Next Article in Journal
A Molecular Identification and Resistance Evaluation of the Blast Resistance Genes in Japonica Rice in Northern China
Next Article in Special Issue
Exogenous Silicon Application Improves Chilling Injury Tolerance and Photosynthetic Performance of Citrus
Previous Article in Journal
Co-Inoculation with Bradyrhizobium and Humic Substances Combined with Herbaspirillum seropedicae Promotes Soybean Vegetative Growth and Nodulation
Previous Article in Special Issue
The Flowering of Black Locust (Robinia pseudoacacia L.) in Italy: A Phenology Modeling Approach
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 13
Issue 10
10.3390/agronomy13102659
agronomy-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Breaking Buds—Stop and Go? Acid Invertase Activities in Apple Leaf Buds during Dormancy Release until Bud Break

by
Anna M. Hubmann
*,†,
Alexandra Roth
† and
Stephan Monschein
Institute of Biology, Plant Sciences, University of Graz, Schubertstraße 51, 8010 Graz, Austria
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(10), 2659; https://doi.org/10.3390/agronomy13102659
Submission received: 14 August 2023 / Revised: 2 October 2023 / Accepted: 13 October 2023 / Published: 23 October 2023
(This article belongs to the Special Issue Physiological Performance of Tree and Fruit Crops under Abiotic Stresses)
Browse Figure
Review Reports Versions Notes

Abstract

:
Bud dormancy enables deciduous fruit trees to endure unfavorable conditions during winter, and considerably impacts growth and reproduction in spring. We investigated acid invertase activities during dormancy release until bud break under natural (orchard) conditions in two consecutive years. Our aim was to relate the activity patterns to the developmental progression and to air temperature, which is a major factor influencing the developmental processes at that stage. The enzyme assays were performed on extracts from leaf buds of the cultivar Idared, sampled from early March to April in the years 2020 and 2021. The air temperature was continually monitored during the observation periods. cwINV activity showed a trend of slight increase at the earlier developmental stages and sharply increased during bud break in both years. cwINV is known to contribute to organ sink strength. Its up-regulation may, therefore, be related to the increasing developmental demand for carbohydrates in apple leaf buds during dormancy release until bud break. vacINV activity was relatively constant at the earlier stages and also showed a pronounced increase in activity during bud break in both years. However, in both years, we observed drops in vacINV activity following cold spells. vacINV activity has been associated with growth via cell elongation through the regulation of cell turgor and may, thus, be involved in bud break. Therefore, we suggest that the down-regulation of vacINV activity as a consequence of cold spells might contribute to a delay in bud break to protect young leaf tissues from exposure to cold stress conditions.

1. Introduction

Woody perennials of the temperate and boreal regions endure unfavorable conditions by reducing their metabolic activity to a minimum, resulting in growth resting phases during the plant life cycle. These resting phases are commonly called dormancy, which is defined as the absence of visible growth in any plant structure containing a meristem [1,2]. Bud dormancy is an adaptive developmental process, which can be triggered by both endogenous and exogenous factors [3]. Based on the main cause for the developmental delay (endogenous or exogenous factors), bud dormancy can be classified into three distinct phases, according to Lang et al. [2]: paradormancy, endodormancy, and ecodormancy. During paradormancy, growth cessation is controlled by internal signals, beyond the bud structure, whereas during endodormancy the internal conditions of the dormant structure itself prevent the buds from leafing out, even under favorable conditions [2]. During ecodormancy, external factors (unfavorable environmental conditions) prevent active growth [4], until buds enter the stage of dormancy release [5,6]. The major environmental factor regulating the onset, progression, and release of bud dormancy in apple trees is the ambient temperature [7]. While buds show high resistance to freezing temperatures during endodormancy [8,9,10,11], they become increasingly sensitive to cold and especially freezing temperatures as they progress from endo- to ecodormancy and, eventually, to dormancy release [12,13,14]. The transition phases from dormancy release to the beginning of ontogenetic development [15,16] and bud break represent particularly sensitive phases in the phenological cycle of plants since young tissues are exposed to the environment without any protection. Consequently, the growth cycle of perennials—i.e., the phases of active growth and dormancy—must be synchronized with the seasonal changes in environmental conditions to minimize the risk of frost damage on the one hand and to maximize the duration of the growth period on the other [17,18]. Therefore, climate change adds another facet to the complexity of dormancy (release): The increase in average surface temperatures causes an acceleration in plant phenology progression [19,20]. Evidence shows that climate change exacerbates weather extremes and local extremes in temperature, especially in spring, which leads to the earlier exposure of the bud tissues of perennial plants to fluctuating conditions [3,21].
Among the perennials, the apple (Malus × domestica Borkh.) is one of the most important fruit crops worldwide and is cultivated on all continents, except for Antarctica [22,23]. As a consequence of climate change, apple blossom has advanced worldwide due to warmer temperatures [20]. Consequently, the investigation of apple bud dormancy and its release is a matter of global interest for two reasons: firstly, to gain a basic understanding of dormancy, and secondly, to develop purposeful protective measures in agriculture and horticulture, particularly concerning the unpredictable impacts of climate change on plant cold stress and freezing damage.
Investigations in the field of dormancy research, especially in recent years, have contributed to the current understanding of the mechanisms underlying early phenological stages [24]. A key role in dormancy control—including dormancy release—has been attributed to the carbohydrate metabolism [3,25,26,27,28,29]. This is because the transition from dormancy to growth resumption and subsequent bud break is an energy-intensive process depending on the accumulated carbohydrates within the buds, as well as on the ability of buds to import energy-rich substances from neighboring tissues [30,31,32,33]. With the onset of dormancy release, the bud sink strength increases [31,34,35], elevating the ability of the buds to attract exogenous carbohydrates [25,33,34,35,36]. Thus, the buds import increasing amounts of sugars from source tissues, which are immediately metabolized to enhance plant growth and development [37].
Within the central carbohydrate metabolism of plants, sucrose is cleaved by two enzymes, namely sucrose synthase (SuSy, EC 2.4.1.13) and invertases (INVs, EC 3.2.1.26). SuSy acts as a glycosyltransferase and reversibly cleaves sucrose in the presence of UDP into UDP-glucose and fructose [38,39,40]. INVs, on the other hand, irreversibly hydrolyze sucrose into glucose and fructose [41,42]. The invertase enzymes are classified into three different isoforms based on their biochemical properties and cellular localization [43]: The neutral or alkaline invertase is localized in the cytoplasm (cytoplasmatic invertase). It typically shows low activity compared to the other INV isoenzymes. The acid invertases have a pH optimum between 4.5 and 5.5 and are either localized in the vacuole as soluble forms (vacuolar invertase; vacINV) or ionically bound to the cell wall (cell-wall-bound invertase, cwINV) [41,43,44,45]. Like various other plant physiological processes, the expression and activity of INVs have been shown to follow a diurnal rhythm [46,47].
Invertases do not only play a major role in primary carbohydrate metabolism, but also appear to have a broad range of regulatory functions during plant development and growth [40,44,45,48,49], including sugar distribution, source–sink relationships, sugar signaling, and stress responses [41,43,50,51]. Within their regulatory functions, cwINV is involved in the partitioning of carbohydrates [38], the modulation of sugar allocation and signaling [52], and the maintenance of the sucrose concentration gradient between source and sink tissues. cwINV activity is, thus, considered to be decisive for the sink strength of a tissue [30,53] and for plant biomass formation [41,43]. vacINV is commonly known for its major roles in sugar accumulation, for fueling the cytoplasmatic hexose pool [54,55,56,57,58], and for promoting cell expansion via osmotic regulation [38,41,43,54,55,56,57,58]. During leaf development, vacINV represents the major sucrose-cleaving enzyme, providing high amounts of reducing sugars that can be used for cell wall biosynthesis and for fueling energy-consuming processes [57,58]. Furthermore, vacINV is involved in leaf development by driving the accumulation of hexoses in the vacuole, which results in the attraction of water and leads to an increase in cell turgor required for leaf expansion [41,58]. vacINV becomes increasingly important with the onset of ontogenetic development by regulating cell turgor in the developing leaf buds, which acts as a major driving force for cell growth and promotes bud break [31,59].
As ontogenetic development occurs in spring when air temperatures strongly fluctuate, the vulnerable young leaf tissues are at constant risk of exposure to cold stress. Cold stress is known to modify source–sink relationships, and thus severely affects plant development and biomass formation [37,51,60,61]. Cold stress responses have also been reported in many studies to alter the activities or transcription levels of acid INVs in different plants [51,60,61,62,63,64]—very recently also in apple leaves [37]. This indicates that acid INVs are also involved in plant responses to cold stress.
As summarized above, the findings from previous results suggest that the acid invertases are involved during dormancy release and growth resumption in spring. We, thus, aimed to investigate the developmental progression of cwINV and vacINV activities in apple leaf buds during dormancy release until bud break. For this purpose, we performed invertase activity assays on extracts obtained from the leaf buds of the cultivar Idared, sampled from early March to April in the years 2020 and 2021. As air temperature is a major factor influencing dormancy release, it was also closely monitored and taken into consideration when interpreting the data.

