hormonal interactions underlying responses to abiotic stress and insect herbivory

14 Pages·2016·1.15 MB·English

by  Duy Nguyen

PlantMolBiol(2016)91:727–740
DOI10.1007/s11103-016-0481-8
How plants handle multiple stresses: hormonal interactions
underlying responses to abiotic stress and insect herbivory
Duy Nguyen1 • Ivo Rieu1 • Celestina Mariani1 • Nicole M. van Dam1,2,3
Received:31October2015/Accepted:9April2016/Publishedonline:19April2016
(cid:2)TheAuthor(s)2016.ThisarticleispublishedwithopenaccessatSpringerlink.com
Abstract Adaptive plant responses to specific abiotic involvement of signaling pathways in single stress respon-
stresses or biotic agents are fine-tuned by a network of ses.Moreexperimentaldataonnon-modelplantandinsect
hormonal signaling cascades, including abscisic acid species are needed to reveal general patterns and better
(ABA), ethylene, jasmonic acid (JA) and salicylic acid. understand the molecular mechanisms allowing plants to
Moreover, hormonal cross-talk modulates plant responses optimize their responses incomplex environments.
to abiotic stresses and defenses against insect herbivores
when they occur simultaneously. How such interactions Keywords Drought (cid:2) Flooding (cid:2) Herbivory (cid:2) Hormonal
affect plant responses under multiple stresses, however, is cross-talk (cid:2) Induced resistance (cid:2) Stress responses
less understood, even though this may frequently occur in
natural environments. Here, we review our current knowl- Abbreviations
edge on how hormonal signaling regulates abiotic stress ABF ABA-responsive element binding factor
responsesanddefensesagainstinsects,anddiscussthefew AP2/ERF Apetala2/ethylene response factor
recent studies that attempted to dissect hormonal interac- COI1 Coronatine insensitive1
tions occurring under simultaneous abiotic stress and her- CTR1 Constitutive triple response1
bivory. Based on this we hypothesize that drought stress EAR ERF-associated amphiphilic repression
enhances insect resistance due to synergistic interactions EBF EIN3-binding F-box protein
between JA and ABA signaling. Responses to flooding or EIL1 EIN3-like protein1
waterlogging involve ethylene signaling, which likely EIN2 Ethylene insensitive2
reduces plant resistance to chewing herbivores due to its EIN3 Ethylene insensitive3
negative cross-talk with JA. However, the outcome of JAZ Jasmonate-ZIM domain corepressor
interactions between biotic and abiotic stress signaling is LAP Leucine aminopeptidase
often plant and/or insect species-dependent and cannot LOX Lipoxygenase
simply be predicted based on general knowledge on the NINJA Novel interactor of JAZ
PDF1.2 Plant defensin
PP2C Type 2C protein phosphatase
& NicoleM.vanDam PR Pathogenesis-related
[email protected] PYR/PYL/ Pyrabactin resistance1/PYR-like/
RCAR regulatory component of ABA receptor
1 MolecularPlantPhysiology,InstituteforWaterandWetland
SCF Skp, Cullin, F-box containing
Research(IWWR),RadboudUniversity,POBox9010,
SnRK2 Sucrose non-fermenting1-related protein
6500GLNijmegen,TheNetherlands
kinase2 protein
2 GermanCentreforIntegrativeBiodiversityResearch(iDiv)
TPL Groucho/Tup1-type co-repressor
Halle-Jena-Leipzig,DeutscherPlatz5e,04103Leipzig,
Germany TOPLESS
3 InstituteofEcology,FriedrichSchillerUniversityJena, TPR TPL-related protein
Dornburger-Str.159,07743Jena,Germany VSP Vegetative storage protein
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728 PlantMolBiol(2016)91:727–740
Introduction Fig.1 Schematic overview of hormonal signaling. a A model ofc
jasmonicacid(JA)signaling,adaptedfromPauwelsetal.(2010).In
the absence of JA, JAZs recruit the co-repressor TPL andTPRs via
Plants have to constantly cope with a suite of biotic and the EAR motif of the adaptor protein NINJA to suppress JA-
responsivegeneexpression.ThiscanalsooccurdirectlyviatheJAZ’s
abiotic stress factors. Their performance thus depends on
EAR motif (Shyu et al. 2012). In the presence of JA, JA-isoleucine
the ability to quickly perceive changes in the environment
conjugatesareformedandfacilitatetheinteractionbetweenJAZsand
and to express an adaptive response. Much effort has been SCFCOI1,amulti-proteinE3ubiquitinligasecomplex.Thispromotes
made to understand the molecular mechanisms underlying JAZubiquitinationandsubsequentdegradationby26Sproteasomes,
resulting in the release of NINJA-TPL complex and activation of
plant adaptive responses because of their potential to
basic helix-loop-helix MYC transcription factors (TFs) to regulate
improve agricultural production under adverse conditions.
