2017/12/04 by Santiago Signorelli, Patricia Agudelo‐Romero, Patricia Agudelo-Romero +4 · 45 citations
Agricultural and Biological Sciences · Biochemistry, Genetics and Molecular Biology · Chemistry · #Axillary bud #Biochemistry #Biology #Botany #Cell biology #Chemistry #Commit #Computer science #Endocrinology #Energy (signal processing) #Energy metabolism #Light effects on plants #Oxygen #Physics #Plant Molecular Biology Research #Plant Reproductive Biology
paper · doi:10.1104/pp.17.01479
published in PLANT PHYSIOLOGY 176(2), 1171-1181 (Oxford University Press)
openalex publication_date 2017/12/04 · openalex created_date 2025/10/10 · openalex updated_date 2026/07/30
The hierarchy of events governing the resumption of growth of a quiescent axillary bud are poorly understood. During quiescence, a homeostasis exists in phytohormone and source/sink regulation, which represses the metabolic and mitotic progression of the bud. Environmental change and shoot development can alter the homeostasis, leading to a binary state change and the commitment to growth. Within this context, light and oxygen availability can serve both metabolic and signaling functions. However, the question of substrate versus signal has proven challenging to resolve; in the case of sugars, there are disparities in the data from apical and axillary buds in juvenile shoots, while in postdormant perennial buds, light has only a facultative role in the decision, but signaling may still be essential for bud fate. We briefly update the roles and hierarchies of light-, energy-, and oxygen-dependent functions in axillary bud outgrowth of annual shoots, before focusing discussion on the role of chloroplast-to-nucleus retrograde signaling genes such as GENOMES UNCOUPLED4 (GUN4) and ELONGATED HYPOCOTYL5 (HY5) in bud burst responses to light, examining available transcriptome data from postdormant grapevine (Vitis vinifera) buds. We discuss the evidence implicating cryptochromes (CRY) in the activation of HY5 expression in grapevine, leading to chloroplast biogenesis in the buds, and that this occurs via a biogenic rather than an adaptive developmental process. The cytokinin (CK) signaling pathways and the light-regulated expression of chloroplast processes, especially those involved in carbon and oxygen metabolism, may also play an important role in bud burst. The mechanisms that control apical dominance in juvenile or annual shoots are well characterized. Removing the apex can result in axillary bud outgrowth, as can changes in light intensity and quality. Here, axillary bud outgrowth is regulated by signals arising from the apex, which contain several light quality and quantity sensing pigments. Of these, phytochromes (PHY) are perhaps the best characterized. PHY sense red and far-red light, while cryptochromes and phototropins are involved in the perception of blue light. These photoreceptors regulate the expression of different transcription factors to coordinate light-dependent photomorphogenesis. Some plant species require light for axillary bud outgrowth (annual shoots), but in others the requirement for light is facultative (Leduc et al., 2014). In addition, the buds of many perennial plants can resume growth following a period of dormancy. In this case, apical suppression may temporarily break down, and the axillary bud may be considered more independent, at least until a new homeostasis is established along the shoot. Moreover, there is no evidence postdormant perennial buds require light, although increased light intensity can accelerate bud burst in a range of species (Maynard et al., 1990; Rageau et al., 1998; Søgaard et al., 2008; Caffarra and Donnelly, 2011). The influence of light on meristem activity involves at least two distinct but possibly cross-regulatory processes: direct regulation of gene expression via photoreceptors, and an indirect process involving the generation of energy through photosynthesis and respiration. A potential third pathway is the signaling of tissue oxygen status, which has been shown to be a primary cue for developmental transitions in plants, including photomorphogenesis (Considine et al., 2017). In this Update, we consider the respective roles of light, energy, and oxygen as primary cues for axillary bud outgrowth, with a particular focus on the signaling pathways that trigger the resumption of growth following quiescence. We provide a concise overview of (1) the physiology of axillary meristems and buds, focusing on genotypic differences in bud requirements for light and energy to trigger outgrowth, and (2) the importance of transcriptional regulation of plastid functions in the resumption of growth in quiescent grapevine buds following dormancy. Vascular plants display indeterminate growth and a branched root and shoot structure, which is enabled by the spatial distribution