علوم باغبانی ایران

علوم باغبانی ایران

مقاومت آنتی‌زنوزی در پایه‌های سیب نسبت به شته مومی: رمزگشایی ارتباط صفات ریشه و اکولوژی شته

نوع مقاله : مقاله پژوهشی

نویسندگان
سازمان تحقیقات، آموزش و ترویج کشاورزی، مؤسسه تحقیقات علوم باغبانی، پژوهشکده میوه‌های معتدله و سردسیری، کرج، ایران
چکیده
مقاومت آنتی‌زنوزی پایه‌های سیب به شته مومی (Eriosoma lanigerum Hausmann) نقش کلیدی در کاهش خسارات اقتصادی ناشی از این آفت دارد. این پژوهش با هدف شناسایی مکانیسم‌های مقاومت و بررسی ارتباط آن‌ها با ویژگی‌های ریشه، طی هفت سال انجام شد؛ به‌طوری‌که سه سال نخست پژوهش (۱۳۹۶–۱۳۹۸) به تولید و آماده‌سازی مواد گیاهی و چهار سال بعد (۱۳۹۹–۱۴۰۲) به ارزیابی مقاومت اختصاص یافت. این مطالعه روی ده ژنوتیپ هیبرید حاصل از تلاقی پایه‌های پاکوتاه بومی و تجاری (M9، M27، B9) در ایستگاه تحقیقات کمالشهر کرج انجام شد. نمونه‌برداری دوهفته‌ای از کلنی‌های شته و ارزیابی شاخص‌هایی مانند ترجیح میزبانی، شیوع، تجمع کلنی و طاقچه زیستگاهی انجام گرفت. تحلیل عاملی دو مؤلفه اصلی شامل جذابیت میزبانی و استقرار موفق (با تبیین ۸۷/۱ درصد از واریانس) و محدودیت زیستگاهی (با تبیین ۱۲/۵ درصد از واریانس) را شناسایی کرد. خوشه‌بندی پایه‌ها چهار گروه مقاومتی شامل حساس، نیمه‌حساس، نیمه‌مقاوم و مقاوم را نشان داد. پایه M9op3 به‌عنوان مقاوم‌ترین ژنوتیپ، با کمترین شاخص ترجیح (۰/۶۳) و بالاترین شاخص طاقچه بهره‌برداری‌نشده (۰/۶۳)، شناسایی شد. همبستگی مثبت بین تراکم ریشه‌های مولد و شاخص ترجیح (۰/۵۱) و همبستگی منفی بین طول منطقه ریشه‌زا و پتانسیل زیستگاهی (۰/۵۹−) نشان داد که صفات ریشه با مقاومت آنتی‌زنوزی ارتباط دارند. نتایج بر اهمیت تلفیق صفات مورفولوژیک ریشه، شامل کاهش تراکم ریشه‌های مولد و افزایش طول منطقه ریشه‌زا، با سازوکارهای اکولوژیک در توسعه پایه‌های مقاوم تأکید دارد. این یافته‌ها می‌تواند مبنایی برای تدوین راهبردهای اصلاحی به‌منظور گزینش ژنوتیپ‌های پایدارتر، کاهش مصرف سموم و توسعه باغبانی پایدار فراهم کند.
کلیدواژه‌ها
موضوعات

عنوان مقاله English

Antixenosis Resistance in Apple Rootstocks Against the Woolly Apple Aphid: Deciphering the Relationship Between Root Traits and Aphid Ecology

نویسندگان English

Masoud Latifian
Dariush Atashkar
Agricultural Research, Education and Extension Organization, Horticultural Sciences Research Institute, Temperate Fruits Research Center, Karaj. Iran,
چکیده English

