To grow or not to grow, a power-saving program induced in dormant buds

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ScienceDirect To grow or not to grow, a power-saving program induced in dormant buds Elena Sa´nchez Martı´n-Fontecha1, Carlos Taranco´n1 and Pilar Cubas Plant shoot branching patterns determine leaf, flower and fruit production, and thus reproductive success and yield. Branch primordia, or axillary buds, arise in the axils of leaves and their decision to either grow or enter dormancy is coordinated at the whole plant level. Comparisons of transcriptional profiles of axillary buds entering dormancy have identified a shared set of responses that closely resemble a Low Energy Syndrome. This syndrome is aimed at saving carbon use to support essential maintenance functions, rather than additional growth, and involves growth arrest (thus dormancy), metabolic reprogramming and hormone signalling. This response is widely conserved in distantly related woody and herbaceous species, and not only underlies but also precedes the growth-to-dormancy transition induced in buds by different stimuli. Address Plant Molecular Genetics Department, Centro Nacional de Biotecnologı´a/CSIC, Campus Universidad Auto´noma de Madrid, 28049 Madrid, Spain Corresponding author: Cubas, Pilar ([email protected]) These authors have contributed equally.

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Current Opinion in Plant Biology 2017, 41:102–109 This review comes from a themed issue on Growth and development Edited by Gwyneth Ingram and Ari Pekka Ma¨ho¨nen

http://dx.doi.org/10.1016/j.pbi.2017.10.001 1369-5266/ã 2017 Elsevier Ltd. All rights reserved.

Plant shoot architecture largely determines leaf, flower and fruit production, light capture efficiency, reproductive success and yield. Branching patterns are in part determined by the arrangement of leaves in the shoot ( phyllotaxis), as branches initiate from meristems located in the leaf axils. These meristems develop rudimentary, compressed branches, the axillary buds, which may grow out without delay, or enter a dormant state. Dormant buds can, at later times, elongate into branches. Bud growth displays a plasticity that helps the plant match the degree of shoot development to resource availability, thus maximizing its adaptation to changing Current Opinion in Plant Biology 2018, 41:102–109

environmental and endogenous conditions. Almost universally, plants respond to removal of the shoot apex (decapitation) by activating axillary bud growth to form new shoots. By contrast, several environmental and endogenous conditions (e.g. high-planting density, low nutrient soil status, a strong sink organ competing for photoassimilates) promote bud growth arrest. When branch-suppressing stimuli are no longer present, buds can usually resume growth, but a more lasting dormancy occurs in perennial plants during the summer, where dormant buds can only reactivate after a chilling period. Lang et al. [1] distinguished three types of bud dormancy: ecodormancy, induced by environmental factors; paradormancy, promoted by other plant organs; and endodormancy maintained by signals internal to the bud. It is yet unclear whether these different types of dormancy are controlled by unrelated genetic mechanisms or whether diverse endogenous and environmental stimuli trigger signaling pathways that converge into the activation of a common genetic programme. Here we will use the term dormancy to refer to any temporary growth arrest of axillary meristems and buds. Bud activity is coordinated at the plant level but has different outcomes for each individual bud. Accordingly, axillary bud status is determined both by long-range signals and local gene activity. Excellent reviews have summarized the current knowledge on the systemic determinants controlling shoot branching at the plant level. One such determinant is the dynamic competition between buds to export auxin into the polar auxin transport stream (PATS) of the stem, whose strength is modulated by strigolactone (SL) signalling [2]. Another is the competition for sugar between the shoot apex and the buds acting as sinks [3]. Here we will review recent discoveries of the transcriptional responses induced locally, inside the buds, during the growth-to-dormancy transition in response to various stimuli and widely conserved in distantly related species.

Different signals induce a power-saving genetic program in Arabidopsis buds A number of transcriptomic studies have analysed the differential gene expression of buds before and after entering dormancy in a variety of woody and herbaceous species (e.g. [4,5,6,7,8,9,10,11,12,13,14,15,16,17]). Three ‘active versus (vs) dormant’ bud experiments have been reported in Arabidopsis (Arabidopsis thaliana) [4,8,10]. Meta-analyses of these experiments have www.sciencedirect.com

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revealed that, although they are diverse in treatment (decapitation, changes in the red-to-far-red light ratio (R:FR)) and duration (24, 8 and 3 h), they share key features [18]. All three ‘dormant-bud’ samples show a transcriptional response that resembles a carbon (C) -starvation syndrome described in other Arabidopsis tissues exposed to energy-limiting conditions (e.g. sucrose depletion, night extensions, short-day photoperiods) [19,20]. This syndrome, also termed Low Energy Syndrome (LES [21]), is a ‘power-saving’ genetic program aimed at retaining C to support essential maintenance functions by reducing new growth (i.e. inhibiting protein and DNA synthesis, cell division and anabolism), and obtaining C skeletons and energy from sources other than sucrose (such as amino acids, lipids and proteins) via catabolism, senescence and autophagy. Tissues undergoing this syndrome—including Arabidopsis dormant buds—present a down-regulation of sucrose-induced and ribosome-encoding genes, in addition to genes related to cell division and anabolism. In contrast, genes related to catabolism, protein ubiquitination and degradation, autophagy and senescence are up-regulated. Hormone signalling pathways that promote senescence (i.e. abscisic acid (ABA) and ethylene) are induced, whereas cytokinin signalling, which antagonizes senescence, is repressed [18,19,21]. Remarkably, this syndrome induced in Arabidopsis paraand ecodormant buds is also detected in grapevine axillary buds collected in July, months before they enter endodormancy, at a time when day-length is shortening. This response is maintained through endo-, eco- and paradormancy [7,18]. Apical buds of poplar exposed to 1 week of short days also display this response, weeks before they enter endodormancy [5,18]. This indicates that a conserved LES response precedes and underlies the transition of buds into para-, eco- and endodormancy in distantly related herbaceous and woody species and supports the view that the three types of dormancy share at least some core genetic mechanisms.