2. Materials and Methods

2.1. Plant Material

For the investigation of the acid invertase activities during dormancy release until bud break, leaf buds were sampled from fifty 14-year-old apple espalier trees of the cultivar Idared grafted on Malling 9 rootstocks (Malus × domestica Borkh.) over two consecutive years (2020 and 2021), from early March to April. The trees were located in a plantation of an experimental station for pomiculture and viticulture, “Versuchstation für Obst- und Weinbau”, in Haidegg, Graz (coordinates 47.07987, 15.50271). Per sampling date, fifteen buds were collected per tree and the sampled buds of ten trees were combined into mixed samples. Thus, five mixed samples per sampling date were generated, each comprising the buds from ten apple trees. The sampling took place from 06 March 2020 (DOY [day of the year] 66) to 10 April 2020 (DOY 101) on DOY 66, DOY 73, DOY 80, DOY 87, DOY 94, and DOY 101, and from 04 March 2021 (DOY 64) to 02 April 2021 (DOY 92) on DOY 64, DOY 71, DOY 78, DOY 85, and DOY 92. As the activities of the acid invertases show a diurnal rhythm [46,47], the leaf buds were always sampled at the same time of day (i.e., midday). The respective ends of the sampling periods in both years were determined by the phenological stage of bud break of the apple leaf buds. Sampled buds were immediately frozen in liquid nitrogen, followed by freeze-drying for at least 48 h. The samples were ground with a vibrating tube mill (Retsch© MM 400, Haan, Germany) at maximum vibration frequency for 3 min. Until further use, the freeze-dried and ground plant material was stored at −80 °C.

2.2. Determination of the Adjusted Dry Weight [aDW]

The determination of the adjusted dry weight [aDW] was carried out according to Hubmann et al. [65]. Briefly, fifty leaf buds were collected on each sampling date and, subsequently, the sampled buds were divided into five mixed samples, each comprising ten buds. Before freeze-drying, the bud scales were separated from the remaining tissues. After freeze-drying, the dry weight (DW) of the scales and remaining tissues of each mixed sample was recorded, and the percentage of scales and remaining physiologically active tissues was calculated for each sampling date. To express the enzyme activity on an adjusted DW (aDW) basis, the percentage of physiologically active tissues (on each sampling date) was calculated from the respective initial dry weight of the buds.

2.3. Extraction Procedure for Intracellular and Cell Wall-Bound Proteins

Protein extraction was performed according to protocols slightly modified from Jammer et al. [66] and Fimognari et al. [67]. A detailed description of the extraction procedure for intracellular and cell-wall-bound proteins in apple buds can be found in our previous study [65]. Until further use, all extracts were stored in aliquots at −20 °C.

2.4. Acid Invertase Activity Assay

cwINV and vacINV activities were assayed according to Jammer et al. [66]. All measurements were performed in triplicate in flat-bottom 96-well plates (Sarstedt, Nümbrecht, Germany) in a microplate photometer (SpectraMax® ABS Plus, Molecular Devices, San Jose, CA, USA). Enzymatic activities were expressed in nkat on an adjusted dry weight (aDW) basis as described above [65].

2.5. Air Temperature

Air temperature [°C] was continually recorded from DOY 59 until DOY 101 in 2020 and from DOY 57 until DOY 92 in 2021. The data logger was positioned in the center of the espalier tree row, and the air temperature was recorded at one-hour intervals. Out of a final data set, the mean air temperatures during the day (daily means; data points between sunrise and sunset) and night (nightly means; data points between sunset and sunrise) were calculated, resulting in two values per 24 h (per DOY). Astronomical information for day and night lengths in the years 2020 and 2021 was obtained from the Federal Institute for Geology, Geophysics, Climatology, and Meteorology of Austria [68,69]. Additionally, the average temperature was calculated for each of the one-week intervals before the individual sampling date. These intervals were labeled as I1–I6 for 2020 and as I1–I5 for 2021 (see Figure 1).

3. Results

3.1. Phenological Growth Stages of Apple Leaf Buds

The developmental stages of the leaf buds were documented at the beginning and the end of the observation period of the respective year. Subsequently, illustrations of the respective phenological stages were generated (see Figure 1).
At the beginning of the sampling period in the year 2020 (DOY 66) and in the year 2021 (DOY 64), leaf buds could be categorized as BBCH 00 (Figure 1). This means the buds were tightly closed and covered by dark brown bud scales [70]. At the end of the observation period in the year 2020 (DOY 101) and in the year 2021 (DOY 92), leaf buds could be categorized as a late stage of BBCH 07 (Figure 1), which is the beginning of bud break, when the first green leaf tips are just visible [70].

3.2. Air Temperature

3.2.1. Air Temperature during the Observation Period in 2020

At the beginning of the recording in 2020, the average temperature was 5.5 °C in interval I1 (before the first sampling date) and remained at a similar level in I2 and I3. In I4, the average temperature was lower than in the previous intervals due to low daily and nightly means throughout the interval. The average temperature in I5 was similar to the previous interval; however, there was a pronounced heterogeneity in the dynamics of the daily and nightly means during I5. The first half of this interval was characterized by relatively warm temperatures, but a sudden drop in temperature led to much colder conditions during the second half of I5. The daily and nightly means constantly increased again during I6, resulting in an average temperature of 9.3 °C for this interval (see Figure 1).

3.2.2. Air Temperature during the Observation Period in 2021

At the beginning of the recording in 2021, the average temperature was 5.5 °C in interval I1 and 2.2 °C in I2. Both intervals were characterized by moderate fluctuations in the daily and nightly means. Similar to I5 in 2020, the dynamics of the daily and nightly temperature means in I3 were more heterogeneous: The daily and nightly means continuously decreased throughout the second half of the interval and were much lower at the end of the interval. This trend continued into I4, culminating in a particularly cold night at the beginning of that interval. From the second half of I4, the temperatures increased until the end of the observation period, resulting in an average temperature of 11.8 °C in the last interval I5 (see Figure 1).

