Research Papers
Unraveling the infection process of garlic by Fusarium proliferatum, the causal agent of root rot
Christel LEYRONAS
Published 2020-07-17
Keywords
- Fusarium,
- histology,
- electron microscopy,
- garlic rot,
- host-parasite interaction
How to Cite
[1]
P. L. CHRÉTIEN, S. . LAURENT, I. BORNARD, C. TROULET, M. EL MAÂTAOUI, and C. LEYRONAS, “Unraveling the infection process of garlic by Fusarium proliferatum, the causal agent of root rot”, Phytopathol. Mediterr., vol. 59, no. 2, pp. 285–293, Jul. 2020.
Funding data
-
Agence Nationale de la Recherche
Grant numbers n°2017/1440
Abstract
Since the mid-2000s, and despite demanding production rules, Fusarium proliferatum (Matsushima) Niremberg has been found on garlic heads during storage inducing root and bulbs rots. Brown spots on the surface of garlic cloves and water-soaking of heads were noted. Histological observations of the fungus during early stages of infection were made from clove to the cellular levels. Fusarium proliferatum germinates, colonizes roots and degrades the outer root and parechchyma cell layers 72 h post inoculation. Conidium germination and host colonization are facilitated by the emergence of garlic roots, creating cellular debris and natural wounds. Hyphae of the pathogen did not penetrate healthy host cells and appeared to degrade them before penetration. These results provide understanding of when and how quickly F. prolife-ratum penetrates garlic bulbs. This is a primary step towards elucidating the life cycle of this pathogen during the garlic drying process, and development of an efficient and sustainable bulb rot management strategy.
Downloads
Download data is not yet available.
Metrics
Metrics Loading ...
References
Agrios GN, 2005. Plant Pathology. 5th edition. Elsevier, 922p.
Alberti I., Prodi A., Montanari M., Paglia G., Asioli C., Nipoti P., 2018. First report of Fusarium proliferatum associated with Allium fistulosum L. in Italy. Journal of Plant Diseases and Protection. 125:231–233.
Basallote-Ureba M.J., Melero-Vara J.M., 1993. Control of garlic white rot by soil solarization. Crop Protection. 12:219–223.
Bjelić D., Ignjatov M., Marinković J., Milošević D., Nikolić Z., Gvozdanović-Varga J., Karaman M., 2018. Bacillus isolates as potential biocontrol agents of Fusarium clove rot of garlic. Zemdirbyste-Agriculture. 105:369–376.
Borrero C., Capote N., Gallardo M.A., Avilés M., 2018. First report of vascular wilt caused by Fusarium proliferatum on strawberry in Spain. Plant Disease. 103:581.
Clark G., 1981. Staining Procedures. 4th Edition. Williams & Wilkins. Baltimore. 512p.
Chen C., Liu C.-H., Cai J., Zhang W., Qi W.-L., Wang Z., Liu Z.-B., Yang Y., 2018. Broad-spectrum antimicrobial activity, chemical composition and mechanism of action of garlic (Allium sativum) extracts. Food Control. 86:117–125.
Curtis H., Noll U., Störmann J., Slusarenko A.J., 2004. Broad-spectrum activity of the volatile phytoanticipin allicin in extracts of garlic (Allium sativum L.) against plant pathogenic bacteria, fungi and oomycetes. Physiological and Molecular Plant Pathology. 65:79–89.
Delgado-Ortiz J.C., Ochoa-Fuentes Y.M., Cerna-Chávez E., Beltrán-Beache M., Rodríguez-Guerra R., Aguirre-Uribe L.A., Vázquez-Martínez O., 2016. Patogenicidad de especies de Fusarium asociadas a la pudrición basal del ajo en el centro norte de México. Revista Argentina de Microbiologia. 48:222–228.
Díaz Arias M.M., Munkvold G.P., Leandro L. F., 2011. First Report of Fusarium proliferatum causing root rot on soybean (Glycine max) in the United States. Plant Disease. 95:1316.
Dugan F.M., Hellier B.C., Lupien S. L., 2003. First report of Fusarium proliferatum causing rot of garlic bulbs in North America. Plant Pathology. 52:426.
El Maâtaoui M., Pichot C., 1999. Nuclear and cell fusion cause polyploidy in the megagametophyte of common cypress, Cupressus sempervirens L. Planta. 208:345–351.
European Parliament. Establishing a framework for Community action to achieve the sustainable use of pesticides. DIRECTIVE 2009/128/EC.
