Survival of Fusarium Graminearum, the Causal Agent of Fusarium Head Blight
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Survival of Fusarium graminearum, the causal agent of Fusarium head blight. A review Johann Leplat, Hanna Friberg, Muhammad Abid, Christian Steinberg To cite this version: Johann Leplat, Hanna Friberg, Muhammad Abid, Christian Steinberg. Survival of Fusarium gramin- earum, the causal agent of Fusarium head blight. A review. Agronomy for Sustainable Development, Springer Verlag/EDP Sciences/INRA, 2012, 33 (1), pp.97-111. 10.1007/s13593-012-0098-5. hal- 01201382 HAL Id: hal-01201382 https://hal.archives-ouvertes.fr/hal-01201382 Submitted on 17 Sep 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Agron. Sustain. Dev. (2013) 33:97–111 DOI 10.1007/s13593-012-0098-5 REVIEW ARTICLE Survival of Fusarium graminearum, the causal agent of Fusarium head blight. A review Johann Leplat & Hanna Friberg & Muhammad Abid & Christian Steinberg Accepted: 10 May 2012 /Published online: 14 June 2012 # INRA and Springer-Verlag, France 2012 Abstract Wheat is one of the most cultivated crops world- dead organic matter, particularly on crop residues. F. gra- wide. In 2010, 20 % of wheat and durum wheat were minearum adapts to a wide range of environmental varia- cultivated in Europe, 17 % in China and 9 % in Russia tions, and produces extracellular enzymes allowing feeding and in North America. Wheat yield can be highly decreased on different crop residues. However, F. graminearum com- by several factors. In particular Fusarium graminearum petes with other decomposers such as other Fusarium spp. Schwabe is a worldwide fungal pest impacting wheat pro- belonging to the same complex of species. Actually, it is not duction. F. graminearum is the causal agent of Fusarium known whether F. graminearum mycotoxins give F. grami- head blight, root and stem-base rot of cereals. Losses caused nearum a competitive advantage during the saprotrophic by Fusarium head blight in Northern and Central America period. Anthropogenic factors including preceding crops, from 1998 to 2002 reached $2.7 billion. Moreover, F. gra- tillage system and weed management can alter the develop- minearum produces mycotoxins which affect human and ment of the soil biota, which in turn can change the sapro- animal health. The threshold of these mycotoxins in food- trophic development of F. graminearum and disease risk. stuffs is regulated in Europe since 2007. F. graminearum We review the ecological requirements of F. graminearum survives for several years saprotrophically in the soil, on saprotrophic persistence. The major conclusions are: (1) temperature, water, light and O are key conditions for F. : : 2 J. Leplat M. Abid C. Steinberg (*) graminearum growth and the development of its sexual INRA, UMR1347 Agroécologie, reproduction structures on crop residues, although the fun- – Interactions Plante Microorganismes (IPM), gus can resist for a long time under extreme conditions. (2) 21065 Dijon, France e-mail: [email protected] F. graminearum survival is enhanced by high quantities of available crop residues and by rich residues, while sexual J. Leplat e-mail: [email protected] reproduction structures occur on poor residues. (3) F. gra- minearum is a poor competitor over time for residues de- M. Abid e-mail: [email protected] composition. F. graminearum survival can be controlled by : : the enhancement of the decomposition processes by other J. Leplat M. Abid C. Steinberg organisms. In addition, the development of F. graminearum Université de Bourgogne, UMR1347 Agroécologie, on crop residues can be limited by antagonistic fungi and Interactions Plante–Microorganismes (IPM), 21065 Dijon, France soil animals growing at the expense of F. graminearum- : : infested residues. (4) Agricultural practices are key fac- J. Leplat M. Abid C. Steinberg tors for the control of F. graminearum survival. A Agrosup, UMR1347 Agroécologie, suitable crop rotation and an inversive tillage can limit Interactions Plante–Microorganismes (IPM), 21065 Dijon, France the risk of Fusarium head blight development. H. Friberg Keywords Crop residues . Ecological requirements . Swedish University of Agricultural Sciences (SLU), Habitat . Mycotoxins . Preceding crop . Saprotrophic Department of Forest Mycology and Pathology, . Box 7026, 750 07 Uppsala, Sweden development Soil microbial ecology Tillage Wheat e-mail: [email protected] diseases 98 J. Leplat et al. Contents an important role in arable soils by breaking down and recy- cling plant residues, primarily cellulose and