Antixenosis resistance in apple rootstocks against the woolly apple aphid (Eriosoma lanigerum Hausmann) plays a pivotal role in reducing the economic losses caused by this pest. This study aimed to elucidate the mechanisms underlying antixenosis resistance and their association with root traits. The study was conducted over seven years, with the first three years (2017–2019) devoted to the production and preparation of plant materials and the subsequent four years (2020–2023) to resistance assessment. Ten hybrid genotypes derived from crosses between dwarfing native genotypes and commercial rootstocks (M9, M27, and B9) were evaluated at the Kamalshahr Research Station in Karaj, Iran. Biweekly sampling of aphid colonies was conducted, and indices including host preference, prevalence, colony aggregation, and habitat niche were evaluated. Factor analysis identified two principal components, namely host attractiveness and successful establishment (87.1% of the variance) and habitat limitation (12.5% of the variance). Hierarchical clustering categorized the rootstocks into four resistance groups: susceptible, semi-susceptible, semi-resistant, and resistant. M9op3 was identified as the most resistant genotype, exhibiting the lowest host preference index (0.63) and the highest unexploited habitat niche index (0.63). Positive correlations between root sucker density and host preference (r = 0.51), along with negative correlations between root elongation zone length and habitat potential (r = −0.59), confirmed the association of root traits with antixenosis resistance. The results emphasize the importance of integrating morphological root traits, particularly reduced sucker density and increased root elongation zone length, with ecological mechanisms in the development of resistant rootstocks. These findings provide a basis for breeding strategies aimed at selecting resilient genotypes, reducing pesticide use, and promoting sustainable horticulture.

کلیدواژه‌ها English

rootstock breeding
hybrid genotypes
biotic stress
ecological niches
integrated pest management

Extended Abstract

Introduction

Apple (Malus domestica Borkh.) is a cornerstone of Iran's horticultural economy. However, its productivity is severely threatened by the woolly apple aphid (Eriosoma lanigerum), a pest responsible for significant economic losses. Antixenosis resistance, a non-preference mechanism that deters pest colonization, plays a pivotal role in mitigating aphid damage. Historically, breeding programs such as the Malling–Merton (MM) series have developed resistant rootstocks; however, evolving aphid biotypes and ecological variability continue to pose persistent challenges. This study aimed to elucidate the relationship between root morphological traits and aphid ecology to identify hybrid rootstocks with enhanced antixenosis resistance. By combining root architecture analysis with ecological indices, this research sought to promote sustainable apple cultivation by reducing reliance on pesticides and enhancing rootstock resilience. The objectives were to evaluate host preference, colony aggregation, and habitat niche utilization across ten hybrid rootstocks derived from crosses between dwarfing Iranian native genotypes (e.g., Azop and AZ) and commercial rootstocks (M9, M27, and B9). The study also examined how root traits, including density, length, and the extent of the rhizogenic zone, influence aphid behavior, thereby providing a framework for future breeding strategies.

 

Materials and Methods

The seven-year study (2017–2023) was conducted at the Kamalshahr Research Station in Karaj, Iran, under controlled environmental conditions. Ten hybrid rootstocks were evaluated, including crosses between dwarfing Iranian native genotypes (Azop and AZ) and commercial rootstocks (M9, M27, and B9). Aphid colonies were sampled biweekly across the root, collar, trunk, and branch zones using non-destructive counting methods to minimize disruption to natural aphid behavior. Key resistance indices, including the Colony Preference Index (C-Aphis), Prevalence Index (PI), and Unexploited Habitat Niche (zi), were calculated to quantify host preference, aphid prevalence, and ecological constraints, respectively. Root morphological traits, including root density, length, rhizogenic zone extent, and rooting percentage, were measured using standardized protocols. Statistical analyses included Principal Component Analysis (PCA) to identify latent resistance factors and hierarchical clustering to categorize rootstocks according to resistance levels. Data normality was assessed using the Kolmogorov–Smirnov test, and correlations between root traits and aphid responses were analyzed using SPSS v27. The experimental design incorporated replication across multiple growing seasons to account for environmental variability.

 

Results and Discussion

Principal Component Analysis revealed two dominant factors explaining 99.6% of the total variance in resistance: Host Attractiveness and Colonization Success (87.1% of the variance) and Habitat Limitation (12.5% of the variance). The first factor was strongly correlated with indices such as C-Aphis (loading = 0.993) and PI (loading = 0.993), emphasizing the role of rootstock attractiveness in aphid colonization. The second factor, associated with zi (loading = 0.997), highlighted ecological constraints limiting aphid exploitation. Cluster analysis grouped the rootstocks into four resistance categories: susceptible, semi-susceptible, semi-resistant, and resistant. Highly susceptible genotypes, such as Azop2-85, exhibited a high C-Aphis value (0.59) and a low zi value (0.59), indicating limited ecological deterrence, whereas semi-susceptible (e.g., B9op) and semi-resistant (e.g., AZ*M27) rootstocks showed incremental improvements. The most resistant genotype, M9op3, exhibited the lowest C-Aphis value (0.63) and the highest zi value (0.63), suggesting strong antixenosis resistance through reduced host attractiveness and enhanced ecological barriers.

