Journal of Endocytobiosis and Cell Research (2015) 100-111 | International Society of Endocytobiology
zs.thulb.uni-jena.de/content/main/journals/ecb/info.xml
Journal of Endocytobiosis and
Cell Research
Improvement of root architecture under abiotic stress through
control of auxin homeostasis in Arabidopsis and Brassica crops
Branka Salopek-Sondi1, Stephan Pollmann2,
Kristina Gruden3, Ralf Oelmüller4 and Jutta
Ludwig-Müller5*
1RuđerBoškovićInstitute,Zagreb,Croatia; 2CentrodeBio‐
tecnologíayGenómicadePlantas,Madrid,Spain; 3National
Institute of Biology, Ljubljana, Slovenia; 4Institute for Gen‐
eralBotanyandPlantPhysiology,Friedrich‐SchillerUniver‐
sityJena,Dornburgerstr.,159,07743Jena,Germany;5Insti‐
tutfürBotanik,TechnischeUniversitätDresden,Helmholtz‐
straße10,01069Dresden,Germany;
*correspondenceto:Jutta.Ludwig‐Mueller@tu‐dresden.de
Auxinplaysanimportantroleinmanyaspectsofplant
development including stress responses. Here we
brieflysummarizehowauxinisinvolvedinsaltstress,
drought (i.e. mostly osmotic stress), waterlogging and
nutrientdeficiencyinBrassicaplants.Inaddition,some
mechanismstocontrolauxinlevelsandsignalinginre‐
lationtorootformation(understress)willbereviewed.
Molecular studies are mainly described for the model
plant Arabidopsis thaliana, but we also like to demon‐
stratehowthisknowledgecanbetransferredtoagricul‐
turally important Brassica species, such as Brassica
rapa, Brassica napus and Brassica campestris. Moreo‐
ver,beneficialfungicouldplayaroleintheadaptation
responseofBrassicarootstoabioticstresses.Therefore,
thepossibleinfluenceofPiriformosporaindicawillalso
be covered since the growth promoting response of
plantscolonizedbyP.indicaisalsolinkedtoplanthor‐
mones,amongthemauxin.
JournalofEndocytobiosisandCellResearch(2015)100‐111
Category:Review
Keywords:Auxin,rootdevelopment,abioticstress,Brassicae
Accepted:19November2015
____________________________________________________________________ Introduction
Plantdevelopmentisdependentontheavailabilityofwater
andnutrientsinagivengrowthhabitat.Severedisbalances
inthesoilstatussuchaselevatedsalinity,nutrientdeficien‐
cies,andcriticalfluctuationsinwatercontentusuallycaused
byclimatechanges(droughtandwaterlogging),determined
asabioticsoilstressesorbelow‐groundstresses,affectplant
developmentandcropproductivity.Plantshavedeveloped
differentmechanismstorespondtoenvironmentalchanges
by employing plasticity in their growth and development.
These molecular mechanisms define a multi‐dimensional
100
network of gene regulation, environmental signal sensing,
signaltransduction,signalresponsesandphenotyperealisa‐
tion(YiandShao2008).Theplantrootisdirectlyexposedto
below‐groundstresses,andresponsibleforsensingandre‐
sponding to such unfavorable environmental conditions.
Theresponsesofplantstoabioticstressincludenumerous
endogenous signals that coordinate processes within the
roottissue,butalsobetweenrootandsubsequentshoottis‐
suesinordertoachievestressadaptationwithinthewhole
plant.Therefore,theimprovementoftherootresponseswill
alsoresultinlargeraerialplantpartsunderabioticstresses
translatingeventuallyintohigheryield.
Improvementofrootarchitectureiscentralfortheadap‐
tationofplantstoabioticstress.Amongthecrucialregula‐
tors in controlling these adaptation processes are rather
simple indolic compounds called auxins. These hormones
areparticularlyimportantforrootadaptationprocessesin
Brassicacrops.Thus,thequestionariseswhetheritispossi‐
bletoobtainbetterresistanceagainstabioticstressinBras‐
sica species by co‐cultivation with the endophyte P. indica
sincethefunguschangestheauxinhomeostasisintheroots
(Leeetal.2011;Dongetal.2013).
Thespatiotemporalcontrolofauxinlevelsiscrucialto
thedevelopmentofplants;inparticular,totheproliferation
of the plant root system. This kind of control cannot be
achievedbydirectedandundirectedauxintransportalone,
but rather has to include biochemical processes that are
known to alter cellular auxin levels. A set of interesting
genesspecificallycontributingtoindole‐3‐aceticacid(IAA)
conjugationanddeconjugationaswellasanumberofauxin
biosynthesisgenesthathavebeenshowntobeexpressedin
rootsandtobeaffectedbyanumberofdifferentstresscon‐
ditionsplayimportantrolesinthecontrolofrootdevelop‐
ment.ThemodelsystemBrassicacanadapttoenvironmen‐
talstressconditionsbyoptimizingtherootarchitectureand
itscommunicationwiththeshootbycocultivationwiththe
root‐colonizingendophyteP.indica.Thisadaptationprocess
ismediatedbyre‐adjustmentoftheauxinhomeostasisand
that this is mainly caused by local increase in auxin levels
(Sirrenbergetal.2007;Vadasseryetal.2008;Schäferetal.
2009;Hilbertetal.2012,2013;Leeetal.2011,Dongetal.
2013).
Auxinhomeostasisandabioticstress
Whatistheexactroleofauxininregulatingabioticstressre‐
sponsesandhowcanmanipulationoftheauxinhomeostasis
generatemoreabioticstresstolerantinBrassicaplants?P.
indica‐inducedadaptationprocesstodroughtstress,e.g.,re‐
sultsinmoreresistantplantswith>20%increaseinbiomass
andseedproduction,whichisassociatedwithamassiveal‐
terationoftherootarchitecture,root‐shootcommunication
andlocalauxinlevels(Peškan‐Berghöferetal.2004).These
Journal of Endocytobiosis and Cell Research VOL 26 | 2015 Root architecture under abiotic stress, Salopek-Sondi B et al.
processesaretriggeredbyalow‐molecularmasselicitorre‐
leasedbythefungusintotherhizospherethattargetsplant
auxinmetabolisminBrassicacrops(Vadasseryetal.2009a;
Lee et al. 2011; Dong et al. 2013). Expression profiles of
auxinbiosynthesisandmetabolismgenesunderstresscon‐
ditions can be compared with global gene expression pro‐
filesobtainedunderabioticstresstreatmentsandafterP.in‐
dicacolonizationinthemodelplantArabidopsisthalianaand
thecropplants Brassica rapaand Brassica napusbyasys‐
temsbiologyapproach.Targetgenescanbeidentifiedwhich
couldbeusedasmarkersforbreedingstrategies.Differen‐
tial display identified many P. indica‐stimulated genes for
regulatoryproteinsinroots(Vahabietal.2015).Interesting
candidategenesarealsoregulatedbyauxin,althoughexog‐
enousauxinapplicationtoBrassicarootsdoesnotinduces
theroothairphenotype.
Root system architecture is mainly determined by the
complexinterplayofseveralplanthormones,e.g.auxin,eth‐
ylene(ET),andcytokinin.Inthisnetwork,auxiniselemen‐
tarytotheformationoflateralroots,whichlargelycontrib‐
utetotheplasticityoftherootsystem.Thecontrolofroot
branchingdeterminestheexpansionoftherootsystemand,
thus,theareaofsoilpenetratedbyaplant.Togetherwiththe
obviousincreaseintheabsorbing‐activesurface,thisiscru‐
cial for optimal waterlogging and nutrient uptake via the
root system. The potential to take up water and dissolved
saltsfromtherhizosphereessentiallydecidesonthebiolog‐
icalfitnessofaplant.Itmightbepossibletostudythesepro‐
cessesbyusingP.indica,whichinducesamassivestimula‐
tionofroothairdevelopment,bothinPetridishesandnatu‐
ralsoil.