JA-responsive genes. b A model for abscisic acid (ABA) signaling,
Plantmolecularresponsestosingleabioticstresses,such adaptedfromCutleretal.(2010).IntheabsenceofABA,PP2Csare
asdrought,soilflooding,highorlowtemperatures,aswell activetopreventSnRK2activity.InthepresenceofABA,PYR/PYL/
RCARs bind to and inhibit PP2Cs, which allows phosphorylated
as to biotic interactions, such as insect herbivory and
SnRK2s to accumulate and subsequently phosphorylate ABFs to
pathogen attacks, have been gradually elucidated. These
regulate ABA-responsive gene expression. c A model of ethylene
responses are modulated by a complicated network of (ET)signaling,adaptedfromChoandYoo(2014).Intheabsenceof
signaling pathways induced by a variety of small mole- ET, the negative regulator CTR1 binds to membrane-bound ET
cules, including Ca2? signaling (Seybold et al. 2014), receptors (ETRs) and inactivate the positive regulator EIN2. More-
over, the downstream primary TFs, EIN3 and EIL1, are constantly
reactive oxygen and nitrogen species (Wang et al. 2013;
subjected to proteasomal degradation guided by EBF1 and EBF2.
Baxter et al. 2014) and phytohormones (Peleg and Blum- WhenEThasaccumulatedandbindstoETreceptors,theETR-CTR1
wald 2011; Pieterse et al. 2012; De Vleesschauwer et al. isinactivated.ThisleadstocleavageofC-terminalhalfofEIN2and
itstranslocationintonucleustostabilizeEIN3byinactivatingEBFs.
2014; Kazan 2015). Hormones and hormonal cross-talk
EIN3 then regulates expression of downstream ET-responsive AP2/
play an important role in the molecular mechanisms that
ERFTFs,suchasERF1andORA59
optimizeplantresponsestostresseswhichcommonlyoccur
simultaneouslyintheenvironment,suchasabioticstresses knowledge on how hormonal pathways regulate plant
and herbivory. Over the years several reviews have dis- responses to single stresses. Then we discuss how inter-
cussed cross-talk between defense-related hormonal path- actions between these pathways may modulate defense
waysinplantschallengedbydifferentherbivores,different responses in plants under combined stress conditions,
pathogens or combinations thereof (e.g. Pieterse et al. consideringthathormonalcross-talkmayservetooptimize
2002; Erb et al. 2008; De Vleesschauwer et al. 2014). plant performance in complex environments. Finally, we
Independently, ecophysiologists acquired substantial will specify which testable hypotheses follow from our
knowledge on the role of hormonal signaling pathways in current knowledge that may help to better understand the
responsestoabioticstresses,suchasdrought,floodingand role of signaling interactions in plants under multiple
shading (e.g. Peleg and Blumwald 2011; Voesenek and stresses.
Bailey-Serres 2015).Since long, several ecological studies
revealed that (induced) resistance to herbivores can be
affected by simultaneously occurring abiotic stresses, such Regulation of induced plant responses to insect
as drought (English-Loeb et al. 1997; Huberty and Denno herbivores
2004; Khan et al. 2010; Gutbrodt et al. 2011; Tariq et al.
2013).However,only recently there hasbeen anincreased In natural habitats, plants have to defend themselves
interest to identify the molecular mechanisms underlying against herbivorous insects with different feeding strate-
theseinteractiveeffects(Luetal.2015;DavilaOlivasetal. gies, including, but not limited to, leaf chewing beetles or
2016; Foyer et al. 2016; Nguyen et al. 2016). For this caterpillars, piercing-sucking thrips or spider mites, and
reason, thisagoodmoment formergingthe knowledgeon phloem-sucking aphids or whiteflies. Plant defense mech-
hormonalsignalinginabioticandbioticinducedresponses anisms may vary from morphological (e.g. trichomes,
withtheaimtocometoaunifiedconceptualframeworkof waxes) tochemicaldefenses[e.g. alkaloids,glucosinolates
how the signaling pathways induced by different stresses (GS), protease inhibitors (PIs)], which are often induced
may interact. Thereby, we focus on the interactions upon herbivory (Schaller 2008). When insects are feeding
between herbivore induced responses and water related on plants, herbivore associated molecular patterns
stresses, specifically drought and flooding. Both drought (HAMPs) and endogenous damage associated molecular
and soil flooding or waterlogging are common phenomena patterns (DAMPS) are released (Acevedo et al. 2015).
innaturalandagriculturalecosystems,andthefrequencyof Upon perception of these cues, phytohormones, including
their occurrence is expected to increase due to climate jasmonicacid(JA),abscisicacid(ABA)andethylene(ET),
change(IPCC2013).Here,wefirstreviewthemostrecent accumulate to activate signaling cascades that regulate
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downstream transcriptional responses (summarized in
Fig. 1a–c). Among them, JA and particularly its most
activeisoleucineconjugate(JA-Ile),aregenerallyaccepted
as the core inducers of many herbivore-induced defenses
(Howe and Schaller 2008; Tytgat et al. 2013; Wasternack
and Hause 2013). JA-insensitive or deficient mutants,
therefore, exhibit very low levels of resistance to a wide
range of herbivorous insects from different orders (Thaler
et al. 2002; Bodenhausen and Reymond 2007; Schweizer
et al. 2013).
