2017.evolution of Hormone Signaling Networks in Plant Defense

PY55CH18-Tsuda ARI 15 June 2017 8:49
Review in Advance first posted online

V I E W
E on June 23, 2017. (Changes may
R
still occur before final publication
S
online and in print.)
C E
I N
A
D V A
Evolution of Hormone
Signaling Networks in
Plant Defense
Access provided by El Colegio de la Frontera Sur (ECOSUR) on 07/18/17. For personal use only.
Matthias L. Berens,1 Hannah M. Berry,2 Akira Mine,1

Annu. Rev. Phytopathol. 2017.55. Downloaded from www.annualreviews.org
Cristiana T. Argueso,2 and Kenichi Tsuda1

1
Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research,
50829 Cologne, Germany; email: tsuda@mpipz.mpg.de
2
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
phyto.annualreviews.org
https://doi.org/10.1146/annurev-phyto-080516- Abstract
035544
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.
18.1
Changes may still occur before final publication online and in print
INTRODUCTION
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
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).
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).
Antagonism:
A B A B A B A B
Response
Response
prioritization Xa Xb Xa Xb Xa Xb Xa Xb
Synergism:
A B A B A B A B
Response
Response
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.
18.2 Berens et al.
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
improve crop production.

CONSERVED ROLES OF PHYTOHORMONES IN PLANT DEFENSE

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
www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.3
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
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
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
18.4 Berens et al.
ancient role of JA/OPDA signaling. This may be answered by extensive comparative analysis in
bryophytes.
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
is required to understand the emergence of JA roles in triggering defense.

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
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
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
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).
18.6 Berens et al.
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,
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).
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
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
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
(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).
CONSERVED HUBS IN HORMONE SIGNALING NETWORKS

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.
18.8 Berens et al.
in)
3.X
ma
9
GH
g
do
A5
lin
S1
LA
g,
R
na
,O
, IC
lin
EL
sig
l. D
N3
na
s
AL
re
inc
sig
s
I
93
,E
-A
,P
co
A(
2
iR3
AC
xin
R1
YC
A
LL
Z
NP
AB
SN
m
au
JA
DE
M
Medicago truncatula
a Fabidae
Glycine max
Arabidopsis thaliana
Arabidopsis lyrata
Brassicaceae Capsella rubella
Eutrema salsugineum
Carica papaya
Gossypium raimondii
Citrus
Rosid Citrus sinensis
Malvidae
Pentapetalae Linum usitatissimum
Eucalyptus grandis
Eudicot
Vitis vinifera
Kalanchoe laxiflora
Solanum tuberosum
Solanum lycopersicum
Angiosperm Aquilegia coerulea
Zea mays
Grass
Oryza sativa
Tracheophyte
Brachypodium distachyon
Embryophyte Amborella trichopoda
Lycophytes
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
ICS1 ICS1 IAA

ABA SA TIR1
PALs TIR1 miR393
PALs
TIR
SCF
SA NPR1 Immunity AUX/IAA
Stomatal
closure ARFs IAA response Immunity
d GA JA-Ile e ABA JA-Ile ANACs

JA-Ile
GA JA-Ile ANACs
GID1 COI1 MYC2 MYC2
SLY1 JAZs
SCF COI1
SCF ORA59 SA
JA MYC2
DELLA JAZs response SA
DELLA Immunity
ORA59
GA PIFs JA MYC2
response MYCs JA/ET
response GA EIN3
(and others) response
Activation Inhibition Protein degradation Transcription
NPR1
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
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
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
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
18.10 Berens et al.
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
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
(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).
JAZ and DELLA

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.
miR393
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
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
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
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.
EVOLUTIONARY ADVANTAGES OF DEFENSE HORMONE

CROSS TALK
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
18.12 Berens et al.
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
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
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).
ENGINEERING HORMONE CROSS TALK

