Skip to main content
Log in

Evaluating physiological and genetic variation of Quercus brantii response to Brenneria goodwinii in Iran

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Brenneria goodwinii is a bacterial pathogen causing severe decline in Quercus brantii. We explored the effects of B. goodwinii on physiological traits of Q. brantii seedlings and assessed differences between families in the response to the pathogen. We examined 210 seedlings from 14 half-sib families. To evaluate disease resistance, foliar symptoms and several physiological traits, including chlorophyll fluorescence and electrolyte leakage were measured in pathogen-inoculated and mock-inoculated seedlings. In addition, seven EST-SSR markers associated with stress resistance were genotyped in two resistant and two susceptible families. All physiological traits were negatively affected by pathogen inoculation. There was significant genetic variation among the families, with the most susceptible ones showing a worse physiological condition. The heritability and coefficient of genotypic variation of the resistance increased during the experimental period reaching relatively high values (0.49 and 35%, respectively) five weeks after inoculation. EST-SSR analysis revealed that resistant families showed the highest heterozygosity. Two of the seven evaluated loci were associated with the measured physiological traits and showed high FST values. Our results support that resistant mother trees can be selected for disease management. The putative alleles of FIR053 locus could be useful for identifying resistant Q. brantii families to the pathogen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll level

DSI:

Disease severity index

DRI:

Disease resistance index

EL:

Electrolyte leakage

Fv/Fm:

Maximum quantum yield of PSII

ΦPSII:

Photochemical yield of PSII

σ2 f :

Variance components of family variations

σ2 f :

Total phenotypic variance

\({h}^{2}\) :

Narrow-sense heritability

FST:

Genetic differentiation

DFA:

Discriminant function analysis

References

  • Alcaide, F., Solla, A., Mattioni, C., Castellana, S., & Martín, M. Á. (2019). Adaptive diversity and drought tolerance in Castanea sativa assessed through genic markers EST-SSR. Forestry, 92(3), 287–296.

    Article  Google Scholar 

  • Alcaide, F., Solla, A., Cherubini, M., Mattioni, C., Cuenca, B., Camisón, Á., & Martín, M. Á. (2020). Adaptive evolution of chestnut forests to the impact of ink disease in Spain. Journal of Systematic and Evololution, 58(4), 504–516. https://doi.org/10.1111/jse.12551

    Article  Google Scholar 

  • Bayoumi, T. Y., Eid, M. H., & Metwali, E. M. (2008). Application of physiological and biochemical indices as a screening technique for drought tolerance in wheat genotypes. African Journal of Biotechnology, 7(14), 2341–2352.

    CAS  Google Scholar 

  • Beaumont, M. A., & Nichols, R. A. (1996). Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society b: Biological Sciences, 263, 1619–1626. https://doi.org/10.1098/rspb.1996.0237

    Article  ADS  Google Scholar 

  • Bilska, K., & Szczecińska, M. (2016). Comparison of the effectiveness of ISJ and SSR markers and detection of outlier loci in conservation genetics of Pulsatilla patens populations. PeerJ, 4, e2504. https://doi.org/10.7717/peerj.2504

    Article  PubMed  PubMed Central  Google Scholar 

  • Boshier, D., & Buggs, R. J. (2015). The potential for field studies and genomic technologies to enhance resistance and resilience of British tree populations to pests and pathogens. Forestry, 88(1), 27–40. https://doi.org/10.1093/forestry/cpu046

    Article  Google Scholar 

  • Bradbury, D., Smithson, A., & Krauss, S. L. (2013). Signatures of diversifying selection at EST-SSR loci and association with climate in natural Eucalyptus populations. Molecular Ecology, 22(20), 5112–5129. https://doi.org/10.1111/mec.12463

    Article  CAS  PubMed  Google Scholar 

  • Brady, C., Orsi, M., Doonan, J. M., Denman, S., & Arnold, D. (2022). Brenneria goodwinii growth in vitro is improved by competitive interactions with other bacterial species associated with Acute Oak Decline. Current Research in Microbial Sciences, 3, 100102. https://doi.org/10.1016/j.crmicr.2021.100102