Duetoherbivore-specificHAMPs(Acevedoetal.2015;
Xuetal.2015),othersignalinghormonesinadditiontoJA
are induced upon feeding to tailor the defenses against the
attacker. The signal signature that is induced for a part is
duetodifferencesinherbivorefeedingstrategies.Piercing-
sucking insects, such as aphids, have a ‘stealthy feeding
strategy’ (De Vos et al. 2005) that avoids massive cell
damage. On the other hand, the salivary sheet lining their
mandibles contains specific enzymes that interact with the
cells along the stylet path (Foyer et al. 2016). Aphid Fig.2 Schematic representation of interactions between hormonal
cascades regulating induced defenses against biotic agents (see text
feeding thus induces a significantly different set of sig-
and legend Fig.1 for further details and abbreviations). Insect
naling pathways and transcripts than chewing herbivores, herbivoresinduceJA-dependentMYC2regulationofdefense-related
thatcausemorecelldamageandpossessdifferentelicitors genes,whichisenahncedbyABAsignaling.Necrotrophicpathogens
in their saliva (De Vos et al. 2005; Bidart-Bouzat and induceJA/ET-dependentsignalingtoregulateERF1andORA59and
downstream defense-related genes. The two branches of defense
Kliebenstein 2011). On the other hand, herbivore-induced
responses mutually antagonize one another. GA and SA signaling
signal signatures can also be species-specific within her- generallyinhibitJA-dependentdefenseresponses
bivore feedingguilds. Forexample,feedingbycaterpillars
ofManducasextainducestheaccumulationofJAandET,
whereas Spodoptera exigua caterpillars induce JA and (Thaler and Bostock 2004; Bodenhausen and Reymond
salicylic acid (SA) in Nicotiana attenuata (Diezel et al. 2007; Vos et al. 2013b; Dinh et al. 2013). Furthermore,
2009). In contrast, S. exigua induces JA and ET accumu- ABA is involved in signaling process inducing JA-depen-
lation in maize (Zea mays) and Arabidopsis thaliana dentdefenseresponsesinsystemictissues(Erbetal.2009;
(Schmelz et al. 2003; Rehrig et al. 2014), whereas Pieris Vos et al. 2013b). The synergistic interaction between JA
rapaetriggersJAandABAlevelsinthelatterspecies(Vos andABAcanoccurviathetranscriptionfactor(TF)MYC2
et al. 2013b). Simultaneous SA and JA accumulation also and its homologs MYC3 and MYC4 in Arabidopsis
occurs upon herbivory by the Colorado potato beetle (Fig. 2). ABA induces COI-dependent expression of
(Leptinotarsa decemlineata) and the mealy bug MYCs, which induce plant resistance to insects by regu-
(Phenacoccus solenopsis) on tomato plants (Solanum lating many wound/herbivore-responsive genes, e.g. VSPs,
lycopersicum) (Chung et al. 2013; Zhang et al. 2015a). LOXs and glucosinolate biosynthetic genes (Lorenzo et al.
Although not all hormones were measured in each study, 2004; Dombrecht et al. 2007; Schweizer et al. 2013). In
this strongly suggests that plant hormonal responses to tomato, the ABA/JA/wounding-responsive expression of
herbivores depend on the specific plant–insect interaction. LAPandthePIgenePIN2aredirectlyregulatedbyMYC2
Cross-talk between JA and other phytohormones has been orthologs, JAMYC2 and JAMYC10 (Pen˜a-Corte´s et al.
proposed to fine-tune plant defense responses to specific 1995;Boteretal.2004).However,duetothestrongmutual
attackers (Pieterse et al. 2012; Erb et al. 2012). antagonism between ABA and ET, and the fact that some
JA-responsive defenses are mediated by ET (discussed
below),logicallyABAalsonegativelyaffectssomeJA/ET-
ABA in defense regulation dependent defenses, such as nicotine biosynthesis in
tobaccoplants(Nicotianatabacum)(Lackmanetal.2011).
