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ISSN : 1225-8504(Print)
ISSN : 2287-8165(Online)
Journal of the Korean Society of International Agriculture Vol.37 No.3 pp.241-249
DOI : https://doi.org/10.12719/KSIA.2025.37.3.241

Evaluation of Varietal Resistance to Grapevine Leaf Rust and Change of Chlorophyll Contents in Grapevine Genotypes by Infection with Phakopsora euvitis

Zar Le Myint*, Ji Min Yun*, Jae Hyun Lee*, Ramalingam Srinivasan*, Soon Young Ahn*, Seung Heui Kim**, Hae Keun Yun*,†
*Department of Horticulture and Life Science, Yeungnam University, Gyeongsan 38541, Republic of Korea
**Fruit Tree Department, Korea National University for Agriculture and Fisheries, Jeonju 54874, Republic of Korea
† Corresponding author (Phone) +82-53-810-2942 (E-mail) haekeun@ynu.ac.kr
September 3, 2025 September 10, 2025 September 15, 2025

Abstract


Grapevine l eaf rust (GLR) c aused b y Phakopsora euvitis diminishes fruit quality and reduces yield in viticulture, making it one of the world’s most significant fruit crop threats. To develop GLR-resistant grape varieties, substantial efforts have been made to select rust-resistant genes and determine effective strategies f or achieving durab le resistance in grapevines. This study aims to identify genetic resources resistant to GLR by investigating disease incidence in vineyards and symptom development in grapevines inoculated with pathogens. Fifty-seven genotypes from Ampelopsis brevipedunculata, Vitis acerifolia, V. aestivalis, V. amurensis, V. cinerea, V. coignetiae, V. flexuosa, V. labrusca, V. labruscana, V. rotundifolia, and V. vinifera were evaluated for rust disease incidence over four years (2021 –2024) at Yeunganm University. Three plants per genotype were potted and sprayed with a pathogen suspension to assess disease incidence on their adaxial leaf surfaces in a greenhouse. Variation in resistance to GLR was observed among genotypes within each species. Resistant genotypes of V. coignetiae exhibited no symptoms on their leaves, while severe infections were noted in the leaves of susceptible genotypes of A. brevipedunculata, V. amurensis, V. flexuosa, V. labruscana, and V. vinifera. None of the tested V. rotundifolia genotypes displayed yellow pustules and remained unaffected for three weeks after artificial inoculation. These findings highlight the potential of V. rotundifolia and V. coignetiae as valuable genetic resources for breeding rust-resistant grapevines. Chlorophyll content was comparable across all uninfected genotypes. While resistant genotypes maintained relatively stable chlorophyll levels, the average chlorophyll content in the majority of susceptible genotypes was significantly lower following inoculation than before. This negative relationship indicates a general decline in photosynthetic capacity due to disease development in grapevines. Identifying resistant genotypes among both resistant and susceptible genotypes across different Vitis species provides crucial insights for developing new grape varieties with improved resistance to GLR.


