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Towards engineering of hormonal crosstalk in plant

immunity
Alexandra M Shigenaga1, Matthias L Berens2, Kenichi Tsuda2
and Cristiana T Argueso1

Plant hormones regulate physiological responses in plants, hormonal pathways is presumed to confer advantages
including responses to pathogens and beneficial microbes. The to plants, allowing for the concomitant regulation of
last decades have provided a vast amount of evidence about different hormone-regulated physiological processes,
the contribution of different plant hormones to plant immunity, thus leading to increased ability to respond to different
and also of how they cooperate to orchestrate immunity types of pathogens as well as beneficial organisms, and
activation, in a process known as hormone crosstalk. In this changing developmental and environmental conditions.
review we highlight the complexity of hormonal crosstalk in This review will cover the importance of hormonal cross-
immunity and approaches currently being used to further talk in immune responses, approaches to understand
understand this process, as well as perspectives to engineer complex hormonal networks such as quantification of
hormone crosstalk for enhanced pathogen resistance and hormones and hormonal signaling, mathematical model-
overall plant fitness. ing, synthetic biology, and how hormonal crosstalk could
be engineered to increase plant overall fitness.
Addresses
1
Department of Bioagricultural Sciences and Pest Management,
Colorado State University, Fort Collins, CO, USA Hormonal crosstalk and plant immunity
2
Department of Plant–Microbe Interactions, Max Planck Institute for Plant hormones are essential regulators of the responses
Plant Breeding Research, 50829 Cologne, Germany of plants to microbes. The hormones salicylic acid (SA)
Corresponding authors: Tsuda, Kenichi ([email protected]),
and jasmonate (JA) are recognized as the most important
Argueso, Cristiana T ([email protected]) hormones for plant immune responses. These two classes
of hormones are believed to form the hormonal backbone
of plant immune responses to pathogens [1]. Defense
Current Opinion in Plant Biology 2017, 38:164–172
against biotrophic pathogens, which keep the host alive to
This review comes from a themed issue on Biotic interactions obtain nutrients, requires SA biosynthesis and signaling,
Edited by Sarah Lebeis and Silke Robatzek whereas JA biosynthesis and signaling are required for
resistance against necrotrophic pathogens, which acquire
nutrients from decaying host tissue [3]. In many plant-
pathogen interactions involving JA, ethylene (ET) has
http://dx.doi.org/10.1016/j.pbi.2017.04.021 been shown to assist in defense responses, resulting in
1369-5266/ã 2017 Elsevier Ltd. All rights reserved. increased resistance to necrotrophic pathogens [4]. In the
last two decades, various studies have shown that other
plant hormones important for growth, such as auxins
(AUX), cytokinins (CK), brassinosteroids (BR), gibber-
ellins (GA) and strigolactones (SL), as well as the abiotic
stress hormone abscisic acid (ABA), participate in plant
Introduction defense [2]. These hormones typically function through
Plant hormones are small signaling molecules withimpor- action on the SA and JA pathways in plant immunity.
tant regulatory roles in various plant processes. Molecules Such crosstalk is frequently exploited by pathogens
with plant hormone activity have historically been classi- through manipulations of their metabolic and signaling
fied based on their chemical structures, and also on their pathways by pathogen effectors (reviewed in Refs.
primary function in physiological processes, such as [2,5,6]). In addition, several pathogens and beneficial
growth, biotic or abiotic stress hormones. Such functional microbes are able to synthesize and secrete plant hor-
classifications are now considered loose categorizations, as mones, or mimics thereof, affecting the SA–JA hormonal
many hormones first thought to be only associated with backbone and influencing host physiological status. A
growth processes have now been linked to immune well-studied example is the phytotoxin coronatine
responses against pathogens [1,2]. The complex network (COR), which is secreted by several Pseudomonas syringae
of communication among plant hormone signaling path- pathovars and functions as a JA-mimic, resulting in inhi-
ways is often referred to as hormone crosstalk, and is bition of SA-regulated defense responses and decreased
employed in many plant processes, not just in the case of host resistance to biotrophic pathogens [7–9]. Nonethe-
immune responses. Such interplay among different less, pathogenic organisms can also secrete other classes