Correlations among root traits and aphid responses revealed that greater root density was positively associated with aphid preference (r = 0.51, p < 0.01), possibly due to enhanced vascular access, whereas greater root elongation zone length was negatively correlated with habitat exploitation (r = −0.59, p < 0.01), suggesting that structural characteristics may limit aphid habitat utilization. Shorter root lengths were also associated with reduced habitat potential (r = −0.59, p < 0.01), consistent with the compact root architecture observed in M9op3. These findings are consistent with previous studies emphasizing the role of root morphology in pest resistance, in which sparse feeder roots may limit nutrient access and compact rhizogenic zones may reduce the availability of chemical attractants. The integration of ecological metrics such as zi provides a novel framework for evaluating resistance, complementing traditional indices and improving the precision of rootstock selection.

 

Conclusions

This study demonstrates that antixenosis resistance is a multifactorial trait shaped by root morphology and ecological dynamics. The resistant rootstock M9op3, characterized by low root density and compact rhizogenic zones, effectively deterred aphid colonization by restricting access to vascular tissues and minimizing chemical attractants. Breeding programs targeting root architectural traits, such as sparse feeder roots and limited rhizogenic zones, may enhance resistance and provide a sustainable alternative to pesticide-dependent pest management. The integration of ecological metrics, such as zi, offers a novel approach to resistance evaluation, supporting precision in rootstock selection and addressing challenges associated with evolving aphid biotypes. The practical implications include reduced reliance on pesticides and greater alignment with Integrated Pest Management (IPM) goals. Future research should investigate the biochemical role of root exudates in aphid behavior and evaluate rootstocks under abiotic stresses, such as drought, to ensure climate resilience. By bridging agronomy and ecology, this study contributes to efforts toward sustainable horticulture and provides practical insights for developing aphid-resistant apple cultivars while balancing productivity and environmental stewardship.

 

Author Contributions

All authors contributed equally to the development of this manuscript from the initial draft to the final submitted version, including all subsequent revisions. 

 

Data Availability Statement

Data available on request from the authors.

 

 

Acknowledgements 

This research was supported by grants from Agricultural Biotechnology Research Institute of Iran (ABRII) Project No. 3-33-99-046992.

 

Ethical considerations

The authors avoided data fabrication, falsification, plagiarism, and misconduct.

 

Conflict of interest 

The author declares no conflict of interest.

منابع

آتشکار، د.، عبدالهی، ح.، و ارشادی، ع. (1399). تأثیر تنش خشکی بر شاخص‌های فیزیولوژیکی و بیوشیمیایی پایه‌های هیبرید سیب. مجله علوم و فناوری باغبانی ایران، 21(2)،  107-122 https://doi.org/20.1001.1.16807154.1399.21.2.2.8 .
آتشکار، د.، پیرخضری، م.، و تقی‌زاده، ع. ا. (1395). تولید و ارزیابی اولیه پایه‌های هیبرید سیب (Malus domestica Borkh.). مجله علوم باغبانی ایران، 47(2)،   235-229 https://doi.org/10.22059/ijhs.2016.5834 .
قائدی، ح.، کچیلی، ف.، لطیفیان، م.، و فرخی نیا، ر. (1399). پراکنش مکانی و زمانی سوسک‌های کرگدنی (Oryctes spp.) در نخلستان‌های استان خوزستان. تحقیقات آفات گیاهی، 10(2)، 1- 12. https://doi.org/10.22124/iprj.2020.4292
لطیفیان، م.، سیدالاسلامی، ح.، و خواجه علی، ج. (1388). مقایسه چند روش نمونه‌برداری برای برآورد تراکم جمعیت زنجره برگ مو (Arboridia kermanshah Dlabola) (Hem., Cicadellidae).  مجله تحقیقات حشره‌شناسی دانشگاه آزاد اسلامی، 1(2)، 95- 108. https://sanad.iau.ir/Journal/jer/Article/915520
 
