1 Introduction

Cucurbitaceae plants, commonly known as gourds or cucurbits, encompass a wide variety of species including pumpkins, squashes, and gourds, which hold significant agricultural importance due to their nutritional value and economic impact. These species are cultivated globally and are integral to food systems and agro-biodiversity. However, the productivity and quality of Cucurbitaceae crops are severely threatened by PM, a widespread fungal disease caused predominantly by Podosphaera xanthii, which leads to substantial yield losses and affects the sustainability of cucurbit production (Cohen et al., 2003; Park et al., 2020; Caligiore-Gei et al., 2023).

PM is characterized by white, powdery fungal growth on the surface of leaves, stems, and sometimes fruits. The disease thrives in warm, dry climates and can spread rapidly, making it a persistent issue for growers. The impact of PM on agriculture is profound, as it not only reduces the marketability of the crops but also necessitates increased use of fungicides, which can be environmentally detrimental and economically burdensome (Cohen et al., 2003; Park et al., 2020; Caligiore-Gei et al., 2023).

Given the challenges posed by PM, there is a pressing need for genetic research to develop resistant cultivars. Recent studies have identified single-gene resistance in zucchini squash, which provides a promising avenue for breeding resistant varieties (Cohen et al., 2003). Additionally, quantitative trait locus (QTL) mapping and molecular markers have been utilized to identify resistance in pumpkin, offering valuable tools for the genetic improvement of Cucurbita moschata (Park et al., 2020). These advancements in understanding the genetic bases of PM resistance are crucial for the development of sustainable management strategies and the continued success of cucurbit agriculture (Cohen et al., 2003; Guo et al., 2019; Park et al., 2020).

The systematic review will delve into the research progress on pM in Cucurbitaceae plants, highlighting the genetic mechanisms of resistance, the identification of causal agents, and the screening for resistance among different squash genotypes. This comprehensive analysis aims to synthesize the current knowledge and provide insights for future research directions in the fight against this pervasive plant disease (Cohen et al., 2003; Guo et al., 2019; Park et al., 2020; Caligiore-Gei et al., 2023).

2 What is Powdery Mildew

2.1 Description of the disease

Powdery Mildew (PM) is a widespread fungal disease that affects a variety of vegetable crops, with cucurbits being one of the most severely impacted groups. This disease is characterized by white powdery colonies that develop on the surfaces of leaves, petioles, and stems (Figure 1). Under favorable conditions, these colonies can coalesce, leading to chlorosis and early senescence of the host tissue (Pérez-García et al., 2009).

Under favorable conditions, these colonies can coalesce, leading to chlorosis and early senescence of the host tissue. A: Symptoms on a zucchini leaf; B: Detail of a PM colony; C: Zucchini cotyledon maintained in vitro and infected with P. fusca showing typical PM colonies (Pérez-García et al., 2009).

This study by Pérez-García et al. (2009) provides significant insights into the pathogenesis of P. fusca in cucurbit plants, specifically zucchini. Understanding the specific conditions that favor the growth of PM and its impact on plant health is crucial for developing effective control strategies. The research highlights the need for detailed investigations into both the biological aspects of the fungus and the environmental factors that contribute to disease outbreaks. Effective management of PM in cucurbits could greatly enhance crop yield and quality, which is vital for agricultural productivity. The study underscores the importance of integrated disease management strategies that combine cultural, biological, and chemical approaches to control the spread of PM in susceptible crops.

2.2 Causal fungal species associated with PM in Cucurbitaceae

The main causal agent of cucurbit PM is Podosphaera xanthii (synonym P. fusca), which is considered one of the most important limiting factors for cucurbit production worldwide (Figure 2) (Pérez-García et al., 2009). Other species such as Golovinomyces cichoracearum have also been identified as pathogens causing PM in cucurbits, although Podosphaera xanthii (P. xanthii) is the predominant species (Křístková et al., 2009; Aguiar et al., 2012).

2.3 Symptoms and diagnosis of PM in different Cucurbitaceae species

The initial symptoms of PM in cucurbits include circular or irregular white powdery areas on both surfaces of the leaves. As the disease progresses, the fungal mycelia can cover entire leaves, petioles, and stems, resulting in leaf yellowing and senescence but not necessarily defoliation (Liang et al., 2020).