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 Engineering of hormonal crosstalk in plant immunity Shigenaga et al. 165

of plant hormones, such as ET [10,11], GA [12], AUX brassicicola, and led to decreased expression of the JA/ET
[13], ABA [14] and CK [15,16], although it is unclear markers PDF1.2, HEL and CHI-B [22]. Similarly,
whether this virulence mechanism is used to increase host exogenous application of an SA analogue reduced JA-
susceptibility or counteract defense responses. Similarly, regulated defenses against A. brassicicola [22]. This
beneficial microbes are also able to produce plant hor- reciprocal antagonistic crosstalk between the SA and JA
mones, using them to promote plant immunity and shape pathways, initially demonstrated in Arabidopsis, is also
community composition [17,18], thus adding another observed in other plant species, and phylogenetic studies
level of complexity to hormone crosstalk in indicate that it may have evolved with the development
plant–microbe interactions. of angiosperms [23]. Nonetheless, evidence exists for
deviations of this antagonism, particularly in the case
With a variety of both plant and pathogen-derived mole- of monocotyledonous plants [24,25]. Antagonistic or
cules with hormone activity affecting plant immunity, synergistic interactions of other plant hormones with
crosstalk among the different hormonal networks is often the SA–JA backbone, as well as among themselves, also
observed. The antagonistic nature of the crosstalk contribute to plant immunity (Table 1). For example,
between the SA and JA pathways in plant immune high levels of CK potentiate the SA pathway [26,27].
responses was first suggested in experiments involving Interestingly, in some cases, different levels of the same
exogenous hormone treatment of plants, followed by hormone will lead to opposing physiological/resistance
measurements of gene expression or gene product activ- responses [25,27,28].
ity of SA- or JA/ET-specific markers [4,19–21]. Activation
of the SA or JA sectors was triggered depending on Understanding hormone crosstalk in plant
whether Arabidopsis plants were inoculated with a immunity
(hemi-)biotrophic or necrotrophic pathogen. A trade-off The contributions of the different plant hormones to
between these two pathways was demonstrated by hormone crosstalk during pathogen attack have been
experiments in which inoculation with a hemi-biotrophic determined predominantly by the use of mutants
pathogen (P. syringae pv. tomato DC3000) rendered plants impaired in the signaling/metabolism of single hormones.
more susceptible to the necrotrophic pathogen Alternaria However, such analyses may be misleading because they

Table 1

Reports of hormone crosstalk interactions in relation to biotic stresses in various plant species

Hormone crosstalk Interaction Plant species Outcome Reference

SA–JA/ET Antagonistic Conserved among various SA-responses increase resistance to (hemi-)biotrophic Reviewed in
monocot and eudicot pathogens; JA-responses increase resistance to Ref. [24]
species necrotrophic pathogens; in some species SA & JA are
effective against both biotrophic and necrotrophic pathogens
JA–ET Synergistic Arabidopsis thaliana Increased resistance to necrotrophic pathogens [4,21,85,86]
SA–CK One-way Antagonism Arabidopsis thaliana Increased susceptibility to biotrophic pathogens [27]
CK–SA One-way Synergism Arabidopsis thaliana Increased resistance to (hemi-)biotrophic pathogens [26,27,84]
Oryza sativa
CK–JA Unclear Arabidopsis thaliana Unknown, may increase resistance to necrotrophic pathogens [26]
CK–ABA Antagonistic Nicotiana tabacum Increased resistance to (hemi-)biotrophic pathogens [83]
ABA–JA/ET Antagonistic Arabidopsis thaliana Decreased resistance to necrotrophic pathogens [81]
ABA–ET Antagonistic Oryza sativa Increased resistance to necrotrophic pathogens [82]
ABA–SA Antagonistic Arabidopsis thaliana Increased susceptibility to biotrophic pathogens [39,92]
Oryza sativa
AUX–JA One-way Synergism Arabidopsis thaliana Increased resistance to necrotrophic pathogens [90]
AUX–SA Antagonistic Arabidopsis thaliana SA-responses increase resistance to (hemi-)biotrophic [91]
pathogens; AUX-responses increase susceptibility
AUX–CK Antagonistic Arabidopsis thaliana CK-responses increase resistance to biotrophic pathogens, [37]
AUX-responses increases susceptibility
GA–JA/ET Antagonistic Arabidopsis thaliana Increased susceptibility to necrotrophic pathogens [62,88]
GA–SA Synergistic Arabidopsis thaliana Increased resistance to biotrophic pathogens [88]
BR–GA Antagonistic Oryza sativa Decreased resistance to necrotrophic pathogens [93]
BR–SA Antagonistic Oryza sativa Decreased resistance to necrotrophic pathogens [93]
BR–JA Antagonistic Oryza sativa Decreased resistance to nematodes [87]
SL–AUX Unclear Arabidopsis thaliana Increased resistance to bacterial pathogens [89]

