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This study endeavors to explore the transcriptomic profiles of two apple cultivars, namely, 'Honeycrisp' and 'Cripps Pink,' which represent late and early-blooming cultivars, respectively. Using RNA-sequencing technology, we analyzed floral bud samples collected at five distinct time intervals during both endodormancy and ecodormancy. To evaluate the transcriptomic profiles of the 30 sequenced samples, we conducted principal component analysis (PCA). PC1 explained 43% of the variance, separating endodormancy and ecodormancy periods, while PC2 explained 16% of the variance, separating the two cultivars. The number of differentially expressed genes (DEGs) increased with endodormancy progression and remained elevated during ecodormancy. The majority of DEGs were unique to a particular time point, with only a few overlapping among or between the time points. This highlights the temporal specificity of gene expression during the dormancy transition and emphasizes the importance of sampling at multiple time points to capture the complete transcriptomic dynamics of this intricate process. We identified a total of 4204 upregulated and 7817 downregulated DEGs in the comparison of endodormancy and ecodormancy, regardless of cultivar, and 2135 upregulated and 2413 downregulated DEGs in the comparison of 'Honeycrisp' versus 'Cripps Pink,' regardless of dormancy stage. Furthermore, we conducted a co-expression network analysis to gain insight into the coordinated gene expression profiles across different time points, dormancy stages, and cultivars. This analysis revealed the most significant module (ME 14), correlated with 1000 GDH and consisting of 1162 genes. The expression of the genes within this module was lower in 'Honeycrisp' than in 'Cripps Pink.' The top 20 DEGs identified in ME 14 were primarily related to jasmonic acid biosynthesis and signaling, lipid metabolism, oxidation-reduction, and transmembrane transport activity. This suggests a plausible role for these pathways in governing bud dormancy and flowering time in apple.

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In olive trees, fluctuations in the onset of phenological stages have been reported due to weather conditions. The present study analyses the reproductive phenology of 17 olive cultivars grown in Elvas (Portugal) in 3 consecutive years (2012-2014). Through 2017-2022, the phenological observations continued with four cultivars. The phenological observations followed the BBCH scale. Over the course of the observations, the bud burst (stage 51) occurred gradually later; a few cultivars did not follow this trend in 2013. The flower cluster totally expanded phase (stage 55) was achieved gradually earlier, and the period between stages 51-55 was shortened, especially in 2014. Date of bud burst showed a negative correlation with minimum temperature (Tmin) of November-December, and, in 'Arbequina' and 'Cobrançosa', the interval stage 51-55 showed a negative correlation with both the Tmin of February and the Tmax of April, whereas in 'Galega Vulgar' and 'Picual' there was instead a positive correlation with the Tmin of March. These two seemed to be more responsive to early warm weather, whereas 'Arbequina' and 'Cobrançosa' were less sensitive. This investigation revealed that olive cultivars behaved differently under the same environmental conditions and, in some genotypes, the ecodormancy release may be linked to endogenous factors in a stronger way.

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Models used to predict the onset of fruit tree blossom under changed climate conditions should be physiologically based as much as possible. Pure optimized phenology models carry the risk of unrealistic predictions due to a misinterpretation of metabolic processes. This was the motivation determining the relevant phases for chill and heat accumulation, which induces cherry blossom (cv. Summit). Investigations are based on 8 years of observational and analytical data, as well as on controlled experiments. For 'Summit' buds, to be released from endodormancy, 43 chill portions from 1 September are necessary. After endodormancy release (t1), on average on 30 November, no further chilling is required, because no correlation between chill accumulation during ecodormancy and the subsequent heat accumulation until 'Summit' blossom exist. The declining amount of heat, which induces cherry blossom after t1-shown in several forcing experiments-seems to be the result of the declining bud's abscisic acid (ABA) content, up to ~50% until the beginning of ontogenetic development. Shortly after t1, when the bud's ABA content is high, a huge amount of heat is necessary to induce cherry blossom under controlled conditions. Heat requirement reduces during ecodormancy along with the reduction in the ABA content. According to these findings, plant development during ecodormancy is suppressed by low temperatures in the orchard and a slowly declining bud's ABA content. These results should lead to a better consideration of the ecodormancy phase in phenology models.