3.3. Acid Invertase Activities in Apple Leaf Buds

3.3.1. Acid Invertase Activities during the Observation Period in 2020

cwINV activity in the apple leaf buds was relatively low at 0.13 nkat/g aDW at the beginning of the observation period (DOY 66) in the year 2020. The curve progression of cwINV activity showed a trend of slight increase until DOY 94. From DOY 94 (0.35 nkat/g aDW) to the last sampling date (DOY 101), cwINV activity sharply increased to approximately 0.9 nkat/g aDW, corresponding to a 157% increase in activity.
vacINV activity in the apple leaf buds was slightly below 0.6 nkat/g aDW at the beginning of the observation period (DOY 66) in the year 2020. Until DOY 87, the curve progression of vacINV activity was relatively constant. Then, from DOY 87 to DOY 94, the activity of vacINV sharply decreased from 0.59 nkat/g aDW to approximately 0.2 nkat/g aDW, which corresponds to a 66% decrease in activity. From DOY 94 to the last sampling date (DOY 101), vacINV activity sharply increased to approximately 1.5 nkat/g aDW, which corresponds to a 650% increase in activity.

3.3.2. Acid Invertase Activities during the Observation Period in 2021

cwINV activity in the apple leaf buds was relatively low at 0.22 nkat/g aDW at the beginning of the observation period (DOY 64) in the year 2021. The curve progression of cwINV activity showed a trend of slight increase until DOY 85. From DOY 85 (0.45 nkat/g aDW) to the last sampling date (DOY 92), cwINV activity sharply increased to approximately 1.5 nkat/g aDW, which corresponds to a 230% increase in activity.
vacINV activity in the apple leaf buds was slightly above 1 nkat/g aDW at the beginning of the observation period (DOY 64) in the year 2021. Until DOY 71, the curve progression of vacINV activity was relatively constant. From DOY 71 (0.85 nkat/g aDW) to DOY 78, vacINV activity decreased to 0.33 nkat/g aDW, corresponding to a 61% decrease in activity. From DOY 85 (0.45 nkat/g aDW) to the last sampling date (DOY 92), vacINV activity sharply increased to approximately 2.3 nkat/g aDW, corresponding to a 411% increase in activity.

4. Discussion

Bud dormancy enables deciduous fruit trees to endure unfavorable conditions during the winter months. When dormancy is released and the buds begin to sprout early in spring, young tissues are exposed to highly fluctuating weather conditions and have an increased risk of frost damage [17,71]. Thus, the annual cycle of dormancy and active growth also critically affects growth and reproduction in spring, as well as fruit growth regulation and fruit quality in many perennial fruit crops such as apple trees [72,73]. Consequently, bud dormancy release is not only of interest from a scientific point of view but has also gained importance for agricultural and horticultural production, particularly in times of climate change.
The endogenous factors influencing and/or controlling dormancy release are interconnected with environmental cues, forming a highly complex regulatory network [25,74,75,76,77,78]. Thus, when investigating developmental changes in biochemical parameters in the field of dormancy research, it is of particular importance to also consider the environmental conditions that occur during the period of observation. This is especially the case for investigations under natural (orchard) conditions. One of the most important environmental factors influencing various phases of apple bud dormancy is air temperature [7,78,79,80,81,82]. Dormancy release occurs in spring when short-term weather changes are common, resulting in high fluctuations in air temperatures. Warm temperatures promote bud break and growth resumption, whereas cold and freezing temperatures may constrain growth, thus prolonging bud outgrowth and/or leading to frost damage [8,20,82,83]. In our present study, two temperature change events appear to be of particular interest: the temperature drops in I5 in 2020 and in I3 in 2021, both resulting in much colder conditions during the second halves of these intervals (see Figure 1).
The timing of the phenological development in spring is strongly dependent on temperature. In our study, the apple leaf buds entered the phenological stage of bud break (BBCH 07) [70] nine days earlier in 2021 than in 2020. This deviation in the timing of bud break in the two consecutive years is likely related to the points in time when cold spells occurred: In 2020, the last major cold spell occurred in week five of the observation period (second half of I5). The temperatures increased in interval I6, and bud break occurred six weeks after the beginning of the observations. In 2021, there was a temperature drop in weeks three and four of the observation period (second half of I3 and beginning of I4). From then onwards, the temperatures increased strongly, and bud break occurred within five weeks—one week earlier than in 2020. This data underpins the importance of (a) analyzing data from more than just one dormancy cycle and (b) closely monitoring environmental parameters when investigating physiological parameters during dormancy release under natural (orchard) conditions.
When analyzing the activity data for cwINV and vacINV in apple leaf buds during dormancy release until bud break, both enzymes showed characteristic activity patterns throughout the periods of observation. However, distinct differences could be observed in the behaviors of cwINV and vacINV. cwINV activity was initially low, then showed a trend of slight increase, and, finally, a strong increase at the last sampling date (see Figure 1). vacINV was constant at the early stages, followed by a transient decrease in activity, and finally, a strong increase in activity at the last sampling date. For both enzymes, the observed increases in activity at the last sampling date coincided with the event of bud break. The transient decrease in vacINV occurred earlier in 2021 than in 2020 (see Figure 1).
Both cwINV and vacINV have been shown to follow distinct patterns of developmental regulation in various plant organs, particularly in sink organs [84,85,86]. Leaf buds—as soon as the ontogenetic development begins in spring—are sink organs dependent on the import of sugars once they have depleted their carbohydrate reserves [32,33,87,88,89,90,91]. The heterotrophic growth processes occurring in the buds require (a) a constant supply of carbohydrates that provide energy and carbon skeletons for biomass production, and (b) an increase in cell turgor for cell expansion and leaf outgrowth [26,31,57,58,89,92]. It has been stated that buds are unable to attract osmotic and energetic molecules as long as they are dormant, as the carbohydrate absorption potential of dormant peach leaf buds was low while the endogenous concentration of sucrose was high [33]. During dormancy release, however, the buds generated sink strength via active sugar transport, and thus were able to import carbohydrates for subsequent use in growth metabolism and bud break induction [33]. It has therefore been assumed that bud sink strength increases with the onset of dormancy release and the beginning of ontogenetic development [31,34,35]. cwINV activity is generally associated with organ sink strength [41,53,93,94]. Previous studies have also linked cwINV activity to sink strength generation in the context of bud development and to a commitment to bud break: firstly, increasing cwINV activities were observed in the context of bud break in the buds of different plant species [89,95]. Secondly, it has been proposed that cwINV activity potentially contributes to sink strength generation in buds by mediating sugar transport in the apoplast [89,95]. Thirdly, an increase in the levels of cwINV-encoding transcripts was observed in grapevine leaf buds as the temperatures grew warmer and the buds resumed growth [3]. Therefore, we assume that the increase in cwINV activity we observed in the apple leaf buds was correlated with the induction of sink strength taking place during dormancy release and the onset of ontogenetic development, thus promoting bud break.
While cwINV is probably involved in sink strength generation, vacINV is supposed to play another role in developing buds. High vacINV activities have repeatedly been associated with cell expansion [96] through increasing cell turgor [97,98,99,100]. As extensive growth via cell expansion is required to achieve bud break, it is not surprising that vacINV has been attributed a role in the process. Several studies have shown increases in vacINV activities before/at the stage of bud break in different plant species [31,36,59,92,101]. Girault et al. [31] suggested that the regulation of cell turgor via vacINV represents a main mechanism for promoting bud break. Our observations of high vacINV activities at the stage of bud break are consistent with the data obtained in previous studies. Thus, we take up the proposal of Girault et al. [31] and assume that the increase in vacINV activity at our last sampling date is related to the necessity of a turgor increase to induce growth via cell expansion, which, in turn, is required for the induction of bud break.
What is striking in the context of the developmental regulation of enzyme activities is that these patterns are generally very stable regardless of the environmental conditions [84,86]. This is also reflected by the patterns of developmental regulation observed for the acid invertases in our study and in the literature cited above. While there are plausible explanations for the increases in cwINV and vacINV activities around the stage of bud break (see above), the transient decreases we observed in vacINV activity in both years are more challenging to interpret from a developmental point of view. However, there is one aspect that stands out when looking at the curve progressions of vacINV and air temperature in parallel (see Figure 1): In both years, the samples showing the lowest vacINV activities were collected on days immediately preceded by cold spells (second half of I5 in 2020 and second half of I3 in 2021). This suggests that the low vacINV activities detected in these samples may be related to the impact of the low temperatures directly before the sampling events. Exposure to low-temperature stress is not unusual for woody perennials, and they are well-equipped with adaptive mechanisms to cope with cold during the winter months [3]. When dormancy is released and growth resumes, however, the buds become increasingly sensitive to low and freezing temperatures. This is because of the high risk of intracellular ice formation in the developing tissues, which would inevitably lead to cell death [8]. Previous studies have shown that invertases are involved in plant responses to cold stress [51,60,61,62,63,64]. The most common observation regarding invertases in general and vacINV in particular in the context of cold stress is an up-regulation of activities/expression levels. These changes are usually associated with increases in hexose levels and are interpreted as a contribution to the osmoprotection of the cold-exposed tissues by the soluble sugars [37,102,103,104]. Very recently, the expression profiles of invertases under low-temperature conditions have also been investigated in apple leaves. The authors found significant changes in the expression levels of several INV-encoding genes and thus concluded that INVs also play a role in the cold stress response in apple leaves [37]. Amongst the apple INV genes responsive to cold, there was one out of the three vacINV genes that are found in the apple genome. The expression of this gene was found to be transiently down-regulated 12 h after the onset of the cold exposure, followed by a strong up-regulation after 24 h [37]. Also in sugar cane seedlings, a down-regulation of the expression of the only vacINV gene as a consequence of cold stress—accompanied by a decrease in enzyme activity—has been observed [62]. However, these authors only analyzed vacINV transcript levels and activity at one point in time and did not provide details of the duration of the cold exposure, which makes it impossible to relate the response of vacINV to a timeline in this case. The information summarized above supports our assumption of a low-temperature impact on vacINV activity in leaf buds that are approaching bud break. vacINV is not only assumed to promote the plant developmental processes in general [41,43,44,54], but also bud break in particular [31]. It could, thus, be speculated that a cold-induced decrease in vacINV will contribute to temporarily slowing down bud development, inevitably delaying bud break. This delay might keep the vulnerable young leaves from emerging from the bud scales during a cold spell, and protect the young leaf tissues from chilling injury or frost/freezing damage [105,106]. Therefore, we suggest that vacINV activity is one of many factors causing developmental delay as a consequence of cold spells, which might indirectly protect the vulnerable young leaf tissues from cold exposure.