Theplasticityofplantdevelopmentanditspotentialto
adapttoconstantlychangingenvironmentalconditionsim‐
ply that the underlying regulatory mechanisms are highly
complex.Inthisrespect,thedifferentialdistributionofauxin
withinagiventissue,i.e.theformationoflocalauxinmaxima
orgradients,isaparticularlyimportantregulatorymatter.
Auxingradientshavebeenimplicatedinnumerousdevelop‐
mentalprocesses,forexample,patternformation,embryo‐
genesis,andtropisms.Sofar,theformationofauxingradi‐
ents has been attributed to two different processes, local
auxinbiosynthesis(Zhao2010)anddirectionalintercellular
auxin transport (Tanaka et al. 2006). Both processes are
tightlycontrolledbyawealthofbioticandabiotic,aswellas
developmentalsignals. Hence,the controlof cellular auxin
formationanditsdistributionprovidesavaluablemeansto
efficientlytranslateinternalandexternalsignalsintoplant
growth responses. Basically any plant cell is assumed to
have the ability to perceive auxin signals, including root
cells.
Auxininrootdevelopment
Overthepastyears,mostworkhasbeenfocusedontheelu‐
cidationofmolecularmechanismsbywhichtheintegration
ofauxinsignalsinrootsisrealized.Thestudiesprovidedev‐
idence for a number of short signal transduction cascades
thatgovernrootgrowthresponsesbytranscriptionalrepro‐
gramming of responding cells. Herein, they control both
priming of pericycle cells to become lateral root founder
cellsandactivationofasymmetricalcelldivisionsastheini‐
tialstepoflateralrootformation.Thepathwaysinvolvean
auxin specific receptor, an Fbox protein named TIR1, and
several transcriptional repressors of the Aux/IAA family,
whicharetargetedforproteolysisbythereceptorcomplex.
Journal of Endocytobiosis and Cell Research VOL 26 | 2015
The Aux/IAAs orchestrate the activity of a group of tran‐
scriptionfactors,mainlyfromtheARFfamily(DeRybeletal.
2010;Overvoordeetal.2010).Alongsidethesesignaltrans‐
ductionandtranscriptioncontrollingprocesses,directional
auxintransporthasbeenextensivelystudiedoverthepast
coupleofyears.MembersofthePIN‐formed(PIN)protein
family have been shown to govern auxin efflux in plant as
well as in heterologous systems (Grunewald and Friml
2010).However,ithasalsobecomeincreasinglyclearthat
localauxinbiosynthesisiscrucialtothegenerationoflocal
auxinmaxima.Thisholdstruenotonlyforpatternformation
inaerialplantorgans,butalsoforroots,asnumerousgenetic
andpharmacologicstudiesrevealedthatauxincanbesyn‐
thesizednotonlyinleavesandshootapicalmeristems,but
alsoinroottissues(Mülleretal.1998;Ljungetal.2001;Pe‐
terssonetal.2009;Hentrichetal.2013a).Likewise,IAAcon‐
jugationhasbeenshowntocontributetothecomplexregu‐
lationofrootdevelopment(KhanandStone2007;Zhanget
al.2007).Ingeneral,asophisticatednetworkofseveralbio‐
chemical reactions including de novo biosynthesis, for‐
mationanddecompositionofIAAsugarandIAAaminoacid
conjugates, and translocation processes control cellular
auxin levels. Each of these reactions is differentially regu‐
lated and can respond to environmental triggers in an ap‐
propriatemanner.
Auxinconjugatesarethoughttoplayimportantrolesas
storageformsfortheactiveplanthormoneIAA.Initsfree
form, IAA comprises only up to 25 percent of the total
amountofIAA,dependingonthetissueandtheplantspecies
studied.ThemajorformsofIAAconjugatesarelowmolecu‐
larweightesteroramideforms,butthereisincreasingevi‐
denceontheoccurrenceofpeptidesandproteinsmodified
byIAA(reviewedinLudwig‐Müller2011).Sincethediscov‐
eryofgenesandenzymesinvolvedinsynthesisandhydrol‐
ysisofauxinconjugates,muchknowledgehasbeengained
on the biochemistry and function of these compounds. In
mosttissuestheauxinresponsesareconcentrationdepend‐
entanddifferenttissuesrespondinadistinctmannertovar‐
yingamountsofexogenousauxins(Thimann1938).Higher
auxinconcentrationsmightbeofteninhibitory,sotheopti‐
mumendogenouslevelmustbetightlycontrolled.Thistight
controlofauxinhomeostasisisalsoinvolvedintheregula‐
tionofrootgrowthsinceprimaryrootgrowthisinhibitedby
high auxin levels, but lateral root initiation is triggered by
localmaximaofauxin.Forexample,mutantsinGH3‐9,apro‐
teinbelongingtoclassIIenzymesofauxinconjugatesynthe‐
tases,displayedashorterrootphenotypeandhighersensi‐
tivity to auxin‐regulated root growth, indicating a role for
GH3‐9inrootdevelopment(KhanandStone2007).Another
example provides the symbiosis of P. indica with an Ara‐
bidopsis auxin overproducer, where the fungus promotes
growthbyconvertingfreeauxinintoconjugates(Vadassery
etal.2008).
Indicationsforfunctionsofauxinconjugationinabiotic
stressresponsescomefromworkwithavarietyofplantspe‐
cies.Junghansetal.(2006)foundanauxinconjugatehydro‐
lase from poplar in salt stressed tissue. Overexpression of
PcILL3inArabidopsisalsorenderedthesetransgeniclines
moresalttolerant.Duringawaterloggingexperimentwith
soybean,aputativeauxinconjugatehydrolasewasfoundto
be upregulated (Alam et al. 2010). Furthermore, tempera‐
turesensitivecellsofhenbanehadalteredauxinconjugate
levels(OetikerandAeschbacher1997).GH3auxinconjugate
synthetase genes are also directly involved in stress toler‐
ance.WES1(GH3‐5)forexamplewasalsoinducedbyvarious
stressconditionssuchascold,droughtandheattreatment
101
Root architecture under abiotic stress, Salopek-Sondi B et al. aswellasbythestresshormonessalicylicacid(SA)andab‐
scisicacid(ABA).ItisinterestingtonotethatWES1cannot
only adenylate IAA but also SA (Staswick et al. 2005). A
WES1overproducingline(wes1‐D)wasresistanttoabiotic
stressessuchasdrought,freezingandsalt,butalsohightem‐
peratures (Park et al. 2007), whereas a T‐DNA insertional
mutant showed reduced stress resistance. In addition,
stress‐responsive genes were up‐regulated in the wes1‐D
mutant.Interestingly,CBF(C‐repeat/dehydration‐responsive
element‐binding factor) genes were directly regulated by
auxin(repressedbyIAA),andtherepressionwasattenuated
inthelinewithhigherauxinconjugateformation(Parketal.
2007).
Rootarchitecturalalterationbyanendophyte
As already insinuated, a potential help for optimizing the
rootarchitectureunderabioticstressconditionsmightpro‐
videthesymbiotic,root‐colonizingendophyticfungusP.in‐
dica,abasidiomyceteoftheSebacinales.Thisprimitivefun‐
gusinteractsalsowiththemodelplantA.thaliana.P.indica
isacultivablefungusandcangrowonsyntheticmediawith‐
outahost(Peškan‐Berghöferetal.2004).P.indicapromotes
nitrateandphosphateuptakeandmetabolism(Shahollariet
al. 2005; Sherameti et al. 2005; Yadav et al. 2010), allows
plantstosurviveunderwaterandsaltstress(Sherametiet
al.2008a;Baltruschatetal.2008;Sunetal.2010),andstim‐
ulates growth, biomass and seed production (Verma et al.