hemicellulose 1. Introduction ...............................2 (Stromberg 2005). Among them, some plant pathogenic fungi 2. Fusarium graminearum ......................3 take place and their role should be considered. Indeed, plant 2.1 Fusarium diseases on wheat ...............3 pathogenic fungi are categorised as either biotrophs or necrotr- 2.2 Saprotrophic growth ....................4 ophs, and as either obligate pathogens or facultative sapro- 2.3 Environmental factors controlling saprotrophic trophs. For example, the disease cycle of the deleterious survival ..............................5 fungus Fusarium graminearum (Fig. 1), the anamorph stage 3. Effect of crop residues as F. graminearum growth of Gibberella zeae (Schwein.) Petch is well studied (Trail substrates in the soil .........................6 2009). In a previous review, Goswami and Kistler (2004) 3.1 Effect of crop residues quantities ............6 provided an update on the pathogenesis, genetics, evolution 3.2 Effect of plant species ....................6 and genomics of F. graminearum but the ecological require- 4. Competition and antagonism ...................7 ments of its saprotrophic stage are less well understood. Fusarium head blight, root rot and foot rot (crown rot) are 4.1 Organisms succession during residue decomposition ..7 diseases that cause significant yield loss in several crops 4.2 Interactions with soil microorganisms .........7 worldwide such as wheat (Fig. 2), maize, oat (Avena sativa 4.3 Fusarium species displacement on residues .....8 L.), barley (Hordeum vulgare L.) and rice (Oryza sativa L.) 4.4 Interactions with the soil fauna .............8 (Parry et al. 1995; Pereyra and Dill-Macky 2008; Trail et al. 5. Importance of agricultural practices for the disease 2003). Yield losses caused by Fusarium head blight in development ...............................9 Northern and Central America from 1998 to 2002 were 5.1 Preceding crop .........................9 evaluated to reach $2.7 billion (Nganje et al. 2002). Several 5.2 Soil tillage ................................9 species are involved in the fungal complex that causes these 5.3 Fertilization and pesticides ...............10 diseases. Many of them also produce mycotoxins, such as 6. Conclusion ..............................11 deoxynivalenol (commonly known as DON) and its acety- lated forms 3-acetyl-4-deoxynivalenol (3-ADON) and 15- acetyl-4-deoxynivalenol (15-ADON), nivalenol (NIV) and zearalenone (ZEA) (Desjardins and Proctor 2007). These 1 Introduction mycotoxins are of major concern because of their effect on human and animal health and because they persist during Wheat (Triticum aestivum L. ssp. aestivum) is the second storage and are heat-resistant (JEFCA 2001). The threshold most cultivated crop in the world after maize (Zea mays L.). of these mycotoxins in foodstuffs is regulated in Europe since In 2010, 653 million tons of wheat and durum wheat were 2007 (CE N°1881/2006). Among the species involved in the produced in the world, of which 140.7 million tons were complex causing Fusarium disease on wheat, F. graminearum produced in Europe (FAO 2011). Moreover, the wheat is predominates in many parts of the world (Bottalico 1998; one of the most traded crops worldwide, with 125.9 million Bottalico and Perrone 2002; Parry et al. 1995). tons traded in 2010 (AGPB 2012). The cultural practices Like other Fusarium species in the complex, F. grami- trends due to economical and environmental reasons, nearum survives saprotrophically on crop residues in the i.e., reduction of soil tillage and pesticides use, raise absence of its hosts (Sutton 1982). Fusarium head blight the issue of re-emerging wheat diseases, such as fungal severity and deoxynivalenol contamination significantly diseases (McMullen et al. 1997; Millennium Ecosystem increase with the density of residues left from the preceding Assessment 2005). crop (Blandino et al. 2010). Moreover, surface residues Studies of plant pathogenic fungi generally focus on infec- provide a substrate for active growth of F. graminearum tion processes, disease development and other concerns in for a longer period of time than buried residues (Pereyra et plant–microorganism interactions, but the saprotrophic period al. 2004). Burying F. graminearum-infested crop residues of these pathogens’ life cycle is not well known. Most soil deeper in the soil can efficiently reduce F. graminearum fungi are decomposers or saprotrophs that feed on decaying populations; however, the pathogen may survive for several organic material. In fact, they play