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[This corrects the article DOI: 10.3389/fpls.2021.803341.].

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Perennial species in the boreal and temperate regions are subject to extreme annual variations in light and temperature. They precisely adapt to seasonal changes by synchronizing cycles of growth and dormancy with external cues. Annual dormancy-growth transitions and flowering involve factors that integrate environmental and endogenous signals. MADS-box transcription factors have been extensively described in the regulation of Arabidopsis flowering. However, their participation in annual dormancy-growth transitions in trees is minimal. In this study, we investigate the function of MADS12, a Populus tremula × alba SUPPRESSOR OF CONSTANS OVEREXPRESSION 1 (SOC1)-related gene. Our gene expression analysis reveals that MADS12 displays lower mRNA levels during the winter than during early spring and mid-spring. Moreover, MADS12 activation depends on the fulfillment of the chilling requirement. Hybrid poplars overexpressing MADS12 show no differences in growth cessation and bud set, while ecodormant plants display an early bud break, indicating that MADS12 overexpression promotes bud growth reactivation. Comparative expression analysis of available bud break-promoting genes reveals that MADS12 overexpression downregulates the GIBBERELLINS 2 OXIDASE 4 (GA2ox4), a gene involved in gibberellin catabolism. Moreover, the mid-winter to mid-spring RNAseq profiling indicates that MADS12 and GA2ox4 show antagonistic expression during bud dormancy release. Our results support MADS12 participation in the reactivation of shoot meristem growth during ecodormancy and link MADS12 activation and GA2ox4 downregulation within the temporal events that lead to poplar bud break.

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Studies addressing endodormancy release in adult trees are usually carried out using twigs detached from the trees in the experiments. Potential problems caused by cutting the root-shoot connection when detaching the twigs can be avoided by using grafts as the experimental material. We studied the effects of chilling on the endodormancy release in Norway spruce (Picea abies (L.) Karst.) grafts where twigs of 16-, 32- and 80-year-old trees were used as the scions. The grafts were first exposed to chilling in natural conditions and then samples of them were transferred at intervals to a regrowth test in forcing conditions in a greenhouse. The bud burst percentage, BB%, in the forcing conditions generally increased from zero to near 100% with increasing previous chilling accumulation from mid-October until mid-November, indicating that endodormancy was released in almost all of the grafts by mid-November. The days to bud burst, DBB, decreased in the forcing conditions with successively later transfers until the next spring. Neither BB% nor DBB was dependent on the age of the scion. However, in the early phase of ecodormancy release, the microscopic internal development of the buds was more advanced in the grafts representing the 16-year-old than in those representing the 32- or 80-year-old trees. In conclusion, our findings suggest that no major change in the environmental regulation of endodormancy release in Norway spruce takes place when the trees get older. Taken together with earlier findings with Norway spruce seedlings, our results suggest that regardless of the seedling or tree age, the chilling requirement of endodormancy release is met in late autumn. The implications of our findings for Norway spruce phenology under climatic warming and the limitations of our novel method of using grafts as a proxy of trees of different ages are discussed.

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Winter dormancy - a period of low metabolic activity and no visible growth - appears as an adaptation to harsh winter conditions and can be divided into different phases. It is tightly controlled by environmental cues, with ambient temperature playing a major role. During endodormancy, a cultivar-specific amount of cold needs to be perceived, and during ecodormancy, heat hours accumulate before bud burst and anthesis in spring. Expression analysis, performed in several key fruit tree species, proved to be very useful in elucidating the molecular control of onset and release of dormancy. However, the time resolution of these experiments has been limited. Therefore, in this study, dense time-series expression analysis was conducted for 40 candidate genes involved in dormancy control, under the cool-temperate climate conditions in Dresden. Samples were taken from the cultivars 'Pinova' and 'Gala,' which differ in flowering time. The set of candidate genes included well-established dormancy genes such as DAM genes, MdFLC-like, MdICE1, MdPRE 1, and MdPIF4. Furthermore, we tested genes from dormancy-associated pathways including the brassinosteroid, gibberellic acid, abscisic acid (ABA), cytokinin response, and respiratory stress pathways. The expression patterns of well-established dormancy genes were confirmed and could be associated with specific dormancy phases. In addition, less well-known transcription factors and genes of the ABA signaling pathway showed associations with dormancy progression. The three ABA signaling genes HAB1_chr15, HAI3, and ABF2 showed a local minimum of gene expression in proximity of the endodormancy to ecodormancy transition. The number of sampling points allowed us to correlate expression values with temperature data, which revealed significant correlations of ambient temperature with the expression of the Malus domestica genes MdICE1, MdPIF4, MdFLC-like, HAB1chr15, and the type-B cytokinin response regulator BRR9. Interestingly, the slope of the linear correlation of temperature with the expression of MdPIF4 differed between cultivars. Whether the strength of inducibility of MdPIF4 expression by low temperature differs between the 'Pinova' and 'Gala' alleles needs to be tested further.