    Article  CAS  PubMed  Google Scholar 

  • Brummer, M., Arend, M., Fromm, J., Schlenzig, A., & Osswald, W. F. (2002). Ultrastructural changes and immunocytochemical localization of the elicitin quercinin in Quercus robur L. roots infected with Phytophthora quercina. Physiological and Molecular Plant Pathology, 61, 109–120. https://doi.org/10.1006/pmpp.2002.0419

    Article  CAS  Google Scholar 

  • Cabanás, C. G. L., Valverde-Corredor, A., & Mercado-Blanco, J. (2015). Systemic responses in a tolerant olive (Olea europaea L.) cultivar upon root colonization by the vascular pathogen Verticillium dahliae. Frontiers in Microbiology, 6, 928. https://doi.org/10.3389/fmicb.2015.00928

    Article  Google Scholar 

  • Chang, Q., Liu, J., Wang, Q., Han, L., Liu, J., Li, M., & Kang, Z. (2013). The effect of Puccinia striiformis f. sp. tritici on the levels of water-soluble carbohydrates and the photosynthetic rate in wheat leaves. Physiological and Molecular Plant Pathology, 84, 131–137. https://doi.org/10.1016/j.pmpp.2013.09.001

    Article  CAS  Google Scholar 

  • Charoenporn, C., Kanokmedhakul, S., Lin, F. C., Poeaim, S., & Soytong, K. (2010). Evaluation of bio-agent formulations to control Fusarium wilt of tomato. African Journal of Biotechnology, 9(36), 5836–5844.

    CAS  Google Scholar 

  • Chen, Y. E., Cui, J. M., Su, Y. Q., Yuan, S., Yuan, M., & Zhang, H. Y. (2015). Influence of stripe rust infection on the photosynthetic characteristics and antioxidant system of susceptible and resistant wheat cultivars at the adult plant stage. Frontiers of Plant Science, 6, 779. https://doi.org/10.3389/fpls.2015.00779

    Article  Google Scholar 

  • Cuervo-Alarcon, L., Arend, M., Müller, M., Sperisen, C., Finkeldey, R., & Krutovsky, K. V. (2018). Genetic variation and signatures of natural selection in populations of European beech (Fagus sylvatica L.) along precipitation gradients. Tree Genetics & Genomes, 14(6), 84. https://doi.org/10.1007/s11295-018-1297-2

    Article  Google Scholar 

  • Domínguez, J., Macaya-Sanz, D., Gil, L., & Martín, J. A. (2022). Excelling the progenitors: Breeding for resistance to Dutch elm disease from moderately resistant and susceptible native stock. Forest Ecology and Management, 511, 120113. https://doi.org/10.1016/j.foreco.2022.120113

    Article  Google Scholar 

  • Dorado, F. J., Solla, A., Alcaide, F., & Martín, M. A. (2022). Assessing heat stress tolerance in Castanea sativa. Forestry, 95(5), 667–677. https://doi.org/10.1093/forestry/cpac021

    Article  Google Scholar 

  • Dow, B. D., & Ashley, M. V. (1998). High levels of gene flow in bur oak revealed by paternity analysis using microsatellites. Journal of Heredity, 89(1), 62–70. https://doi.org/10.1093/jhered/89.1.62

    Article  Google Scholar 

  • Ercan, S., Ertugrul, F., Aydin, Y., Akfirat, F. S., Hasancebi, S., Akan, K., Mert, Z., Bolat, N., Yorgancilar, O., & Altinkut-Uncuoglu, A. (2010). An EST-SSR marker linked with yellow rust resistance in wheat. Biologia Plantarum, 54(4), 691–696. https://doi.org/10.1007/s10535-010-0122-z

    Article  CAS  Google Scholar 

  • Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1, 117693430500100000.