Dormant buds express dark-induced, sugar-repressed genes Promoters of genes upregulated in Arabidopsis para- and ecodormant buds have a significant overrepresentation of the sucrose-repressible element (SRE) TATCCA [4,18]. Furthermore, analyses of Arabidopsis, grapevine and poplar dormant-bud transcriptomes revealed a significant upregulation of dark-induced, sugar-repressed genes [22], upstream regulators of the transcriptional response to sucrose [23], and members of a robust core of a C-signalling response [24,18]. These results are in agreement with recent evidence that sugar availability to buds controls bud outgrowth [25,26,27,28,29]. In pea plants for instance, sucrose is rapidly translocated into buds from leaves after www.sciencedirect.com

decapitation, and this movement precedes the earliest signs of bud growth. Furthermore, exogenous sugar application to axillary buds of intact plants mimics decapitation, and leads to bud outgrowth [28]. In this process sugar probably not only acts as a nutrient, essential for growth and development, but also as a signal that informs of C availability, and triggers sugar-related genetic responses. A mediator of this sugar signal is probably trehalose 6-phosphate (Tre6P), a signalling molecule that acts as a sensitive proxy for C status in plants. Indeed Tre6P levels in buds directly correlate with the initiation of bud outgrowth following decapitation [30]. Furthermore, cues other than a sugar shortfall (i.e. brief treatments of plants to low R:FR, exposure to short days and mutations in phytochrome genes) also promote induction of sugar-repressed genes in buds [18,14,31]. This indicates that such responses are also promoted by stimuli that signal situations which compromise C assimilation or respiration, and by environmental changes that help anticipate future suboptimal energy conditions [32]. All these signals may feed—through different pathways—into the power-saving program that results in a moderation of axillary bud growth (Figure 1). Indeed, in rose, sugar treatments are not sufficient to overcome the bud growth inhibition induced by darkness or low light intensity [33,34]; in Sorghum, defoliation (and consequent reduction in leaf-derived sucrose) and low R:FR induce dormancy through partially independent pathways [26]. A well-known integrator of the LES in other tissues is the SUCROSE-NON-FERMENTING-1-RELATED PROTEIN KINASE (SnRK1), a sensor of stress and energy that coordinates energy balance, metabolism and growth [32]. SnRK1 is inactivated by sugars and Tre6P, and activated by energy deprivation and ABA signalling. Gene Set Enrichment Analyses (GSEA) in Arabidopsis, poplar and grapevine dormant buds revealed a very significant enrichment of genes responsive to AKIN10, one of the catalytic subunits of SnRK1, among them, robust bud dormancy markers such as histone HIS13 and DORMANCY1 [18]. Also, the SnRK1 regulatory subunit AKINBETA1, whose mRNA levels correlate directly with night duration [35] is induced in dormant buds [18]. SnRK1 activates autophagy [32], controls senescence [36], and causes downregulation of anabolism, cell division and protein synthesis [32], all responses detected in buds entering dormancy [18] (Figure 1). These observations point to a potentially important role of SnRK1 in the promotion of bud growth arrest. However, the contribution of this kinase remains to be established, as multiple mutants of the SnRK1 catalytic subunits have low viability in Arabidopsis. As mentioned above, buds entering dormancy show a down-regulation of ribosomal-, cell cycle-, cell divisionand DNA synthesis-related genes [4,10,18], whose Current Opinion in Plant Biology 2018, 41:102–109

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Figure 1

Active bud Low R:FR Low light

Short days

(Phytochromes)

(Phytochromes, circadian rythmn genes, Flowering time genes)

Low C availability (Tre6P, G6P, G1P)

ABA

SnRK1?

1 BRC1

SL

CK

REPRESSED

INDUCED

(energy consuming procceses)

Autophagy

Catabolism

Senescence

Anabolism

C recycling

Cell division

Protein synthesis

Growth arrest

Dormant bud Current Opinion in Plant Biology

Model of some of the events that take place during the growth-to-dormancy transition in buds. Different stimuli (low sugar levels, low R:FR, short photoperiods) trigger a low energy syndrome or power-saving mode in buds [21]. Note that this status is reversible; buds may reactivate in response to changes in these stimuli. This syndrome may be coordinated, at least in part by BRC1, ABA and probably SnRK1 signaling. For the latter no genetic evidence, only correlations based on transcriptomic data, are available. This syndrome is aimed at reducing energy use and recycling C from molecules other than sugars. The molecular pathways linking stimuli and responses remain to be established and may be partially independent. Some of the known relationships between BRC1, ABA and SnRK1 signaling and different aspects of the LES are indicated. SnRK1 activates autophagy via inhibition of the TOR signalling pathway and causes downregulation of anabolism, cell division and protein synthesis. BRC1 promotes ABA signalling and downregulation of cell cycle and ribosomal genes. In other tissues ABA antagonizes PP2CAs phosphatases, which are negative regulators of SnRK1, induces senescence, causes arrest of cell cycle in G1/S phase, and down-regulates CK signalling. SLs promote senescence and induce BRC1 expression. In some species, CK downregulates MAX2 and BRC1. Ethylene signalling is also induced (not indicated). In blue boxes, genes and processes induced during the growth-to-dormancy transition; in grey boxes, genes and processes repressed. G1P, glucose 1-phosphate; G6P, glucose 6-phosphate.

