Ecological relevance of strigolactones in nutrient uptake and other abiotic stresses, and in plant

19 Pages·2015·0.86 MB·English

PlantSoil(2015)394:1–19
DOI10.1007/s11104-015-2544-z
MARSCHNERREVIEW
Ecological relevance of strigolactones in nutrient uptake
and other abiotic stresses, and in plant-microbe interactions
below-ground
BeatrizAndreo-Jimenez&CarolienRuyter-Spira&
HarroJ.Bouwmeester&JuanA.Lopez-Raez
Received:12January2015/Accepted:1June2015/Publishedonline:10June2015
#SpringerInternationalPublishingSwitzerland2015
Abstract shortage. Belowground, besides regulating root archi-
Background Plants are exposed to ever changing and tecture,theyalsoactasmolecularcuesthathelpplants
often unfavourable environmental conditions, which tocommunicatewiththeirenvironment.
cause both abiotic and biotic stresses. They have Scope Thisreviewdiscussescurrentknowledgeonthe
evolved sophisticated mechanisms to flexibly adapt different roles of SLs below-ground, paying special
themselves to these stress conditions. To achieve such attentiontotheirinvolvementinphosphorusuptakeby
adaptation,theyneedtocontrolandcoordinatephysio- the plant by regulating root architecture and the estab-
logical, developmental and defence responses. These lishment of mutualistic symbiosis with arbuscular my-
responses are regulated through a complex network of corrhizalfungi.Theirinvolvementinplantresponsesto
interconnectedsignallingpathways,inwhichplanthor- other abiotic stresses such as drought and salinity, as
mones play a key role. Strigolactones (SLs) are multi- well as in other plant-(micro)organisms interactions
functional molecules recently classified as a new class such as nodulation and root parasitic plants are also
ofphytohormones,playingakeyroleasmodulatorsof highlighted. Finally, the agronomical implications of
thecoordinatedplantdevelopmentinresponsetonutri- SLsbelow-groundandtheirpotentialuseinsustainable
ent deficient conditions, especially phosphorus agricultureareaddressed.
Conclusions Experimental evidence illustrates the bio-
logical and ecological importance of SLs in the rhizo-
ResponsibleEditor:PhilippeHinsinger.
sphere. Their multifunctional nature opens up a wide
: :
B.Andreo-Jimenez C.Ruyter-Spira H.J.Bouwmeester range of possibilities for potential applications in agri-
LaboratoryofPlantPhysiology,WageningenUniversity, culture.However,amorein-depthunderstandingonthe
Droevendaalsesteeg1,6708PBWageningen,
SL functioning/signalling mechanisms is required to
TheNetherlands
allowustoexploittheirfullpotential.
C.Ruyter-Spira
BusinessUnitBioscience,PlantResearchInternational,
Keywords Abioticstress.Arbuscularmycorrhizal
Droevendaalsesteeg1,6708PBWageningen,
TheNetherlands fungi.Phosphorusacquisition.Rootarchitecture.
Rhizosphere.Rootparasiticplants.Strigolactones
H.J.Bouwmeester
CentreforBiosystemsGenomics,POBox98,6700
ABWageningen,TheNetherlands
Introduction
J.A.Lopez-Raez(*)
DepartmentofSoilMicrobiologyandSymbioticSystems,
Themostimportantassignmentofmodernagricultureis
EstaciónExperimentaldelZaidín(CSIC),Granada,Spain
e-mail:[email protected] toprovideglobalfoodsecurityinasustainablemanner.
2 PlantSoil(2015)394:1–19
Fifty years ago, the challenge to feed the growing rhizosphere, nodulation, was described (Fig. 1) (Foo
world population was solved by the development of andDavies2011;Sotoetal.2010).
new high-yielding crop varieties and high-intensity
agricultural management (Gianinazzi et al. 2010). SLbiosynthesisandsignalling
However, optimal production of these improved
varieties/strategies could not be achieved with the SLs are mainly produced in the roots and secreted
natural reserves of nutrients available in most soils. into the rhizosphere, but biosynthesis also has been
Thus, chemical fertilizers containing nitrogen, phos- suggested to occur throughout the plant, although at
phorus and potassium (NPK) became an indispens- loworevenundetectablelevels(Dunetal.2009;Xie
able source of the nutrients required for proper crop et al. 2010). They are produced at extremely low
growth and food production. However, the cheap levels, being active at pico- and nanomolar concen-
source of one of these nutrients, rock phosphate, trations, and are unstable in the soil, which hampers
will be exhausted in a few decades (Cordell et al. their isolation and characterization (Xie et al. 2010).
2009). Therefore, there is a need to develop new Todate19differentSLshavebeencharacterized,but
agronomical strategies to optimize phosphorus (P) it hasbeenestimated thatthetotalnumberofnatural
usage. Plants can only assimilate P in its inorganic SLsmightbeover1000(Akiyamaetal.2010;Ćavar
mineral phosphate form, which is usually present in et al. 2014; Zwanenburg and Pospíšil 2013). They
only low concentrations and is rather immobile in have been detected in a wide range of monocotyle-
the soil, which results in P deficiency (Péret et al. donous and dicotyledonous plant species, and each
2011; Schachtman et al. 1998). To cope with P plantisproducingablendofdifferentSLsdepending
deficiency, plants have evolved a wide array of on the species (Ruyter-Spira et al. 2013; Xie et al.
