Skip to main content
Log in

Introducing a cut-stem inoculation method for fast evaluation of sunflower resistance to Macrophomina phaseolina

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

The fast adaptation to different growing conditions of a fungus Macrophomina phaseolina, led to its becoming one of the sunflower (Helianthus annuus L.) disease causal agents in regions with a temperate climate. Methods currently used to determine sunflower resistance require laborious manual inoculation and confirmation of pathogen appearance, due to the late stage of testing. The paper proposes a cut-stem method for inoculating sunflower plants in the controlled conditions and the possibility of early-stage disease evaluation. A set of 15 sunflower inbred lines was inoculated using M. phaselolina isolate in the growth chamber and the obtained data were analysed using Cut-stem Disease Severity (CSDS) and compared with disease severity obtained from field experiments using traditional inoculation methods (toothpick, Unwounded Stem Base Inoculation (USBI) and non-inoculated plants). The results showed that, based on CSDS, inbred lines infected with the cut-stem inoculation method significantly differed regarding resistance to M. phaseolina. None of the inbred lines exhibited complete resistance but three lines could be proposed as a source of resistance to this pathogen. Ranking of inbred lines which was based on resistance to M.phaseolina was similar in all inoculation methods and in non-inoculated plants. There were highly significant correlations between the values obtained from growth chamber experiment and disease severity scores from field evaluations. Thus, the obtained results indicate that the cut-stem method could potentially complement field testing methods and be valuable tool in sunflower breeding for resistance to M. phaseolina.

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

Similar content being viewed by others

References

  • Akhtar, K. P., Sarwar, G., & Arshad, H. M. I. (2011). Temperature response, pathogenicity, seed infection and mutant evaluation against Macrophomina phaseolina causing charcoal rot disease of sesame. Archives of Phytopathology and Plant Protection, 44(4), 320–330. https://doi.org/10.1080/03235400903052945

    Article  Google Scholar 

  • Altinok, H. H., Can, C., Boyaci, H. F., & Topcu, V. (2013). Genetic variability among breeding lines and cultivars of eggplant against Fusarium oxysporum f. sp. melongenae from Turkey. Phytoparasitica, 42(1), 75–84. https://doi.org/10.1007/s12600-013-0340-y

    Article  Google Scholar 

  • Anđelković, V., Cvejić, S., Jocić, S., Kondić-Špika, A., Jeromela, A. M., Mikić, S., Prodanović, S., Radanović, A., Savić Ivanov, M., Trkulja, D. & Miladinović, D. (2020). Use of plant genetic resources in crop improvement–example of Serbia. Genetic Resources and Crop Evolution, 1–14. https://doi.org/10.1007/s10722-020-01029-9

  • Botha, C., McLaren, N. W., & Swart, W. J. (2009). Evaluation of greenhouse inoculation techniques used to screen for Sclerotinia stem rot resistance in soybeans. South African Journal of Plant and Soil, 26(1), 48–50. https://doi.org/10.1080/02571862.2009.10639932

    Article  Google Scholar 

  • Coser, S. M., Chowda Reddy, R. V., Zhang, J., Mueller, D., Mengistu, A., Wise, K. A., Allen, T. W., Singh, A., & Singh, A. K. (2017). Genetic architecture of charcoal rot (Macrophomina phaseolina) resistance in soybean revealed using a diverse panel. Frontiers in Plant Science, 8, 1626. https://doi.org/10.3389/fpls.2017.01626

    Article  PubMed  PubMed Central  Google Scholar 

  • Csöndes, I., Cseh, A., Taller, J., & Poczai, P. (2012). Genetic diversity and effect of temperature and pH on the growth of Macrophomina phaseolina isolates from sunflower fields in Hungary. Molecular Biology Reports, 39(3), 3259–3269. https://doi.org/10.1007/s11033-011-1094-6

    Article  CAS  PubMed  Google Scholar 

  • Cvejić, S., Radanović, A., Dedić, B., Jocković, M., Jocić, S., & Miladinović, D. (2020). Genetic and genomic tools in sunflower breeding for broomrape resistance. Genes, 11(2), 152. https://doi.org/10.3390/genes11020152