promoters are significantly enriched in TCP (TEOSINTE BRANCHED1, CYCLOIDEA, PCFs) transcription factor binding sites (UP1 motif, GGCCCAWW; [4]; AGGCCCAT; [10]). Indeed, some TCP factors bind and Current Opinion in Plant Biology 2018, 41:102–109

directly control the expression of genes of these functional categories [37]. The finding that some of these factors (TCP3, TCP13) interact with SnRK1 in yeast twohybrid assays [38] and that SnRK1 affects the expression www.sciencedirect.com

A low energy syndrome induced in dormant buds Martı´n-Fontecha, Taranco´n and Cubas 105

of some TCPs [39] raises the possibility of a regulation of these TCP by SnRK1, and a possible link with the LES.

Abscisic acid signalling in dormant buds: a link between dormancy and senescence? Another response detected both in dormant buds and Cstarved tissues is ABA accumulation and signalling [5,6,7,8,10,18,19,40,41,42]. ABA is a stress-induced hormone with growth-inhibiting functions, whose crosstalk with sugar signalling is well-known. Indeed several glucose insensitive (gin) mutants are affected in genes related to ABA biosynthesis and response (e.g. [43]). ABA signalling is required to promote bud dormancy in Arabidopsis: ABA biosynthesis (nced3, aba2/gin1) and ABA insensitive (abi1) mutants display increased branching [8,40], most markedly under light-limiting conditions, such as a low R:FR light ratio or short-day photoperiods [8,41]. Also, ABA treatments in buds reduce the shoot branching of bushy mutants and wild-type plants exposed to standard light or low R:FR conditions [8,40,41]. In the context of a LES in buds, several roles can be proposed for ABA signalling. First, ABA causes downregulation of cell cycle genes and induces expression of the INHIBITOR OF CDK, which arrests cell cycle in G1/S, phase in which cells of dormant buds are typically found [44] (Figure 1). Second, ABA antagonizes PP2CAs phosphatases, which are negative regulators of SnRK1 [45]. This raises the possibility that ABA boosts SnRK1 activity and helps promote responses mediated by this kinase (Figure 1). Third, ABA activates the SnRK2s, which indirectly induce senescence. SnRK2s cause activation of upstream regulators of senescence-associated genes (SAGs), involved in protein modification, macromolecule degradation, autophagy, transport and antioxidation [46], activities induced in dormant buds [21] (Figure 1). Three of these SAG upstream factors, NAC genes ORESARA1, NAP and ATAF1, are potential master regulators of bud dormancy gene regulatory networks (GRNs) [18,41]. It is worth pointing out that senescence, a response associated with the LES, is not just a irreversible degenerative process linked to aging, but one of nutrient relocation, in which C and N are recycled for growth at a later stage. A limited senescence response at the cellular level can thus be reversed when C is available [47]. Interestingly, other hormone signalling pathways acting in buds are also connected to senescence responses. Ethylene signaling, induced in dormant buds (e.g. [5,10,18]) is well-known for its relationship with low sugar and senescence [48]. Strigolactones (SL), key hormones that suppress shoot branching through multiple pathways (see below), promote senescence via ethylene-dependent and independent pathways in leaves [49,50]. In contrast cytokinins (CK) whose levels are reduced in dormant buds [18,33,51] are negative regulators of senescence: a www.sciencedirect.com

reduction in CK levels is a key signal for senescence initiation in Arabidopsis [52] (Figure 1). Therefore one function (among others) of ABA, SL and ethylene in buds could be to prepare cells for a status in which energy saving and C recycling via catabolism are predominant.

Strigolactones act locally in axillary buds

SLs are hormones that prevent shoot branching [53]. They not only play a systemic role in the control of bud activity but they also act locally, inside axillary buds. Indeed, some genes encoding SL-synthesis enzymes, and key components of the SL perception machinery -the receptor D14 and the F-box protein MAX2- are expressed inside the buds [54,55,56,57]. Moreover, transgenic lines expressing D14 only in the vascular tissue, still have detectable levels of D14 protein in buds, which indicates that D14 can either passively move or be transported into these structures [58]. Also, clonal analysis showed that a wild-type MAX2 function is required in the bud or its proximity to repress bud growth, regardless of whether the bud is surrounded by wild-type tissue [54]. Finally, when SLs are directly applied to buds, they cause bud growth arrest in wild-type plants and in SL synthesis mutants [51,59,60,61,62]. SL signalling is mediated by proteasomal degradation of the transcriptional repressor D53-like proteins [63,64,66]. In addition to its systemic effect in auxin transport dampening [67,68,69], SL signalling promotes mRNA accumulation of the growth repressor BRANCHED1 (BRC1) in the axillary buds [70] (Figure 1): mutants deficient in SL biosynthesis or signalling have lower BRC1 mRNA levels [51,56,61,70,71], whereas those deficient in D53-like genes display constitutive BRC1 upregulation [72,65,66]. It has been proposed that this regulation could be partly mediated (at least in monocots) by SQUAMOSA PROMOTER BINDING PROTEINLIKE (SPL) factors that bind the promoter of TEOSINTE BRANCHED1 (TB1, the BRC1 ortholog in monocots [73]) and control its expression [74,75,76]. Although the relation of these factors with SL signalling is still unclear [77,78], D53-like factors can bind some SPLs [76,79]. In particular, rice D53 binds SPL14/IPA1 and suppresses its transcriptional activity [79]. This raises the possibility that SPLs are inactive or act as TB1 transcriptional repressors except when D53-like proteins are destabilized and degraded by SL signalling, when the SPLs would be released for transcriptional activation of TB1 [76]. In addition, IPA1/SPL14 binds to and controls the expression of D53 thus playing a critical role in the feedback regulation of SL-induced D53 expression [79].

