Update on Light, Oxygen, and Bud Burst

Roles for Light, Energy, and Oxygen in the Fate ofQuiescent Axillary Buds1[OPEN]

Santiago Signorelli,a,b,d,g,2 Patricia Agudelo-Romero,a,b,d,f,2 Karlia Meitha,b,d Christine H. Foyer ,a,c,3 andMichael J. Considinea,b,c,d,e,3

aSchool of Molecular Science, The University of Western Australia, Perth, Western Australia 6009, AustraliabSchool of Agriculture and Environment, The University of Western Australia, Perth, Western Australia 6009,AustraliacCentre for Plant Sciences, School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS29JT, United KingdomdUWA Institute of Agriculture, The University of Western Australia, Perth, Western Australia 6009, AustraliaeIrrigated Agriculture Development, Department of Primary Industries and Regional Development, SouthPerth, Western Australia 6151, AustraliafDepartamento de Biología Vegetal, Universidad de la República, Montevideo 12900, UruguaygARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, WesternAustralia 6009, Australia

ORCID IDs: 0000-0002-1854-3164 (S.S.); 0000-0002-3703-4111 (P.A.-R.); 0000-0002-8392-6807 (K.M.); 0000-0002-4468-6820 (M.J.C.);0000-0001-5989-6989 (C.H.F.).

The hierarchy of events governing the resumptionof growth of a quiescent axillary bud are poorly un-derstood. During quiescence, a homeostasis exists inphytohormone and source/sink regulation, whichrepresses the metabolic and mitotic progression of thebud. Environmental change and shoot developmentcan alter the homeostasis, leading to a binary statechange and the commitment to growth. Within thiscontext, light and oxygen availability can serve bothmetabolic and signaling functions. However, thequestion of substrate versus signal has proven chal-lenging to resolve; in the case of sugars, there are dis-parities in the data from apical and axillary buds injuvenile shoots, while in postdormant perennial buds,light has only a facultative role in the decision, butsignaling may still be essential for bud fate. We brieflyupdate the roles and hierarchies of light-, energy-, andoxygen-dependent functions in axillary bud outgrowthof annual shoots, before focusing discussion on the roleof chloroplast-to-nucleus retrograde signaling genessuch as GENOMES UNCOUPLED4 (GUN4) andELONGATED HYPOCOTYL5 (HY5) in bud burst re-sponses to light, examining available transcriptome

data from postdormant grapevine (Vitis vinifera) buds.We discuss the evidence implicating cryptochromes(CRY) in the activation ofHY5 expression in grapevine,leading to chloroplast biogenesis in the buds, and that

1 This work was supported by the Australian Research Council(DP150103211). C.H.F. thanks the Biotechnology and Biological Sci-ences Research Council (UK; BB/M009130/1) for financial support.

2 These authors contributed equally to the article.3 Address correspondence to c.foyer@leeds.ac.uk and michael.

considine@uwa.edu.au.M.J.C. and C.H.F. conceived the study; P.A.-R. reanalyzed data;

and M.J.C. and S.S. wrote the manuscript. All authors approved thearticle.

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this occurs via a biogenic rather than an adaptive de-velopmental process. The cytokinin (CK) signalingpathways and the light-regulated expression of chlo-roplast processes, especially those involved in carbonand oxygen metabolism, may also play an importantrole in bud burst.

The mechanisms that control apical dominance injuvenile or annual shoots are well characterized. Re-moving the apex can result in axillary bud outgrowth,as can changes in light intensity and quality. Here, ax-illary bud outgrowth is regulated by signals arisingfrom the apex, which contain several light quality andquantity sensing pigments. Of these, phytochromes(PHY) are perhaps the best characterized. PHY sensered and far-red light, while cryptochromes and photo-tropins are involved in the perception of blue light.These photoreceptors regulate the expression of differ-ent transcription factors to coordinate light-dependentphotomorphogenesis. Some plant species require lightfor axillary bud outgrowth (annual shoots), but inothers the requirement for light is facultative (Leducet al., 2014). In addition, the buds of many perennialplants can resume growth following a period of dor-mancy. In this case, apical suppression may tempo-rarily break down, and the axillary bud may beconsidered more independent, at least until a newhomeostasis is established along the shoot. Moreover,there is no evidence postdormant perennial buds re-quire light, although increased light intensity can ac-celerate bud burst in a range of species (Maynard et al.,1990; Rageau et al., 1998; Søgaard et al., 2008; Caffarraand Donnelly, 2011).

The influence of light on meristem activity involves atleast two distinct but possibly cross-regulatory processes:direct regulation of gene expression via photoreceptors,and an indirect process involving the generation of en-ergy through photosynthesis and respiration.A potentialthird pathway is the signaling of tissue oxygen status,which has been shown to be a primary cue for devel-opmental transitions in plants, including photomorpho-genesis (Considine et al., 2017).