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Bud dormancy of plants has traditionally been explained either by physiological growth arresting conditions in the bud or by unfavourable environmental conditions, such as non-growth-promoting low air temperatures. This conceptual dichotomy has provided the framework also for developing process-based plant phenology models. Here, we propose a novel model that in addition to covering the classical dichotomy as a special case also allows the quantification of an interaction of physiological and environmental factors. According to this plant-environment interaction suggested conceptually decades ago, rather than being unambiguous, the concept of "non-growth-promoting low air temperature" depends on the dormancy status of the plant. We parameterized the model with experimental results of growth onset for seven boreal plant species and found that based on the strength of the interaction, the species can be classified into three dormancy types, only one of which represents the traditional dichotomy. We also tested the model with four species in an independent experiment. Our study suggests that interaction of environmental and physiological factors may be involved in many such phenomena that have until now been considered simply as plant traits without any considerations of effects of the environmental factors.

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BACKGROUND: The reduced growth of plants during the winter causes a lack in the perceptibility of the phenological events making challenging the study of dormancy. For deciduous crops, dormancy is generally determined by evaluating budbreak of single-node cuttings that are exposed to conditions suitable for growth. However, the absence of a statistical basis for analyzing and interpreting the budbreak behavior evaluated as the percent budbreak, the average time to budbreak and the time to reach 50% budbreak, has caused inconsistent and contradictory criteria to identify the dormancy status of different deciduous crops. RESULTS: In this study, a method was developed to analyze the duration between sampling and budbreak of single-node cuttings and to estimate the dormancy status for grapevines (Vitis vinifera L.) based on the time-to-event distribution of the observations. This method estimates the probability curve of budbreak for each sample and classifies each curve into paradormancy, endodormancy, and ecodormancy according to the significance when compared to a sample curve estimated from cuttings collected during paradormancy and referred to as "reference." CONCLUSION: The approach described in this study provided a comparison of the budbreak distribution of cuttings collected during distinct phases with a confidence of 95%. It also allowed the estimation of the date of occurrence of the dormancy stages for two grapevine cultivars 'Cabernet Sauvignon' and 'Chardonnay,' based on the variability within the sampling season rather than on fixed arbitrary criteria. This approach can also be used to analyze budbreak data of single-node cuttings from other common deciduous crops.

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Spring bud-break phenology is a critical adaptive feature common to temperate perennial woody plants. Understanding the molecular underpinnings of variation in bud-break is important for elucidating adaptive evolution and predicting outcomes relating to climate change. Field and controlled growth chamber tests were used to assess population-wide patterns in bud-break from wild-sourced black cottonwood (Populus trichocarpa) genotypes. We conducted a genome-wide association study (GWAS) with single nucleotide polymorphisms (SNPs) derived from whole genome sequencing to test for loci underlying variation in bud-break. Bud-break had a quadratic relationship with latitude, where southern- and northern-most provenances generally broke bud earlier than those from central parts of the species' range. Reduced winter chilling increased population-wide variation in bud-break, whereas greater chilling decreased variation. GWAS uncovered 16 loci associated with bud-break. Phenotypic changes connected with allelic variation were replicated in an independent set of P. trichocarpa trees. Despite phenotypic similarities, genetic profiles between southern- and northern-most genotypes were dissimilar based on our GWAS-identified SNPs. We propose that the GWAS-identified loci underpin the geographical pattern in P. trichocarpa and that variation in bud-break reflects different selection for winter chilling and heat sum accumulation, both of which can be affected by climate warming.