ABAsynthesisandsignalingisrequiredforplants,suchas A key question is where in the signaling cascades
Arabidopsis, tomato and N. attenuata, to fully activate interactions between JA and ABA occur. The requirement
defenses and resistance against their herbivores; ABA ofnormalABAbiosynthesisforJAproduction(Adieetal.
deficiency increases plant susceptibility to herbivory 2007), the COI-dependency of the ABA-induced MYC2
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expression (Lorenzo et al. 2004) and the fact that methyl- involvement of ET in modulating herbivore/JA-induced
jasmonate (MeJA) still induces LAP and PIN2 in ABA- defense responses also shows in nicotine biosynthesis.
deficient mutants (Carrera and Prat 1998), suggest that the Defective ET signaling in N. attenuata, in one case,
interactionoccursupstreamofJAsignaling.Indeed,JAand resulted in reduced basal nicotine contents but enhanced
ABA mutually enhance their biosynthesis (Adie et al. inducibility of nicotine biosynthesis after M. sexta her-
2007; Fan et al. 2009; Brossa et al. 2011). Mechanistic bivory (von Dahl et al. 2007), but in other experiments, it
details on such interaction, however, are still lacking. did not affect basal levels and attenuated JA-induced
Interestingly, it has been shown that interactions may also nicotine response (Shoji et al. 2000; Winz and Baldwin
occur more downstream. A mechanism similar to the 2001; Onkokesung et al. 2010a). Nevertheless, both maize
suppression of JA-induced TFs by JAZ–NINJA–TPL was andN.attenuatawithcompromisedETsignalingaremore
identified for the ABA-dependent TF ABI5 (ABA insen- susceptible to M. sexta and S. frugiperda, respectively,
sitive5) in Arabidopsis. ABI5 binding proteins (AFPs) are demonstrating the role of ET in fortifying plant defenses
NINJA homologs and contain the EAR motif to interact (Harfouche et al. 2006; Onkokesung et al. 2010a). On the
with the corepressors TPL or TPRs for ABI5 inactivation other hand, ET signaling, via ERF1/ORA59 and their
(Pauwels et al. 2010). Although the tested AFPs do not upstream TFs EIN3/EIL1 (Fig. 1c), also inhibits the JA/
interact with JAZ1, this similarity nevertheless suggests ABA-co-induced MYC2 and subsequently MYC2-medi-
thattheJA–ABAinteractionmayexistatthisJAZ–NINJA ated defense-related genes in Arabidopsis (Lorenzo et al.
connection, downstream of JA biosynthesis, dependent on 2004; Zhu et al. 2011; Song et al. 2014a). Consequently,
the binding specificity of different JAZs to NINJA or disruptions of ET perception and signaling in etr1, ein2-1
ABPs. This is supported by the recent finding that andein3/eil1mutantsallincreaseArabidopsisresistanceto
ZmJAZ14, a JAZ protein in maize, is involved in both JA thegeneralistinsectsS.exiguaandS.littoralis,whereasET
and ABA signaling (Zhou et al. 2015). application results in plant susceptibility. ET signaling,
however,doesnotinfluencetheresponsesandresistanceof
ArabidopsistothespecialistsPlutellaxylostellaandPieris
ET in defense regulation rapae (Stotz et al. 2000; Mewis et al. 2005; Bodenhausen
and Reymond 2007; Song et al. 2014a).
LikeJA,ETsignalinguponfeedingbyinsectherbivoresis Recent findings also shed light on the mechanism of
common among plants. However, ET has very variable how these hormonal cascades interact (Fig. 2). Several JA
effects on defense regulation, acting more as a modulator signalingrepressorJAZsbindtoandinactivateEIN3/EIL1
of herbivore-induced responses than a direct elicitor (von and recruit HDA6 (histone deacetylase6) to repress EIN3/
Dahl and Baldwin 2007). Very few plant defenses are EIL1-dependent transcription (Zhu et al. 2011). Upon
directly regulated by ET. One known case is the induction herbivore-induced ET and JA accumulation, ET signaling
of defensive 1-cysteine protease (Mir1-CP) against both stabilizes EIN3/EIL1 while JAZ removal by JA signaling
chewing Spodoptera frugiperda and phloem-feeding disassociates HDA6-EIN3/EIL1 and activates EIN3/EIL1
Rhopalosiphum maidis in maize. JA also induces Mir1-CP to transcribe downstream ERF1/ORA59. Interestingly, the
expressionuponS.frugiperdafeeding,whichisdependent ABA-inducible MYCs also physically interact with EIN3/
on ET signaling, since MeJA treatment had no effect on EIL1, which mutually inhibits their function. Moreover,
Mir1-CP induction in maize plants with blocked ET sig- MYC2 indirectly promotes proteasomal degradation of
naling (Ankala et al. 2009; Louis et al. 2015). In many EIN3 by enhancing EBF1 expression (Song et al. 2014a;
cases, ET has been shown to modulate JA-mediated insect Zhang et al. 2014). This illustrates how the balance
defenses,similartothewell-documentedET–JAsynergism between ABA and ET signaling fine-tunes JA-mediated
in regulating defensive genes induced upon infestation by defenses induced by insect herbivory.