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

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-
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
18.14 Berens et al.
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
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
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.
CONCLUDING REMARKS
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.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
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
manuscript.
LITERATURE CITED
1. Albrecht T, Argueso CT. 2016. Should I fight or should I grow now? The role of cytokinins in plant
growth and immunity and in the growthdefence trade-off. Ann. Bot. 119(5):72535
2. Aleman F, Yazaki J, Lee M, Takahashi Y, Kim AY, et al. 2016. An ABA-increased interaction of the
PYL6 ABA receptor with MYC2 transcription factor: a putative link of ABA and JA signaling. Sci. Rep.
6:28941
3. Alvarez A, Montesano M, Schmelz E, de Leon IP. 2016. Activation of shikimate, phenylpropanoid,
oxylipins, and auxin pathways in Pectobacterium carotovorum elicitors-treated moss. Front. Plant Sci. 7:328
4. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, et al. 2004. Antagonistic interac-
tion between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression
and disease resistance in Arabidopsis. Plant Cell 16:346079
5. Andersson RA, Akita M, Pirhonen M, Gammelgard E, Valkonen JPT. 2005. Moss-Erwinia pathosystem
reveals possible similarities in pathogenesis and pathogen defense in vascular and nonvascular plants.
J. Gen. Plant Pathol. 71:2328
6. Argueso CT, Ferreira FJ, Epple P, To JPC, Hutchison CE, et al. 2012. Two-component elements
mediate interactions between cytokinin and salicylic acid in plant immunity. PLOS Genet. 8:e1002448
7. Assante G, Merlini L, Nasini G. 1977. (+)-Abscisic acid, a metabolite of the fungus Cercospora rosicola.
Experientia 33:155657
8. Atkinson NJ, Lilley CJ, Urwin PE. 2013. Identification of genes involved in the response of Arabidopsis
to simultaneous biotic and abiotic stresses. Plant Physiol. 162:202841
9. Audenaert K, De Meyer GB, Hofte MM. 2002. Abscisic acid determines basal susceptibility of tomato to
Botrytis cinerea and suppresses salicylic aciddependent signaling mechanisms. Plant Physiol. 128:491501
10. Beckman KB, Ingram DS. 1994. The inhibition of the hypersensitive response of potato-tuber tissues
by cytokinins: similarities between senescence and plant defense responses. Physiol. Mol. Plant Pathol.
44:3350
11. Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns
and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379406
12. Bomblies K, Weigel D. 2007. Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant
species. Nat. Rev. Genet. 8:38293
13. Boter M, Ruiz-Rivero O, Abdeen A, Prat S. 2004. Conserved MYC transcription factors play a key role
in jasmonate signaling both in tomato and Arabidopsis. Gene Dev. 18:157791
14. Bressendorff S, Azevedo R, Kenchappa CS, Ponce de Leon I, Olsen JV, et al. 2016. An innate immunity
pathway in the moss Physcomitrella patens. Plant Cell 28:132842
15. Bruggeman Q, Raynaud C, Benhamed M, Delarue M. 2015. To die or not to die? Lessons from lesion
mimic mutants. Front. Plant Sci. 6:24
16. Burra DD, Muhlenbock P, Andreasson E. 2015. Salicylic and jasmonic acid pathways are necessary for
defence against Dickeya solani as revealed by a novel method for Blackleg disease screening of in vitro
grown potato. Plant Biol. 17:103038
18.16 Berens et al.
17. Cai Q, Yuan Z, Chen MJ, Yin CS, Luo ZJ, et al. 2014. Jasmonic acid regulates spikelet development in
rice. Nat. Commun. 5:3476
18. Campos ML, Yoshida Y, Major IT, de Oliveira Ferreira D, Weraduwage SM, et al. 2016. Rewiring
of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat. Commun.
7:12570
19. Catinot J, Buchala A, Abou-Mansour E, Metraux JP. 2008. Salicylic acid production in response to biotic
and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Lett. 582:47378
20. Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, et al. 2011. Regulatory mechanism
controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr. Biol.
21:102529
21. Chen HM, Xue L, Chintamanani S, Germain H, Lin HQ, et al. 2009. ETHYLENE INSEN-
SITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 Repress SALICYLIC ACID INDUCTION
DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21:2527
40
22. Chen R, Jiang HL, Li L, Zhai QZ, Qi LL, et al. 2012. The Arabidopsis mediator subunit MED25
differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and
ABI5 transcription factors. Plant Cell 24:2898916

23. Chen X, Steed A, Travella S, Keller B, Nicholson P. 2009. Fusarium graminearum exploits ethylene
signalling to colonize dicotyledonous and monocotyledonous plants. New Phytol. 182:97583
24. Chen Y, Shen H, Wang MY, Li Q, He ZH. 2013. Salicyloyl-aspartate synthesized by the acetyl-amido
synthetase GH3.5 is a potential activator of plant immunity in Arabidopsis. Acta Biochim. Biophys. Sin.
45:82736
25. Cheon J, Fujioka S, Dilkes BP, Choe S. 2013. Brassinosteroids regulate plant growth through distinct
signaling pathways in Selaginella and Arabidopsis. PLOS ONE 8:e81938
26. Choi J, Huh SU, Kojima M, Sakakibara H, Paek KH, Hwang I. 2010. The cytokinin-activated tran-
scription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in
Arabidopsis. Dev. Cell 19:28495
27. Chono M, Honda I, Zeniya H, Yoneyama K, Saisho D, et al. 2003. A semidwarf phenotype of barley
uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant
Physiol. 133:120919
28. Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, et al. 2013. Herbivore exploits orally secreted
bacteria to suppress plant defenses. PNAS 110:1572833
29. Cook DE, Mesarich CH, Thomma BPHJ. 2015. Understanding plant immunity as a surveillance system
to detect invasion. Annu. Rev. Phytopathol. 53:54163
30. Cui HT, Tsuda K, Parker JE. 2015. Effector-triggered immunity: from pathogen perception to robust
defense. Annu. Rev. Plant Biol. 66:487511
31. Cuming AC, Stevenson SR. 2015. From pond slime to rain forest: the evolution of ABA signalling and
the acquisition of dehydration tolerance. New Phytol. 206:57
32. De Bruyne L, Hofte M, De Vleesschauwer D. 2014. Connecting growth and defense: the emerging roles
of brassinosteroids and gibberellins in plant innate immunity. Mol. Plant 7:94359
33. Delaguardia M, Benlloch M. 1980. Effects of potassium and gibberellic acid on stem growth of whole
sunflower plants. Physiol. Plant. 49:44348
34. de Leon IP, Montesano M. 2013. Activation of defense mechanisms against pathogens in mosses and
flowering plants. Int. J. Mol. Sci. 14:3178200
35. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF. 2011. Salicylic acid biosynthesis and metabolism.
Arabidopsis Book 9:e0156
36. Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, et al. 2008. Activation of defense response
pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol. Plant 1:42345
37. Depuydt S, Hardtke CS. 2011. Hormone signalling crosstalk in plant growth regulation. Curr. Biol.
21:R36573
38. de Torres Zabala M, Zhai B, Jayaraman S, Eleftheriadou G, Winsbury R, et al. 2016. Novel JAZ co-
operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae
infection. New Phytol. 209:112034
39. De Vleesschauwer D, Seifi HS, Filipe O, Haeck A, Huu SN, et al. 2016. The DELLA protein SLR1
integrates and amplifies salicylic acid and jasmonic aciddependent innate immunity in rice. Plant Physiol.
170:183147
40. De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, et al. 2012. Brassinosteroids
antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol. 158:183346
41. De Vleesschauwer D, Yang Y, Cruz CV, Hofte M. 2010. Abscisic acidinduced resistance against the
brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene
signaling. Plant Physiol. 152:203652
42. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT. 2009. Different lepidopteran elicitors account for
cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150:157686
43. Ding X, Cao Y, Huang L, Zhao J, Xu C, et al. 2008. Activation of the indole-3-acetic acid-amido
synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent
basal immunity in rice. Plant Cell 20:22840
44. Ding Y, Wei W, Wu W, Davis RE, Jiang Y, et al. 2013. Role of gibberellic acid in tomato defence against
potato purple top phytoplasma infection. Ann. Appl. Biol. 162:19199
45. Ding YZ, Dommel M, Mou ZL. 2016. Abscisic acid promotes proteasome-mediated degradation of the
transcription coactivator NPR1 in Arabidopsis thaliana. Plant J. 86:2034

46. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, et al. 2011. Metabolic priming by a secreted fungal
effector. Nature 478:39598
47. Dobzhansky T. 1937. Genetics and the Origin of Species. New York: Columbia Univ. Press
48. Du MM, Zhai QZ, Deng L, Li SY, Li HS, et al. 2014. Closely related NAC transcription factors of tomato
differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell 26:316784
49. Ekengren SK, Liu YL, Schiff M, Dinesh-Kumar SP, Martin GB. 2003. Two MAPK cascades, NPR1, and
TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J. 36:90517
50. Fan M, Bai MY, Kim JG, Wang TN, Oh E, et al. 2014. The bHLH transcription factor HBI1 mediates the
trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis.
Plant Cell 26:82841
51. Feng SG, Yue RQ, Tao S, Yang YJ, Zhang L, et al. 2015. Genome-wide identification, expression analysis
of auxin-responsive GH3 family genes in maize (Zea mays L.) under abiotic stresses. J. Integr. Plant Biol.
57:78395
52. Fu J, Liu HB, Li Y, Yu HH, Li XH, et al. 2011. Manipulating broad-spectrum disease resistance by
suppressing pathogen-induced auxin accumulation in rice. Plant Physiol. 155:589602
53. Fu J, Wang SP. 2011. Insights into auxin signaling in plant-pathogen interactions. Front. Plant Sci. 2:74
54. Fu ZQ, Yan SP, Saleh A, Wang W, Ruble J, et al. 2012. NPR3 and NPR4 are receptors for the immune
signal salicylic acid in plants. Nature 486:22832
55. Gaige AR, Ayella A, Shuai B. 2010. Methyl jasmonate and ethylene induce partial resistance in Medicago
truncatula against the charcoal rot pathogen Macrophomina phaseolina. Physiol. Mol. Plant Pathol. 74:41218
56. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.
Annu. Rev. Phytopathol. 43:20527
57. Gong T, Shu D, Zhao M, Zhong J, Deng HY, Tan H. 2014. Isolation of genes related to abscisic acid
production in Botrytis cinerea TB-3-H8 by cDNA-AFLP. J. Basic Microb. 54:20414
58. Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, et al. 2012. Phytozome: a comparative
platform for green plant genomics. Nucleic Acids Res. 40:D117886
59. Grellet-Bournonville CF, Martinez-Zamora MG, Castagnaro AP, Daz-Ricci JC. 2012. Temporal accu-
mulation of salicylic acid activates the defense response against Colletotrichum in strawberry. Plant Physiol.
Biochem. 54:1016
60. Gross J, Cho WK, Lezhneva L, Falk J, Krupinska K, et al. 2006. A plant locus essential for phylloquinone
(vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J. Biol. Chem. 281:1718996
61. Grosskinsky DK, Naseem M, Abdelmohsen UR, Plickert N, Engelke T, et al. 2011. Cytokinins mediate
resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis
independent of salicylic acid signaling. Plant Physiol. 157:81530
62. Gu YN, Zebell SG, Liang ZZ, Wang S, Kang BH, Dong XN. 2016. Nuclear pore permeabilization is a
convergent signaling event in effector-triggered immunity. Cell 166:152638
18.18 Berens et al.
63. Haberlach GT, Budde AD, Sequeira L, Helgeson JP. 1978. Modification of disease resistance of tobacco
callus tissues by cytokinins. Plant Physiol. 62:52225
64. Halim VA, Eschen-Lippold L, Altmann S, Birschwilks M, Scheel D, Rosahl S. 2007. Salicylic acid
is important for basal defense of Solanum tuberosum against Phytophthora infestans. Mol. Plant-Microbe
Interact. 20:134652
65. Hayashi K, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S, et al. 2010. Endogenous diterpenes derived
from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss
Physcomitrella patens. Plant Physiol. 153:108597
66. Hedden P, Phillips AL. 2000. Gibberellin metabolism: new insights revealed by the genes. Trends Plant
Sci. 5:52330
67. Heijari J, Nerg AM, Kainulainen P, Viiri H, Vuorinen M, Holopainen JK. 2005. Application of methyl
jasmonate reduces growth but increases chemical defence and resistance against Hylobius abietis in Scots
pine seedlings. Entomol. Exp. Appl. 115:11724
68. Heinrich M, Hettenhausen C, Lange T, Wunsche H, Fang JJ, et al. 2013. High levels of jasmonic acid
antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems. Plant J.
73:591606
69. Helliwell EE, Wang Q, Yang YN. 2013. Transgenic rice with inducible ethylene production exhibits
broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani.
Plant Biotechnol. J. 11:3342
70. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, et al. 2007. The GID1-mediated gib-
berellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the
bryophyte Physcomitrella patens. Plant Cell 19:305879
71. Hoffman T, Schmidt JS, Zheng X, Bent AF. 1999. Isolation of ethylene-insensitive soybean mutants that
are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiol. 119:93550
72. Hoffmannbenning S, Kende H. 1992. On the role of abscisic acid and gibberellin in the regulation of
growth in rice. Plant Physiol. 99:115661
73. Hok S, Allasia V, Andrio E, Naessens E, Ribes E, et al. 2014. The receptor kinase IMPAIRED
OOMYCETE SUSCEPTIBILITY1 attenuates abscisic acid responses in Arabidopsis. Plant Physiol.
166:150618
74. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY. 2012. Arabidopsis MYC2 interacts with DELLA
proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:263548
75. Hou XL, Lee LYC, Xia KF, Yen YY, Yu H. 2010. DELLAs modulate jasmonate signaling via competitive
binding to JAZs. Dev. Cell 19:88494
76. Howe GA, Jander G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:4166