In this Update, we consider the respective roles oflight, energy, and oxygen as primary cues for axillarybud outgrowth, with a particular focus on the signalingpathways that trigger the resumption of growth fol-lowing quiescence. We provide a concise overview of(1) the physiology of axillary meristems and buds, fo-cusing on genotypic differences in bud requirementsfor light and energy to trigger outgrowth, and (2)the importance of transcriptional regulation of plastidfunctions in the resumption of growth in quiescentgrapevine buds following dormancy.

LIGHT AND ENERGY DEPENDENCY OF AXILLARYBUD OUTGROWTH, AND A PUTATIVE ROLE FOROXYGEN-DEPENDENT SIGNALING

Vascular plants display indeterminate growth and abranched root and shoot structure, which is enabled by

the spatial distribution and activation of meristems(Sussex and Kerk, 2001). Most terrestrial species exhibitaxillary branching rather than the more ancestral di-chotomous branching. Axillary buds are classed assylleptic or proleptic, and both types may be quiescentfor sustained periods of time, being able to resumegrowth immediately upon perception of appropri-ate developmental, metabolic, or environmental cues.Additionally, proleptic buds of some species pos-sess the ability to exhibit true dormancy, which is adevelopmental and internally repressed condition thatrequires environmental entrainment to enable a tran-sition to quiescence (Considine and Considine, 2016).Dormant buds aremetabolically isolated from the shootby physiological barriers such as the deposition of cal-lose. In this situation, apical dominance in its strictestsensemay not apply, at least until dormancy is relieved.In the following discussion, we focus on quiescence andthe role of light in the processes promoting axillary budoutgrowth, particularly in intact juvenile or annualshoots.

The dominance behavior of the apical meristem,which enforces and maintains axillary bud quiescence,is facilitated by mobile signals such as Suc and phyto-hormones, particularly auxin. The role of apically de-rived auxin in maintaining axillary bud quiescence wasestablished nearly a century ago (Thimann and Skoog,1934; for a detailed review, refer to Rameau et al., 2015).However, auxin signaling intersects with other phyto-hormones such as strigolactones and CKs to regulatethe outgrowth of axillary buds. Each phytohormonefunctions downstream of light signaling pathways ini-tiated by photoreceptors (Leduc et al., 2014). Phyto-hormone signaling pathways are thought to convergeat the level of the BRANCHED1 transcription factor(and homologs), which is a central repressor of axillarybud outgrowth (Dun et al., 2012). However, auxintransport may be too slow to account for observed budoutgrowth kinetics, while Suc availability may providea more rapid regulatory trigger (Renton et al., 2012;Mason et al., 2014). The application of Suc results in adose-dependent activation of bud outgrowth, a processthat apparently antagonizes auxin- and strigolactone-mediated signaling, although Suc effects were at leastpartly independent of these pathways (Barbier et al.,2015a).

Light and Suc can act both as signals and sources ofenergy for bud growth. Suc functions both as a meta-bolic substrate and signal controlling development,notably via the TARGET OF RAPAMYCIN (TOR) ki-nase and SUCROSE NONFERMENTING1-RELATEDKINASE1 (SnRK1). Several species such as Rosa sp. andpea (Pisum sativum) require light for axillary bud out-growth, while others have varying facultative require-ments for light (Leduc et al., 2014). In axillary buds ofRosa sp., the expression of genes involved in Suc hy-drolysis and mobilization is promoted by light; how-ever, Suc cannot compensate for light in activating budoutgrowth (Girault et al., 2008). Application of Suc andnonmetabolizable analogs such as palatinose promotes

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the rate of bud outgrowth in Rosa, Arabidopsis (Arabi-dopsis thaliana), and pea when light is present (Rabotet al., 2012; Barbier et al., 2015b). These data suggestthat photoreceptor-mediated signaling is a primaryrequirement for bud outgrowth, and that Suc syn-thesis and metabolism via photosynthesis are essen-tial downstream components.Several lines of evidence suggest that Suc may func-

tion as a signal rather than energy substrate in aug-menting bud outgrowth (Barbier et al., 2015a). Thealtered shoot branching phenotype of Arabidopsismutants deficient in trehalose-6-P (T6P) cannot beexplained by metabolic or energy functions becauseT6P only accumulates to low concentrations even inwild-type plants (Chary et al., 2008). Overexpression ofHEXOKINASE1 leads to increased bud outgrowth andexpression of genes involved in abscisic acid-relatedprocesses, together with reduced expression of auxin-related genes (Kelly et al., 2012). Nevertheless, otherstudies have linked the effects of Suc to metabolic re-quirements (Leduc et al., 2014; Otori et al., 2017).Further insights into the question of whether Suc