    Article  CAS  PubMed Central  Google Scholar 

  • De Sousa Linhares, C. M., Ambrósio, M. M. Q., Castro, G., Torres, S. B., Esteras, C., de Sousa Nunes, G. H., & Picó, B. (2020). Effect of temperature on disease severity of charcoal rot of melons caused by Macrophomina phaseolina: Implications for selection of resistance sources. European Journal of Plant Pathology, 158(2), 431–441. https://doi.org/10.1007/s10658-020-02083-w

    Article  CAS  Google Scholar 

  • Evans, C. K., Hunger, R. M., & Siegerist, W. C. (1999). Comparison of greenhouse and field testing to identify wheat resistant to tan spot. Plant Disease, 83(3), 269–273. https://doi.org/10.1094/PDIS.1999.83.3.269

    Article  CAS  PubMed  Google Scholar 

  • Foolad, M. R., Ntahimpera, N., Christ, B. J., & Lin, G. Y. (2000). Comparison of field, greenhouse, and detached-leaflet evaluations of tomato germ plasm for early blight resistance. Plant Disease, 84(9), 967–972. https://doi.org/10.1094/PDIS.2000.84.9.967

    Article  CAS  PubMed  Google Scholar 

  • García-Olivares, J. G., López-Salinas, E., Cumpián-Gutiérrez, J., Cantú-Almaguer, M. A., Zavala-García, F., & Mayek-Pérez, N. (2012). Grain yield and charcoal rot resistance stability in common beans under terminal drought conditions. Journal of Phytopathology, 160(2), 98–105. https://doi.org/10.1111/j.1439-0434.2011.01864.x

    Article  Google Scholar 

  • Ghimire, K., Petrović, K., Kontz, B. J., Bradley, C. A., Chilvers, M. I., Mueller, D. S., Smith, D. L., Wise, K. A., & Mathew, F. M. (2019). Inoculation method impacts symptom development associated with Diaporthe aspalathi, D. caulivora, and D. longicolla on soybean (Glycine max). Plant disease, 103(4), 677–684. https://doi.org/10.1094/PDIS-06-18-1078-RE

    Article  CAS  PubMed  Google Scholar 

  • Harveson, R., Mathew, F., Gulya, T., Markell, S., Block, C., & Thompson, S. (2018). Sunflower stalk diseases initiated through leaf inoculations. Plant Health Progress, 19(1), 82–91. https://doi.org/10.1094/PHP-12-17-0083-DG

    Article  Google Scholar 

  • Hashmi, R. Y., Bond, J. P., Schmidt, M. E., & Klein, J. H. (2005). A temperature-controlled water bath method for evaluating soybean reaction to sudden death syndrome (SDS). Plant Health Progress, 6(1), 5. https://doi.org/10.1094/PHP-2005-0906-01-RS

    Article  Google Scholar 

  • Hussien, Z. N., Ibrahim, M. M., Ahmed, M., & Khalil, A. A. (2018). Thermotherapy of sunflower seeds controlling charcoal-rot caused by Macrophomina phaseolina. Egyptian Journal of Phytopathology, 46(2), 179–194. https://doi.org/10.21608/ejp.2018.115842

    Article  Google Scholar 

  • Ijaz, S., Sadaqat, H. A., & Khan, M. N. (2013). A review of the impact of charcoal rot (Macrophomina phaseolina) on sunflower. The Journal of Agricultural Science, 151(2), 222–227. https://doi.org/10.1017/S0021859612000512

    Article  Google Scholar 

  • IPCC, (2018). Global Warming of 1.5°C.An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty [Masson-Delmotte, V., P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P.R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J.B.R. Matthews, Y. Chen, X. Zhou, M.I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, and T. Waterfield (eds.)].

  • Iqbal, U. & Mukhtar, T. (2014). Morphological and pathogenic variability among Macrophomina phaseolina isolates associated with mungbean (Vigna radiata L.) Wilczek from Pakistan. The Scientific World Journal, 1–9. https://doi.org/10.1155/2014/950175

  • Jiménez-Díaz, R. M., & Blanco-Lópaz, M. A. (1983). Incidence and distribution of charcoal rot of sunflower caused by Macrophomina phaseolina in Spain. Plant Disease, 67, 1033–1036.