BRANCHED1/TEOSINTE BRANCHED1 mediate local transcriptional responses that promote bud dormancy The TCP transcriptional regulators BRC1 and TB1 promote bud growth arrest locally, as they are expressed Current Opinion in Plant Biology 2018, 41:102–109

106 Growth and development

inside the buds. However this growth-inhibiting activity is context-independent, at least in dicots: when BRC1like genes are ectopically expressed in seedlings, they cause severe growth cessation in root and shoot meristems and leaf primordia [10,80]. BRC1 expression responds rapidly to conditions that affect C availability and energy levels: it is significantly induced shortly after exposure to low R:FR and repressed within 1–2 h post-decapitation [70,72], or after sucrose application to axillary buds [25,28,41]. In phyb mutants, BRC1/TB1 mRNA levels are increased in Arabidopsis and Sorghum [10,26]. Several components of the SL synthesis and signalling pathways are also modulated by these factors (and by darkness) in different species [25,26,33,56,71,81]. Therefore it is possible that some of the changes observed in BRC1 expression reflect in part the modulation of SL signalling by these cues. The genetic pathways controlled by BRC1 have begun to be identified in Arabidopsis. A GRN down-regulated in response to BRC1 is enriched in cell-cycle, cell-division and DNA-replication genes; another in chloroplast ribosomal genes [10] (Figure 1). These GRNs largely overlap with those described above, down-regulated in dormant buds, whose promoters are significantly enriched in TCP binding sites. Therefore BRC1 may repress these GRNs directly or indirectly via competition with other TCPs. A third, induced, GRN controlled by BRC1, largely overlaps with the ABA responses identified in dormant buds (Figure 1, see above) [10,41]. BRC1 directly controls the transcription of three closely related HD-zip genes critical for ABA-related responses in buds: HB21, HB40 and HB53. These factors, required for wild-type expression of NCED3 (a rate-limiting ABA biosynthesis enzyme) in buds, are also sufficient to induce ectopic NCED3 expression and ABA accumulation and response in seedlings. Furthermore, each of these factors (as well as BRC1), can bind the NCED3 promoter and may control NCED3 transcription directly [41].

but also by stimuli that signal impending limitations of C and energy. These cues may converge into a power saving mode, which results in a local moderation of growth rate, and eventually in quiescence and dormancy of buds. The pathways connecting these stimuli and the LES are still unclear, but BRC1, SL, ABA and probably SnRK1 signaling could participate in the coordination of some of these responses (Figure 1). This early-induced, widely conserved syndrome may reflect an ancient response, evolved as a universal adaptation for cell and tissue survival under energy and nutrient limitations. Previously described in yeast and animal cells and other plant tissues, it has now been identified in axillary buds of herbaceous and woody plants. This response may have played a critical evolutionary role during plant colonization of habitats with seasonal climate fluctuations.

Acknowledgements We thank Desmond Bradley for constructive criticisms of the manuscript. This work was supported by the Spanish Ministry of Economy (MINECO) [grant BIO2014- 57011-R]. E.S. is a MINECO FPI predoctoral fellow, C.T. is a La Caixa predoctoral fellow. We apologize to colleagues whose work was not cited because of space limitations.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of outstanding interest 1.

Lang GA, Early JD, Martin GC, Darnell RL: Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. HortScience 1987, 22:371-377.

2.

Domagalska MA, Leyser O: Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 2011, 12:211-221.

3.

Barbier FF, Lunn JE, Beveridge CA: Ready, steady, go! A sugar hit starts the race to shoot branching. Curr Opin Plant Biol 2015, 25:39-45.

4.

Tatematsu K, Ward S, Leyser O, Kamiya Y, Nambara E: Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis. Plant Physiol 2005, 138:757-766.

5.

Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, Bhalerao RP, Boerjan W, Rohde A: A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 2007, 19:2370-2390.

6.

Horvath DP, Chao WS, Suttle JC, Thimmapuram J, Anderson JV: Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics 2008, 9:536.

HB21/40/53 are essential only in low R:FR and short-day photoperiods: the excess of branching phenotype of the hb21 hb40 hb53 triple mutants is only detectable under these conditions [29]. Remarkably, their maize ortholog GRASSY TILLERS1, is involved in branch suppression also in low R:FR, and it has been shown to be downstream of TB1 [14,82]. This indicates that this TCP/HD-zip pathway, induced in light-limiting conditions, is conserved across angiosperms.

7. 

Concluding remarks

8. 

