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Article

Putrescine Increases Frost Tolerance and Effectively Mitigates Sweet Cherry (Prunus avium L.) Cracking: A Study of Four Different Growing Cycles

by
María Celeste Ruiz-Aracil
1,
Juan Miguel Valverde
1,
Aleixandre Beltrà
2,
Alberto Carrión-Antolí
1,
José Manuel Lorente-Mento
1,
Marta Nicolás-Almansa
1 and
Fabián Guillén
1,*
1
Postharvest Research Group of Fruit and Vegetables, CIAGRO, University Miguel Hernández, Ctra. Beniel Km. 3.2, 03312 Orihuela, Spain
2
Mas de Roc Cooperativa Valenciana, Partida Canal Alta 5, 03801 Alcoi, Spain
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(1), 23; https://doi.org/10.3390/agronomy14010023 (registering DOI)
Submission received: 28 November 2023 / Revised: 14 December 2023 / Accepted: 19 December 2023 / Published: 21 December 2023
(This article belongs to the Special Issue Crop and Vegetable Physiology under Environmental Stresses)
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Abstract

:
Sweet cherry producers must deal with different climactic challenges annually, specifically the impact of spring frost and the inherent risk of fruit cracking. This susceptibility arises from the simultaneous occurrence of spring frost during the bloom stage or the sweet cherry cracking at vulnerable maturity stages in sweet cherry trees during persistent rainfall. Given the change in climatic patterns, the implementation of new strategies and innovative approaches becomes imperative to alleviate potential damage from these climatic adversities. This study aims to explore—for the first time—the effectiveness of preharvest putrescine applications during the flowering stage and ripening on-tree to increase tolerance in sweet cherry against adverse climatic events throughout its on-tree development and at the time of harvest. In this context, foliar applications of putrescine at concentrations of 1 and 10 mM were administered to distinct sweet cherry cultivars, namely, ‘Prime Giant’ and ‘Sweetheart’. Over the course of four growing seasons, our investigation focused on evaluating the influence of this natural elicitor on the frost resilience of flower buds during the preharvest period and its impact on reducing fruit cracking in these selected cultivars. In this sense, the overall malondialdehyde content exhibited a reduction in flower buds treated with putrescine, and the fruit set experienced an increase across the majority of evaluated growing seasons. On the other hand, the incidence of sweet cherry cracking in putrescine-treated sweet cherries showed a consistent reduction in all the studied growing seasons. Our results indicate that preharvest treatments with putrescine effectively alleviate the susceptibility of flower buds to spring frost and significantly diminish fruit cracking, thereby enhancing the overall tolerance to abiotic stress. Furthermore, we evaluated different quality parameters at the time of harvest, including fruit firmness, external color, total soluble solids, and total acidity. Generally, the observed changes in these parameters were delayed in putrescine-treated fruit as compared to the control batch or remained unaffected. For this reason, the implementation of preharvest treatments based on putrescine emerges as a valuable strategy for adapting to climate change and mitigating the impact of abiotic stress, potentially increasing sweet cherry production.

1. Introduction

Sweet cherry production is a system highly susceptible to adverse climatic conditions. Over the past years sweet cherry growers have witnessed a substantial drop in production, largely attributed to the detrimental impact of spring frost and the occurrence of sweet cherry cracking. This decline in production serves as clear evidence of the anticipated consequences of climate change on the Mediterranean area, and adverse climate conditions become less predictable [1]. Spring frost is a recurrent challenge for sweet cherry growers, especially during the ‘open cluster stage’ and ‘full bloom’ phenological stages. Sudden temperature drops during these stages can lead to frost damage, causing reduced fruit set and significantly impacting the overall yield [2]. Climate change can also have an additional impact on sweet cherry production due to different factors, such as heavy rainfall and high humidity, which contribute to fruit cracking [3]. These environmental influences, in addition to sudden temperature changes, affect the final production. On the other hand, a multifactorial process is involved in sweet cherry cracking, but factors such as sudden rainfalls, high humidity [4,5], or the stage of ripeness at which sweet cherries are exposed to these conditions [6] play a crucial role and can lead to significant losses for producers. As a result, climate change becomes an additional challenge for sweet cherry growers, necessitating the development of innovative strategies to mitigate the impact of these abiotic events.
To prevent frost damage in sweet cherry trees, only a limited number of management approaches have been assayed. Bioregulators have been shown to delay the developmental process. In this regard, the use of aminoethoxyvinylglycine (AVG, ReTain), an ethylene inhibitor, extends ovule functionality [7]. The timing of bud break can also be modulated by methyl esters of fatty acids [8]. Additionally, seaweed extracts have increased production when applied before fruit set [9]. Other methods aim to regulate plant temperature, such as the preharvest application of coatings made from cellulose nanocrystals [10] or traditional frost protection candles [11]. Furthermore, irrigation and protective structures, such as rain covers, impact orchard conditions and may enhance resilience against frost damage [12,13]. To mitigate sweet cherry cracking, the number of strategies developed is as limited as those to prevent frost damage. Researchers have applied different preharvest technologies in sweet cherry orchards. Among these approaches are the use of protective cover structures [14,15], the application of calcium-based sprays [4,16], sodium silicate [17], and the implementation of treatments involving seaweed extracts [18]. Growth regulators, including gibberellic acid [19], glycine betaine [20], and methyl jasmonate (MeJA) [6,21], also have been shown to control sweet cherry cracking.
The preharvest application of plant-derived hormones, such as polyamines, can impact a multitude of metabolic and physiological processes in plant tissues. These processes are as diverse as the flowering, fruit set, and embryogenesis or protection against certain types of stress [22]. The application of putrescine before fruit set has been studied, and these treatments were able to maintain the number of flowers in apricot trees with satisfactory results. This was attributed to the fact that polyamines stimulate fruit sets, playing a role in floral stimulation and the formation of several organs of the flower, including the ovary development [22,23]. Putrescine, like many other polyamines, has exhibited remarkable effectiveness in delaying fruit ripening and senescence as a preharvest or postharvest strategy [24]. It helps to maintain antioxidant balance and delays tissue disintegration in climacteric [25,26] and non-climacteric fruit [27]. Additionally, as with many other elicitors, putrescine has been demonstrated to be involved in the stimulation of energy supply pathways, which is critical in energy-demanding periods, such as abiotic stress and senescence [28]. Positive effects on fruit quality have been demonstrated through the application of preharvest treatments based on putrescine in mango [29], plum [30,31], jujube [32], and pears [33] with additional cold storage tolerance benefits in this fruit [34]. This effect has been associated with an increase in bioactive compounds and antioxidant levels. Similarly, in other non-climacteric fruits, such as table grapes, the preharvest anti-senescence effects of putrescine have been observed [27] and associated with an increased antioxidant balance. However, there is no previous report in which putrescine has been evaluated to control frost tolerance or sweet cherry cracking. In this study, the main goal has been to evaluate the effectiveness of preharvest putrescine treatments for enhancing frost tolerance up to the fruit set stage and reducing fruit cracking during on-tree fruit development across four distinct growing seasons (2020–2023).