5. Conclusions and Outlook

Enzymatic activities in plants are regulated by developmental programs, as well as by external factors. Both aspects were of interest in our present study. We aimed to relate acid invertase activities (cwINV and vacINV) in apple leaf buds during dormancy release and the onset of ontogenetic development to the developmental stages on the one hand and to air temperature on the other.
Concerning the patterns of developmental regulation, our results were in agreement with the findings of other studies, suggesting a role for cwINV and vacINV in promoting bud break. In this context, cwINV activity is likely involved in generating bud sink strength to achieve the import of the carbohydrates required for growth and development. vacINV is thought to promote bud break through its role in enhancing the osmotic potential of the vacuole, as required for growth via cell expansion.
When it comes to the influence of external factors, we detected transient decreases in vacINV activity in the samples collected directly after sudden cold spells. This observation suggests that vacINV responds negatively to temperature stress in apple leaf buds approaching bud break. As vacINV is generally assumed to promote plant developmental processes, including bud break, this observation led us to the speculation that vacINV might be one of many factors delaying bud development during cold spells and shifting bud break to a later point in time.
In order to substantiate our assumptions, further investigations will be required: To address the sink strength potentially generated by cwINV, analyses of sugar levels and of the carbohydrate absorption potential of the buds at different developmental stages could provide valuable information. Concerning the supposed role of vacINV in turgor-driven growth via cell expansion, it would be necessary to investigate the correlation between the expansion growth rates of the buds/the cell sizes in the buds and the vacINV activities measured at different developmental stages. In this context, air temperature should also be taken into consideration to follow up on the potential connection between cold spells and vacINV activity.

Author Contributions

Conceptualization, S.M. with input from A.M.H. and A.R.; methodology, S.M., A.R. and A.M.H.; investigation, A.M.H.; writing—original draft preparation, A.M.H.; writing—review and editing, A.M.H., A.R. and S.M.; visualization, A.M.H.; supervision, S.M. and A.R.; project administration, S.M. All authors have read and agreed to the published version of the manuscript.

Funding

Open Access Funding by the University of Graz.

Data Availability Statement

Not applicable.