acts as a signal rather than a substrate come fromstudies of the shoot apical meristem (SAM). Auxin-and Suc-mediated pathways independently promotethe cell cycle by activating TOR kinase, which in turndirectly activates key cell cycle regulators, as well asthe stem cell identity protein WUSCHEL (WUS;Pfeiffer et al., 2016; Li et al., 2017). The fact that bothauxin and Suc are required is particularly interestingfor two reasons. First, the auxin response in the SAMis dependent on a small GTPase Rho-like protein(ROP2). This protein was shown to be activated byboth the direct application of auxins and the light-induced auxins in shoot apices (Li et al., 2017). In ad-dition, the application of auxin effectively substitutedlight to activate the TOR-dependent formation of trueleaves, when Suc was present (Li et al., 2017). TheROP2 was shown to directly interact with TOR kinase,promoting its kinase activity (Cai et al., 2017). ROP2also functions in oxygen- and redox-dependent sur-vival (Baxter-Burrell et al., 2002). The expression ofROP2 is promoted by HYPOXIA RESPONSIVE UNI-VERSAL STRESS PROTEIN1 that transduces the hy-poxic cue via Group VII ETHYLENE RESPONSEFACTORs (ERF-VII), which are stabilized in hypoxicconditions (Gonzali et al., 2015). Hence, these datastrongly suggest auxin and Suc pathways convergewith oxygen signaling upstream of TOR kinase(Considine, 2017). We will return to oxygen signalingbelow. Second, the Suc effect on TOR and WUS isconsistent with a metabolic function because Glc, notpalatinose, is able to substitute for Suc (Pfeiffer et al.,2016), which conflicts with reports on axillary buds(Rabot et al., 2012; Barbier et al., 2015b).The above points demonstrate the incomplete nature

of current understanding of how auxin and Suc func-tion together in axillary bud outgrowth. Interestingly,the addition of Suc is sufficient to trigger the growth ofthe root apical meristem but not the SAM. This finding

may be explained by the relatively higher concentra-tions of auxin in the root apical meristem comparedwith the SAM, and also the light dependency of auxinsynthesis in the SAM (Li et al., 2017). Increased auxinsynthesis and transport from the axillary buds occurduring the transition to bud outgrowth, suggesting thatphotoreceptor-dependent auxin synthesis in the axil-lary bud meristems may be a primary trigger for budoutgrowth. However, strigolactone has also been sug-gested to be a signal output from photosynthesis. In-creased axillary branching is evident in an Arabidopsismutant lacking the PsbP Domain Protein5 (PPD5),which is a key component of photosystem II (Rooseet al., 2011). While PPD5 is essential for autotrophicmetabolism and optimal oxygen-evolving activity, theppd5mutants are able to sustain electron transport, andthe phenotype can be rescued by the application ofstrigolactone, indicating that the phenotype is morelikely to be due to hormone defects than energy deficits.Perhaps also relevant, axis initiation in tomato (Solanumlycopersicum) requires light signaling via phytochromesbut not photosynthesis (Yoshida et al., 2011). Meristemscultured with Suc in darkness, or in the presence of thecarotenoid inhibitor norflurazon in the light, fail toinitiate new leaf primordia. Nevertheless, axis initiationis a different process than organ development, i.e. theresumption of growth following quiescence.

Figure 1. Morphology, tissue oxygen status, and light-affected growth ofsingle-node cuttings of postdormant grapevine buds. Shown is a longi-tudinal section of a quiescent grapevine bud with three preformed shoots(1°, 2°, and 3°), enclosed by layers of bracts, hairs, and lignified scales. Astylized plot of the tissue oxygen concentration of a bud during quies-cence (dotted white line) and bud burst (dotted black line), as determinedby an oxygen microsensor, is overlaid. The path of the probe, from ex-ternal scales to the core of the primary meristem, is the x axis (blue line),and 260 mM [O2] approximates the air-saturated concentration in water atstandard temperature and pressure (refer to Meitha et al., 2015).