adaptive responses in plant growth, development, 2010). All natural SLs isolated and characterized so
metabolism and interaction with soil microorgan- farhaveasimilarchemicalstructure,withastructural
isms (Péret et al. 2011; Rouached et al. 2010; coreconsistingofatricycliclactone(theABC-rings)
Smith and Read 2008). connectedviaanenoletherbridgetoabutyrolactone
Strigolactones (SLs) are multifunctional molecules group (the D-ring) (Fig. 1) (Ćavar et al. 2014; Xie
classifiedasanewclassofphytohormonesthatcontrols et al. 2010). The bridge between the C- and D-rings
severaldifferentprocessesinplants.Theyplayapivotal can be rapidly cleaved in aqueous and/or alkaline
role as modulators of the coordinated development of environments,resultingintheirshort-livedcharacter,
rootsandshootsinresponsetonutrientdeficientcondi- which supports their role as signalling molecules
tions,especiallyphosphorusshortage.Accordingly,SLs (Akiyama et al. 2010; Xie et al. 2010; Zwanenburg
regulate above- and belowground plant architecture, andPospíšil2013).SLshaverecentlybeenclassified
adventitious root formation, secondary growth, repro- into two groups of diastereoisomers, the strigol-type
ductivedevelopmentandleafsenescence(Agustietal. and the orobanchol-type, depending on their C-ring
2011;Gomez-Roldanetal.2008;Kapulniketal.2011a; orientation(Fig.1)(Xieetal.2013;Zwanenburgand
Kohlenetal.2012;Rasmussenetal.2012;Ruyter-Spira Pospíšil2013).TheAB-ringsarelessconservedthan
etal. 2011; Umeharaetal.2008;Yamada etal. 2014). theCD-ringsandcanbedecoratedormodifiedbyfor
However, novel roles for SLs are emerging, for exam- example methylation, hydroxylation, acetylation,
ple, recently they were also shown to play a role in etc., giving rise to the different SLs known today
defence responses (Torres-Vera et al. 2014). Despite (Akiyama et al. 2010; Zwanenburg and Pospíšil
theirimportanceasplanthormones,theywereinitially 2013). The stereochemistry and structural features
identified as signalling molecules in the rhizosphere. ofthedifferentSLsareimportantfortheirbiological
Here, SLs act as host detection cues for root parasitic activity.Forexample,theCDpartisessentialforthe
plants of the Orobanchaceae and symbiotic arbuscular parasitic weed seed germination inducing activity,
mycorrhizal (AM) fungi from the phylum but modifications in the A-ring have little effect on
Glomeromycota (Fig. 1) (Akiyama et al. 2005; this activity (Akiyama et al. 2010; Xie et al. 2010;
Bouwmeester et al. 2007; López-Ráez et al. 2011b). Zwanenburg and Pospíšil 2013). For their hyphal
More recently, a role for SLs in another important branching inducing activity in AM fungi the D-ring
plant-symbiotic microorganism interaction in the isalsoessential,butthebridgebetweentheCD-rings
PlantSoil(2015)394:1–19 3
Fig.1 Chemicalstructuresof
strigolactonesandrolestheyplay
belowground.Strigolactones
R1 R2 R1 R2
(SLs)aremultifunctional O O O O
moleculesplayingseveral C C
differentrolesinplants.Asplant A B A B
hormones,theymodulateroot O O OO O O OO
systemarchitecture.Inthe R3 R4 D R3 R4 D
rhizosphere,theyfavourthe Strigol-type Orobanchol-type
establishmentofbeneficial
associationswitharbuscular
mycorrhizalfungi(AMfungi) RHIZOSPHERE
andrhizobia.SLsalsopromote
thegerminationofrootparasitic
plants,allowingaparasitic
interaction.Novelrhizosphere
rolesforSLsmayemergeas PARASITIC
AM FUNGI
indicatedby? PLANTS
RHIZOBIA
ROOT
ARCHITECTURE
does not necessarily have to be an enol ether epi-5-deoxystrigolbyacytochromeP450,Os900,thatis
(Akiyama et al. 2010; Zwanenburg and Pospíšil homologoustoArabidopsisMAX1(Zhangetal.2014).
2013). Akiyama and co-workers also showed that Another rice MAX1 homolog, Os1400, then converts
the hyphal branching activity depended on the mod- ent-2′-epi-5-deoxystrigol into orobanchol (Zhang et al.