77. Huang JL, Gu M, Lai ZB, Fan BF, Shi K, et al. 2010. Functional analysis of the Arabidopsis PAL gene
family in plant growth, development, and response to environmental stress. Plant Physiol. 153:152638
78. Berlanger I, Powelson ML. 2000. Verticillium wilt. Plant Health Instr. https://doi.org/10.1094/
PHI-I-2000-0801-01
79. Ishikawa T, Okazaki K, Kuroda H, Itoh K, Mitsui T, Hori H. 2007. Molecular cloning of Brassica rapa
nitrilases and their expression during clubroot development. Mol. Plant Pathol. 8:62337
80. Jiang CJ, Shimono M, Sugano S, Kojima M, Liu XQ, et al. 2013. Cytokinins act synergistically with
salicylic acid to activate defense gene expression in rice. Mol. Plant-Microbe Interact. 26:28796
81. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:32329
82. Ju CL, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR, et al. 2015. Conservation of ethylene as a
plant hormone over 450 million years of evolution. Nat. Plants 1:14004
83. Kakei Y, Mochida K, Sakurai T, Yoshida T, Shinozaki K, Shimada Y. 2015. Transcriptome analysis of
hormone-induced gene expression in Brachypodium distachyon. Sci. Rep. 5:14476
84. Kazan K, Lyons R. 2014. Intervention of phytohormone pathways by pathogen effectors. Plant Cell
26:2285309
85. Kazan K, Manners JM. 2013. MYC2: the master in action. Mol. Plant 6:686703
86. Kim DS, Hwang BK. 2014. An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in
salicylic aciddependent signalling of the defence response to microbial pathogens. J. Exp. Bot. 65:2295
306
87. Kissoudis C, Sri S, van de Wiel C, Visser RGF, van der Linden CG, Bai YL. 2016. Responses to combined
abiotic and biotic stress in tomato are governed by stress intensity and resistance mechanism. J. Exp. Bot.
67:511932
88. Kliebenstein DJ, Figuth A, Mitchell-Olds T. 2002. Genetic architecture of plastic methyl jasmonate
responses in Arabidopsis thaliana. Genetics 161:168596
89. Koga H, Dohi K, Mori M. 2004. Abscisic acid and low temperatures suppress the whole plant-specific
resistance reaction of rice plants to the infection of Magnaporthe grisea. Physiol. Mol. Plant Pathol. 65:39
90. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, et al. 2008. Kinetics of salicylate-
mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147:1358
68
91. Kumar R, Agarwal P, Tyagi AK, Sharma AK. 2012. Genome-wide investigation and expression analysis
suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli
in tomato (Solanum lycopersicum). Mol. Genet. Genom. 287:22135
92. Kusajima M, Yasuda M, Kawashima A, Nojiri H, Yamane H, et al. 2010. Suppressive effect of abscisic
acid on systemic acquired resistance in tobacco plants. J. Gen. Plant Pathol. 76:16167
93. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, et al. 2010. Interfamily transfer of
a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365
69
94. Lahey KA, Yuan RC, Burns JK, Ueng PP, Timmer LW, Chung KR. 2004. Induction of phytohormones
and differential gene expression in citrus flowers infected by the fungus Colletotrichum acutatum. Mol.
Plant-Microbe Interact. 17:1394401
95. Lavy M, Prigge MJ, Tao S, Shain S, Kuo A, et al. 2016. Constitutive auxin response in Physcomitrella
reveals complex interactions between Aux/IAA and ARF proteins. eLife 5:e13325
96. Li J, Besseau S, Toronen P, Sipari N, Kollist H, et al. 2013. Defense-related transcription factors
WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis.
New Phytol. 200:45772
97. Li J, Brader G, Palva ET. 2004. The WRKY70 transcription factor: a node of convergence for jasmonate-
mediated and salicylate-mediated signals in plant defense. Plant Cell 16:31931
98. Li YZ, Zhang L, Lu WJ, Wang XL, Wu CA, Guo XQ. 2014. Overexpression of cotton GhMKK4
enhances disease susceptibility and affects abscisic acid, gibberellin and hydrogen peroxide signalling in
transgenic Nicotiana benthamiana. Mol. Plant Pathol. 15:94108
99. Lind C, Dreyer I, Lopez-Sanjurjo EJ, von Meyer K, Ishizaki K, et al. 2015. Stomatal guard cells co-opted
an ancient ABA-dependent desiccation survival system to regulate stomatal closure. Curr. Biol. 25:92835
100. Liu J, Zhang TR, Jia JZ, Sun JQ. 2016. The wheat mediator subunit TaMED25 interacts with the
transcription factor TaEIL1 to negatively regulate disease resistance against powdery mildew. Plant
Physiol. 170:1799816
101. Liu TL, Song TQ, Zhang X, Yuan HB, Su LM, et al. 2014. Unconventionally secreted effectors of two
filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 5:4686
102. Liu YD, Zhang SQ. 2004. Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by
MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis.
Plant Cell 16:338699
103. Liu ZJ, Bushnell WR. 1986. Effects of cytokinins on fungus development and host response in powdery
mildew of barley. Physiol. Mol. Plant Pathol. 29:4152
104. Livne S, Lor VS, Nir I, Eliaz N, Aharoni A, et al. 2015. Uncovering DELLA-independent gibberellin
responses by characterizing new tomato procera mutants. Plant Cell 27:157994
105. Lozano-Duran R, Macho AP, Boutrot F, Segonzac C, Somssich IE, Zipfel C. 2013. The transcriptional
regulator BZR1 mediates trade-off between plant innate immunity and growth. eLife 2:e00983
106. Ludwig-Muller J, Julke S, Bierfreund NM, Decker EL, Reski R. 2009. Moss (Physcomitrella patens) GH3
proteins act in auxin homeostasis. New Phytol. 181:32338