    Article  Google Scholar 

  • Fernandes, C., Duarte, L., Naves, P., Sousa, E., & Cruz, L. (2022). First report of Brenneria goodwinii causing acute oak decline on Quercus suber in Portugal. Journal of Plant Pathology, 104, 837–838. https://doi.org/10.1007/s42161-022-01046-w

    Article  Google Scholar 

  • Fleischmann, F., Gottlein, A., Rodenkirchen, H., Lutz, C., & Oßwald, W. (2004). Biomass, nutrient and pigment content of beech (Fagus sylvatica) saplings infected with Phytophthora citricola, P. cambivora, P. pseudosyringae and P. undulata. Forest Pathology, 34, 79–92. https://doi.org/10.1111/j.1439-0329.2004.00349.x

    Article  Google Scholar 

  • Fleischmann, F., Koehl, J., Portz, R., Beltrame, A. B., & Oßwald, W. (2005). Physiological change of Fagus sylvatica seedlings infected with Phytophthora citricola and the contribution of its elicitin “Citricolin” to pathogenesis. Plant Biology, 7, 650–658. https://doi.org/10.1055/s-2005-872891

    Article  CAS  PubMed  Google Scholar 

  • Frampton, J., Isik, F., & Benson, D. M. (2013). Genetic variation in resistance to Phytophthora cinnamomi in seedlings of two Turkish Abies species. Tree Genetics & Genomes, 9(1), 53–63. https://doi.org/10.1007/s11295-012-0529-0

    Article  Google Scholar 

  • Gallego, F. J., De Algaba, A. P., & Fernandez-Escobar, R. (1999). Etiology of oak decline in Spain. European Journal of Plant Pathology, 29, 17–27. https://doi.org/10.1046/j.1439-0329.1999.00128.x

    Article  Google Scholar 

  • Garcia-Gonzalez, F., & Simmons, L. W. (2007). Paternal indirect genetic effects on offspring viability and the benefits of polyandry. Current Biology, 17, 32–36. https://doi.org/10.1016/j.cub.2006.10.054

    Article  CAS  PubMed  Google Scholar 

  • Ghanbary, E., Tabari Kouchaksaraei, M., Mirabolfathy, M., Modarres Sanavi, S. A. M., & Rahaie, M. (2017). Growth and physiological responses of Quercus brantii seedlings inoculated with Biscogniauxia mediterranea and Obolarina persica under drought stress. Forest Pathology, 47(5), e12353. https://doi.org/10.1111/efp.12353

    Article  Google Scholar 

  • Gkizi, D., Santos-Rufo, A., Rodríguez-Jurado, D., Paplomatas, E. J., & Tjamos, S. E. (2015). The β-amylase genes: Negative regulators of disease resistance for Verticillium dahliae. Plant Pathology, 64(6), 1484–1490. https://doi.org/10.1111/ppa.12360

    Article  CAS  Google Scholar 

  • Goodarzi, M., Pourhashemi, M., & Azizi, Z. (2019). Investigation on Zagros forests cover changes under the recent droughts using satellite imagery. Journal of Forensic Sciences, 65(1), 9–17. https://doi.org/10.17221/61/2018-JFS

    Article  Google Scholar 

  • Guimarães, L. M. D. S., Resende, M. D. V. D., Lau, D., Rosse, L. N., Alves, A. A., & Alfenas, A. C. (2010). Genetic control of Eucalyptus urophylla and E. grandis resistance to canker caused by Chrysoporthe cubensis. Genetics and Molecular Biology, 33(3), 525–531. https://doi.org/10.1590/S1415-47572010005000069

    Article  Google Scholar 

  • Hasancebi, S., Mert, Z., Ertugrul, F., Akan, K., Aydin, Y., Akfirat, F. S., & Uncuoglu, A. A. (2014). An EST-SSR marker, bu099658, and its potential use in breeding for yellow rust resistance in wheat. Czech Journal of Genetics and Plant Breeding, 50(1), 11–18. https://doi.org/10.17221/109/2013-CJGPB

  • Huang, B. L., Li, X., Liu, P., Ma, L., Wu, W., Zhang, X., & Huang, B. (2019). Transcriptomic analysis of Eruca vesicaria subs sativa lines with contrasting tolerance to polyethylene glycol-simulated drought stress. BMC Plant Biology, 19(1), 419. https://doi.org/10.1186/s12870-019-1997-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • SAS Institute. (2004). SAS/ETS 9.1 User's Guide. SAS Institute.

  • Jump, A. S., Marchant, R., & Peñuelas, J. (2009). Environmental change and the option value of genetic diversity. Trends in Plant Science, 14(1), 51–58. https://doi.org/10.1016/j.tplants.2008.10.002

    Article  CAS  PubMed  Google Scholar 

  • Kjær, E. D., McKinney, L. V., Nielsen, L. R., Hansen, L. N., & Hansen, J. K. (2012). Adaptive potential of ash (Fraxinus excelsior) populations against the novel emerging pathogen Hymenoscyphus pseudoalbidus. Evolutionary Applications, 5, 219–228. https://doi.org/10.1111/j.1752-4571.2011.00222.x

    Article  PubMed  Google Scholar 

  • Laporte, D., Olate, E., Salinas, P., Salazar, M., Jordana, X., & Holuigue, L. (2012). Glutaredoxin GRXS13 plays a key role in protection against photooxidative stress in Arabidopsis. The Journal of Experimental Botany, 63(1), 503–515. https://doi.org/10.1093/jxb/err301

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler, H. K. (1996). Vegetation stress: An introduction to the stress concept in plants. Journal of Plant Physiology, 148, 4–14. https://doi.org/10.1111/j.1749-6632.1998.tb08993.x

    Article  CAS  Google Scholar 

  • Linaldeddu, B. T., Sirca, C., Spano, D., & Franceschini, A. (2011). Variation of endophytic cork oak-associated fungal communities in relation to plant health and water stress. Forest Pathology, 41, 193–201. https://doi.org/10.1111/j.1439-0329.2010.00652.x

    Article  Google Scholar 

  • Lind-Riehl, J. F., & Gailing, O. (2017). Adaptive Variation and Introgression of a CONSTANS-Like Gene in North American Red Oaks. Forests, 8(1), 3. https://doi.org/10.3390/f8010003

    Article  Google Scholar 

  • Luikart, G., England, P. R., Tallmon, D., Jordan, S., & Taberlet, P. (2003). The power and promise of population genomics: From genotyping to genome typing. Nature Reviews Genetics, 4(12), 981–994. https://doi.org/10.1038/nrg1226

    Article  CAS  PubMed  Google Scholar 

  • Luque, J., Cohen, M., Savé, R., Biel, C., & Álvarez, I. (1998). Effects of three fungal pathogens on water relations, chlorophyll fluorescence and growth of Quercus suber L. Annals of Forest Science, 56, 19–26. https://doi.org/10.1051/forest:19990103

    Article  Google Scholar 

  • Mandal, M. S. N., Fu, Y., Zhang, S., & Ji, W. (2014). Proteomic analysis of the defense response of wheat to the powdery mildew fungus, Blumeria graminis f. sp. tritici. Protein Journal, 33(6), 513–524. https://doi.org/10.1007/s10930-014-9583-9

    Article  CAS  PubMed  Google Scholar 

  • Martín, J. A., Solla, A., García-Vallejo, M. C., & Gil, L. (2012). Chemical changes in Ulmus minor xylem tissue after salicylic acid or carvacrol treatments are associated with enhanced resistance to Ophiostoma novo-ulmi. Phytochemistry, 83, 104–109.

    Article  PubMed  Google Scholar 

  • Martín, J. A., Sobrino-Plata, J., Coira, B., Medel, D., Collada, C., & Gil, L. (2019). Growth resilience and oxidative burst control as tolerance factors to Ophiostoma novo-ulmi in Ulmus minor. Tree Physiology, 39(9), 1512–1524. https://doi.org/10.1093/treephys/tpz067

    Article  CAS  PubMed  Google Scholar 

  • Martín, J. A., Dominguez, J., Solla, A., Brasier, C. M., Webber, J. F., Santini, A., Martínez-Arias, C., Bernier, L., & Gil, L. (2021). Complexities underlying the breeding and deployment of Dutch elm disease resistant elms. New Forests, 1-36. https://doi.org/10.1007/s11056-021-09865-y

  • Martínez-Arias, C., Sobrino-Plata, J., Ormeno-Moncalvillo, S., Gil, L., Rodriguez-Calcerrada, J., & Martín, J. A. (2021). Endophyte inoculation enhances Ulmus minor resistance to Dutch elm disease. Fungal Ecology, 50, 101024. https://doi.org/10.1016/j.funeco.2020.101024

    Article  Google Scholar 

  • Miranda, A. C., de Moraes, M. L. T., Tambarussi, E. V., Furtado, E. L., Mori, E. S., da Silva, P. H. M., & Sebbenn, A. M. (2013). Heritability for resistance to Puccinia psidii Winter rust in Eucalyptus grandis Hill ex Maiden in Southwestern Brazil. Tree Genetic & Genomes, 9(2), 321–329. https://doi.org/10.1007/s11295-012-0572-x

    Article  Google Scholar 

  • Molik, K., Pawlowska, E., Kantarek, Z., & Milczarski, P. (2014). QTL analysis of chlorophyll content and chlorophyll fluorescence parameter in mapping population of rye. Folia Pomeranae Universitatis Technologiae Stetinensis, 312(31), 105–116.

    Google Scholar 

  • Moradi-Amirabad, Y., Rahimian, H., Babaeizad, V., & Denman, S. (2019). Brenneria spp and Rahnella victoriana associated with acute oak decline symptoms on oak and hornbeam in Iran. Forest Pathology, 49, e12535. https://doi.org/10.1111/efp.12535

    Article  Google Scholar 

  • Müller, M., Nelson, C. D., & Gailing, O. (2018). Analysis of environment-marker associations in American chestnut. Forests, 9(11), 695. https://doi.org/10.3390/f9110695

    Article  Google Scholar 

  • Nayyar, H. (2003). Accumulation of osmolytes and osmotic adjustment in water-stressed wheat (Triticum aestivum) and maize (Zea mays) as affected by calcium and its antagonists. Environmental and Experimental Botany, 50, 253–264. https://doi.org/10.1016/S0098-8472(03)00038-8

    Article  CAS  Google Scholar 

  • Pike, S. M., Adam, A. L., Pu, X. A., Hoyos, M. E., Laby, R., Beer, S. V., & Novacky, A. (1998). Effects of Erwinia amylovoraharpin on tobacco leaf cell membranes are related to leaf necrosis and electrolyte leakage and distinct from perturbations caused by inoculated E. amylovora. Physiological and Molecular Plant Pathology, 53(1), 39–60. https://doi.org/10.1006/pmpp.1998.0167

    Article  CAS  Google Scholar 

  • Pitino, M., Allen, V., & Duan, Y. (2018). LasΔ5315 effector induces extreme starch accumulation and chlorosis as Ca. Liberibacter asiaticus infection in Nicotiana benthamiana. Frontiers of Plant Science, 9, 113. https://doi.org/10.3389/fpls.2018.00113

    Article  Google Scholar 

  • Raymond, M., & Rousset, F. (1995). An exact test for population differentiation. Evolution, 49(6), 1280–1283. https://doi.org/10.2307/2410454

    Article  PubMed  Google Scholar 

  • Rochon, C., Margolis, H. A., & Weber, J. C. (2007). Genetic variation in growth of Guazuma crinita (Mart.) trees at an early age in the Peruvian Amazon. Forest Ecology and Management, 243(2–3), 291–298. https://doi.org/10.1016/j.foreco.2007.03.025

    Article  Google Scholar 

  • Sánchez-Hernández, C., & Gaytán-Oyarzún, J. C. (2006). Two mini-preparation protocols to DNA extraction from plants with high polysaccharide and secondary metabolites. African Journal of Biotechnology, 5(20), 1864–1867.

    Google Scholar 

  • Santos, C., Zhebentyayeva, T., Serrazina, S., Nelson, C. D., & Costa, R. (2015). Development and characterization of EST-SSR markers for mapping reaction to Phytophthora cinnamomi in Castanea spp. Scientia Horticulturae, 194, 181–187. https://doi.org/10.1016/j.scienta.2015.07.043

    Article  CAS  Google Scholar 

  • Sayed, O. (2003). Chlorophyll fluorescence as a tool in cereal crop research. Photosyntetica, 41(3), 321–330. https://doi.org/10.1023/B:PHOT.0000015454.36367.e2

    Article  CAS  Google Scholar 

  • Scariot, V., De Keyser, E., Handa, T., & De Riek, J. (2007). Comparative study of the discriminating capacity and effectiveness of AFLP, STMS and EST markers in assessing genetic relationship among evergreen azaleas. Plant Breeding, 126, 207–212. https://doi.org/10.1111/j.1439-0523.2007.01326.x

    Article  CAS  Google Scholar 

  • Skrøppa, T., Solhim, H., & Steffenrem, A. (2015). Genetic variation, inheritance patterns and parent offspring relationships after artificial inoculations with Heterobasidion parviporum and Ceratocystis polonica in Norway spruce seed orchards and progeny tests. Silva Fennica, 49, 1–122. https://doi.org/10.14214/sf.1191

  • Smirnoff, N. (1993). The role of active oxygen in the response of plants to water deficit and desiccation. New Phytologist, 125, 27–58. https://doi.org/10.1111/j.1469-8137.1993.tb03863.x

    Article  CAS  PubMed  Google Scholar 

  • Smith, A. M., Zeeman, S. C., & Smith, S. M. (2005). Starch Degradation. Annual Review of Plant Biology, 56, 73–98. https://doi.org/10.1146/annurev.arplant.56.032604.144257

    Article  CAS  PubMed  Google Scholar 

  • Solla, A., Lopez-Almansa, J. C., Martin, J. A., & Gil, L. (2015). Genetic variation and heritability estimates of Ulmus minor and Ulmus pumila hybrids for budburst, growth and tolerance to Ophiostoma novo-ulmi. IForest-Biogeosciences and Forestry, 8, 422–430. https://doi.org/10.3832/ifor1227-007

    Article  Google Scholar 

  • Sun, J., Hang, Y., Han, Y., Zhang, X., Gan, L., Cai, C., Houhui, S., & Yang, Y. (2019). Deletion of glutaredoxin promotes oxidative tolerance and intracellular infection in Listeria monocytogenes. Virulence, 10(1), 910–924. https://doi.org/10.1080/21505594.2019.1685640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tessier Du Cross, E., Matyas, C., & Kriebel, H. (1999). Contribution of genetics to the sustained management of global forest resources – Conclusions and recommendations. In: Forest genetics and sustainability, Forestry Sciences MÀTYÀS C (eds), pp. 281–287. Kluwer Academic Publishers, Dordrecht.

  • Thiel, T., Michalek, W., Varshney, R. K., & Graner, A. (2003). Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theoretical and Applied Genetics, 106, 411–422. https://doi.org/10.1007/s00122-002-1031-0

    Article  CAS  PubMed  Google Scholar 

  • Thomas, B. R., Macdonald, S. E., & Dancik, B. P. (1997). Variance components, heritability’s and gain estimates for growth chamber and field performance of Populus tremuloides: Gas exchange parameters. Silvae Genetica, 46, 309–316.

