Integrated Management of Damping-Off Diseases PDF

Agron. Sustain. Dev. (2017) 37: 10 DOI 10.1007/s13593-017-0417-y REVIEW ARTICLE Integrated management of damping-off diseases. A review Jay Ram Lamichhane 1 & Carolyne Dürr 2 & André A. Schwanck 3 & Marie-Hélène Robin 4 & Jean-Pierre Sarthou 5 & Vincent Cellier 6 & Antoine Messéan 1 & Jean-Noë...

Agron. Sustain. Dev. (2017) 37: 10 DOI 10.1007/s13593-017-0417-y REVIEW ARTICLE Integrated management of damping-off diseases. A review Jay Ram Lamichhane 1 & Carolyne Dürr 2 & André A. Schwanck 3 & Marie-Hélène Robin 4 & Jean-Pierre Sarthou 5 & Vincent Cellier 6 & Antoine Messéan 1 & Jean-Noël Aubertot 3 Accepted: 8 February 2017 / Published online: 16 March 2017 # INRA and Springer-Verlag France 2017 Abstract Damping-off is a disease that leads to the decay of However, this still is not the case and major knowledge gaps germinating seeds and young seedlings, which represents for must be filled. Here, we review up to 300 articles of the farmers one of the most important yield constraints both in damping-off literature in order to highlight major knowledge nurseries and fields. As for other biotic stresses, conventional gaps and identify future research priorities. The major findings fungicides are widely used to manage this disease, with two are (i) damping-off is an emerging disease worldwide, which major consequences. On the one hand, fungicide overuse affects all agricultural and forestry crops, both in nurseries and threatens the human health and causes ecological concerns. fields; (ii) over a dozen of soil-borne fungi and fungus-like On the other hand, this practice has led to the emergence of organisms are a cause of damping-off but only a few of them pesticide-resistant microorganisms in the environment. Thus, are frequently associated with the disease; (iii) damping-off there are increasing concerns to develop sustainable and du- may affect from 5 to 80% of the seedlings, thereby inducing rable damping-off management strategies that are less reliant heavy economic consequences for farmers; (iv) a lot of re- on conventional pesticides. Achieving such a goal requires a search efforts have been made in recent years to develop bio- better knowledge of pathogen biology and disease epidemiol- control solutions for damping-off and there are interesting ogy in order to facilitate the decision-making process. It also future perspectives; and (v) damping-off management re- demands using all available non-chemical tools that can be quires an integrated pest management (IPM) approach com- adapted to regional and specific production situations. bining both preventive and curative tactics and strategies. Given the complex nature of damping-off and the numerous factors involved in its occurrence, we recommend further re- * Jay Ram Lamichhane search on critical niches of complexity, such as seeds, seed- [email protected]; [email protected] bed, associated microbes and their interfaces, using novel and robust experimental and modeling approaches based on five 1 research priorities described in this paper. INRA, Eco-Innov Research Unit, Avenue Lucien Brétignières, F-78850 Thiverval-Grignon, France 2 INRA, IRHS 1345, 42 rue George Morel, Keywords Abiotic stresses. Best management practices. F-49071 Beaucouzé, France Economic losses. Integrated pest management. Interactions. 3 INRA, UMR AGIR 1248, 24 chemin de Borderouge–Auzeville, Seed germination. Seedling decay. Soil-borne pathogens F-31320 Castanet-Tolosan, France 4 Université de Toulouse, INPT, EI-Purpan, UMR AGIR 1248, 24 chemin de Borderouge–Auzeville, F-31320 Castanet-Tolosan, France Contents 5 Université de Toulouse, INPT, ENSAT, UMR AGIR 1248, 24 1. Introduction chemin de Borderouge–Auzeville, 2. Symptoms of damping-off F-31320 Castanet-Tolosan, France 2.1 Pre-emergence symptoms 6 INRA, Domaine expérimental d’Epoisses UE 0115, 2.2 Post-emergence symptoms F-21110 Bretenière, France 2.3 Occurrence of damping-off symptoms 10 Page 2 of 25 Agron. Sustain. Dev. (2017) 37: 10 3. Integrated management of damping-off Overall, damping-off can be caused by a number of biotic 3.1 Seed treatment to enhance germination and seed- or abiotic stresses/factors, which prevent seeds to germinate or ling vigor seedlings to emerge, including those caused by plant- 3.2 Deployment of host-plant resistance and/or toler- pathogenic bacteria or insect pests notably those living in soil ance such as Delia spp. Agriotes spp., or Melolontha spp. (Fig. 1). 