SA—salicylic acid; JA—jasmonate; ET—ethylene; ABA—abscisic acid; AUX—auxin; CK—cytokinin; GA—gibberellin; BR—brassinosteroids;
SL—strigolactones. ‘Synergistic’ indicates a positive interaction between hormones involved in crosstalk, while ‘Antagonistic’ indicates a negative
interaction between the hormones. ‘One-way’ indicates that the first hormone listed is either positively or negatively interacting with the second
hormone listed in the ‘Hormone Crosstalk’ column, resulting in a unique outcome or pathogen response. ‘Unclear’ indicates a possible synergistic or
antagonistic relationship that has not yet been confirmed [4,21,24,26,27,37,39,62,81–93].

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166 Biotic interactions

reveal the effects of not only the loss of the disrupted Dynamics in plant hormone accumulation influence sig-
hormone signaling sector, but also the loss of hormone naling outputs mediated by a given plant hormone, as
crosstalk [29,30]. This caveat can be overcome through well as any resulting hormone crosstalk. For example,
the use of higher order mutants, as well as exhaustive antagonism between ABA and SA during plant immunity
combinatorial mutants followed by modeling-based anal- is dependent on both the hormone concentration and the
ysis of quantitative crosstalk outputs, such as pathogen timing of hormone application [38,39]. Thus, measuring
growth or changes in pathogen-regulated gene expres- phytohormone concentrations, as well as the resulting
sion. This approach has been successfully applied to signaling, is vital to understanding hormone crosstalk.
reveal the individual and combined contributions of One approach for the measurement of hormone signaling
the SA, JA and ET signaling sectors to hormone crosstalk relies on the use of hormone-specific transcriptional fluo-
in relation to resistance against P. syringae and A. brassi- rescent reporters [40]. These reporters, such as the auxin
cicola [29] and to genome-wide transcriptional changes reporter DR5 [41] and the CK reporter TCSn [42], are
triggered by pathogen elicitors [30]. An expanded analysis driven by synthetic promoters engineered to contain cis-
using multiple immune outputs at two time points fol- elements targeted by central transcription factors in hor-
lowed by a multiple regression or Bayesian network mone signaling, thus bypassing hormone-independent
model showed a temporally dynamic plant hormone regulatory elements. This synthetic approach may repre-
signaling network model during pattern-triggered immu- sent an advantage over the use of native promoters of
nity (PTI) with high predictability [31]. These modeling- hormone marker genes for measuring activity of hormone
based studies revealed important network properties of signaling. For instance, the expression of the classical SA
plant hormone signaling networks in plant immunity, marker gene PATHOGENESIS-RELATED 1 (PR-1) can
such as network robustness and tunability, and can gen- be regulated independently of SA [43], pointing to a need
erate sometimes-unexpected hypotheses that can be fur- for caution in using marker gene expression to measure
ther tested. For instance, with a generated hypothesis as hormonal activity.
the starting point, a follow-up study uncovered the molec-
ular detail for positive and negative effects of JA on SA Similarly, understanding of hormonal crosstalk can
accumulation during PTI [32]. benefit from direct measurements of plant hormones
levels. Several mass spectrometry-based high-throughput
protocols to simultaneously quantify multiple classes of
Systems biology and mathematical modeling are powerful plant hormones have been established. Such methods
approaches to disentangle complex biological systems. have already been used, for example, in systemic analysis
The high degree of complexity observed in hormonal of hormonal crosstalk during abiotic stress responses [44].
crosstalk during plant immunity renders it particularly Other methods based on immunological detection have
suitable for such analyses. For instance, analyses of also been used, although with limited sensitivity [45].
genome-wide transcriptional responses of plants to exog- Genetically encoded plant hormone sensors, which
enously applied plant hormones, immune elicitors or exploit native hormone recognition mechanisms and
pathogen infection, have contributed significantly to allow for quantitative measurement of hormones in vivo,
our holistic understanding of plant hormone signaling have recently been developed and provide extraordinary
networks [33]. Co-expression analyses using publicly sensitivity. While such hormone sensors for ABA [46,47],
available transcriptome data have revealed cis-regulatory AUX [48,49], JA [50] and SL [51] have been established,
elements that are implicated in hormone crosstalk during sensors for other plant hormones such as SA, ET, CK, GA
plant immunity [34,35]. Through integrated analysis of and BR await method development. Although the use of
protein–protein interaction and transcriptomic responses fluorescent and genetically encoded hormone sensors in
during pathogen infection, Jiang et al. identified compo- the context of plant immunity has so far been limited
nents of auxin response as hubs in a defense network [36]. [52], these approaches should provide excellent
Similarly, in silico dynamic simulations using Boolean opportunities to understand temporal and spatial/cellular
network approaches of various information reported in dynamics of plant hormone activities and hormone cross-
the literature have been used to predict synergism talk. This is an important consideration given that hor-
between CK and SA and antagonism between CK and mone crosstalk in plant immunity is not only pathogen-
AUX in plant immunity [37], confirming interactions specific, but also spatially-regulated [22].
previously identified in biological studies [26,27]. How-
ever the predominance of single mutant studies in the Engineering of hormone crosstalk in plant
literature, rather than the more informative approaches immunity
based on double and higher mutant analyses, could also Hormone crosstalk is believed to balance defense
produce a bias in literature-based in silico examinations. response activation, plant development, and abiotic stress
Nevertheless, the above-mentioned approaches have tolerance. In nature, plants are frequently exposed to
been successfully used to understand hormone crosstalk, multiple abiotic and biotic stresses at the same time.
as well as generate new hypotheses. In such conditions, the involvement of hormone crosstalk