107. Lund ST, Stall RE, Klee HJ. 1998. Ethylene regulates the susceptible response to pathogen infection in
tomato. Plant Cell 10:37182
108. Ma KW, Ma WB. 2016. Phytohormone pathways as targets of pathogens to facilitate infection. Plant
Mol. Biol. 91:71325
18.20 Berens et al.
109. Ma X, Xu G, He P, Shan L. 2016. SERKing coreceptors for receptors. Trends Plant Sci. 21:101733
110. Makandar R, Nalam VJ, Lee H, Trick HN, Dong YH, Shah J. 2012. Salicylic acid regulates basal
resistance to Fusarium head blight in wheat. Mol. Plant-Microbe Interact. 25:43149
111. McAdam SAM, Brodribb TJ, Banks JA, Hedrich R, Atallah NM, et al. 2016. Abscisic acid controlled sex
before transpiration in vascular plants. PNAS 113:1286267
112. McCune DC, Galston AW. 1959. Inverse effects of gibberellin on peroxidase activity and growth in
dwarf strains of peas and corn. Plant Physiol. 34:41618
113. Melotto M, Underwood W, He SY. 2008. Role of stomata in plant innate immunity and foliar bacterial
diseases. Annu. Rev. Phytopathol. 46:10122
114. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 2006. Plant stomata function in innate
immunity against bacterial invasion. Cell 126:96980
115. Mine A, Nobori T, Salazar-Rondon MC, Winkelmuller TM, Anver S, et al. 2017. An incoherent feed-
forward loop mediates robustness and tunability in a plant immune network. EMBO Rep. 18(3):46476
116. Mittag J, Sola I, Rusak G, Ludwig-Muller J. 2015. Physcomitrella patens auxin conjugate synthetase (GH3)
double knockout mutants are more resistant to Pythium infection than wild type. J. Plant Physiol. 183:75
83
117. Montes RAC, Rosas-Cardenas FD, De Paoli E, Accerbi M, Rymarquis LA, et al. 2014. Sample sequencing
of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat. Commun.
5:3722
118. Mosher S, Moeder W, Nishimura N, Jikumaru Y, Joo SH, et al. 2010. The lesion-mimic mutant cpr22
shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic aciddependent
manner. Plant Physiol. 152:190113
119. Muller H. 1942. Isolating mechanisms, evolution, and temperature. Biol. Symp. 6:71124
120. Mutka AM, Fawley S, Tsao T, Kunkel BN. 2013. Auxin promotes susceptibility to Pseudomonas syringae
via a mechanism independent of suppression of salicylic acidmediated defenses. Plant J. 74:74654
121. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2012. NAC transcription
factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819:97103
122. Navarro L, Bari R, Achard P, Lison P, Nemri A, et al. 2008. DELLAs control plant immune responses
by modulating the balance and salicylic acid signaling. Curr. Biol. 18:65055
123. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, et al. 2006. A plant miRNA contributes to
antibacterial resistance by repressing auxin signaling. Science 312:43639
124. Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, et al. 2010. Genome-wide analysis
of NAC transcription factor family in rice. Gene 465:3044
125. ODonnell PJ, Schmelz E, Block A, Miersch O, Wasternack C, et al. 2003. Multiple hormones act
sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiol. 133:118189
126. Okrent RA, Brooks MD, Wildermuth MC. 2009. Arabidopsis GH3.12 (PBS3) conjugates amino acids to
4-substituted benzoates and is inhibited by salicylate. J. Biol. Chem. 284:974254
127. Okrent RA, Wildermuth MC. 2011. Evolutionary history of the GH3 family of acyl adenylases in rosids.
Plant Mol. Biol. 76:489505
128. Olivas N, Kruijer W, Gort G, Wijen CL, van Loon J, Dicke M. 2017. Genome-wide association analysis
reveals distinct genetic architectures for single and combined stress responses in Arabidopsis thaliana. New
Phytol. 213:83851
129. Olsen AN, Ernst HA, Lo Leggio L, Skriver K. 2005. NAC transcription factors: structurally distinct,
functionally diverse. Trends Plant Sci. 10:7987
130. Ostrowski M, Jakubowska A. 2013. GH3 expression and IAA-amide synthetase activity in pea (Pisum
sativum L.) seedlings are regulated by light, plant hormones and auxinic herbicides. J. Plant Physiol.
170:36168
131. Pallas JA, Paiva NL, Lamb C, Dixon RA. 1996. Tobacco plants epigenetically suppressed in phenylalanine
ammonialyase expression do not develop systemic acquired resistance in response to infection by tobacco
mosaic virus. Plant J. 10:28193
132. Park JE, Park JY, Kim YS, Staswick PE, Jeon J, et al. 2007. GH3-mediated auxin homeostasis links
growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282:1003646
133. Pascual MB, Canovas FM, Avila C. 2015. The NAC transcription factor family in maritime pine (Pinus
pinaster): molecular regulation of two genes involved in stress responses. BMC Plant Biol. 15:254
134. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC. 2009. Networking by small-molecule
hormones in plant immunity. Nat. Chem. Biol. 5:30816
135. Pinheiro GL, Marques CS, Costa MDBL, Reis PAB, Alves MS, et al. 2009. Complete inventory of
soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct
roles in stress response. Gene 444:1023
136. Pinweha N, Asvarak T, Viboonjun U, Narangajavana J. 2015. Involvement of miR160/miR393 and their
targets in cassava responses to anthracnose disease. J. Plant Physiol. 174:2635
137. Ponce De Leon I, Schmelz EA, Gaggero C, Castro A, Alvarez A, Montesano M. 2012. Physcomitrella
patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary
conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid,
upon Botrytis cinerea infection. Mol. Plant Pathol. 13:96074