2. Materials and Methods

2.1. Plant Material and Experimental Design

Over the period from 2020 to 2023, this four-year investigation was carried out in diverse field plots situated in Alcoy (Mas de Roc Coop. Agrícola, Alcoi, Spain). Sweet cherry trees (Prunus avium L.) of the ‘Prime Giant’ and ‘Sweet-heart’ cultivars, grafted onto SL-64 rootstock, were utilized for the study. Different trees and orchards were selected during the 2020–2022 period, and in 2023, the same plot as in 2022 was chosen. The sweet cherry trees were subjected to consistent agronomic practices throughout the different growing seasons.
Putrescine (Sigma-Aldrich, Germany, >99% D13208) treatments (3 L per tree) were applied using a manual sprayer machine (2020, 2021, and 2023 growing cycles). In 2022, the different solutions were applied using a spraying tractor following regular agronomic practices. Freshly prepared putrescine solutions were applied at concentrations of 1 and 10 mM, with the addition of 1 mL L−1 of Tween 20 as a surfactant. These concentrations were proposed and increased after studying those assayed by previous authors in different species [27,33]. Control trees were treated with 3 L of distilled water containing 1 mL L−1 Tween 20. For every treatment and cultivar, three sets of 3 trees were utilized as replicates. Each treatment involved four spray applications during the 2020 and 2021 growing cycles at key moments or phenological stages using the BBCH scale (Biologische Bundesantalt, Bundessortenamt und Chemische Industrie): before open cluster stage (BBCH 54), full bloom (BBCH 65), pit hardening (BBCH 77), and the beginning of color changes (BBCH 81). In 2022 and 2023, only three applications were applied, omitting the full bloom stage in order to optimize the number of applications. Only the lower concentration was applied in the 2022 and 2023 periods. Notably, 2020 and 2021 served as a screening phase for concentrations involving two sweet cherry cultivars.
For the MDA and fruit set evaluations, a total of 36 branch segments (equally divided around the tree and at opposite sides of the canopy) were labeled into three groups, with three trees of each cultivar. The evaluation of cracking incidence on the tree was carried out on four specified branches of each tree located at opposite sides of the tree, with 100 fruits evaluated for this disorder in each tree. This evaluation was assayed only for two consecutive growing seasons (2021 and 2022).

2.2. Sweet Cherry Frost Tolerance Evaluation

In March and April of 2020, during the onset of the COVID-19 pandemic, circumstances did not allow the evaluation of frost tolerance in sweet cherry trees. In 2021, 2022, and 2023, the recorded freezing temperatures in April during the flowering stage were −0.4, −0.7, and −3.4 °C, respectively. Remarkably, in 2023, the lowest temperature recorded (−3.4 °C) coincided with the ‘Prime Giant’ cultivar in the full bloom stage, showing no resilience against suboptimal temperature. For this reason, the fruit set was very low in this cultivar as compared with the rest of the growing seasons evaluated.
MDA content was evaluated in flower bud tissues one week after trees were treated in 2021 and 2022. Initially, a set of flower buds (BBCH 55) was taken from four different and equidistant branches located at both sides of each tree. MDA was assayed following the method of Zhang et al. [35], with some modifications. The fresh sample was homogenized in three different replicates (n = 3) of three trees per replica.
A tissue sample (1.0 g) was homogenized in a 10 mL solution of 10% trichloroacetic acid and subsequently centrifuged at 10,000× g for 10 min. Following centrifugation, 2 mL of the supernatant was combined with 6 mL of a 0.6% thiobarbituric acid solution for each duplicate and thoroughly mixed. The resulting test tubes were then subjected to a temperature of 95 °C for a duration of 20 min. Then, after cooling, they were left to temper at room temperature and measured using a spectrophotometer (1900 UV/Vis, Shimadzu, Kyoto, Japan) with absorbance measurements taken at 450, 532, and 600 nm. The calculation of MDA content was carried out according to previously established equations [35] and expressed as μmol kg−1 (n = 3).
The percentage of undamaged pistils was evaluated in 2022 and 2023 following the important impact of suboptimal temperatures on pistils of both cultivars at the full blossom stage (BBCH 65). One hundred flowers from each tree (taken from both tree sides) were individually checked to determine the presence of green pistils or if this tissue was affected by internal browning as a result of frost damage. Pistils affected by frost damage exhibited signs of necrosis or internal damage. The proportion of non-damaged flowers was expressed as a percentage. This percentage was obtained from three replicates of three trees (n = 3) and represents the proportion of flowers that could tolerate frosting conditions and potentially be functional.
Fruit set percentage was determined based on flower bud counts in four branch segments equally divided at both sides of the tree branches (n = 3). Flower buds that had not yet opened represented the flowers that could potentially develop into fruits and were carefully counted in each labeled branch during the last three years of this research (2021–2023). After the fruit set (BBCH 75) and before the fourth preharvest treatment (BBCH 77), the number of developed sweet cherries was counted. The percentage of fruit set was quantified as the ratio of mature sweet cherries to the previously reported number of flower buds within the corresponding branch segment.