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LIGHT, OXYGEN, AND CHLOROPLAST FUNCTIONSIN PERENNIAL BUD BURST—AN ILLUSTRATIONWITH GRAPEVINE BUDS

In many perennial species, proleptic buds resumegrowth following a prolonged period of dormancy(Considine and Considine, 2016). The dormant budbecomes desiccated and metabolically isolated bycallose deposition in the plasmodesmata (Rinne et al.,2011). In this state, the meristem tissues are enclosed,typically by lignified bracts and scales (Fig. 1). Fol-lowing dormancy, the bud resumes a quiescent butreceptive state with a connected symplast. Studies ofseveral woody species have shown that the inter-nal tissues and leaf primordia of quiescent buds arelargely etiolated and lack chlorophyll (Solymosi et al.,2012). The plastids in such buds, however, exist indifferent developmental stages that are partly relatedto the nature of the tissues in which they reside(Solymosi et al., 2012). For example, proplastid-like andetio-chloroplasts, respectively, were identified in theinner and outer leaf primordia of compactly closedcommon ash (Fraxinus excelsior) buds (Solymosi et al.,2012). After bud burst, the emerging leaves containregular chloroplasts, although they are not fully de-veloped (Solymosi et al., 2012). However, in horsechestnut (Aesculus hippocastanum), closed buds containproplastids, and the leaf primordia of the opening budscontain etioplasts or etio-chloroplasts, but not chlo-roplasts (Solymosi et al., 2006). In tree-of-heaven(Ailanthus altissima) buds, both inner and outer leafprimordia contain chloroplasts and etio-chloroplasts(Solymosi et al., 2012). Hence, outer leaf primordia donot always contain more developed plastids than theinner leaf primordia.

There is also evidence of regulated oxygenationduring bud burst in grapevine. The postdormant bud ishypoxic (,10% saturation; Fig. 1), and oxygen con-centration gradually increases in a spatially regulatedmanner during the first week of bud burst, prior to leafemergence (Meitha et al., 2015, 2018). Independentstudies show the seeds and fruits of several speciesshow spatially and developmentally regulated tissueoxygen status (Verboven et al., 2008; Borisjuk andRolletschek, 2009; Cukrov et al., 2016). In grapevinebuds as in seeds, the outer scales were shown to be abarrier to oxygen diffusion; however, this did not ex-plain the elevated levels of oxygen in the primary budafter bud burst commenced, particularly where theoxygen minimumwas not at the core of the bud (Fig. 1;Meitha et al., 2015). Although not yet demonstrated inbuds, the low oxygen status (hypoxia) of seeds isreflected in the spatial patterns of metabolic control,particularly in relation to anaerobic glycolysis and en-ergy status (Borisjuk and Rolletschek, 2009). It has sinceemerged that oxygen status (and nitric oxide) has aregulatory role in seed dormancy and germination,where the oxygen-dependent degradation of ERF-VIIregulates the effective transition from anaerobic toaerobic metabolism and quiescence to growth (Holman

et al., 2009; Gibbs et al., 2014). No such research hasbeen applied directly to bud outgrowth; however, it isnotable that Arabidopsis mutants impaired in the reg-ulated degradation of the ERF-VII transcription factorsshow reduced apical dominance (Graciet et al., 2009).

Gene expression data of grapevine budsmay providesome insight into the roles of light and oxygen in reg-ulating bud burst. Postdormant grapevine buds do notrequire light to burst; however, dark-grown buds areimpaired in chlorophyll synthesis and develop an eti-olated phenotype (Meitha et al., 2018). We have con-trasted the gene expression of buds, grown in single-nodecuttings, during bud burst in the presence (DL) andabsence of light (D) at 72 and 144 h (SupplementalTable S1; fold change [FC] $ |2|, false discoveryrate [FDR] P # 0.05), which preceded leaf emergence(data available at NCBI BioProject PRJNA327467,http://www.ncbi.nlm.nih.gov/bioproject/327467). Acomplementary study investigated the developmentalcontrol of gene expression and primary metabolism(Meitha et al., 2018). Interestingly, there were fewchanges in physiological status or global transcriptprofiles of light- and dark-grown buds over the term; atotal of 436 geneswere differentially expressed at one orboth time points, 47 genes consistently regulated atboth (Supplemental Table S1). A small subset of genesshowed quite starkly differential expression in responseto light, and these will now be discussed in detail.

A key component of photomorphogenesis is HY5, abZIP transcription factor known to bind the promotersof light-inducible genes to activate their expression(Chattopadhyay et al., 1998). This transcription factor isactivated by different types of light, through the actionof the photoreceptors PHYA, PHYB, CRY1, and CRY2(Eberhard et al., 2008), at least in part due to theirnegative regulation of CONSTITUTIVE PHOTOMOR-PHOGENIC1 (COP1, also known as FUSCA1), whichtargets HY5 to the proteasome (Ang et al., 1998). Al-though the function of HY5 in seedling photomorpho-genesis in Arabidopsis has been reported, its expressionand response to light in perennial buds had not beendescribed. From the transcriptome analysis of thegrapevine buds (Supplemental Table S1), we observedthat the expression of genes coding for the HY5, or theupstream photoreceptors PHYA, PHYB, CRY1, andCRY2, was not differentially regulated by the presenceof light at 72 h of growth. However, the expression oftwo CRY genes and HY5 was increased at 144 h in thebuds exposed to light (Supplemental Table S1; Fig. 2). Inrose species and cultivars, blue light is sufficient topromote bud outgrowth until flowering (Girault et al.,2008; Abidi et al., 2013). Together, this evidence sug-gests that in perennials buds, CRY photoreceptors arecapable of stimulating bud burst by promoting HY5expression. The data also suggest that in grapevinebuds, light penetration and perception is not appre-ciable until after 72 h growth.