138. Pye MF, Hakuno F, MacDonald JD, Bostock RM. 2013. Induced resistance in tomato by SAR activators
during predisposing salinity stress. Front. Plant Sci. 4:116
139. Qiu DY, Xiao J, Ding XH, Xiong M, Cai M, et al. 2007. OsWRKY13 mediates rice disease resistance
by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol. Plant-Microbe
Interact. 20:49299
140. Radhika V, Kost C, Bonaventure G, David A, Boland W. 2012. Volatile emission in bracken fern is
induced by jasmonates but not by Spodoptera littoralis or strongylogaster multifasciata herbivory. PLOS
ONE 7:e48050
141. Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR. 2000. Jasmonic acid signaling modulates ozone-
induced hypersensitive cell death. Plant Cell 12:163346
142. Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, et al. 2013. Transcriptome re-
sponses to combinations of stresses in Arabidopsis. Plant Physiol. 161:178394
143. Riemann M, Muller A, Korte A, Furuya M, Weiler EW, Nick P. 2003. Impaired induction of the
jasmonate pathway in the rice mutant hebiba. Plant Physiol. 133:182030
144. Robert-Seilaniantz A, Grant M, Jones JDG. 2011. Hormone crosstalk in plant disease and defense: more
than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49:31743
145. Ross JJ, Reid JB. 2010. Evolution of growth-promoting plant hormones. Funct. Plant Biol. 37:795805
146. Schmiesing A, Emonet A, Gouhier-Darimont C, Reymond P. 2016. Arabidopsis MYC transcription
factors are the target of hormonal salicylic acid/jasmonic acid cross talk in response to Pieris brassicae egg
extract. Plant Physiol. 170:243243
147. Seyfferth C, Tsuda K. 2014. Salicylic acid signal transduction: the initiation of biosynthesis, perception
and transcriptional reprogramming. Front. Plant Sci. 5:697
148. Sheikh AH, Raghuram B, Eschen-Lippold L, Scheel D, Lee J, Sinha AK. 2014. Agroinfiltration by
cytokinin-producing Agrobacterium sp. strain GV3101 primes defense responses in Nicotiana tabacum.
Mol. Plant-Microbe Interact. 27:117585
149. Shen XL, Liu HB, Yuan B, Li XH, Xu CG, Wang SP. 2011. OsEDR1 negatively regulates rice bacterial
resistance via activation of ethylene biosynthesis. Plant Cell Environ. 34:17991
150. Shibata Y, Kawakita K, Takemoto D. 2010. Age-related resistance of Nicotiana benthamiana against
hemibiotrophic pathogen Phytophthora infestans requires both ethylene- and salicylic acidmediated sig-
naling pathways. Mol. Plant-Microbe Interact. 23:113042
151. Shigenaga AM, Argueso CT. 2016. No hormone to rule them all: interactions of plant hormones during
the responses of plants to pathogens. Semin. Cell Dev. Biol. 56:17489
152. Shine MB, Yang JW, El-Habbak M, Nagyabhyru P, Fu DQ, et al. 2016. Cooperative functioning
between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid
biosynthesis in soybean. New Phytol. 212:62736
153. Shoji T, Hashimoto T. 2011. Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes
directly and by way of the NIC2-locus ERF genes. Plant Cell Physiol. 52:111730
154. Smith-Becker J, Marois E, Huguet EJ, Midland SL, Sims JJ, Keen NT. 1998. Accumulation of salicylic
acid and 4-hydroxybenzoic acid in phloem fluids of cucumber during systemic acquired resistance is
18.22 Berens et al.
preceded by a transient increase in phenylalanine ammonia-lyase activity in petioles and stems. Plant
Physiol. 116:23138
155. Spaepen S, Vanderleyden J. 2011. Auxin and plant-microbe interactions. Cold Spring Harb. Perspect. Biol.
3:a001438
156. Spoel SH, Johnson JS, Dong X. 2007. Regulation of tradeoffs between plant defenses against pathogens
with different lifestyles. PNAS 104:1884247
157. Staswick PE, Tiryaki I, Rowe ML. 2002. Jasmonate response locus JAR1 and several related Arabidopsis
genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and
indole-3-acetic acids in an assay for adenylation. Plant Cell 14:140515
158. Stintzi A, Browse J. 2000. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid
reductase required for jasmonate synthesis. PNAS 97:1062530
159. Strange RN, Scott PR. 2005. Plant disease: a threat to global food security. Annu. Rev. Phytopathol.
43:83116
160. Strawn MA, Marr SK, Inoue K, Inada N, Zubieta C, Wildermuth MC. 2007. Arabidopsis isochorismate
synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role
in diverse stress responses. J. Biol. Chem. 282:591933