Accumulating evidence indicates that the decision of axillary buds to grow out into branches is negatively controlled not only by a shortfall of sugar at the nodes, Current Opinion in Plant Biology 2018, 41:102–109

Dı´az-Riquelme J, Grimplet J, Martı´nez-Zapater JM, Carmona MJ: Transcriptome variation along bud development in grapevine (Vitis vinifera L.). BMC Plant Biol 2012, 12:181. This paper reports a detailed transcriptional profiling of Vitis vinifera axillary buds during the year, under natural conditions. It provides invaluable transcriptomic information of the gene expression changes occurring at the different bud dormancy stages in this basal woody dicotyledonoeus species. Reddy SK, Holalu SV, Casal JJ, Finlayson SA: Abscisic acid regulates axillary bud outgrowth responses to the ratio of red to far-red light. Plant Physiol 2013, 163:1047-1058. This paper shows that ABA plays a role in the regulation of Arabidopsis axillary bud activity: ABA biosynthesis mutants display increased branching in low R:FR, and hormone quantifications demonstrate that ABA levels www.sciencedirect.com

A low energy syndrome induced in dormant buds Martı´n-Fontecha, Taranco´n and Cubas 107

in buds inversely correlate with bud activity in wild-type and in excess of branching mutants. 9.

Ueno S, Klopp C, Leple´ JC, Derory J, Noirot C, Le´ger V, Prince E, Kremer A, Plomion C, Le Provost G: Transcriptional profiling of bud dormancy induction and release in oak by nextgeneration sequencing. BMC Genomics 2013, 14:236.

10. Gonza´lez-Grandı´o E, Poza-Carrio´n C, Sorzano COS, Cubas P:  BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis. Plant Cell 2013, 25:834-850. This paper reports for the first time in Arabidopsis the induction of ABA (and ethylene) response in buds under low R:FR, and the requirement of BRC1 for this induction. In addition, these global transcriptomic studies demonstrate that BRC1 is necessary for downregulation of two corregulated clusters of genes related with cell division and plastid ribosomal proteins. 11. Howe GT, Horvath DP, Dharmawardhana P, Priest HD, Mockler TC, Strauss SH: Extensive transcriptome changes during natural onset and release of vegetative bud dormancy in populus. Front Plant Sci 2015, 6:1-28. 12. Fennell AY, Schlauch KA, Gouthu S, Deluc LG, Khadka V, Sreekantan L, Grimplet J, Cramer GR, Mathiason KL: Short day transcriptomic programming during induction of dormancy in grapevine. Front Plant Sci 2015, 6:834. 13. Zhang H, Li H, Lai B, Xia H, Wang H, Huang X: Morphological characterization and gene expression profiling during bud development in a tropical perennial, Litchi chinensis Sonn. Front Plant Sci 2016, 7:1-20. 14. Kebrom TH, Mullet JE: Transcriptome profiling of tiller buds  provides new insights into phyb regulation of tillering and indeterminate growth in sorghum. Plant Physiol 2016, 170:2232-2250. Transcriptome analyses of wild-type and phyB Sorghum mutants show that bud outgrowth correlates with increased sugar and cytokinin signalling and conversely, that phyB dormant buds display upregulation of Trehalose phosphate phosphatase, DARK-INDUCED1 as well as ABAand senescence-related genes. 15. Hao X, Yang Y, Yue C, Wang L, Horvath DP, Wang X: Comprehensive transcriptome analyses reveal differential gene expression profiles of Camellia sinensis axillary buds at para-, endo-, ecodormancy, and bud flush stages. Front Plant Sci 2017, 8:1-19. 16. Kerr SC, Gaiti F, Beveridge CA, Tanurdzic M: De novo transcriptome assembly reveals high transcriptional complexity in Pisum sativum axillary buds and shows rapid changes in expression of diurnally regulated genes. BMC Genomics 2017, 18:221. 17. Khalil-Ur-Rehman M, Sun L, Li C-X, Faheem M, Wang W, Tao J-M: Comparative RNA-seq based transcriptomic analysis of bud dormancy in grape. BMC Plant Biol 2017, 17:18. 18. Taranco´n C, Gonza´lez-Grandı´o E, Oliveros JC, Nicolas M,  Cubas P: A conserved carbon starvation response underlies bud dormancy in woody and herbaceous species. Front Plant Sci 2017, 8:1-21. Gene Set Enrichment Analyses of ‘active vs dormant’ bud transcriptomic data from Arabidopsis, poplar and grapevine reveal a widely conserved C starvation (or LES) syndrome that anticipates and underlies bud eco-, para-, and endodormancy in these distantly related species. 19. Thimm O, Bla¨sing O, Gibon Y, Nagel A, Meyer S, Kru¨ger P, Selbig J, Mu¨ller LA, Rhee SY, Stitt M: MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 37:914-939. 20. Rolland F, Baena-Gonzalez E, Sheen J: Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 2006, 57:675-709. 21. Tome´ F, Na¨gele T, Adamo M, Garg A, Marco-Llorca C, Nukarinen E, Pedrotti L, Peviani A, Simeunovic A, Tatkiewicz A et al.: The low energy signaling network. Front Plant Sci 2014, 5:353. 22. Gonzali S, Loreti E, Solfanelli C, Novi G, Alpi A, Perata P: Identification of sugar-modulated genes and evidence for in www.sciencedirect.com

vivo sugar sensing in Arabidopsis. J Plant Res 2006, 119:115-123. 23. Osuna D, Usadel B, Morcuende R, Gibon Y, Bla¨sing OE, Ho¨hne M, Gu¨nter M, Kamlage B, Trethewey R, Scheible W-R et al.: Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 2007, 49:463-491. 24. Sulpice R, Pyl E-T, Ishihara H, Trenkamp S, Steinfath M, WituckaWall H, Gibon Y, Usadel B, Poree F, Piques MC et al.: Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci 2009, 106:10348-10353. 25. Barbier F, Pe´ron T, Lecerf M, Perez-Garcia M-D, Barrie`re Q,  Rol9 c´ık J, Boutet-Mercey S, Citerne S, Lemoine R, Porcheron B et al.: Sucrose is an early modulator of the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida. J Exp Bot 2015, 66:2569-2582. This work shows that sugar causes sustained bud outgrowth as well as early down-regulation of RhMAX2 and RhBRC1 in Rosa hybrida. Moreover, sugar induces auxin synthesis and signalling thus establishing a relationship between auxin, SL and sugar during bud development. 26. Kebrom TH, Brutnell TP, Finlayson SA: Suppression of sorghum axillary bud outgrowth by shade, phyB and  defoliation signalling pathways. Plant Cell Environ 2009, 33:48-58. This paper provides evidence that low R:FR and defoliation act through independent pathways to promote bud dormancy in Sorghum. SbTB1 is specifically induced by shade whereas cell-cycle genes studied are exclusively downregulated by defoliation. Interestingly, SbMAX2 is upregulated in buds under both types of stimuli. 27. Kebrom TH, Chandler PM, Swain SM, King RW, Richards RA, Spielmeyer W: Inhibition of tiller bud outgrowth in the tin mutant of wheat is associated with precocious internode development. Plant Physiol 2012, 160:308-318. 28. Mason MG, Ross JJ, Babst Ba, Wienclaw BN, Beveridge Ca:  Sugar demand, not auxin, is the initial regulator of apical dominance. Proc Natl Acad Sci 2014, 111:6092-6097. This paper provides evidence that in pea, apical dominance is controlled by the shoot apex demand for sugars, which limits sugar availability to the axillary buds. Furthermore, it shows that apical dominance correlates with sugar availability, but not with apically supplied auxin. 29. Kebrom TH, Mullet JE: Photosynthetic leaf area modulates  tiller bud outgrowth in sorghum. Plant Cell Environ 2015, 38:1471-1478. This paper shows that even small changes in photosynthetic leaf area (and probably sucrose availability) affect the propensity of tiller buds to grow out in Sorghum 30. Fichtner F, Barbier FF, Feil R, Watanabe M, Annunziata MG,  Chabikwa TG, Ho¨fgen R, Stitt M, Beveridge CA, Lunn JE: Trehalose 6-phosphate is involved in triggering axillary bud outgrowth in garden pea (Pisum sativum L.). Plant J 2017 http:// dx.doi.org/10.1111/tpj.13705. This paper reports evidence of the tight association between the rise in Tre6P levels and the initiation of bud outgrowth, and supports the view that Tre6P acts as a signal of sucrose availability in nodes and mediates the response of bud dormancy release in pea. 31. Kebrom TH, Burson BL, Finlayson SA: Phytochrome B represses teosinte branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol 2006, 140:1109-1117. 32. Baena-Gonza´lez E, Rolland F, Thevelein JM, Sheen J: A central integrator of transcription networks in plant stress and energy signalling. Nature 2007, 448:938-942. n9 33. Wen H, Girault T, Barbier F, Pe´ron T, Brouard N, Pe cı´k A, Nova´k O, Vian A, Sakr S, Lothier J et al.: Cytokinins are initial targets of light in the control of bud outgrowth. Plant Physiol 2016, 172:489-509. 34. Corot A, Roman H, Douillet O, Autret H, Perez-Garcia M-D, Citerne S, Bertheloot J, Sakr S, Leduc N, Demotes-Mainard S: Cytokinins and abscisic acid act antagonistically in the regulation of the bud outgrowth pattern by light intensity. Front Plant Sci 2017, 8:1724. Current Opinion in Plant Biology 2018, 41:102–109

108 Growth and development

35. Pokhilko A, Flis A, Sulpice R, Stitt M, Ebenho¨h O: Adjustment of carbon fluxes to light conditions regulates the daily turnover of starch in plants: a computational model. Mol Biosyst 2014, 10:613.

49. Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M: Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 2014, 240:399-408.

36. Cho Y-H, Hong J-W, Kim E-C, Yoo S-D: Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol 2012, 158:1955-1964.

50. Ueda H, Kusaba M: Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol 2015, 169:138-147.

37. Martı´n-Trillo M, Cubas P: TCP genes: a family snapshot ten years later. Trends Plant Sci 2010, 15:31-39. 38. Nietzsche M, Landgraf R, Tohge T, Bo¨rnke F: A protein–protein interaction network linking the energy-sensor kinase SnRK1 to multiple signaling pathways in Arabidopsis thaliana. Curr Plant Biol 2016, 5:36-44.

51. Dun EA, de Saint Germain A, Rameau C, Beveridge CA: Antagonistic action of strigolactone and cytokinin in bud  outgrowth control. Plant Physiol 2012, 158:487-498. This study proposes that SL and CK have antagonistic effects on bud outgrowth in pea and probably act directly inside the buds to regulate shoot branching. In addition it shows that PsBRC1 expression is regulated by CK and SL without a requirement for protein synthesis.

39. Confraria A, Martinho C, Elias A, Rubio-Somoza I, BaenaGonza´lez E: miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis. Front Plant Sci 2013, 4:197.