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 Engineering of hormonal crosstalk in plant immunity Shigenaga et al. 167

is Figure 1

(a)
PATHOGEN ABIOTIC GROWTH

SA JA ET ABA CK AUX GA BR SL

NPR1 JAZ ERF MED25 Type-B ARR AUX/IAA MAX2

WRKY TGA MYC EIN/EIL DELLA

(b) GROWTH

CK AUX BR GA

?
Type-B ARR
SL

NPR1 JAZ DELLA

BIOTROPHIC PATHOGEN TGA SA JA NECROTROPHIC PATHOGEN

RESISTANCE RESISTANCE

ABA ET

Legend:

= Crosstalk Interaction

ABIOTIC STRESS
= Crosstalk Interaction
RESISTANCE
Current Opinion in Plant Biology

Complex hormone crosstalk interactions in response to biotic stress, abiotic stress and during plant growth. (a) Interactions between
different plant hormone pathways (lines) during plant immunity through shared signaling proteins that may function as potential hormone crosstalk
hubs (dark-gray boxes). Purple boxes indicate general hormone classifications. Gray circles represent the major classes of plant hormones
SA—salicylic acid; JA—jasmonate; ET—ethylene; ABA—abscisic acid; AUX—auxin; CK—cytokinin; GA—gibberellin; BR—brassinosteroids;
SL—strigolactones. A ‘?’ indicates an unclear interaction in hormone crosstalk. For explanation of crosstalk shown, see Table 1 and Ref. [2]. (b)
Potential crosstalk engineering of hormonal pathways to improve biotic and abiotic stress tolerance and plant growth. Although hormone
crosstalk is highly complex, it may be engineered for particular outcomes. Each line represents an established crosstalk interaction among various
hormones in relation to biotic and abiotic stress responses, as well as growth. Colored lines represent pathways that could be engineered by