    Article  Google Scholar 

  • Jordaan, E., Van der Waals, J. E., & McLaren, N. W. (2019). Effect of irrigation on charcoal rot severity, yield loss and colonization of soybean and sunflower. Crop Protection, 122, 63–69. https://doi.org/10.1007/s10658-020-02083-w

    Article  CAS  Google Scholar 

  • Kaya, Y. (2016). Sunflower In Gupta S. (Eds.), Breeding oilseed crops for sustainable production (1st edn., pp. 55–88) Elsevier Inc. https://doi.org/10.1016/B978-0-12-801309-0.00004-5

  • Kumar, B., Hooda, K. S., Singh, V., Sekhar, J. C., Kumar, V., Parihar, C. M., Jat, L. S., Singh, A. K., Kaul, J., Kaur, H., Kaur, H., & Yadav, O. P. (2016). Multi-environment field testing to identify stable sources of resistance to charcoal rot (Macrophomina phaseolina) disease in tropical maize germplasm. Maydica, 62(2), 1–7.

    Google Scholar 

  • Larfeil, C., Barrault, G., & Dechamp-Guillaume, G. (2010). Assessment of sunflower genotype tolerance to Phoma macdonaldii. OCL, 17(3), 161–166. https://doi.org/10.1051/ocl.2010.0304

    Article  Google Scholar 

  • Leiete, R. (2014). Disease menagment in suflower. In Arribas J. (Eds.), Sunflowers, growth and development, environmental influences and pests/diseases. (1st edn, pp. 165–185). Nova Science.

  • Mah, K. M., Uppalapati, S. R., Tang, Y., Allen, S., & Shuai, B. (2012). Gene expression profiling of Macrophomina phaseolina infected Medicago truncatula roots reveals a role for auxin in plant tolerance against the charcoal rot pathogen. Physiological and Molecular Plant Pathology, 79, 21–30. https://doi.org/10.1016/j.pmpp.2012.03.004

    Article  CAS  Google Scholar 

  • Mahlein, A. K., Kuska, M. T., Thomas, S., Wahabzada, M., Behmann, J., Rasher, U., & Kersting, K. (2019). Quantitative and qualitative phenotyping of disease resistance of crops by hyperspectral sensors: Seamless interlocking of phytopathology, sensors, and machine learning is needed! Current Opinion in Plant Biology, 50, 156–162. https://doi.org/10.1016/j.pbi.201906.007

    Article  CAS  PubMed  Google Scholar 

  • Mahmoud, A. (2010). Molecular and biological investigations of damping-off and charcoal-rot diseases in sunflower. Sabanci University.

    Google Scholar 

  • Marquez, N., Giachero, M. L., Declerck S., & Ducasse D. A. (2021). Macrophomina phaseolina: general characteristics of pathogenicity and methods of control. Frontiers in Plant Science12. https://doi.org/10.3389/fpls.2021.634397

  • McKinney, H. H. (1923). Influence of soil, temperature and moisture on infection of wheat seedling by Helminthosporium sativum. Journal of Agricultural Research, 31(9), 827–840.

    Google Scholar 

  • Mihaljčević, M. (1983). Pronalaženje izvora otpornosti prema Sclerotiumbataticola Taub. kod inbred linija i hibrida suncokreta. Bachelor tesis, Faculty of Agriculture University of Novi Sad

  • Neto, F. A. L. D., Schmidt, M., Hartman, G. L., Shuxian, L., & Diers, B. W. (2008). Inoculation methods under greenhouse conditions for evaluating soybean resistance to sudden death syndrome. Pesquisa Agropecuária Brasileira, 43(11), 1475–1482. https://doi.org/10.1590/S0100-204X2008001100005

    Article  Google Scholar 

  • Ohunakin, A. O., Odiyi, A. C., & Akinyele, B. O. (2019). Comparison of rank sum and Area under Disease Progress Curve (AUDPC) as determinant for relative resistance status of maize populations to Northern leaf blight disease of maize. Advanced Plants & Agriculural Research, 9(3), 395–400. https://doi.org/10.15406/apar.2019.09.00455

    Article  Google Scholar 

  • Pavlović, S., Ristić, D., Aleksić, G., Milošević, D., Stević, T., & Starović, M. (2015). The first report of Macrophomina phaseolina of Immortelle (Helichrysum italicum) in Serbia. Plant Disease, 99(9), 1279–1279.