161. Stumpe M, Gobel C, Faltin B, Beike AK, Hause B, et al. 2010. The moss Physcomitrella patens contains
cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered
sporophyte morphology. New Phytol. 188:74049
162. Sugano S, Sugimoto T, Takatsuji H, Jiang CJ. 2013. Induction of resistance to Phytophthora sojae in
soyabean (Glycine max) by salicylic acid and ethylene. Plant Pathol. 62:104856
163. Sunkar R, Zhu JK. 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis.
Plant Cell 16:200119
164. Taheri P, Tarighi S. 2010. Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-
mediated priming of phenylpropanoid pathway. J. Plant Physiol. 167:2018
165. Takasaki H, Maruyama K, Takahashi F, Fujita M, Yoshida T, et al. 2015. SNAC-As, stress-responsive
NAC transcription factors, mediate ABA-inducible leaf senescence. Plant J. 84:111423
166. Takezawa D, Watanabe N, Ghosh TK, Saruhashi M, Suzuki A, et al. 2015. Epoxycarotenoid-mediated
synthesis of abscisic acid in Physcomitrella patens implicating conserved mechanisms for acclimation to
hyperosmosis in embryophytes. New Phytol. 206:20919
167. Terol J, Domingo C, Talon M. 2006. The GH3 family in plants: genome wide analysis in rice and
evolutionary history based on EST analysis. Gene 371:27990
168. Thaler JS, Humphrey PT, Whiteman NK. 2012. Evolution of jasmonate and salicylate signal crosstalk.
Trends Plant Sci. 17:26070
169. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, et al. 2007. JAZ repressor proteins are targets of
the SCF(COI1) complex during jasmonate signalling. Nature 448:66165
170. Tintor N, Ross A, Kanehara K, Yamada K, Fan L, et al. 2013. Layered pattern receptor signaling via
ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. PNAS
110:621116
171. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 2009. Network properties of robust immunity
in plants. PLOS Genet. 5:e1000772
172. Ueno Y, Yoshida R, Kishi-Kaboshi M, Matsushita A, Jiang C-J, et al. 2015. Abiotic stresses antagonize the
rice defence pathway through the tyrosine-dephosphorylation of OsMPK6. PLOS Pathog. 11:e1005231
173. Ulferts S, Delventhal R, Splivallo R, Karlovsky P, Schaffrath U. 2015. Abscisic acid negatively interferes
with basal defence of barley against Magnaporthe oryzae. BMC Plant Biol. 15:7
174. Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, et al. 2007. The phytotoxin coronatine
contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato
inoculated with Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 20:95565
175. Van Den Boom CEM, Van Beek TA, Posthumus MA, De Groot A, Dicke M. 2004. Qualitative and
quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from
various families. J. Chem. Ecol. 30:6989
176. van Leeuwen H, Kliebenstein DJ, West MAL, Kim K, van Poecke R, et al. 2007. Natural variation
among Arabidopsis thaliana accessions for transcriptome response to exogenous salicylic acid. Plant Cell
19:2099110
177. van Wersch R, Li X, Zhang YL. 2016. Mighty dwarfs: Arabidopsis autoimmune mutants and their usages
in genetic dissection of plant immunity. Front. Plant Sci. 7:1717
178. Vos IA, Moritz L, Pieterse CMJ, Van Wees SCM. 2015. Impact of hormonal crosstalk on plant resistance
and fitness under multi-attacker conditions. Front. Plant Sci. 6:639
179. Vriet C, Lemmens K, Vandepoele K, Reuzeau C, Russinova E. 2015. Evolutionary trails of plant steroid
genes. Trends Plant Sci. 20:3018
180. Wang CY, Liu Y, Li SS, Han GZ. 2015. Insights into the origin and evolution of the plant hormone
signaling machinery. Plant Physiol. 167:87286
181. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong XN. 2007. Salicylic acid inhibits pathogen growth
in plants through repression of the auxin signaling pathway. Curr. Biol. 17:178490
182. Wang H, Mao HL. 2014. On the origin and evolution of plant brassinosteroid receptor kinases. J. Mol.
Evol. 78:11829
183. Wang HH, Wijeratne A, Wijeratne S, Lee S, Taylor CG, et al. 2012. Dissection of two soybean QTL
conferring partial resistance to Phytophthora sojae through sequence and gene expression analysis. BMC
Genom. 13:428
184. Ward EWB, Cahill DM, Bhattacharyya MK. 1989. Abscisic acid suppression of phenylalanine ammonia-
lyase activity and mRNA, and resistance of soybeans to Phytophthora megasperma f. sp. glycinea. Plant
Physiol. 91:2327
185. Wasternack C, Hause B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in
plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann.
Bot. 111:102158
186. Westfall CS, Sherp AM, Zubieta C, Alvarez S, Schraft E, et al. 2016. Arabidopsis thaliana GH3.5 acyl acid
amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis. PNAS 113:13917
22
187. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 2001. Isochorismate synthase is required to synthesize
salicylic acid for plant defence. Nature 414:56265
188. Wolter M, Hollricher K, Salamini F, Schulze-Lefert P. 1993. The MLO resistance alleles to powdery
mildew infection in barley trigger a developmentally controlled defense mimic phenotype. Mol. Gen.
Genet. 239:12228
189. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, et al. 2012. The Arabidopsis NPR1 protein is a receptor for
the plant defense hormone salicylic acid. Cell Rep. 1:63947
190. Xin XF, Nomura K, Aung K, Velasquez AC, Yao J, et al. 2016. Bacteria establish an aqueous living space
in plants crucial for virulence. Nature 539:52429
191. Xu MJ, Dong JF, Wang HZ, Huang LQ. 2009. Complementary action of jasmonic acid on salicylic acid
in mediating fungal elicitor-induced flavonol glycoside accumulation of Ginkgo biloba cells. Plant Cell
Environ. 32:96067
192. Yan Y, Christensen S, Isakeit T, Engelberth J, Meeley R, et al. 2012. Disruption of OPR7 and OPR8
reveals the versatile functions of jasmonic acid in maize development and defense. Plant Cell 24:142036
193. Yang JW, Yi H-S, Kim H, Lee B, Lee S, et al. 2011. Whitefly infestation of pepper plants elicits defence
responses against bacterial pathogens in leaves and roots and changes the below-ground microflora.
J. Ecol. 99:4656
194. Yang Y, Ou B, Zhang JZ, Si W, Gu HY, et al. 2014. The Arabidopsis Mediator subunit MED16 regulates
iron homeostasis by associating with EIN3/EIL1 through subunit MED25. Plant J. 77:83851
195. Yang YJ, Yue RQ, Sun T, Zhang L, Chen W, et al. 2015. Genome-wide identification, expression
analysis of GH3 family genes in Medicago truncatula under stress-related hormones and Sinorhizobium
meliloti infection. Appl. Microbiol. Biot. 99:84154
196. Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, et al. 2008. Antagonistic interaction between
systemic acquired resistance and the abscisic acidmediated abiotic stress response in Arabidopsis. Plant
Cell 20:167892
18.24 Berens et al.
197. Yin C, Park JJ, Gang DR, Hulbert SH. 2014. Characterization of a tryptophan 2-monooxygenase gene
from Puccinia graminis f. sp. tritici involved in auxin biosynthesis and rust pathogenicity. Mol. Plant-
Microbe Interact. 27:22735
198. Yuan YA, Chung JD, Fu XY, Johnson VE, Ranjan P, et al. 2009. Alternative splicing and gene dupli-
cation differentially shaped the regulation of isochorismate synthase in Populus and Arabidopsis. PNAS
106:2202025
199. Yuan YX, Zhong SH, Li Q, Zhu ZR, Lou YG, et al. 2007. Functional analysis of rice NPR1-like genes
reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore
susceptibility. Plant Biotechnol. J. 5:31324
200. Yue JP, Hu XY, Huang JL. 2014. Origin of plant auxin biosynthesis. Trends Plant Sci. 19:76470
201. Zaveska Drabkova L, Dobrev PI, Motyka V. 2015. Phytohormone profiling across the bryophytes. PLOS
ONE 10:e0125411
202. Zhai QZ, Yan LH, Tan D, Chen R, Sun JQ, et al. 2013. Phosphorylation-coupled proteolysis of the
transcription factor MYC2 is important for jasmonate-signaled plant immunity. PLOS Genet. 9:e1003422
203. Zhang HT, Hedhili S, Montiel G, Zhang YX, Chatel G, et al. 2011. The basic helix-loop-helix tran-
scription factor CrMYC2 controls the jasmonate-responsive expression of the ORCA genes that regulate
alkaloid biosynthesis in Catharanthus roseus. Plant J. 67:6171
204. Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, et al. 2009. Altered architecture and enhanced drought
tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant
Physiol. 151:1889901
205. Zhang X, Zhu ZQ, An FY, Hao DD, Li PP, et al. 2014. Jasmonate-activated MYC2 represses
ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Ara-
bidopsis. Plant Cell 26:110517
206. Zhang ZQ, Li Q, Li ZM, Staswick PE, Wang MY, et al. 2007. Dual regulation role of GH3.5 in salicylic
acid and auxin signaling during ArabidopsisPseudomonas syringae interaction. Plant Physiol. 145:45064
207. Zhao YF, Thilmony R, Bender CL, Schaller A, He SY, Howe GA. 2003. Virulence systems of Pseu-
domonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling
pathway. Plant J. 36:48599
208. Zhao YT, Wang M, Wang ZM, Fang RX, Wang XJ, Jia YT. 2015. Dynamic and coordinated expression
changes of rice small RNAs in response to Xanthomonas oryzae pv. oryzae. J. Genet. Genom. 42:62537
209. Zheng X-Y, Spivey Natalie W, Zeng W, Liu P-P, Fu Zheng Q, et al. 2012. Coronatine promotes
Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accu-
mulation. Cell Host Microbe 11:58796

