Current IssueEditorial BoardOnline First ArticlesArchive
Current IssueEditorial BoardOnline First ArticlesArchive

Review Article

Complex Analysis of Physiological, Biochemical and Molecular Mechanisms of Drought Adaptation in Apple (Malus domestica Borkh.)

F
Farhod Abdurasulov1
S
Sherzod Rajametov2
A
Alisher Botirov3,*
S
Shukhrat Abdurasulov4
J
Jaloliddin Shavkiev5
1Academician Makhmud Mirzayev Scientific Research Institute of Horticulture, Viticulture, and Winemaking.
2Coordinator of the World Bank Project “Livestock Sector Development-Phase II”.
3Faculty of Economics, Forestry and veterinary Medicine, Termez State University of Engineering and Agrotechnology, Surkhandarya 190100, Uzbekistan.
4Tashkent State Agrarian University.
5Institute of Genetics and Experimental Plant Biology, Academy of Sciences of the Republic of Uzbekistan.

ABSTRACT

Drought is one of the most critical abiotic stresses limiting apple (Malus domestica Borkh.) growth, productivity and fruit quality worldwide. Understanding the complex physiological, biochemical and molecular mechanisms underlying drought tolerance is essential for developing stress-resilient cultivars. The present review highlights integrated responses of apple varieties to drought stress, focusing on water relations, gas exchange, osmotic regulation, antioxidant defense and hormonal signaling. Physiologically, drought-tolerant genotypes maintain higher relative water content, stomatal conductance and water-use efficiency. Biochemically, accumulation of osmolytes (proline, soluble sugars, glycine betaine) and enhanced activity of antioxidant enzymes (SOD, CAT, POD, APX) mitigate oxidative damage. Molecular mechanisms involve activation of drought-responsive transcription factors (AREB/ABF, DREB, NAC, MYB), signal transduction through ABA pathways and upregulation of stress-protective genes. Integration of these responses enables better nutrient and water uptake, osmotic adjustment and improved photosynthetic performance under water deficit. Future research should focus on genome editing, marker-assisted selection and omics-based approaches to accelerate the breeding of drought-resilient apple cultivars.

INTRODUCTION

Apple (Malus x  domestica Borkh.) is one of the most widely cultivated and economically important fruit crops globally, valued for its nutritional content, industrial use and contribution of over 73 billion USD to the global economy (FAOSTAT, 2020). In Uzbekistan, apple is the leading fruit crop, where intensive production largely relies on high-yielding commercial cultivars. However, these modern varieties often lack adaptability to local environmental stresses.
       
Due to global climate change, decreasing water availability, unpredictable rainfall patterns and rising temperatures pose serious threats to agricultural systems worldwide. Among fruit trees, apple (Malus x domestica Borkh.) is particularly vulnerable to drought stress, which adversely affects not only vegetative growth but also fruit yield and quality. In drought-prone regions, such as the Mediterranean, Central Asia and parts of Uzbekistan, these stresses directly impact the economic viability and sustainability of apple production.
       
Identifying drought-tolerant cultivars and rootstocks and understanding their physiological and molecular mechanisms of stress response, is therefore of both scientific and practical significance. Such knowledge enables the development of resilient apple varieties better adapted to climate change, while also supporting improved agronomic practices and resource-efficient production systems. In Uzbekistan-where apples are the most cultivated fruit and water scarcity is an increasing concern-the preservation and study of traditional apple germplasm offer a promising avenue. These varieties, often naturally adapted to local environmental conditions, can serve as valuable genetic resources for breeding drought-tolerant, high-quality cultivars.
       
This research provides an essential foundation for modern breeding strategies by elucidating the physiological, biochemical and genetic basis of drought tolerance in apples. The findings have the potential to contribute significantly to sustainable fruit production and food security in water-limited environments.
       
Due to climate change, apple production faces increasing threats from abiotic stress factors such as drought, extreme heat and salinity. These stressors negatively affect physiological and molecular processes, including photosynthesis, stomatal conductance and oxidative balance, ultimately reducing fruit yield and quality (Berger et al., 2016; Pérez  et al., 2008). As agriculture consumes over 70% of the world’s freshwater, the need for drought-resilient cultivars is more urgent than ever.
       
Traditional apple cultivars, though underutilized, are better adapted to local conditions and often show enhanced resistance to environmental stresses. They contain higher levels of bioactive compounds and demonstrate stable performance under drought (Donno et al., 2012; Cvetković et al., 2012). Therefore, understanding and utilizing their genetic potential is critical for future breeding strategies.
       
This study aims to comprehensively examine the physiological, biochemical and molecular responses of apple plants to drought stress. Special focus is given to identifying drought-responsive genes and pathways that contribute to improved stress adaptation. The findings will provide a basis for developing high-performing, drought-tolerant apple varieties to ensure sustainable production in a changing climate.
 
The effect of drought stress on the physiological, biochemical and molecular mechanisms of apple plants
 
Drought is a major limiting factor in crop production. Due to increasing global temperatures and limited water resources, drought has become a global issue threatening future crop production (Zhao et al., 2020, Botirov et al., 2021). Naturally, plants have developed multiple molecular and physiological mechanisms to withstand stress. Drought activates key regulatory genes that control physiological processes such as stomatal closure (Taiz et al., 2002) and detoxification of reactive oxygen species (ROS) (Sun et al., 2018; Chen et al., 2019). Additionally, heat and drought conditions generate ROS, leading to membrane damage and oxidative stress.
       
Recent studies published in ARCC journals have high-lighted the importance of integrating physiological, biochemical and molecular approaches for improving drought tolerance in horticultural crops. These studies emphasize the role of antioxidant systems, transcription factors and stress signaling networks in enhancing plant resilience under water deficit conditions, which is essential for developing climate-resilient fruit production systems (Kumar et al., 2021; Singh et al., 2020; Patel et al., 2019; Sharma et al., 2022).
       
Water deficiency in plants induces oxidative stress (Lei et al., 2006; Noctor et al., 2014), including excessive production of reactive oxygen species such as superoxide radicals (O2-) and hydrogen peroxide (H2O2) resulting in lipid peroxidation and damage to membranes, proteins, chlorophyll, nucleic acids and ultimately cell death (Scandalios, 1993). Drought can significantly reduce photosyn- thesis and cause chlorophyll degradation (Viljevac et al., 2013; Bhusal et al., 2019). According to Chaves et al., (2002), the negative effects of drought on plant physiology depend on the intensity and duration of the drought stress as well as the plant’s ability to adapt and survive under such conditions.
       
To withstand drought stress and protect against oxidative damage, plants have developed antioxidant defense mechanisms, including antioxidant enzymes such as peroxidase (POD), superoxide dismutase (SOD), catalase (CAT) and non-enzymatic antioxidants such as phenolic compounds, ascorbic acid, glutathione and carotenoids (Asensi., 2010; Farooq et al., 2012). Some plants accumulate osmolytes like proline, glycine betaine and soluble sugars to protect themselves and mitigate drought stress (Shehab et al., 2010; Xu et al., 2018; Dien et al., 2019). Recent studies have shown that certain plant organ compounds like terpenes (Mahdavi et al., 2020) and phytohormones like brassinolide (Naservafaei et al., 2021) can alleviate drought effects by enhancing the plant’s defense systems.
       
Chlorophylls, as the main photosynthetic pigments in plant leaves, reflect the photosynthetic capacity and overall vitality of plants. The chlorophyll content in leaves is considered a good indicator of stress tolerance in various crops, including drought tolerance (Arunyanark et al., 2008). Previous studies have documented that drought stress negatively affects chlorophyll accumulation in apple rootstock cuttings (Alizadeh et al., 2011; Bolat et al., 2014). Under drought conditions, a decrease in chlorophyll content has been observed in plants, with a greater decrease recorded in the commercial cultivar ‘Golden Delicious Reinders’ compared to ‘Crvenka’ (Mihaljevic et al., 2021). These results are consistent with observations by Bhusal et al., (2019), where a smaller decrease in total chlorophyll content was found in the drought-tolerant ‘Fuji’ apple compared to the ‘Hongro’ apple.
       
Carotenoids play an essential role in photosynthesis, as they protect photosystem II from photooxidative damage (Cogdell and Gardiner, 1993). Khoyerdi et al., (2016) reported that high carotenoid content in pistachio cultivars leads to greater drought tolerance.
       
Under drought conditions, the decline in photosystem II activity is associated with oxidative stress and cell membrane damage caused by increased lipid peroxidation (Benhassaine et al., 2002). Malondialdehyde (MDA) is a product of lipid peroxidation and is commonly used to assess oxidative stress during drought (Farooq et al., 2010). Various abiotic stresses, including drought, induce the generation of ROS such as H2O2 which damages membrane lipids (Kocsy et al., 2005). Our findings indicate that higher MDA concentrations under drought stress are associated with elevated H2O2 levels in plants. During drought stress, significant increases in MDA and H2O2  contents were observed in both the ‘Golden Delicious Reinders’ and ‘Dugara’ cultivars, indicating oxidative damage in both. As the intensity of stress increased, so did the levels of H2O2 and consequently MDA. Møller  et al. (2007) suggested that higher MDA levels indicate more severe oxidative damage.
       
In our study, the commercial ‘Golden Delicious Reinders’ cultivar exhibited a faster increase in MDA and H2O2  concentrations compared to the traditional ‘Dugara’ cultivar and significant early-stage changes in H2O2  suggest that ‘Dugara’ is more drought-tolerant. Several researchers have reported increased MDA and H2O2  levels under drought stress in plants (Petridis et al., 2012; Yang and Miao., 2010). In the traditional ‘Crvenka’ cultivar, MDA content remained stable under drought, while H2O2  levels decreased after 12 days of drought, consistent with earlier findings (Umar and Shaheed., 2018), suggesting that reduced H2O2 production is likely associated with increased antioxidant enzyme activities, particularly CAT.
       
Leaf water content (WC) is an indicator of plant water status and is used to evaluate drought tolerance (Bandurska and Joswiak., 2010). After 12 days of stress, a significant decrease in leaf water content in response to drought stress was observed only in the ‘Golden Delicious Reinders’ cultivar, which had the lowest photosynthetic efficiency. In contrast, the traditional cultivars maintained better photosynthetic efficiency and stable water content. Similarly, Tounekti et al., (2018) found that a drought-tolerant coffee cultivar exhibited higher water content along with better photosynthetic efficiency under drought conditions. These observations, confirmed by photochemical parameters, highlight the better drought tolerance of traditional cultivars.
       
Proline is an important organic osmolyte that accumulates and increases under drought conditions and also acts as a ROS scavenger (Sumera and Asghari, 2010; Liang et al., 2013). Numerous previous studies have reported higher proline accumulation in drought-tolerant plants (Anjum et al., 2016; Man et al., 2011). However, our results showed that proline measurement was not a reliable screening method for determining drought tolerance in the studied apple cultivars. The proline content in the drought-tolerant ‘Crvenka’ was not higher than that in the drought-sensitive ‘Golden Delicious Reinders. The lower proline accumulation in ‘Crvenka’ may suggest the activation of other drought defense mechanisms. Rampino et al., (2006) also reported that drought-tolerant wheat plants exhibited higher relative water content (RWC) and lower proline accumulation.
       
Plant phenolic compounds are secondary metabolites that serve as antioxidants and have been described as indicators of abiotic stress tolerance in plants (Blokhina et al., 2003; Quan et al., 2016). Hura et al., (2009) found that in triticale plants, higher phenolic content was associated with better photosynthetic activity. However, this does not align with our findings, as the total phenolic content accumulated in the leaves of the studied apple cultivars was highly variable, with the highest phenolic content observed in the commercial cultivar “Golden Delicious Reinders.” These results suggest that phenolic compounds may not play a major role in the defense responses of the studied apple cultivars. Similarly, Puente-garza and colleagues reported that total phenolic content was not correlated with antioxidant activity in Agave plants.
       
Although we hypothesized that higher concentrations of proline and secondary metabolites (phenolics) would improve osmotic adjustment and drought tolerance, this hypothesis was not supported. This likely indicates that antioxidant enzyme systems were activated as a protective mechanism in this study. According to Mihaljevic et al., (2021), there are significant differences among cultivars in their physiological and biochemical responses to drought stress. The most drought-tolerant cultivars showed high photosynthetic efficiency, high chlorophyll content and strong membrane stability, whereas the commercial cultivar “Golden Delicious Reinders” was found to be the most sensitive under the studied conditions. The good quality traits of “Crvenka” (Jakobek et al., 2020) and its high drought tolerance make it a promising cultivar for cultivation under dry conditions in the region. These cultivars could be used to update the production assortment and support the development of fruit cultivation. Preserving traditional cultivars is also important for maintaining genetic material for breeding purposes; therefore, the results of this study could provide valuable information for future breeding programs.
       
Plants have developed morphological, physiological and molecular resistance mechanisms in response to abiotic stress. Among these molecular mechanisms are the regulation of gene expression through transcription factors (TFs) and the roles of specific functional genes. NAC genes are plant-specific transcription factors that influence plant growth and development and participate in the transcriptional regulation of responses to various abiotic stresses such as drought, salinity, cold and pathogen infection (Sun et al., 2012; Tak et al., 2017). Members of the NAC gene family are differentially expressed in response to abiotic stress.
       
Here, we isolated the MdNAC29 gene, a NAC transcription factor, from apples. Our results showed that MdNAC29 is localized in the nucleus and responds to drought stress. Overexpression of MdNAC29 was found to negatively regulate drought tolerance in transgenic apple plants, callus and tobacco plants.
       
Moreover, genes such as MdERD5, MdRD22, MdRD29A, MdAREB1, MdDREB2A and MdMYB46 have been reported to be extensively involved in improving drought tolerance in plants (An et al., 2018; Chen et al., 2019; Li et al., 2022; Liu et al., 2022). We hypothesize that MdNAC29 regulates the expression of these drought-responsive genes. qRT-PCR results showed that the overexpression of MdNAC29 significantly downregulated the expression of these genes in apple trees.
       
Drought in apple trees is generally understood as a persistent water deficit due to an imbalance between water supply and demand or a low water budget throughout the growth cycle. This leads to leaf wilting, yellowing and premature leaf drop, as well as early fruit ripening and fruit drop (Yang et al., 2021). In apple trees, drought stress can temporarily inhibit shoot growth due to reduced leaf area, stomatal closure and disruption of the plant’s carbon balance caused by hydraulic failure (Lauri et al., 2016). During hot summer months, drought stress, often combined with heat stress, can cause leaf scorch. Frequent drought stress events caused by dry weather conditions resulting from global warming have significantly reduced apple yield and quality (Aras and Keles., 2019). Therefore, apple trees must sense soil water availability and activate appropriate molecular stress responses to survive under such conditions.
       
Research has shown that one of the key genes involved in improving drought tolerance in apple trees is MdDREB2A. Overexpression of this gene activates stress-responsive genes under stress conditions, thereby enhancing drought tolerance. Furthermore, other transcription factor families, such as NAC, MYB and ERF, also participate in forming drought adaptation responses, but many studies particularly emphasize the importance of MdDREB2A. To date, many genes from the APETALA2/ethylene-responsive factor (AP2/ERF), ZFP, bHLH, MYB and NAC families have been identified and characterized for their roles in apple drought responses (Fig 1).

Fig 1: Effects of drought on apple (Malus domestica Borkh.): physiological, biochemical and molecular responses.


       
In the study by Sun et al., (2018), overexpression of the MdATG18a gene in apple trees enhanced their drought tolerance. These processes help degrade aggregated proteins and limit oxidative damage. Another important agricultural practice to improve drought tolerance is the inoculation of plants with arbuscular mycorrhizal fungi (AMFs) (Chitarra et al., 2016). AMFs are well-known symbionts of many terrestrial plants and play critical roles in adapting to various stresses (Huang et al., 2020). The effects of AMFs on plant drought tolerance are highly complex, involving multiple metabolic pathways. They assist in drought adaptation by improving nutrient and water uptake and transport, enhancing osmotic regulation, inducing hormone signaling, improving gas exchange capability, increasing water use efficiency and strengthening antioxidant capacity (Yang et al., 2014).
       
Moreover, during drought conditions, MAPK signaling genes are highly expressed, facilitating the interaction between AMFs and apple trees and enhancing drought tolerance (Huang et al., 2020). Plant transcription factors (TFs) also play important roles in regulating stress responses (Century et al., 2008). Among these TFs, the homeodomain-leucine zipper (HD-Zip) family is particularly important in regulating drought responses (Yang et al., 2014). In apples, the HD-Zip gene MdHB-7 leads to the accumulation of endogenous abscisic acid (ABA) in response to drought, promoting ROS detoxification and stomatal closure, while RNA interference (RNAi) lines of this gene showed opposite effects (Zhao et al., 2020).
       
Additionally, ethylene response factors (ERFs) influence anthocyanin biosynthesis. The well-characterized ERF protein MdERF38 participates in anthocyanin biosynthesis induced by drought stress. Molecular experiments showed an interaction between the ERF protein (MdERF38) and the positive regulator of anthocyanin (MdMYB1), which promotes drought tolerance. MdMYB88 and MdMYB124 also act as positive regulators of drought tolerance (Li et al., 2020). In apple, 42 apple-specific miRNAs have been identified, among which miR156, miRn249, miR408 and miR395 act as positive regulators of drought tolerance (Li et al., 2020).
       
The drought-responsive gene families and their regulatory roles in stress adaptation in apple are illustrated in Table 1. The schematic depicts the major drought-responsive gene families in apple and their roles in physiological and molecular pathways of stress adaptation. Abbreviations: NAC - NAM/ATAF/CUC transcription factors; DREB - dehydration-responsive element-binding proteins; ERF - ethylene response factors; MYB - MYB transcription factors; HD-Zip - homeodomain-leucine zipper proteins.

Table 1: Specific gene families in apple are involved in stress responses.


       
The pie chart (Fig 2) illustrates the percentage distribution of genes across different transcription factor (TF) families. The largest portions are represented by the MYB, AP2/ERF and NAC families, which play critical roles in gene expression. Other families, such as bZIP, HSF, bHLH, Dof and G2-like, occupy relatively smaller proportions. The smaller segments include transcription factor families such as WRKY, GRAS, C2H2, Trihelix, NF-YA, DBB, C3H, BES1-HD-ZIP, E2F/DP, LBD, Nin-like, SBP, SRS and ZF-HD.

Fig 2: Stress-responsive specific gene families.


       
This distribution visually represents the allocation of transcription factor families within the plant genome and analyzing their expression profiles provides deeper insights into stress responses, development and molecular regulatory mechanisms in plants. The highly represented MYB, AP2/ERF and NAC families constitute major regulatory genes in plants, making them central targets for molecular biology and breeding research.

CONCLUSION

This study analyzed drought resistance mechanisms in apple plants at physiological, biochemical, and molecular levels. The results indicate that apples adapt to drought through stomatal closure, reduced leaf area, osmoprotectant synthesis, and activation of antioxidant enzymes such as SOD, CAT, and POD, which mitigate oxidative damage caused by ROS. At the molecular level, stress-responsive genes including MdNAC29 and MdDREB2A regulate signaling pathways and activate downstream defense mechanisms. The findings suggest that combining the natural drought tolerance of traditional varieties with transgenic approaches offers strong potential for breeding resilient apple cultivars capable of maintaining yield and fruit quality under climate change.

ACKNOWLEDGEMENT

The authors express their deep gratitude to the scientific staff of the Institute of Genetics and Experimental Biology of Plants of the Academy of Sciences of Uzbekistan and the Academician M. Mirzayev Research Institute of Horticulture, Viticulture and Winemaking.
 
Author contribution
 
Farhod Abdurasulov conceived and structured the study, conducted the literature search and selection and drafted the initial version of the manuscript. Farhod Abdurasulov and Jaloliddin Shavkiev contributed to the critical analysis of the literature and the revision of the manuscript. Sherzod Rajametov assisted in data organization.
 
Data availability
 
The data supporting the findings of this review are entirely derived from peer-reviewed publications and publicly available databases, including PubMed, ScienceDirect, Scopus and Web of Science. A comprehensive list of these sources is provided in the References section. No proprietary or unpublished data were used.
 
Ethical approval
 
Not applicable to this study.
 

CONFLICT OF INTEREST

The authors declare no conflicts of interest.

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    Review Article

    Complex Analysis of Physiological, Biochemical and Molecular Mechanisms of Drought Adaptation in Apple (Malus domestica Borkh.)

    F
    Farhod Abdurasulov1
    S
    Sherzod Rajametov2
    A
    Alisher Botirov3,*
    S
    Shukhrat Abdurasulov4
    J
    Jaloliddin Shavkiev5
    1Academician Makhmud Mirzayev Scientific Research Institute of Horticulture, Viticulture, and Winemaking.
    2Coordinator of the World Bank Project “Livestock Sector Development-Phase II”.
    3Faculty of Economics, Forestry and veterinary Medicine, Termez State University of Engineering and Agrotechnology, Surkhandarya 190100, Uzbekistan.
    4Tashkent State Agrarian University.
    5Institute of Genetics and Experimental Plant Biology, Academy of Sciences of the Republic of Uzbekistan.

    ABSTRACT

    Drought is one of the most critical abiotic stresses limiting apple (Malus domestica Borkh.) growth, productivity and fruit quality worldwide. Understanding the complex physiological, biochemical and molecular mechanisms underlying drought tolerance is essential for developing stress-resilient cultivars. The present review highlights integrated responses of apple varieties to drought stress, focusing on water relations, gas exchange, osmotic regulation, antioxidant defense and hormonal signaling. Physiologically, drought-tolerant genotypes maintain higher relative water content, stomatal conductance and water-use efficiency. Biochemically, accumulation of osmolytes (proline, soluble sugars, glycine betaine) and enhanced activity of antioxidant enzymes (SOD, CAT, POD, APX) mitigate oxidative damage. Molecular mechanisms involve activation of drought-responsive transcription factors (AREB/ABF, DREB, NAC, MYB), signal transduction through ABA pathways and upregulation of stress-protective genes. Integration of these responses enables better nutrient and water uptake, osmotic adjustment and improved photosynthetic performance under water deficit. Future research should focus on genome editing, marker-assisted selection and omics-based approaches to accelerate the breeding of drought-resilient apple cultivars.

    INTRODUCTION

    Apple (Malus x  domestica Borkh.) is one of the most widely cultivated and economically important fruit crops globally, valued for its nutritional content, industrial use and contribution of over 73 billion USD to the global economy (FAOSTAT, 2020). In Uzbekistan, apple is the leading fruit crop, where intensive production largely relies on high-yielding commercial cultivars. However, these modern varieties often lack adaptability to local environmental stresses.
           
    Due to global climate change, decreasing water availability, unpredictable rainfall patterns and rising temperatures pose serious threats to agricultural systems worldwide. Among fruit trees, apple (Malus x domestica Borkh.) is particularly vulnerable to drought stress, which adversely affects not only vegetative growth but also fruit yield and quality. In drought-prone regions, such as the Mediterranean, Central Asia and parts of Uzbekistan, these stresses directly impact the economic viability and sustainability of apple production.
           
    Identifying drought-tolerant cultivars and rootstocks and understanding their physiological and molecular mechanisms of stress response, is therefore of both scientific and practical significance. Such knowledge enables the development of resilient apple varieties better adapted to climate change, while also supporting improved agronomic practices and resource-efficient production systems. In Uzbekistan-where apples are the most cultivated fruit and water scarcity is an increasing concern-the preservation and study of traditional apple germplasm offer a promising avenue. These varieties, often naturally adapted to local environmental conditions, can serve as valuable genetic resources for breeding drought-tolerant, high-quality cultivars.
           
    This research provides an essential foundation for modern breeding strategies by elucidating the physiological, biochemical and genetic basis of drought tolerance in apples. The findings have the potential to contribute significantly to sustainable fruit production and food security in water-limited environments.
           
    Due to climate change, apple production faces increasing threats from abiotic stress factors such as drought, extreme heat and salinity. These stressors negatively affect physiological and molecular processes, including photosynthesis, stomatal conductance and oxidative balance, ultimately reducing fruit yield and quality (Berger et al., 2016; Pérez  et al., 2008). As agriculture consumes over 70% of the world’s freshwater, the need for drought-resilient cultivars is more urgent than ever.
           
    Traditional apple cultivars, though underutilized, are better adapted to local conditions and often show enhanced resistance to environmental stresses. They contain higher levels of bioactive compounds and demonstrate stable performance under drought (Donno et al., 2012; Cvetković et al., 2012). Therefore, understanding and utilizing their genetic potential is critical for future breeding strategies.
           
    This study aims to comprehensively examine the physiological, biochemical and molecular responses of apple plants to drought stress. Special focus is given to identifying drought-responsive genes and pathways that contribute to improved stress adaptation. The findings will provide a basis for developing high-performing, drought-tolerant apple varieties to ensure sustainable production in a changing climate.
     
    The effect of drought stress on the physiological, biochemical and molecular mechanisms of apple plants
     
    Drought is a major limiting factor in crop production. Due to increasing global temperatures and limited water resources, drought has become a global issue threatening future crop production (Zhao et al., 2020, Botirov et al., 2021). Naturally, plants have developed multiple molecular and physiological mechanisms to withstand stress. Drought activates key regulatory genes that control physiological processes such as stomatal closure (Taiz et al., 2002) and detoxification of reactive oxygen species (ROS) (Sun et al., 2018; Chen et al., 2019). Additionally, heat and drought conditions generate ROS, leading to membrane damage and oxidative stress.
           
    Recent studies published in ARCC journals have high-lighted the importance of integrating physiological, biochemical and molecular approaches for improving drought tolerance in horticultural crops. These studies emphasize the role of antioxidant systems, transcription factors and stress signaling networks in enhancing plant resilience under water deficit conditions, which is essential for developing climate-resilient fruit production systems (Kumar et al., 2021; Singh et al., 2020; Patel et al., 2019; Sharma et al., 2022).
           
    Water deficiency in plants induces oxidative stress (Lei et al., 2006; Noctor et al., 2014), including excessive production of reactive oxygen species such as superoxide radicals (O2-) and hydrogen peroxide (H2O2) resulting in lipid peroxidation and damage to membranes, proteins, chlorophyll, nucleic acids and ultimately cell death (Scandalios, 1993). Drought can significantly reduce photosyn- thesis and cause chlorophyll degradation (Viljevac et al., 2013; Bhusal et al., 2019). According to Chaves et al., (2002), the negative effects of drought on plant physiology depend on the intensity and duration of the drought stress as well as the plant’s ability to adapt and survive under such conditions.
           
    To withstand drought stress and protect against oxidative damage, plants have developed antioxidant defense mechanisms, including antioxidant enzymes such as peroxidase (POD), superoxide dismutase (SOD), catalase (CAT) and non-enzymatic antioxidants such as phenolic compounds, ascorbic acid, glutathione and carotenoids (Asensi., 2010; Farooq et al., 2012). Some plants accumulate osmolytes like proline, glycine betaine and soluble sugars to protect themselves and mitigate drought stress (Shehab et al., 2010; Xu et al., 2018; Dien et al., 2019). Recent studies have shown that certain plant organ compounds like terpenes (Mahdavi et al., 2020) and phytohormones like brassinolide (Naservafaei et al., 2021) can alleviate drought effects by enhancing the plant’s defense systems.
           
    Chlorophylls, as the main photosynthetic pigments in plant leaves, reflect the photosynthetic capacity and overall vitality of plants. The chlorophyll content in leaves is considered a good indicator of stress tolerance in various crops, including drought tolerance (Arunyanark et al., 2008). Previous studies have documented that drought stress negatively affects chlorophyll accumulation in apple rootstock cuttings (Alizadeh et al., 2011; Bolat et al., 2014). Under drought conditions, a decrease in chlorophyll content has been observed in plants, with a greater decrease recorded in the commercial cultivar ‘Golden Delicious Reinders’ compared to ‘Crvenka’ (Mihaljevic et al., 2021). These results are consistent with observations by Bhusal et al., (2019), where a smaller decrease in total chlorophyll content was found in the drought-tolerant ‘Fuji’ apple compared to the ‘Hongro’ apple.
           
    Carotenoids play an essential role in photosynthesis, as they protect photosystem II from photooxidative damage (Cogdell and Gardiner, 1993). Khoyerdi et al., (2016) reported that high carotenoid content in pistachio cultivars leads to greater drought tolerance.
           
    Under drought conditions, the decline in photosystem II activity is associated with oxidative stress and cell membrane damage caused by increased lipid peroxidation (Benhassaine et al., 2002). Malondialdehyde (MDA) is a product of lipid peroxidation and is commonly used to assess oxidative stress during drought (Farooq et al., 2010). Various abiotic stresses, including drought, induce the generation of ROS such as H2O2 which damages membrane lipids (Kocsy et al., 2005). Our findings indicate that higher MDA concentrations under drought stress are associated with elevated H2O2 levels in plants. During drought stress, significant increases in MDA and H2O2  contents were observed in both the ‘Golden Delicious Reinders’ and ‘Dugara’ cultivars, indicating oxidative damage in both. As the intensity of stress increased, so did the levels of H2O2 and consequently MDA. Møller  et al. (2007) suggested that higher MDA levels indicate more severe oxidative damage.
           
    In our study, the commercial ‘Golden Delicious Reinders’ cultivar exhibited a faster increase in MDA and H2O2  concentrations compared to the traditional ‘Dugara’ cultivar and significant early-stage changes in H2O2  suggest that ‘Dugara’ is more drought-tolerant. Several researchers have reported increased MDA and H2O2  levels under drought stress in plants (Petridis et al., 2012; Yang and Miao., 2010). In the traditional ‘Crvenka’ cultivar, MDA content remained stable under drought, while H2O2  levels decreased after 12 days of drought, consistent with earlier findings (Umar and Shaheed., 2018), suggesting that reduced H2O2 production is likely associated with increased antioxidant enzyme activities, particularly CAT.
           
    Leaf water content (WC) is an indicator of plant water status and is used to evaluate drought tolerance (Bandurska and Joswiak., 2010). After 12 days of stress, a significant decrease in leaf water content in response to drought stress was observed only in the ‘Golden Delicious Reinders’ cultivar, which had the lowest photosynthetic efficiency. In contrast, the traditional cultivars maintained better photosynthetic efficiency and stable water content. Similarly, Tounekti et al., (2018) found that a drought-tolerant coffee cultivar exhibited higher water content along with better photosynthetic efficiency under drought conditions. These observations, confirmed by photochemical parameters, highlight the better drought tolerance of traditional cultivars.
           
    Proline is an important organic osmolyte that accumulates and increases under drought conditions and also acts as a ROS scavenger (Sumera and Asghari, 2010; Liang et al., 2013). Numerous previous studies have reported higher proline accumulation in drought-tolerant plants (Anjum et al., 2016; Man et al., 2011). However, our results showed that proline measurement was not a reliable screening method for determining drought tolerance in the studied apple cultivars. The proline content in the drought-tolerant ‘Crvenka’ was not higher than that in the drought-sensitive ‘Golden Delicious Reinders. The lower proline accumulation in ‘Crvenka’ may suggest the activation of other drought defense mechanisms. Rampino et al., (2006) also reported that drought-tolerant wheat plants exhibited higher relative water content (RWC) and lower proline accumulation.
           
    Plant phenolic compounds are secondary metabolites that serve as antioxidants and have been described as indicators of abiotic stress tolerance in plants (Blokhina et al., 2003; Quan et al., 2016). Hura et al., (2009) found that in triticale plants, higher phenolic content was associated with better photosynthetic activity. However, this does not align with our findings, as the total phenolic content accumulated in the leaves of the studied apple cultivars was highly variable, with the highest phenolic content observed in the commercial cultivar “Golden Delicious Reinders.” These results suggest that phenolic compounds may not play a major role in the defense responses of the studied apple cultivars. Similarly, Puente-garza and colleagues reported that total phenolic content was not correlated with antioxidant activity in Agave plants.
           
    Although we hypothesized that higher concentrations of proline and secondary metabolites (phenolics) would improve osmotic adjustment and drought tolerance, this hypothesis was not supported. This likely indicates that antioxidant enzyme systems were activated as a protective mechanism in this study. According to Mihaljevic et al., (2021), there are significant differences among cultivars in their physiological and biochemical responses to drought stress. The most drought-tolerant cultivars showed high photosynthetic efficiency, high chlorophyll content and strong membrane stability, whereas the commercial cultivar “Golden Delicious Reinders” was found to be the most sensitive under the studied conditions. The good quality traits of “Crvenka” (Jakobek et al., 2020) and its high drought tolerance make it a promising cultivar for cultivation under dry conditions in the region. These cultivars could be used to update the production assortment and support the development of fruit cultivation. Preserving traditional cultivars is also important for maintaining genetic material for breeding purposes; therefore, the results of this study could provide valuable information for future breeding programs.
           
    Plants have developed morphological, physiological and molecular resistance mechanisms in response to abiotic stress. Among these molecular mechanisms are the regulation of gene expression through transcription factors (TFs) and the roles of specific functional genes. NAC genes are plant-specific transcription factors that influence plant growth and development and participate in the transcriptional regulation of responses to various abiotic stresses such as drought, salinity, cold and pathogen infection (Sun et al., 2012; Tak et al., 2017). Members of the NAC gene family are differentially expressed in response to abiotic stress.
           
    Here, we isolated the MdNAC29 gene, a NAC transcription factor, from apples. Our results showed that MdNAC29 is localized in the nucleus and responds to drought stress. Overexpression of MdNAC29 was found to negatively regulate drought tolerance in transgenic apple plants, callus and tobacco plants.
           
    Moreover, genes such as MdERD5, MdRD22, MdRD29A, MdAREB1, MdDREB2A and MdMYB46 have been reported to be extensively involved in improving drought tolerance in plants (An et al., 2018; Chen et al., 2019; Li et al., 2022; Liu et al., 2022). We hypothesize that MdNAC29 regulates the expression of these drought-responsive genes. qRT-PCR results showed that the overexpression of MdNAC29 significantly downregulated the expression of these genes in apple trees.
           
    Drought in apple trees is generally understood as a persistent water deficit due to an imbalance between water supply and demand or a low water budget throughout the growth cycle. This leads to leaf wilting, yellowing and premature leaf drop, as well as early fruit ripening and fruit drop (Yang et al., 2021). In apple trees, drought stress can temporarily inhibit shoot growth due to reduced leaf area, stomatal closure and disruption of the plant’s carbon balance caused by hydraulic failure (Lauri et al., 2016). During hot summer months, drought stress, often combined with heat stress, can cause leaf scorch. Frequent drought stress events caused by dry weather conditions resulting from global warming have significantly reduced apple yield and quality (Aras and Keles., 2019). Therefore, apple trees must sense soil water availability and activate appropriate molecular stress responses to survive under such conditions.
           
    Research has shown that one of the key genes involved in improving drought tolerance in apple trees is MdDREB2A. Overexpression of this gene activates stress-responsive genes under stress conditions, thereby enhancing drought tolerance. Furthermore, other transcription factor families, such as NAC, MYB and ERF, also participate in forming drought adaptation responses, but many studies particularly emphasize the importance of MdDREB2A. To date, many genes from the APETALA2/ethylene-responsive factor (AP2/ERF), ZFP, bHLH, MYB and NAC families have been identified and characterized for their roles in apple drought responses (Fig 1).

    Fig 1: Effects of drought on apple (Malus domestica Borkh.): physiological, biochemical and molecular responses.


           
    In the study by Sun et al., (2018), overexpression of the MdATG18a gene in apple trees enhanced their drought tolerance. These processes help degrade aggregated proteins and limit oxidative damage. Another important agricultural practice to improve drought tolerance is the inoculation of plants with arbuscular mycorrhizal fungi (AMFs) (Chitarra et al., 2016). AMFs are well-known symbionts of many terrestrial plants and play critical roles in adapting to various stresses (Huang et al., 2020). The effects of AMFs on plant drought tolerance are highly complex, involving multiple metabolic pathways. They assist in drought adaptation by improving nutrient and water uptake and transport, enhancing osmotic regulation, inducing hormone signaling, improving gas exchange capability, increasing water use efficiency and strengthening antioxidant capacity (Yang et al., 2014).
           
    Moreover, during drought conditions, MAPK signaling genes are highly expressed, facilitating the interaction between AMFs and apple trees and enhancing drought tolerance (Huang et al., 2020). Plant transcription factors (TFs) also play important roles in regulating stress responses (Century et al., 2008). Among these TFs, the homeodomain-leucine zipper (HD-Zip) family is particularly important in regulating drought responses (Yang et al., 2014). In apples, the HD-Zip gene MdHB-7 leads to the accumulation of endogenous abscisic acid (ABA) in response to drought, promoting ROS detoxification and stomatal closure, while RNA interference (RNAi) lines of this gene showed opposite effects (Zhao et al., 2020).
           
    Additionally, ethylene response factors (ERFs) influence anthocyanin biosynthesis. The well-characterized ERF protein MdERF38 participates in anthocyanin biosynthesis induced by drought stress. Molecular experiments showed an interaction between the ERF protein (MdERF38) and the positive regulator of anthocyanin (MdMYB1), which promotes drought tolerance. MdMYB88 and MdMYB124 also act as positive regulators of drought tolerance (Li et al., 2020). In apple, 42 apple-specific miRNAs have been identified, among which miR156, miRn249, miR408 and miR395 act as positive regulators of drought tolerance (Li et al., 2020).
           
    The drought-responsive gene families and their regulatory roles in stress adaptation in apple are illustrated in Table 1. The schematic depicts the major drought-responsive gene families in apple and their roles in physiological and molecular pathways of stress adaptation. Abbreviations: NAC - NAM/ATAF/CUC transcription factors; DREB - dehydration-responsive element-binding proteins; ERF - ethylene response factors; MYB - MYB transcription factors; HD-Zip - homeodomain-leucine zipper proteins.

    Table 1: Specific gene families in apple are involved in stress responses.


           
    The pie chart (Fig 2) illustrates the percentage distribution of genes across different transcription factor (TF) families. The largest portions are represented by the MYB, AP2/ERF and NAC families, which play critical roles in gene expression. Other families, such as bZIP, HSF, bHLH, Dof and G2-like, occupy relatively smaller proportions. The smaller segments include transcription factor families such as WRKY, GRAS, C2H2, Trihelix, NF-YA, DBB, C3H, BES1-HD-ZIP, E2F/DP, LBD, Nin-like, SBP, SRS and ZF-HD.

    Fig 2: Stress-responsive specific gene families.


           
    This distribution visually represents the allocation of transcription factor families within the plant genome and analyzing their expression profiles provides deeper insights into stress responses, development and molecular regulatory mechanisms in plants. The highly represented MYB, AP2/ERF and NAC families constitute major regulatory genes in plants, making them central targets for molecular biology and breeding research.

    CONCLUSION

    This study analyzed drought resistance mechanisms in apple plants at physiological, biochemical, and molecular levels. The results indicate that apples adapt to drought through stomatal closure, reduced leaf area, osmoprotectant synthesis, and activation of antioxidant enzymes such as SOD, CAT, and POD, which mitigate oxidative damage caused by ROS. At the molecular level, stress-responsive genes including MdNAC29 and MdDREB2A regulate signaling pathways and activate downstream defense mechanisms. The findings suggest that combining the natural drought tolerance of traditional varieties with transgenic approaches offers strong potential for breeding resilient apple cultivars capable of maintaining yield and fruit quality under climate change.

    ACKNOWLEDGEMENT

    The authors express their deep gratitude to the scientific staff of the Institute of Genetics and Experimental Biology of Plants of the Academy of Sciences of Uzbekistan and the Academician M. Mirzayev Research Institute of Horticulture, Viticulture and Winemaking.
     
    Author contribution
     
    Farhod Abdurasulov conceived and structured the study, conducted the literature search and selection and drafted the initial version of the manuscript. Farhod Abdurasulov and Jaloliddin Shavkiev contributed to the critical analysis of the literature and the revision of the manuscript. Sherzod Rajametov assisted in data organization.
     
    Data availability
     
    The data supporting the findings of this review are entirely derived from peer-reviewed publications and publicly available databases, including PubMed, ScienceDirect, Scopus and Web of Science. A comprehensive list of these sources is provided in the References section. No proprietary or unpublished data were used.
     
    Ethical approval
     
    Not applicable to this study.
     

    CONFLICT OF INTEREST

    The authors declare no conflicts of interest.

    REFERENCES


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