    Article  Google Scholar 

  • Pawlowski, M. L., Hill, C. B., & Hartman, G. L. (2015). Resistance to charcoal rot identified in ancestral soybean germplasm. Crop Science, 55(3), 1230–1235. https://doi.org/10.2135/cropsci2014.10.0687

    Article  Google Scholar 

  • Popović, T., Blagojević, J., Aleksić, G., Jelušić, A., Krnjajić, S., & Milovanović, P. (2018). A blight disease on highbush blueberry associated with Macrophomina phaseolina in Serbia. Canadian Journal of Plant Pathology, 40(1), 121–127. https://doi.org/10.1080/07060661.2017.1415977

    Article  Google Scholar 

  • Retig, N., Rabinowitch, H. D., & Kedar, N. A. (1973). Simplified method for determining the resistance of tomato seedlings to Fusarium and Verticillium wilts. Phytoparasitica, 1(2), 111–114. https://doi.org/10.1007/BF02981040

  • RHSS, (2020a). Mesečni bilten za Srbiju, Avgust 2020a. Godine, Odeljenje za monitoring klime i klimatske prognoze, Sektor Nacionalnog centra za klimatske promene, razvoj klimatskih modela i ocenu rizika elementarnih nepogoda Available from: http://www.hidmet.gov.rs/podaci/meteorologija/latin/Avgust_l.pdf. [assessed 21.11.2020a].

  • RHSS, (2020b). Mesečni bilten za Srbiju, Jul 2020b. Godine, Odeljenje za monitoring klime i klimatske prognoze, Sektor Nacionalnog centra za klimatske promene, razvoj klimatskih modela i ocenu rizika elementarnih nepogoda Available from: http://www.hidmet.gov.rs/podaci/meteorologija/latin/Jul_l.pdf [assessed 21.11.2020b].

  • RHSS, (2020c). Mesečni bilten za Srbiju, Jun 2020c. Godine, Odeljenje za monitoring klime i klimatske prognoze Sektor Nacionalnog centra za klimatske promene, razvoj klimatskih modela i ocenu rizika elementarnih nepogoda. Available from: http://www.hidmet.gov.rs/podaci/meteorologija/latin/Jun_l.pdf [assessed 21.11.2020c]

  • RHSS, (2020d). Meteorološki godišnjak 1 Klimatološki podaci 2019, Republika Srbija, Beograd Available from: http://www.meteologos.rs/mesecni-meteoroloski-podaci/ [assessed 21.11.2020d]

  • Rotem, J. (1988). Techniques of controlled-condition experiments. In Kranz, J., & Rotem, J. (Eds.), Experimental techniques in plant disease epidemiology. Springer Science & Business Media, (1st edn, pp. 19–31). Springer-Verlag https://doi.org/10.1007/978-3-642-95534-1_3

  • Schneiter, A., & Miller, J. F. (1981). Description of sunflower growth stages. Crop Science, 21, 901–903. https://doi.org/10.2135/cropsci1981.0011183X002100060024x

    Article  Google Scholar 

  • Shehbaz, M., Rauf, S., Al-Sadi, A. M., Nazir, S., Bano, S., Shahzad, M., & Hussain, M. M. (2018). Introgression and inheritance of charcoal rot (Macrophomina phaseolina) resistance from silver sunflower (Helianthus argophyllus Torr. & A. Gray) into cultivated sunflower (Helianthus annuus L.). Australasian Plant Pathology, 47(4), 413–420. https://doi.org/10.1007/s13313-018-0573-9