Hernández-Fernaud J.R., Marina A., González K., Vázquez J., Falcón M.A., 2006. Production, partial characterization and mass spectrometric studies of the extracellular laccase activity from Fusarium proliferatum. Applied Microbiology and Biotechnology. 70:212–221.
Food and Agriculture Organization of the United Nations website. http://www.fao.org/faostat/en/#data/QC/visualize. Accessed 6 Sep 2018.
Gil-Serna J., Gálvez L., París M., Palmero D., 2016. Fusarium proliferatum from rainwater and rooted garlic show genetic and pathogenicity differences. European Journal of Plant Pathology. 146:199–206.
Ignjatov M., Bjelić D., Nikolić Z., Milošević D., Gvozdanović-Varga J., Marinković J., Ivanović Ž., 2017. First report of Fusarium acuminatum causing garlic bulb rot in serbia. Plant Disease. 101:1047.
INAO website. https://www.inao.gouv.fr. Accessed 6 Jun 2019.
Keshri G., Magan N., 2000. Detection and differentiation between mycotoxigenic and non-mycotoxigenic strains of two Fusarium spp. using volatile production profiles and hydrolytic enzymes. Journal of Applied Microbiology. 89:825–833.
Koike S.T., Gordon T.R., 2015. Management of Fusarium wilt of strawberry. Crop Protection. 73:67–72.
Koleva K., 2004. Variety of species and spread of fungi of genus Fusarium related to rotting of garlic. Bulgarian Journal of Agricultural Science. 10:177–180.
Lebiush-Mordechai S., Erlich O., Maymon M., Freeman S., Ben-David T., Ofek T., Palevski E., Tsror Lahkin L., 2014. Bulb and root rot in lily (Lilium longiflorum) and onion (Allium cepa) in Israel. Journal of Phytopathology. 162:466–471.
Leontiev R., Hohaus N., Jacob C., Gruhlke M.C.H., Slusarenko A.J., 2018. A comparison of the antibacterial and antifungal activities of thiosulfinate analogues of allicin. Scientific Reports. 8:1–19.
Leyronas C., Chrétien P.L., Troulet C., Duffaud M., Villeneuve F., Morris C.E., Hunyadi H., 2018. First Report of Fusarium proliferatum causing garlic clove rot in France. Plant Disease. 102:2658.
Linder T., 2018. Assimilation of alternative sulfur sources in fungi. World Journal of Microbiology and Biotechnology. 34:51.
Moharam M.H.A., Farrag E.S.H., Mohamed M.D.A., 2013. Pathogenic fungi in garlic seed cloves and first report of Fusarium proliferatum causing cloves rot of stored bulbs in upper Egypt. Archives of Phytopathology and Plant Protection. 46:2096–2103.
Ndambi B., Cadisch G., Elzein A., Heller A., 2012. Tissue specific reactions of sorghum roots to the mycoherbicide Fusarium oxysporum f. sp. strigae versus the pathogenic F. proliferatum. Biocontrol Science and Technology. 22:135–150.
Nelson P.E., 1981. Chapter 3: Life cycle and epidemiology of Fusarium oxysporum. In: Mace M. Fungal wilt diseases of plants. Academic press. p. 51-78.
Ochoa Fuentes Y.M., Cerna Chávez E., Gallegos Morales G., Landeros Flores J., Delgado Ortiz J.C., Hernández Camacho S., Rodríguez Guerra R., Olalde Portugal V., 2012. Identificación de especies de Fusarium en semilla de ajo en Aguascalientes, México. Revista Mexicana de Micologia. 36:27–32.
O’Donnell K., Rooney A.P., Proctor R.H., Brown D.W., McCormick S.P., Ward T.J., Frandsen R.J.N., Lysøe E., Rehner S.A., Aoki T., 2013. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genetics and Biology. 52:20–31.
Regalado V., Perestelo F., Rodríguez A., Carnicero A., Sosa F.J., De la Fuente G., Falcón M.A., 1999. Activated oxygen species and two extracellular enzymes: laccase and aryl-alcohol oxidase, novel for the lignin-degrading fungus Fusarium proliferatum. Applied Microbiology and Biotechnology. 51:388–390.
Ricard P., 2017. Les premiers pas vers l’étiologie et l’épidémiologie d’une maladie multifactorielle et en expansion : la fusariose de l’ail (Allium sativum L.). https://dumas.ccsd.cnrs.fr/dumas-01618306. Accessed 14 Oct 2019.