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Timely responses to environmental cues enable the synchronization of phenological life-history transitions essential for the health and survival of north-temperate and boreal tree species. While photoperiodic cues will remain persistent under climate change, temperature cues may vary, contributing to possible asynchrony in signals influencing developmental and physiological transitions essential to forest health. Understanding the relative contribution of photoperiod and temperature as determinants of the transition from active growth to dormancy is important for informing adaptive forest management decisions that consider future climates. Using a combination of photoperiod (long = 20 h or short = 8 h day lengths) and temperature (warm = 22 °C/16 °C and cool = 8 °C/4 °C day/night, respectively) treatments, we used microscopy, physiology and modeling to comprehensively examine hallmark traits of the growth-dormancy transition-including bud formation, growth cessation, cold hardiness and gas exchange-within two provenances of white spruce [Picea glauca (Moench) Voss] spanning a broad latitude in Alberta, Canada. Following exposure to experimental treatments, seedlings were transferred to favorable conditions, and the depth of dormancy was assessed by determining the timing and ability of spruce seedlings to resume growth. Short photoperiods promoted bud development and growth cessation, whereas longer photoperiods extended the growing season through the induction of lammas growth. In contrast, cool temperatures under both photoperiodic conditions delayed bud development. Photoperiod strongly predicted the development of cold hardiness, whereas temperature predicted photosynthetic rates associated with active growth. White spruce was capable of attaining endodormancy, but its release was environmentally determined. Dormancy depth varied substantially across experimental treatments suggesting that environmental cues experienced within one season could affect growth in the following season, which is particularly important for a determinate species such as white spruce. The joint influence of these environmental cues points toward the importance of including local constant photoperiod and shifting temperature cues into predictive models that consider how climate change may affect northern forests.

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Few studies have focused on the characterization of bud dormancy and growth dynamics for temperate fruit species in temperate and mild cropping areas, although this is an appropriate framework to anticipate phenology adaptation facing future warming contexts which would potentially combine chill declines and heat increases. To examine this issue, two experimental approaches and field observations were used for high- and low-chill apple cultivars in temperate climate of southern France and in mild climates of northern Morocco and southern Brazil. Low-chill almond cultivars offered an additional relevant plant material for comparison with apple in northern Morocco. Divergent patterns of dormancy and growth dynamics were clearly found in apple tree between southern France and southern Brazil. Divergences were less pronounced between France and Morocco. A global view outlined main differences in the dormancy chronology and intensity, the transition between endordormancy and ecodormancy and the duration of ecodormancy. A key role of bud rehydration in the transition period was shown. High-chill cultivars would be submitted in mild conditions to heterogeneous rehydration capacities linked to insufficient chill fulfillment and excessive forcing linked to high temperatures. This would favor bud competitions and consequently excessive flowering durations and weak flowering. Low chilling requirements in apple and almond would conversely confer biological capacities to tolerate superficial dormancy and abrupt transition from endordormancy to ecodormancy without important heterogeneous rehydration states within buds. It may also assume that low-chill cultivars can also tolerate high temperatures during ecodormancy as well as extended flowering durations.

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BACKGROUND AND AIMS: Plants regulate cellular oxygen partial pressures (pO2), together with reduction/oxidation (redox) state in order to manage rapid developmental transitions such as bud burst after a period of quiescence. However, our understanding of pO2 regulation in complex meristematic organs such as buds is incomplete and, in particular, lacks spatial resolution. METHODS: The gradients in pO2 from the outer scales to the primary meristem complex were measured in grapevine (Vitis vinifera) buds, together with respiratory CO2 production rates and the accumulation of superoxide and hydrogen peroxide, from ecodormancy through the first 72 h preceding bud burst, triggered by the transition from low to ambient temperatures. KEY RESULTS: Steep internal pO2 gradients were measured in dormant buds with values as low as 2·5 kPa found in the core of the bud prior to bud burst. Respiratory CO2 production rates increased soon after the transition from low to ambient temperatures and the bud tissues gradually became oxygenated in a patterned process. Within 3 h of the transition to ambient temperatures, superoxide accumulation was observed in the cambial meristem, co-localizing with lignified cellulose associated with pro-vascular tissues. Thereafter, superoxide accumulated in other areas subtending the apical meristem complex, in the absence of significant hydrogen peroxide accumulation, except in the cambial meristem. By 72 h, the internal pO2 gradient showed a biphasic profile, where the minimum pO2 was external to the core of the bud complex. CONCLUSIONS: Spatial and temporal control of the tissue oxygen environment occurs within quiescent buds, and the transition from quiescence to bud burst is accompanied by a regulated relaxation of the hypoxic state and accumulation of reactive oxygen species within the developing cambium and vascular tissues of the heterotrophic grapevine buds.

