs in certain environmental conditions.

Studies with model plant species such as A. thaliana have significantly contributed to dissection of
the mechanisms of hormone cross talk. Comparative genomics based on the knowledge obtained
from model plant species reveals that the core signaling components, including hubs of phyto-
hormone signaling networks, are highly conserved in land plants. Although further functional
characterization and validation are required, the conservation of core phytohormone signaling
components in land plants suggests that phytohormone-mediated signal processing is crucial for
plant adaptation to changing terrestrial environments. Indeed, the model species-based research
has demonstrated that interactions between defense and growth, as well as abiotic and biotic stress,
are often mediated by hormone cross talk (32, 138, 196). The evolution of phytohormone signal-
ing networks is a recurring theme, as specific plant lineages appear to have specialized networking
of phytohormone signaling pathways (115).
A goal of plant defense research is to translate basic knowledge gained from model species to
crops. This will be facilitated by a further mechanistic understanding of conservation and diversifi-
cation of phytohormone signaling networks, especially in species representative of plant evolution.
Notably, in A. thaliana, growth defense trade-offs can be genetically uncoupled (18), illustrating
the great opportunity to improve plant fitness and crop production through engineering hormone
cross talk. With the power of fast-developing genome-editing technologies, we may be able to
overcome evolutionary constraints on plant defense and growth. Evolution of Hormone Signaling Networks in Plant Defense 18.15

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PY55CH18-Tsuda ARI 15 June 2017 8:49

The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.

Work in the lab of K.T. is supported by the Max Planck Society and Deutsche Forschungsgemein-
schaft (DFG). Work in the Argueso lab is supported by funds from Colorado State University
and the United States Department of Agriculture. The authors thank Tsuda laboratory members
for insightful discussions and Jane Glazebrook and Fumiaki Katagiri for critical review of the
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