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Bud dormancy is an essential characteristic of deciduous woody perennials, including apple, to cope with the low temperatures during winter. The release from dormancy and subsequent budburst in apple can only occur after fulfillment of chilling and heat requirements. In the Mid-Atlantic region, dormancy release and bud break of apple often coincide with late-spring freezes that cause severe damages to flowers, and small fruitlets. Therefore, the present study aimed to better understand mechanisms underlying bud dormancy in apple, with an ultimate goal of exploring chemical and/or genetic approaches for bloom-time modulation to avoid spring frost. Using two apple cultivars, 'Cripps Pink' and 'Honeycrisp,' representing early- and late-blooming cultivars, respectively, the present study specifically investigated the accumulation kinetics of plant hormones, carbohydrates, and reactive oxygen species (ROS) throughout the dormancy-regrowth cycle. Our results indicated that both cultivars required 1000 chilling hours for endodormancy release, but 'Honeycrisp' required 1000 growing degree hours (GDHs) more than 'Cripps Pink' for ecodormancy release and budburst. Among plant hormones, abscisic acid (ABA) showed remarkably elevated levels in the dormant buds of both cultivars during endodormancy, but its levels were significantly higher in 'Honeycrisp'. The decline of the ABA level at bud burst was combined with increased levels of cytokinin (CK). The ABA accumulation pattern during dormancy paralleled with an upregulation and downregulation of ABA biosynthetic and catabolic genes, respectively. On the other hand, the levels of hydrogen peroxide (H2O2) and superoxide (O2.-) were significantly higher in 'Cripps Pink' than 'Honeycrisp', particularly by the time of endodormancy and ecodormancy release, respectively. Our findings also showed a gradual decline in starch levels with the dormancy progression and increased levels of total soluble sugars (TSS) that were generally higher in the early-blooming cultivars. Transcriptomic profiling and module-trait relationship identified two modules that contrast between two cultivars mainly during eco-dormancy. Gene ontology (GO) analysis indicated that these DEGs were mostly involved in pathways related to hormones and signaling and co-expressed with H2O2 whereas, during ecodormancy pathways related to glutathione metabolism, auxin biosynthesis, carbohydrate metabolism and reproductive development were co-expressed with O2.-. Together, our results suggest that the contrasting bloom dates between 'Cripps Pink' and 'Honeycrisp' can be explained, at least partially, by the differential accumulation levels of ABA, ROS, antioxidants, and their associated genes in the buds of these cultivars throughout the dormancy cycle. Doctor of Philosophy Spring frosts represent a significant threat to apple production in many fruit-producing states of the United States including Virginia. The risk of frost damage is rising due to global climate change, and there is a high demand for effective measures to reduce frost damage. Exogenous applications of plant growth regulators (PGRs) to delay bloom has been suggested as an effective frost avoidance strategy, but with limited success. Therefore, the present study aimed to investigate molecular and biochemical pathways regulating bud dormancy and bloom time in apple, which can ultimate lead to novel approaches for bloom delay and frost mitigation. To this end, the accumulation patterns of major plant hormones (e.g. abscisic acid, ABA, cytokinin, CK and jasmonic acid, JA), reactive oxygen species (ROS) and carbohydrates (e.g. starch, sucrose, glucose and fructose) were thoroughly monitored throughout the dormancy-regrowth cycle in two apple cultivars, 'Cripps Pink' and 'Honeycrisp,' representing early- and late-blooming cultivars, respectively. Both these cultivars had similar chilling requirements (1000 chilling hours) but differed in their heat requirements; with 'Honeycrisp' requiring 1000 growing degree hours more than 'Cripps Pink'. Among plant hormones, ABA increased with the progression of dormancy and decreased with dormancy release in both cultivars. However, ABA levels were significantly higher in 'Honeycrisp' compared to 'Cripps Pink'. On the contrary, during dormancy release, the growth-promoting hormone, CK, increased earlier in 'Cripps Pink'. The levels of ROS, e.g., hydrogen peroxide (H2O2), and superoxide (O2.-), were also higher in 'Cripps Pink' than 'Honeycrisp', particularly by the time of endodormancy and ecodormancy release, respectively. Our data showed that starch levels generally declined during dormancy, whereas soluble sugars increased. However, there was no significant alternations in the carbohydrate accumulation profiles between the two cultivars that could account for the differences in their bloom dates. These results were verified further at the transcriptomic level. Using the RNA-sequencing technology, identified two modules that contrast between two cultivars mainly during eco-dormancy. Gene ontology (GO) analysis indicated that these genes were mostly involved in pathways related to hormones and signaling and co-expressed with H2O2 whereas during ecodormancy pathways related to glutathione metabolism, auxin biosynthesis, carbohydrate metabolism and reproductive development were co-expressed with O2.-. Overall, our results suggest that ABA, cytokinin, H2O2, and O2.- may, at least partially, explain the differences in the bloom time between the two apple cultivars. Further analysis of these molecules and their associated genes in other apple cultivars with contrasting bloom dates is necessary for better understanding of bloom time regulation in apple and developing strategies against frost damage.