2.3. Sweet Cherry Cracking Evaluation

In 2020, we conducted the assessment of sweet cherry cracking only at harvest. The COVID-19 pandemic circumstances did not allow the evaluation of fruit cracking during development. Subsequently, in the consecutive growing seasons of 2021, 2022, and 2023, we investigated the effect of putrescine treatments on sweet cherry cracking as the fruit developed through several ripening stages while still on the tree. The selection of these ripening stages was determined as follows: the ‘Prime Giant’ cultivar was coincident with the onset of color change (Stage 1), the appearance of pink color (Stage 2), bright red color (Stage 3), and dark red color (Stage 4). In the case of the ‘Sweetheart’ cultivar, the ripening stages at which sweet cherry cracking was studied corresponded to the stages of immature green-yellow color (Stage 1), the beginning of color change (Stage 2), pink color surface (Stage 3), bright red color (Stage 4), and dark red color (Stage 5). The evaluation of sweet cherry cracking on a tree was carried out on four specified branches of each tree, with 100 fruits evaluated for this disorder in each tree, and the results were reported as a percentage. Coincident with these measurements, we also assessed sweet cherry cracking in undamaged fruits with the traditional methodology described by different authors [21,36]. In this sense, each treatment batch comprised three replicates, each consisting of 50 fruits subjected to distilled water immersions simulating a heavy rainfall and expressed as a cracking index. In 2023, the ‘Prime Giant’ cultivar was not evaluated since it did not show any production after frost damage during early spring in this production cycle.

2.4. Fruit Quality Parameters at Harvest

The experiment was assayed across a four-year duration, covering the years 2020 to 2023. Sweet cherries were harvested at their respective commercial ripening stages, following commercial standards, which are primarily determined by the skin color of each different cultivar studied. Subsequently, for each replicate of 3 trees per treatment, sweet cherry lots were blended, and the resulting mixture was promptly transported to the laboratory. Then, at room temperature, three sets of 20 uniformly sized and colored fruits from each replicate and treatment in the field without apparent defects were chosen randomly. These sweet cherries were selected for the analytical assessments. Results were organized, displaying the effect of 1 mM concentration as the common and effective preharvest treatment throughout all seasons and cultivars under investigation, being also the lowest concentration assayed in this study.
For the evaluation of fruit firmness, each individual sweet cherry was measured using a TX-XT2i texture analyzer (Stable Microsystems, Godalming, UK) equipped with a flat plate probe. The descent rate of the disc was set at 20 mm min−1 until a 5% deformation was achieved. Fruit firmness was calculated as the ratio of the applied force to the distance traveled (N mm−1).
Color measurements were conducted individually for each fruit using a Minolta colorimeter (CR-C400, Konica Minolta Camera Co.; Kantō, Tokyo, Japan). Two measurements were taken for each fruit at two opposing and equidistant points in the equatorial zone. These measurements were expressed in terms of CIE hue* (arctg b*/a*) based on CIELab coordinates.
To evaluate the total soluble solids (TSS) and titratable acidity (TA), the flesh from 20 cherries in each replicate was homogenized to obtain a consistent sample, and approximately 50 g of this sample was passed through two layers of cotton cloth. The resulting juice was used for measurements of TSS and TA. Both parameters were evaluated in duplicate for each filtered juice extracted, as previously described [37], in each replicate per batch. TSS in sweet cherry juice was measured at 20 °C using an Atago PR-101 digital refractometer (Atago Co., Ltd., Tokyo, Japan), with results expressed as g per 100 g−1. TA was also determined in each sample per duplicate through automatic titration (785 DMP Titrino, Metrohm, Herisau, Switzerland) and reported as g of malic acid equivalents per 100 g−1.

2.5. Statistical Analysis

The experiments were conducted using a completely randomized design. Statistical analyses were performed using the SPSS package program, version 22 (IBM Corp., Armonk, NY, USA). During the 2020–2021 period, results were expressed as mean ± SE, and the data were subjected to analysis of variance (ANOVA). Mean comparisons were conducted using a multiple-range test (Tukey’s HSD test) to identify significant differences (p < 0.05) among treatments for the same sampling date. These differences were represented for treatments on the same sampling date using lowercase letters. For the 2022–2023 results, a one-way analysis of variance was employed, and the data are presented as mean  ±  standard error (n = 3). (*) indicates significant differences between putrescine-treated and control samples, determined through Student’s unpaired t-test; * p  <  0.05, ** p < 0.01.