Acknowledgments

The authors acknowledge the financial support of the University of Graz. The authors wish to acknowledge Leonhard Steinbauer and Thomas Rühmer at the experimental station for pomiculture and viticulture, “Versuchstation für Obst-und Weinbau” in Haidegg (Graz) for providing the apple trees for this study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Lang, G.A. Dormancy: A New Universal Terminology. HortScience 1987, 22, 817–820. [Google Scholar] [CrossRef]
  2. Lang, G.A.; Early, J.D.; Martin, G.C.; Darnell, R.L. Endo-, Para-, and Ecodormancy: Physiological Terminology and Classification for Dormancy Research. HortScience 1987, 22, 371–377. [Google Scholar] [CrossRef]
  3. de Rosa, V.; Falchi, R.; Moret, E.; Vizzotto, G. Insight into Carbohydrate Metabolism and Signaling in Grapevine Buds during Dormancy Progression. Plants 2022, 11, 1027. [Google Scholar] [CrossRef] [PubMed]
  4. Leida, C.; Conejero, A.; Arbona, V.; Gómez-Cadenas, A.; Llácer, G.; Badenes, M.L.; Ríos, G. Chilling-dependent release of seed and bud dormancy in peach associates to common changes in gene expression. PLoS ONE 2012, 7, e35777. [Google Scholar] [CrossRef] [PubMed]
  5. Lempe, J.; Peil, A.; Flachowsky, H. Time-Resolved Analysis of Candidate Gene Expression and Ambient Temperature during Bud Dormancy in Apple. Front. Plant Sci. 2021, 12, 803341. [Google Scholar] [CrossRef]
  6. Naor, A.; Flaishman, M.; Stern, R.; Moshe, A.; Erez, A. Temperature Effects on Dormancy Completion of Vegetative Buds in Apple. J. Am. Soc. Hortic. Sci. 2003, 128, 636–641. [Google Scholar] [CrossRef]
  7. Heide, O.M.; Prestrud, A.K. Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol. 2005, 25, 109–114. [Google Scholar] [CrossRef]
  8. Vitra, A.; Lenz, A.; Vitasse, Y. Frost hardening and dehardening potential in temperate trees from winter to budburst. New Phytol. 2017, 216, 113–123. [Google Scholar] [CrossRef]
  9. Bilavcik, A.; Zamecnik, J.; Faltus, M. Cryotolerance of apple tree bud is independent of endodormancy. Front. Plant Sci. 2015, 6, 695. [Google Scholar] [CrossRef]
  10. Faust, M.; Liu, D.; Millard, M.M.; Stutte, G.W. Bound versus Free Water in Dormant Apple Buds—A Theory for Endodormancy. HortScience 1991, 26, 887–890. [Google Scholar] [CrossRef]
  11. Erez, A.; Fishman, S.; Linsley-Noakes, G.C.; Allan, P. The Dynamic Model for Rest Completion in Peach Buds. Acta Hortic. 1990, 276, 165–174. [Google Scholar] [CrossRef]
  12. Farokhzad, A.; Nobakht, S.; Alahveran, A.; Sarkhosh, A.; Mohseniazar, M. Biochemical changes in terminal buds of three different walnut (Juglans regia L.) genotypes during dormancy break. Biochem. Syst. Ecol. 2018, 76, 52–57. [Google Scholar] [CrossRef]
  13. Ashworth, E.N. Properties of peach flower buds which facilitate supercooling. Plant Physiol. 1982, 70, 1475–1479. [Google Scholar] [CrossRef]
  14. Proebsting, E.L. The role of air temperatures and bud development in determining hardiness of dormant Elberta peach fruit buds. Proc. Amer. Soc. Hort. Sc. 1963, 83, 259–269. [Google Scholar]
  15. Chmielewski, F.-M.; Götz, K.-P. Metabolites in Cherry Buds to Detect Winter Dormancy. Metabolites 2022, 12, 247. [Google Scholar] [CrossRef]
  16. Chmielewski, F.M.; Götz, K.-P.; Homann, T.; Huschek, G.; Rawel, H.M. Identification of Endodormancy Release for Cherries (Prunus avium L.) by Abscisic Acid and Sugars. J. Hortic. 2017, 4, 1000210. [Google Scholar] [CrossRef]
  17. Vitasse, Y.; Lenz, A.; Körner, C. The interaction between freezing tolerance and phenology in temperate deciduous trees. Front. Plant Sci. 2014, 5, 541. [Google Scholar] [CrossRef] [PubMed]
  18. Li, Z.; Reighard, G.L.; Abbott, A.G.; Bielenberg, D.G. Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J. Exp. Bot. 2009, 60, 3521–3530. [Google Scholar] [CrossRef]
  19. IPCC. 2022: Climate Change 2022: Impacts, Adaptation and Vulnerability. In Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change; Pörtner, H.-O., Roberts, D.C., Tignor, M., Poloczanska, E.S., Mintenbeck, K., Alegría, A., Craig, M., Langsdorf, S., Löschke, S., Möller, V., et al., Eds.; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2022; p. 3056. [Google Scholar] [CrossRef]
  20. Sapkota, S.; Liu, J.; Islam, M.T.; Ravindran, P.; Kumar, P.P.; Sherif, S.M. Contrasting bloom dates in two apple cultivars linked to differential levels of phytohormones and heat requirements during ecodormancy. Sci. Hortic. 2021, 288, 110413. [Google Scholar] [CrossRef]
  21. Unterberger, C.; Brunner, L.; Nabernegg, S.; Steininger, K.W.; Steiner, A.K.; Stabentheiner, E.; Monschein, S.; Truhetz, H. Spring frost risk for regional apple production under a warmer climate. PLoS ONE 2018, 13, e0200201. [Google Scholar] [CrossRef]
  22. Food and Agriculture Organization of the United Nations. FAOSTA: Food and Agriculture Organization of the United Nations. Available online: https://www.fao.org/faostat/en/#data (accessed on 24 September 2023).
  23. Olhnuud, A.; Liu, Y.; Makowski, D.; Tscharntke, T.; Westphal, C.; Wu, P.; Wang, M.; van der Werf, W. Pollination deficits and contributions of pollinators in apple production: A global meta-analysis. J. Appl. Ecol. 2022, 59, 2911–2921. [Google Scholar] [CrossRef]
  24. Fadón, E.; Fernandez, E.; Behn, H.; Luedeling, E. A Conceptual Framework for Winter Dormancy in Deciduous Trees. Agronomy 2020, 10, 241. [Google Scholar] [CrossRef]
  25. Beauvieux, R.; Wenden, B.; Dirlewanger, E. Bud Dormancy in Perennial Fruit Tree Species: A Pivotal Role for Oxidative Cues. Front. Plant Sci. 2018, 9, 657. [Google Scholar] [CrossRef]
  26. Tixier, A.; Gambetta, G.A.; Godfrey, J.; Orozco, J.; Zwieniecki, M.A. Non-structural Carbohydrates in Dormant Woody Perennials; The Tale of Winter Survival and Spring Arrival. Front. For. Glob. Chang. 2019, 2, 18. [Google Scholar] [CrossRef]
  27. Götz, K.-P.; Chmielewski, F.-M. Response of sweet cherry buds and twigs to temperature changes—Evaluated by the determination of the degradation and synthesis of sucrose. Hortic. Sci. 2021, 48, 149–157. [Google Scholar] [CrossRef]
  28. Liang, D.; Huang, X.; Shen, Y.; Shen, T.; Zhang, H.; Lin, L.; Wang, J.; Deng, Q.; Lyu, X.; Xia, H. Hydrogen cyanamide induces grape bud endodormancy release through carbohydrate metabolism and plant hormone signaling. BMC Genom. 2019, 20, 1034. [Google Scholar] [CrossRef] [PubMed]
  29. Zhuang, W.; Gao, Z.; Wen, L.; Huo, X.; Cai, B.; Zhang, Z. Metabolic changes upon flower bud break in Japanese apricot are enhanced by exogenous GA4. Hortic. Res. 2015, 2, 15046. [Google Scholar] [CrossRef]
