Root and crown rot caused by Fusarium pseudograminearum in the euhalophyte Salicornia europaea: pathogenicity and mycotoxin production in plants grown in soilless culture
Published 2025-05-14
Keywords
- Deoxynivalenol,
- fungi,
- glasswort,
- hydroponic system,
- plant disease
- zearalenone ...More
How to Cite
Copyright (c) 2025 Emiliano DELLI COMPAGNI, Alberto PARDOSSI, Susanna PECCHIA

This work is licensed under a Creative Commons Attribution 4.0 International License.
Funding data
-
Università di Pisa
Grant numbers PRA_2020_43
Abstract
Salicornia europaea L. is a euhalophyte increasingly cultivated as a high-value green vegetable. In July 2021, root and crown rot occurred on 6-month-old S. europaea plants grown in peat-filled pots under a greenhouse, affecting 25% of plants. The causal agent was identified as Fusarium pseudograminearum O’Donnell & T. Aoki using morphological and molecular analyses. An experiment to assess the pathogenicity of this fungus to S. europaea was conducted with 96 seedlings in hydroponic culture. Half of these plants were inoculated with a conidial suspension of F. pseudograminearum. At 24 days post inoculation (dpi), half of the plants were transferred into a new hydroponic system, while the other plants were transplanted into pots. At 80 dpi, all inoculated plants grown in pots had shoot browning and desiccation symptoms, while these symptoms developed more slowly in 70% of the hydroponically grown inoculated plants. A qualitative symptom severity assessment scale showed that disease severity was greater (63%) in pot-grown plants than in hydroponically grown plants (46%). Fusarium pseudograminearum was consistently reisolated from diseased plants in both cultivation systems (62% from pots and 83% from hydroponics) fulfilling Koch’s postulates. Production of deoxynivalenol (DON) and zearalenone (ZEA) was investigated in vitro and in planta. Traces of DON (0.029 ± 0.012 mg kg-1) were found in severely damaged plants grown in hydroponics. In the in vitro test, F. pseudograminearum isolates from wheat crops in Spain (isolate ColPat-351) and Italy (isolate PVS Fu-7) were also assessed, and all tested isolates produced considerable amounts of ZEA. Fusarium pseudograminearum isolates obtained from S. europaea produced more DON (6.81 ± 0.24 mg kg-1, on average) than the Italian isolate PVS Fu-7 (0.37 ± 0.06 mg kg-1), while DON production by the Spanish isolate ColPat-351 was less than the limit of detection (< 0.25 mg kg-1). This is the first report of root and crown rot caused by F. pseudograminearum on S. europaea.
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- Abdallah-Nekache N., Laraba I., Ducos C., Barreau C., Bouznad Z., Boureghda H., 2019. Occurrence of Fusarium head blight and Fusarium crown rot in Algerian wheat: identification of associated species and assessment of aggressiveness. European Journal of Plant Pathology 154(3): 499–512. https://doi.org/10.1007/s10658-019-01673-7 DOI: https://doi.org/10.1007/s10658-019-01673-7
- Agustí-Brisach C., Raya-Ortega M.C., Trapero C., Roca L.F., Luque F., … Trapero A., 2018. First report of Fusarium pseudograminearum causing crown rot of wheat in Europe. Plant Disease 102(8): 1670. https://doi.org/10.1094/PDIS-11-17-1840-PDN DOI: https://doi.org/10.1094/PDIS-11-17-1840-PDN
- Akinsanmi O.A., Chakraborty S., Backhouse D., Simpfendorfer S., 2007. Passage through alternative hosts changes the fitness of Fusarium graminearum and Fusarium pseudograminearum. Environmental Microbiology 9(2): 512–520. https://doi.org/10.1111/j.1462-2920.2006.01168.x DOI: https://doi.org/10.1111/j.1462-2920.2006.01168.x
- Alkadri D., Nipoti P., Döll K., Karlovsky P., Prodi A., Pisi A., 2013. Study of fungal colonization of wheat kernels in Syria with a focus on Fusarium species. International Journal of Molecular Science 14(3): 5938–5951. https://doi.org/10.3390/ijms14035938 DOI: https://doi.org/10.3390/ijms14035938
- Aoki T., O’Donnell K., 1999a. Morphological and molecular characterization of Fusarium pseudograminearum sp. nov., formerly recognized as the Group 1 population of F. graminearum. Mycologia 91(4): 597–609. https://doi.org/10.1080/00275514.1999.12061058 DOI: https://doi.org/10.1080/00275514.1999.12061058