and activation of meristems (Sussex and Kerk, 2001). Most terrestrial species exhibit axillary branching rather than the more ancestral dichotomous branching. Axillary buds are classed as sylleptic or proleptic, and both types may be quiescent for sustained periods of time, being able to resume growth immediately upon perception of appropriate developmental, metabolic, or environmental cues. Additionally, proleptic buds of some species possess the ability to exhibit true dormancy, which is a developmental and internally repressed condition that requires environmental entrainment to enable a transition to quiescence (Considine and Considine, 2016). Dormant buds are metabolically isolated from the shoot by physiological barriers such as the deposition of callose. In this situation, apical dominance in its strictest sense may not apply, at least until dormancy is relieved. In the following discussion, we focus on quiescence and the role of light in the processes promoting axillary bud outgrowth, particularly in intact juvenile or annual shoots. The dominance behavior of the apical meristem, which enforces and maintains axillary bud quiescence, is facilitated by mobile signals such as Suc and phytohormones, particularly auxin. The role of apically derived auxin in maintaining axillary bud quiescence was established nearly a century ago (Thimann and Skoog, 1934; for a detailed review, refer to Rameau et al., 2015). However, auxin signaling intersects with other phytohormones such as strigolactones and CKs to regulate the outgrowth of axillary buds. Each phytohormone functions downstream of light signaling pathways initiated by photoreceptors (Leduc et al., 2014). Phytohormone signaling pathways are thought to converge at the level of the BRANCHED1 transcription factor (and homologs), which is a central repressor of axillary bud outgrowth (Dun et al., 2012). However, auxin transport may be too slow to account for observed bud outgrowth kinetics, while Suc availability may provide a more rapid regulatory trigger (Renton et al., 2012; Mason et al., 2014). The application of Suc results in a dose-dependent activation of bud outgrowth, a process that apparently antagonizes auxin- and strigolactone-mediated signaling, although Suc effects were at least partly independent of these pathways (Barbier et al., 2015a). Light and Suc can act both as signals and sources of energy for bud growth. Suc functions both as a metabolic substrate and signal controlling development, notably via the TARGET OF RAPAMYCIN (TOR) kinase and SUCROSE NONFERMENTING1-RELATED KINASE1 (SnRK1). Several species such as Rosa sp. and pea (Pisum sativum) require light for axillary bud outgrowth, while others have varying facultative requirements for light (Leduc et al., 2014). In axillary buds of Rosa sp., the expression of genes involved in Suc hydrolysis and mobilization is promoted by light; however, Suc cannot compensate for light in activating bud outgrowth (Girault et al., 2008). Application of Suc and nonmetabolizable analogs such as palatinose promotes the rate of bud outgrowth in Rosa, Arabidopsis (Arabidopsis thaliana), and pea when light is present (Rabot et al., 2012; Barbier et al., 2015b). These data suggest that photoreceptor-mediated signaling is a primary requirement for bud outgrowth, and that Suc synthesis and metabolism via photosynthesis are essential downstream components. Several lines of evidence suggest that Suc may function as a signal rather than energy substrate in augmenting bud outgrowth (Barbier et al., 2015a). The altered shoot branching phenotype of Arabidopsis mutants deficient in trehalose-6-P (T6P) cannot be explained by metabolic or energy functions because T6P only accumulates to low concentrations even in wild-type plants (Chary et al., 2008). Overexpression of HEXOKINASE1 leads to increased bud outgrowth and expression of genes involved in abscisic acid-related processes, together with reduced expression of auxin-related genes (Kelly et al., 2012). Nevertheless, other studies have linked the effects of Suc to metabolic requirements (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 from studies of the shoot apical meristem (SAM). Auxin- and Suc-mediated pathways independently promote the cell cycle by activating TOR kinase, which in turn directly activates key cell cycle regulators, as well as the stem cell identity protein WUSCHEL (WUS; Pfeiffer et al., 2016; Li et al., 2017). The fact that both auxin and Suc are required is particularly interesting for two reasons. First, the auxin response in the SAM is dependent on a small GTPase Rho-like protein (ROP2). This protein was shown to be activated by both the direct application of auxins and the light-induced auxins in shoot apices (Li et al., 2017). In addition, the application of auxin effectively substituted light to activate