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- W3202673263 abstract "This article is a Commentary on Ding et al. (2021), 232: 2339–2352. ‘… further dissection of phyB-PIF8 signaling will help reveal the complex interactions among environmental cues, local and long distance signaling and developmental stages.’ Upon absorption of red (R) light, the PrB form of phyB converts to an active PfrB form that photoreverts to the PrB form upon absorption of far red (FR) light (Legris et al., 2019). The PfrB form also reverts to the inactive PrB form in a process called ‘dark reversion’ and studies in Arabidopsis have shown that phyB is a thermal sensor with warm temperatures promoting and cold temperatures repressing this light-independent reversion. Photoactivated phyB initiates light signaling by repressing PIFs, mainly by promoting their degradation. PIFs are a small subfamily of basic helix-loop-helix transcription factors that have redundant as well as unique roles in Arabidopsis. Ding et al. studied loss- and gain-of-function PHYB, PIF4 and PIF8 poplar transgenics under a series of different daylength and temperature conditions that induce trees to approximate the phenophases of an annual growth and dormancy cycle. In long-day and warm temperature conditions, transgenics with PHYB downregulated, PIF4 overexpressed or PIF8 overexpressed showed characteristics of the shade avoidance syndrome (SAS) such as increased shoot elongation. Shaded plants receive FR-enriched light, favoring photoreversion to the inactive PrB form and PIF activity; hence, these results illustrate the conserved role of phyB in sensing and signaling the R : FR light ratio (Fig. 1). In contrast to their effects on shoot elongation in long day/warm temperature conditions, Ding et al. showed that PHYB promoted and PIF8 repressed growth when they manipulated the primary phenology signals to induce growth transitions (Fig. 1). However, the growth effects in these different environmental conditions are not completely opposite. In dicots, increases in internode elongation are due to enhanced activity of the rib meristem (Paul et al., 2014). In Populus and many trees, short days induce changes in the shoot apical meristem that cease the production of phytomers and induce bud formation, as well as terminate activity of the rib meristem. The rapid downregulation of FT2, an ortholog of the florigen FLOWERING LOCUS T (FT), in leaf is a key signaling event in this short-days response (Bohlenius et al., 2006; Hsu et al., 2011). Ding et al. showed that downregulation of PHYB or PIF8 reduced or increased FT2 expression, respectively, suggesting that the phyB-PIF8 module regulates short-days-induced growth cessation at least in part by altering FT2 expression. However, they reported similar changes in FT2 expression in long days, suggesting that growth effects in long days are independent of FT2. It is also possible that FT2 mediates different signaling in the shoot apical meristem and rib meristem and that coordination among these meristems depends on daylength. Additionally, comparisons of shoot apex and leaf transcriptomes of wild-type and PHYB transgenic trees indicated that daylength affects the spatial pattern of phyB signaling – phyB-mediated transcriptional effects were mostly limited to leaf in long days, but occur in both tissues, especially the shoot apex, after two weeks in short days. Together, these results hint that the interactions between local developmental factors and long-distance environmental signals contribute to the different outcomes of phyB-PIF8 signaling in Populus. The timing of bud flush mainly depends on a prolonged exposure to chilling temperature to release meristems from the dormant state, an adaptation that prevents growth during sporadic warm-temperature periods during winter, and a subsequent cumulative warm-temperature exposure to resume growth. Most genes have only been shown to regulate bud flush or bud set perhaps reflecting differences in the primary signals for these responses. Ding et al. show that similar to their effects on short-day-induced growth cessation, phyB promotes and PIF8 represses bud flush, suggesting that these phenophases differentially exploit the light- and temperature-sensing abilities of phyB. Moreover, transcriptomics suggested that the phyB-PIF8 module regulates bud set and bud flush by targeting some of the same genes. These included transcription factors such as BRANCHED 1 that are also regulated by SHORT VEGETATIVE PHASE-LIKE (SVL), a repressor of bud flush (Singh et al., 2018), suggesting possible integration of SVL- and phyB-PIF-mediated pathways. Ding et al. were also able to link the phyB-PIF8 regulon to the expression of CENL1, a homolog of CENTRORADIALIS (CEN)/TERMINAL FLOWER1; a reduced level of CENL1 accelerates chilling-induced dormancy release (Mohamed et al., 2010). These results highlight the complexity of bud phenology and the difficulty of parsing out gene functions among phases that are often intertwined. The two temperature phases influencing bud flush time are difficult to separate as dormancy is dynamic (Cooke et al., 2012). For example, the depth of dormancy affects the amount of warm temperature units needed to promote bud flush. Additionally, concurrent changes in cell-to-cell communication capacity due to the reopening of plasmodesmata as dormancy is released as well as in daylength likely modify the temperature responses. Albeit challenging, the work of Ding et al. indicates that further dissection of phyB-PIF8 signaling will help reveal the complex interactions among environmental cues, local and long distance signaling and developmental stages. Moving forward there is a need to consider the broader goals of understanding the genetic regulation × development × environment interactions that govern tree phenology and how we can best meet these. Not only does optimal fruit, nut and wood yield depend on phenology being appropriately matched to the environment, but also the health of forests that provide extensive ecosystem services at local to global scales. Shifts in phenology are among the most consistent indicators of climate change and effective management strategies depend on understanding the capacity of forest trees to adapt as well as the extent to which phenotypic plasticity allows persistence (Isabel et al., 2020). This has mostly been addressed by population genomics approaches, and integration with studies of gene function and regulatory mechanisms have been limited. Starting with the ‘model tree’ Populus, the latter can better inform these goals if we: (1) expand our approaches to identifying candidate genes; and (2) evaluate genetically manipulated trees in field trials. Genome wide association studies (GWAS) offer an unbiased approach to identifying genes, and although these have identified genes also selected based on comparative approaches, they have identified more candidates that do not obviously relate to environmental signaling pathways identified in herbaceous plants (e.g. Evans et al., 2014). Integrating GWAS with other methods – the systems biology approach – can hone in on high-confidence candidates (Anderson & Song, 2020). Additionally, advances in techniques and methods have made it more feasible, for example, to determine more extensive protein–protein and protein–DNA interaction networks and to more accurately predict gene regulatory networks from time series transcriptomics. Controlled studies will continue to be important, but field study is needed to fully understand the environmental regulation of phenology and connect this to adaptive variation and plasticity. Recent studies of flowering time in Arabidopsis have mimicked more natural conditions and indicated, for example, that previous laboratory studies employing constant temperatures overestimated the effect of a flowering repressor (Burghardt et al., 2016). In contrast to laboratory studies (Singh et al., 2018), a multi-year field study of Populus overexpressing SVL reported no effect on growth and minimal effects on bud flush (Goralogia et al., 2021), perhaps indicating that in field environments other signaling pathways are activated that can overcome SVL-mediated repression. Though little understood, there is evidence that roles of the secondary signals (Table 1) and the complexity of interactions among signals are significant (Cooke et al., 2012; Brunner et al., 2017). Finally, the precision and efficiency of gene editing has made field studies more feasible and powerful by enabling not only gene-specific and multi-gene knock outs but also reductions (e.g. monoallelic mutation) and increases in expression (Pan et al., 2021). AMB acknowledges support from USDA National Institute of Food and Agriculture, McIntire Stennis project 1025004." @default.
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- W3202673263 date "2021-10-06" @default.
- W3202673263 modified "2023-10-18" @default.
- W3202673263 title "To grow or not to grow: new roles for a conserved regulon in tree phenology" @default.
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