3. Results and Discussion

3.1. Effect of Exogenous Putrescine on Sweet Cherry Frost Tolerance: MDA, Ovary Integrity, and Fruit Set

MDA is a recognized biomarker for oxidative stress, reflecting the peroxidation of plasma membranes and its direct association with the structural integrity of plant tissues [38]. The observed levels of MDA in flower buds treated with putrescine exhibited a significant decrease (p < 0.05) in MDA content compared to control flower buds for both studied cultivars (Figure 1).
Although there was no dose-dependent effect in the ‘Prime Giant’ cultivar (Figure 1A), this effect was indeed observed in the ‘Sweetheart’ cultivar (Figure 1B). In this cultivar, the 10 mM putrescine concentration exhibited a significantly (p < 0.05) greater impact on reducing MDA levels compared to the concentration tested (1 mM). In a previous study, the application of diverse preharvest concentrations of putrescine was observed to decrease the generation of hydrogen peroxide and enhance the antioxidant activity of citrus leaves exposed to frost stress [39]. Additionally, in both growing cycles studied (2021 and 2022), putrescine applications reduced MDA content, with the putrescine treatment having a similar effect in the 2021 growing season as compared to the 2022 results. The occurrence of spring frosts is linked to considerable stress, triggering the synthesis of oxidative radicals (ROS), as reported by Sachdev et al. [40]. Cold stress dramatically increases the generation of ROS, leading to the formation of highly active radicals such as MDA. These radicals have the potential to exert detrimental effects on cellular tissues [41]; hence, the variations in MDA content among different growing seasons could be directly associated with the abiotic conditions in each growing season. The observed reduction in MDA content in putrescine-treated trees may be associated with better control of the antioxidant balance in the evaluated tissues, as reported previously [25,26,27,28,29,30,31,32,33,34].
The impact of spring frosts on the reproductive organs of sweet cherries is frequently related to internal and external irregularities that disrupt the usual fruit development process. Indeed, sweet cherry flower buds affected by spring frosts typically display a browning of the pistil [42]. In this study, only important frost events occurred in 2022 and 2023 in periods close to the full bloom stage. Spring frost dramatically affected this species, compromising the whole production in this growing season. Probably because of the important effect on pistil browning (90–98%), we did not find significant differences (p > 0.05) related to the exogenous preharvest putrescine treatment applied in flower buds harvested in these two different cycles (2022 and 2023) (Figure 2).
Although a higher percentage (p > 0.05) of green pistils was observed in putrescine-treated pistils in 2023 (Figure 2C,D), the previous growing cycle displayed a contrary pattern (Figure 2A,B). It seems that the putrescine content in flower bud tissues is related to the developmental stages, showing reduced levels of polyamines in advanced stages of development, as has been reported in other species, such as in apricot ovaries [23]. According to the authors, this decreased level contrasts with the higher levels observed during the early stages of ovary and ovule development.
The fruit set in sweet cherry depends on a combination of factors related to pollination, nutrition factors, management practices, and weather conditions [43]. Fruit set is a promising start to the development of sweet cherry fruit, but in both cultivars, fruit set was reduced across the growing cycles studied (Figure 3). This reduced fruit set could be associated with adverse effects on flower organs during consecutive growing seasons, as reported previously in this study.
In terms of fruit set percentages, significant differences were not observed (p > 0.05) between putrescine-treated and control ‘Prime Giant’ trees in the first period study (2021) (Figure 3A). However, ‘Sweetheart’ trees displayed significant differences (p < 0.05) in fruit set percentages after preharvest treatments, with a 10 mM putrescine concentration showing a higher fruit set as compared to the rest of the batches (Figure 3B). In contrast, in the subsequent 2022 growing cycle, significant differences (p < 0.05) were observed in fruit set percentages for both cultivars when treated with 1 mM of putrescine. In this sense, an important increase in fruit set for both cultivars under these conditions was observed (Figure 3C,D). Nevertheless, the adverse effects of spring frost in 2023 significantly diminished the fruit set percentage in both cultivars, with a particularly pronounced impact on the ‘Prime Giant’ cultivar (Figure 3E). These findings emphasize the substantial variability observed in fruit set percentages across different growing seasons and cultivars, as reported in previous studies [35], which is a problem in commercial production. In sweet cherry cultivation, an inadequate fruit set represents a significant physiological issue triggered by climatic factors, which has a considerable impact on yield [35,44,45]. For sweet cherries, achieving a favorable fruit-setting ratio ranging between 25% and 40% is essential for optimal production [46]. This optimal fruit setting range was only reached in 2021 (Figure 3A,B). The increase in fruit set observed by putrescine has also been observed in other studies for different species [47] and has been related to improved ovule viability [23] and fruit retention on trees [48] in other fruit species, such as apricot and pear.