3.3 Adoption of best cropping practices As a consequence, the symptoms associated with damping-off 3.4 Timely treatment interventions of seedlings with widely vary depending on the type of stress associated with it effective products and time of its occurrence. In general, many fungi and fungi- 3.4.1 Biological control like species (Table 1) have been reported as the most impor- 3.4.2 Chemical control tant biotic stress weakening or destroying seeds and seedlings 4. Key challenges and future priorities for damping-off of almost all species including fruit, vegetable, field, ornamen- management tal, and forestry crops (Filer and Peterson 1975; Kraft et al. 4.1 Correct identification of damping-off pathogens 2000). However, this paper will focus on damping-off caused including non-secondary colonizers and anasto- by Fusarium spp., Rhizoctonia spp., Pythium spp. and mosis groups Phytophthora spp. since these pathogens are the most fre- 4.2 Determination of potential interactions within and/ quently associated with damping-off and are considered the or between damping-off pathogens and other liv- most important causal agents of this problem in the literature ing organisms (Table 1). Furthermore, the role of abiotic stresses will be also 4.3 A better knowledge of the role of abiotic factors discussed as they indirectly affect damping-off occurrence. that predispose seeds and seedlings to damping-off Favorable abiotic conditions for damping-off problems gener- diseases ally involve excessive soil moisture and excessive overhead 4.4 Development of disease-suppressive seedbed soils misting, lower soil temperatures before emergence, higher soil with or without conservation agriculture temperatures after emergence, and overcrowded flats or seed- 4.5 Modeling to help design integrated management beds (Wright 1957; Papavizas and Davey 1961; Duniway strategies of damping-off diseases 1983a; James 2012a; Starkey and Enebak 2012). 5. Conclusions and perspectives In recent years, numerous soil-borne fungi belonging to Acknowledgements over a dozen of genera and oomycetes (Pythium and References Phytophthora), and some seed-borne fungi, have been report- ed to cause damping-off on a large number of crops (Table 1). Most of these pathogens are common in agricultural soils and can be spread via non-anthropic and anthropic activities, in- cluding water run-off through irrigation or rain (Zappia et al. 1 Introduction 2014), soil contamination by improperly sanitized tools, intro- duction of infected plants (mainly in case of seed-borne path- Damping-off is a historical term coined during the early nine- ogens), improperly sanitized greenhouse, and the use of con- teenth century, and represents one of the oldest worldwide taminated irrigation water (Papavizas and Davey 1961; nursery problems as discussed in detail in the classic nursery Duniway 1983b; Schmitthenner and Canaday 1983; Huang manual (Hartley and Pierce 1917; Tillotson 1917; Hartley and Kuhlman 1990; James 2012a; Starkey and Enebak 1921). Damping-off was considered “the most serious prob- 2012). Once established, damping-off pathogens are able to lem encountered in raising nursery seedlings,” and conse- survive for many years in the soil, even in the absence of host quently was one of the most focused research subject since plants, either as saprophytes or as living resting structures that the beginning of its description (Hartley and Pierce 1917). The are capable of enduring adverse conditions (Menzies 1963). definition of damping-off