  30. Marafon, A.C.; Citadin, I.; Amarante, L.d.; Herter, F.G.; Hawerroth, F.J. Chilling privation during dormancy period and carbohydrate mobilization in Japanese pear trees. Sci. Agric. 2011, 68, 462–468. [Google Scholar] [CrossRef]
  31. Girault, T.; Abidi, F.; Sigogne, M.; Pelleschi-Travier, S.; Boumaza, R.; Sakr, S.; Leduc, N. Sugars are under light control during bud burst in Rosa sp. Plant Cell Environ. 2010, 33, 1339–1350. [Google Scholar] [CrossRef]
  32. Bonhomme, M.; Rageau, R.; Lacointe, A.; Gendraud, M. Influences of cold deprivation during dormancy on carbohydrate contents of vegetative and floral primordia and nearby structures of peach buds (Prunus persica L. Batch). Sci. Hortic. 2005, 105, 223–240. [Google Scholar] [CrossRef]
  33. Marquat, C.; Vandamme, M.; Gendraud, M.; Pétel, G. Dormancy in vegetative buds of peach: Relation between carbohydrate absorption potentials and carbohydrate concentration in the bud during dormancy and its release. Sci. Hortic. 1999, 79, 151–162. [Google Scholar] [CrossRef]
  34. Hussain, S.; Liu, G.; Liu, D.; Ahmed, M.; Hussain, N.; Teng, Y. Study on the expression of dehydrin genes and activities of antioxidative enzymes in floral buds of two sand pear (Pyrus pyrifolia Nakai) cultivars requiring different chilling hours for bud break. Turk. J. Agric. For. 2015, 39, 930–939. [Google Scholar] [CrossRef]
  35. Ito, A.; Hayama, H.; Kashimura, Y. Sugar metabolism in buds during flower bud formation: A comparison of two Japanese pear [Pyrus pyrifolia (Burm.) Nak.] cultivars possessing different flowering habits. Sci. Hortic. 2002, 96, 163–175. [Google Scholar] [CrossRef]
  36. Ben Mohamed, H.; Vadel, A.M.; Geuns, J.M.; Khemira, H. Carbohydrate changes during dormancy release in Superior Seedless grapevine cuttings following hydrogen cyanamide treatment. Sci. Hortic. 2012, 140, 19–25. [Google Scholar] [CrossRef]
  37. Peng, Y.; Zhu, L.; Tian, R.; Wang, L.; Su, J.; Yuan, Y.; Ma, F.; Li, M.; Ma, B. Genome-wide identification, characterization and evolutionary dynamic of invertase gene family in apple, and revealing its roles in cold tolerance. Int. J. Biol. Macromol. 2023, 229, 766–777. [Google Scholar] [CrossRef] [PubMed]
  38. Roitsch, T.; González, M.-C. Function and regulation of plant invertases: Sweet sensations. Trends Plant Sci. 2004, 9, 606–613. [Google Scholar] [CrossRef]
  39. Klotz, K.L.; Finger, F.L.; Shelver, W.L. Characterization of two sucrose synthase isoforms in sugarbeet root. Plant Physiol. Biochem. 2003, 41, 107–115. [Google Scholar] [CrossRef]
  40. Sturm, A.; Tang, G.Q. The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci. 1999, 4, 401–407. [Google Scholar] [CrossRef] [PubMed]
  41. Wan, H.; Wu, L.; Yang, Y.; Zhou, G.; Ruan, Y.-L. Evolution of Sucrose Metabolism: The Dichotomy of Invertases and Beyond. Trends Plant Sci. 2018, 23, 163–177. [Google Scholar] [CrossRef]
  42. Braun, D.M.; Wang, L.; Ruan, Y.-L. Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. J. Exp. Bot. 2014, 65, 1713–1735. [Google Scholar] [CrossRef]
  43. Ruan, Y.-L. Sucrose metabolism: Gateway to diverse carbon use and sugar signaling. Annu. Rev. Plant Biol. 2014, 65, 33–67. [Google Scholar] [CrossRef] [PubMed]
  44. Ruan, Y.-L.; Jin, Y.; Yang, Y.-J.; Li, G.-J.; Boyer, J.S. Sugar input, metabolism, and signaling mediated by invertase: Roles in development, yield potential, and response to drought and heat. Mol. Plant 2010, 3, 942–955. [Google Scholar] [CrossRef] [PubMed]
  45. Sturm, A. Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol. 1999, 121, 1–8. [Google Scholar] [CrossRef] [PubMed]
  46. González, M.-C.; Roitsch, T.; Cejudo, F.J. Circadian and developmental regulation of vacuolar invertase expression in petioles of sugar beet plants. Planta 2005, 222, 386–395. [Google Scholar] [CrossRef]
  47. Proels, R.K.; Roitsch, T. Extracellular invertase LIN6 of tomato: A pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. J. Exp. Bot. 2009, 60, 1555–1567. [Google Scholar] [CrossRef] [PubMed]
  48. Ahiakpa, J.K.; Karikari, B.; Magdy, M.; Munir, S.; Mumtaz, M.A.; Li, F.; Wang, Y.; Shang, L.; Zhang, Y. Regulation of invertase and sucrose for improving tomato fruit flavor: A review. Veg. Res. 2021, 1, 10. [Google Scholar] [CrossRef]
  49. Ruan, Y.-L.; Jin, Y.; Huang, J. Capping invertase activity by its inhibitor: Roles and implications in sugar signaling, carbon allocation, senescence and evolution. Plant Signal. Behav. 2009, 4, 983–985. [Google Scholar] [CrossRef]
  50. Coluccio Leskow, C.; Conte, M.; Del Pozo, T.; Bermúdez, L.; Lira, B.S.; Gramegna, G.; Baroli, I.; Burgos, E.; Zavallo, D.; Kamenetzky, L.; et al. The cytosolic invertase NI6 affects vegetative growth, flowering, fruit set, and yield in tomato. J. Exp. Bot. 2021, 72, 2525–2543. [Google Scholar] [CrossRef]
  51. Qian, W.; Xiao, B.; Wang, L.; Hao, X.; Yue, C.; Cao, H.; Wang, Y.; Li, N.; Yu, Y.; Zeng, J.; et al. CsINV5, a tea vacuolar invertase gene enhances cold tolerance in transgenic Arabidopsis. BMC Plant Biol. 2018, 18, 228. [Google Scholar] [CrossRef] [PubMed]
  52. Ruan, Y.-L. CWIN-sugar transporter nexus is a key component for reproductive success. J. Plant Physiol. 2022, 268, 153572. [Google Scholar] [CrossRef]
  53. Eschrich, W. Free Space Invertase, its Possible Role in Phloem Unloading1. Ber. Dtsch. Bot. Ges. 1980, 93, 363–378. [Google Scholar] [CrossRef]
  54. Koch, K. Sucrose metabolism: Regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 2004, 7, 235–246. [Google Scholar] [CrossRef]
  55. Winter, H.; Huber, S.C. Regulation of sucrose metabolism in higher plants: Localization and regulation of activity of key enzymes. Crit. Rev. Biochem. Mol. Biol. 2000, 35, 253–289. [Google Scholar] [CrossRef] [PubMed]
  56. Tymowska-Lalanne, Z.; Kreis, M. The Plant Invertases: Physiology, Biochemistry and Molecular Biology. Adv. Bot. Res. 1998, 28, 71–117. [Google Scholar] [CrossRef]
  57. Zhu, J.; Qi, J.; Fang, Y.; Xiao, X.; Li, J.; Lan, J.; Tang, C. Characterization of Sugar Contents and Sucrose Metabolizing Enzymes in Developing Leaves of Hevea brasiliensis. Front. Plant Sci. 2018, 9, 58. [Google Scholar] [CrossRef] [PubMed]
  58. Pantin, F.; Simonneau, T.; Muller, B. Coming of leaf age: Control of growth by hydraulics and metabolics during leaf ontogeny. New Phytol. 2012, 196, 349–366. [Google Scholar] [CrossRef]
  59. Le Hir, R.; Leduc, N.; Jeannette, E.; Viemont, J.-D.; Pelleschi-Travier, S. Variations in sucrose and ABA concentrations are concomitant with heteroblastic leaf shape changes in a rhythmically growing species (Quercus robur). Tree Physiol. 2006, 26, 229–238. [Google Scholar] [CrossRef]