1998; Shahollari et al. 2004, 2005; Sherameti et al. 2005,
2008b;Vadasseryetal.2008;Walleretal.2005,2008;Oel‐
müller et al. 2009). In Arabidopsis and Chinese cabbage
(Brassicarapa)growthpromotioncanalsobeachievedby
an exudate component released by the fungus into its cell
wallandintothegrowthmedium(Vadasseryetal.2009a;
Leeetal.2011).Thisandotherdatasupporttheconceptthat
(an)elicitorreleasedbythefungusisperceivedbythehost
cell,activatingareceptor‐mediatedsignallingpathway.Phy‐
tohormonesandtheirhomeostasisintherootsarecrucial
forP.indicaeffectsinplants(Sirrenbergetal.2007;Vadas‐
seryetal.2009b;Schäferetal.2009;Leeetal.2011;Donget
al. 2013). The exudate component induces massive root
branching,andresultsinamorethan2‐foldincreaseinthe
auxinlevelintheroots(butnotintheshoots)ofChinesecab‐
bage seedlings (Lee et al. 2011). Furthermore, the aerial
parts of these plants are significantly more resistant to
drought (Sun et al. 2010). Since exogenous application of
auxintoChinesecabbagerootscannotreplacethebeneficial
effectsofthefungus,characterizationofthealreadyidenti‐
fiedP.indica‐andauxin‐relatedtargetsof P. indicainChi‐
nesecabbagerootsmightcontributesubstantiallytothebet‐
terunderstandingofthisscenario.
Recentpublicationshaveemphasizedthatatightcontrol
oflocalauxincontentsishighlyimportantfortheregulation
of root development. This requires sophisticated mecha‐
nisms,whichcontrolauxinbiosynthesis,andthehydrolysis
ofauxinconjugatesinrootsduringabioticstress.Thebene‐
ficialgrowth‐promotingfungusP.indicainducesstresstol‐
eranceandrootgrowthbycontrollinglocalauxinlevelsand
auxinrelatedprocesses, providingatooltoinducethede‐
sired phentype, which can be studied with the aim of bio‐
technologicalapplications.Howrootsperceiveandrespond
tobelow‐groundabioticstresses,andhowtherootarchitec‐
tureisadaptedtothenovelconditionsintermsofdevelop‐
ment,root‐shootcommunicationandinteractionswiththe
bioticenvironmentisstillunclear.Theresponseismediated
102
byadaptationoftheauxinhomeostasistochangerootdevel‐
opmentinresponsetoabioticstresses.Theperceptionofthe
signal by P. indica trigger auxin response pathways under
normalgrowthandstressconditions,resultinginenhanced
abioticstresstolerancetraitsofthecolonizedplants.Inad‐
dition,P.indicaprotectstheplantsystemicallyunderstress
using root to shoot communication, which is achieved by
takingadvantageoftheplant’ssignalingpathways.Thisgen‐
eratesastronginteractionoftheplantrootswiththeenvi‐
ronmentalsoil.Responsetochangingenvironmentsandad‐
aptationoftherootstothesenovelconditionsrequirespri‐
marily(local)increaseinauxinlevels.Changesinauxinho‐
meostasis, i.e. via biosynthesis and release from inactive
conjugatesmightbeadirectorindirectconsequenceofP.in‐
idca colonization. P. indica confers stress tolerance to Chi‐
nese cabbage roots via changes in the auxin homeostasis.
Moreover,thefungusutilizesseveralplanthormonesignal‐
ingpathwaystoconferincreasedtoleranceandthusinflu‐
ences the hormonal networks in roots under given stress
conditions(Schäferetal.2009;Sunetal.2014).
Four kinds of abiotic stresses impairing plant growth
andbiomassproductionplaymajorrolesinagriculture:salt
stress, drought, waterlogging and nutrient deficiency. In
termsofnutrientdeficiency,phosphate(P)deficiencystud‐
ieshavedemonstratedthatlimitingPconditionshavedra‐
maticimpactonrootarchitecture.Theeffectisgovernedby
theinterplayofauxin‐dependentcellcyclecontrol,modula‐
tion of auxin perception, and auxin accumulation (López‐
Bucio et al. 2005; Sánchez‐Calderón et al. 2005; Pérez‐
Torresetal.2008;Miuraetal.2010).Additionally,asout‐
linedabove,P.indicapromotesPuptake(Yadevetal.2010;
Kumaretal.2011;Molitoretal.2011;Petersenetal.2013;
Dasetal.2014).Thissuggestsalinkagebetweenthebenefi‐
cialpropertiesattributedtothesymbiosisofthehostplant
withtheendophyteandtheinfluenceontheauxinlevelin
thecourseoffungusinfection.However,theselectedkinds
ofstressarecausingsevereproblemsinagricultureandre‐
ducecropyieldsallovertheworld.Itisestimatedthatcon‐
siderablelossesincropproductivity(morethan50%)are
causedbyabioticstresses(Qinetal.2011);hence,threaten
thefoodsecurityworldwide.throughoutEurope.Over6%of
thegloballandareahasestimatedtobeaffectedbysalinity,
64% by drought, 13% by flooding, and about 57% by ex‐
tremetemperatures(MunnsandTester2008;Crameretal.
2011;Ismailetal.2014).Inthelastfewyearswaterlogging
becameatopicarisingconsiderablepublicandscientificat‐
tentioninCentralEurope,wherelargerainfallsresultedin
riversoverflowedmoreoftenthaninthepast.Membersof
theBrassicaceaearefoundmoreorlessallovertheworld
and represent a large number of economically important
plantculturecrops.Brassicavegetableslikecabbages,broc‐
coli, turnip greens and leaf rape, among others, are con‐
sumedthroughouttheworld.FAOStatistics(FAOStat2013)
showedthattheproductionofcabbagesandotherbrassicas
was6.3%,and8%ofthetotalvegetableproductionofthe
world, and European Union, respectively, in 2013. The
model plant A. thaliana can be used to elucidate general
mechanismsbyfunctionalandgeneticanalysis.
In conclusion, understanding auxin homeostasis‐based
networks that govern the outcomes of plant growth re‐
sponsestoanumberofdifferentabioticstressconditionsin
rootsisanimportanttaskforthefuture.Theresultswillbe
of great significance for studies of crosstalk signaling not
onlyinplant‐pathogenbutalsoinplant‐stressinteractions.
Thebroadermeritcouldresultinimprovedstressresistance
Journal of Endocytobiosis and Cell Research VOL 26 | 2015
Root architecture under abiotic stress, Salopek-Sondi B et al.
incorporatedintocommerciallinesthatisofgreatandim‐
mediate significance for the general public, seed industry,
oilseed rape growers and breeders. Ultimately, improved
stresstoleranceisexpectedtoleadtoincreasedseedyield
andbiomassproduction.Withthebackgroundknowledgeof
asteadyrisingdemandforagriculturalproductsandlimited
resources (arable land), this is and will become an even
more important matter of concern. Achievement of these
goalsispossible,asdemonstratedbyP.indicacolonization,
howeverourpresentknowledgeabouttheauxintargetsof
the fungus prevents the development of biotechnological
applicationaltools.