KnownHY5 target genes encode proteins involved inchlorophyll biosynthesis, light harvesting, and theCalvin cycle (Eberhard et al., 2008). The expression

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of many genes involved in these processes wasup-regulated at 144 h in illuminated buds comparedwith those kept in continuous darkness (Figs. 2 and 3).Homologs of many of the light-regulated genes ingrapevine buds are also induced during photomor-phogenesis in Arabidopsis (Ghassemian et al., 2006)and in rice (Oryza sativa; Kleffmann et al., 2007; Su et al.,2007). The subset of light-regulated genes in thesespecies includes those coding for photosystem compo-nents (PsaD, PsaG, PsaH, PsaK, PsaL, and PsaN; PsbS;LHCA1, LHCA2, LHCA4, and LHCA6; and LHCII B2and B3), as well as ATP synthase epsilon, Ferredoxin,Ferredoxin NADP-reductase, Rubisco subunits, andchlorophyll biosynthesis. Moreover, the expression ofgenes encoding two ankyrin domain-containing pro-teins, which are involved in successful insertion of lightharvesting complex (LHC) components in the thyla-koidmembrane, was up-regulated in grapevine buds at144 h under illumination (Supplemental Table S1).Furthermore, the levels of transcripts encoding several

enzymes of the Calvin cycle were also higher in illu-minated buds at 144 h, as described in further detailbelow.

From the up-regulated genes in DL condition at144 h, a total of 48 genes contained the target G-Boxsequence (CACGTG) of HY5 (Supplemental Table S2),including homologs of genes known to be regulatedby HY5 as well as likely candidates in light- andenergy-dependent functions. This includes genes cod-ing for two T6P phosphatases, the malic enzyme,the CK-responsive GATA factor 1, cryptochrome, andGUN4, among others (Fig. 2; Supplemental Table S2).Some evidence has been provided that links CK sig-naling pathwayswith HY5 (Vandenbussche et al., 2007;Das et al., 2012). It may be that the CK-responsiveGATA factor 1 is responsible for this cross talk. In fur-ther studies, it would be interesting to evaluate whetherHY5 can modulate the expression of these genes.

Early markers of light perception or prolongeddarkness were differentially expressed according to the

Figure 2. Scatterplot showing the differential expression and functional category of grapevine genes specifically discussed here.Full data presented in Supplemental Table S1. Differential expression analysis was carried out from grapevine buds grown at 22°Cin the presence (DL) or absence (D) of light at 72 and 144 h following removal from 4°C storage (FC$ |2|, FDR P# 0.05). Lettersfrom A to L summarize the functional categories. Size of dots represents the log10(adjusted P value). Color scale proportional toFC values: green (down-regulated genes), gray (not differentially expressed), and purple (up-regulated genes).

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presence of light. For example, the expression of a ho-molog of EARLY LIGHT-INDUCIBLE PROTEIN wasup-regulated in the light (Fig. 2; Supplemental TableS2). Conversely, the expression of a homolog of DARK-INDUCED6 (DIN6, also known as ASPARAGINE

SYNTHETASE1) was progressively down-regulated inthe presence of light, relative to continuous darkness.The up-regulation ofDIN6 is a hallmark of stresses suchas extended darkness and hypoxia, which limit photo-synthesis and/or respiration (Baena-González et al.,

Figure 3. Differential expression of genes during grapevine bud burst coding for photosynthetic and chlorophyll metabolicfunctions at 144 h in the presence (DL) or absence (D) of light. Purple color indicates up-regulation at 144 h of DL with respectto D. Abbreviations not defined in the text: ALA, aminolevulinic acid; CAO, CHLOROPHYLL A OXYGENASE; CHL,Mg-CHLOROPHYLLASE1; CHLH, Mg-CHELATASE subunit; CRD, Mg-PROTOPORPHYRIN IX MONOMETHYLESTER CYCLASE;CytB6/F, CYTOCHROME b6-F COMPLEX IRON-SULFUR subunit (PETC); Fd, FERREDOXIN; FLU, FLUORESCENT IN BLUELIGHT; FNR, Fd NADP+ OXIDOREDUCTASE; HCF136, PSII STABILITY/ASSEMBLY FACTOR; HEMA, GLUTAMYL-TRNA RE-DUCTASE; POR, NADPH-PROTOCHLOROPHYLLIDE OXIDOREDUCTASE; PSI, PHOTOSYSTEM I; PSII, PHOTOSYSTEM II;PsaD, PSI REACTION CENTRE (RC) subunit II, chloroplast precursor; PsaE B, PSI RC subunit IV B; PsaG, PSI RC subunit V; PsaH,PSI RC subunit VI; PsaK, PSI subunit X; PsaL, PSI subunit XI; PsaN, PSI RC subunit N; PsaO, PSI subunit O; PsbS, PSII 22-kDprotein; PsbW, PSII RC W; PsbX, PSII subunit X; PsbY, PSII CORE COMPLEX PROTEIN (chloroplast precursor); PsbZ, PSII corecomplex proteins; Rubisco, RIBULOSE BISPHOSPHATE CARBOXYLASE; RuBP, Ribulose 1,5-bisphosphate.