52. Gan S, Amasino RM: Inhibition of leaf senescence by autoregulated production of cytokinin. Science 1995, 270:1986-1988.

40. Yao C, Finlayson SA: Abscisic acid is a general negative  regulator of Arabidopsis axillary bud growth. Plant Physiol 2015, 169:611-626. Using ABA biosynthesis mutants (nced3, aba2), the authors show that ABA acts as a growth repressor of Arabidopsis axillary buds both in low and high R:FR. They propose that this activity occurs downstream of, or independently of, the MAX pathway and BRC1.

53. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Page`s V, Dun EA,  Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC et al.: Strigolactone inhibition of shoot branching. Nature 2008, 455:189-194. This paper characterized SL as a novel carotenoid-derived hormonal signal that inhibits shoot branching in plants. The citation in this review is in relation to the experiment in which exogenous application of SL to buds is able to suppress shoot branching in pea and Arabidopsis.

41. Gonza´lez-Grandı´o E, Pajoro A, Franco-Zorrilla JM, Taranco´n C,  Immink RGH, Cubas P: Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds. Proc Natl Acad Sci 2017, 114:E245-E254. This paper describes for the first time the direct relationship between BRC1 and ABA signalling, places this TCP transcription factor upstream of ABA synthesis and response in the control of axillary bud dormancy and proposes a genetic pathway involving three HD-ZIP-encoding genes and NCED3 as direct targets of BRC1. 42. Holalu SV, Finlayson SA: The ratio of red light to far red  light alters Arabidopsis axillary bud growth and abscisic acid signalling before stem auxin changes. J Exp Bot 2017, 68:943-952. This work studies the dynamics of bud elongation and the molecular changes occurring in Arabidopsis buds in low and high R:FR. They confirm that a BRC1 downregulation and decrease in ABA levels precede bud elongation induced by high R:FR. 43. Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leo´n P: Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 2000, 14:2085-2096. 44. Vergara R, Noriega X, Aravena K, Prieto H, Pe´rez FJ: ABA represses the expression of cell cycle genes and may modulate the development of endodormancy in grapevine buds. Front Plant Sci 2017, 8:812. 45. Rodrigues A, Adamo M, Crozet P, Margalha L, Confraria A,  Martinho C, Elias A, Rabissi A, Lumbreras V, Gonzalez-Guzman M et al.: ABI1 and PP2CA phosphatases are negative regulators of snf1-related protein kinase1 signaling in Arabidopsis. Plant Cell 2013, 25:3871-3884. This paper shows that the ABI1 and PP2CA phosphatases (ABA signalling repressors) interact with and inhibit SnRK1 function. Accordingly, mutants of these genes display altered sugar responses similar to those caused by SnRK1 overexpression. 46. Zhao Y, Chan Z, Gao J, Xing L, Cao M, Yu C, Hu Y, You J, Shi H,  Zhu Y et al.: ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci 2016, 113:1919-1923. This study describes a signalling cascade that links ABA perception and senescence responses. 47. Trivellini A, Jibran R, Watson LM, O’Donoghue EM, Ferrante A, Sullivan KL, Dijkwel PP, Hunter DA: Carbon deprivation-driven transcriptome reprogramming in detached developmentally arresting Arabidopsis inflorescences. Plant Physiol 2012, 160:1357-1372. 48. Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR: Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front Plant Sci 2017, 8:475. Current Opinion in Plant Biology 2018, 41:102–109

54. Stirnberg P, Furner IJ, Ottoline Leyser HM: MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 2007, 50:80-94. 55. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J: d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 2009, 50:1416-1424. 56. Chevalier F, Nieminen K, Sa´nchez-Ferrero JC, Rodrı´guez ML, Chagoyen M, Hardtke CS, Cubas P: Strigolactone promotes degradation of DWARF14, an a/b hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 2014, 26:1134-1150. 57. Brewer PB, Yoneyama KKK, Filardo F, Meyers E, Scaffidi A,  Frickey T, Akiyama K, Seto Y, Dun EA, Cremer JE et al.: Lateral branching oxidoreductase acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc Natl Acad Sci U S A 2016, 113:6301-6306. This paper describes the discovery of a novel component of the SL biosynthesis in Arabidopsis, Lateral Branching Oxidoreductasa (LBO), which acts downstream of MAX1 to further process MeCLA into a yet unknown bioactive product. 58. Kameoka H, Dun EA, Lopez-Obando M, Brewer PB, de Saint  Germain A, Rameau C, Beveridge CA, Kyozuka J: Phloem transport of the receptor DWARF14 protein is required for full function of strigolactones. Plant Physiol 2016, 172:1844-1852. This study provides evidence of a non-cell autonomous activity of D14 in pea and rice to inhibit branching. RAMOSUS3, the D14 pea ortholog, moves both acropetally and basipetally in pea grafting experiments. Moreover, rice D14 moves from the phloem cells, where the gene is expressed, into the axillary buds in a SL-independent manner. 59. Brewer PB, Dun EA, Gui R, Mason MG, Beveridge CA:  Strigolactone inhibition of branching independent of polar auxin transport. Plant Physiol 2015, 168:1820-1829. This article emphasizes the direct action of SL in bud outgrowth control independently of auxin transport: impaired auxin transport in pea SLdeficient plants does not inhibit branching, whereas SL suppresses shoot branching even in the presence of auxin transport inhibitors. 60. Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA: Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 2009, 150:482-493. 61. Braun N, de Saint Germain A, Pillot J-P, Boutet-Mercey S, Dalmais M, Antoniadi I, Li X, Maia-Grondard A, Le Signor C, Bouteiller N et al.: The pea TCP transcription factor PsBRC1 acts downstream of Strigolactones to control shoot branching. Plant Physiol 2012, 158:225-238. www.sciencedirect.com