Howtocontrolauxinsignalling,biosynthesisand
metabolism
Unlikeanimals,plantsremainfixedinoneplaceabsorbing
wateraswellasmicro‐andmacronutrientsfromtheirenvi‐
ronment.Therootsystemplaysahighlyimportantrolein
thiswayoflife.Ontheonehand,itservesastheorganofab‐
sorptionforwateranddissolvedsalts;ontheotherhand,it
is the organ of attachment, anchoring the plant to the
ground.Asplantshavetocopewithever‐changingandoften
adverseenvironmentalconditions,theyremainedtheability
torespondtochangesinnutrientandwateravailability,as
wellastoanswerbioticandabioticstresscues.Ingeneral,
optimizingthemetabolismoradaptingthebodyplantothe
given environmental demands mediates these responses.
Withrespecttotherootsystemarchitecture,eitherincreas‐
ingordecreasingthevelocityofrootgrowthandexpansion
achievesthelatter.
Abioticstressresultsinaseriesofmorphological,physi‐
ological,biochemical,andmolecularchangesthatadversely
affect plant growth and productivity (Wang et al. 2001).
Muchabioticstresses,e.g.drought,salinity,orextremetem‐
peratures, appear to be interconnected and seemingly in‐
ducesimilarcellulardamage.Asanexample,droughtandsa‐
linityaredisclosedprimarilyasosmoticstress,resultingin
thedisruptionofhomeostasisandiondistributioninthecell
(Serranoetal. 1999;Zhu2001).Asaconsequence,thedi‐
verse environmental stress cues often activate similar cell
signalling cascades (Shinozaki and Yamaguchi‐Shinozaki
2000;KnightandKnight2001;Zhu2002)andtriggersimilar
cellularresponses,suchastheproductionofstressproteins,
up‐regulationofanti‐oxidants,andaccumulationofcompat‐
ible solutes (Vierling and Kimpel 1992; Zhu et al. 1997;
CushmanandBohnert2000).Likewise,theyinducealtera‐
tionofplanthormonehomeostasis,inparticularofABAand
jasmonicacid(JA)(Chavesetal.2003;CreelmanandMullet
1995;Dombrowski2003),which,inturn,translatesintoad‐
aptation of the plant developmental program. Due to the
high degree of developmental plasticity, plants are able to
respond by completing their life cycle before prevalent
stressconditionscausephysiologicaldeficits.However,such
prematurecompletionofthelifecycletoensuresurvivalof
theprogenyleadstoasignificantlossinplantproductivity.
ExperimentsemployingtheendophyticfungusP.indicapro‐
videdevidenceforasignificantlyincreasedstresstolerance
andproductivityofinfectedplants,indicatingthatthereign
ofgrowthinhibitingplanthormonescanbebroken.Itisbe‐
comingincreasinglyclearthatthefungusproducesitsbene‐
ficialimpactbymanipulatingauxinhomeostasis,buttheun‐
derlyingmolecularmechanismshaveyettobedisclosed.
Research on abiotic stress involved the screening for
mutants directly affected in individual stress components
suchassaltordroughtorwaterlogging,etc.Bythisapproach
Journal of Endocytobiosis and Cell Research VOL 26 | 2015
individualcomponentsofaparticularstresspathwayhave
beenidentifiedamongthemtransportersforsodium(Qiuet
al.2004)ormembersofsignaltransductionchains(Gonget
al.2002).However,therootarchitecturehasbeenneglected
asacommontargetinthesestudies.Theidentificationofa
singlecomponenttransferringstresstolerancetoonlyone
stressistheresultofthesestudies.Ontheotherhand,im‐
provingtherootarchitectureasawholeinresponsetoava‐
rietyofstressesandstresscombinationswillresultinplants
tolerant to more than one abiotic stress situation. To im‐
provetherootsystembyusingnaturalcompounds,i.e.aux‐
ins will be important for the understanding root develop‐
ment. So far, the involvement of auxins as signaling mole‐
culesinplantstressresponsesisonlypoorlyexploited.How‐
ever,therearealreadyafewlinesofevidencefromgenomic
studiesthatindicateacontributionofauxininthisprocess
(Sreenivasuluetal.2007;Wangetal.2010;Dombrechtetal.
2007;Hentrichetal.2013a).Inthiscontextitisimportant
to analyse also hormonal crosstalk between stress and
growth‐relatedhormonesasoneaspecttoidentifycombina‐
tionsincreasingstresstolerance.
Theinitiationoflateralrootsisofparticularimportance
fortheabsorptionefficiencyofaplant,asitdirectlydeter‐
minestheactivesurfaceoftherootsystem.Plantsproduce
neworgans,suchaslateralroots,primarilypostembryoni‐
cally. The formation of these new lateral organs proceed
fromrudimentaryformedfoundercellsthatfollowaprecise
pattern, which guarantees an even and optimal spacing of
thelateralrootsthatcontributestothefunctionalityofthe
newlyformedplantorgans.Althoughseveraldifferentcom‐
poundsareknownasplanthormonesandtocontributeto
plantstressresponses,eitheractingindividuallyorincross‐
talkwithotherphytohormones(Davies2004),plantshape
islargelycontrolledbyauxins(VannesteandFriml2009).In
roots,bothprimingofthelateralrootfoundercellsaswell
asinitiationoftheasymmetricaldividingofthesepericycle
cellsandtheirdevelopmentispredominantlygovernedby
auxin,andanumberofAUXINRESPONSEFACTORS(ARFs)
and AUXIN/INDOLE‐3‐ACETIC ACID (Aux/IAA) proteins
thatactasinhibitorsoftheARFs.
It has been reported that the control of lateral root
founder cell identity is facilitated by an IAA28‐dependent
auxinsignallingmoduleinthebasalmeristemregionofthe
primaryrootthatregulatestheexpressionofthetranscrip‐
tionfactorGATA23thatseeminglyplaysakeyroleinspeci‐
fying pericycle cells to become lateral root founder cells
priortolateralrootinitiation(DeRybeletal.2010).Lateral
rootinitiationitself,islargelymaintainedbytheSOLITARY
ROOT (SLR)/IAA14‐ARF7‐ARF19 auxin response system
thatisnecessaryforproperactivationofthebasiccellcycle
machineryandforthecontroloftheinitial,asymmetricper‐
icyclecelldivisions(Fukakietal.2002;Vannesteetal.2005;
FukakiandTasaka2009).
Ascanbetakenfromthesefewexamples,thedynamic
andspatiotemporalpresenceofIAAaswellastheabilityto
perceiveandintegratethissignalhastobetightlycontrolled,
inordertoenableappropriategrowthoftherootsystem.Ex‐
tremelysimplified,itcanbeassumedthatlowIAAcontents
translateintoarepressionoflateralrootformation,whileel‐
evatedlevelsofIAAresultinanincreasednumberoflateral
rootfoundercellsand,hence,anincreasednumberoflateral
roots.Thissummaryisnotentirelycorrect,though,sinceit
is well‐knownthat, especially in roots, high IAA levels can
havegrowthinhibitoryeffects(Thimann1938;Ivanchenko
etal.2010).Nevertheless,itprovokesthecrucialquestion
onhowcellularauxinlevelsarecontrolled.Onemajoraspect
103
Root architecture under abiotic stress, Salopek-Sondi B et al. inthegenerationoflocalauxinmaximaissurelythecell‐to‐
celltransportofIAAbypolarlocalizedauxinexportersofthe
PIN‐FORMED (PIN) family and some evenly distributed
ATP‐bindingcassettesubfamilyB(ABCB)‐typetransporters
of the multidrug resistant/phosphoglycoprotein (ABCB/
MDR/PGP) protein family. Accompanied are these trans‐
portersbyauxinimportersoftheAUX1/LAXfamily(Petra‐
sekandFriml2009).However,severalrecentstudieshave
ledtothediscoverythatalsolocalauxinbiosynthesisiscru‐
cialtomanydevelopmentalprocessesincludingpatternfor‐
mation, gametogenesis, embryogenesis, seedling growth,
andflowerdevelopment(Zhao2010).Moreover,ithasbeen
suggested that the release of free auxin from auxin‐conju‐
gatesadditionallycontributestovariousdevelopmentalas‐
pects(Ludwig‐Müller2011;seeFigure1).