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To survive winter, many perennial plants become endodormant, a state of suspended growth maintained even in favorable growing environments. To understand vegetative bud endodormancy, we collected paradormant, endodormant, and ecodormant axillary buds from Populus trees growing under natural conditions. Of 44,441 Populus gene models analyzed using NimbleGen microarrays, we found that 1,362 (3.1%) were differentially expressed among the three dormancy states, and 429 (1.0%) were differentially expressed during only one of the two dormancy transitions (FDR p-value < 0.05). Of all differentially expressed genes, 69% were down-regulated from paradormancy to endodormancy, which was expected given the lower metabolic activity associated with endodormancy. Dormancy transitions were accompanied by changes in genes associated with DNA methylation (via RNA-directed DNA methylation) and histone modifications (via Polycomb Repressive Complex 2), confirming and extending knowledge of chromatin modifications as major features of dormancy transitions. Among the chromatin-associated genes, two genes similar to SPT (SUPPRESSOR OF TY) were strongly up-regulated during endodormancy. Transcription factor genes and gene sets that were atypically up-regulated during endodormancy include a gene that seems to encode a trihelix transcription factor and genes associated with proteins involved in responses to ethylene, cold, and other abiotic stresses. These latter transcription factors include ETHYLENE INSENSITIVE 3 (EIN3), ETHYLENE-RESPONSIVE ELEMENT BINDING PROTEIN (EBP), ETHYLENE RESPONSE FACTOR (ERF), ZINC FINGER PROTEIN 10 (ZAT10), ZAT12, and WRKY DNA-binding domain proteins. Analyses of phytohormone-associated genes suggest important changes in responses to ethylene, auxin, and brassinosteroids occur during endodormancy. We found weaker evidence for changes in genes associated with salicylic acid and jasmonic acid, and little evidence for important changes in genes associated with gibberellins, abscisic acid, and cytokinin. We identified 315 upstream sequence motifs associated with eight patterns of gene expression, including novel motifs and motifs associated with the circadian clock and responses to photoperiod, cold, dehydration, and ABA. Analogies between flowering and endodormancy suggest important roles for genes similar to SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL), DORMANCY ASSOCIATED MADS-BOX (DAM), and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1).

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The transcriptomes of endodormant and ecodormant Japanese pear (Pyrus pyrifolia Nakai 'Kosui') flower buds were analyzed using RNA-seq technology and compared. Among de novo assembly of 114,191 unigenes, 76,995 unigenes were successfully annotated by BLAST searches against various databases. Gene Ontology (GO) enrichment analysis revealed that oxidoreductases were enriched in the molecular function category, a result consistent with previous observations of notable changes in hydrogen peroxide concentration during endodormancy release. In the GO categories related to biological process, the abundance of DNA methylation-related gene transcripts also significantly changed during endodormancy release, indicating the involvement of epigenetic regulation. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis also showed the changes in transcript abundance of genes involved in the metabolism of various phytohormones. Genes for both ABA and gibberellin biosynthesis were down-regulated, whereas the genes encoding their degradation enzymes were up-regulated during endodormancy release. In the ethylene pathway, 1-aminocyclopropane-1-carboxylate synthase (ACS), a gene encoding the rate-limiting enzyme for ethylene biosynthesis, was induced towards endodormancy release. All of these results indicated the involvement of phytohormones in endodormancy release. Furthermore, the expression of dormancy-associated MADS-box (DAM) genes was down-regulated concomitant with endodormancy release, although changes in the abundance of these gene transcripts were not as significant as those identified by transcriptome analysis. Consequently, characterization of the Japanese pear transcriptome during the transition from endormancy to ecodormancy will provide researchers with useful information for data mining and will facilitate further experiments on endodormancy especially in rosaceae fruit trees.

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