necrotrophicpathogens,suchasPDF1.2andPR1,4and5,
via their co-regulation of the AP2/ERF TFs ERF1 and
ORA59(Lorenzoetal.2003;Pre´etal.2008).Forexample, SA antagonizes herbivore-induced defenses
ET signaling contributes to the JA-mediated volatile
emission upon S. exigua herbivory on maize or Bemisia SA signaling mediates defense responses to hemi(-
tabaci infestation on Arabidopsis (Schmelz et al. 2003; biotrophic) pathogens (Derksen et al. 2013). This is
Zhang et al. 2013). The wound-induced expression of achievedviaitsreceptorandregulatorNPR1(nonexpressor
tomatoPIN2requiresbothintactJAandETpathways,but of PR genes1) and the action of two NPR1 homologs,
compromising ET signaling does not affect the M. sexta- NPR3andNPR4,whicharealsoSAreceptorsandmediate
increased PI transcript levels in N. attenuata (O’Donnell NPR1degradationinSA-concentration-dependentmanners
et al. 1996; Onkokesung et al. 2010a). The complex (Kuai et al. 2015). In some cases, SA-induced defense
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responses are effective against sedentary sucking insects, 2014). For example, GA signaling interacts with JA sig-
such as aphids (Klingler et al. 2009; Zhang et al. 2015b). naling via the negative regulators DELLAs. DELLAs and
SAaccumulationinhostplantscanbeinducedbyHAMPs JAZs directly bind and deactivate each other (Fig. 2; Hou
and can also be exploited by insects to suppress JA-me- et al. 2013; Song et al. 2014b). In the presence of GA,
diated defenses (Thaler et al. 2012; Caarls et al. 2015). DELLAs are degraded via the 26S proteasome, releasing
Glucose oxidase in S. exigua oral secretion induces an SA JAZs to suppress MYC2 (Hou et al. 2010; Wild et al.
burst in N. attenuata, which suppresses JA and ET accu- 2012). On the other hand, DELLAs are necessary to
mulation (Diezel et al. 2009). Moreover, several insects attenuate S. exigua-induced JA accumulation in Ara-
carry viruses or microbes that trigger SA accumulation. bidopsis, and consequently GA can promote JA biosyn-
Tomato spotted wilt virus transmitted by thrips feeding thesis (Cheng et al. 2009; Lan et al. 2014). Moreover, the
increases SA concentrations in Arabidopsis, resulting in DELLA protein RGA (repressor of GA1-3), binds to
increasedperformanceandpreferenceofthripsforinfected MYC2; its removal thus increases MYC2 activity (Hong
plants (Abe et al. 2012). Flagellin from Pseudomonas sp. et al. 2012). Another DELLA, RGL3 (RGA-like3), whose
present on the mouth parts of L. decemlineata can induce expression is enhanced by JA in a MYC2-dependent
SA accumulation in tomato leaves upon feeding, thereby manner, can competitively bind to JAZs and further
suppressing JA-dependent defenses, such as PIs and increase MYC2 activity (Wild et al. 2012). This JA-GA
polyphenol oxidases, and herbivore-induced resistance synergistic interaction plays a role in trichome initiation
(Chung and Felton 2011; Chung et al. 2013). and sesquiterpene biosynthesis (Hong et al. 2012; Qi et al.
The SA antagonism of JA-dependent defenses occurs 2014). Similarly, BRs, AUXs and CKs influence JA sig-
downstream of JA biosynthesis and independently of the naling both positively and negatively in regulating
COI1-JAZspathway.Itinhibitsdefensesmediatedbyboth responses to herbivores (Dervinis et al. 2010; Yang et al.
ABA and ET signaling (Fig. 2). Disruption of SA accu- 2011; Meldau et al. 2011).
mulation or NPR1 function thus increases resistance to In conclusion, interactions between hormonal signaling
several chewing and sucking insects (Stotz et al. 2002; cascades help plants to fine-tune their defenses against a
Mewis et al. 2005; Zarate et al. 2007). Cytosolic NPR1 specific attacker. Conversely, insects may have the ability
activity is also a mediator of the SA–JA antagonism, to interfere with these hormonal interactions to suppress
which, however, is bypassed if herbivores also induce ET defense responses to their benefit.