Figure1:Pathwaystoregulateauxinhomeostasisbybiosynthesis
andconjugation.
Regulationofauxin
Despitethemountingknowledgeoftheprocessesgoverned
byauxinsandofauxintransport,thebiosynthesisofIAAis
stilluncertain.IAAbiosynthesisissuggestedtoproceedvia
anumberofdifferentmetabolicroutes.Uptodate,onlyone
oftheproposedpathwaysisfullydisclosedwithrespectto
thecatalyzedreactionstepsandtheenzymesinvolved.How‐
ever,itisproposedthatthedifferentpathwaysacteitherin
parallelorredundantlytooneanother,inadevelopmentally
regulatedmanner(Zhao2010).InA.thaliana,comprehen‐
sive mutant analyses have implicated two major biosyn‐
theticpathwaysinauxinbiosynthesis;theseeminglypreva‐
lentIAA‐biosyntheticpathwaythattakesatryptophanami‐
notransferase(TAA1/SAV3)dependentroute(Stepanovaet
al.2008;Taoetal.2008),whichproceedsviaafinalYUCCA
(YUC)monooxygenase‐likefamily‐dependentreactionstep
(Zhaoetal.2001;Mashiguchietal.2011;Wonetal.2011;
Stepanova et al. 2011), and the CYP79B2/B3 cytochrome
P450 monooxygenase family‐dependent pathway (Zhao et
al. 2002; Sugawara et al. 2009). The lack of CYP79B2/B3
homologs in genera other than Arabidopsis and very few
closelyrelatedspeciesmostlikelyrestrictsthelatterpath‐
waytotheBrassicaceaefamilyandcontradictawidespread
104
distribution of this route within the plant kingdom (Quit‐
tendenetal.2009;Sugawaraetal.2009).Besidestheabove‐
mentioned biosynthetic pathways, several other publica‐
tionsreportedtheoperationofanIAMhydrolase‐dependent
pathwaytooccurinplanta(Pollmannetal.2003;Araietal.
2004; Nemoto et al. 2009). Especially the identification of
IAMasanendogenouscompoundinArabidopsis(Pollmann
etal.2002),andthesubsequentisolationandcharacteriza‐
tionofanIAMhydrolase(AMI1)fromthisspecies,butalso
severalothermonoanddicotspecies,implicatedthefunc‐
tionalityofsuchapathwayinplants(Pollmannetal.2003,
2006;Neuetal.2007;Sánchez‐Parraetal.2014).
Various features in root architecture such as in‐
crease/decrease of primary root length, number of lateral
rootsandroothairsallareconnectedtorootsurfacewhich
affectsviabilityoftheupperpartoftheplant.Auxinsplaya
major role in root growth and development, and
thus also in abiotic stress tolerance. In additon to
auxinseveralotherplanthormonesareinvolvedin
thecontrolofrootdevelopment,suchascytokinin,
JAs,andET.
Previous research characterized the first de‐
scribed IAM hydrolase from plants, referred to as
AMIDASE1(AMI1)(Pollmannetal.2003,2006;Neu
etal.2007).TheArabidopsisAMI1showshighho‐
mology to bacterial iaaH auxin biosynthesis en‐
zymesfromplantpathogens,suchasPseudomonas
and Agrobacterium. Metabolic and genetic studies
haveunderlinedthecontributionofAMI1toauxin
biosynthesisinplanta,too(Lehmannetal.inrevi‐
sion). The induced ectopic expression of AMI1 re‐
sultsinauxin‐relatedmutantphenotypes,i.e.short
primary roots, reduced growth, and curled leaf
shapes. Moreover, the overexpressors have in‐
creased IAM hydrolase activities, and elevated en‐
dogenousIAAcontents.Promoterreporterlinesas
wellasqRT‐PCRexperimentsrevealedstrongAMI1
expressionduringseedlingdevelopmentandinpro‐
liferating tissues (Pollmann et al. 2006; Hoffmann et al.
2010;Lehmannetal.inrevision),resemblingtheexpression
pattern of other auxin biosynthesis genes, such as YUC4,
TAA1, and CYP79B2, and of the synthetic auxin reporter
DR5::GUS(Ulmasovetal.1997;Mikkelsenetal.2000;Cheng
etal.2007;Taoetal.2008).Besidesseveralbioticcues,nu‐
merousabioticstimulihavebeenobservedtoregulatethe
expression of AMI1. In particular, salt stress has been re‐
ported to significantly up‐regulate the expression of AMI1,
whereashighsugarcontentshavebeenshowntosuppress
AMI1 transcription. The latter implies crosstalk between
auxin formation and sugar signaling networks, whereby
plantgrowthispresumablylinkedwithphotosynthesisand
carbonfixation(Lehmannetal.2010).
Incontrasttotheresultsobtainedinthegain‐of‐function
experiments,theanalysisofan AMI1T‐DNAinsertionmu‐
tantdisclosedreducedIAMhydrolaseactivitiesandasignif‐
icantlyreducedendogenousIAAlevels.Interestingly,thein‐
depth analysis of the root architecture of the three ami1
knockoutlineundercontrolandsaltstressconditionspro‐
videdstrongevidenceforafunctionofAMI1asasuppressor
ofrootbranchingandoftheexpansionoftherootsystem.
Thisfunctionbecameevenmorepronouncedwhenplantlets
weregeminatedundersaltstressconditions.Whilethewild
typerespondedwithaslightreductionofrootbranchingto
highsalinityinthemedia,theami1nullmutantansweredto
thistypeofabioticstresswithareasonableinductionofroot
branching.Sofar,itisnotentirelyclearhowAMI1‐governed
Journal of Endocytobiosis and Cell Research VOL 26 | 2015
Root architecture under abiotic stress, Salopek-Sondi B et al.
auxinproductioncannegativelyaffectlateralrootformation
andtheexpansionoftherootsystem.Currently,wefavour
the working hypothesis that this way of auxin formation
counteractslocalauxinmaximainsuchwaythatitreduces
thesteepnessoftheauxingradientsbytheproductionofIAA
insurroundingtissues.Consequently,thismayoverridelo‐
calauxinsignalsnecessaryfortheinitiationoflateralroot
formation,andtranslateinanarrestoflateralrootdevelop‐
ment. Alternatively, AMI1‐mediated auxin biosynthesis
might result in general auxin overproduction, which may
have a global inhibitory effect on root proliferation. How‐
ever,itisyettooearlytodecidewhichmolecularmechanism
is responsible for the suppressive function of AMI1, as in‐
sightintothedynamicexpressionofAMI1duringthecourse
oflateralrootformationisyettobeprovided.