2017.evolution of Hormone Signaling Networks in Plant Defense

Hochgeladen von

Dokumentinformationen

Originaltitel

Copyright

Verfügbare Formate

Dieses Dokument teilen

Dokument teilen oder einbetten

Freigabeoptionen

Stufen Sie dieses Dokument als nützlich ein?

Sind diese Inhalte unangemessen?

Copyright:

Verfügbare Formate

2017.evolution of Hormone Signaling Networks in Plant Defense

Hochgeladen von

Copyright:

Verfügbare Formate

PY55CH18-Tsuda ARI 15 June 2017 8:49

Review in Advance first posted online

still occur before final publication

Matthias L. Berens,1 Hannah M. Berry,2 Akira Mine,1

Cristiana T. Argueso,2 and Kenichi Tsuda1

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

18.2 Berens et al.

improve crop production.

CONSERVED ROLES OF PHYTOHORMONES IN PLANT DEFENSE

Salicylic Acid and Jasmonate as Conserved Positive Regulators of Plant Defense

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.3

of SA in resistance against biotrophs and hemibiotrophs is widely conserved in angiosperms.

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

18.4 Berens et al.

is required to understand the emergence of JA roles in triggering defense.

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

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.5

of auxin/indole-3-acetic acid (Aux/IAA) transcriptional repressors through the 26S proteasome

18.6 Berens et al.

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

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.7

CONSERVED HUBS IN HORMONE SIGNALING NETWORKS

18.8 Berens et al.

Pentapetalae Linum usitatissimum

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

ICS1 ICS1 IAA

SA NPR1 Immunity AUX/IAA

d GA JA-Ile e ABA JA-Ile ANACs

Activation Inhibition Protein degradation Transcription

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.9

JAZ and DELLA

Gretchen Hagen 3 Family

EVOLUTIONARY ADVANTAGES OF DEFENSE HORMONE

Hormone Cross Talk in Combined Stress

18.12 Berens et al.

Hormone Cross Talk in Plant Growth and Defense Trade-Offs

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.13

ENGINEERING HORMONE CROSS TALK

Challenges in Hormone Cross Talk Engineering

Opportunities in Hormone Cross Talk Engineering

18.14 Berens et al.

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.15

18.16 Berens et al.

ABI5 transcription factors. Plant Cell 24:2898916

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.17

transcription coactivator NPR1 in Arabidopsis thaliana. Plant J. 86:2034

18.18 Berens et al.

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.19

18.20 Berens et al.

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.21

upon Botrytis cinerea infection. Mol. Plant Pathol. 13:96074

18.22 Berens et al.

in diverse stress responses. J. Biol. Chem. 282:591933

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.23

18.24 Berens et al.

www.annualreviews.org Evolution of Hormone Signaling Networks in Plant Defense 18.25

Das könnte Ihnen auch gefallen