is not straightforward in the litera- Their wide host range also aids in the longevity of these fungi ture. Many authors refer to damping-off as a “disease” and fungus-like organisms. (McNew 1960; Horst 2013), while others refer to damping- Despite a long history behind and a number of research off as a “symptomatic condition” (Agrios 2005; Kemerait and works conducted on damping-off, it still represents one of Vidhyasekaran 2006). In the former case, damping-off is usu- the most difficult problems to be managed both in the nurser- ally associated to soil-borne pathogens while in the latter case, ies and fields. There is no country or geographic area without seed-borne pathogens can promote damping-off. damping-off problems, on a number of economically impor- Nevertheless, both interpretations comprehend that damping- tant crops. Indeed, since only the beginning of the twenty-first off involves non-germination, prevention of seedling emer- century, almost 50 new reports of damping-off diseases have gence after germination, or the rotting and collapse of seed- been noticed on over 30 crops and from over 20 countries lings at the soil level. (Table 1). This clearly suggests that damping-off problem is Agron. Sustain. Dev. (2017) 37: 10 Page 3 of 25 10 Fig. 1 Damping-off is either a disease of germinating seeds (pre- emergence—A) or young seedlings (post-emergence—B). The latter also comprises cotyledon blight. While damping- off is usually refereed to diseases caused by soil-borne fungi or oomycetes, a number of abiotic stresses may contribute to damping-off symptoms (C) (adapted from Landis (2013) multifaceted, and requires more research efforts to generate et al. 2013). Nevertheless, other conventional fungicides play further knowledge needed for a durable and sustainable man- an increasingly important role in mitigating seed and seedling agement of damping-off. damage caused by damping-off pathogens. The frequent use Overall, the economic losses due to damping-off are of these fungicides has led to the development of fungicide- represented by a direct cost, due to damages of seed or resistant isolates with additional challenges for farmers to seedlings (Fig. 2), and an indirect cost, which consists manage damping-off (Taylor et al. 2002; Moorman et al. of an additional cost of replanting and the consequent 2002; Lamichhane et al. 2016). lower yields due to the later planting dates (Babadoost In light of the high economic impact of damping-off and and Islam 2003; Bacharis et al. 2010; Horst 2013). negative environmental effects generated by conventional Although there is no detailed and precise estimation fungicide-based control strategies, there is a need to develop about the real economic impact of damping-off at the alternative and sustainable solutions to manage damping-off. global level in monetary terms, a previous study report- Integrated pest management (IPM) exemplifies a sustainable ed that 40 million extra seedlings are planted each year approach to this aim as it combines preventive measures (e.g., only in Georgia (the USA) to counterbalance losses due enhancement of seed health, which represents the core of re- to non-viable seeds and damping-off of seedlings silient agroecosystems) as well as best agronomic and cultural (Huang and Kuhlman 1990). Likewise, in 2016, in practices first and pesticide-based tactics as the last option. Brittany (France), the grass or cereal fly Geomyza Therefore, the objectives of this work were to (i) highlight tripunctata damaged thousands of hectares of maize the major features of damping-off diseases, especially those crops with significant economic losses in the region caused by Fusarium spp., Rhizoctonia spp., Pythium spp., and (BSV 2016). An extensive literature research showed Phytophthora spp.; (ii) report and discuss currently used dis- that the incidence of damping-off may vary from 5 to ease management strategies and knowledge gaps; and (iii) 80% (Table 1). suggest key challenges and