Some other previous studies unraveled substantial
crosstalkbetweenoxylipinsandauxin.Thisisremarkablein
suchasthesetwoplanthormonesusuallyhaveantagonistic
effects. However, it appeared that the expression of one
YUCCA(YUC)genefamilymember,YUC9,isstronglyinduced
by JA and coronatine, a bacterial phytotoxin that mimicks
thephysiologicallyactiveformofJA,JA‐Ile.Bycontrast,the
bioactiveJAprecursor,12‐oxo‐octadecatrienicacid(OPDA),
suppressesYUC9transcription.Mutantanalysis,employing
the JA receptor mutant coi1, reveaved that JA‐mediated
auxin biosynthesis proceeds via the COI1 signalling path‐
way.Metabolicstudiesondissectedorgansofwildtypeand
yucmutantlinesprovidedseverallinesofevidenceforapar‐
tiallyredundantsysteminwhichYUC9actstogetherwithits
closehomolog,YUC8.However,YUC8showsonlyaweakand
lateresponsetoJA,butiscapableofpartiallycompensating
foralossofYUC9,asintheyuc9backgroundYUC8showsan
inducedresponsivenesstoJA.Thoroughgeneticandmeta‐
bolicanalysesindicatedthatbothgenescontributetoauxin
biosynthesisinplanta.Comparedtothewildtype,yuc8and
yuc9knockoutshaveshorterprimaryroots,hypocotyls,and
petioles.Moreover,especiallytheyuc9mutantsshowanab‐
errant root branching phenotype. Noteably, a loss of both
loci,YUC8andYUC9,translatesintoanearlycompletelack
of IAA production in response to the administration of JA
(Hentrich et al. 2013a). Interestingly, JA has additionally
beenreportedtoinducetheexpressionofseveralIAA‐amino
acid hydrolases, i.e. IAR3, ILR1, ILL3, and ILL5 (Taki et al.
2005; Salopek‐Sondi et al. 2013). The corresponding en‐
zymescould,inturn,beresponsiblefortheremainingIAA
formation in the yuc8/yuc9 double‐knockout line, thereby
providingafunctionalconnectionbetweenauxindenovobi‐
osynthesis and auxin release from diverse storage pools.
However,theseresultsareinagreementwithpromoterre‐
porter studies that disclosed expression pattern for both
YUC8andYUC9thatimplyaparticipationinlateralrootde‐
velopment.Apparently,YUC9,butnotYUC8,isdownstream
of the repressor protein SOLITARY ROOT/IAA14, as it is
clearlyup‐regulatedintheslr1nullmutantbackground.In‐
triguingly, YUC9 is seemingly not controlled by ARF7/
ARF19, the transcription factors mainly affected by
SLR/IAA14,sinceYUC9isnotsignificantlyrepressedinthe
arf7/arf19double‐knockoutline.However,withrespectto
theexpressionpattern,itisstricinglyclearthatYUC9goes
aheadofYUC8inthecourseoflateralrootformation.YUC9
expression gets visible at stage II to III of primordia for‐
mationinthecentralcylinderoftheroot,directlybeneath
proliferatinglateralrootprimordia.Theexpressionlevelin‐
creases with the onset of lateral root growth but stays re‐
strictedtothecentralcylinderoftheprimaryroot.YUC8ex‐
Journal of Endocytobiosis and Cell Research VOL 26 | 2015
pression,however,lacksbehindshowingfirstdetectablesig‐
nals clearly later than stage five at the central base of the
newlyformedlateralroot.Lateron,YUC8expressionstays
restrictedtothelateralrootandincreaseswithinthecentral
cylinderofthenewlyformedorgan.
JAsaregenerallyconsideredtobebasicplantstresshor‐
monesproducedafterherbivoreorpathogenattack.None‐
theless,thereisalsoawealthofdataprovidingevidencefor
acontributionofJAincontrollingbothdevelopmentalpro‐
cessesandplantresponsestowaterdeficit,saltstress,and
heavymetalstress(CreelmanandMullet1995;Dombrowski
2003;Maksymiec2007).ItseemsevidentthatplantsuseJA
asabridgetolinkplantstressandgrowthresponses.Inthis
framework, the JA‐induced and YUC8‐ and YUC9‐mediated
auxinbiosynthesisissuggestedtoresultinlocalIAAover‐
production,whichleadstotwodifferentoutcomes:i)high
IAAdosesrepressplantgrowth,therebyassistingthegen‐
eralgrowthinhibitinginfluenceofJA;ii)highIAAcontents
areknowntoinduceETbiosynthesis.ETisknowntostimu‐
latetheformationofsclerenchymatictissueandtopromote
secondary plant growth. Both of these effects can be ob‐
served in respective YUC8 and YUC9 gain‐of‐function mu‐
tants(Hentrichetal.2013a,b).
Taken together, AMI1 and the two YUCCA genes, YUC8
andYUC9,fromArabidopsis,arelikelyinvolvedinregulating
lateralrootdevelopment.Publiclyavailablemicroarraydata
pointtowardsadifferentialregulationofthethreecandidate
genesuponvariousabioticstressconditions,includingsalt‐,
drought‐,andosmoticstress.Furthermore,severaltypesof
nutrientstresses,suchasnitrogen,phosphorous,sulfur,po‐
tassium,orirondeficiencyordepletionhavebeenshownto
transcriptionally control target gene expression. Possibly
even more importantly, the three target genes show very
broad distribution in the plant kingdom, implying an im‐
portantandperhapsbasicfunction.Currently,thereare47
identified AMI1 homologous proteins derived from 38 dif‐
ferent species, covering both mono‐ and dicot genera
(Sánchez‐Parraetal.2014).LikeAMI1homologs,YUC‐like
proteinshavebeenidentifiedfromvariousplantspecies,in‐
cludingtherelevantcropplantsmaize,rice,andtomato.As
Brassicacrops,suchasBrassicarapaandBrassicanapus,are
phylogeneticallycloselyrelatedwithA.thalianatheidentifi‐
cationandfunctionalcharacterizationofpendantstoAMI1,
YUC8,andYUC9intheBrassicacropsisnotexpectedtobea
majorobstacle.Anotherremarkableaspectwithrespectto
thethreeselectedtargetgenesisthatalossofneitherofthe
genescauseslethality,whichmakesthemtoidealcandidates
forthegenerationoftransgenicplantlinesorforthedevel‐
opment of targeted breeding programs that yield in elite
germplasmswithimprovedtraits.
IAA is found mostly in its conjugated form (approxi‐
mately95%)inalltheseedplantsstudiedsofar,thussug‐
gestingthatreversibleconjugationis,inadditiontoauxinbi‐
osynthesis,anothercriticalmechanismtoregulateIAAavail‐
ability(Szteinetal.1995).Differentplantspecieshavedis‐
tinctprofilesofauxinconjugates;monocotspreferablyaccu‐
mulate ester conjugates, whereas dicots synthesize mostly
amide conjugates (reviewed by Bajguz and Piotrowska
2009).Since1955,whenIAA‐Aspwasdetectedasafirstam‐
ideconjugateinpeaseedlings,differentaminoacids(seefor
review Woodward and Bartel 2005; Ludwig‐Müller et al.
2009; Penčik et al. 2009) and peptide (Walz et al. 2002,
2008;Seideletal.2006)conjugatesofIAAwerereportedto
be identified in different plants. It is generally postulated
thatIAAconjugatedtoAspandGluisanirreversiblecatabo‐
lite being important for auxin detoxification, while other
105
Root architecture under abiotic stress, Salopek-Sondi B et al. amidconjugatesaresuggestedtoparticipateinstorageand
hormonehomeostasisasaslow‐releasingsourceoffreeIAA
(HangarterandGood1981).Amideconjugatesofthelong‐
chain auxin, 4‐(indol‐3‐yl)butyric acid (IBA) (particularly
IBA‐Asp)werereportedtobefoundinafewplantssuchas
peatissue(Nordströmetal.1991),andpetuniacellsuspen‐
sionculture(EpsteinandLudwig‐Müller1993)afterfeeding
withIBA,andinmaizerootsduringarbuscularmycorrhiza
formation(Fitzeetal.2005).Intheviewofapplication,ex‐
ogenousIBAconjugateshavebeensuccessfullyusedforthe
rootingofcuttings(EpsteinandWiesman1987;Wiesmanet
al. 1989; Mihaljević and Salopek‐Sondi 2012), although
mechanismofrootinitiationhasremainedunclear.
The conjugate IAA‐Trp has a different function from
other auxin conjugates, i.e. it is not a storage compound
(Staswick2009).IAA‐Trpcausedagravitropicrootgrowthin
seedlings, while Trp alone did not. In addition, IAA‐Trp
nearly eliminated seedling root inhibition caused by high
concentrationsofIAAandinhibitedIAA‐dependentstimula‐
tion of lateral root growth (Staswick 2009). These results
showedthatIAA‐Trpconstituteapreviouslyunrecognized
mechanismtoregulateauxinactionandcouldbetherefore
animportantcompoundincontrollingrootarchitecture.
Ithasbeenshownthatreversibleauxinconjugationmay
playanimportantroleinplantadaptationtoabioticstress.
Inpoplartrees,theauxincontentwasfoundtodeclinedur‐
ingstressconditionswhileauxinconjugateswereincreased
(Junghansetal.2006;Popkoetal.2010),suggestingthatdi‐
minishedauxincontentmaybeafactorthatadaptsgrowth
(generally reduce) during adverse environmental condi‐
tions.Furthermore,perturbationinauxinprofilesuchasel‐
evatedleveloflongchainauxinIBAanditssugarconjugate
IBA‐Glc in Arabidopsis transgenic plants ectopically ex‐
pressed UDP‐glucosyltransferase (UGT74E2) has been
shown to improve survival during drought and salt stress
significantly (Tognetti et al. 2010). A cascade of signals
causedbystressconditionsseemstomediateauxinprofile
andlevelbyinfluencingexpressionandactivityofenzymes
responsibleforreversibleauxinconjugation,suchasauxin
conjugate synthases (GH3), UDP‐glucosyltransferases
(UGTs),andauxinamidohydrolases(IARandILL).Thusvar‐
iousenvironmentalstresses,includinghighsalinityandos‐
moticstress,areshowntoinduceGH3genesandoverpro‐
duce GH3 enzymes in Arabidopsis (Park et al. 2007). Fur‐
thermore, activation of GH3 promoter has been found in
poplarundersaltstressbyusingpGH3::GUSasanauxin‐re‐
sponsive reporter (Teichman et al. 2008). Tognetti et al.
(2010) showed that UDP‐glucosyltransferase (UGT74E2),
which preferentially glucosylates IBA as a substrate was
strongly upregulated during drought and salt stress. The
mechanism of regulation has appeared to be mediated by
H2O2,usuallyreleasedduringstressconditions.Ontheother
side, Arabidopsis plants transformed with auxin‐amidohy‐
drolase gene ILL3 from poplar were more resistant to salt
stress than the wild‐type plants (Junghans et al. 2006).
Basedonproteomeanalysis,auxin‐amidohydrolasewasalso
reportedasanovelproteinidentifiedinsoybeanrootinre‐
sponse to waterlogging (Alam et al. 2010). Despite a few
above‐mentionedevidences,areversibleauxinconjugation
as a mechanism of abiotic stress adaptation is mostly un‐
clear,particularlyincropplants.
The enzymology involved in the metabolism of amide
conjugatesisjustbeginningtobeunderstood.Thebiosyn‐
thesisofamideconjugatesiscatalyzedbyasubsetofpro‐
teinsfromtheso‐calledGH3familyandappearedtoinclude
auxins activated by adenylation as critical intermediates
106
(Staswicketal.2002,2005).ThefamilyofGH3genesinAra‐
bidopsis consists of 19 family members (Staswick et al.
2005),ofwhichatleastsevenareabletocatalyzethesyn‐
thesisofIAAamideconjugates.Thesebelongtotheso‐called
groupIIgenes(Staswicketal.2005).Thefirstmemberofthe
auxininducibleGH3genefamilywasisolatedfromsoybean
(HagenandGuilfoyle1985).UptonowGH3familymembers
involvedmostlikelyinIAAconjugationhavebeenreported
fromavarietyofplantspecies(formoredetailsseethere‐
viewonGH3sbyWangetal.2008),amongthemthemoss
Physcomitrellapatens(Bierfreundetal.2004;Ludwig‐Mül‐
ler et al. 2009), tobacco (Roux and Perrot‐Rechenmann
1997),rice(Jainetal.2006),andpungentpepper(Liuetal.
2005), the latter regulated by auxin and ET. Despite this,
onlyforafewplantspecies,inadditiontoArabidopsis,the
activity of GH3 proteins as adenylating enzymes has been
demonstrated,e.g.forP.patens(Ludwig‐Mülleretal.2009),
andrice(Chenetal.2009).Inaddition,theGH3proteinfam‐
ilyhasbeenimpliedinthestressresponseandstresstoler‐
anceinArabidopsis(Parketal.2007),poplar(Teichmannet
al.2008),sorghum(Wangetal.2010),rice(Duetal.2012),
andapple(Yuanetal.2013).
The hydrolysis of IAA amide conjugates results in free
auxins and is mediated by auxin amidohydrolases, metal‐
loenzymesbelongingtotheM20familyofpeptidases.Sev‐
eralsuchhydrolases(namedIARandILL)werefirstcloned
fromA.thalianaandtestedforactivitytowardsconjugates
ofthemostcommonauxin,IAA(BartelandFink1995;Da‐
vies et al. 1999; Lasswell et al. 2000; LeClere et al. 2002;
Rampeyetal.2004).Eachoftheseenzymesshowsdifferent
but overlapping substrate specificity. Auxin conjugate hy‐
drolaseswerethenisolatedandpartiallycharacterizedfrom
Arabidopsis suecica (sILR1), a close relative of A. thaliana
(Campanellaetal.2003a,b).Someofauxinconjugatehydro‐
lasesfromthelegumeMedicagotruncatuladisplayedactiv‐
ity towards IAA‐aspartate (Campanella et al. 2008), which
hasearlierbeendescribedonlyassubstrateforbacterialIAA
conjugatehydrolases(Chouetal.1998).Anorthologofthe
A.thalianaIAR3fromthemonocotspecieswheat(Triticum
aestivum)(TaIAR3)showedsubstratespecificityforlonger
sidechainauxinssuchasaminoacidconjugateswithindole‐
3‐butyricacid(IBA)andindole‐3‐propionicacid(IPA)(Cam‐
panellaetal.2004).Furthermore,afamilyofauxinconjugate
hydrolases from Chinese cabbage also showed substrates
preferencestowardsaminoacidconjugatesinthefirstplace
withIPA,thenIBA(Savićetal.2009).Inaddition,recentthe‐
oreticalstudyconfirmedthatalanineconjugatesofIBAand
IPA make stronger interactions with the binding site of
BrILL2incomparisontoIAA(Šimunovićetal.2011).Also,
thesehydrolasesweredifferentiallyregulatedduringthein‐
teraction of Chinese cabbage with the obligate biotrophic
pathogen Plasmodiophora brassicae (Schuller and Ludwig‐
Müller2006).Long‐chainauxinIBAappearstobestoredin
amannersimilartothatofIAAinaformconjugatedtoamino
acids,allowingitsslowhydrolysisandrelease.IPAhasalso
auxinactivity,butitsoccurrenceasanendogenousauxinis
stillquestionable.Ithasbeen foundsofarin rootsofAra‐
bidopsisupontreatmentwithSA(Walkeretal.2003),while
IBAwasshowntobeelevatedintheconditionsofdrought
andhighsalinity(Tognettietal.2010).Thisisinaccordance
withearlyworkfromLudwig‐Mülleretal.(1995),showing
that IBA synthesis was drought and salt inducible. These
preliminary findings may imply the involvement of long‐
chain auxins in stress responses. Despite the isolation and
characterizationofnumerousauxinamidohydrolasesform
differentplantstodate,thereactionmechanismsaswellas
Journal of Endocytobiosis and Cell Research VOL 26 | 2015
Root architecture under abiotic stress, Salopek-Sondi B et al.
regulationofauxinamidohydrolasesonthegeneexpression
levelandproteinactivitylevelarestillunclear.Thefirstx‐
raystructureoftheILL2enzymefromArabidopsishasbeen
reportedasan apoenzyme(Bittoetal.2009),stillmissing
detailsaboutsubstratebindingsiteandaminoacidresidues
importantforsubstratespecificity.Basedonmodelingapo‐
tentialsubstratebindingclefthasbeenproposedfortheAr‐
abidopsisenzyme(AtILL2)(Bittoetal.2009),aswellasthe
Chinese cabbage enzyme (BrILL2), in which additionally
severalsubstratebindingmodeshavebeenpredictedforthe
preferredsubstrateIPA‐Ala(Savićetal.2009;Smolkoetal.
underreview).
Conclusionsandperspectives–P.indicamayhelp
tounderstandtheroleofauxininmutualisticin‐
teraction
Studiesontheinteractionofthesymbiotic,root‐colonizing
endophyticfungusP.indicawiththemodelplantArabidop‐
sis showed general growth‐promoting effects (Peškan‐
Berghöfer2004;Leeetal.2011;Lahrmannetal.2013).P.
indica‐insensitive mutants are also insensitive to the exu‐
datefraction(Vadasseryetal.2009a;Leeetal.2011;John‐
sonetal.2014a,b).Thisandotherdatasupporttheconcept
that(an)elicitorreleasedbythefungusisperceivedbythe
hostcellandactivatesareceptor‐mediatedsignallingpath‐
way.Consistentwiththishypothesis,anatypicalreceptor‐
likekinasewithleucine‐richrepeatsisrequiredforthein‐
teraction(Shahollarietal.2007)andarapidincreaseinthe
intercellularcalciumconcentrationandofthesecondmes‐
sengerphospholipidphosphatidicacidrepresentearlysig‐
nallingevents(lessthan2minutes)intherootcells(Vadas‐
seryetal.2009a;Camehletal.2010).Mutationspreventing
theincreaseintheintracellularCa2+elevationinrootcellsor
theaccumulationofphosphatidicacidinresponsetotheex‐
udate of P. indica completely prevent the benefits for Ara‐
bidopsis plants (Camehl et al. 2010). Phytohormones and
theirhomeostasisintherootsarecrucialforP.indicaeffects
in plants (Sirrenberg et al. 2007; Vadassery et al. 2008;
Schäferetal.2009).P.indicaexudatecomponentalsostim‐
ulates growth of Chinese cabbage plants. Much work has
beenperformedtounderstandtheroleofauxininthebene‐
ficialinteractionbetweenP.indicaandotherplantspecies.
In Arabidopsis, growth promotion is achieved without an
overallupregulationoftheauxinlevelinroots.However,the
draftphenotypeoftheauxin‐overproducersur1isentirely
rescuedbythefungusbyconvertingfreeauxinintoconju‐
gates(Vadasseryetal.2008).TheP.indica‐inducedgrowth
promotioninChinesecabbageismuchstrongerthaninAra‐
bidopsis,resultinginmassiveroothairdevelopment(Leeet
al.2011).Interestingly,thebenefitsfortheplantdonotre‐
quirealivingfungus,butcanalsobetriggeredbyalowmo‐
lecularmassexudatecomponentreleasedfromthefungus
intothefungalcellwallandgrowthmedium.InChinesecab‐
bagerootsthiscomponentinducesmassiverootbranching,
andamorethan2‐foldincreaseintheauxinlevelintheroots
(butnotintheshoots)ofChinesecabbageseedlings(Leeet
al.2011),and‐aftertransfertosoil‐resultsinplants,which
produce23%moreseeds.Furthermore,theaerialpartsof
theseplantsaresignificantlymoreresistanttodrought(Sun
etal.2010):theadultplantsrequire440mllesswaterfor
seed production in the greenhouse (control plants require
5100mlwater),andaremoreresistantagainstinfectionsby
Alternaria brasssicae (Johnson et al. 2014a, b). The fungus
confers stress tolerance by strongly reducing endogenous
and stress‐induced reactive oxygen species in Arabidopsis
Journal of Endocytobiosis and Cell Research VOL 26 | 2015
(Matsuoetal.2015).SincetheexudatecomponentofP.in‐
dicadoesnotcontainauxin(Leeetal.2011),buttriggersthe
benefits in Chinese cabbage plants via the stimulation of
auxinhomeostasisintheroots,andsinceexogenousappli‐
cationofauxintoChinesecabbagerootscannotreplacethe
beneficialeffectsofthefungus,characterizationofauxin‐re‐
latedtargetgenesinChinesecabbageroots,whichareup‐
regulatedbythefungusmightcontributesubstantiallytothe
betterunderstandingofthisscenario.Overexpressionofthe
B. rapa AUX1 IAA influx carrier in Arabidopsis resulted in
larger roots even without P. indica colonization (Lee et al.
2011).AUX1wasfoundtobeupregulatedbyP.indicainChi‐
nesecabbage(Leeetal.2011;Dongetal.2013).Thisshows
thatauxin‐relatedgenesidentifiedinatranscriptomeanaly‐
siscanserveastargetsforimprovingtherootsystem.
Theprocessesinvolvedinauxinsignallingintherootun‐
derstressconditionsareverycomplexandcannotbetack‐
ledbyanalysingsingleoronlyafewcomponentsofasystem.
Asystemsbiologyapproachdealswiththebiologicalprob‐
lemsinthemostgeneralwaypossiblewiththehelpofboth
advancemoleculartechniquesandmathematicalmodelling.
Technologies available for gene expression profiling allow
simultaneousanalysisofallgenesintheorganism.However,
this is linked with collection of immense amounts of data
that have strong dimensionality problem, representing a
challengebothtobiologistsaswellastostatisticians.Itwas
shownthatadataanalysisworkflowwhereonlytheinter‐
sectionofdifferentiallyexpressedgeneslistobtainedusing
different preprocessing methods (background correction,
normalization, greatly improves the robustness of the ob‐
tained results (Rotter et al. 2007). Another implication of
hugedatasetsistheirreportingandsharingandFAIRprin‐
ciples (Findable, Accessible, Interoperable and Reusable;
Starretal.2015).Foreasiersharingofinformationandpos‐
siblere‐analyses,datamustbestoredinpermanentpublic
databases (e.g. GEO, ArrayExpress, CIBEX), following ade‐
quateMIBBIstandard(Tayloretal.2008)andapplyingFAIR
principlesofdatasharing.Appropriate‘in‐house’organiza‐
tionoftranscriptomedataisanexcellentstartingpointfor
designingexperiments,generatinghypothesesorconceptu‐
alizingaswellasforcross‐speciescomparison(Mochidaand
Shinozaki2010).Anotherimportantpointisefficienttrans‐
lationofknowledgebetweenmodelspeciesandcropspecies
whichisenabledinGOMapManApplication(Ramšaketal.
2014).Besidesstatisticalanalyses,pathwayanalysis(gene
setenrichmentmethods),dataintegrationanddatavisuali‐
zationinthecontextofbiologicalpathways(suchas Map‐
Man)cancontributesignificantlytotherelevantbiological
interpretation(Rotteretal.2007,2009).Finally,asystems
biology approach can, through integration of several data
sources,leadtoconstructionofregulatorynetworkmodels
of the studied process (Breitling 2010). Those approaches
mightcontributesubstantiallytoabetterunderstandingof
theroleoftheauxinhomeostasisunderstress.
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