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2007). The expression of DIN6 is repressed by Suc andGlc, and is specifically induced by the Arabidopsishomologs of the catalytic subunits of SnRK1 (KIN10,KIN11), a conserved hub for starvation signaling(Baena-González et al., 2007).These facets of the transcript profiles of developing

grapevine buds further demonstrate that a light-dependent photomorphogenesis becomes apparent at144 h of exposure of the buds to environmental favor-able conditions, but not earlier (i.e. 72 h). This findingsuggests that at the beginning of bud burst other envi-ronmental cues, such as temperature, are required topromote skotomorphogenic development. Thereafter,growth in the light provides signals that induce pho-tomorphogenic development.Chloroplast-to-nucleus and mitochondria-to-nucleus

retrograde signals are very important for organelledevelopment (Chan et al., 2016). Components that actas retrograde signals participate in biogenic and op-erational processes. Some genes that are involved inretrograde signaling, such as GUN4 and HY5, are dif-ferentially expressed in grapevine buds in response tolight. The gun mutants of Arabidopsis are defective intetrapyrrole metabolism, suggesting that this pathwayis important in biogenic signaling. The expression ofsix genes involved in tetrapyrrole metabolism waschanged in grapevine buds in response to light at144 h. In particular, GUN4 participates in the bio-synthesis of Mg-Protoporphyrin-IX, which in turnbinds to a Heat Shock 90-type protein and interactswith HY5 to regulate the expression of photosynthesis-associated nuclear genes (Chan et al., 2016). The ex-pression of Protoporphyrin-IX biosynthetic genesand HY5 was up-regulated by light in grapevine budsat 144 h, suggesting that the retrograde activation ofphotosynthesis-associated nuclear genes occurs in illu-minated buds. Hence, the plastids in the buds of pe-rennials species may be undergoing a biogenic processrather than an operational adaptation to the environ-mental conditions at the early stages of bud burst.Light adaptation also occurs through the induction of

CK signaling pathways in plants. The expression of a genecoding for a His-containing phosphotransfer protein wasup-regulated by light at 72 h in grapevine buds (Fig. 2;Supplemental Table S1). This protein plays a key role inpropagating CK signal transduction (Hwang et al., 2002).The expression of the CK-responsive GATA factor 1 isknown to respond to light and CKs (Naito et al., 2007). Italsoplays a role in chloroplast development (Hudson et al.,2013). The expression of the CK-responsive GATA factor1was increased at 144 hDL in grapevine buds (Fig. 2). Thistranscription factor represses gibberellic acid signalingdownstream of PIF and DELLA regulators (Richter et al.,2010). The expression of genes coding for repressors of CKsignaling, such as ARR1 type B and APRR7, was down-regulated by light in grapevine buds. These findings sug-gest that the influence of light on grapevine buds involvesCK signaling pathways. The expression of two othercomponents (ARABIDOPSIS HISTIDINE PHOSPHO-TRANSFER1 [AHP1] and HISTIDINE KINASE3 [AHK3])

involved in CK signaling was down-regulated by light.Since there is considerable redundancy in the functionsof the different AHP proteins (AHP1, AHP2, AHP3, andAHP5), which act as positive regulators of CK signaling topromote development, the significance of this observationis uncertain (Hutchison et al., 2006).

As described above, evidence now suggests thatSuc and light-dependent auxin signaling convergeupon meristem activators in Arabidopsis, promotingmeristem growth. We found few primarily auxin-related functions in the grapevine data shown here(Fig. 2; Supplemental Table S1). Auxin has previouslybeen shown to function in the removal of dormancycallose in grapevine buds and to accumulate duringbud swell; however, direct application has apparentlylittle effect (Aloni et al., 1991; Lavee and May 1997, andreferences therein). A more recent, limited transcriptanalysis in developing grapevine buds (predormant,paradormant) showed no relationship between genesselected as auxin and Suc function markers, or withauxin-function markers and the outgrowth potential(He et al., 2012). Nevertheless, none of these studieswere designed to elaborate auxin or Suc functions, andhence any relationships may be obscured.