 
 
 
REFERENCES
Antônio, A. D. C., Silva, D. J. H. D., Picanço, M. C., Santos, N. T., & Fernandes, M. E. D. S. (2011). Tomato plant inheritance of antixenotic resistance to tomato leaf miner. Pesquisa Agropecuária Brasileira, 46, 74–80. https://doi.org/10.1590/S0100-204X2011000100010
Atashkar, D., Ershadi, A., & Abdollahi, H. (2020). Effects of drought stress on physiological and biochemical indices in hybrid apple rootstocks. Iranian Journal of Horticultural Science and Technology, 21(2), 107–122. (In Persian). https://doi.org/20.1001.1.16807154.1399.21.2.2.8
Atashkar, D., Pirkhezri, M., & Taghizadeh, A. A. (2016). Production and primary evaluation of apple (Mallus domestica Borkh.) hybrid rootstocks. Iranian Journal of Horticultural Science, 47(2), 229–235. )In Persian). https://doi.org/10.22059/ijhs.2016.5834
Baldin, E. L. L., Cruz, P. L., Morando, R., Silva, I. F., Bentivenha, J. P. F., Tozin, L. R. S., & Rodrigues, T. M. (2017). Characterization of antixenosis in soybean genotypes to Bemisia tabaci (Hemiptera: Aleyrodidae) biotype B. Journal of Economic Entomology, 110(4), 1869–1876. https://doi.org/10.1093/jee/tox228
Beers, E. H., Cockfield, S. D., & Gontijo, L. M. (2010). Seasonal phenology of woolly apple aphid (Hemiptera: Aphididae) in Central Washington. Environmental Entomology, 39(2), 286–294. https://doi.org/10.1603/EN09062
Damavandian, M. R. (2000). Biology of subterranean populations of woolly apple aphid, Eriosoma lanigerum (Hausmann) (Homoptera: Aphididae), in apple orchards [Doctoral dissertation, Stellenbosch University].
Divya Rani, V., & Sudini, H. (2013). Management of soilborne diseases in crop plants: An overview. International Journal of Plant, Animal and Environmental Sciences, 3(4), 156–164. (No DOI available)
Ehteshami-Moinabadi, M. (2022). Properties of fault zones and their influences on rainfall-induced landslides, examples from Alborz and Zagros ranges. Environmental Earth Sciences, 81(5), Article 168. https://doi.org/10.1007/s12665-022-10283-2
Fazio, G., Aldwinckle, H., & Robinson, T. (2013). Unique characteristics of Geneva® apple rootstocks. Encontro Nacional sobre Fruticultura de Clima Temperado.
Ferrier, S., Manion, G., Elith, J., & Richardson, K. (2007). Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Diversity and Distributions, 13(3), 252–264. https://doi.org/10.1111/j.1472-4642.2007.00341.x
Fluke, C. L. (1930). The influence of resistant apple scions on the susceptibility of non-resistant stocks with relation to woolly aphid attacks. Journal of Economic Entomology, 23(4), 741–743. https://doi.org/10.1093/jee/23.4.741
Frades, I., & Matthiesen, R. (2010). Overview on techniques in cluster analysis. In R. Matthiesen (Ed.), Bioinformatics methods in clinical research (pp. 81–107). Humana Press. https://doi.org/10.1007/978-1-60327-194-3_5
Fürstenberg-Hägg, J., Zagrobelny, M., & Bak, S. (2013). Plant defense against insect herbivores. International Journal of Molecular Sciences, 14(5), 10242–10297. https://doi.org/10.3390/ijms140510242
Ghaedi, H., Kocheili, F., Latifian, M., & Nejad, R. F. (2020). Spatial and temporal distribution of rhinoceros beetles Oryctes Hellwig (Col.: Scarabaeidae) in date palm plantations of Khuzestan province. Plant Pest Research, 10(2), 1–12. (In Persian). https://doi.org/10.22124/iprj.2020.4292.
Godfrey, C. J. (2024). Resistance and susceptibility in interactions between apple and woolly aphid [Doctoral dissertation, Harper Adams University].
Gogtay, N. J., & Thatte, U. M. (2017). Principles of correlation analysis. Journal of the Association of Physicians of India, 65(3), 78–81.