accumulation (Spoel et al. 2003; Leon-Reyes et al. 2009;
Van der Does et al. 2013). Moreover, SA leads to degra-
dationoftheJA/ET-responsiveORA59andsuppressesJA/ Hormonal regulation of plant responses to abiotic
ET-responsive GCC-box-containing genes, including stresses
ORA59, by recruiting the SA-induced GRX480 (Glutare-
doxin480) to their promoters. This inhibits the positive Due to its involvement in many developmental processes,
transcription regulators class II TGAs thereby repressing such as shoot growth inhibition, stomatal movement, leaf
JA/ET-induced responses (Zander et al. 2012, 2014; Van senescenceandprimaryrootgrowth,ABAisconsideredas
derDoesetal.2013).LessisknownabouthowSAinhibits a master regulator of responses to abiotic stresses, such as
JA/ABA-responsive defenses. Potential points of conver- drought, salt, heat and high light intensity (Fig. 3; Sharp
gence in this interaction are WRKY TFs. WRKY62 and et al. 2004; Daszkowska-Golec and Szarejko 2013; Liang
WRKY70 regulate the SA–JA antagonism in defense et al. 2014). JA, SA and BRs also interact with ABA to
responses and ABA-responsive defense genes (Li et al. promote stomatal closure, prevent water loss during
2004;Mao etal.2007),whereasWRKY18,WRKY40 and osmotic stresses, and induce leaf senescence for resource
WRKY60 are ABA-responsive and blocked by SA (Xu remobilization (Hossain et al. 2011; Miura et al. 2012; Qi
et al. 2006; Chen et al. 2010). et al. 2015). Stomatal opening, on the other hand, is pro-
moted by CKs and AUXs, while leaf senescence is inhib-
ited by GAs, CKs and AUXs (Daszkowska-Golec and
Growth hormones in defense regulation Szarejko2013;Jibranetal.2013).ETisalsoconsideredas
a major inducer of leaf senescence (Kim et al. 2015),
Recently, phytohormones such as gibberellins (GAs), whereas ABA and ET show a clear antagonism in regu-
brassinosteroids (BRs), auxins (AUXs) and cytokinins lating stomatal movement (Tanaka et al. 2005) and shoot
(CKs) have also been shown to modulate JA-mediated androotgrowthunderdrought(Fig. 3;SharpandLeNoble
responses to herbivores (Figs. 2, 3), besides their involve- 2002; Sharp et al. 2004; Yin et al. 2015). Similarly, ABA
ment in regulating defenses against pathogens (Naseem antagonizes ET in controlling flooding responses, such as
andDandekar2012;Denance´ etal.2013;DeBruyneetal. shoot elongation, leaf hyponasty and adventitious root
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Fig.3 Hormonal interactions regulating plant responses to abiotic defenses: ET induces defense responses to necrotrophic pathogens
stresses and defenses against biotic agents. Arrow heads indicate a and some responses to insect herbivores but suppresses other insect
positive interaction, whereas a T end, indicates an inhibitory effect. induced defenses. ABA and ET strongly antagonize each other in
Abscisicacid(ABA) hasstrongsynergisticeffectsonJA-dependent many responses, but both induce leaf senescence. Interactions
defenses,whilejasmonicacid(JA)promotesABA-mediatedstomatal between JA and gibberellic acid (GA) or auxin (AUX) to mediate
closure and leaf senescence, but not primary root growth. Dashed growth-defensebalancearealsoindicated
arrowsindicatethemixedeffectsofethylene(ET)onJA-dependent
formation (Voesenek and Bailey-Serres 2015). The ET- herbivorymayalsofollowthisstrategy.Thebestillustrated
mediated responses to flooding as well as shading, on the hormonal interaction to regulate growth-defense tradeoffs
other hand, are synergistically regulated by GAs, BRs and is between JA and GA. Similar to their interaction in
AUXs (Cox et al. 2006; Gommers et al. 2013; van Veen regulating defenses, JA also antagonizes GA-dependent
et al. 2013;PierikandTesterink 2014;Ayano et al. 2014). growthresponsesviaJAZs-DELLAs.IntheabsenceofJA,
These insights demonstrate that plant responses to abiotic ArabidopsisJAZ9bindstheDELLAproteinRGA,thereby
stresses and defense responses are controlled by the same preventing it from inhibiting the growth promoting TF
interactive hormonal network. PIF3 (phytochrome-interacting factor3). Upon herbivory,
JA induces JAZ degradation and delays GA-mediated
DELLA degradation, allowing DELLAs to inhibit GA-
Hormonal interactions regulate growth-defense dependent plant growth responses (Yang et al. 2012).