Genotypes , Germplasm , Grapevine leaf rust , Phakopsora euvitis , Vitis

Phakopsora euvitis 감염에 따른 포도나무 유전자원의 잎녹병 품종 저항성 검정 및 엽록소 함량 변화

자리민*, 윤지민*, 이재현*, 라말인감스리니바산*, 안순영*, 김승희**, 윤해근*,†
*영남대학교 원예생명과학과
**한국농수산대학교 과수과

초록

    INTRODUCTION

    Grapevine is essential to the food industry, providing economic, cultural, scientific, and environmental advantages, and cultivated for thousands of years in the world. However, grapevines are susceptible to various diseases caused by fungi, bacteria, and viruses resulting in reduction of productivity and quality of grapes. Among diseases, grape leaf rust (GLR), infected with by the Phakopsora euvitis, mainly manifests as chlorotic patches on the adaxial surface and yellow orange uredinia on the abaxial surface of the leaves (Ono, 2000). Severe infections cause premature defoliation, which lowers photosynthesis and affects vine health, yield, and fruit quality in tropical, subtropical, and a few temperate areas of the Americas, Asia and Australia (Nogueira Júnior et al., 2017). The polycyclic disease GLR spreads quickly through urediniospores by contaminated tools, infected plant material, rain splashes, and winds. Defoliation caused by GLR inhibits the carbohydrate reserves in roots to prevent the early development of grapevines in following seasons (Keller, 2010;Vida and Tessmann, 2005). Although synthetic fungicides have been sprayed to protect effectively the vines and grapes from the pathogens, the use of chemicals is costly, and causes harmful effects on the environment. In contrast, the plantation of genetic resistant varieties is a cost-effective, long-lasting, and environmentally beneficial method of disease control (Salgotra and Gupta, 2015). Thus, the use of rust-resistant grape varieties and cultivars is considered as a crucial element of integrated disease management and sustainable viticulture.

    Grapevine germplasm, which includes both cultivated kinds and wild species, is essential for breeding programs to enhance disease resistance, climate change adaptability, and fruit quality. Wild grapevine species are valuable genetic resources for breeding program for resistance to pests, diseases, and environmental challenges, characteristics which are frequently absent in cultivated varieties (Engels, 2003;Day-Rubenstein et al., 2005;Healy and Dawson, 2019). Breeding for resistance to foreign stresses has emerged as a major objective in genetic improvement attempts in grapevines.

    In grapevine, rust incidence causes a significant decrease in leaf chlorophyll by chloroplast degeneration and results in reduction of photosynthetic capacity, carbohydrate metabolism, and yield in viticulture (Nogueira Júnior et al., 2017;Rasera et al., 2019). Thus, chlorophyll content monitoring offers insights into the physiological consequences of infection and the severity of the disease.

    Identifying and characterizing resistant genotypes are therefore a primary step for enhancing grapevine resistance to rust in breeding programs. Therefore, the objectives of present research were to select genetic resources resistant to rust disease by evaluating the development of lesions in the grapevine leaves infected with pathogens among grape germplasm, and to explore the relationship between disease resistance and chlorophyll content in the leaves by measuring chlorophyll levels in leaves affected by pathogen infections. This study can help the effective use of genetic resources to develop varieties resistant to rust and support the management of sustainable viticulture in the future.

    MATERIALS AND METHODS

    1. Plant materials and pathogens

    A total of 57 genotypes (Table 2), including eleven species_ Ampelopsis brevipedunculata, Vitis acerifolia, V. aestivalis, V. amurensis, V. cinerea, V. coignetiae, V. flexuosa, V. labrusca, V. labruscana, V. rotundifolia, and V. vinifera, were evaluated for rust disease incidence from 2021 to 2024 in a vineyard at Yeungnam University, Gyeongsan, Korea. In 2024, cuttings of these genotypes were planted in pots filled with fine soil and cultivated to have developed 15-20 leaves suitable for artificial inoculation with P. euvitis in a controlled-environment greenhouse. Urediniospores of P. euvitis, collected from infected leaves of grapevines were used for artificial inoculation. The spores were harvested in 2023 using a mini vacuum cleaner equipped with brushes and subsequently stored at –80°C to maintain their viability for future use.

    2. Inoculation of pathogen

    In the field investigation, inoculation was unnecessary, as the genotypes were naturally infected by the pathogen. In contrast, artificial inoculations were performed on potted plants from 57 grapevine genotypes maintained in a controlled- environment greenhouse. A spore suspension of Phakopsora euvitis (8 × 10⁵ spores/mL in distilled water) was sprayed onto the abaxial (lower) leaf surfaces. The plants inoculated with pathogens were kept in a dark, moist chamber at 25°C for 48 hours to facilitate infection and moved to the controlled-environment greenhouse for evaluation.