A low energy syndrome induced in dormant buds Martı´n-Fontecha, Taranco´n and Cubas 109

62. Dun EA, de Saint Germain A, Rameau C, Beveridge CA: Dynamics of strigolactone function and shoot branching responses in Pisum sativum. Mol Plant 2013, 6:128-140. 63. Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H,  Yuan Y et al.: DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 2013, 504:401-405. This study along with [64], report the discovery of DWARF53 as the repressor of SL signalling in rice, which is degraded through a SLdependent, proteasome-mediated pathway. 64. Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H,  Dong W, Gan L et al.: D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature 2013, 504:406-410. See annotation to Ref. [63]. 65. Soundappan I, Bennett T, Morffy N, Liang Y, Stanga JP, Abbas A, Leyser O, Nelson DC: SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 2015, 27:3143-3159. 66. Wang L, Wang B, Jiang L, Liu X, Li X, Lu Z, Meng X, Wang Y, Smith SM, Li J: Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 2015, 27:3128-3142. 67. Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Mu¨ller D, Domagalska MA, Leyser O: Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 2010, 137. 68. Shinohara N, Taylor C, Leyser O: Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 2013, 11:e1001474. 69. Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O: The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 2006, 16:553-56369. 70. Aguilar-Martı´nez JA, Poza-Carrio´n C, Cubas P: Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 2007, 19:458-472. 71. Drummond RSM, Janssen BJ, Luo Z, Oplaat C, Ledger SE, Wohlers MW, Snowden KC: Environmental control of branching in petunia. Plant Physiol 2015, 168:735-751. 72. Seale M, Bennett T, Leyser O: BRC1 expression regulates bud  activation potential but is not necessary or sufficient for bud growth inhibition in Arabidopsis. Development 2017, 144:1661-1673. This study proposes that BRC1 modulates bud activation potential in coordination with the systemic auxin transport-mediated regulatory system. 73. Doebley J, Stec A, Hubbard L: The evolution of apical dominance in maize. Nature 1997, 386:485-488.

www.sciencedirect.com

74. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X et al.: Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 2010, 42:541-544. 75. Lu Z, Yu H, Xiong G, Wang J, Jiao Y, Liu G, Jing Y, Meng X, Hu X, Qian Q et al.: Genome-wide binding analysis of the transcription activator IDEAL PLANT ARCHITECTURE1 reveals a complex network regulating rice plant architecture. Plant Cell 2013, 25:3743-3759. 76. Liu J, Cheng X, Liu P, Sun J: miR156-targeted SBP-box transcription factors interact with DWARF53 to Regulate TEOSINTE BRANCHED1 and BARREN STALK1 expression in bread wheat. Plant Physiol 2017, 174:1931-1948. 77. Luo L, Li W, Miura K, Ashikari M, Kyozuka J: Control of tiller growth of rice by OsSPL14 and strigolactones, which work in two independent pathways. Plant Cell Physiol 2012, 53:1793-1801. 78. Bennett T, Liang Y, Seale M, Ward S, Mu¨ller D, Leyser O: Strigolactone regulates shoot development through a core signalling pathway. Biol Open 2016, 5 bio.021402. 79. Song X, Lu Z, Yu H, Shao G, Xiong J, Meng X, Jing Y, Liu G,  Xiong G, Duan J et al.: IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res 2017, 27:1128-1141. This work provides evidence of the potential role of the rice SPL transcription factor Ideal Plant Architecture 1 (IPA1) as a mediator of SLinduced control of tiller development. D53 interacts with IPA1 in vivo and in vitro and suppresses IPA1 transcriptional activity. 80. Nicolas M, Rodrı´guez-Buey ML, Franco-Zorrilla JM, Cubas P: A recently evolved alternative splice site in the BRANCHED1a gene controls potato plant architecture. Curr Biol 2015, 25:1799-1809. n9 c´ık A, 81. Roman H, Girault T, Barbier F, Pe´ron T, Brouard N, Pe Nova´k O, Vian A, Sakr S, Lothier J et al.: Cytokinins are initial  targets of light in the control of bud outgrowth. Plant Physiol 2016, 172:489-509. This study proposes that CK signalling is the initial effector of the pathway controlling bud outgrowth by light in Rosa hybrida. Exogenous CK application is sufficient to promote bud outgrowth in darkness. Moreover buds treated with CK show a downregulation of genes involved in bud repression (RhMAX2 and RhBRC1), and upregulation of genes involved in auxin metabolism and transport and in regulation of sugar sink strength. 82. Whipple CJ, Kebrom TH, Weber AL, Yang F, Hall D, Meeley R,  Schmidt R, Doebley J, Brutnell TP, Jackson DP: Grassy tillers1 promotes apical dominance in maize and responds to shade signals in the grasses. Proc Natl Acad Sci 2011, 108:506-512. This paper characterizes the maize grassy tillers 1 (gt1) gene, induced by FR-rich light and which encodes an HD-Zip transcription factor. It first proposed that the gt1 gene was genetically downstream of tb1. This pathway has been later demonstrated at the molecular level in Arabidopsis.

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