Hajnajari, H. (2021). Thirty-three half-sib apple clonal rootstocks tolerant to crown rot produced in a 14-year pathology breeding program. Acta Hortic. 1315, 227-236. https://doi.org/10.17660/ActaHortic.2021.1315.35
Han, Y., & Korban, S. S. (2010). Strategies for map-based cloning in apple. Critical Reviews in Plant Sciences, 29(5), 265–284. https://doi.org/10.1080/07352689.2010.502084
Hengl, T., Sierdsema, H., Radović, A., & Dilo, A. (2009). Spatial prediction of species’ distributions from occurrence-only records: Combining point pattern analysis, ENFA and regression-kriging. Ecological Modelling, 220(24), 3499–3511. https://doi.org/10.1016/j.ecolmodel.2009.06.038
Isah, T. (2019). Stress and defense responses in plant secondary metabolites production. Biological Research, 52, Article 39. https://doi.org/10.1186/s40659-019-0246-3
Krisnawati, A., Bayu, M. S. Y. I., & Adie, M. M. (2017). Identification of soybean genotypes based on antixenosis and antibiosis to the armyworm (Spodoptera litura). Nusantara Bioscience, 9(2), 164–169.
Latifian, M., Seyedoleslami, H., & Khajeali, J. (2009). Comparison of several sampling techniques to estimate population densities of the grape leafhopper Arboridia kermanshah Dlabola (Hem., Cicadellidae). IAU Entomological Research Journal, 1(2), 95–108. (In Persian).  https://sanad.iau.ir/Journal/jer/Article/915520
Latifian, M., Atashkar, D. & Ghaemi, R. (2023a). Relative establishment rate and host preference of wooly apple aphid Eriosoma lanigerum (Hausmann, 1802) (Hemiptera: Aphididae) on promising apple hybrid rootstocks. Journal of Entomological Society of Iran, 43(3), 233-245. https://doi.org/ 10.61186/jesi.43.3.4
Latifian, M., Atashkar, D. & Ghaemi, R. (2023b). Antibiosis Resistance Of Promising Apple Rootstocks To Woolly Aphid [(Eriosoma lanigerum (Hausm.)] under Environmental Conditions of Karaj in Iran. Seed and Plant Journal, 39(1), 120-93. https://doi.org/ 10.22092/spj.2023.363992.1331
Latifian, M. & Atashkar, D. (2024). Resistance of Promising Apple Rootstocks to the Woolly Aphid [Eriosoma lanigerum (Hausmman)] under Forced Feeding Conditions. Seed and Plant Journal, 40(1), 72-47. https://doi.org/10.22092/spj.2025.367587.1385
Le Pelley, R. (1927). Studies on the resistance of apple to the woolly aphis (Eriosoma lanigerum Hausm.). Journal of Pomology and Horticultural Science, 6(3), 209–241. (No DOI available)
Lepaja, L., Musa, F., Lepaja, K., Krasniqi, N., & Zajmi, R. (2014). The comparison of the presence of the woolly apple aphid (Eriosoma lanigerum) on the two different apple cultivars and rootstocks. 49th Croatian and 9th International Symposium on Agriculture. https://doi.org/10.13140/2.1.2392.8968
Machlitt, D. (1998). Persea mite on avocados: Quick field counting method. Subtropical Fruit, 6, 1–4.
Mathulwe, L. L. (2019). Control of the woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae), using entomopathogenic fungi [Doctoral dissertation, Stellenbosch University]. (No DOI available)
Moinina, A., Lahlali, R., MacLean, D., & Boulif, M. (2018). Farmers’ knowledge, perception and practices in apple pest management and climate change in the Fes-Meknes region, Morocco. Horticulturae, 4(4), Article 42. https://doi.org/10.3390/horticulturae4040042
Montllor, C. B. (2017). The influence of plant chemistry on aphid feeding behavior. In E. A. Bernays (Ed.), Insect-Plant Interactions (pp. 125–174). CRC Press. https://doi.org/10.1201/9780203711699-4Osborne, J. (2010). Improving your data transformations: Applying the Box-Cox transformation. Practical Assessment, Research, and Evaluation, 15(1), Article 12. https://doi.org/10.7275/qbpc-gk17