    3. Evaluation of rust disease incidence in field and greenhouse environments

    From 2021 to 2024, annual field assessments to evaluate rust disease incidence were conducted in October each year following the method of Myint et al. (2022) among 57 grapevine genotypes representing eleven species grown at Yeungnam University vineyard. For the evaluation of rust incidence in greenhouse trials, three potted plants per genotype were inoculated with spore suspension of pathogen on the adaxial leaf surfaces. The incidence of lesions by artificial inoculation was assessed from one week post-inoculation at approximately weekly intervals for three consecutive weeks. In the vineyard evaluation, rust severity was assessed annually (2021-2024) on five leaves per shoot, beginning with the fourth leaf from the shoot apex. Three shoots per vine were evaluated per replicate, with three replicates per genotype. For the evaluation of incidence of rust by pathogen inoculation in greenhouse, all leaves from one potted plant (15-20 leaves) were assessed per replicate, with three replicates conducted under controlled conditions. Assessments focused on the abaxial (underside) surface of the leaves, where yellow rust pustules typically developed. Rust severity was quantified using a lesion index ranging from 0 to 5 as described Table 1, based on the percentage of the leaf area covered with the yellow pustules (Myint et al., 2022;Angelotti et al., 2008). A score of 0 indicated no visible symptoms; 1 corresponded to 0.1–15% lesion coverage; 2 to 15–30%; 3 to 30–50%; 4 to 50–75%; a nd 5 i ndicated s evere infections, with 7 5– 100% of the leaf area affected. Based on lesion index scores, inoculated plants were classified into six categories: highly resistant (score 0), resistant (score 1), moderately resistant (score 2), moderately susceptible (score 3), susceptible (score 4), and highly susceptible (score 5).

    4. Measurement of leaf chlorophyll content following artificial inoculation

    Chlorophyll content was monitored in vines artificially inoculated with pathogens simultaneously with disease assessments from one week after the first inoculation at weekly intervals for three weeks. To explore whether rust infection (under controlled greenhouse conditions) has a physiological effect on the plant’s photosynthetic capacity, as reflected by chlorophyll content. The chlorophyll content was determined using the Soil Plant Analysis Development (SPAD) index, which reflects the chlorophyll level in leaves. The chlorophyll content of each potted plant’s leaves was measured using a SPAD502 Plus chlorophyll meter, a small, portable device from Konica Minolta Sensing, Inc., Sakai, Osaka, Japan, that assesses chlorophyll concentration without causing damage. For each leaf, two SPAD readings were taken and averaged to produce a single measurement. The SPAD (Soil Plant Analysis Development) meter, which measures chlorophyll content based on light absorption at red and near-infrared wavelengths, was used to measure the chlorophyll content of each leaf (avoiding major veins). The two readings were averaged to produce a single SPAD value for each leaf. The chlorophyll content of three representative plants of each genotype was determined using the SPAD meter. The SPAD readings from weeks 1, 2, and 3 after inoculation were averaged and compared with pre-inoculation values in order to assess the overall physiological impact of rust infection.

    RESULTS AND DISCUSSIONS

    1. Assessment of rust disease severity across grapevine species and genotypes under greenhouse and field conditions

    A total of fifty-seven genotypes from eleven grapevine species (Table 2) were evaluated for their resistance to P. euvitis infection by both natural field assessment (FA) and controlled greenhouse inoculation (GI).