The detailed description of the life cycle of P. fusca provided by Pérez-García et al. (2009) is essential for developing targeted and effective management strategies for PM in cucurbits. Understanding the developmental stages of the fungus, from spore germination to mycelial expansion, is crucial for timing fungicidal applications and implementing cultural practices that can disrupt the pathogen's growth and reproduction. This comprehensive study of the pathogen's biology could aid researchers and agricultural practitioners in devising more sustainable and integrated disease management practices that reduce dependency on chemical controls and favor agricultural sustainability.

The diagnosis of PM is often based on these visible symptoms and can be confirmed by the identification of the fungal species responsible for the infection. Morphological characteristics such as conidia shape, the presence of fibrosing bodies, and the formation of cleistothecia are used for species identification (Pérez-García et al., 2009; Aguiar et al., 2012; Liang et al., 2020). Molecular tools, such as sequencing of the ITS region of rDNA, have also been employed to accurately identify the causal agents of PM in cucurbits (Liang et al., 2020; Caligiore-Gei et al., 2022).

3 What Problems Does PM Cause

3.1 Economic impact on Cucurbitaceae cultivation and yields

PM, primarily caused by the fungus P. fusca (synonym P. xanthii), poses a significant threat to the cultivation of Cucurbitaceae, which includes economically important crops such as cucumbers, melons, and squashes. The disease can lead to substantial yield losses worldwide, as it affects the plants during critical growth stages. In China, for instance, the incidence of PM on hulless Cucurbita pepo reached 100%, indicating the potential for complete crop failure if the disease is left unmanaged (Liang et al., 2020). The economic impact is further exacerbated by the costs associated with disease control measures, including chemical treatments and the development of resistant cultivars (Pérez-García et al., 2009).

3.2 Effects on plant health and productivity

PM affects plant health by forming white colonies on leaf surfaces, petioles, and stems, which can coalesce under favorable conditions, leading to chlorosis and early senescence of the host tissue (Pérez-García et al., 2009). This disease reduces plant growth and can cause premature defoliation, which in turn diminishes the photosynthetic capacity of the plant and its overall productivity (Priyanka et al., 2020). The severity of the disease varies with environmental conditions and can range from mild to severe, affecting the plants in different seasons (Wani, 2012).

3.3 Impact on fruit quality and marketability

The presence of PM not only reduces the quantity of the harvest but also impacts the quality and marketability of the fruits. Infected plants produce fruits that are often of inferior quality due to the compromised health of the plant. The disease can lead to a reduction in both the aesthetic and nutritional value of the fruits, which affects their marketability and the economic returns for farmers (Priyanka et al., 2020). The control of PM is therefore crucial not only for maintaining the yield but also for ensuring the quality of the produce that reaches the market.

4 Genetic Characteristics of PM

The genetic characteristics of PM fungi, particularly P. xanthii, are marked by a large and complex genome with significant genetic diversity and variability. Comparative genomics has provided valuable insights into the mechanisms of adaptation and pathogenesis, which are essential for developing effective disease management strategies for cucurbit crops.

4.1 Overview of the fungal genome

The genome of P. xanthii, a pathogen causing PM in Cucurbitaceae, has been characterized and assembled, revealing a size of 209.08 MB and 142 Mb in two separate studies, with the latter resulting in 14 911 complete genes identified (Table 1) (Kim et al., 2020; Polonio et al., 2020). The genome contains a significant proportion of repetitive sequences, which comprise 76.2% of the genome (Polonio et al., 2020). Comparative analysis with other fungal pathogens has been conducted to identify candidate secreted effector proteins, which are crucial for the pathogenesis of P. xanthii (Kim et al., 2020).

4.2 Genetic diversity and variability among different PM species

Genetic variation among isolates of P. xanthii from various cucurbit hosts and geographic locations has been investigated, showing a trend of isolates clustering from New York and Italy (Xiang et al., 2019). This diversity is also reflected in the virulence of the isolates, with significant differences observed among them (Xiang et al., 2019). Additionally, the mitochondrial genomes of PM pathogens, including P. xanthii, exhibit remarkable variation in size and nucleotide composition, further underscoring the genetic diversity within these species (Kim et al., 2019; Zaccaron and Stergiopoulos, 2021).

4.3 Comparative genomics: insights from other pathogenic fungi

Comparative genomics has provided insights into the evolution and adaptation of PM fungi. For instance, the PM fungi have large genomes with a high content of repetitive DNA sequences, primarily composed of retrotransposons (Vela-Corcía et al., 2016; Kusch et al., 2023). These elements play a key role in shaping the genome architecture and contribute to the rapid evolution of the fungi by enabling them to overcome plant immunity and evolve fungicide resistance (Kusch et al., 2023). Comparative analysis of the mitochondrial genomes of different PM pathogens has revealed unusual bimodal GC distributions and exceptionally long cytochrome b genes, which are indicative of complex evolutionary processes (Zaccaron and Stergiopoulos, 2021).

5 Localization of Genes Resistant to PM

5.1 Techniques used for gene mapping in Cucurbitaceae

Recent advancements in gene mapping techniques have significantly contributed to the identification of PM resistance genes in Cucurbitaceae plants. CRISPR/Cas9-mediated mutagenesis has been effectively used to generate PM resistance in cucumber by targeting the CsaMLO8 gene, which encodes susceptibility factors for the pathogen P. xanthii (Figure 3) (Shnaider et al., 2022). Additionally, QTL-seq combined with bulked segregant analysis has been employed to identify resistance loci in Korean cucumber inbred lines, leading to the discovery of two QTLs on chromosomes 5 and 6 (Zhang et al., 2020). High-resolution melting markers (HRM) have also been used to map resistance regions in melon, narrowing down candidate intervals to specific chromosomal regions (López-Martín et al., 2022).

This study by Shnaider et al. (2022) exemplifies the power of genomic tools in advancing our understanding of disease resistance in crops. By mapping specific genomic regions linked to resistance against PM in melons, researchers provide valuable insights that could lead to the development of more robust melon varieties. The integration of new genomic data with previous findings allows for a more comprehensive understanding of the genetic basis of resistance traits. Such knowledge is crucial for breeding programs aiming to combine various resistance sources to develop cultivars with enhanced durability against PM. The identification of candidate genes within these regions further directs functional studies which are essential for confirming their role in resistance mechanisms and for future applications in precision breeding.

5.2 Recent discoveries in gene localization

Recent discoveries have pinpointed several genes and chromosomal regions associated with PM resistance in Cucurbitaceae. In cucumber, the CsGy5G015660 gene, encoding a putative leucine-rich repeat receptor-like serine/threonine-protein kinase, has been identified as a strong candidate for PM resistance (Zhang et al., 2020). In zucchini, the CpPM10.1 locus on chromosome 10 has been associated with resistance, with three genes containing the RPW8 domain being identified as potential contributors to resistance (Wang et al., 2021). Similarly, in melon, resistance to PM has been linked to a 250 and 381 kb region on chromosomes 5 and 12, respectively (López-Martín et al., 2022).

5.3 Chromosomal regions associated with resistance

Chromosomal regions associated with PM resistance have been identified across various Cucurbitaceae species. In cucumber, a major resistance gene, pm-s, has been mapped to chromosome 5, with the closest flanking markers being SSR20486 and SSR06184/SSR13237 (Liu et al., 2017). In zucchini, the major dominant locus CpPM10.1 conferring resistance to PM has been located in a 382.9 kb region on chromosome10 (Wang et al., 2021). In melon, the resistance to PM races 1, 2, and 5 has been associated with regions on chromosomes 5 and 12 (Figure 4) (López-Martín et al., 2022). Furthermore, a single major QTL conferring resistance to PM in pumpkin (Cucurbita moschata) has been located in a 6.9~7.3 Mb region on chromosome 3 (Park et al., 2020).

This study by López-Martín et al. (2022) exemplifies the power of genomic tools in advancing our understanding of disease resistance in crops. By mapping specific genomic regions linked to resistance against PM in melons, researchers provide valuable insights that could lead to the development of more robust melon varieties. The integration of new genomic data with previous findings allows for a more comprehensive understanding of the genetic basis of resistance traits. Such knowledge is crucial for breeding programs aiming to combine various resistance sources to develop cultivars with enhanced durability against PM. The identification of candidate genes within these regions further directs functional studies which are essential for confirming their role in resistance mechanisms and for future applications in precision breeding.

6 Cloning of Genes Resistant to PM

The cloning of genes resistant to PM in Cucurbitaceae plants has seen significant advancements through various methodologies, including the use of molecular markers and GWAS. The case studies highlighted here demonstrate the potential for developing resistant cultivars and the importance of understanding the genetic basis of resistance. However, the ongoing challenges underscore the need for continued research in this field.

6.1 Methodologies for gene cloning in plant-fungal systems

The study of plant-pathogen interactions, particularly in the context of PM in Cucurbitaceae, has been advanced through the cloning of genes that confer resistance to this disease. A key methodology involves the isolation and characterization of genes from the pathogen itself, such as the β-tubulin-encoding gene from P. fusca, which has been used to develop molecular tools for various applications in PM research (Vela-Corcía et. al., 2014). This approach allows for the identification of genetic markers for molecular phylogenetics and the development of allele-specific assays for detecting resistance to fungicides (Vela-Corcía et. al., 2014).

6.2 Case studies of successful gene cloning in Cucurbitaceae

In Cucurbitaceae, the Mildew Locus O (MLO) gene family has been identified as a significant factor in PM susceptibility. Through genomic analysis, researchers have identified multiple MLO homologs in species such as melon, watermelon, and zucchini, providing a comprehensive overview of this gene family's structure and evolution (Figure 5) (Iovieno et al., 2015).

Another case study involves the identification of a novel candidate gene, CmoAP2/ERF, in pumpkin, which has been implicated in resistance to PM through a genome-wide association study (GWAS). This gene's allelic variation has been validated as a key factor in resistance, and a polymorphic marker has been developed for breeding purposes (Figure 6) (Alavilli et al., 2022).

The exploration of allelic variation in the CmoAP2/ERF gene between PM resistant and susceptible lines as detailed in the research by Alavilli et al. (2022) is a significant step forward in understanding plant defense mechanisms at the genetic level. By pinpointing specific missense mutations and nucleotide changes that differentiate resistant from susceptible phenotypes, this research offers potential molecular markers for breeding programs aimed at enhancing disease resistance. This approach not only aids in the precise manipulation of plant genomes for improved traits but also contributes to the broader understanding of the functional dynamics of stress response genes in plants. Such detailed genetic insights are crucial for advancing plant breeding strategies, particularly in the context of increasing crop resilience to diseases amidst changing global climate conditions.

6.3 Challenges and advancements in cloning resistance genes

Despite the progress made in cloning resistance genes, challenges remain. One of the main difficulties is the complexity of plant-pathogen interactions and the genetic diversity of both the host plants and the pathogens. However, advancements continue to be made, such as the overexpression of the Cucurbita moschata CmSGT1 gene in Nicotiana benthamiana, which resulted in increased resistance to PM. This study not only provided valuable genetic information for breeding disease-resistant pumpkin varieties but also contributed to understanding the molecular mechanisms underlying the functions of resistance genes (Guo et al., 2019).

7 Molecular Mechanisms of Resistance to PM

The molecular mechanisms of resistance to PM in Cucurbitaceae plants involve a complex interplay of genetic pathways, specific resistance genes, and the molecular interactions between host plants and pathogens. These mechanisms are mediated by a variety of molecular components, including transcription factors, signaling molecules, and noncoding RNAs, which together contribute to the plant's ability to resist infection by PM pathogens (Guo et al., 2018; 2019; Nie et al., 2021; Wang et al., 2021; Shnaider et al., 2022; Tian et al., 2022).

7.1 Genetic pathways involved in resistance

The genetic pathways that confer resistance to PM in Cucurbitaceae plants involve a complex network of genes and molecular interactions. Recent studies have identified several key components of these pathways. For instance, the Mildew Resistance Locus O (MLO) gene family plays a crucial role in susceptibility to PM, with natural mutations in genes such as CsaMLO8 in cucumber conferring resistance to the pathogen P. xanthii (Shnaider et al., 2022). Additionally, the SGT1 gene, a component of the plant disease-associated signal transduction pathway, has been implicated in resistance. Overexpression of the Cucurbita moschata CmSGT1 gene in transgenic plants has been shown to enhance resistance to PM by accelerating cell necrosis and increasing the accumulation of hydrogen peroxide (H₂O₂), which is associated with the activation of salicylic acid (SA)-dependent defense genes (Guo et al., 2019).

7.2 Role of specific genes in conferring resistance

Specific genes have been identified that play a direct role in conferring resistance to PM. For example, the CpPM10.1 gene in zucchini has been associated with dominant resistance to PM, and its expression is positively correlated with resistance (Wang et al., 2021). Similarly, transcriptome profiling of pumpkin leaves infected with PM has revealed differentially expressed genes (DEGs) such as bHLH87, ERF014, WRKY21, HSF, MLO3, and SGT1, which have distinct expression patterns in resistant versus susceptible plants (Guo et al., 2018). These genes are part of a broader regulatory network that includes hormone signal transduction pathways and defense responses.

7.3 Interaction between host plants and pathogens at the molecular level

At the molecular level, the interaction between host plants and pathogens involves a dynamic exchange of signals and responses. Long noncoding RNAs (lncRNAs) and microRNAs (miRNAs) have been shown to play important roles in plant immunity, including the response to PM (Nie et al., 2021; Tian et al., 2022). For instance, differentially expressed lncRNAs and mRNAs have been identified in cucumber that correlate with resistance to PM, and these are associated with pathways such as phenylpropanoid biosynthesis and ubiquinone biosynthesis (Nie et al., 2021). In Cucurbita pepo, PM-responsive lncRNAs have been linked to various biological processes, including the plant-pathogen interaction pathway and the MAPK signaling pathway (Tian et al., 2022). These findings suggest that noncoding RNAs are integral components of the molecular mechanisms underlying resistance to PM in Cucurbitaceae plants.

8 Discussion

8.1 Synthesis of reviewed literature: major findings and their implications

The collective research on PM in Cucurbitaceae plants has made significant strides in understanding the pathogenesis and resistance mechanisms against P. xanthii, the primary causal agent of the disease. The genome of P. xanthii has been characterized, providing a valuable resource for future genomic and proteomic studies aimed at understanding host-specific pathogenesis (Kim et al., 2020). This genomic information has been crucial in identifying candidate secreted effector proteins that play a role in the infection process, which could lead to the development of targeted strategies for disease prevention.

Field trials and genetic studies have identified differences in resistance among Cucurbitaceae cultivars, with some showing promising resistance traits (Cohen et al., 2003; Caligiore-Gei et al., 2022). For instance, the advanced breeding line BL717/1 has been highlighted as a potential source of resistance for the development of open-pollinated resistant cultivars (Caligiore-Gei et al., 2022). Additionally, the use of CRISPR/Cas9-mediated mutagenesis has been successful in generating PM resistance in cucumber by targeting the CsaMLO8 gene, which encodes a susceptibility factor for fungus penetration (Shnaider et al., 2022). This approach offers a direct method for enhancing resistance in commercial cultivars and hybrid parental lines, potentially simplifying the breeding process.

The Mildew Locus O (MLO) gene family has been extensively studied, revealing its role as a susceptibility factor for PM. Inactivation of specific MLO genes leads to a form of resistance known as mlo resistance, which has been observed in several Cucurbitaceae species (Iovieno et al., 2015). Furthermore, the identification of a single-gene resistance to PM in zucchini squash, designated Pm-0, derived from a wild species, has been a significant breakthrough in breeding resistant cultivars (Cohen et al., 2003; Holdsworth et al., 2016).

Biocontrol agents, such as Bacillus amyloliquefaciens LJ02, have shown potential in inducing systemic resistance against cucurbits PM by stimulating the salicylic acid-mediated defense response (Li et al., 2015). This highlights the possibility of integrating biological control methods with traditional breeding approaches for disease management.

8.2 Comparison with resistance mechanisms in other plant families

The resistance mechanisms observed in Cucurbitaceae share similarities with those in other plant families. For example, the role of MLO genes in susceptibility to PM is not unique to Cucurbitaceae but has been documented in other families as well (Iovieno et al., 2015). The use of biocontrol agents to induce systemic resistance is also a common strategy across different plant species (Li et al., 2015).

8.3 Gaps in current research and potential areas for future study

Despite the progress made, there are still gaps in the current research. The exact molecular mechanisms by which effector proteins facilitate P. xanthii infection remain to be fully elucidated (Kim et al., 2020). Additionally, while the role of MLO genes in disease susceptibility is known, the specific interactions between these genes and other plant defense pathways require further investigation (Iovieno et al., 2015).

Future studies could focus on the long-term effectiveness and environmental impact of using CRISPR/Cas9-mediated resistance in commercial crops (Shnaider et al., 2022). The potential for resistance gene stacking to create cultivars with durable resistance to PM is another area worth exploring. Moreover, the development of rapid detection methods for resistant isolates, such as the loop-mediated isothermal amplification (LAMP) technique, could facilitate the monitoring of resistance in the field (Vielba-Fernández et al., 2019).

The exploration of biocontrol agents and their integration into crop management systems could also be expanded, with a focus on understanding the molecular basis of induced resistance and its interaction with plant genetics (Li et al., 2015). Finally, the potential for cross-resistance to other pathogens when overexpressing genes like CmSGT1 in transgenic plants should be carefully assessed (Guo et al., 2019).

9 Concluding Remarks

9.1 Summary of key insights from the systematic review

The systematic review has highlighted significant advancements in the understanding and management of PM in Cucurbitaceae plants. CRISPR/Cas9-mediated mutagenesis has been successfully employed to induce PM resistance in cucumber by targeting the CsaMLO8 gene, demonstrating a promising approach for breeding resistant cultivars. The identification of a single-gene resistance to PM in zucchini squash suggests the potential for simpler breeding strategies. Moreover, the study of genotypic variation in field resistance among Cucurbita pepo cultivars has provided insights into the epidemiological aspects of PM resistance. The role of the MLO gene family in PM susceptibility has been further elucidated, offering a comprehensive overview of potential targets for resistance breeding in melon, watermelon, and zucchini. Additionally, the use of biocontrol agents such as Bacillus amyloliquefaciens LJ02 has been shown to induce systemic resistance against PM in cucurbits, presenting an alternative to chemical control.

9.2 The importance of continuing research on PM resistance in Cucurbitaceae

Continued research on PM resistance in Cucurbitaceae is of paramount importance due to the economic impact of the disease on cucurbit crops worldwide. The development of PM-resistant varieties is critical, as chemical control is often insufficient and can lead to fungicide resistance. Understanding the biology and evolution of PM pathogens, such as P. fusca, is essential for the development of effective control strategies. Moreover, the emergence of fungicide-resistant isolates of P. xanthii necessitates the exploration of alternative control methods and the monitoring of resistance. The integration of genetic resistance, biocontrol agents, and sustainable agricultural practices is crucial for the long-term management of PM in cucurbits.

9.3 Recommendations for researchers and breeders

1) Exploit CRISPR/Cas9 technology: Researchers should continue to explore gene editing techniques, such as CRISPR/Cas9, to develop PM-resistant cultivars in a variety of genetic backgrounds, as demonstrated by the successful mutagenesis of CsaMLO8 in cucumber.

2) Investigate single-gene resistance: Breeders should consider utilizing single-gene resistance, as identified in zucchini squash, to simplify the breeding process for PM resistance.

3) Characterize genetic variability: It is recommended to characterize the genetic variability in field resistance to PM among different Cucurbita pepo cultivars to identify and utilize the most resistant genotype.

4) Explore biocontrol options: The potential of biocontrol agents, such as B. amyloliquefaciens LJ02, to induce systemic resistance should be further investigated as a component of integrated disease management strategies.

5) Monitor fungicide resistance: The development of rapid detection methods for fungicide resistance, such as the LAMP technique, should be utilized to monitor and manage the spread of resistant PM isolates.

6) Understand MLO gene family: Further research into the MLO gene family across Cucurbitaceae species can provide insights into the evolution and function of susceptibility factors, aiding in the identification of new targets for resistance breeding.

7) Integrate disease management strategies: An integrated approach combining genetic resistance, biocontrol, and careful fungicide use is essential to sustainably manage PM and reduce the risk of resistance development.

By following these recommendations, researchers and breeders can contribute to the development of durable PM resistance in Cucurbitaceae crops, ensuring food security and agricultural sustainability.

Acknowledgments

We would like to thank Prof. X. Fang for his careful reading of this manuscript and for his revisions and polishing of the text. We are also grateful to the two anonymous peer reviewers for their serious and rigorous academic comments, which have greatly improved the quality of the paper.

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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