3.2. Effect of Exogenous Putrescine on Sweet Cherry Cracking during Ripening on Tree

The occurrence of cracking is a significant problem for sweet cherry producers, as it has the potential to produce notable economic losses. Once the fruit undergoes cracking, its susceptibility to pests and diseases is higher, diminishing its quality and market value [49]. The factors contributing to the different cracking tolerance among cultivars are still not clear. However, it is worth noting that localized occurrences like rain cracking exert a notable influence on sweet cherry cracking [50,51]. Regarding this factor, the ‘Sweetheart’ cultivar was not coincident with substantial rainfall between 2020 and 2022, as it is atypical for significant precipitation to occur across the month of July, which is the usual harvest time for this cultivar. In fact, the absence of heavy rainfall in 2022 during the on-tree development, when sweet cherries are most susceptible, played a critical role in preventing cracking disorders in both cultivars (Figure 4E,F).
In 2023, the impact of the spring frost (Figure 3E) affected the entire ‘Prime Giant’ production, but we had the opportunity to evaluate ‘Sweetheart’ trees (Figure 4G). During this growing season, heavy rainfalls coincided with the development of this cultivar, leading to a notably high incidence of cracking, displaying the highest rate of fruit cracking among the different cultivars and growing seasons studied. In contrast, this cultivar showed the lowest incidence as compared to ‘Prime Giant’ during the previous growing seasons, both exposed to uncontrolled weather conditions (Figure 4). All the preharvest treatments containing putrescine successfully decreased the incidence of cracking, though they did not exhibit a dose-dependent effect in general when the putrescine concentration was increased up to 10 mM (Figure 4A–D). In the ‘Prime Giant’ cultivar, reductions in cracking at harvest reached 68.5% and 56.2% as compared to control trees in 2020 and 2021, respectively (Figure 4A,C). However, this effect was even more pronounced at harvest with the ‘Sweetheart’ cultivar, where reductions in fruit cracking of 62.1%, 71.8%, and 64.2% were observed in 2020, 2021, and 2023, respectively (Figure 4B,D,G).
Considering the distinct fruit ripening stages during on-tree development in both cultivars and their correlation with sweet cherry cracking from 2021 to 2023, the highest levels of fruit cracking were observed after the S2 developmental stage, coinciding with color changes. Significant increases in fruit cracking were not observed beyond this phenological stage during the consecutive periods studied.
Fruit cracking is a multifactorial event, and for this reason, it is very difficult to determine the specific reasons affecting the different resistance levels among distinct cultivars [50]. However, rainfall emerges as a predominant factor in the complex equation of fruit cracking, with a clear effect related to the degree of fruit ripeness coinciding with rain events [6,52,53]. Our present findings showed a reduction in sweet cherry cracking after preharvest putrescine treatments during on-tree ripening, although the impact on cracking incidence exhibits divergent patterns among the cultivars we examined. Applying putrescine, synchronized with the pit hardening stage (prior to S1), was effective in reducing cracking in the ‘Prime Giant’ and ‘Sweetheart’ cultivars, coinciding with changes in fruit color during on-tree development (S1 for ‘Prime Giant’ and S2 for ‘Sweetheart’). On the other hand, our previous studies [6] demonstrated a strong correlation between sweet cherry fruit ripeness and susceptibility to abiotic stress conditions. In this context, the different efficacy of preharvest treatments against rain-induced cracking seems to be closely linked to the ripening stage [6,53]. Furthermore, the susceptibility to cracking appeared to be cultivar-dependent in the present study, which is consistent with earlier research findings [6,51] since cultivars with thinner skin are generally more susceptible to cracking compared to those with thicker skin.
Winkler et al. [52] have proposed that the occurrence of rain-induced cracking should not be mostly attributed to excessive water absorption through the tree roots. Instead, it appears to be triggered mainly by the time of contact with liquid water on the fruit skin. These findings elucidated the clear connection between rain cracking and the overall water balance of the fruit. For this reason, as fruit cracking on the tree appears to be directly influenced by various weather factors that can act synergistically under uncontrolled field conditions, we employed the immersion method [21,36] to evaluate the susceptibility of different cultivars at different ripening stages. In this sense, when healthy sweet cherries were exposed to water immersions, both cultivars showed a lower resilience to fruit cracking under controlled conditions (Figure 5) as compared to the cracking results obtained under weather conditions (Figure 4). However, on-tree cracking evaluations and cracking induced by immersions showed a similar pattern between them. The ‘Prime Giant’ cultivar exhibited the highest incidence of sweet cherry cracking in 2020 (Figure 5A) at the harvest stage. Notably, the application of putrescine (1 mM) resulted in a significant reduction (p < 0.05) in fruit cracking for both cultivars. Our results highlight the most pronounced effect in the ‘Prime Giant’ cultivar in 2022 and the ‘Sweetheart’ cultivar in 2020, 2021, and 2022, demonstrating the highest reduction in fruit cracking (around 75% in all these growing cycles) as compared to control fruit at the time of harvest (Figure 5B,D–F). There are no studies examining the effects of putrescine on the occurrence of sweet cherry cracking at harvest or during development. However, a similar effect was observed when it was evaluated on different fruit species as a preharvest treatment. In this sense, putrescine was able to reduce fruit cracking at harvest in litchi [54], and fruit drop in peach [55] increased fruit yield, as also observed in table grapes [56].
It is worth noting that the ‘Sweetheart’ and ‘Prime Giant’ trees displayed a similar susceptibility to fruit cracking on trees in both cultivars. However, in practice, this equivalence is not frequently observed, primarily since ‘Prime Giant’ ripening starts earlier than ‘Sweetheart,’ thus more advanced ripening stages in ‘Prime Giant’ are coincident with the spring rainfall period. In this sense, immersion studies (Figure 5) have also allowed us to confirm that in both cultivars, sensitivity to cracking was similar, reaching its maximum at the beginning of the color changes in coincidence with the cracking counts on-tree (Figure 4). In the ‘Sweetheart’ cultivar, the earliest ripening stages (S1 and S2) or the most advanced ripening stages (S5) exhibit greater tolerance compared to ripening stages S3 or S4, in which the fruit adopts a uniform reddish color. However, in ‘Prime Giant’, resilience to fruit cracking remains similar after color changes during ripening on-tree (S1–S4). This observation matched our previous findings conducted on these same cultivars [6]. Consequently, controlled conditions through immersions in distilled water revealed that early and late stages of ripening exhibited reduced susceptibility to cracking in ‘Sweetheart’. Coincidently, Faizy et al. [53] also did not observe a significantly higher cracking in control fruit after delaying harvest for a week in the ‘0900 Ziraat’ cultivar.
In the ‘Prime Giant’ cultivar, the effects of putrescine preharvest treatments on fruit cracking were quite effective. In 2021, the 1 mM putrescine treatments resulted in a significant reduction of 50.5% and 33.5% in fruit cracking for the S1 and S2 ripening stages, respectively (Figure 5C). However, the treatments showed even greater effectiveness in 2022, with cracking reduced by 85.2% for the S1 stage and 86.04% for the S2 stage (Figure 5E). On the other hand, in the ‘Sweetheart’ cultivar, the putrescine treatments also demonstrated their effectiveness in 2021, leading to a 52.1% reduction in fruit cracking for the S3 stage and a 46.81% reduction for the S4 stage (Figure 5D). The following year, in 2022, the effectiveness of these treatments became even more pronounced, resulting in a remarkable 83.34% reduction in fruit cracking for the S3 stage and a 52.63% reduction for the S4 stage (Figure 5F). Hence, the impact of putrescine on reducing cracking was positive for both cultivars across consecutive growing seasons and ripening stages in this research.
It is important to highlight that the fruit’s ripeness level, which may coincide with environmental stress factors such as heavy rainfalls during its maturation on the tree, will change from year to year. This fact is highly significant because, during cherry ripening, several intrinsic attributes undergo changes, such as fruit firmness, TSS, and the volume of the fruit [57]. These attributes are closely related to susceptibility to sweet cherry cracking [4,19,58]. For this reason, differences in ethylene production on-tree [5] and the level of firmness [21], along with reduced levels of soluble solids and acidity, may play a role in diminishing the fruit’s vulnerability to cracking [59]. Sweet cherries tend to experience a lower occurrence of cracking when parenchyma cells in the epidermis and the hypodermis undergo an enlargement process during the later stages of ripening. This highlights the importance of the flexibility and integrity of the fruit skin to mitigate fruit cracking [4,60]. Consequently, the delayed fruit ripening will also impact the cracking incidence of sweet cherries, especially under the influence of persistent rainfalls, and may also be postponed. Furthermore, the vulnerability to cracking in sweet cherries is highly cultivar-dependent [51], and the impact of putrescine fruit quality parameters can be dependent on agronomical practices, weather conditions, species, and cultivars [22,52], and the number of applications. In this context, a comparable effect of putrescine was observed with four putrescine applications in both the 2020 and 2021 growing seasons and with three on-tree applications in 2022 and 2023.