the TOR-dependent formation of true leaves, when Suc was present (Li et al., 2017). The ROP2 was shown to directly interact with TOR kinase, promoting its kinase activity (Cai et al., 2017). ROP2 also functions in oxygen- and redox-dependent survival (Baxter-Burrell et al., 2002). The expression of ROP2 is promoted by HYPOXIA RESPONSIVE UNIVERSAL STRESS PROTEIN1 that transduces the hypoxic cue via Group VII ETHYLENE RESPONSE FACTORs (ERF-VII), which are stabilized in hypoxic conditions (Gonzali et al., 2015). Hence, these data strongly suggest auxin and Suc pathways converge with oxygen signaling upstream of TOR kinase (Considine, 2017). We will return to oxygen signaling below. Second, the Suc effect on TOR and WUS is consistent with a metabolic function because Glc, not palatinose, 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 function together in axillary bud outgrowth. Interestingly, the addition of Suc is sufficient to trigger the growth of the root apical meristem but not the SAM. This finding may be explained by the relatively higher concentrations of auxin in the root apical meristem compared with the SAM, and also the light dependency of auxin synthesis in the SAM (Li et al., 2017). Increased auxin synthesis and transport from the axillary buds occur during the transition to bud outgrowth, suggesting that photoreceptor-dependent auxin synthesis in the axillary bud meristems may be a primary trigger for bud outgrowth. However, strigolactone has also been suggested to be a signal output from photosynthesis. Increased axillary branching is evident in an Arabidopsis mutant lacking the PsbP Domain Protein5 (PPD5), which is a key component of photosystem II (Roose et al., 2011). While PPD5 is essential for autotrophic metabolism and optimal oxygen-evolving activity, the ppd5 mutants are able to sustain electron transport, and the phenotype can be rescued by the application of strigolactone, indicating that the phenotype is more likely to be due to hormone defects than energy deficits. Perhaps also relevant, axis initiation in tomato (Solanum lycopersicum) requires light signaling via phytochromes but not photosynthesis (Yoshida et al., 2011). Meristems cultured with Suc in darkness, or in the presence of the carotenoid inhibitor norflurazon in the light, fail to initiate new leaf primordia. Nevertheless, axis initiation is a different process than organ development, i.e. the resumption of growth following quiescence. In many perennial species, proleptic buds resume growth following a prolonged period of dormancy (Considine and Considine, 2016). The dormant bud becomes desiccated and metabolically isolated by callose deposition in the plasmodesmata (Rinne et al., 2011). In this state, the meristem tissues are enclosed, typically by lignified bracts and scales (Fig. 1). Following dormancy, the bud resumes a quiescent but receptive state with a connected symplast. Studies of several woody species have shown that the internal tissues and leaf primordia of quiescent buds are largely etiolated and lack chlorophyll (Solymosi et al., 2012). The plastids in such buds, however, exist in different developmental stages that are partly related to the nature of the tissues in which they reside (Solymosi et al., 2012). For example, and were in the and leaf primordia of buds (Solymosi et al., 2012). bud the contain although they are not (Solymosi et al., 2012). However, in buds contain and the leaf primordia of the buds contain or but not (Solymosi et al., In buds, both and leaf primordia contain and (Solymosi et al., 2012). Hence, leaf primordia not contain more plastids than the leaf primordia. tissue oxygen status, and growth of of postdormant grapevine buds. is a of a quiescent grapevine bud with shoots and by of and lignified A of the tissue oxygen of a bud during quiescence and bud burst as by an oxygen is The of the from scales to the of the primary meristem, is the axis and the in at and to et al., 2015). is also evidence of regulated during bud burst in The postdormant bud is hypoxic and oxygen in a regulated during the of bud to leaf et al., studies the and of several species and regulated tissue oxygen et al., 2008; and et al., 2016). In grapevine buds as in the scales were shown to be a to oxygen however, this not the of oxygen in the primary bud bud burst particularly the oxygen was not at the of the bud (Fig. et al., 2015). not in buds, the low oxygen of is in the spatial of metabolic particularly in to and energy and has that oxygen (and has a regulatory role in dormancy and the oxygen-dependent of the transition from to metabolism and quiescence to growth et al., et al., 2014). such has been directly to bud however, is that Arabidopsis mutants in the regulated of the transcription factors reduced apical dominance et al., expression data of grapevine buds may