Long-term Impact of Virus-Free Apple Seedlings on Fruit Quality and Yield in Commercial Orchards of Korea

Article information

Plant Pathol J. 2025;41(6):876-883

Publication date (electronic) : 2025 December 1

doi : https://doi.org/10.5423/PPJ.NT.09.2025.0135

Sang-Yun Cho, Hyun Ran Kim, Se Hee Kim, Byeonghyeon Yun, Sewon Oh

Fruit Foundation Division, National Institute of Horticultural and Herbal Science, Wanju 55365, Korea

^*Corresponding author. Phone) +82-63-238-6712, FAX) +82-63-238-6705, E-mail) chosy80@korea.kr

Handling Editor : Ju-Yeon Yoon

Received 2025 September 29; Revised 2025 October 31; Accepted 2025 November 4.

The apple (Malus domestica Borkh.) is the most economically important fruit crop worldwide (Food and Agriculture Organization of the United Nations, 2025). Apple trees are highly susceptible to a wide variety of viruses and viroids, which can significantly reduce tree vigor, fruit quality, and overall yield (Baumann and Bonn, 1988; Campbell, 1963; Hansen, 1982; Posnette et al., 1963; van Oosten et al., 1982). The main viruses affecting apples include apple chlorotic leaf spot virus (ACLSV), apple stem grooving virus (ASGV), apple stem pitting virus (ASPV), and apple mosaic virus (ApMV), while apple scar skin viroid (ASSVd) is the most common viroid (Hadidi et al., 2011). These pathogens mainly spread through vegetative propagation, such as grafting with infected scions or rootstocks, and they often remain in a latent state for long periods, making visual diagnosis difficult (Maliogka et al., 2018; Manzoor et al., 2023; Wunsch et al., 2024). Additionally, nursery practices and contaminated tools facilitate mechanical transmission, and researchers have occasionally observed seed or pollen transmission in specific virus–host interactions (Wunsch et al., 2024). In Korea, the rate of virus and viroid infections in apple orchards has been reported to reach as high as 97.3% (Lee et al., 2020).

In 2017, the domestic fruit-tree seedling market in Korea was approximately KRW 61.8 billion, and production amounted to 13.39 million units, of which 5.57 million units from the major five fruit-tree species (apple, pear, peach, grape, mandarin) were produced and 3.90 million units were distributed (Ministry of Agriculture, Food and Rural Affairs, 2019). Historically, most seedlings have been distributed by nurseries without virus indexing. In contrast, the Netherlands (Naktuinbouw), the United States (National Clean Plant Network, NCPN), Japan (National Agriculture and Food Research Organization, NARO), and Italy (Council for Agricultural Research and Analysis of Agricultural Economics, CREA) recognized decades ago that fruit tree seedlings are a high-value sector. Since the 1960s, these countries have implemented comprehensive systems for producing, certifying, and distributing virus-free (VF) seedlings, greatly strengthening their fruit industries (Barba et al., 2015; Bostock et al., 2014; Fuchs et al., 2021; Yamaguchi, 1983). In Korea, the Ministry of Agriculture, Food and Rural Affairs (MAFRA) launched initiatives in 2005, and revised them in 2016 and 2019, to promote the production and distribution of VF, high-quality fruit tree seedlings. Through these efforts, MAFRA aims to stabilize fruit production, reduce losses from viral diseases, and enhance the overall competitiveness of Korea’s fruit tree industry.

Building on these policies, the National Institute of Horticultural and Herbal Science (NIHHS) developed a program to eliminate viruses from government-bred and widely cultivated fruit tree varieties, providing VF planting materials. For apples, NIHHS first established VF propagation stock of ‘Hongro’ and ‘Fuji’ in 2008 and began distributing them as foundation material. By 2014, large-scale distribution to commercial orchards had started, improving orchard productivity and slowing the spread of latent viral infections.