ifications on the AB-ring (Akiyama et al. 2010; 2014).RicehasfiveMAX1orthologs,ofwhichfour-
Zwanenburg and Pospíšil 2013). The presence of Os900, Os1400, Os5100and Os1900- were shown to
the D-ring is also necessary for hormonal activity of rescuetheArabidopsismax1mutantphenotype(Challis
SLs (Boyer et al. 2012). In addition, Boyer and co- et al. 2013; Cardoso et al. 2014). Although upon ex-
workers showed that lipophilicity is an important pressioninNicotianabenthamianaOs5100andOs1900
factorforthisactivity,withtheSLshavingahydrox- catalysedtheconversionofcarlactoneintoent-2′-epi-5-
yl group on the AB-rings being more active (Boyer deoxystrigol (and minute amounts of 5-deoxystrigol),
et al. 2012). this occurred with very low efficiency, just as for
SLs biosynthetically derive from the carotenoids ArabidopsisMAX1(Zhangetal.2014).Theapplication
(López-Ráezetal.2008a;Matusovaetal.2005)through of labelled carlactone to Arabidopsis resulted in the
the conversion of all-trans-β-carotene to 9-cis-β-caro- formation of a product called SL-LIKE1 and not ent-
tenemediatedbyaβ-caroteneisomerase(D27)(Alder 2′-epi-5-deoxystrigol (Seto et al. 2014), although the
et al. 2012). 9-Cis-β-carotene is transformed into level of the latter compound may have been beyond
carlactonebysequentialoxidativecleavagebytwo ca- the detection level. SL-LIKE1 was recently identified
rotenoid cleavage dioxygenases (CCD7 and CCD8) asmethylcarlactonateandshowedthatitisbiologically
(Alder et al. 2012), and thus SLs belong to the activeininhibitingshootbranchinginArabidopsis(Abe
apocarotenoids, as the phytohormone abscisic acid etal.2014).Therefore,itseemsthatinArabidopsisthe
(ABA)(Ohmiya2009;WalterandStrack2011).Inrice, thus far reported canonical strigolactones (Goldwasser
carlactoneisthenconvertedintothestrigolactoneent-2′- etal.2008;Kohlenetal.2011)areminorsideproducts
4 PlantSoil(2015)394:1–19
orartefacts.Thatcould imply thatMAX1and the rice (Fooetal.2013b;López-Ráezetal.2008a;Yoneyama
MAX1orthologsOs5100andOs1900haveadifferent et al. 2007, 2012), and it has been suggested that they
enzymatic activity than rice MAX1 orthologs Os900 play a pivotal role as modulators of the coordinated
and Os1400. Interestingly, although Os1400 is absent development of roots and shoots under these
in the rice cultivar Bala, this line still produces unfavourable conditions. On the one hand, increased
orobanchol.Therefore,theremustbeanasyetuniden- SL production suppresses the outgrowth of axillary
tifiedcytochromeP450presentinthericegenomethat branches/tillers (Kohlen et al. 2011; Umehara et al.
hasasimilaractivityasthisMAX1orthologue(Zhang 2010),whileatthesametimetheyaffectvariousaspects
et al. 2014; Cardoso et al. 2014). Since Arabidopsis ofrootgrowthallaimedtoimprovephosphateforaging
MAX1 also lacks the capacity to convert ent-2′-epi-5- (Mayzlish-Gatietal.2012;Ruyter-Spiraetal.2011;Sun
deoxystrigol to orobanchol, the minute amounts of etal.2014).
orobanchol observed in Arabidopsis root exudates are Changes in root development during P starvation
also likely to result from a similar mechanism (Zhang have been most intensively studied in Arabidopsis.
etal.2014). Here,itwasshowntostimulatelateralrootandroothair
SLperceptionandsignallingrequireanF-boxleucine- formation,aswellastheirsubsequentdevelopment,and
richrepeatprotein(MAX2)andanα/β-hydrolase(D14) toinhibitprimaryrootgrowth(Fig.2)(reviewedbyNiu
(Gomez-Roldan et al. 2008; Hamiaux et al. 2012; et al. 2013). In maize and rice, P starvation inhibits
Umehara et al. 2008). Binding of SLs by D14 enables lateral root formation, while it promotes primary root
theirinteractionwithMAX2andthiscomplexfacilitates growth (Li et al. 2012; Sun et al. 2014). Different
thedegradationofthetargetproteinD53andthetranscrip- responses to low P between these plant species might
tionaleffectorBES1viatheubiquitin-proteasomesystem beduetothefactthatArabidopsisisanon-mycorrhizal
(Jiangetal.2013;Wangetal.2013;Zhouetal.2013),a plant.However,weshouldbecarefulwithgeneralizing
similar mechanism as forgibberellin perception and sig- rootarchitecturalchangeswhenonlystudyingonespe-
nalling.D53isaclassIClpATPaseproteinwhichactsa cific ecotype or variety for each species. For instance,
repressor of SL signalling, and its degradation prevents variousArabidopsisecotypesdisplayedadifferentroot
axillary-bud outgrowth in rice (Jiang et al. 2013; Zhou architectural response to low P conditions, suggesting
etal.2013).Interestingly,ithasbeensuggestedthatSLs thatthereisnaturalvariationforthisresponseandthatit
promote proteasome-mediated degradation of D14 in is genetically determined (Chevalier et al. 2003). In
Arabidopsis,thuslimitingtheirownsignallingbyaneg- Arabidopsis,inthepresenceofsufficientP,SLshavea
ativefeedbackloop(Chevalieretal.2014). suppressive effect on lateral root formation (Fig. 2).
In the present work, we review the current knowl- Accordingly,SL-deficientmutantshaveahigherlateral
edge on the different roles of SLs in the rhizosphere, root density (Kapulnik et al. 2011a). They also have a
paying special attention to their involvement in phos- shorterprimaryroot,notonlyinArabidopsis,butalsoin
phorusuptakebytheplant.Wefocusontheirabilityto rice and maize (Arite et al. 2012; Guan et al. 2012;
regulaterootsystemarchitectureandtofavoursymbio- Ruyter-Spiraetal.2011).Thesephenotypescouldonly
sis establishment with beneficial microorganisms such be rescued by the application of the synthetic SL ana-
as AM fungi and rhizobia. Finally, because of their logueGR24totheSLbiosynthesismutants,butnotin
multifunctional character, the potential use of SLs to thoseaffectedinsignalling,indicatingthatSLsregulate
develop new more sustainable agricultural strategies root architecture in a MAX2-dependent manner
willbediscussed. (Kapulnik et al. 2011a; Koltai et al. 2010; Mayzlish-
Gatietal.2012;Ruyter-Spiraetal.2011).Kapulnikand
co-workersalsoshowedthattheapplicationofGR24(1
SLsandrootsystemarchitecture and 3 μM) to Arabidopsis seedlings led to a MAX2-
dependentincreaseinroothairlength(Fig.2)(Kapulnik
OneofthefunctionsofSLsbelow-groundistoregulate etal.2011a,b).