provide some into the roles of light and oxygen in bud burst. grapevine buds not require light to however, buds are in chlorophyll synthesis and an etiolated phenotype et al., We have the gene expression of buds, in during bud burst in the presence and of light at and change rate which leaf available at A the developmental control of gene expression and primary metabolism et al., Interestingly, there were changes in physiological or of and buds the a of genes were at or both genes regulated at both A small of genes expression in response to light, and these will be in A key component of photomorphogenesis is a transcription factor to the of genes to activate expression et al., This transcription factor is activated by different types of light, through the of the photoreceptors and et al., at least in due to regulation of also as which HY5 to the et al., the function of HY5 in photomorphogenesis in Arabidopsis has been its expression and response to light in perennial buds not been the transcriptome of the grapevine buds we observed that the expression of genes for the or the upstream photoreceptors and was not regulated by the presence of light at of growth. However, the expression of two genes and HY5 was increased at in the buds to light In species and blue light is sufficient to promote bud outgrowth until (Girault et al., 2008; et al., this evidence that in buds, photoreceptors are of bud burst by promoting HY5 The data also suggest that in grapevine buds, light and perception is not until growth. the expression and of grapevine genes data in expression was from grapevine buds at in the presence or of light at and following from from A to the of the to and HY5 genes involved in chlorophyll light and the cycle et al., 2008). The expression of many genes involved in these processes was at in buds compared with those in and of many of the light-regulated genes in grapevine buds are also during photomorphogenesis in Arabidopsis et al., and in et al., et al., The of light-regulated genes in these species those for photosystem and and and and as well as and chlorophyll Moreover, the expression of genes two which are involved in of light in the was in grapevine buds at the of several of the cycle were also higher in buds at as in below. expression of genes during grapevine bud burst for and chlorophyll metabolic functions at in the presence or of light. at of with to not in the A chloroplast the genes in condition at a of genes the of HY5 including of genes to be regulated by HY5 as well as likely in and functions. This genes for two T6P the the factor and others (Fig. Some evidence has been that signaling pathways with HY5 et al., et al., 2012). may be that the factor is for this In be interesting to whether HY5 can the expression of these of light perception or prolonged were to the presence of light. For example, the expression of a of was in the light (Fig. the expression of a of also as was in the presence of light, to The of is a of such as and which photosynthesis et al., The expression of is repressed by Suc and Glc, and is by the Arabidopsis of the of a for signaling et al., These of the of grapevine buds demonstrate that a light-dependent photomorphogenesis becomes at of of the buds to environmental but not This finding that at the of bud burst other environmental such as are required to promote growth in the light signals that and retrograde signals are important for development et al., 2016). that act as retrograde signals in biogenic and Some genes that are involved in retrograde signaling, such as and are in grapevine buds in response to light. The mutants of Arabidopsis are in metabolism, suggesting that this pathway is important in biogenic The expression of genes involved in metabolism was in grapevine buds in response to light at In in the of which in turn to a protein and with HY5 to regulate the expression of genes et al., 2016). The expression of genes and HY5 was by light in grapevine buds at suggesting that the retrograde activation of genes occurs in buds. Hence, the plastids in the buds of species may be a biogenic process rather than an to the environmental conditions at the stages of bud burst. Light also occurs through the of signaling pathways in The expression of a gene for a protein was by light at in grapevine buds (Fig. This protein a key role in signal et al., 2002). The expression of the factor is to to light and CKs et al., also a role in chloroplast development et al., The expression of the factor was increased at in grapevine buds (Fig. This transcription factor represses signaling downstream of and et al., The expression of genes for of signaling, such as and was by light in grapevine buds. These suggest that the influence of light on grapevine buds involves signaling The expression of two other and involved in signaling was by light. there is