    Resistance levels were classified as highly resistant (HR), resistant (R), moderately resistant (MR), moderately susceptible (MS), susceptible (S) and highly susceptible (HS) as described in table 1. It was shown that there was variation in resistance to GLR among genotypes even within each species. The disease severity scores ranged widely, indicating distinct resistance profiles across the evaluated species. There was a high variation in resistance among genotypes in A. brevipedunculata to GLR, with most genotypes rated MS or MR in the field and R in greenhouse inoculation tests. Only one genotype, SVITKO 1307-2, achieved HR in both field assessment and greenhouse inoculation, while the rest were more susceptible in field conditions suggesting high susceptibility possibly due to environmental stress or pathogen preference. V. cinerea genotypes ranged from MS to R in the field and generally R in the greenhouse. Three genotypes of V. coignetiae, Meoru SVITKO 17-2, Meoru SVITKO 21-1, and Wolchulmeoru, maintained HR or R in both assessments. It was shown that V. flexuosa presented moderate resistance (MR) in both field assessment and greenhouse inoculation, indicating limited rust tolerance. The genotypes of V. labrusca were mostly MR in the field and R in greenhouse assessments, except ‘Super Hamburg’, which graded to MR in greenhouse inoculation. The genotypes of V. vinifera exhibited high susceptibility compared to other species, with several genotypes rated MR or MS in both environments. Species such as V. labruscana, V. acerifolia, V. amurensis, and V. aestivalis were proven to show moderate and variable responses to GLR disease. None of the tested V. rotundifolia genotypes displayed yellow pustules and were kept unaffected for three weeks after artificial inoculation. All of the tested genotypes of V. rotundifolia exhibited resistance in greenhouse conditions and nearly complete resistance in the field, making it the most rust-resistant species in this study.

    According to Clayton and Ridings (1970), certain varieties of V. rotundifolia and V. labrusca exhibit high resistance to leaf rust. It is reported that cultivars derived from V. labrusca, V. vinifera, and V. aestivalis were susceptible, with most V. vinifera and V. labrusca cultivars, as well as their interspecific hybrids exhibited susceptibility to GLR (Hennessy et al., 2007;Angelotti et al., 2008). Camargo (2008) reported that Vitis labrusca and Vitis vinifera, the most widely cultivated grapevine species in Brazilian vineyards, were hosts of grapevine leaf rust. Moreover, Sonego et al. (2005) that cultivars originating from Vitis labrusca, V. vinifera, and V. rotundifolia are susceptible to GLR under Brazilian field conditions. Clayton and Ridings (1970) reported that V. rotundifolia cultivars showed remarkable resistance, and in many cases complete immunity, to the rust fungus, in contrast to the higher susceptibility observed in cultivars derived from V. labrusca and V. vinifera. This comparative assessment highlights that there is the significant variation in rust disease resistance among grapevine species and that V. rotundifolia stands out as the most promising source of rust resistance, followed closely by V. tiaecoigne. In contrast, V. vinifera, V. flexuosa, and A. brevipedunculata showed high susceptibility, indicating their vulnerability under both controlled and field conditions. These findings provide critical insights for selecting parental material in breeding programs aimed at developing rust-resistant grapevine cultivars.

    2. Correlation between disease incidence of field infection and greenhouse inoculation

    The scatter plot (Fig. 3) shows the correlation between disease severity observed in controlled greenhouse inoculation (x-axis) and disease incidence in field (y-axis) across eleven Vitis species. Each point represents disease severity with the same color in the same species among genotypes. The slope value of 0.3241 indicates a weak positive relationship in a-linear equation, as there is high severity in greenhouse inoculation, there is a slight severity in field infection test in group pf genotypes.

    The intercept of 0.8082 suggests that even genotypes with very low greenhouse disease incidence tend to show some infection in the field, which would result from the environmental factors or natural susceptibility in the vineyards. The very low R² value (0.0772) indicates that the resistance to GLR in assessment in the greenhouse does not predict consistently with the resistance in the field for among genotypes. Some species like V. rotundifolia appear to maintain low disease severity in both conditions (consistent resistance), while others such as A. brevipedunculata show high variations in susceptibility of GLR disease between field investigation and inoculation test in the greenhouse. Variability among species shows that disease occurrence is influenced by environmental factors like temperature and humidity. It is hard to find close connection between the evaluation of disease severity in controlled greenhouse and the assessment of disease incidence in actual field conditions. Disease severity can be altered by environmental conditions and inoculation pressure, therefore, testing in various environments is recommended to improve reliability in selecting resistant to GLR in breeding program. The analysis of resistance to GLR among Vitis species indicates that validation of resistance to disease by the assessment by natural infection in the field is required as well as by inoculation in the greenhouse.