Roberts P.A., Matthews W.C., 1995. Disinfection alternatives for control of Ditylenchus dipsaci in garlic seed cloves. Journal of Nematology. 27:448–456.
Sankar N.R., Babu G.P., 2012. First Report of Fusarium proliferatum causing rot of garlic bulbs (Allium sativum) in India. Plant Disease. 96:290.
Seefelder W., Gossmann M., Humpf H.-U., 2002. Analysis of fumonisin B(1) in Fusarium proliferatum-infected asparagus spears and garlic bulbs from Germany by liquid chromatography-electrospray ionization mass spectrometry. Journal of Agricultural and Food Chemistry. 50:2778–2781.
Shvetsova S.V., Zhurishkina E.V., Bobrov K.S., Ronzhina N.L., Lapina I.M., Ivanen D.R., Gagkaeva T.Y., Kulminskaya A.A., 2015. The novel strain Fusarium proliferatum LE1 (RCAM02409) produces α- L -fucosidase and arylsulfatase during the growth on fucoidan: Alfa-L-fucosidase and arylsulfatase from the novel strain Fusarium proliferatum. Journal of Basic Microbiology. 55:471–479.
Stankovic S., Levic J., Petrovic T., Logrieco A., Moretti A., 2007. Pathogenicity and mycotoxin production by Fusarium proliferatum isolated from onion and garlic in Serbia. European Journal of Plant Pathology. 118:165–172.
Toit L.J., Inglis D.A., Pelter G.Q., 2003. Fusarium proliferatum pathogenic on onion bulbs in Washington. Plant Disease. 87:750.
Tonti S., Prà M.D., Nipoti P., Prodi A., Alberti I., 2012. First Report of Fusarium proliferatum causing rot of stored garlic bulbs (Allium sativum L.) in Italy. Journal of Phytopathology. 160:761–763.
This H., 2006. Molecular gastronomy: exploring the science of flavor. Columbia University Press.
Totelin L., 2015. When foods become remedies in ancient Greece: The curious case of garlic and other substances. Journal of Ethnopharmacology. 167:30–37.
Tridge website. https://www.tridge.com/search?q=garlic. Accessed 10 Aug 2019.
Xie S.H., Zhang C., Chen M.S., Wei Z.P., Jiang Y.B.., Lin X., Zheng Y.Q., 2018. Fusarium proliferatum : a new pathogen causing fruit rot of peach in Ningde, China. Plant Disease. 102:1858.
Yamazaki M., Morita Y., Kashiwa T., Teraoka T., Arie T., 2013. Fusarium proliferatum, an additional bulb rot pathogen of Chinese chive. Journal of General Plant Pathology. 79:431–434.
Yao Y., Xue Z., Hong C., Zhu F., Chen X., Wang W., Cai Z., Huang N., Yang X., 2016. Efficiency of different solarization-based ecological soil treatments on the control of Fusarium wilt and their impacts on the soil microbial community. Applied Soil Ecology. 108:341–351.
Alberti I., Prodi A., Montanari M., Paglia G., Asioli C., Nipoti P., 2018. First report of Fusarium proliferatum associated with Allium fistulosum L. in Italy. Journal of Plant Diseases and Protection. 125:231–233.
Basallote-Ureba M.J., Melero-Vara J.M., 1993. Control of garlic white rot by soil solarization. Crop Protection. 12:219–223.
Bjelić D., Ignjatov M., Marinković J., Milošević D., Nikolić Z., Gvozdanović-Varga J., Karaman M., 2018. Bacillus isolates as potential biocontrol agents of Fusarium clove rot of garlic. Zemdirbyste-Agriculture. 105:369–376.
Borrero C., Capote N., Gallardo M.A., Avilés M., 2018. First report of vascular wilt caused by Fusarium proliferatum on strawberry in Spain. Plant Disease. 103:581.
Clark G., 1981. Staining Procedures. 4th Edition. Williams & Wilkins. Baltimore. 512p.
Chen C., Liu C.-H., Cai J., Zhang W., Qi W.-L., Wang Z., Liu Z.-B., Yang Y., 2018. Broad-spectrum antimicrobial activity, chemical composition and mechanism of action of garlic (Allium sativum) extracts. Food Control. 86:117–125.