in the functions of the different and which act as of signaling to promote development, the of this is et al., evidence that Suc and light-dependent auxin signaling converge upon meristem in promoting meristem growth. We auxin-related functions in the grapevine data shown (Fig. has been shown to function in the of dormancy callose in grapevine buds and to during bud however, direct application has apparently effect et al., and and A more in grapevine buds no genes as auxin and Suc function or with and the outgrowth potential et al., 2012). Nevertheless, of these studies were to auxin or Suc and may be Several involved in and metabolism were strongly regulated by light in grapevine buds at in the light. These of and two SUCROSE (Fig. The light-induced activation of expression of and Suc genes was largely at although at higher at a of were in the buds in the light at In Rosa sp., the light-dependent of is considered to be important in promoting and bud burst (Girault et al., 2008; et al., 2011). The finding that the expression of a was not regulated by light in grapevine may the differences in the light requirements of bud burst in Rosa sp. and in the expression of genes plastid carbon metabolism in grapevine buds was by light at Moreover, a of the were increased in the light, suggesting a for regulation of homeostasis and of for cycle activity et al., In the expression of genes involved in the of in the plastid was increased in the as were the of a (Fig. These suggest a requirement for to the pathway in the condition et al., 2012; et al., 2015). expression of genes during grapevine bud burst for and functions at in the presence or of light. and in and and at in the not in the SUCROSE T6P is a primary of energy two T6P were increased by light at while and T6P were in (and increased in the and These transcriptional differences suggest that reduced T6P or increased T6P occurs in the buds in the light compared with the We compared the grapevine bud gene expression at the data of the Arabidopsis transcriptional in et al., 2008). We the of the Arabidopsis of the grapevine genes and genes The Arabidopsis were the and compared with available Arabidopsis data the with the Arabidopsis Some of the Arabidopsis not a from the of the of studies to photomorphogenesis. Each of the were wild-type studies that light signaling and light conditions for example, the role of plastid biogenesis in light-dependent signaling et al., and the role of light-dependent regulation in photomorphogenesis et al., 2012). Several of the studies involving mutant lines that to grapevine buds also related to light and carbon signaling, for example, a of the role of the in light-dependent signaling et al., and a mutants et al., 2008). We of the data to developmental studies of or which The of data with from et of suggested the condition in was more than the of were of control of wild-type or mutants of the TOR protein kinase, indicating the condition was consistent with metabolism of et al., In addition, the to the of the Arabidopsis et al., the of involved in the of and the regulation of expression in this regulation of two genes for and two of the in responses et al., these data suggest that transcriptional changes by light in grapevine buds are to those observed in evidence of a role for chloroplast processes in carbon and oxygen metabolism during bud burst and the requirement for light to chloroplast also evidence of the effect of light on pathways for evident darkness, suggesting of to the The commitment to resume growth of postdormant perennial buds is by developmental such as CKs and While light can function as an upstream of these phytohormones, light is only a facultative requirement for the in many The of evidence that light rather than development, while other cues such as promote the outgrowth. from may also in the activation as both a and signaling While the present discussion has on the importance of light, blue light may also play a key role in bud burst. evidence the function of photoreceptors in blue light perception in HY5 which in turn activates gene bud outgrowth. and may also roles in light perception as they in Arabidopsis The developmental stages of plastids of buds can different perennial plants but also different tissues of the bud. The developmental regulation of the hypoxic state also important but largely roles in bud burst. The role of in and plastid and at the stages of bud burst is largely of the evidence the of light-induced signaling and transcriptional changes that the resumption of growth a period of quiescence in perennial buds and Arabidopsis Several particularly in to the role of light and oxygen in bud burst the required to even in are The following are genes which change and rate in the presence or of light at and and of genes the in genes at from of gene with data available at