- Aoki T., O’Donnell K., 1999b Morphological characterization of Gibberella coronicola sp. nov., obtained through mating experiments of Fusarium pseudograminearum. Mycoscience 40(6): 443–453. https://doi.org/10.1007/BF02461021 DOI: https://doi.org/10.1007/BF02461021
- Araus J.L., Rezzouk F.Z., Thushar S., Shahid M., Elouafi I.A., … Serret M.D., 2021. Effect of irrigation salinity and ecotype on the growth, physiological indicators and seed yield and quality of Salicornia europaea. Plant Science 304: 110819. https://doi.org/10.1016/j.plantsci.2021.110819 DOI: https://doi.org/10.1016/j.plantsci.2021.110819
- Balmas V., 1994. Root rot of wheat in Italy caused by Fusarium graminearum Group I. Plant Disease 78: 317A. https://doi.org/10.1094/PD-78-0317A DOI: https://doi.org/10.1094/PD-78-0317A
- Belizán M.M.E., Gomez A. de los, Terán Baptista Z.P., Jimenez C.M., Sánchez Matías M. del H., … Sampietro D.A., 2019. Influence of water activity and temperature on growth and production of trichothecenes by Fusarium graminearum sensu stricto and related species in maize grains. International Journal of Food Microbiology 305: 108242. https://doi.org/10.1016/j.ijfoodmicro.2019.108242 DOI: https://doi.org/10.1016/j.ijfoodmicro.2019.108242
- Blaney B.J., Dodman R.L., 2002. Production of zearalenone, deoxynivalenol, nivalenol, and acetylated derivatives by Australian isolates of Fusarium graminearum and F. pseudograminearum in relation to source and culturing conditions. Australian Journal of Agricultural Research 53(12): 1317–1326. https://doi.org/10.1071/AR02041 DOI: https://doi.org/10.1071/AR02041
- Burgess L.W., Klein T.A., Bryden W.L., Tobin N.F., 1987. Head blight of wheat caused by Fusarium graminearum Group 1 in New South Wales in 1983. Australasian Plant Pathology 16: 72–78. https://doi.org/10.1071/APP9870072 DOI: https://doi.org/10.1071/APP9870072
- Cárdenas-Pérez S., Piernik A., Chanona-Pérez J.J., Grigore M.N., Perea-Flores M.J., 2021. An overview of the emerging trends of the Salicornia L. genus as a sustainable crop. Environmental and Experimental Botany 191: 104606. https://doi.org/10.1016/j.envexpbot.2021.104606 DOI: https://doi.org/10.1016/j.envexpbot.2021.104606
- Chakraborty S., Liu C.J., Mitter V., Scott J.B., Akinsanmi O.A., … Simpfendorfer S., 2006. Pathogen population structure and epidemiology are keys to wheat crown rot and Fusarium head blight management. Australasian Plant Pathology 35: 643–655. https://doi.org/10.1071/AP06068 DOI: https://doi.org/10.1071/AP06068
- Clear R.M., Patrick S.K., Gaba D., Roscoe M., Demeke T., … Turkington T.K., 2006. Trichothecene and zearalenone production, in culture, by isolates of Fusarium pseudograminearum from western Canada. Canadian Journal of Plant Pathology 28(1): 131–136. https://doi.org/10.1080/07060660609507279 DOI: https://doi.org/10.1080/07060660609507279
- Cui H., Wang S., Yang X., Zhang W., Chen M., … Wang S., 2022. Predictive models for assessing the risk of Fusarium pseudograminearum mycotoxin contamination in post-harvest wheat with multi-parameter integrated sensors. Food Chemistry: X 16:100472. https://doi.org/10.1016/j.fochx.2022.100472 DOI: https://doi.org/10.1016/j.fochx.2022.100472
- De Santis B., Debegnach F., Gregori E., Russo S., Marchegiani F., … Brera C., 2017. Development of a LC-MS/MS method for the multi-mycotoxin determination in composite cereal-based samples. Toxins 9(5): 169. https://doi.org/10.3390/toxins9050169 DOI: https://doi.org/10.3390/toxins9050169
- Delli Compagni E., Pardossi A., Pecchia S., 2024. Fungal and fungal-like diseases of halophytes in the Mediterranean basin: a state-of-the-art review. Horticulturae 10(4): 313. https://doi.org/10.3390/horticulturae10040313 DOI: https://doi.org/10.3390/horticulturae10040313
- Deng Y.Y., Li W., Zhang P., Sun H.Y., Zhang X.X., … Chen H.G., 2020 Fusarium pseudograminearum as an emerging pathogen of crown rot of wheat in eastern China. Plant Pathology 69(2):240–248. https://doi.org/10.1111/ppa.13122 DOI: https://doi.org/10.1111/ppa.13122
- Desjardins A.E., Proctor R., Bai G., McCormick S., Shaner G., … Hohn T.M., 1996 Reduced virulence of trichothecene-nonproducing mutants of Gibberella zeae in wheat field tests. Molecular Plant-Microbe Interactions. 9(9): 775. http://doi.org/10.1094/MPMI-9-0775 DOI: https://doi.org/10.1094/MPMI-9-0775
- EFSA Panel on Plant Health (PLH), Bragard C, Baptista P, Chatzivassiliou E, Di Serio F, Gonthier P, … Reignault P.L., 2022 Pest categorisation of Fusarium pseudograminearum. EFSA Journal 20:e07399. https://doi.org/10.2903/j.efsa.2022.7399 DOI: https://doi.org/10.2903/j.efsa.2022.7399
- Han Z., Shen Y., Di Mavungu J.D., Zhang D., Nie D., Jiang K., … Zhao Z., 2018. Relationship between environmental conditions, TRI5 gene expression and deoxynivalenol production in stored Lentinula edodes infected with Fusarium graminearum. World Mycotoxin Journal 11(2): 177–186. https://doi.org/10.3920/WMJ2017.2245 DOI: https://doi.org/10.3920/WMJ2017.2245
- Hope R., Aldred D., Magan N., 2005. Comparison of environmental profiles for growth and deoxynivalenol production by Fusarium culmorum and F. graminearum on wheat grain. Letters in Applied Microbiology 40(4): 295–300. https://doi.org/10.1111/j.1472-765X.2005.01674.x DOI: https://doi.org/10.1111/j.1472-765X.2005.01674.x
- Iqbal S.Z., 2021. Mycotoxins in food, recent development in food analysis and future challenges; a review. Current Opinion in Food Science 42: 237–247. https://doi.org/10.1016/j.cofs.2021.07.003 DOI: https://doi.org/10.1016/j.cofs.2021.07.003
- Kammoun L.G., Gargouri S., Hajlaoui M.R., Marrakchi M., 2009. Occurrence and distribution of Microdochium and Fusarium species isolated from durum wheat in northern Tunisia and detection of mycotoxins in naturally infested grain. Journal of Phytopathology 157(9): 546–551. https://doi.org/10.1111/j.1439-0434.2008.01522.x DOI: https://doi.org/10.1111/j.1439-0434.2008.01522.x
- Kazan K., Gardiner D.M., 2018. Fusarium crown rot caused by Fusarium pseudograminearum in cereal crops: recent progress and future prospects. Molecular Plant Pathology 19(7): 1547–1562. https://doi.org/10.1111/mpp.12639 DOI: https://doi.org/10.1111/mpp.12639
- Khatri B.B., Tegg R.S., Brown P.H., Wilson C.R., 2011. Temporal association of potato tuber development with susceptibility to common scab and Streptomyces scabiei-induced responses in the potato periderm. Plant Pathology 60(4): 776–786. https://doi.org/10.1111/j.1365-3059.2011.02435.x DOI: https://doi.org/10.1111/j.1365-3059.2011.02435.x
- Kokkonen M., Ojala L., Parikka P., Jestoi M., 2010. Mycotoxin production of selected Fusarium species at different culture conditions. International Journal of Food Microbiology 143(2): 17‒25. https://doi.org/10.1016/j.ijfoodmicro.2010.07.015 DOI: https://doi.org/10.1016/j.ijfoodmicro.2010.07.015
- Lombardi T., Bertacchi A., Pistelli L., Pardossi A., Pecchia S., … Sanmartin C., 2022. Biological and agronomic traits of the main halophytes widespread in the Mediterranean region as potential new vegetable crops. Horticulturae 8(3): 195. https://doi.org/10.3390/horticulturae8030195 DOI: https://doi.org/10.3390/horticulturae8030195
- Lopes M., Castilho M., Sanches-Silva A., Freitas A., Barbosa J., … Ramos F., 2020. Evaluation of the mycotoxins content of Salicornia spp.: a gourmet plant alternative to salt. Food Additives & Contaminants: Part B 13(3): 162–170. https://doi.org/10.1080/19393210.2020.1741692 DOI: https://doi.org/10.1080/19393210.2020.1741692
- Lysøe E., Klemsdal S.S., Bone K.R., Frandsen R.J.N., Johansen T., … Giese H., 2006. The PKS4 gene of Fusarium graminearum is essential for zearalenone production. Applied Environmental Microbiology 72(6): 3924–3932. https://doi.org/10.1128/AEM.00963-05 DOI: https://doi.org/10.1128/AEM.00963-05
- Maurer D., Sadeh A., Chalupowicz D., Barel S., Shimshoni J.A., Kenigsbuch D., 2023. Hydroponic versus soil-based cultivation of sweet basil: impact on plants’ susceptibility to downy mildew and heat stress, storability and total antioxidant capacity. Journal of the Science of Food and Agriculture 103(15): 7809–7815. https://doi.org/10.1002/jsfa.12860 DOI: https://doi.org/10.1002/jsfa.12860
- McKinney H.H., 1923. Influence of soil temperature and moisture on infection of wheat seedlings by Helminthosporium sativum. Journal of Agricultural Research 26: 195–218.
- Meng K., Wang Y., Yang P., Luo H., Bai Y., Yao B., 2010. Rapid detection and quantification of zearalenone-producing Fusarium species by targeting the zearalenone synthase gene PKS4. Food Control 21(2): 207–11. https://doi.org/10.1016/j.foodcont.2009.05.014 DOI: https://doi.org/10.1016/j.foodcont.2009.05.014
- Miličević T., Kaliterna J., Ivić D., Stričak A., 2013. Identification and occurrence of Fusarium species on seeds of common vetch, white lupin and some wild legumes. Poljoprivreda 19(1): 25–32.
- Moulin F., Lemanceau P., Alabouvette C., 1994. Pathogenicity of Pythium species on cucumber in peat-sand, rockwool and hydroponics. European Journal of Plant Pathology 100: 3–17. https://doi.org/10.1007/BF01871963 DOI: https://doi.org/10.1007/BF01871963
- Nahle S., El Khoury A., Atoui A., 2021. Current status on the molecular biology of zearalenone: its biosynthesis and molecular detection of zearalenone producing Fusarium species. European Journal of Plant Pathology 159: 247‒258. https://doi.org/10.1007/s10658-020-02173-9 DOI: https://doi.org/10.1007/s10658-020-02173-9
- Niessen M.L., Vogel R.F., 1998. Group specific PCR-detection of potential trichothecene-producing Fusarium-species in pure cultures and cereal samples. Systematic and Applied Microbiology 21(4): 618–631. https://doi.org/10.1016/S0723-2020(98)80075-1 DOI: https://doi.org/10.1016/S0723-2020(98)80075-1
- Nirenberg H.I., 1981. A simplified method for identifying Fusarium spp. occurring on wheat. Canadian Journal of Botany 59(9): 1599–1609. https://doi.org/10.1139/b81-217 DOI: https://doi.org/10.1139/b81-217
- O’Donnell K., Kistler H.C., Cigelnik E., Ploetz R.C., 1998. Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proceedings of the National Academy of Science 95(5): 2044–2049. https://doi.org/10.1073/pnas.95.5.2044 DOI: https://doi.org/10.1073/pnas.95.5.2044
- Obanor F., Neate S., Simpfendorfer S., Sabburg R., Wilson P., Chakraborty S., 2013. Fusarium graminearum and Fusarium pseudograminearum caused the 2010 head blight epidemics in Australia. Plant Pathology 62(1): 79–91. https://doi.org/10.1111/j.1365-3059.2012.02615.x DOI: https://doi.org/10.1111/j.1365-3059.2012.02615.x
- Pasquali M., Migheli Q., 2014. Genetic approaches to chemotype determination in type B-trichothecene producing Fusaria. International Journal of Food Microbiology. 189: 164‒182. https://doi.org/10.1016/j.ijfoodmicro.2014.08.011 DOI: https://doi.org/10.1016/j.ijfoodmicro.2014.08.011
- Poole G.J., Smiley R.W., Walker C., Huggins D., Rupp R., … Paulitz T.C., 2013. Effect of climate on the distribution of Fusarium spp. causing crown rot of wheat in the Pacific Northwest of the United States. Phytopathology 103(11): 1130–1140. https://doi.org/10.1094/PHYTO-07-12-0181-R DOI: https://doi.org/10.1094/PHYTO-07-12-0181-R
- Proctor R.H., Hohn T.M., McCormick S.P., 1995. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Molecular Plant-Microbe Interactions 8(4): 593–601. https://doi.org/10.1094/mpmi-8-0593 DOI: https://doi.org/10.1094/MPMI-8-0593
- Rueda Puente E.O., Hernandez Montiel L.G., Holguin Peña J., Murillo Amador B., Rivas Santoyo F.J., 2014. First report of Botrytis cinerea Pers. on Salicornia bigelovii Torr. in North-West México. Journal of Phytopathology 162(7-8): 513–515. https://doi.org/10.1111/jph.12205 DOI: https://doi.org/10.1111/jph.12205
- Rybecky A.I., Chulze S.N., Chiotta M.L., 2018. Effect of water activity and temperature on growth and trichothecene production by Fusarium meridionale. International Journal of Food Microbiology 285: 69–73. https://doi.org/10.1016/j.ijfoodmicro.2018.07.028 DOI: https://doi.org/10.1016/j.ijfoodmicro.2018.07.028
- Sabburg R., Obanor F., Aitken E., Chakraborty S., 2015. Changing fitness of a necrotrophic plant pathogen under increasing temperature. Global Change Biology 21(8): 3126–3137. https://doi.org/10.1111/gcb.12927 DOI: https://doi.org/10.1111/gcb.12927
- Sever Z., Ivić D., Kos T., Miličević T., 2012. Identification of Fusarium species isolated from stored apple fruit in Croatia. Archives of Industrial Hygiene and Toxicology 63(4): 463–470. https://doi.org/10.2478/10004-1254-63-2012-2227 DOI: https://doi.org/10.2478/10004-1254-63-2012-2227
- Shan X., Zhu Y., Redman R., Rodriguez R.J., Yuan Z., 2021. The chromosome-scale genome resource for two endophytic Fusarium species, F. culmorum and F. pseudograminearum. Molecular Plant-Microbe Interactions 34(6): 703–706. https://doi.org/10.1094/MPMI-07-20-0205-A DOI: https://doi.org/10.1094/MPMI-07-20-0205-A
- Song A., Xue G., Cui P., Fan F., Liu H., … Liang Y., 2016.The role of silicon in enhancing resistance to bacterial blight of hydroponic- and soil-cultured rice. Scientific Reports 6: 24640. https://doi.org/10.1038/srep24640 DOI: https://doi.org/10.1038/srep24640
- Spada M., Pugliesi C., Fambrini M., Palpacelli D., Pecchia S., 2023. Knockdown of BMP1 and PLS1 virulence genes by exogenous application of RNAi-Inducing dsRNA in Botrytis cinerea. International Journal of Molecular Sciences 24(5): 4869. https://doi.org/10.3390/ijms24054869 DOI: https://doi.org/10.3390/ijms24054869
- Starkey D.E., Ward T.J., Aoki T., Gale L.R., Kistler H.C., O’Donnell K., 2007. Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genetics and Biology 44(11): 1191–1204. https://doi.org/10.1016/j.fgb.2007.03.001 DOI: https://doi.org/10.1016/j.fgb.2007.03.001
- Tunali B., Nicol J.M., Hodson D., Uçkun Z., Büyük O., … Bağci H., 2008. Root and crown rot fungi associated with spring, facultative, and winter wheat in Turkey. Plant Disease 92(9): 1299–1306. https://doi.org/10.1094/PDIS-92-9-1299 DOI: https://doi.org/10.1094/PDIS-92-9-1299
- Ventura Y., Sagi M., 2013. Halophyte crop cultivation: the case for Salicornia and Sarcocornia. Environmental and Experimental Botany 92: 144–153. https://doi.org/10.1016/j.envexpbot.2012.07.010 DOI: https://doi.org/10.1016/j.envexpbot.2012.07.010
- Xu F., Song Y.L., Wang J.M., Liu L.L., Zhao K., 2017. Occurrence of Fusarium crown rot caused by Fusarium pseudograminearum on barley in China. Plant Disease 101(5): 837. https://doi.org/10.1094/PDIS-10-16-1436-PDN DOI: https://doi.org/10.1094/PDIS-10-16-1436-PDN
- Zhou H., He X., Wang S., Ma Q., Sun B., Ding S., … Li H., 2019. Diversity of the Fusarium pathogens associated with crown rot in the Huanghuai wheat-growing region of China. Environmental Microbiology 21(8): 2740–2754. https://doi.org/10.1111/1462-2920.14602 DOI: https://doi.org/10.1111/1462-2920.14602