    Article  CAS  Google Scholar 

  • Siddique, S., Shoaib, A., Khan, S. N., & Mohy-Ud-Din, A. (2020). Screening and histopathological characterization of sunflower germplasm for resistance to Macrophomina phaseolina. Mycologia, 113(1), 1–16. https://doi.org/10.1080/00275514.2020.1810516

    Article  CAS  Google Scholar 

  • Souza, E. M. D. S., Silva, L. A. B. D., Pinto, F. Á. C., Borel, J. C., Capucho, A. S., & Ishikawa, F. H. (2021). Inoculation methods and agressiveness of Macrophomina phaseolina isolates in cowpea. Ciência Rural52. https://doi.org/10.1590/0103-8478cr20210072

  • Taha, M. M., Mahmoud, A. F., Hassan, M. A., Mahmoud, A. M., & Sallam, M. A. (2018). Potential resistance of certain sunflower cultivars and inbred lines against charcoal rot disease caused by Macrophomina phaseolina (Tassi) Goid. Journal of Phytopathology and Pest Management, 5(3), 55–66.

    Google Scholar 

  • Talapov, T., Yuceer, S., Dedecan, O., Demirel, O., & Can, C. (2021). Comparison of Macrophomina phaseolina inoculation techniques for screening sunflower and soybean germplasm in a controlled environment. Canadian Journal of Plant Pathology, 43(6), 859–870. https://doi.org/10.1080/07060661.2021.1937321

    Article  CAS  Google Scholar 

  • Terzić, S., Dedić, B., Atlagić, J., Jocić, S., & Tančić, S. (2010). Screening wild sunflower species and F1 interspecific hybrids for resistance to broomrape. Helia, 33(53), 25–30. https://doi.org/10.2298/HEL1053025T

    Article  Google Scholar 

  • Twizeyimana, M., Hill, C. B., Pawlowski, M., Paul, C., & Hartman, G. L. (2012). A cut-stem inoculation technique to evaluate soybean for resistance to Macrophomina phaseolina. Plant Disease, 96(8), 1210–1215. https://doi.org/10.1094/PDIS-02-12-0126-RE

    Article  CAS  PubMed  Google Scholar 

  • Veverka, K., Palicová, J., & Křížková, I. (2009). The incidence and spreading of Macrophomina phaseolina (Tassi) Goidanovich on sunflower in the Czech Republic. Plant Protection Science, 44(4), 127–137. https://doi.org/10.17221/31/2008-PPS

    Article  Google Scholar 

  • Živanov, D., Živanov, S. T., Nagl, N., Savić, A., Katanski, S., & Milić, D. (2019). First report of Macrophomina phaseolina causing dry root rot of chickpea (Cicer arietinum) in Serbia. Plant Disease, 103(10), 2685. https://doi.org/10.1094/PDIS-03-19-0652-PDN

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Sonja Đukić for the help with correction of English grammar and language of the manuscript.

Funding

This work was supported by the Science Fund of the Republic of Serbia, through IDEAS project, grant number #7732457, Creating climate smart sunflower for future challenges – SmartSun, Ministry of Education, Science and Technological Development of the Republic of Serbia, grant number: 451–03-68/2020–14/200032 and Center of Excellence for Innovations in Breeding of Climate Resilient Crops—Climate Crops, Institute of Field and Vegetable Crops, Novi Sad, Serbia.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design “Conceptualization, S.C. and V.M.; methodology, B.D.; software, N.Ć.; validation, S.C., B.D. and V.M.; formal analysis, N.Ć.; investigation, N.Ć., B.B; resources, S.J., V.M; data curation, N.Ć.; writing—original draft preparation, N.Ć and B.B.; writing—review and editing, N.Ć, and S.C.; visualization, B.B.; supervision, D.M.; project administration, D.M.; funding acquisition, V.M. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Boško Dedić.

Ethics declarations

Conflicts of interest

The authors declare no conflict of interest.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor 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

Ćuk, N., Cvejić, S., Mladenov, V. et al. Introducing a cut-stem inoculation method for fast evaluation of sunflower resistance to Macrophomina phaseolina. Phytoparasitica 50, 775–788 (2022). https://doi.org/10.1007/s12600-022-01015-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-022-01015-0

Keywords

Navigation