www.sciencedirect.com Current Opinion in Plant Biology 2017, 38:164–172

168 Biotic interactions

evident, as reported by transcriptome analysis and biosynthetic pathways, as well as the genetic redundancy
genome-wide association studies [53–56]. Increased often observed in these pathways. Thus, effector targets
understanding of the role of hormones and hormonal with hormone regulatory activity are likely to substan-
interplay during plant immunity paves the way for tially change host physiological status and function as
attempts at engineering of hormonal crosstalk to generate hormone crosstalk hubs. For example, effectors are
plants with increased disease resistance and abiotic stress known to target NPR1 function [38,64], a suitable hor-
tolerance, maintaining overall plant fitness. mone crosstalk hub for target as it plays a key role in the
SA-JA antagonism. P. syringae pathovars also secrete
The mechanisms that mediate hormonal crosstalk have effectors to target JAZ proteins for degradation and acti-
not been completely defined. While examples of co- vate JA signaling [65,66]. Recent efforts of effector target
regulation of transcriptional targets can be found, in identification through high-throughput yeast two-hybrid
general hormone-regulated transcriptional networks are approaches have been very successful and reveal that the
mostly non-overlapping [57]. One common theme in hormone signaling proteins targeted by pathogen effec-
hormone crosstalk is the sharing of signaling proteins. tors are conserved even among effectors from different
For example, NONEXPRESSOR OF PR GENES1 pathogens [67,68]. Finally, natural plant genetic diversity
(NPR1) is a known regulator of SA signaling. Given can also be used to determine hormone crosstalk hubs
the antagonistic relationship between SA and JA, a nega- with different levels of crosstalk activity. Natural genetic
tive regulation of NPR1 by post-translational mechanisms variation in relation to hormone crosstalk pathways has
also functions as mechanism of JA signaling activation been demonstrated not only among different plant spe-
[58–61]. In another example, DELLA proteins, known cies, but also among accessions/varieties of the same
negative regulators of GA signaling, can positively regu- species [23,24,69]. In Arabidopsis, ecotypes treated with
late the JA pathway. In the absence of GA, DELLAs can SA- or JA-derivatives responded differently, suggesting
actively compete with the JA-regulated transcription fac- the existence of natural genetic variation and phenotypic
tor MYC2 for binding to the negative regulators of JA plasticity in relation to hormone crosstalk [70–73], thus
signaling Jasmonate-ZIM-domain proteins (JAZ), thus opening possibilities for genetic mapping of genes with
enabling crosstalk between the GA and JA pathways functions in hormone crosstalk regulation.
[62]. NPR1 and DELLA proteins can thus be considered
hormone crosstalk hubs, or proteins that mediate the One expected limitation of a hormone crosstalk engineer-
interplay between different hormonal signaling pathways ing approach is the high level of interconnectivity of
(Figure 1a,b). Such hubs are integral for hormone cross- hormonal networks (Figure 1a). Because hormonal net-
talk and may be engineered to shift hormonal networks to works control several physiological responses, engineer-
the desired physiological responses, and theoretically lead ing efforts may lead to undesired pleiotropic effects.
to outcomes of enhanced pathogen resistance without Thus, the same plasticity that allows plants to respond
plant fitness reduction. The recent demonstration that to varying stimuli can also be a constraint in engineering
growth tradeoffs and defense activation can be unlinked hormone crosstalk for increased fitness. However, recent
[63] indicates that biotic trade-offs can be overcome, advances in synthetic biology may allow for the develop-
paving the way for the manipulation of hormonal path- ment of synthetic hormonal crosstalk networks with tun-
ways not only for increased defense to pathogens, but also able properties that may help circumvent pleiotropic
for enhanced abiotic stress tolerance and plant growth. effects. Such approaches may make use of synthetic
promoters, harboring cis-regulatory elements to drive
So far, many hormone crosstalk hubs in plant immunity the expression of particular hormone crosstalk hubs under
have been identified through genetic screens, however specific conditions [74], as well as more complex genetic
the computational and systems biology approaches men- circuits driven by tunable switches. Recent efforts to
tioned above are likely to reveal not only patterns of quantitatively characterize genetic parts for plant syn-
crosstalk, but also novel hormone crosstalk hubs. Another thetic biology have been promising [75], including syn-
possible strategy for the identification of hormonal cross- thetic small RNAs, repressible promoters/repressors pairs
talk hubs lies on pathogen effector targets. Several path- [76] and chemically or optogenetically inducible switches
ogen effectors are known to target plant hormone signal- [77,78]. Moreover, effective recapitulation of a hormonal
ing or metabolic pathways. Effective manipulation of signaling pathway has been demonstrated in yeast [79],
hormonal networks to favor conditions for pathogenicity indicating the feasibility of engineering synthetic hor-
and virulence requires overcoming the multiple regula- monal pathways, albeit in a far less complex system. The
tory steps commonly present in plant hormone signaling/ use of tissue-specific regulatory elements may also allow

(Figure 1 Legend Continued) certain crosstalk signaling hubs (dark-gray boxes) to increase certain responses/processes (colored boxes), such as
pathogen resistance or plant growth. An arrow indicates a positive/synergistic interaction, while a blunt end indicates a negative/antagonistic
interaction. Solid lines represent engineering for increased crosstalk interaction. Dotted lines represent engineering for a decreased crosstalk
interaction. Plant hormone abbreviations as in (a). A ‘?’ indicates an unclear interaction in hormonal crosstalk.

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 Engineering of hormonal crosstalk in plant immunity Shigenaga et al. 169

for activation of localized defense responses, likely dimin-

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Dr. Karl Ravet for his help in figure preparations. This work was supported 16. Chanclud E, Kisiala A, Emery NR, Chalvon V, Ducasse A, Romiti-
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