    3. Correlation between disease incidence of greenhouse inoculation and leaf chlorophyll content in grapevine genotypes

    The loss of chlorophyll content in grapevine leaves is strongly correlated with the presence and severity of fungal pathogens, making it a valuable indicator of disease status (Del F rari e t al., 2025). There is a s catter plot o f greenhouse inoculation intensity versus leaf chlorophyll levels across different grapevine genotypes (Fig. 4). Each point with the same color in diagram represents the results from the analysis of one Vitis species. The regression line (y = −0.0711x + 0.0204) indicates a slight negative trend with a low coefficient of determination (R² = 0.1365). It suggests that while some genotypes with high disease incidence exhibited moderate to high chlorophyll loss, others maintained the content of chlorophyll even in the leaves infected with pathogens. There were comparable basic levels in chlorophyll content, with SPAD values between 20.9 and 35.4 in all the genotypes in uninfected with pathogen. It was found that relatively stable chlorophyll levels were kept in the resistant genotypes, suggesting a limited physiological impact of the pathogen. In particularly, relatively stable SPAD values were maintained in highly resistant species, V. rotundifolia, and some genotypes including SVITKO 1141, SVITKO 13072, Rem NE4 (GVIT 0994), and wolchulmeoru all over time. In contrast, the average chlorophyll content during the three weeks following inoculation were considerably lower than the pre-inoculation values in the majority of susceptible genotypes, suggesting a decline in photosynthetic efficiency brought about by the onset of the process of pathogen infection. The moderately susceptible genotypes (188. 08 rootsotck, Canadice, and Sylvaner) showed a significant decrease in mean chlorophyll content throughout the three-week post-inoculation period with continuous physiological stress.

    Rust fungi, such as P. euvitis, infect many crops to mostly harm leaves, interfering with photosynthesis and lowering potential output (Agrios, 2005). Plant diseases frequently distrupt the photosynthesis system, resulting in a reduction in chlorophyll content, which can be used as a physiological indicator of the health and vigor of the plant (Anić et al., 2024;CabelloPasini et al., 2011;Canton et al., 2017). In grapevine, rust disease caused by P. euvitis causes a significant decrease in leaf chlorophyll by inducing chloroplast degeneration and disrupting pigment synthesis (Nogueira Júnior et al., 2017;Rasera et al., 2019). The loss of chlorophyll is characterized by yellowing, necrosis, and premature senescence, and is linked to a decline in photosynthetic capacity, carbohydrate metabolism, and overall plant growth and yield (Reynard et al., 2022;Teixeira et al., 2020;Petit et al., 2006). The leaves infected with pathogens may exhibit virtual lesions, where photosynthesis is impaired even in asymptomatic areas surrounding pustules, while localized green islands may temporarily retain chlorophyll (Scholes and Rolfe, 1996).

    This negative relationship reflects the general decline in photosynthetic capacity and overall plant vitality as lesions were developed to severe disease. Such patterns occur because fungal, bacterial, or viral infections commonly interfere with chloroplast function, reducing photosynthesis and chlorophyll production in date palm seedlings, apple leaves, and jujube trees (Arafat, 2024;Bertamini et al., 2002;Xue et al., 2018). These data show that chlorophyll degradation is linked to rust susceptibility and occurs consistently throughout the infection period. According to these findings, the extent of chlorophyll degradation is related to the severity of the illness and may be used as a physiological marker for resistance screening in various grapevine genotypes.

    CONCLUSIONS

    These findings highlight the potential of Vitis rotundifolia and V. coignetiae as valuable genetic resources for breeding rust-resistant grapevines. It points out that there are both resistant and susceptible types among different grapevine species, showing genetic diversity useful for breeding. Selecting resistant genotypes is important for managing diseases sustainably, which can reduce the need for chemicals and help grapevines healthy from leaf rust. Future research should focus on understanding the genetic mechanisms of resistance and integrating certified traits into commercial grapevine varieties. Elucidating a diverse genetic background in grapevines is vital for successful viticulture, and useful in developing new varieties resistant to disease by identification of the genes related with the expression of resistance in vines. It provides the important information necessary in resources resistant to diseases, in production of high-quality grapes, and in breeding new varieties lowering environmental and economic impacts related to disease control.