Painter, R. H. (1951). Insect resistance in crop plants. Macmillan. (No DOI available)
Petersen, M. K., & Sandström, J. P. (2001). Outcome of indirect competition between two aphid species mediated by responses in their common host plant. Functional Ecology, 15(4), 525–534. https://doi.org/10.1046/j.0269-8463.2001.00552.x
Pinheiro, D. G. D. S., Espirito-Santo, A. B. M. M. D., Fasoli, J. V. B., Sobral-Souza, T., & Campos, M. L. (2024). Unravelling the secrets of non-host resistance in plant–insect interactions. Journal of Experimental Botany. Advance online publication. https://doi.org/10.1093/jxb/erae359
Reiczigel, J., Lang, Z., Rózsa, L., & Tóthmérész, B. (2005). Properties of crowding indices and statistical tools to analyze parasite crowding data. Journal of Parasitology, 91(2), 245–252. https://doi.org/10.1645/GE-331R
Robert, C. A., Erb, M., Hibbard, B. E., Wade French, B., Zwahlen, C., & Turlings, T. C. (2012). A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner. Functional Ecology, 26(6), 1429–1440. https://doi.org/10.1111/j.1365-2435.2012.02030.x
Russo, N. L., Robinson, T. L., Fazio, G., & Aldwinckle, H. S. (2007). Field evaluation of 64 apple rootstocks for orchard performance and fire blight resistance. HortScience, 42(7), 1517–1525. https://doi.org/10.21273/HORTSCI.42.7.1517
Sandanayaka, W. R. M., Bus, V. G. M., Connolly, P., & Newcomb, R. (2003). Characteristics associated with woolly apple aphid Eriosoma lanigerum, resistance of three apple rootstocks. Entomologia Experimentalis et Applicata, 109(1), 63–72. https://doi.org/10.1046/j.1570-7458.2003.00093.x
Sandanayaka, W. R. M., Bus, V. G. M., & Connolly, P. (2005). Mechanisms of woolly aphid [Eriosoma lanigerum (Hausm.)] resistance in apple. Journal of Applied Entomology, 129(9–10), 534–541. https://doi.org/10.1111/j.1439-0418.2005.01003.x
Tu, X. B., Fan, Y. L., McNeill, M., & Zhang, Z. H. (2018). Including predator presence in a refined model for assessing resistance of alfalfa cultivar to aphids. Journal of Integrative Agriculture, 17(2), 397–405. https://doi.org/10.1016/S2095-3119(17)61767-5
Verghese, A., & Jayanthi, P. K. (2002). A technique for quick estimation of aphid numbers in field. Current Science, 82(9), 1165–1168. (No DOI available)
Wu, T., Wittkamper, J., & Flores, H. E. (1999). Root herbivory in vitro: Interactions between roots and aphids grown in aseptic coculture. In Vitro Cellular & Developmental Biology-Plant, 35, 259–264. https://doi.org/10.1007/s11627-999-0089-7
Young, E., Rock, G. C., Zeiger, D. C., & Cummins, J. N. (1982). Infestation of some Malus cultivars by the North Carolina woolly apple aphid biotype. HortScience, 17(5), 787–788. https://doi.org/10.21273/HORTSCI.17.5.787
Zaayman, D., Lapitan, N. L., & Botha, A. M. (2009). Dissimilar molecular defense responses are elicited in Triticum aestivum after infestation by different Diuraphis noxia biotypes. Physiologia Plantarum, 136(2), 209–222. https://doi.org/10.1111/j.1399-3054.2009.01222.x
Zhao, L., He, N., Wang, J., Siddique, K. H., Gao, X., & Zhao, X. (2022). Plasticity of root traits in a seedling apple intercropping system driven by drought stress on the Loess Plateau of China. Plant and Soil, 480(1–2), 541–560. https://doi.org/10.1007/s11104-022-05603-1
دوره 56، شماره 3
پاییز 1404
صفحه 583-603

  • تاریخ دریافت 18 فروردین 1404
  • تاریخ بازنگری 12 تیر 1404
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