Curtis H., Noll U., Störmann J., Slusarenko A.J., 2004. Broad-spectrum activity of the volatile phytoanticipin allicin in extracts of garlic (Allium sativum L.) against plant pathogenic bacteria, fungi and oomycetes. Physiological and Molecular Plant Pathology. 65:79–89.
Delgado-Ortiz J.C., Ochoa-Fuentes Y.M., Cerna-Chávez E., Beltrán-Beache M., Rodríguez-Guerra R., Aguirre-Uribe L.A., Vázquez-Martínez O., 2016. Patogenicidad de especies de Fusarium asociadas a la pudrición basal del ajo en el centro norte de México. Revista Argentina de Microbiologia. 48:222–228.
Díaz Arias M.M., Munkvold G.P., Leandro L. F., 2011. First Report of Fusarium proliferatum causing root rot on soybean (Glycine max) in the United States. Plant Disease. 95:1316.
Dugan F.M., Hellier B.C., Lupien S. L., 2003. First report of Fusarium proliferatum causing rot of garlic bulbs in North America. Plant Pathology. 52:426.
El Maâtaoui M., Pichot C., 1999. Nuclear and cell fusion cause polyploidy in the megagametophyte of common cypress, Cupressus sempervirens L. Planta. 208:345–351.
European Parliament. Establishing a framework for Community action to achieve the sustainable use of pesticides. DIRECTIVE 2009/128/EC.
Hernández-Fernaud J.R., Marina A., González K., Vázquez J., Falcón M.A., 2006. Production, partial characterization and mass spectrometric studies of the extracellular laccase activity from Fusarium proliferatum. Applied Microbiology and Biotechnology. 70:212–221.
Food and Agriculture Organization of the United Nations website. http://www.fao.org/faostat/en/#data/QC/visualize. Accessed 6 Sep 2018.
Gil-Serna J., Gálvez L., París M., Palmero D., 2016. Fusarium proliferatum from rainwater and rooted garlic show genetic and pathogenicity differences. European Journal of Plant Pathology. 146:199–206.
Ignjatov M., Bjelić D., Nikolić Z., Milošević D., Gvozdanović-Varga J., Marinković J., Ivanović Ž., 2017. First report of Fusarium acuminatum causing garlic bulb rot in serbia. Plant Disease. 101:1047.
INAO website. https://www.inao.gouv.fr. Accessed 6 Jun 2019.
Keshri G., Magan N., 2000. Detection and differentiation between mycotoxigenic and non-mycotoxigenic strains of two Fusarium spp. using volatile production profiles and hydrolytic enzymes. Journal of Applied Microbiology. 89:825–833.
Koike S.T., Gordon T.R., 2015. Management of Fusarium wilt of strawberry. Crop Protection. 73:67–72.
Koleva K., 2004. Variety of species and spread of fungi of genus Fusarium related to rotting of garlic. Bulgarian Journal of Agricultural Science. 10:177–180.
Lebiush-Mordechai S., Erlich O., Maymon M., Freeman S., Ben-David T., Ofek T., Palevski E., Tsror Lahkin L., 2014. Bulb and root rot in lily (Lilium longiflorum) and onion (Allium cepa) in Israel. Journal of Phytopathology. 162:466–471.
Leontiev R., Hohaus N., Jacob C., Gruhlke M.C.H., Slusarenko A.J., 2018. A comparison of the antibacterial and antifungal activities of thiosulfinate analogues of allicin. Scientific Reports. 8:1–19.
Leyronas C., Chrétien P.L., Troulet C., Duffaud M., Villeneuve F., Morris C.E., Hunyadi H., 2018. First Report of Fusarium proliferatum causing garlic clove rot in France. Plant Disease. 102:2658.
Linder T., 2018. Assimilation of alternative sulfur sources in fungi. World Journal of Microbiology and Biotechnology. 34:51.
Moharam M.H.A., Farrag E.S.H., Mohamed M.D.A., 2013. Pathogenic fungi in garlic seed cloves and first report of Fusarium proliferatum causing cloves rot of stored bulbs in upper Egypt. Archives of Phytopathology and Plant Protection. 46:2096–2103.
Ndambi B., Cadisch G., Elzein A., Heller A., 2012. Tissue specific reactions of sorghum roots to the mycoherbicide Fusarium oxysporum f. sp. strigae versus the pathogenic F. proliferatum. Biocontrol Science and Technology. 22:135–150.