tradeoffs Furthermore, JA in concert with ET repress cell cycle
processes and expansion of leaf cells by suppressing the
The simultaneous roles of hormones in plant development cell expansion enhancers, AUXs. Conversely, AUXs were
and defense led to the view that they interact to prioritize proposed as repressors of JA synthesis and JA/ET-depen-
resources towards growth or defense. This is a relevant dent nicotine response. AUXs and JA, however, synergis-
concept when considering abiotic-biotic stress interaction, tically constrain N. attenuata regrowth after M. sexta
asabioticstressusuallyseverelyimpairsplantgrowth.The herbivory (Shi et al. 2006; Onkokesung et al. 2010b; Noir
probability to survive under adverse conditions may et al. 2013; Machado et al. 2013). ABA and JA signaling
increase if limited resources are efficiently allocated to also synergistically suppress plant growth and yield under
tolerate abiotic stresses or to defend valuable tissues drought stress (Kim et al. 2009; Harb et al. 2010). On the
against herbivores (Van Dam and Baldwin 2001; Skirycz other hand, ABA signaling antagonizes nicotine biosyn-
and Inze´ 2010; Atkinson and Urwin 2012; Vos et al. thesisinN.tabacumrootsviaPYL4,anABAreceptorthat
2013a). There is substantial evidence that this happens in controls root metabolic responses to drought and drought
case of pathogen attack (Denance´ et al. 2013; Huot et al. resistance;whereasJAsuppressesPYL4expressioninroots
2014); and the regulation of the growth-defense tradeoff but enhances it in leaves (Fig. 2; Lackman et al. 2011;
when plants are under combined abiotic stress and insect Pizzio et al. 2013; Gonza´lez-Guzma´n et al. 2014). These
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734 PlantMolBiol(2016)91:727–740
examples show that the growth-defense balance is tightly brassicae moth preference to lay eggs on drought-stressed
regulated by a sophisticated network of hormonal cross- plants but no differences in larval performance compared
talk. to those on well-watered plants. Interestingly, ABA accu-
Furthermore, the growth-defense balance can also be mulation was observed upon herbivory but not in drought-
controlled by master mediators that regulate multiple hor- stressed plants, possibly due to the intermittent drought
monal cascades. For example, the Arabidopsis CML42 stress regime with recovery periods, during which ABA
(calmodulin-like protein42) suppresses both JA-dependent catabolism may be induced (Wang 2002; Fleta-Soriano
insect resistance and drought-responsive ABA accumula- et al. 2015). In contrast, drought enhanced resistance of
tion; and the rice WRKY70 induces JA but represses GA Solanum dulcamara plants to S. exigua larvae (Nguyen
biosynthesis andsignaling (Vadassery et al. 2012;Li et al. et al. 2016). Both dought and herbivory induced ABA and
2015). However, the WRKY70-dependent prioritization of JAaccumulationinS.dulcamara.Transcriptomicanalyses
defenses over growth leads to resistance to the stem borer showed drought further enhanced several herbivore-in-
Chilo suppressalis but susceptibility to the brown plan- duced defense-related responses, such as terpenoid
thopper Nilaparvata lugens, suggesting that defense pri- biosynthesis and PIs (Nguyen et al. 2016). Similarly,
oritization is species-specific (Li et al. 2015). drought increased leaf ABA and JA concentrations, JA-
dependent defense and Medicago truncatula plant resis-
tance to the pea aphids Acyrthosiphon pisum (Gou et al.
Hormonal regulation of defense responses 2016).Therefore,thesynergisticinteractionbetween ABA
under combined stresses and JA signaling is suggested to play an important role in
regulating plant defense under drought. This is supported
Despite our extensive knowledge on hormonal regulatory by the finding that ABA signaling is required for the full
pathways and their interactions, predicting plant responses activation of VOC emission and JA-responsive direct
and phenotypes under combined biotic and abiotic stress defensesinN.attenuata(Dinhetal.2013).Silencingofan
remains difficult. Hormonal cascades may interact in non- ABA catabolism suppressor, NaHER1 (herbivore elicitor-
additive manners and the results may enhance plant toler- regulated1), in N. attenuata resulted in reduced levels of
ance/resistance to one stress but not to another (Atkinson thesedefenseresponsesuponherbivorybyM.sextaaswell
and Urwin 2012; Stam et al. 2014; Suzuki et al. 2014; asplantresistance.Moreover,NaHER1-silencedplantsare
Foyer et al. 2016). Also at the transcriptional level, stress alsodrought-sensitive,suggestingthatNaHER1servesasa
combinations evoke responses that are unique or unpre- connection between responses to the two stresses.
dictable from the responses to single stresses even if the Ontheotherhand,theremaybemechanismsunderlying
points of convergence are known (Rasmussen et al. 2013; plant increased resistance to herbivores under drought that
Atkinson et al. 2013). Abiotic stresses, such as drought, are independent of the ABA-JA signaling interaction. In
salt, heat or flooding, have been found to exert both posi- maize, drought and root herbivory by Diabrotica virgifera
tiveandnegativeinfluencesonresistancetopathogensand synergisticallyenhancelevelsofABAandABA-dependent
insect herbivores (DeLucia et al. 2012; Suzuki et al. 2014; defense gene transcripts in the leaves and resistance to the
Ramegowda and Senthil-Kumar 2015). For example, the leaf herbivore Spodoptera littoralis (Erb et al. 2011).
strong JA-ABA synergism in many stress responses sug- However, leaf water loss, but not the induced ABA level
gests that drought may promote plant resistance to herbi- itself, was strongly correlated to the resistance. Therefore,
vores. However, drought increases defense responses and hydraulic changes induced by drought and root herbivory
render plants resistant to insect herbivores in some cases, were suggested to play a role in inducing ABA/JA-inde-
butreducesdefensesandresistanceinothers(English-Loeb pendentsignalingthatincreasesresistancetoabove-ground
et al. 1997; Huberty and Denno 2004; Khan et al. 2010; herbivores.