root development in response to phosphorus shortage The effect of SLs on the regulation of root system
(De Cuyper et al. 2015; Kapulnik et al. 2011a; Koltai architecture(RSA)wasshowntodependontheplant’sP
2011; Ruyter-Spira et al. 2011). Interestingly, SL bio- status(Kapulniketal.2011b;Ruyter-Spiraetal.2011).
synthesisispromotedbyP-limitingconditions(Table1) In contrast to the observed response in the presence of
PlantSoil(2015)394:1–19 5
Table1 EffectofdifferentabioticstressesonSLproductionand/orSLbiosyntheticgeneexpressionandAMFcolonisationindifferent
plantspecies
Stress Plant EffectonSLs EffectonAMFcolonisation AMfungus Reference
-P M.truncatula + + R.irregularis Bonneauetal.2013
-P M.truncatula + ND ND Yoneyamaetal.2012
-P P.sativum + + R.irregularis Fooetal.2013a,b
-P O.sativa + ND ND Jamiletal.2011a,b
-P O.sativa + ND ND Umeharaetal.2010
-P S.lycopersicum + ND ND López-Ráezetal.2008a,b
-P S.lycopersicum + ND ND Yoneyamaetal.2012
-P S.bicolor + ND ND Yoneyamaetal.2007
-P T.aestivum + ND ND Yoneyamaetal.2012
-P L.sativa + ND ND Yoneyamaetal.2012
-P A.sinicus + ND ND Yoneyamaetal.2012
-P A.thaliana + ND ND Kohlenetal.2011
-P T.pratense + ND ND Yoneyamaetal.2012
-P C.officinalis + ND ND Yoneyamaetal.2012
-P L.japonicus + ND ND Liuetal.2015
-N M.truncatula = ND ND Yoneyamaetal.2012
-N P.sativum + ND ND Fooetal.2013a,b
-N O.sativa + ND ND Jamiletal.2011a;b
-N S.lycopersicum = ND ND Yoneyamaetal.2012
-N S.bicolor + ND ND Yoneyamaetal.2007
-N S.bicolor + ND ND Yoneyamaetal.2013
-N T.aestivum + ND ND Yoneyamaetal.2012
-N L.sativa + ND ND Yoneyamaetal.2012
-N A.sinicus + ND ND Yoneyamaetal.2012
-N C.officinalis + ND ND Yoneyamaetal.2012
Drought S.lycopersicum ND = R.irregularis Arocaetal.2008
Drought T.aestivum ND − G.etunicatum Al-Karakietal.2004
Drought T.aestivum ND + F.mosseae Al-Karakietal.2004
Drought T.aestivum ND = G.etunicatum Al-Karakietal.2004
Drought T.aestivum ND = F.mosseae Al-Karakietal.2004
Drought C.lanatus ND + R.irregularis Omirouetal.2013
Drought C.lanatus ND + F.mosseae Omirouetal.2013
Drought Z.mays ND − G.etunicatum Zhuetal.2012
Drought A.majus ND − G.deserticola Asraretal.2012
Salinity L.sativa −/+ + R.irregularis Arocaetal.2013
Osmotic L.japonicus − ND ND Liuetal.2015
LowT S.bicolor ND − R.irregularis Augéetal.2004
LowT O.sativa = = R.irregularis Liuetal.2013
HighT M.truncatula ND + R.irregularis Huetal.2015
Cd T.aestivum ND − F.mosseae Shahabivandetal.2012
6 PlantSoil(2015)394:1–19
Table1 (continued)
Stress Plant EffectonSLs EffectonAMFcolonisation AMfungus Reference
Cu M.truncatula ND − R.irregularis Hagerbergetal.2011
Al A.virginicus ND − A.morrowiae Kellyetal.2005
Al A.virginicus ND + G.clarum Kellyetal.2005
Stressesinclude:phosphorusstarvation(−P),nitrogenstarvation(−N),drought,salinity,lowtemperature(LowT),hightemperature(High
T),cadmium(Cd),copper(Cu)andaluminium(Al).Thelevelsarecomparedwithcontrolplants(non-stressed),andarehigher(+),lower(−)
ornotdifferent(=).NDnotdetermined
sufficientP,underPlimitationSLspromotedlateralroot transportstream,whichismainlyfedbyauxinproduced
developmentinArabidopsistoimprovePuptake(Fig.2) in the apex and young leaves (Aloni 2013; Dubrovsky
(Ruyter-Spiraetal.2011).TheinvolvementofSLsinthe et al. 2011). In Arabidopsis, GR24 application reduced
regulation of root architecture occurs through its cross- the auxin level in young developing rosette leaves,
talk with the phytohormones auxin and ethylene resulting in a decreased leaf area (Ruyter-Spira et al.