SUGAR METABOLISM IS REGULATED BY LIGHT ATEARLY STAGES OF GRAPEVINE BUD BURST

Several transcripts encoding enzymes involved instarch, Suc, and hexose metabolism were strongly reg-ulated by light in grapevine buds at 72 h in the light.These include homologs of STARCH PHOSPHORYL-ASE, BETA-1,3-GLUCANASE, and two SUCROSESYNTHASE (Fig. 2; Supplemental Table S1). The light-induced activation of expression of starch and Suc hy-drolytic genes was largely attenuated at 144 h, althoughSTARCH PHOSPHORYLASE transcripts remained athigher levels at 144 h. Transcripts encoding a homologof CALLOSE SYNTHASEwere decreased in the buds inthe light at 144 h. In Rosa sp., the light-dependentup-regulation of VACUOLAR INVERTASE is consid-ered to be important in promoting sugar degradationand bud burst (Girault et al., 2008; Henry et al., 2011).The finding that the expression of a VACUOLAR IN-VERTASE, GIN2, was not differentially regulated bylight in grapevine may partially explain the differencesin the light requirements of bud burst in Rosa sp. andgrapevine.

As illustrated in Figure 4, the expression of genesencoding plastid carbon metabolism enzymes ingrapevine buds was clearly up-regulated by light at144 h. Moreover, transcripts encoding a homolog of theplastid-localized NADP+-dependent MALIC ENZYMEwere increased in the light, suggesting a need for reg-ulation of NADP+/NADPH homeostasis and provisionof reducing power for Calvin cycle activity (Wheeleret al., 2005). In contrast, the up-regulated expressionof genes encoding proteins involved in the catabolismof branched-chain amino acids in the plastid was

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increased in the dark, as were the levels of transcriptsencoding a cytosolic PHOSPHOENOLPYRUVATECARBOXYKINASE (Fig. 4). These findings suggest arequirement for alternative substrates to fuel the mito-chondrial tricarboxylic acid pathway in the dark-treatedcondition (Araújo et al., 2012;Avin-Wittenberg et al., 2015).

T6P is a primary sensor of cellular energy status.Transcripts encoding two T6P PHOSPHATASE (TPP)homologswere increased by light at 144 h, while TPP andT6P SYNTHASE (TPS) mRNAs were decreased in a-bundance (and increased in the dark; Figs. 2 and 4). Thesetranscriptional differences suggest that reduced T6Plevels or alternatively, increased T6P turnover, occurs inthe buds in the light compared with the dark condition.

We then compared the grapevine bud differentialgene expression at 144 h (Supplemental Table S1)against the public data of the Arabidopsis transcrip-tional perturbation database in Genevestigator (Hruzet al., 2008). We used the accession identifiers of theArabidopsis homologs of the grapevine differentially

expressed genes and selected unique genes, leaving317 differentially expressed genes (Supplemental TableS3A). The corresponding Arabidopsis accessions wereentered using the Signature tool and compared with allavailable Arabidopsis data using the Perturbationsprofile, with the Manhattan Distance algorithm (Affy-metrix Arabidopsis ATH1 Genome Array, all geneticbackgrounds, 9,552 samples). Some of the Arabidopsisaccessions submitted did not match a probe from theATH1 microarray, leaving 306 probes (SupplementalTable S3B). Nearly all of the top 50 most similar of 3,020Perturbation studies attended to postgerminationphotomorphogenesis. Each of the top five most similarwere wild-type studies that investigated light signalingand contrasted light conditions against continuousdarkness (Supplemental Table S3B), for example, therole of plastid biogenesis in mediating light-dependentsignaling (GEO accession GSE24517; Ruckle et al., 2012)and the role of light-dependent translational regulationin photomorphogenesis (GEO accession GSE29657; Liu

Figure 4. Differential expression of genes during grapevine bud burst coding for carbon- and energy-related functions at144 h in the presence (DL) or absence (D) of light. Processes and reactions in purple and green reflect up- and down-regulation, respectively, at 144 h in the DL/D comparison. Abbreviations not defined in the text: a1,4G, a-1,4-GLUCO-SIDASE; BCAAs, branched-chain amino acids; BCAT, BRANCHED-CHAIN AMINO ACID AMINOTRANSFERASE; Epi,ALDOSE 1-EPIMERASE; FBP, FRUCTOSE 1,6-BISPHOSPHATASE; FBPA, FRUCTOSE-BISPHOSPHATE ALDOLASE; G3PDH,GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE B; ME, NADP-DEPENDENT MALIC ENZYME; PEPC, PHOS-PHOENOLPYRUVATE CARBOXYKINASE; Rubisco, RIBULOSE BISPHOSPHATE CARBOXYLASE; SUS, SUCROSE SYN-THASE; TP, TREHALOSE-PHOSPHATASE.