Nelson P.E., 1981. Chapter 3: Life cycle and epidemiology of Fusarium oxysporum. In: Mace M. Fungal wilt diseases of plants. Academic press. p. 51-78.
Ochoa Fuentes Y.M., Cerna Chávez E., Gallegos Morales G., Landeros Flores J., Delgado Ortiz J.C., Hernández Camacho S., Rodríguez Guerra R., Olalde Portugal V., 2012. Identificación de especies de Fusarium en semilla de ajo en Aguascalientes, México. Revista Mexicana de Micologia. 36:27–32.
O’Donnell K., Rooney A.P., Proctor R.H., Brown D.W., McCormick S.P., Ward T.J., Frandsen R.J.N., Lysøe E., Rehner S.A., Aoki T., 2013. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genetics and Biology. 52:20–31.
Regalado V., Perestelo F., Rodríguez A., Carnicero A., Sosa F.J., De la Fuente G., Falcón M.A., 1999. Activated oxygen species and two extracellular enzymes: laccase and aryl-alcohol oxidase, novel for the lignin-degrading fungus Fusarium proliferatum. Applied Microbiology and Biotechnology. 51:388–390.
Ricard P., 2017. Les premiers pas vers l’étiologie et l’épidémiologie d’une maladie multifactorielle et en expansion : la fusariose de l’ail (Allium sativum L.). https://dumas.ccsd.cnrs.fr/dumas-01618306. Accessed 14 Oct 2019.
Roberts P.A., Matthews W.C., 1995. Disinfection alternatives for control of Ditylenchus dipsaci in garlic seed cloves. Journal of Nematology. 27:448–456.
Sankar N.R., Babu G.P., 2012. First Report of Fusarium proliferatum causing rot of garlic bulbs (Allium sativum) in India. Plant Disease. 96:290.
Seefelder W., Gossmann M., Humpf H.-U., 2002. Analysis of fumonisin B(1) in Fusarium proliferatum-infected asparagus spears and garlic bulbs from Germany by liquid chromatography-electrospray ionization mass spectrometry. Journal of Agricultural and Food Chemistry. 50:2778–2781.
Shvetsova S.V., Zhurishkina E.V., Bobrov K.S., Ronzhina N.L., Lapina I.M., Ivanen D.R., Gagkaeva T.Y., Kulminskaya A.A., 2015. The novel strain Fusarium proliferatum LE1 (RCAM02409) produces α- L -fucosidase and arylsulfatase during the growth on fucoidan: Alfa-L-fucosidase and arylsulfatase from the novel strain Fusarium proliferatum. Journal of Basic Microbiology. 55:471–479.
Stankovic S., Levic J., Petrovic T., Logrieco A., Moretti A., 2007. Pathogenicity and mycotoxin production by Fusarium proliferatum isolated from onion and garlic in Serbia. European Journal of Plant Pathology. 118:165–172.
Toit L.J., Inglis D.A., Pelter G.Q., 2003. Fusarium proliferatum pathogenic on onion bulbs in Washington. Plant Disease. 87:750.
Tonti S., Prà M.D., Nipoti P., Prodi A., Alberti I., 2012. First Report of Fusarium proliferatum causing rot of stored garlic bulbs (Allium sativum L.) in Italy. Journal of Phytopathology. 160:761–763.
This H., 2006. Molecular gastronomy: exploring the science of flavor. Columbia University Press.
Totelin L., 2015. When foods become remedies in ancient Greece: The curious case of garlic and other substances. Journal of Ethnopharmacology. 167:30–37.
Tridge website. https://www.tridge.com/search?q=garlic. Accessed 10 Aug 2019.
Xie S.H., Zhang C., Chen M.S., Wei Z.P., Jiang Y.B.., Lin X., Zheng Y.Q., 2018. Fusarium proliferatum : a new pathogen causing fruit rot of peach in Ningde, China. Plant Disease. 102:1858.
Yamazaki M., Morita Y., Kashiwa T., Teraoka T., Arie T., 2013. Fusarium proliferatum, an additional bulb rot pathogen of Chinese chive. Journal of General Plant Pathology. 79:431–434.
Yao Y., Xue Z., Hong C., Zhu F., Chen X., Wang W., Cai Z., Huang N., Yang X., 2016. Efficiency of different solarization-based ecological soil treatments on the control of Fusarium wilt and their impacts on the soil microbial community. Applied Soil Ecology. 108:341–351.