(Kapulniketal.2011b;Koltai2011;Ruyter-Spiraet al. 2011).Alogicalexplanationforthiseffectcouldbethat
2011).InArabidopsis,theexpressionoftheauxinrecep- because GR24 has an inhibitory effect on the auxin
tor TRANSPORT INHIBITOR RESPONSE1 (TIR1) transportcapacityofthepolarauxintransportstreamin
wasincreasedbylowPlevels.Interestingly,thisincrease the stem (Crawford et al. 2010), auxin levels initially
only occurred in wild-type plants but not in the SL accumulate, which negatively feeds back on auxin bio-
signalling mutant (Mayzlish-Gati et al. 2012). synthesis.Interestingly,bothGR24applicationandlowP
Therefore, SLs may regulate RSA by affecting auxin conditionsreducedauxintransportandtheactivityofthe
sensitivity. Lateral root development and primary root auxin reporter DR5::GUS in rice root tips, suggesting
growth depend on auxin influx from the polar auxin that,likeinArabidopsis,SL-mediatedrootdevelopment
Fig.2 Impactofphosphorus
+Pi -Pi
statusonstrigolactoneproduction
SLs SLs
andplantdevelopmentin
Arabidopsisthaliana(ecotype
Columbia).Phosphate(P)
deficiencypromotesstrigolactone
(SL)productionintheroots,
affectingplantarchitecture.Under
theseconditions,SLsare
involvedinreducingprimaryroot
growth,inducinglateralroot
densityanddevelopment,and
stimulatingroothairelongation
anddensity.Thesemodifications
allowtheplanttoincreasethe
exploratorycapacityofthesoil.
SLsarealsotransportedtothe
shoot,wheretheyinhibitshoot
branching,henceincreasingthe
root-to-shootratio
-
Shootbranching
-
Primaryrootgrowth
+ Lateral rootformation
+ Roothairelongation
PlantSoil(2015)394:1–19 7
isregulatedviaareductionofauxintransportfromshoot 2010).Alternativelytothe‘directpathway’ofobtaining
toroot(Sunetal.2014).Indeed,GR24hasbeenshown Pbyroothairsandlateralroots,anotherplantstrategyto
toreducetheexpressionofthegeneencodingtheauxin improvePacquisitionisbyestablishingsymbiosiswith
efflux protein PIN1 in the stem (Crawford et al. 2010). certain soil microorganisms suchasAM fungi,the so-
Moreover, GR24 was found to rapidly (within 10 min) called‘AMpathway’(SmithandRead2008;Smithand
inducethedepletionofPIN1fromtheplasmamembrane Smith 2011). AM symbiosis is one of the most wide-
ofstemxylemparenchymacells(Shinoharaetal.2013). spread plant associations with beneficial microorgan-
Although GR24 application also caused a reduction of isms. About 80 % of land plants, including most agri-
PIN1proteinlevelsintheprovascularregionofroottips culturalandhorticulturalcropspecies,areabletoestab-
(Ruyter-Spira et al. 2011), this was only observed after lishthistypeofsymbiosiswithfungifromthephylum
6 days when seedlings were grown in the continuous Glomeromycota (Barea et al. 2005; Smith and Read
presence of GR24, and is therefore likely a secondary 2008).Itisolderthan450millionyearsandisconsid-
effect due to reduced auxin import from upper parts of ered a key step in the evolution of terrestrial plants
theplant.Still,adirecteffectonauxintransportcapacity (Smith and Read 2008). By this mutualistic beneficial
in certain regions of the root tip cannot be excluded. association, the fungus obtains photoassimilates from
Recently, it was indeed observed that GR24 stimulates the plant to complete its lifecycle. In turn, it helps the
polar localization of PIN2 in the plasma membrane of plant in the acquisition of water and mineral nutrients,
root epidermal cells (Pandya-Kumar et al. 2014). Thus, mainlyPandnitrogen.AMfungiareobligatebiotrophs
SLsseemtoregulateRSAbyactingasmodulatorsofthe thatcolonizethe rootcortexofthe hostplant,forming
auxin flux hereby altering auxin levels according to the specialized and highly branched tree-like structures
environmentalconditions.Withrespecttotheinteraction called arbuscules in the cells of the host, where the
with ethylene, it was proposed that SLs promote its nutrientexchangebetweenthetwopartnerstakesplace
biosynthesis, which in turn induces auxin biosynthesis, (Genre et al. 2013; Gutjahr and Parniske 2013). The
transport and signalling in the roots (Stepanova and hyphaeofthefungusgrowintothesoilfarbeyondthe
Alonso2009).ThisSL-ethylene-auxincross-talkhason- root rhizosphere and develop an extensive hyphal net-
lybeenproposedfortheregulationofroothairelongation workthattakesupPviafungalhigh-affinitytransporters
(Kapulniketal.2011b),althoughitisverylikelythatit (Harrison2005;SmithandSmith2011),thusactingas
may also be involved in the regulation of lateral root ‘helperroots’thatcansearchforPbeyondthePdeple-
development,aswellasinotherSL-mediatedprocesses. tionzone.Accordingly,symbiosisestablishmentispro-
AlthoughwehavesomeideasabouthowSLsactin motedunderPdeficiencyconditions(Table1)(Fusconi
regulatingrootarchitecture,wearestillfarfromunder- 2014;Harrison2005;SmithandRead2008).Astimu-
standing the exact mechanism and its regulation by latoryeffectofnitrogendeficiencyhasalsobeenreport-
environmental conditions. In addition, other phytohor- ed (Table 1), although its effect seems to be generally
mones such as auxin, ethylene, ABA, gibberellins and weaker than that observed for P (Correa et al. 2014;
cytokinins have been shown to be involved in RSA Nourietal.2014).Thelevelsofotheressentialmineral
regulationand shouldbeincludedinthiscomplexsig- nutrients such as iron, potassium and calcium do not
nallingnetwork. appear to exert any effect on mycorrhizal colonisation
(Fusconi2014;Nourietal.2014).
Mycorrhizal plants can be colonized by several dif-
AlternativestrategiesforPuptake:arbuscular ferentspeciesofAMfungi,suggestingthatthereislittle
mycorrhizas host-specificity. However, there are differences in the
symbiotic efficiency of one AM species on different
Thesoilecosystemisoneofthemainfactorsinvolvedin plantspeciesanddifferentAMspeciesdisplaydifferent
nutrient cycling and plant productivity, which is inti- capacityofcolonisationononeplantspecies(Smithand
mately related to the associated microbiota (van der Read2008).Ingeneral,AMsymbiosispositivelyaffects
Heijden et al. 2008). Root architecture is not only of plant development and plant fitness, especially under
greatimportancefortheuptakeofnutrientsandwater,it unfavourableconditions.However,neutralorevenneg-
isalsovital for the anchorage inthe soiland the inter- ativeeffectsonplantgrowth,attributedtoPdeprivation
action with symbiotic organisms (Den Herder et al. and an excessive carbon use by the AM fungus, have
8 PlantSoil(2015)394:1–19
also been described (Grace et al. 2009; Li et al. 2008; chitin oligomers - into the rhizosphere that act as mo-
SmithandSmith2012).Thenegativeplantresponseto lecularcuesindicatingthepresenceofthefungusinthe
AM colonisation has been proposed to be associated vicinityofthehostrootandinducingtheplantresponses
with the reduced P absorption capacity by the ‘direct required for a successful colonisation (Bucher et al.
pathway’ induced by the symbiosis and to a lower P 2014; Genre et al. 2013; Maillet et al. 2011). Myc
uptake capacity by the AM fungus through the ‘AM factors consist of a mixture of sulphated and non-
pathway’(SmithandSmith2012).Therefore,searching sulphated simple lipochito-oligosaccharides that have
fortheoptimal‘dancepartner’iscrucialforamutualis- structural similarities with the rhizobial Nod factors
ticbeneficialassociation. (Maillet et al. 2011). Maillet and co-workers showed
It is well known that phytohormone homeostasis is thatthese compounds are not only symbiotic cuesthat
altered during AM symbiosis establishment and func- stimulateAMestablishment,butalsoactasplantgrowth
tioning (Bucher et al. 2014; Foo et al. 2013a; Gutjahr regulators affecting the formation of lateral roots, the
2014; Pozo et al. 2015). Some phytohormones control AMfungalentrysites.Interestingly,ithasbeendemon-
the early steps of the interaction regulating root mor- stratedthattheadditionofGR24elicitstheproduction
phology and preparing the plant to accommodate the ofshortchitinoligomersintheAMfungusRhizophagus
fungus,othersareinvolvedinlaterstagescontrollingthe irregularis (formerly known as Glomus intraradices)
extension of colonisation and/or the lifespan of the (Genre etal. 2013).Therefore, it seems thatboth part-
arbuscules and some hormones can be involved at the ners mutually sense each other and that they respond
differentstagesofthesymbiosis.Despitetheirregulato- accordingly. Indeed, using a split-root system with to-
ryfunctionsasplanthormones,SLswereinitiallyiden- matoplants,wehaverecentlyobservedthatSLproduc-
tifiedassignallingmoleculesintherhizosphere,where tion was higher in roots inoculated with R. irregularis
they wereshown toact ashyphal branching factors of compared with non-inoculated roots during the early
AMfungioftheGigasporaceaeandgerminationstimu- stages of interaction/colonisation (López-Ráez et al.
lants in a number of AM fungi of the Glomeraceae 2015).Thisobservationsuggeststhattheplantisreally
(Akiyama et al. 2005; Besserer et al. 2006). It is pro- sensing the presence of the fungus and that it actively
posed thatplants themselves are ableto actively influ- reactstofavourfungaldevelopmentand symbiosis es-
encethelevelofmycorrhizalcolonisationbycontrolling tablishmentbypromotingSLproduction.SLsalsopro-
the production of SLs depending on the P status mote lateral root formation (Ruyter-Spira et al. 2011),
(Table 1) (Foo et al. 2013b; López-Ráez et al. 2008a; therefore, this initial fungal-mediated induction of SLs
Yoneyamaetal.2007,2012).However,theexistenceof mayservetoincreasethenumberofcolonisationsites.
additional molecular signals during the early stages of The characterization and a better knowledge on the
theinteractionhasbeenalsosuggested(Balzergueetal. specificity of these pre-symbiotic signals should pave
2011).SLperceptionbyasofaruncharacterizedrecep- the way for the development of new environmentally-
tor in the AM fungus induces profuse hyphal growth friendlyagriculturalstrategiesbasedonAMsymbiosis.
and branching - the so-called pre-symbiotic stage -,
increasing the chance of encountering the roots of the
host plant and facilitating symbiosis establishment
(Akiyamaetal.2005;Bessereretal.2006).Uponrec- EffectofotherabioticstressesonSLproduction
ognitionofthefungalpartner,theplantactivelyaccom- andAMsymbiosis
modates the fungus within the roots (Bonfante and
Genre2010;GutjahrandParniske2013),butalsocon- Innature,plantsaregenerallyexposedtocombinationsof
trols its proliferation and arbuscule development unfavourable environmental conditions. Besides a better
(Reinhardt 2007; Walter 2013). While the importance nutrient supply, AM symbiosis provides also increased
ofSLsintheinitialstagesofAMfungalcolonisationis tolerance against other abiotic stresses such as heavy
wellaccepted,itisnotclearwhethertheyalsoplayarole metals, drought and salinity (Aroca et al. 2013; Evelin
insubsequentstepsofthesymbiosis. andKapoor2014;Lietal.2014;Ruiz-Lozanoetal.2012;
In addition to SL signalling by the plant, and also Singhetal.2011).Sofar,thereare,however,noindica-
beforesymbiosisestablishment,AMfungiproduceand tions that these stresses also have an (positive) effect on
release diffusible compounds - Myc factors and short symbiosisestablishment,incontrasttoPshortage.
PlantSoil(2015)394:1–19 9
Water-relatedstresses stress reduced SL production also in a dose-
dependent manner (Table 1) (Aroca et al. 2013;
Inrecentyears,harmfuleffectsofwater-relatedstresses López-Ráez et al., unpublished data). A negative
such as drought and salinity are rising dangerously, effect on SL production in the absence of mycorrhi-
having a major impact on plant growth and develop- zal colonization has also been observed in Lotus
ment,andbeingthemostimportantfactorslimitingcrop japonicus plants subjected to osmotic stress
productivity (Albacete et al. 2014; Sunil Kumar and (Table 1) (Liu et al. 2015). These results might sug-
Garampalli2013).Moreover,globalchangeiscontrib- gestthatplantssensethepresenceoftheAMfungus
utingtospreadtheseproblemsworldwide(Chavesand and that they respond by producing SLs under
Oliveira 2004). Therefore, improving the yield under unfavourable conditions to improve colonization. A
these stress conditions is a major goal nowadays. A relationship between drought and salinity with SLs
concept associated to the adaptation to water related has also been proposed in the non-mycorrhizal plant
stresses is the water use efficiency (WUE), defined as Arabidopsis (Ha et al. 2014). Here, a positive effect
theamountofdrymatterorharvestableyieldproduced of SLs on the tolerance to these stresses was ob-
perunitofwater.AMsymbiosishasthecapacitytoalter served. Ha and co-workers showed that SL-deficient
root hydraulic properties, thus helping the plant in the mutants were hypersensitive to drought and salt
uptake of water under unfavourable conditions. As a stress, and that this phenotype was rescued by exog-
consequence, mycorrhizal plants show a higher WUE enous GR24 application. The authors also showed
androotturgor,alleviatingthenegativeeffectsofwater that wild-type plants treated with GR24 were more
shortage on plant physiology (Al-Karaki et al. 2004; tolerant to these stresses than untreated plants (Ha
Augé et al. 2015; Bárzana et al. 2014; Li et al. 2014; et al. 2014). The results from lettuce, tomato and
WuandXia2006).Thiseffecthasbeenassociatedtoan Arabidopsis suggest a different behaviour between
improved nutrient uptake in mycorrhizal plants, which mycorrhizal and non-mycorrhizal plants in response
promotes the photosynthetic capacity and growth (Li to water-related stresses. However, more knowledge
et al. 2014; Smith et al. 2010). However, the extent of isrequiredtodecipherhowSLregulationisinvolved
the benefits depends on both the host plant and AM in these stress responses and how this regulation is
fungal species (Augé et al. 2015). On the other hand, affected by and/or affects AM symbiosis.
theexpressionofgenesencodingaquaporinsisalteredin Asinpreviouscases,thealterationinthephytohor-
mycorrhizal plants which may play a role in the im- mone homeostasis in mycorrhizal plants has been im-
provedwaterstatusinAMplants,althoughtheirregula- plicatedintheenhancedtoleranceagainstthesestresses
tiondependsonthetypeandseverityofthestress(Aroca and here, ABA signalling is the most studied pathway
etal.2007;Bárzanaetal.2014;Uehleinetal.2007). (Calvo-Polanco et al. 2013; Ruiz-Lozano et al. 2012).
Even though it is evident that under drought or ABA isconsideredasthe ‘stresshormone’,asitaccu-
salinity AM plants perform better than non- mulates rapidly in response to drought and salinity
mycorrhizalones,theeffectsofwater-relatedstresses (Hong et al. 2013). Interestingly, a reduction in ABA
in AM symbiosis establishment is not clear and content has been reported in mycorrhizal roots (Aroca
sometimes contradictory (Table 1). Interestingly, an et al. 2008, 2013; Duan et al. 1996; Estrada-Luna and
increasedSLproductionundersaltstressinthepres- Davies 2003; Fernández et al. 2014), suggesting that
ence of the AM fungus R. irregularis was shown in AMplantsarelessstressedthannon-mycorrhizalones.
lettuce (Table 1) (Aroca et al. 2013), which might Incontrast,whenstressed,anincreaseinABAcontentis
indicate the activepromotionofsymbiosisestablish- generally observed in mycorrhizal plants (Aroca et al.
ment. Similarly, the promotion of SL production in 2013;Calvo-Polancoetal.2013),whichhasbeenasso-
mycorrhizal plants has also been observed in lettuce ciatedwithprimingforincreasedstresstolerance.ABA
and tomato under drought stress (López-Ráez et al., is also necessary for a proper establishment and func-
unpublisheddata).Inbothcases,theinductionofSLs tioning of the AM symbiosis. It positively regulates
occurred in a dose-dependent manner, with the arbuscule development and functionality (Herrera-
greatest increase under the strongest stress. A differ- Medina et al. 2007; Martín-Rodríguez et al. 2011).
ent behaviour was observed in the absence of Thus,theincreasedABAlevelsinstressedplantswould
mycorrhization under salinity or drought, where the serve to promote tolerance against stresses, but also to
10 PlantSoil(2015)394:1–19
enhanceandmaintainthesymbiosis.Interestingly,there SLsinotherplantrhizosphereinteractions
alsoseemstobearelationshipbetweenABAandSLs.It
was shown that the tomato ABA-deficient mutants Plant-microbeinteractions
notabilis, sitiens and flacca, blocked at different steps
oftheABAbiosyntheticpathway,andwild-typeplants The rhizosphere is the narrow soil zone surrounding
treatedwithspecificABAinhibitorsproducedlessSLs plantrootsandconstitutesaverydynamicenvironment.
(López-Ráezetal.2010b).Moreover,acorrelationbe- In addition to AM fungi, it harbours many different
tweenABAandSLlevelswasreportedinmycorrhizal organisms and is highly influenced by plant root exu-
lettuceplantssubjectedtosaltstress(Arocaetal.2013). dates (Badri et al. 2009; Bais et al. 2006; Barea et al.
It seems, thus, that SLs play a dual role under stress 2005). Recently, a role for SLs in another important
conditions. On the one hand, they act as signalling beneficialplant-microorganismassociationintherhizo-
moleculesintherhizospherefavouringAMsymbiosis. sphere-nodulation-wasdescribed(Fig.1)(DeCuyper
Ontheotherhand,theyformpartoftheintegrativeplant et al. 2015; Foo and Davies 2011; Soto et al. 2010).
hormonal response to unfavourable conditions, Nodulationisestablishedbetweenlegumesandcertain
interacting with ABA and probably with other stress- rhizobacteriacollectivelyknownasrhizobia,anddates
relatedphytohormonestomaintainthesymbiosisatan backabout60millionyears(GargandGeetanjali2007).
optimallevel. Thissymbiosis is characterized by the development of
nodules on the plant roots, where rhizobia fix atmo-
Otherstresses spheric nitrogen, thus improving plant nutrition.
Nodules provide the proper micro-environment for ni-
StudiesontheinfluenceofotherabioticstressesonAM trogenfixationandnutrientexchangewiththehostplant
symbiosis are scarceand usually contradictory. Aneg- in return for photoassimilates (Garg and Geetanjali
ative effect of low temperature was reported in wheat 2007; Oldroyd and Downie 2008). Accordingly, an
and sorghum, while no effect was observed in rice increase in SL production under nitrogen deficiency
(Table 1) (Augé et al. 2004; Hetrick et al. 1984; Liu has been shown to occur in pea (Table 1) (Foo et al.
et al. 2013). Conversely, a positive effect of high tem- 2013b),butalsoinsomenon-legumeplantspeciessuch
peratureonthesymbiosishasrecentlybeenreportedin asrice,sorghum,wheatandlettuce(Table1)(Jamiletal.
Medicago truncatula (Table 1) (Hu et al. 2015). In 2011a; Yoneyama et al. 2007, 2012). Just as for AM
relation to heavy metals, an inhibitory influence of symbiosis,nodulationrequiresahighdegreeofcoordi-
cadmium on the AM fungus Funneliformis mosseae nationbetweenthetwopartnersbasedonacoordinated
(formerly Glomus mosseae) was detected in wheat molecular communication (Murray 2011; Oldroyd and
(Table1),althoughmycorrhizalplantsweremoretoler- Downie2008).However,hereSLsdonotseemtoactas
antthannon-mycorrhizal(Shahabivandetal.2012).A hostdetection signals (Soto etal. 2010).The chemical
negative effect on AM colonisation was also observed dialogueisinitiatedwiththeproductionandexudation
for copper in maize (Table 1) (Hagerberg et al. 2011). of specific flavonoids by the host plant (Badri et al.
Aluminium affected different species of AM fungi in 2009; Hassan and Mathesius 2012). These flavonoids
broomsedge (Andropogon virginicus), ranging from a act as attractants for rhizobial bacteria and inducers of
negativetoapositiveeffect,dependingontheconcen- Nod factor biosynthesis, which are structurally similar
tration (Kellyetal. 2005).Asfar asweknow, nodata totheAMfungalMycfactors(seeabove)(Mailletetal.
about the influence of these abiotic stresses on SL 2011).AlthoughSLsdonotseemtobeinvolvedinthe
biosynthesis have been reported so far. In any case, it pre-symbiotic stage, it has been shown that they are
seemsthat,unlikeforthenutritionalstress,theeffectsof required for optimal nodule number formation (Foo
other abiotic stresses on SLs and AM symbiosis differ and Davies 2011). Foo and Davies observed that the
betweendifferentspecies ofhostplantsand AMfungi pea SL-deficient mutant rms1 (mutated in CCD8)
and probably depend on the severity of the stress. established about 40 % less nodules than the corre-
Furtherresearchisrequiredtoascertainwhetherthisis spondingwild-type,andthatthephenotypewaspartial-
thecase,butalsotounderstandwhetherandhowthese lyrescuedbyexogenousGR24application.Moreover,
stressesregulateSLproductionandAMsymbiosis,and theyshowedthatGR24increasedthenodulenumberin
viceversa. wild-typeplants(FooandDavies2011).Morerecently,