    Google Scholar 

  • Vivas, M., Zas, A., & Solla, R. (2011). Screening of maritime pine (pinus pinaster) for resistance to Fusarium circinatum, the causal agent of Pitch Canker disease. Forestry, 85, 185–192. https://doi.org/10.1093/forestry/cpr055

    Article  Google Scholar 

  • Wenzel, G. (1985). Strategies in unconventional breeding for disease resistance. Annual Review of Phytopathology, 23(14972), 152.

    Google Scholar 

  • Xu, T. F., Xiang, J., Li, F. J., Li, T. M., Yu, Y. H., Wang, Y. J., & Xu, Y. (2013). Screening proteins interacting with VpPR10. 1 of Chinese wild grapevine using the yeast two-hybrid system. Acta Physiologiae Plantarum, 35(8), 2355–2364.

    Article  CAS  Google Scholar 

  • Yamato, M., Yamada, T., & Suzuki, K. (2003). Water relations of Quercus mongolica var. grosseserrata seedlings inoculated with Raffaelea quercivora: Ambrosia fungi related with mass mortality of oaks in Japan. Proc IUFRO, Forest Insect Population Dynamics and Host Influences, Kanazawa (Japan), September 14–19. pp: 128.

  • Zargaran, M. R., Goudarzi, N., Banj Shafiei, A., & Tavakoli, M. (2019). The role of charcoal disease and wood borers on Quercus brantii Lindl decline under different physiographical conditions. International Journal of Environmental Science and Technology, 16(10), 5797–5806. https://doi.org/10.1007/s13762-018-1955-9

    Article  Google Scholar 

  • Zas, R., Sampedro, L., Prada, E., & Fernández-López, J. (2005). Genetic variation of Pinus pinaster Ait. seedlings in susceptibility to the pine weevil Hylobius abietis L. Annals of Forest Science, 62(7), 681–688. https://doi.org/10.1051/forest:2005064

    Article  Google Scholar 

  • Zilberstein, M., & Pinkas, Y. (1987). Detached root inoculation–a new method to evaluate resistance to Phytophthora root rot in avocado trees. Phytopathology, 77(6), 841–844.

    Article  Google Scholar 

  • Zolfaghari, R., Fayyaz, P., Nazari, M., & Valladares, F. (2013). Interactive effects of seed size and drought stress on growth and allocation of Quercus brantii Lindl. seedlings from two provenances. Turkish Journal of Agriculture and Forestry, 37(3), 361–368. https://doi.org/10.3906/tar-1206-54

    Article  Google Scholar 

  • Zolfaghari, R., Dalvand, F., Fayyaz, P., & Solla, A. (2022). Maternal drought stress on Persian oak (Quercus brantii Lindl.) affects susceptibility to single and combined drought and biotic stress in offspring. Environmental and Experimental Botany, 194, 104716. https://doi.org/10.1016/j.envexpbot.2021.104716

    Article  CAS  Google Scholar 

Download references

Funding

This works was supported by General Department of Natural Resource and Watershed Management of Kohgilouyeh and Boyer-Ahmad province (Grant Number: 93–195) to the project “Investigation of genetical pattern and phenotypic variation between healthy and dried individuals of brant's oak species (Quercus brantii) and provide a suitable solution for Kohgilouyeh and Boyer-Ahmad province”.

Author information

Authors and Affiliations

Authors

Contributions

R. Zolfaghari designed the study; R. Zolfaghari and F. Karimi performed field sampling in their respective field sites; and F. Karimi performed all greenhouse measurements and molecular experiments; P. Fayyaz performed the statistical analyses; JA. Martín analysed the data and R. Zolfaghari and JA. Martín wrote the draft of the paper.

Corresponding author

Correspondence to Roghayeh Zolfaghari.

Ethics declarations

Competing interests

The authors have declared that no competing interests exist.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 23.7 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zolfaghari, R., Karimi, F., Fayyaz, P. et al. Evaluating physiological and genetic variation of Quercus brantii response to Brenneria goodwinii in Iran. Eur J Plant Pathol 168, 607–623 (2024). https://doi.org/10.1007/s10658-023-02788-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-023-02788-8

Keywords

Navigation