A Conserved Carbon Starvation Response Underlies Bud Dormancy in Woody and Herbaceous Species

Abstract

Plant shoot systems give rise to characteristic above-ground plant architectures. Shoots are formed from axillary meristems and buds, whose growth and development is modulated by systemic and local signals. These cues convey information about nutrient and water availability, light quality, sink/source organ activity and other variables that determine the timeliness and competence to maintain development of new shoots. This information is translated into a local response, in meristems and buds, of growth or quiescence. Although some key genes involved in the onset of bud latency have been identified, the gene regulatory networks (GRNs) controlled by these genes are not well defined. Moreover, it has not been determined whether bud dormancy induced by environmental cues, such as a low red-to-far-red light ratio, shares genetic mechanisms with bud latency induced by other causes, such as apical dominance or a short-day photoperiod. Furthermore, the evolution and conservation of these GRNs throughout angiosperms is not well established. We have reanalyzed public transcriptomic datasets that compare quiescent and active axillary buds of Arabidopsis, with datasets of axillary buds of the woody species Vitis vinifera (grapevine) and apical buds of Populus tremula x Populus alba (poplar) during the bud growth-to-dormancy transition. Our aim was to identify potentially common GRNs induced during the process that leads to bud para-, eco- and endodormancy. In Arabidopsis buds that are entering eco- or paradormancy, we have identified four induced interrelated GRNs that correspond to a carbon (C) starvation syndrome, typical of tissues undergoing low C supply. This response is also detectable in poplar and grapevine buds before and during the transition to dormancy. In all eukaryotes, C-limiting conditions are coupled to growth arrest and latency like that observed in dormant axillary buds. Bud dormancy might thus be partly a consequence of the underlying C starvation syndrome triggered by environmental and endogenous cues that anticipate or signal conditions unfavorable for sustained shoot growth.

Abscisic acid catabolism enhances dormancy release of grapevine buds

“…Taken together, it appears that (a) regulation of outgrowth of grapevine summer lateral buds may be similar to that of the axillary buds of annuals. In that context, and in agreement with the findings reported by Yao and Finlayson (2015), it is worth mentioning that significant increases in auxin levels were detected in the shoot tips of the Tarancón, & Cubas, 2018;Tarancón, González-Grandío, Oliveros, Nicolas, & Cubas, 2017). In agreement with the cascades proposed for poplar and grapevine (Ophir et al, 2009;Ruttink et al, 2007), ABA and ethylene are proposed as central regulators that respond to sugar starvation (Tarancón et al, 2017).…”

“…In agreement, regulation of bud activity via modulation of ABA metabolism and/or signalling gained recent significant support that collectively suggests ABA‐mediated repression of growth resumption of both apical and lateral buds during para and endodormancy of annuals and woody perennials. Cell cycle arrest, plasmodesmata closure, regulation of the activities of callose synthase and glucanases, and regulation of movement/availability of FT to the bud meristem are among the proposed targets regulated by ABA, directly or indirectly (Arend et al, ; Tarancón et al, ; Tylewicz et al, ; Vergara et al, ; Yao & Finlayson, ). In light of the central role of ABA in regulation of seed germination, the assumption that conserved primary regulatory mechanism exists that control activity of the meristems may be supported.…”

“…data not shown); (b) regulation of activity of summer lateral and woody dormant buds may share similar regulatory steps, including ABA‐directed repression of the meristem activation. Excitingly, such potential similarity in regulation of activity of summer lateral and woody buds was recently proposed based on preliminary comparison of transcript profiles of Arabidopsis lateral buds, poplar apical buds, and grapevine woody lateral buds (Martín‐Fontecha, Tarancón, & Cubas, ; Tarancón, González‐Grandío, Oliveros, Nicolas, & Cubas, ). In agreement with the cascades proposed for poplar and grapevine (Ophir et al, ; Ruttink et al, ), ABA and ethylene are proposed as central regulators that respond to sugar starvation (Tarancón et al, ).…”

“…Excitingly, such potential similarity in regulation of activity of summer lateral and woody buds was recently proposed based on preliminary comparison of transcript profiles of Arabidopsis lateral buds, poplar apical buds, and grapevine woody lateral buds (Martín‐Fontecha, Tarancón, & Cubas, ; Tarancón, González‐Grandío, Oliveros, Nicolas, & Cubas, ). In agreement with the cascades proposed for poplar and grapevine (Ophir et al, ; Ruttink et al, ), ABA and ethylene are proposed as central regulators that respond to sugar starvation (Tarancón et al, ). However, differences likely exist in regulation of the ABA level in these two types of buds, based on the extremely low level of VvBRC1 transcript in dormant woody buds, suggesting that VvBRC1 is not a player during the endodormancy cycle (Or 2016 unpublished; Fasoli et al, ).…”

Carbon starvation reduces carbohydrate and anthocyanin accumulation in red‐fleshed fruit via trehalose 6‐phosphate and MYB27

“…Class II TPS genes do not appear to encode catalytically active TPS proteins, and the class II TPSs have been proposed to have a regulatory function (Lunn et al ). Some class II TPS genes, especially those from the clades containing AtTPS8‐AtTPS11 , are strongly up‐regulated in different plant species under carbon starvation or have been implicated in the regulation of carbon allocation (Baena‐González et al ; Barraza et al ; Price et al ; Tarancón et al ). In kiwifruit outer pericarp tissue, several class II TPS genes (three TPS7 and two TPS11 ) were strongly up‐regulated under carbon starvation, which may have affected the reduction of Tre6P concentration by modulating catalytic TPSs and contributing to starvation signalling.…”