3.3. Effect of the Preharvest Treatment with Putrescine on the Sweet Cherry Quality at Harvest

In the present study, different quality attributes were positively affected after putrescine preharvest treatments. In this regard, putrescine delayed on-tree fruit firmness evolution in both Prime Giant and Sweetheart cultivars across all growing seasons, displaying higher values at harvest across four consecutive growing cycles. However, statistical significance (p < 0.05) was observed only in specific periods evaluated (Table 1).
In 2021, there was a significant delay (p < 0.05) in fruit firmness at harvest in different growing seasons for ‘Prime Giant’ and ‘Sweetheart’ cultivars and in 2023 also for ‘Sweetheart’. These findings were also reported in plums with a suppressed-climacteric genotype, such as the ‘Golden Japan’ plum, and in non-climacteric fruit, such as table grapes [27,31]. In these studies, similar concentrations of putrescine (1 and 3 mM) demonstrated greater efficacy as compared to lower concentrations (0.1 mM). In different climacteric fruits, such as ‘Angelino’ plums, jujube, and pear fruit [30,32,33], higher fruit firmness was reported in putrescine-treated fruit after preharvest treatments with similar concentrations (1–3) mM than the concentration applied in the present research study. Conversely, postharvest treatments with putrescine have demonstrated efficacy in delaying fruit firmness in various fruit species, including lemons, apricots, and plums, during cold storage [24]. The enhancement of firmness due to polyamines was attributed to their effect in cross-linking pectic molecules within the cell wall. This cross-linking process leads to an immediate solidification, as observed during postharvest storage [61], providing an inhibitory effect on wall-degrading enzymes. Additionally, polyamines maintain cell bio-membranes, protecting phospholipids and proteins from peroxidation [62]. This inhibition serves to mitigate fruit softening during storage, as documented by different authors [24,61,63].
As with fruit firmness, color development was significantly delayed (p < 0.05) in the ‘Prime Giant’ cultivar at harvest time in the 2020 and 2021 seasons. In mango, ‘Golden Japan’ plum, and jujube fruit [29,31,32], the preharvest putrescine effect displayed a delayed color at harvest, which was related to a delayed chlorophyll senescence. In fact, putrescine has been related to the maintenance of thylakoid membranes through the storage period [64]. The observed delay in color development has been noted not only at harvest time but also at postharvest in different fruit species, also increasing cold tolerance against chilling injury [26,65]. However, this delayed pattern of color evolution was not observed (p > 0.05) in the ‘Sweetheart’ cultivar. In a previous study, Mirdheghan and Rahimi [27] observed the same discrepancy between two different table grape cultivars after preharvest putrescine treatments. It seems that color could play a dynamic effect related to the cultivar studied, and for this reason, this effect deserves further investigation across other sweet cherry cultivars.
The preharvest treatment with 1 mM putrescine did not lead to a significant impact (p > 0.05) on the ‘Prime Giant’ cultivar at harvest concerning sugar accumulation and TA content as compared to control batches. However, a significant effect (p < 0.05) was observed for the ‘Sweetheart’ cultivar, resulting in a delay in TSS accumulation in putrescine-treated batches during two different growing seasons (2020 and 2023). On the other hand, no effect on delaying sugar accumulation at harvest was noted in 2021 and 2022 for this cultivar. Furthermore, the efficacy of putrescine in maintaining higher and significant (p < 0.05) TA levels (≈10%) in contrast with control fruit at harvest in most of the growing seasons studied for the ‘Sweetheart’ cultivar. In table grapes, 1 mM putrescine concentrations delayed sugar accumulation at harvest for the ‘Rishbaba’ cultivar, although not significantly in the ‘Olhoghi’ cultivar [27]. Nevertheless, a higher concentration (2 mM) effectively delayed ripening at harvest in both table grape cultivars, delaying sugar accumulation and with higher TA as compared to control batches. On the contrary, higher TSS accumulation after preharvest putrescine treatments was observed in peaches [66]. With respect to TA levels, Shanbehpour et al., [32] did not find any putrescine-related effect in this parameter in different jujube fruit genotypes, although a higher ascorbic acid level was reported in putrescine-treated batches. Additionally, though the putrescine effect at 1 mM or 2 mM was weak at harvest in different table grape cultivars and in pear fruit [27,33], delayed TSS and TA evolution during postharvest storage was evident in most of the reported studies [27,29,30,32,33,66]. Fruits treated with polyamines have exhibited an elevated starch content attributed to a lower starch hydrolysis to sugar and a reduced respiration maintaining organic acid content [26,32,66]. The observed differences among authors, genotypes, and applied concentrations could result from variations in the number of applications during sweet cherry ripening on trees, the ripening stage at harvest, and a cultivar-dependent effect in the mentioned studies.

4. Conclusions

Preharvest treatments with putrescine could effectively enhance frost tolerance, mitigating stress and consequently increasing fruit set in both ‘Prime Giant’ and ‘Sweetheart’ cultivars. This naturally occurring compound increased frost tolerance, reducing MDA content and increasing fruit set, also reducing fruit cracking during preharvest and at harvest. Earlier ripening stages and medium ripening stages during preharvest were found to be more susceptible to the occurrence of fruit cracking in ‘Prime Giant’ and ‘Sweetheart’, respectively. Furthermore, putrescine preharvest treatments delayed fruit ripening on the tree, resulting in higher fruit firmness and delayed color development at harvest. The content of soluble solids and acidity at harvest time was only delayed in the ‘Sweetheart’ cultivar following putrescine treatments. The overall results suggest that putrescine preharvest treatments could serve as a valuable tool to mitigate production losses, reducing the impact of weather-related stress on trees during fruit evolution. Additionally, it contributes to enhancing fruit quality at harvest.

Author Contributions

Conceptualization, F.G.; methodology, J.M.V., A.B., A.C.-A. and F.G.; software, J.M.V. and M.C.R.-A.; validation, M.C.R.-A., J.M.V. and F.G.; formal analysis, M.C.R.-A., J.M.V. and F.G.; investigation, M.C.R.-A., J.M.V., A.B., A.C.-A., J.M.L.-M., M.N.-A. and F.G.; data curation, M.C.R.-A., J.M.V., J.M.L.-M., M.N.-A. and F.G. writing—original draft preparation, M.C.R.-A.; writing—review and editing, J.M.V. and F.G.; visualization, M.C.R.-A., J.M.V. and F.G. supervision, J.M.V., A.B. and F.G.; funding acquisition, J.M.V., A.B. and F.G., project administration: A.B. and F.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Centro para el Desarrollo Tecnológico Industrial (CDTI) of the Ministry of Industry under project number IDI-20200835 (2020–2022). In 2023, this research was funded by Conselleria d’Innovació, Universitats, Ciència i Societat Digital (Generalitat Valenciana) through the Prometeo Program (PROMETEO/2021/089).

Data Availability Statement

The original contributions presented in the study are included in the article. Further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. (A,C) MDA content (µmol kg−1) in ‘Prime Giant’ and (B,D) ‘Sweetheart’ cultivars in flower buds treated with putrescine (1 and 10 mM) and control samples evaluated in 2021 and 2022. Data are the mean ± standard error (n = 3). In 2021, different lowercase letters indicate significant differences (p < 0.05) among treatments for each cultivar. In 2022 study, (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p < 0.05).
Figure 1. (A,C) MDA content (µmol kg−1) in ‘Prime Giant’ and (B,D) ‘Sweetheart’ cultivars in flower buds treated with putrescine (1 and 10 mM) and control samples evaluated in 2021 and 2022. Data are the mean ± standard error (n = 3). In 2021, different lowercase letters indicate significant differences (p < 0.05) among treatments for each cultivar. In 2022 study, (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p < 0.05).
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Figure 2. (A,C) Percentage of green pistils in ‘Prime Giant’ and (B,D) ‘Sweetheart’ cultivars in flower buds treated with putrescine (1 mM) and control samples evaluated in 2022 and 2023. (Student’s unpaired t-test; NS: non-significant differences between putrescine-treated and control samples for each studied cultivar).
Figure 2. (A,C) Percentage of green pistils in ‘Prime Giant’ and (B,D) ‘Sweetheart’ cultivars in flower buds treated with putrescine (1 mM) and control samples evaluated in 2022 and 2023. (Student’s unpaired t-test; NS: non-significant differences between putrescine-treated and control samples for each studied cultivar).
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Figure 3. (A,C,E) Fruit set percentage in ‘Prime Giant’ and (B,D,F) ‘Sweetheart’ cultivars in fruit treated with putrescine (1 and 10 mM) and control samples evaluated in 2021, 2022, and 2023. In 2021, different lowercase letters indicate significant differences (p < 0.05) among treatments for each cultivar. In 2022 and 2023. (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p  <  0.05, ** p <  0.01, NS: non-significant).
Figure 3. (A,C,E) Fruit set percentage in ‘Prime Giant’ and (B,D,F) ‘Sweetheart’ cultivars in fruit treated with putrescine (1 and 10 mM) and control samples evaluated in 2021, 2022, and 2023. In 2021, different lowercase letters indicate significant differences (p < 0.05) among treatments for each cultivar. In 2022 and 2023. (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p  <  0.05, ** p <  0.01, NS: non-significant).
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Figure 4. (A,C,E) Cracking incidence during development on tree (%) in ‘Prime Giant’ and (B,D,F,G) ‘Sweetheart’ cultivars in fruits treated with putrescine (1 and 10 mM) and control samples evaluated between 2020 and 2023. Data are the mean  ±  standard error (n = 3). In 2020 and 2021, different lowercase letters indicate significant differences (p < 0.05) among treatments for each cultivar. In 2022 and 2023, (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p  <  0.05, ** p <  0.01, NS: non-significant).
Figure 4. (A,C,E) Cracking incidence during development on tree (%) in ‘Prime Giant’ and (B,D,F,G) ‘Sweetheart’ cultivars in fruits treated with putrescine (1 and 10 mM) and control samples evaluated between 2020 and 2023. Data are the mean  ±  standard error (n = 3). In 2020 and 2021, different lowercase letters indicate significant differences (p < 0.05) among treatments for each cultivar. In 2022 and 2023, (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p  <  0.05, ** p <  0.01, NS: non-significant).
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Figure 5. (A,C,E) Christensen index during development on tree in ‘Prime Giant’ and (B,D,F,G) ‘Sweetheart’ cultivars in fruit treated with putrescine (1 and 10 mM) and control samples evaluated between 2020 and 2023. Data are the mean  ±  standard error (n = 3). In 2020 and 2021, different lowercase letters indicate significant differences (p < 0.05) among treatments for each cultivar. In 2022 and 2023, (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p  <  0.05, ** p <  0.01, NS: non-significant).
Figure 5. (A,C,E) Christensen index during development on tree in ‘Prime Giant’ and (B,D,F,G) ‘Sweetheart’ cultivars in fruit treated with putrescine (1 and 10 mM) and control samples evaluated between 2020 and 2023. Data are the mean  ±  standard error (n = 3). In 2020 and 2021, different lowercase letters indicate significant differences (p < 0.05) among treatments for each cultivar. In 2022 and 2023, (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p  <  0.05, ** p <  0.01, NS: non-significant).
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Table 1. The effect of the preharvest treatment with putrescine 1 mM on the physical and chemical quality of sweet cherries at harvest.
Table 1. The effect of the preharvest treatment with putrescine 1 mM on the physical and chemical quality of sweet cherries at harvest.
Fruit Firmness (N mm−1)
CultivarYearControlPut 1 mM
‘Prime Giant’20201.82 ± 0.091.88 ± 0.09 NS
‘Prime Giant’20211.51 ± 0.071.66 ± 0.09 *
‘Prime Giant’20221.18 ± 0.051.20 ± 0.06 NS
‘Sweetheart’20202.08 ± 0.102.09 ± 0.10 NS
‘Sweetheart’20211.78 ± 0.092.03 ± 0.04 *
‘Sweetheart’20221.69 ± 0.071.80 ± 0.09 NS
‘Sweetheart’20231.89 ± 0.052.20 ± 0.09 *
Fruit color (CIE h°)
CultivarYearControlPut 1 mM
‘Prime Giant’202021.15 ± 0.8023.29 ± 0.97 *
‘Prime Giant’202113.36 ± 0.3015.66 ± 0.34 **
‘Prime Giant’202223.37 ± 0.3122.91 ± 0.43 NS
‘Sweetheart’202017.57 ± 0.5818.63 ± 0.91 NS
‘Sweetheart’202120.65 ± 0.1920.37 ± 0.16 NS
‘Sweetheart’202219.27 ± 0.2518.77 ± 0.35 NS
‘Sweetheart’202319.22 ± 0.4718.48 ± 0.56 NS
Total soluble solids (g 100 g−1)
CultivarYearControlPut 1 mM
‘Prime Giant’202018.45 ± 0.1218.18 ± 0.34 NS
‘Prime Giant’202117.76 ± 0.1818.20 ± 0.54 NS
‘Prime Giant’202222.75 ± 0.4123.01 ± 0.59 NS
‘Sweetheart’202022.42 ± 0.0721.80 ± 0.23 *
‘Sweetheart’202118.90 ± 0.1619.26 ± 0.29 NS
‘Sweetheart’202222.65 ± 0.4423.07 ± 0.11 NS
‘Sweetheart’202321.56 ± 0.2021.08 ± 0.04 *
Titratable acidity (g 100 g−1)
CultivarYearControlPut 1 mM
‘Prime Giant’20201.00 ± 0.041.07 ± 0.06 NS
‘Prime Giant’20211.09 ± 0.011.10 ± 0.01 NS
‘Prime Giant’20221.58 ± 0.011.53 ± 0.02 NS
‘Sweetheart’20201.22 ± 0.021.36 ± 0.02 *
‘Sweetheart’20211.33 ± 0.021.43 ± 0.02 *
‘Sweetheart’20221.44 ± 0.031.60 ± 0.08 *
‘Sweetheart’20231.98 ± 0.081.89 ± 0.09 NS
Data are the mean ± standard error (n = 3). (*) indicates significant differences between putrescine-treated and control samples for each studied cultivar (Student’s unpaired t-test; * p < 0.05, ** p < 0.01, NS: non-significant).
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Ruiz-Aracil, M.C.; Valverde, J.M.; Beltrà, A.; Carrión-Antolí, A.; Lorente-Mento, J.M.; Nicolás-Almansa, M.; Guillén, F. Putrescine Increases Frost Tolerance and Effectively Mitigates Sweet Cherry (Prunus avium L.) Cracking: A Study of Four Different Growing Cycles. Agronomy 2024, 14, 23. https://doi.org/10.3390/agronomy14010023

AMA Style

Ruiz-Aracil MC, Valverde JM, Beltrà A, Carrión-Antolí A, Lorente-Mento JM, Nicolás-Almansa M, Guillén F. Putrescine Increases Frost Tolerance and Effectively Mitigates Sweet Cherry (Prunus avium L.) Cracking: A Study of Four Different Growing Cycles. Agronomy. 2024; 14(1):23. https://doi.org/10.3390/agronomy14010023

Chicago/Turabian Style

Ruiz-Aracil, María Celeste, Juan Miguel Valverde, Aleixandre Beltrà, Alberto Carrión-Antolí, José Manuel Lorente-Mento, Marta Nicolás-Almansa, and Fabián Guillén. 2024. "Putrescine Increases Frost Tolerance and Effectively Mitigates Sweet Cherry (Prunus avium L.) Cracking: A Study of Four Different Growing Cycles" Agronomy 14, no. 1: 23. https://doi.org/10.3390/agronomy14010023

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