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et al., 2012). Several of the studies involving mutant linesthat had similar profiles to grapevine buds (BioProjectPRJNA327467) also related to light and carbon signaling,for example, a studyof the role of theCOP1 in coordinatinglight-dependent signaling (GEO accession GSE22983;Chang et al., 2011) and a study identifyingCARBONANDLIGHT INSENSITIVE (CLI186) mutants (ArrayExpressaccession E-MEXP-1112; Thum et al., 2008).We then constrained our query of the Genevestigator

data to developmental studies of germination or post-germination seedlings, which retrieved 136 perturba-tions (Supplemental Table S3C). The similarity of ourdata with comparisons from Narsai et al. (2011; GEOaccession GSE30223) of germinating seed against dark-stratified seed suggested the DL condition in our studywas more developmentally advanced than the D con-dition. Also of interest were comparisons of Glc-treatedagainst control seedlings of wild-type or conditionalmutants of the TOR protein kinase, indicating the DLcondition was consistent with active metabolism ofsugars (GEO accession GSE40245; Xiong et al., 2013).In addition, the comparison to the core 600 putative

targets of the Arabidopsis KIN10 (Baena-Gonzálezet al., 2007) corroborated the identification of compo-nents involved in the catabolism of branched-chainamino acids and the regulation of TPS expression un-der continuous darkness (repressed in DL/D). Further-more, this analysis supported conclusions regardinglight-mediated regulation of DORMANCY/AUXINASSOCIATED1, two genes coding for thioredoxins,and two members of the NBS-LRR Leu-rich repeatsuperfamily, each implicated in sugar starvation re-sponses (Baena-González et al., 2007).Together, these data suggest that transcriptional

changes induced by light in grapevine buds are similarto those observed in Arabidopsis, providing evidence ofa prominent role for chloroplast processes in carbon andoxygen (energy) metabolism during bud burst and therequirement for light to orchestrate chloroplast biogen-esis. It also provides considerable evidence of the effectof light on sugar signaling. Alternative pathways forcatabolism became evident under continuous darkness,suggesting catabolism of branched-chain amino acids tofuel the mitochondrial tricarboxylic acid cycle.

CONCLUDING REMARKS

The commitment to resume growth of postdormantperennial buds is driven by developmental activatorssuch as CKs and auxins. While light can function as anupstream regulator of these phytohormones, light isonly a facultative requirement for the decision in manyspecies. The body of evidence discussed here demon-strates that light promotes/enhances rather than drivesphotomorphogenic development, while other cuessuch as temperature promote the initial skotomorpho-genic outgrowth. Suc, resulting from emerging photo-synthesis, may also participate in the light-independentactivation process, acting as both a metabolite andsignaling molecule. While the present discussion has

focused on the importance of white light, blue lightmayalso play a key role in bud burst. Accumulating evi-dence supports the function of CRY photoreceptors inblue light perception resulting in HY5 expression,which in turn activates photomorphogenic gene ex-pression, stimulating bud outgrowth. PHYA and PHYBmay also fulfill roles in light perception as they do inArabidopsis seeds. The developmental stages of plas-tids of buds can vary between different perennial plantsbut also within different tissues of the same bud. Thedevelopmental regulation of the hypoxic state alsoplays important but largely undefined roles in budburst. The role of hypoxia in regulating mitochondrialand plastid numbers and composition at the earlystages of bud burst is largely unexplored. Finally, ouranalysis of the literature evidence highlights the con-servation of light-induced signaling cascades and asso-ciated transcriptional changes that drive the resumptionof growth after a period of quiescence in perennial budsand Arabidopsis seeds. Several exciting questions re-main, particularly in regard to the role of light andoxygen in bud burst (see Outstanding Questions). In-creasingly, the tools required to investigate them, evenin perennials, are becoming available.

Supplemental Data

The following supplemental materials are available.

Supplemental Table S1. Differentially expressed genes (DEG) which metfold change and false discovery rate criteria (FC$j2j, FDR P#0.05) in the

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presence (DL) or absence (D) of light at 72 and 144 h and after functionalenrichment.

Supplemental Table S2. List of genes containing the G-box sequence inupregulated genes at DL 144h from Supplemental Table S1.

Supplemental Table S3. Comparison of differentially expressed gene ex-pression, after functional enrichment with public arabidopsis microarraydata available at Genevestigator.

Received October 10, 2017; accepted November 30, 2017; published December4, 2017.

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