  60. He, X.; Wei, Y.; Kou, J.; Xu, F.; Chen, Z.; Shao, X. PpVIN2, an acid invertase gene family member, is sensitive to chilling temperature and affects sucrose metabolism in postharvest peach fruit. Plant Growth Regul. 2018, 86, 169–180. [Google Scholar] [CrossRef]
  61. Xu, X.-X.; Hu, Q.; Yang, W.-N.; Jin, Y. The roles of call wall invertase inhibitor in regulating chilling tolerance in tomato. BMC Plant Biol. 2017, 17, 195. [Google Scholar] [CrossRef]
  62. Wang, L.; Zheng, Y.; Ding, S.; Zhang, Q.; Chen, Y.; Zhang, J. Molecular cloning, structure, phylogeny and expression analysis of the invertase gene family in sugarcane. BMC Plant Biol. 2017, 17, 109. [Google Scholar] [CrossRef]
  63. Wang, X.; Chen, Y.; Jiang, S.; Xu, F.; Wang, H.; Wei, Y.; Shao, X. PpINH1, an invertase inhibitor, interacts with vacuolar invertase PpVIN2 in regulating the chilling tolerance of peach fruit. Hortic. Res. 2020, 7, 168. [Google Scholar] [CrossRef]
  64. McKenzie, M.J.; Chen, R.K.Y.; Harris, J.C.; Ashworth, M.J.; Brummell, D.A. Post-translational regulation of acid invertase activity by vacuolar invertase inhibitor affects resistance to cold-induced sweetening of potato tubers. Plant Cell Environ. 2013, 36, 176–185. [Google Scholar] [CrossRef]
  65. Hubmann, A.M.; Jammer, A.; Monschein, S. Activities of H2O2-Converting Enzymes in Apple Leaf Buds during Dormancy Release in Consideration of the Ratio Change between Bud Scales and Physiologically Active Tissues. Horticulturae 2022, 8, 982. [Google Scholar] [CrossRef]
  66. Jammer, A.; Gasperl, A.; Luschin-Ebengreuth, N.; Heyneke, E.; Chu, H.; Cantero-Navarro, E.; Großkinsky, D.K.; Albacete, A.A.; Stabentheiner, E.; Franzaring, J.; et al. Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. J. Exp. Bot. 2015, 66, 5531–5542. [Google Scholar] [CrossRef]
  67. Fimognari, L.; Dölker, R.; Kaselyte, G.; Jensen, C.N.G.; Akhtar, S.S.; Großkinsky, D.K.; Roitsch, T. Simple semi-high throughput determination of activity signatures of key antioxidant enzymes for physiological phenotyping. Plant Methods 2020, 16, 42. [Google Scholar] [CrossRef] [PubMed]
  68. Federal Institute for Geology, Geophysics, Climatology and Meteorology. Auf- und Untergangszeiten von Sonne und Mond, Ephemeriden in Graz für Das Jahr 2021. Available online: https://www.zamg.ac.at/cms/de/klima/klimauebersichten/ephemeriden/graz?jahr=2021 (accessed on 24 September 2023).
  69. Federal Institute for Geology, Geophysics, Climatology and Meteorology. Auf- und Untergangszeiten von Sonne und Mond, Ephemeriden in Graz für das Jahr 2020. Available online: https://www.zamg.ac.at/cms/de/klima/klimauebersichten/ephemeriden/graz?jahr=2020 (accessed on 24 September 2023).
  70. Meier, U.; Graf, H.; Hack, H.; Heß, M.; Kennel, W.; Klose, R.; Mappes, D.; Seipp, D.; Strauß, R.; Streif, J.; et al. Phänologische Entwicklungsstadien des Kernobstes (Malus domestica Borkh. und Pyrus communis L.), des Steinobstes (Prunus-Arten), der Johannisbeere (Ribes-Arten) und der Erdbeere (Fragaria ananassa Duch.). Nachr. Dtsch Pflanzenschutzd. 1994, 46, 141–153. [Google Scholar]
  71. Baumgarten, F.; Zohner, C.M.; Gessler, A.; Vitasse, Y. Chilled to be forced: The best dose to wake up buds from winter dormancy. New Phytol. 2021, 230, 1366–1377. [Google Scholar] [CrossRef]
  72. Luedeling, E.; Kunz, A.; Blanke, M.M. Identification of chilling and heat requirements of cherry trees—A statistical approach. Int. J. Biometeorol. 2013, 57, 679–689. [Google Scholar] [CrossRef]
  73. Eccel, E.; Rea, R.; Caffarra, A.; Crisci, A. Risk of spring frost to apple production under future climate scenarios: The role of phenological acclimation. Int. J. Biometeorol. 2009, 53, 273–286. [Google Scholar] [CrossRef]
  74. Viti, R.; Bartolini, S.; Andreini, L. Apricot flower bud dormancy: Main morphological, anatomical and physiological features related to winter climate influence. Adv. Hortic. Sci. 2013, 27, 5–17. [Google Scholar]
  75. Cai, F.; Jin, X.; Tian, Y.; Huang, Z.; Wang, X.; Zhang, Y.; Sun, Y.; Shao, C. Molecular regulation of bud dormancy in perennial plants. Plant Growth Regul. 2023. [Google Scholar] [CrossRef]
  76. Yamane, H.; Singh, A.K.; Cooke, J.E.K. Plant dormancy research: From environmental control to molecular regulatory networks. Tree Physiol. 2021, 41, 523–528. [Google Scholar] [CrossRef]
  77. Yamane, H.; Andrés, F.; Bai, S.; Luedeling, E.; Or, E. Editorial: Environmental and molecular control of bud dormancy and bud break in woody perennials: An integrative approach. Front. Plant Sci. 2023, 14, 1104108. [Google Scholar] [CrossRef] [PubMed]
  78. Noguer, C.G.; Delgado, A.; Else, M.; Hadley, P. Apple (Malus × domestica Borkh.) dormancy—A review of regulatory mechanisms and agroclimatic requirements. Front. Hortic. 2023, 2, 1217689. [Google Scholar] [CrossRef]
  79. Maurya, J.P.; Bhalerao, R.P. Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees: A molecular perspective. Ann. Bot. 2017, 120, 351–360. [Google Scholar] [CrossRef] [PubMed]
  80. Cooke, J.E.K.; Eriksson, M.E.; Junttila, O. The dynamic nature of bud dormancy in trees: Environmental control and molecular mechanisms. Plant Cell Environ. 2012, 35, 1707–1728. [Google Scholar] [CrossRef]
  81. Heide, O.M. Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species. Sci. Hortic. 2008, 115, 309–314. [Google Scholar] [CrossRef]
  82. Zhu, L.H.; Borsboom, O.; Tromp, J. The effect of temperature on flower-bud formation in apple including some morphological aspects. Sci. Hortic. 1997, 70, 1–8. [Google Scholar] [CrossRef]
  83. Thakur, P.; Kumar, S.; Malik, J.A.; Berger, J.D.; Nayyar, H. Cold stress effects on reproductive development in grain crops: An overview. Environ. Exp. Bot. 2010, 67, 429–443. [Google Scholar] [CrossRef]
  84. Jammer, A.; Akhtar, S.S.; Amby, D.B.; Pandey, C.; Mekureyaw, M.F.; Bak, F.; Roth, P.M.; Roitsch, T. Enzyme activity profiling for physiological phenotyping within functional phenomics: Plant growth and stress responses. J. Exp. Bot. 2022, 73, 5170–5198. [Google Scholar] [CrossRef]
  85. Jammer, A.; Albacete, A.; Schulz, B.; Koch, W.; Weltmeier, F.; van der Graaff, E.; Pfeifhofer, H.W.; Roitsch, T.G. Early-stage sugar beet taproot development is characterized by three distinct physiological phases. Plant Direct 2020, 4, e00221. [Google Scholar] [CrossRef]
  86. Biais, B.; Bénard, C.; Beauvoit, B.; Colombié, S.; Prodhomme, D.; Ménard, G.; Bernillon, S.; Gehl, B.; Gautier, H.; Ballias, P.; et al. Remarkable reproducibility of enzyme activity profiles in tomato fruits grown under contrasting environments provides a roadmap for studies of fruit metabolism. Plant Physiol. 2014, 164, 1204–1221. [Google Scholar] [CrossRef]