Understanding the biochemical mechanisms underlying bud dormancy and bloom time regulation in deciduous woody perennials is critical for devising effective strategies to protect these species from spring frost damage. This study investigated the accumulation profiles of carbohydrates, ROS and antioxidants during dormancy in ‘Cripps Pink’ and ‘Honeycrisp’, two apple cultivars representing the early and late bloom cultivars, respectively. Our data showed that starch levels generally declined during dormancy, whereas soluble sugars increased. However, the present study did not record significant alternations in the carbohydrate accumulation profiles between the two cultivars that could account for the differences in their bloom dates. On the other hand, H2O2 accumulation patterns revealed an apparent correlation with the dormancy stage and bloom dates in both cultivars; peaking early in the early-blooming cultivar, sustaining high levels for a longer time in the late-blooming cultivars, and fading by the time of bud burst in both cultivars. Also, the redox balance during dormancy appeared to be maintained mainly by catalase and, to a lesser extent, by glutathione (GSH). Overall, the present study concludes that differences in ROS and the bud redox balance could, at least partially, explain the differences in dormancy duration and bloom date among apple cultivars. Published version

Spring frosts exacerbated by global climate change have become a constant threat to temperate fruit production. Delaying the bloom date by plant growth regulators (PGRs) has been proposed as a practical frost avoidance strategy. Ethephon is an ethylene-releasing PGR found to delay bloom in several fruit species, yet its use is often coupled with harmful effects, limiting its applicability in commercial tree fruit production. Little information is available regarding the mechanisms by which ethephon influences blooming and bud dormancy. This study investigated the effects of fall-applied ethephon on bud phenology, cold hardiness, and hormonal balance throughout the bud dormancy cycle in peach. Our findings concluded that ethephon could alter several significant aspects of peach bud physiology, including accelerated leaf fall, extended chilling accumulation period, increased heat requirements, improved cold hardiness, and delayed bloom date. Ethephon effects on these traits were primarily dependent on its concentration and application timing, with a high concentration (500 ppm) and an early application timing (10% leaf fall) being the most effective. Endogenous ethylene levels were induced significantly in the buds when ethephon was applied at 10% versus 90% leaf fall, indicating that leaves are essential for ethephon uptake. The hormonal analysis of buds at regular intervals of chilling hours (CH) and growing degree hours (GDH) also indicated that ethephon might exert its effects through an abscisic acid (ABA)-independent way in dormant buds. Instead, our data signifies the role of jasmonic acid (JA) in mediating budburst and bloom in peach, which also appears to be influenced by ethephon treatment. Overall, this research presents a new perspective in interpreting horticultural traits in the light of biochemical and molecular data and sheds light on the potential role of JA in bud dormancy, which deserves further attention in future studies that aim at mitigating spring frosts. Published version