    적 요

    포도나무 잎녹병(Phakopsora euvitis)은 세계에서 가장 중요한 과실 중 하나인 포도 재배에서 과실 품질의 저하와 수확량 감소 를 초래한다. 포도나무 잎녹병에 의한 피해를 줄이기 위하여 저 항성인 품종 개발을 위해 저항성 유전자와 지속적인 저항성인 포 도나무 육종소재를 개발하려는 많은 노력이 기울여져 왔다. 본 연구는 포도원에서의 병해 발생과 병원균을 접종한 포도나무에 서의 병징 발현을 조사하여 포도나무 잎녹병 저항성 육종소재를 선발하고자 수행되었다. 영남대학교 포도원에서 Ampelopsis brevipedunculata, Vitis acerifolia, V. aestivalis, V. amurensis, V. cinerea, V. coignetiae, V. flexuosa, V. labrusca, V. labruscana, V. rotundifolia, V. vinifera에 소하는 57개 포도나무 유전자원에 대해 4년 (2021-2024) 동안 녹병 발생을 조사하였다. 각각 3개의 화분에 식 재한 유전자원을 대상으로 병원균 현탁액을 분무한 후 온실에서 잎 뒷면의 병 발생률을 평가하였다. 각 품종의 유전자원 간에 포 도나무 잎녹병 저항성에는 차이가 있었으며, V. coignetiae의 저 항성 계통에는 잎에 병징이 출현하지 않았지만, A. brevipedunculata, V. amurensis, V. flexuosa, V. labruscana 및 V. vinifera의 감수 성 계통에는 잎에 진전된 병징이 출현하였다. 검정된 V. rotundifolia 의 모든 계통에서 인공 접종 후 3주 동안 병징이 나타나지 않았다. V. rotundifolia와 V. coignetiae의 저항성 계통은 포도나무 잎녹병 저항성 포도나무를 육종하기 위한 중요한 육종 소재로서 활용될 수 있을 것이다. 병원균에 감염되지 않은 모든 유전자형 에서 엽록소 함량은 비슷하였다. 병원균을 접종한 저항성 계통에 서 엽록소 수준이 비교적 안정적으로 유지되었지만, 대다수 감수 성 유전자형에서 평균 엽록소 함량은 접종 후에 접종 전보다 유 의성 있게 낮았다. 포도나무 잎녹병 저항성과 엽록소 함량의 관 계는 부의상관 관계를 나타내어, 포도나무 잎에서 병 발생으로 인한 광합성 능력의 전반적인 감소를 초래한다. 다양한 포도나무 계통을 대상으로 포도나무잎녹병 저항성 육종소재의 선발을 통 해 저항성 포도품종의 개발과 저항성 발현 기작 구명에 크게 기 여할 것이다.

    ACKNOWLEDGMENTS

    This study was supported by R&D Grant (Project No. RS-2023-00231592) from Rural Development Administration of Republic of Korea.

    Figure

    JKSIA-37-3-241_F1.jpg

    Grapevine leaf rust incidence among Vitis germplasm from 2021 to 2024 in the vineyard.

    JKSIA-37-3-241_F2.jpg

    Disease incidence in fifty-seven Vitis genotypes following inoculation with P. euvitis under greenhouse condition.

    JKSIA-37-3-241_F3.jpg

    Correlation between greenhouse inoculation and field infection severity across eleven Vitis species.

    JKSIA-37-3-241_F4.jpg

    Relationship between chlorophyll loss (SPAD index; n=15) and disease incidence in P. euvitis-infected grapevine leaves under greenhouse inoculation.

    Table

    Scoring scale for disease incidence of P. euvitis on the abaxial surface of grapevine leaves exhibiting rust symptoms.

    HR is Highly resistant.

    Resistance to P. euvitis evaluated by incidence and list of Vitis spp.

    FA is Field Assessment and, GI is Greenhouse Inoculation

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