Gutbrodtetal.2011;Tariqetal.2013;Nguyenetal.2016). Interestingly,thereismuchlessknowledgeontheeffect
Recently, a few studies have tried to dissect hormonal of soil flooding on herbivore resistance, possibly because
interactions occurring under simultaneous abiotic stress most model plants are crops and drought is more com-
and herbivory. In Brassica oleracea plants, drought and monly recognized as a problem in production systems
Mamestra brassicae herbivory interactively regulate the around the world than flooding or waterlogging. Only
emission of volatile organic compounds (VOCs) as an recently Lu et al. (2015) studied the hormonal interaction
indirect defense (Weldegergis et al. 2015). While drought between flooding and root herbivory in rice. The study
alone induces SA accumulation and reduces the emissions showed, however, that hormonal responses to root her-
of several VOCs, it also reduces herbivore-induced JA bivory or artificial wounding was not altered by flooding.
accumulation and consequently alters the herbivore-in- In S. dulcamara, soil flooding increased ABA, but not JA,
duced emissions of these VOCs. This resulted in M. levels in the leaves and suppressed many transcriptional
123
PlantMolBiol(2016)91:727–740 735
responses involved in primary and secondary metabolism, validate the ecological effects of these molecular interac-
including defense-related responses. These changes, how- tions. Given the common co-occurrence of abiotic and
ever, did not affect the plant resistance to S. exigua larvae biotic stresses, the response to stress combination is likely
(Nguyen et al. 2016). tobeunderstrongnaturalselection.Thus,wearguethatthe
These insights, though not always as expected before- seeminglylowlevelofconservationintheeffectofabiotic
hand, are invaluable to understand how plants fine-tune stressonherbivoredefenses,dependingonplantandinsect
their responses to specific combinations of stress condi- species, does not represent random output of the signaling
tions. Based on what we know about the interactions network. Rather, it may be the consequence of divergent
between hormones and a few experimental studies, we choices in prioritization and thus resource allocation that
suggest that drought in general may enhance resistance onlyappearuponcombinedstressapplication.Recognition
becauseofthesynergisticeffectofABAandJAsignaling. ofgeneral patterns thenrequiresavailabilityofalarger set
Drought and herbivory both significantly reduce plant ofdata.Preferably,experimentsshouldbecarriedoutusing
performance but when a drought period is followed by plant species thriving in both wet and dry habitats as well
herbivory,thenegativeeffectismorethanadditive(Davila as with a diverse natural herbivore community. This will
Olivasetal.2016).Thusitmaybefunctionalforadrought- allow us to ‘learn from nature’ whether plants can be
stressed plant to reduce additional damage by increasing selected to handle multiple stresses at the same time while
herbivore defenses. It should be stressed that the resulting maintaining a high performance.
effectontheherbivoremaydiffer,dependingonitslevelof
host plant specialization or feeding strategy (Foyer et al. Acknowledgments This project is funded by a grant (844.10.001)
in the ALW-Ecogenomics program from the Netherlands Organisa-
2016). On the other hand, flooding or waterlogging elicits
tionforScientificResearch(NWO).NMvDgratefullyacknowledges
the production of ET. The interaction of ET with herbi-
the support of the German Centre for Integrative Biodiversity
vore-induced responses is not as uniform as that found for Research(iDiv)Halle-Jena-LeipzigfundedbytheGermanResearch
ABA. Hence it can be expected that flooding has a neutral Foundation(FZT118).
ornegativeeffectonplantresistance.Itislikelythatplants
Authors contribution Duy Nguyen took the lead in writing this
surrounded by water (temporarily) do not receive as many
review, with active contributions of Nicole M. van Dam, Ivo Rieu,
herbivores as a plant on dry land. Therefore, it is con- andCelestinaMarianiduringthewritingprocess.
ceivablethatfloodedplantsmayincreasetheirperformance
Open Access This article is distributed under the terms of the
more if they invest in overcoming the negative effects of
Creative Commons Attribution 4.0 International License (http://crea
hypoxia, for example by producing aerenchymous adven-
tivecommons.org/licenses/by/4.0/), which permits unrestricted use,
titious roots (Dawood et al. 2016). distribution, and reproduction in any medium, provided you give
appropriatecredittotheoriginalauthor(s)andthesource,providea
linkto the Creative Commons license, andindicate ifchanges were
made.
Conclusions
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