This study represents the first systematic, multi-year, and multi-orchard investigation in Korea evaluating VF apple seedlings distributed to commercial orchards. We compared fruit quality and productivity between VF and virus-infected (VI) plants. We conducted long-term field monitoring of VF apple trees to track whether reinfection occurred, thereby assessing the durability of the VF status under standard orchard conditions.

In 2020, we selected farms based on the distribution records of VF seedlings maintained by the Korea Seed & Variety Service (KSVS). Of the 41 farms that had planted VF seedlings (2015–2017), 22 farms agreed to participate. We chose six farms for detailed comparison, including four that had planted both VF and conventional ‘Hongro’ seedlings (Jangsu-gun, Jeollabuk-do) and two that had planted both VF and conventional ‘Fuji’ seedlings (Andong-si, Gyeongsangbuk-do) in the same year and field. At the time of evaluation, ‘Hongro’ trees were in their fifth year after planting, while ‘Fuji’ trees were in their fourth year. We assessed virus status following the KSVS Seed Testing Guidelines. We tested five pathogens—ACLSV, ASPV, ASGV, ApMV, and ASSVd—using the one-step RT-PCR (reverse transcription polymerase chain reaction) method with the P·CHEK multiplex diagnostic kit (Nexbio, Daejeon, Korea) (Supplementary Fig. 1). VF seedlings showed an infection rate of 1.4% (4/290), while conventional seedlings showed an infection rate of 78.6% (220/280). No viroid infections occurred. Infected trees often carried co-infections with two or three viruses. We attributed the 1.4% infection rate in VF trees to the use of non-sanitized rootstocks during grafting by the nursery company. Monitoring up to 2024 showed no reinfection in VF trees, indicating that these trees remained VF for up to nine years after planting (data not shown). This result suggests that VF apple trees can stay free of reinfection under typical orchard management, likely because no ASSVd-infected trees—which could serve as mechanical transmission sources—were present in the surveyed orchards (Kim et al., 2006).

On each farm, we selected five VF and five conventional (ACLSV-, ASPV-, and ASGV-infected) trees. Each spring, we conducted virus diagnostics on newly sprouted shoots. We harvested fruit in September for ‘Hongro’ and in November for ‘Fuji’, collecting all fruits from VF and VI trees on the same day for each cultivar. Before harvest, we recorded fruit set counts. Marketable and unmarketable fruits were classified based on external appearance according to the Apple Genetic Resources Characterization Manual of the Rural Development Administration (RDA). Fruits showing asymmetry, small size, russeting, or insufficient peel coloration (less than 70%) were categorized as unmarketable. For fruit-quality assessment, we sampled 20 fruits per tree based on average fruit weight. We calculated yield by multiplying the fruit set count by the average fruit weight. We measured peel coloration with a colorimeter (CR-400, Konica Minolta, Tokyo, Japan), soluble solids content (°Brix) with a refractometer (PAL-1, Atago, Tokyo, Japan), fruit firmness with a texture analyzer (FR-5129, Lutron, Taipei, Taiwan), and titratable acidity with an automatic titrator (TitroLine 5000, SI Analytics, Mainz, Germany). We determined anthocyanin content from peel discs (1 cm diameter) using a UV-Vis spectrophotometer (UV-2700, Shimadzu, Kyoto, Japan) at 530 nm. Independent t-tests were performed in IBM SPSS Statistics version 26 (IBM Corp., Armonk, NY, USA), and we regarded differences as statistically significant at P < 0.05 (Siegelman and Hendricks, 1958).

In 2024, data collection was limited to a single orchard per cultivar. This was due to the loss of trees caused by a fire at one survey site and the removal of VI trees following a severe anthracnose outbreak at another. Consequently, the 2024 yield and quality data represent only one farm for each cultivar. Although the reduced number of orchards limited the representativeness of the 2024 dataset, the remaining sites were consistent with prior management and environmental conditions, allowing valid within-cultivar comparison with earlier years.

Fruit appearance evaluations showed minor year-to-year variations, influenced by orchard-specific conditions such as spring frost injury, anthracnose outbreaks, and higher temperatures at harvest time. However, as shown in Fig. 1, we consistently observed significant differences in fruit weight, peel color, and shape between VF and VI trees. VF apples generally appeared larger, had more vibrant color, and were less likely to be misshapen compared to VI apples. These differences were present in both the ‘Hongro’ and ‘Fuji’ cultivars. In ‘Hongro’, orchard A used a color-enhancing agent, which led to more uniform peel coloration between VF and VI fruit. In orchard B, where this treatment was not used, the difference in color intensity between VF and VI fruit was more pronounced.

Fig. 1

External appearance of apples from virus-free (VF) and virus-infected (VI) trees. (A, B) ‘Hongro’. (C, D) ‘Fuji’.

In ‘Hongro’, VF trees consistently showed higher fruit set numbers than VI trees across all surveyed years (2020–2024), with yearly differences ranging from +8.5% (2023) to +28.1% (2020) (Fig. 2). The rate of unmarketable fruit was consistently lower in VF trees compared to VI trees, at 61.9% (2020), 58.9% (2021), 69.3% (2022), 48.1% (2023), and 80.1% (2024) of the values observed in VI trees. These results indicate that virus infection increased the proportion of unmarketable fruit by approximately 20–52% relative to VF trees in this cultivar.

Fig. 2

Average number of fruit sets (NFS) and unmarketable fruits (NNMF) per tree in virus-free (VF) and virus-infected (VI) ‘Hongro’ apple trees from 2020 to 2024. Data are means ± standard deviation (n = 5 trees per treatment per year). Asterisks denote significant differences between VF and VI trees within the same year (*P < 0.05, **P < 0.01).

In ‘Fuji’, monitored from 2021 to 2024, VF trees also outperformed VI trees in fruit set, with annual increases ranging from +0.9% (2022) to +16.7% (2024) (Fig. 3). When expressed relative to VI trees set at 100, the incidence of unmarketable fruit in VF trees was only 49.1% (2021), 49.1% (2022), 51.0% (2023), and 35.2% (2024). As a result, virus infection increased the proportion of unmarketable fruit by 95.8% to 184.1% compared to VF trees. These increases were generally more significant than those seen in ‘Hongro’, indicating that virus infection had a greater negative impact on the proportion of marketable fruit in ‘Fuji’. Such differences between cultivars may be due not only to inherent varietal traits but also to variations in cultivation environments and grower management practices. In 2024, the Fuji data represent a single orchard. Notably, this orchard experienced spring frost damage in the previous year, which resulted in lower fruit set and reduced the need for fruit thinning in 2024. Consequently, more fruits were left on the trees, leading to unusually high fruit load and values that deviate from previous trends. These results should be interpreted in the context of these unique horticultural conditions.

Fig. 3

Average number of fruit sets (NFS) and unmarketable fruits (NNMF) per tree in virus-free (VF) and virus-infected (VI) ‘Fuji’ apple trees from 2021 to 2024. Data are presented as means ± standard deviation (n = 5 trees per treatment each year). Asterisks denote significant differences between VF and VI trees within the same year (*P < 0.05, **P < 0.01).

For the ‘Hongro’ cultivar (Fig. 4), VF trees showed higher per-tree yields than VI controls in all years. When compared to VI trees (set at 100), VF trees demonstrated yield increases of 30.4% in 2020, 39.6% in 2021, 34.9% in 2022, 34.4% in 2023, and 28.2% in 2024. These results highlight a strong and persistent yield benefit of VF trees over the five-year evaluation period.

Fig. 4

Total yield of ‘Hongro’ apples from virus-free (VF) and virus-infected (VI) trees. * and ** indicate significant differences between VF and VI trees at P < 0.05 and P < 0.01, respectively.

Similarly, for the ‘Fuji’ cultivar (Fig. 5), VF trees outperformed VI trees in yield in all years examined. Relative to VI trees (set at 100), VF trees achieved yield increases of 22.7% in 2021, 24.8% in 2022, 24.9% in 2023, and 25.2% in 2024. Although the amount of yield improvement was slightly lower than that seen in ‘Hongro’, VF trees still maintained a steady yield advantage throughout the assessment period.

Fig. 5

Total yield of ‘Fuji’ apples from virus-free (VF) and virus-infected (VI) trees. * denotes significant differences between VF and VI trees at P < 0.05.

For ‘Hongro’ apple trees, fruit weight varied significantly between VF and VI trees across several orchard-year combinations (Table 1). In Orchard 2, VF fruit averaged 213.3 g in 2020, which was 9.8 g heavier than fruit from VI trees (P < 0.05). In Orchard 3, VF fruit in 2020 reached 14.3 °Brix, exceeding VI fruit by 0.5 °Brix (P < 0.05), despite similar fruit weights. By 2024, VF trees in Orchard 1 produced fruit averaging 343.0 g, significantly heavier than the 304.8 g observed in VI trees (P < 0.01). In multiple orchards, no significant differences in firmness were observed between VF and VI trees.

Table 1

Annual fruit quality parameters of ‘Hongro’ apple trees grown from VF and VI stock across three orchards (2020–2024)

In the ‘Fuji’ cultivar, VF trees consistently produced heavier fruit than VI trees across all orchards and years analyzed (Table 2). In 2021, VF trees in Orchard 1 yielded fruit weighing 402.1 g, significantly surpassing the 290.8 g from VI trees (P < 0.01), while soluble sugar and acidity levels remained statistically similar. Orchard 2 showed similar trends, with VF fruit weighing 392.2 g in 2021 compared to 337.1 g for VI fruit (P < 0.01). By 2024, VF fruit in Orchard 1 maintained a notable weight advantage (344.1 g vs. 314.6 g, P < 0.01) and had slightly lower acidity (0.29% vs. 0.27%, P < 0.05). For both cultivars, annual fluctuations in sugar content and acidity likely reflected seasonal climatic variation rather than infection status alone.

Table 2

Annual fruit quality parameters of ‘Fuji’ apple trees grown from VF and VI stock across two orchards (2021–2024)

Across cultivars, VF trees generally produced larger, sweeter fruit with lower acidity than VI trees, with fruit weight showing the most consistent difference. Firmness was mostly unaffected by infection status, while variations in °Brix and acidity depended on the orchard and year. These findings indicate that viral infection in apple trees mainly restricts assimilate partitioning to fruit, which reduces marketable fruit size and secondarily influences the sugar–acid balance.

Our results demonstrate that using VF apple planting materials significantly improves yield and marketable fruit quality in commercial orchards. Both ‘Hongro’ and ‘Fuji’ cultivars showed notable benefits from virus elimination, especially in fruit size and total yield for ‘Fuji’. The substantial reduction in unmarketable fruit highlights the economic advantage of VF materials. The positive impacts of VF status on fruit quality are consistent with previous studies, which indicate that latent virus infections in apple reduce fruit size, yield, and overall tree vigor without causing obvious external symptoms (Lee et al., 2020; Meijneke et al., 1975; van Oosten et al., 1982).

VF apple trees outperformed VI trees in fruit weight, yield, and marketable quality, highlighting the negative effects of viral infections on fruit development. Viral infection in perennial fruit crops disrupts carbohydrate metabolism and translocation from source leaves to developing sinks, reducing assimilate availability for fruit growth (Rodríguez-Verástegui et al., 2022). These infections also reprogram host primary metabolism, lowering photosynthetic efficiency and carbohydrate biosynthesis (Jiang et al., 2025). Consequently, fruit size and marketable yield decline, with more pronounced effects in ‘Fuji’ than in ‘Hongro’. These results underscore the importance of strict nursery sanitation and regular orchard monitoring to minimize reinfection risk and sustain the benefits of VF planting materials under Korean conditions. The higher proportion of unmarketable fruit in VI trees supports previous findings that virus-induced imbalances in assimilates increase the occurrence of low-grade fruit (Anikina et al., 2023).

Supporting these findings, Chen et al. (2014) showed that ASGV infection in apple causes widespread changes in host gene expression without visible symptoms. This asymptomatic but metabolically disruptive effect explains the observed decreases in fruit weight, yield, and sugar content in VI trees that lack clear disease symptoms. Overall, these results demonstrate that latent viral infection can significantly affect host physiology and fruit quality, highlighting the importance of keeping VF stocks for sustainable apple production.

The long-term comparison of VF and VI trees in our study aligns with orchard trials by Meijneke et al. (1975), who showed that VF ‘Golden Delicious’ apple trees had better growth, higher yields, and better fruit quality compared to VI trees. These past data support the idea that the increased fruit set, yield stability, and fruit size seen in VF ‘Hongro’ and ‘Fuji’ trees are lasting benefits of virus removal, consistent with long-standing evidence.

Beyond yield reductions, VI fruit often showed delayed peel color development and lower soluble sugar levels compared to VF fruit. ACLSV infection in apple affects leaf physiology and primary metabolism, leading to decreased concentrations of glucose, fructose, and malic acid, as well as delayed fruit coloring (Pedrelli et al., 2025). Viral infections also interfere with sugar metabolism and secondary metabolite pathways, reducing anthocyanin production and delays ripening (Girdhar et al., 2021). These disruptions in pigment production and carbohydrate distribution closely match our observations, where VF fruit consistently reached higher coloration scores and °Brix values at harvest. Conversely, VI fruit frequently lagged behind in both measures. Overall, maintaining VF status helps preserve normal carbohydrate distribution, pigment synthesis, and sugar accumulation, supporting optimal fruit size, color, and sweetness—key factors for market value. The consistent multi-year stability of VF status in our study shows that high-quality production can be maintained with standard orchard management practices. Collectively, these results highlight the importance of expanding certified VF seedling programs in commercial apple production, aligned with successful models applied in the Netherlands, the USA, Japan, and Italy.

In 2023, an economic evaluation was conducted as part of an RDA-funded project, integrating field trials (Cho et al., 2024) and on-farm surveys of 20 commercial orchards. Based on these data, cumulative income resulting from the nationwide VF seedling supply policy was calculated, and the broader economic ripple effects were analyzed using the input-output model (Leontief, 1936). The results showed that cultivation of VF ‘Hongro’ apple seedlings led to an average net income increase of KRW 825,000 per 10 a. Nationwide adoption is projected to raise annual growers’ income by KRW 160 billion and achieve cumulative gains of KRW 1.86 trillion by 2045. Input-output analysis further indicated a production inducement effect of KRW 515.2 billion, value-added gains of KRW 239.4 billion, and the creation of over 13,000 jobs in related industries. These findings, which have also been reported in a press release, highlight the significant economic and societal impacts of expanding VF seedling programs in Korea (Rural Development Administration, 2023).

In conclusion, this study provides the first systematic, long-term on-farm evaluation of VF apple seedlings in Korea, offering direct evidence of their effectiveness in real-world commercial orchards. Our multi-year monitoring demonstrated that, when certified planting material is used in combination with standard orchard management, the risk of virus reinfection can be greatly reduced, as seen in established European and Japanese certification systems (Yamaguchi, 1983). The clear economic and quality benefits identified in this study strongly support the further expansion of national VF seedling programs in Korea, in line with international best practices. These findings not only highlight the practical advantages of virus elimination but also provide a valuable precedent for future research and policy development in the management of perennial fruit crops.