  87. Marchi, S.; Sebastiani, L.; Gucci, R.; Tognetti, R. Sink-source Transition in Peach Leaves during Shoot Development. J. Am. Soc. Hortic. Sci. 2005, 130, 928–935. [Google Scholar] [CrossRef]
  88. Turgeon, R. The Sink-Source Transition in Leaves. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 1989, 40, 119–138. [Google Scholar] [CrossRef]
  89. Maurel, K.; Leite, G.B.; Bonhomme, M.; Guilliot, A.; Rageau, R.; Pétel, G.; Sakr, S. Trophic control of bud break in peach (Prunus persica) trees: A possible role of hexoses. Tree Physiol. 2004, 24, 579–588. [Google Scholar] [CrossRef] [PubMed]
  90. Harada, T.; Eguchi, Y.; Inada, Y.; Onishi, K.; Hishikawa, K. Successive Induction of Invertase Isoforms During Flower Development in Eustoma. Hort. J. 2021, 90, 334–340. [Google Scholar] [CrossRef]
  91. Zanol, G.C.; Bartolini, S. Changes in intracellular pH in apricot buds during the winter season. Adv. Hortic. Sci. 2003, 17, 97–101. [Google Scholar]
  92. Rady, M.M.; Seif El-Yazal, M.A. Response of “Anna” apple dormant buds and carbohydrate metabolism during floral bud break to onion extract. Sci. Hortic. 2013, 155, 78–84. [Google Scholar] [CrossRef]
  93. Zhang, X.-Y.; Wang, X.-L.; Wang, X.-F.; Xia, G.-H.; Pan, Q.-H.; Fan, R.-C.; Wu, F.-Q.; Yu, X.-C.; Zhang, D.-P. A shift of Phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol. 2006, 142, 220–232. [Google Scholar] [CrossRef]
  94. Chourey, P.S.; Jain, M.; Li, Q.-B.; Carlson, S.J. Genetic control of cell wall invertases in developing endosperm of maize. Planta 2006, 223, 159–167. [Google Scholar] [CrossRef]
  95. Signorelli, S.; Shaw, J.; Hermawaty, D.; Wang, Z.; Verboven, P.; Considine, J.A.; Considine, M.J. The initiation of bud burst in grapevine features dynamic regulation of the apoplastic pore size. J. Exp. Bot. 2020, 71, 719–729. [Google Scholar] [CrossRef]
  96. Kutschera, U. Cell Expansion in Plant Development. Braz. J. Plant Physiol. 2000, 12, 65–95. [Google Scholar]
  97. Feng, Z.; Zheng, F.; Wu, S.; Li, R.; Li, Y.; Zhong, J.; Zhao, H. Functional Characterization of a Cucumber (Cucumis sativus L.) Vacuolar Invertase, CsVI1, Involved in Hexose Accumulation and Response to Low Temperature Stress. Int. J. Mol. Sci. 2021, 22, 9365. [Google Scholar] [CrossRef]
  98. Wang, L.; Cook, A.; Patrick, J.W.; Chen, X.-Y.; Ruan, Y.-L. Silencing the vacuolar invertase gene GhVIN1 blocks cotton fiber initiation from the ovule epidermis, probably by suppressing a cohort of regulatory genes via sugar signaling. Plant J. 2014, 78, 686–696. [Google Scholar] [CrossRef] [PubMed]
  99. Wang, L.; Li, X.-R.; Lian, H.; Ni, D.-A.; He, Y.; Chen, X.-Y.; Ruan, Y.-L. Evidence that high activity of vacuolar invertase is required for cotton fiber and Arabidopsis root elongation through osmotic dependent and independent pathways, respectively. Plant Physiol. 2010, 154, 744–756. [Google Scholar] [CrossRef]
  100. Kutschera, U.; Niklas, K.J. Cell division and turgor-driven stem elongation in juvenile plants: A synthesis. Plant Sci. 2013, 207, 45–56. [Google Scholar] [CrossRef] [PubMed]
  101. Chen, Z.; Gao, K.; Su, X.; Rao, P.; An, X. Genome-Wide Identification of the Invertase Gene Family in Populus. PLoS ONE 2015, 10, e0138540. [Google Scholar] [CrossRef]
  102. Bhaskar, P.B.; Wu, L.; Busse, J.S.; Whitty, B.R.; Hamernik, A.J.; Jansky, S.H.; Buell, C.R.; Bethke, P.C.; Jiang, J. Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiol. 2010, 154, 939–948. [Google Scholar] [CrossRef]
  103. Usadel, B.; Bläsing, O.E.; Gibon, Y.; Poree, F.; Höhne, M.; Günter, M.; Trethewey, R.; Kamlage, B.; Poorter, H.; Stitt, M. Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ. 2008, 31, 518–547. [Google Scholar] [CrossRef] [PubMed]
  104. Dahro, B.; Wang, Y.; Alhag, A.; Li, C.; Guo, D.; Liu, J.-H. Genome-wide identification and expression profiling of invertase gene family for abiotic stresses tolerance in Poncirus trifoliata. BMC Plant Biol. 2021, 21, 559. [Google Scholar] [CrossRef]
  105. Ashworth, E.N.; Davis, G.A.; Wisniewski, M.E. The formation and distribution of ice within dormant and deacclimated peach flower buds. Plant Cell Environ. 1989, 12, 521–528. [Google Scholar] [CrossRef]
  106. Kalberer, S.R.; Wisniewski, M.; Arora, R. Deacclimation and reacclimation of cold-hardy plants: Current understanding and emerging concepts. Plant Sci. 2006, 171, 3–16. [Google Scholar] [CrossRef]
Agronomy 13 02659 g001
Figure 1. Synoptical representation of air temperature (daily/nightly means and interval averages) and acid invertase activities in apple leaf buds during dormancy release until bud break in the years 2020 (left) and 2021 (right). Intervals between sampling days are labeled as I1–I6 (for 2020, left) and I1–I5 (for 2021, right). The enzymatic activities in nkat/g aDW are shown as mean values of the mixed samples (n = 5) ± standard deviation. Sampling dates are indicated by the grey bars. Additionally, the illustrations of the buds show the phenological stages at the beginning and the end of the observation period.
Figure 1. Synoptical representation of air temperature (daily/nightly means and interval averages) and acid invertase activities in apple leaf buds during dormancy release until bud break in the years 2020 (left) and 2021 (right). Intervals between sampling days are labeled as I1–I6 (for 2020, left) and I1–I5 (for 2021, right). The enzymatic activities in nkat/g aDW are shown as mean values of the mixed samples (n = 5) ± standard deviation. Sampling dates are indicated by the grey bars. Additionally, the illustrations of the buds show the phenological stages at the beginning and the end of the observation period.
Agronomy 13 02659 g001
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Hubmann, A.M.; Roth, A.; Monschein, S. Breaking Buds—Stop and Go? Acid Invertase Activities in Apple Leaf Buds during Dormancy Release until Bud Break. Agronomy 2023, 13, 2659. https://doi.org/10.3390/agronomy13102659

AMA Style

Hubmann AM, Roth A, Monschein S. Breaking Buds—Stop and Go? Acid Invertase Activities in Apple Leaf Buds during Dormancy Release until Bud Break. Agronomy. 2023; 13(10):2659. https://doi.org/10.3390/agronomy13102659

Chicago/Turabian Style

Hubmann, Anna M., Alexandra Roth, and Stephan Monschein. 2023. "Breaking Buds—Stop and Go? Acid Invertase Activities in Apple Leaf Buds during Dormancy Release until Bud Break" Agronomy 13, no. 10: 2659. https://doi.org/10.3390/agronomy13102659

APA Style

Hubmann, A. M., Roth, A., & Monschein, S. (2023). Breaking Buds—Stop and Go? Acid Invertase Activities in Apple Leaf Buds during Dormancy Release until Bud Break. Agronomy, 13(10), 2659. https://doi.org/10.3390/agronomy13102659

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop