Journal of Experimental Botany,Vol.60,No.7,pp.1979–1989,2009 doi:10.1093/jxb/erp040Advance Access publication5March,
2009
FLOWERING NEWSLETTER REVIEW
Gibberellin as a factor infloral regulatory networks
Effie Mutasa-Go¨ttgens1and Peter Hedden2,*
1Broom’s Barn Rearch Centre,Rothamsted Rearch Department of Applied Crop Science,Higham,Bury St Edmunds,Suffolk IP28 6NP,UK
2Rothamsted Rearch,Harpenden,Herts AL52JQ,UK
Received11December2008;Revid29January2009;Accepted2February2009
Abstract
Gibberellins(GAs)function not only to promote the growth of plant organs,but also to induce pha transitions during development.Their involvement inflower initiation in long-day(LD)and biennial plants is well established and there is growing insight into the mechanisms by whichfloral induction is achieved.The extent to which GAs mediate the photoperiodic stimulus toflowering in LD plants is,with a few exceptions,less clear.Despite evidence for photoperiod-enhanced GA biosynthesis in leaves of many LD plants,through up-regulation of GA20-oxida gene expression,a function for GAs as transmitted signals from leaves to apices in respon to LD has been demonstrated only in Lolium species.In Arabidopsis thaliana,as one of four quantitativefloral pathways,GA signalling has a relatively minor influence onflowering time in LD,while in SD,in the abnce of the photoperiod flowering pathway,the GA pathway assumes a major role and becomes obligatory.Gibberellins promoteflowering in Arabidopsis through the activation of genes encoding thefloral integrators SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1(SOC1),LEAFY(LFY),and FLOWERING LOCUS T(FT)in the inflorescence andfloral meristems,and in leaves,respectively.Although GA signalling is not required forfloral organ specification,it is esntial for the normal growth and development of the organs.The sites of GA production and action withinflowers,and the signalling pathways involved are beginning to be revealed.
Key words:Arabidopsis,DELLA,floral transcription factors,flower development,flower induction,gibberellin,LEAFY,Lolium, SOC1.
Introduction
The ability of gibberellins(GAs)to promote bolting and flower formation in long-day(LD)and biennial plants under conditions that would not normally permitflowering contributed to the realization that the compounds may function as endogenous growth regulators(Lang,1957). The bolting respon obtained in species such as Hyoscyamus niger(Lang,1956)is one of the most spectacular effects of applying GAs to plants and contributed to the excitement during the early years of GA rearch.Lang(1957) distinguished between the promotion of stem extension (bolting),which he considered a direct effect of GAs,and flower initiation,which he thought must be indirect since,in most species,it follows bolting.Lang discounted the possibility that GA could be a universalflowering stimulus (florigen)since he obtained no promotion offlowering by applying GAs to short-day(SD)plants,despite evidence from grafting experiments that LD and SD plants contain a common stimulatory substance.
qzoneAlmost40years after Lang’s publication,promising candidates forflorigen were identified as the protei
ns encoded by FLOWERING LOCUS T(FT)(Corbesier et al.,2007;Jaeger and Wigge,2007;Lin et al.,2007; Mathieu et al.,2007),and its rice equivalent Hd3a(Tamaki et al.,2007).While the role of GAs inflowering is becoming established for a limited number of species,GA is clearly not a universalflowering stimulus.In some species,such as
*To whom correspondence should be addresd.E-mail:peter.hedden@bbsrc.ac.uk
Abbreviations:AGL,AGAMOUS like;AP1,APETALA1;FM,floral meristem;GA,gibberellin;GAI,gibberellin innsitive;GID,gibberellin innsitive dwarf;IM, inflorescence meristem;LD,long-day photoperiod;RGA,repressor of ga1-3;RGL,repressor of ga1-3like;SAM,shoot apical meristem;SD,short-day photoperiod.ªThe Author[2009].Published by Oxford University Press[on behalf of the Society for Experimental Biology].All rights rerved.
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the LD grass Lolium temulentum there is convincing evidence that it acts as a mobile signal to transmit the photoperiodicflowering stimulus,while in others it appears to have little influence onflower initiation and in many perennials it inhibitsflowering.In Arabidopsis thaliana, a facultative LD and cold-responsive species,GA contrib-utes to one of four interacting pathways forfloral induction (Kobayashi and Weigel,2007;Simpson and Dean,2002), but it is still unclear to what extent GA mediates the environmental inputs to this respon.
Although theflowering role for GAs may be species-specific,their function inflower development is far more general and probably universal.In this review,the in-volvement of GAs infloral initiation and development are discusd at the physiological and molecular levels,drawing heavily from work with Arabidopsis and a limited number of other species.The review will include a consideration of flower development up to the establishment of fertility,but we will not discuss ed or fruit development,in which GAs also have important roles(Ozga and Reinecke,2003;
Serrani et al.,2007).Recent advances in our understanding of the GA-biosynthetic and signal transduction pathways (Ueguchi-Tanaka et al.,2007;Daviere et al.,2008;Hirano et al.,2008a;Itoh et al.,2008;Yamaguchi,2008)are critical to considering the involvement of GAs infloral initiation and development and will be discusd briefly in the following ction.
Gibberellin signalling
Gibberellins are required for the normal growth of almost all plant organs through the promotion of cell division and/ or cell elongation.In addition,they promote certain de-velopmental switches or pha changes,including ed germination and the juvenile to adult transition,as well as the transition from vegetative to reproductive development in some species.Although136different GA structural variants have currently been identified from plants,fungi, and bacteria(www.plant-hormones.info/ga1info.htm), only a limited number of compounds have intrinsic biological activity,with GA1and GA4being the major endogenous active molecules in most plant species.The GA signalling pathway(Fig.1),which includes biosynthesis,turnover and signal transduction,is tightly regulated by developmental and environmental cues,with the regulation of GA concen-tration being of primary importance(Yamaguchi,2008).The biosynthetic pathway to GA4from the common diterpene precursor trans-geranylgeranyl diphosphate compris12 steps catalyd by six enzymes,of which the2-oxoglutarate-dependent dioxygenas,GA20-oxida(GA20ox)and GA 3-oxida(GA3ox),that cataly thefinal steps,are major sites of regulation.A third group of dioxygenas,the GA2-oxidas,which by inactivating GAs and their immediate precursors contribute to turnover,are also highly regulated. The three dioxygena class are encoded by multi
ple genes, but there is not complete gene redundancy becau the paralogues differ in their expression patterns and regulation.
Gibberellin signalling promotes growth by initiating the degradation of DELLA proteins,which are growth-sup-pressing members of the GRAS family of transcriptional regulators.Perception of GA is by soluble nuclear-localized receptors,known as GID1,which,on binding GAs,un-dergo a conformational change that allows them to interact with the DELLA N-terminal domain(Mura et al.,2008; Shimada et al.,2008).It is propod that binding of DELLAs to GID1caus a conformational change in DELLAs,allowing them to bind to the F-box component of an SCF E3ubiquitin liga(Mura et al.,2008), targeting them for degradation via the ubiquitination/26S proteasome pathway.DELLAs have been shown to func-tion by interacting with transcription factors and blocking their activity.This was demonstrated for Arabidopsis hypocotyls,in which DELLAs interact with PHYTO-CHROME INTERACTING FACTORS(PIFs)and thereby suppress their ability to promote gene expression and growth(Feng et al.,2008;de Lucas et al.,2008). Removal of DELLAs as a result of GA action allows PIF function.Since PIFs are also regulated by light through phytochrome,they form a point of convergence between the light and GA growth regulatory pathways.DELLAs appear to have many targets(Zentella et al.,2007;Hou et al.,2008) and,although in
the above example they suppress gene expression,it is becoming clear that they up-regulate at least as many genes as they repress(Hou et al.,2008).DELLAs must,therefore,also function as transcriptional activators, perhaps in partnership with transcription factors or by inactivating transcriptional repressors.
Floral competence
Gibberellins may be involved in the developmental events leading to reproductive competence,as well as infloral determination and commitment.Reproductive competence is often manifested by early visual physiological激励的名人名言
markers Fig.1.Gibberellin signalling pathway.Regulation of the GA concentration is primarily via the biosynthetic enzymes GA20ox and GA3ox,and the inactivating enzymes GA2ox.Bioactive GAs promote binding of the GID1receptor to DELLA proteins,which initiates DELLA degradation via the ubiquitination/26S proteasome pathway.DELLAs function as transcriptional regulators in combi-nation with transcription factors.
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such as internode elongation(bolting),which,in many monocarpic plants,is widely regarded as indicative of the physiological transition to reproductive growth,even though plants may still be growing vegetatively at this stage.The determination of developmental reprogramming leading toflowering is less visible,eventually leading to the formation offloral meristems.In Arabidopsis this is mediated by the transition of the vegetative meristem to the inflorescence meristem(IM),which then enables a commit-ment toflowering through the differentiation of cells in the peripheral zone(lateral anlagen)of the IM to producefloral meristems(FM).Distinctions between the different types of meriste
ms exist not only at the morphological level but also at the molecular level through the spatial and temporal expression of gene regulatory networks defining phyllotaxy and organ development at the shoot apex(Doerner,2003; Sablowski,2007).
Reproductive competence,when the shoot is capable of responding to the external and endogenous inductive cues forflowering,requires the transition from the juvenile to the adult growth pha(Poethig,2003).This transition is often associated with changes in leaf morphology,surface struc-ture(waxiness,trichomes)and leaf vein development and has been widely studied in maize and Arabidopsis(Evans and Poethig,1995;Chien and Susx,1996;Dill and Sun, 2001),where GA acts to promote the transition to the adult pha.The role of GAs in developmental transitions reflects their increasingly recognized function as integrators of wide-ranging developmental and environmental signals through DELLA-mediated pathways(Daviere et al.,2008), coupled with their ability to interact with other plant hormones at different levels throughout development(Weiss and Ori,2007).With the possible exception of the phyto-chromes,no otherfloral initiation factors identified so far participate in vegetative transitions to a similar extent as GAs.However,some evidence of overlap between the regulation of vegetative andfloral transitions is starting to emerge.For example,miRNA172,which is involved in the regulation offloral homeotic genes(Aukerman and Sakai, 2003;Chen,2004)and theflor
al integrator FT(Jung et al., 2007),is now also known to control the juvenile to adult pha change in maize(Lauter et al.,2005).
In some species,competence toflower requires prolonged exposure to low temperature(vernalization).In the LD grass species Lolium perenne,exogenous GA allowed flowering in non-inductive SD conditions only in vernalized plants,whilst non-vernalized plants were unable to respond to GA either by stem elongation orflowering(MacMillan et al.,2005).The lack of respon to GA occurred despite an active GA signalling system,becau DELLA protein abundance was reduced by GA treatment.The limiting factor in this ca could lie down-stream of DELLA or in a non-related pathway;it was not attributed to the action of abscisic acid(ABA),which commonly antagonizes GA signalling.Vernalization-induced bolting is a prerequisite forflowering in the LD sugar beet plant,in which,as in L. perenne,GA can compensate for LD,but not vernalization, with only limited initiation of stem elongation in non-vernalized plants in both LD and SD(ES Mutasa-Gottgens
and P Hedden,unpublished results).Thus,at least in L. perenne and sugar beet,the GA/LD inductive pathway is blocked unless plants are vernalized,although,as reported
by Lang(1957),GA can substitute for vernalization in
a number of biennial species.
Floral induction
A role for GAs inflower induction in reproductively competent plants has been established primarily for LD
and biennial species,in whichflowering in non-inductive conditions can be achieved by the application of GAs (Zeevaart,1983;King et al.,2001).The transition to reproductive development in rotte plants,is frequently
signified by bolting of the main axis,a process that involves
GA-dependent cell division and elongation(Sachs and Lang,1957;Silverstone and Sun,2000),and has been directly correlated with incread bioactive GA in the shoot apex,as,for example,in spinach(Talon et al.,1991),field pennycress(Metzger,1985)and sugar beet(Debenham, 1999;Sorce et al.,2002).In sugar beet,as in many other biennial species,reproductive competence is achieved only
after bolting(Mutasa-Gottgens et al.,2008),which always precedesflowering.
In Arabidopsis,bolting,unlikeflower induction,has an absolute requirement for GA signalling,since the highly
GA-deficient mutant ga1-3(Koornneef and van der Veen, 1980)and plants lacking GA receptors(Griffiths et al., 2006)are verely dwarfed,regardless of photoperiod.The number of internodes that elongate from within the rotte
冬至英语as well as theirfinal length is limited by GA content(Rieu
et al.,2008a).Bolting is preceded byflower initiation,for which the photoperiod-induced CONSTANS(CO)/FT pathway appears to dominate in LD(Kobayashi and Weigel,2007;Turck et al.,2008).However,the delayed
flowering of ga1-3(Wilson et al.,1992)and the triple gid1 mutant(Griffiths et al.,2006)in continuous light or LD, respectively,indicates that the GAflowering pathway makes some contribution tofloral induction even when the
CO pathway is active.New data from Arabidopsis now indicate that GAs may act via FT(a key target of CO)as
well as independently to induceflowering,as,in LD,GA4自然状态
was found to promote FT expression in wild-type(Col-0) plants and to be required for FT expression in ga1-3(Col-0) (Hisamatsu and King,2008).In SD,when expression of FT
is low(Wigge et al.,2005),flowering in Arabidopsis is absolutely dependent on GA signalling(Wilson et al.,1992) although this may not directly involve FT,since there is
little promotion of FT expression by GA in SD(Moon
et al.,2003;Hisamatsu and King,2008).Indeed,Hisamatsu
and King(2008)confirmed the FT-independent role for红楼梦里的人物
GA4,which rescued the lateflowering phenotype in the ft-1 mutant in both LD and SD.Gibberellin and FT have been shown to act independently in Lolium temulentum,in which
吕文静GA application did not increa FT expression in LD or SD (King et al.,2006).Hisamatsu and King(2008)have
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recently reported that ga1-3plants grown in SD for3months did notflower after30subquent LD,but could be induced toflower by treatment with GA4.The reason for the discrepancy between the results and tho from numerous others showingflowering of this mutant when expod to LD from germination is unclear,but may be related to the age of the plants whenfirst receiving LD(Hisamatsu and King,2008).To add further to the confusion,there are reports that triple gid1mutants lacking GA receptors fail toflower in LD(Iuchi et al.,2007;Willige et al.,2007)in contrast to thefinding of Griffiths et al.(2006).In this ca, the explanation could be differences in light quality or intensity:the promotion offlowering by far-red-rich in-candescent light,as well as by photosynthetically active radiation,possibly mediated by sucro,was highlighted recently(King et al.,2008a).
The extent to which GA mediates photoperiod-induction offlowering rather than having a purely permissive role is probably dependent on species.There have been numerous reports showing incread GA biosynthesis when LD plants are transferred from SD to LD,regulation being primarily on the expression of GA20ox genes(Wu et al.,1996;Xu et al.,1997;Hisamatsu et al.,2000;King et al.,
2006;Lee and Zeevaart,2007).In spinach,SoGA20ox1transcript and the encoded protein incread in leaves and shoot apices when plants were transferred from SD to LD,although the change was too slow to account for the rapid induction of stem extension under the conditions(Lee and Zeevaart, 2007).Transcript was detected by in situ hybridization in the shoot apical meristem,as well as in leaf andflower primordia,but not in the expanding subapical region, indicating that stem extension was dependent on the import of active GAs or precursors to this region or that a different SoGA20ox paralogue was expresd there.Leaf expression of the Arabidopsis GA20ox paralogue AtGA20ox2is re-stricted to the petiole where it is up-regulated by far-red-rich LD via phytochrome B(Hisamatsu et al.,2005; Hisamatsu and King,2008).Loss of AtGA20ox2delays flowering in LD and especially in SD,whereas AtGA20ox1, which shows a circadian expression pattern in the leaf blade and petiole,has much less influence onflowering time (Hisamatsu and King,2008;Rieu et al.,2008a).This latter gene,however,is the predominant GA20ox paralogue expresd in Arabidopsis stems and has a major influence on stem extension during bolting(Koornneef and van der Veen,1980;Rieu et al.,2008a).
A function for GAs as mobile signals forflower induction has been investigated in veral studies.In Arabidopsis growing in SD,GA4accumulated in the shoot apex prior to thefloral transition(Eriksson et
al.,2006).This accumulation was not correlated with changes in expression of GA-biosynthetic genes in the apex,indicating that the GA originated from elwhere.It was possible to demon-strate movement of exogenous labelled GA4from leaves to the apex,but the authors did not report on changes in GA4 biosynthesis in leaves beforefloral initiation.In the LD grass, Lolium temulentum,photoperiod induction was shown to be followed rapidly by incread GA20ox expression in the leaf and accumulation of theflorally inductive GA5at this site (King et al.,2006),and in the shoot apex(King et al.,2001). Treating plants with the GA-biosynthetic inhibitor paclobu-trazol prevented LD-inducedflowering,but only when applied before induction,indicating an absolute GA re-quirement forflower initiation(King et al.,2006).
Unlike Arabidopsis,in which GA4is the principal active compound for bothfloral initiation and stem extension (Eriksson et al.,2006),L.temulentum us different GAs for the functions,with GA5,and possibly GA6,rving as floral inducers,but having weak stem extension activity.On the other hand,GA1and GA4,which are strongly growth promoting,but lessflorigenic,accumulate in leaves and shoot apices of ulentum plants more slowly than does GA5(King et al.,2006).It was suggested that GA1and GA4may promote inflorescence differentia-tion and stem extension once thefloral transition has occurred(King et al.,2001).This structural specificity is unlikely to be due to th
正月十e u of different GA receptors for the functions,but may be related to the rate at which the compounds are inactivated(King et al.,2008b).Gibberellin A5,which on account of its2,3-double bond is protected from2b-hydroxylation,would escape inactivation by GA2-oxidas that are expresd immediately below the shoot apical meristem(SAM).Indeed,this GA was shown to be metabolized more slowly than GA1and GA4in isolated shoot apices ulentum(King et al.,2008b).Such a role for GA2-oxidas,in which they restrict access of bioactive GAs to the SAM,was propod from work with rice,in which GA2ox gene expression,located in the rib meristem below the SAM,was reduced following thefloral transition,so allowing GAs to enter the SAM(Sakamoto et al.,2001a).A similar reduction in expression at the shoot apex afterfloral induction was noted for one of two GA2ox genes monitored ulentum(King et al.,2008b). While a pattern of GA2ox gene expression at the shoot apex comparable to that in rice has been reported in Arabidopsis (Jasinski et al.,2005),there is no evidence for a change in expression corresponding withfloral induction(Eriksson et al.,2006).Nevertheless,loss of GA2ox gene expression in Arabidopsis advancesflowering time,particularly in SD, with AtGA2ox4making the largest contribution to this effect(Rieu et al.,2008b).Expression of this paralogue is mainly restricted to the shoot apex,whereas most other AtGA2ox genes have a broader expression pattern(Jasinski et al.,2005;Rieu et al.,2008b).Exclusion of GA from the vegetative SAM is also thought to be necessary for maintaining its indeterminacy;KN
OTTED1-type homeo-box transcription factors have a prominent role by pro-moting GA2ox while repressing GA20ox expression (Sakamoto et al.,2001b;Hay et al.,2002;Jasinski et al., 2005).
The evidence discusd above strongly indicates that GAs act directly to induce thefloral transition at the shoot apex, although they may also promote formation of other mobile signals,such as FT(Hisamatsu and King,2008).In Arabidopsis the switch from a vegetative meristem to an IM coincides with the expression of molecular markers such as
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SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1(SOC1),SHORT VEGETATIVE PHASE (SVP ),and AGAMOUS Like 24(AGL24),whilst formation of FM is promoted by LEAFY (LFY )and APETALA 1(AP1),which have also been shown to repress the activity of the IM genes (Liu et al.,2007).Once established,the IM generally grows indeterminately,continuously generating new lateral mer-istems,while the FM always commits to flowering and terminates with floral organs (Soue
r et al.,2008).Gibber-ellins promote expression of both SOC1(Bonhomme et al.,2000;Moon et al.,2003)and LFY (Blazquez et al.,1998)by independent DELLA (GAI/RGA)-mediated pathways that directly,or indirectly via GAMYB (Gocal et al.,1999,2001),modulate the expression of SOC1and LFY ,re-spectively (Achard et al.,2004)(Fig.2).LFY integrates the LD and GA pathways,through parate cis elements on its promoter (Blazquez and Weigel,2000),while SOC1integra-tes the autonomous/vernalization and GA pathways (Moon et al.,2003).SOC1and AGL24bind to each other’s promoters to create an autoregulatory feedback loop (Liu et al.,2008),and the SOC1/AGL24heterodimer is required for nuclear localization and transcription of LFY (Lee et al.,2008).Gibberellins therefore have an additional indirect route for up-regulating LFY via SOC1and probably also control levels of LFY through the DELLA-dependent regulation of miRNA159which,in Arabidopsis ,negatively regulates MYB33required for LFY transcription (Achard et al.,2004).Different GAs were shown to promote LFY
expression at the Arabidopsis shoot apex and to induce flowering in SD with similar activities,supporting the causal relationship between the events (Eriksson et al.,2006).The expression domains of LFY and SOC1are known to be overlapping within the transitional meristem (Parcy,2005;Turck et al.,2008),and it is reasonable to assume that GAs,in combination with endogen
ous (her hormones)and external (light and temperature)signals,may influence the biological switch that determines cell fate in both the inflorescence and floral meristems.
Flowering in perennial species
The role of GAs in flowering in perennials has mainly been studied in fruit trees (reviewed by Wilkie et al.,2008),in which GAs are generally inhibitory to flowering.In apples,since applied GA and the prence of eded fruit inhibits floral initiation it has been suggested that eds,a rich source of GAs,export the hormones to the buds (Hoad,1978).However,it has been difficult to obtain convincing evidence for the transport of GAs from eds in sufficient quantities and it was propod that in fact auxin is the mobile inhibitory factor (Bangerth,2006).Applied GAs might suppress floral initiation by enhancing the polar transport of IAA from eds.Alternatively,if GAs are indeed floral inhibitors,IAA may stimulate their synthesis in the bud.It has also been suggested that GAs
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Fig.2.Schematic reprentation of events leading to GA-induced floral transition in Arabidopsis .In the leaf,phytochrome-mediated up-regulation of GA20ox results in incread GA concentration,which may up-regulate FT ,also under photoperiod control,via CO.GA and FT protein move from the leaf to the shoot apex.Inactivation of GA by GA2ox in the rib meristem regulates the a
mount of GA entering the shoot apical meristem,where it activates SOC1and LFY via repression of the DELLAs GAI and RGA.Red arrows (promotion)and T-bars (repression)indicate steps that immediately affect or are affected by GA.Boxed numbers refer to supporting data for the reprented scheme as follows:(1)Achard et al.,2004;(2)Liu et al.,2008;(3)Lee et al.,2008;(4)Liu et al.,2007;(5)Gocal et al.,2001;(6)Hisamatsu and King,2008;(7)Hisamatsu et al.,2005;(8)Jasinski et al.,2005.*Authors prented data to show that the two pathways are independent.
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