future priorities for a sustainable In addition to a significant economic importance, there is a management of damping-off diseases. considerable environmental impact due to the widespread use of fungicides to manage this frequently occurring problem. For example, the methyl bromide seed treatment and fumiga- tion, a practice forbidden in the European Union (Mouttet 2 Symptoms of damping-off et al. 2014), still represents one of the major practices adopted elsewhere, including in the USA, to manage damping-off dis- Damping-off symptoms can be observed from seeding until eases (Weiland et al. 2013). However, following the Montreal the fourth to sixth week post-sowing (Horst 2013). The dis- Protocol (UNEP 2006), this practice tends to decline and re- ease symptoms can be divided in two phases based on the time strictions for soil fumigation have been increased (Weiland of its appearance. Table 1 A non-exhaustive list of studies highlighting first reports of damping-off worldwide since 2001 Continent Country Occurrence Type Host Pathogen Incidence (%) Reference Asia China 2015 Post-emergence Oat Rhizoctonia solani AG 2–1 19 (Zhang et al. 2015) 2013 Post-emergence Foxtail millet Rhizoctonia AG-A 30 (Ou et al. 2015) 10 Page 4 of 25 2010 Post-emergence Sugar beet Rhizoctonia AG-A 20 (Wang and Wu 2012) 2011 Post-emergence Chinese cabbage Alternaria japonica ND (Ren et al. 2012) 2010 Post-emergence Rhodiola sachalinensis Rhizoctonia solani AG-4 HG-II 60 (Bai et al. 2011) 2003 Post-emergence Swiss chard Rhizoctonia solani AG-4 HG/AG-A 80 (Yang et al. 2007) 2014 Post-emergence Schisandra chinensis Rhizoctonia solani AG-4 HG-I 10 (Ou et al. 2015) India 2011 Post-emergence Mexican marigold Ceratobasidium sp. 15 (Saroj et al. 2013) Iran 2000 Post-emergence Sugar beet Pythium spp. ND (Babai-Ahary et al. 2004) Iraq 2012 Post-emergence Okra Phytophthora nicotianae ND (Matny 2012) Japan 2005 Pre-emergence Okra Pythium ultimum var. ultimum 25 (Kida et al. 2007) 2007 Post-emergence broccoli Rhizoctonia solani AG-2-2 IV ND (Misawa et al. 2015) Malaysia 2010 Post-emergence Coconut Marasmiellus palmivorus ND (Almaliky et al. 2012) Oman 2004–2005 Post-emergence Cucumber Pythium spp. ND (Al-Sa’di et al. 2007) Turkey 2009 Post-emergence Wheat Rhizoctonia solani AG 8 ND (Ünal and Sara Dolar 2012) Africa Algeria 2008–2009 Pre- and post-emergence Aleppo pine Fusarium equiseti 64–77 (Lazreg et al. 2013a) 2008–2010 Pre- and post-emergence Aleppo pine Globisporangium ultimum ND (Lazreg et al. 2013b) 2008–2009 Pre- and post-emergence Aleppo pine Fusarium chlamydosporum 64–77 (Lazreg et al. 2013c) 2008–2009 Pre- and post-emergence Aleppo pine Fusarium redolens 64–77 (Lazreg et al. 2013d) 2008–2009 Pre- and post-emergence Aleppo pine Fusarium acuminatum 64–77 (Lazreg et al. 2013e) Benin 2001–2002 Post-emergence Cowpea Phoma sp. and other fungal species ND (Adandonon et al. 2004) Egypt 2000 Pre- and post-emergence Wheat Pythium diclinum ND (Abdelzaher 2004) Europe Greece 2007 Post-emergence Cotton and tobacco Rhizoctonia spp ND (Bacharis et al. 2010) Italy 2007 Post-emergence Bottlebrush Cylindrocladium scoparium 30–70 (Polizzi et al. 2007) 2006 Pre- and post-emergence Oak Cylindrocladiella parva 65 (Scattolin and Montecchio 2007) 2004 Pre- and post-emergence Beech Fusarium avenaceum 70 (Montecchio 2005) 2010 Post-emergence Leaf beet Pythium aphanidermatum 20 (Garibaldi et al. 2013) 2011 Post-emergence strawberry tree Colletotrichum acutatum/simmondsii ND (Polizzi et al. 2011) 2010 Post-emergence Pink ipê Rhizoctonia solani AG-4 5 (Polizzi et al. 2010) 2009 Post-emergence Fan palm Rhizoctonia solani AG-4 20 (Polizzi et al. 2009) 2007 Post-emergence African daisy Rhizoctonia solani AG-4 30 (Aiello et al. 2008a) 2008 Post-emergence Lagunaria patersonii Rhizoctonia solani AG-4 20 (Aiello et al. 2008b) Netherlands 2005 Post-emergence Fennel Alternaria petroselini 6–10 (Pryor and Asma 2007) Spain 2011 Post-emergence Swiss chard Rhizoctonia solani 20 (Palmero et al. 2012) 2009 Post-emergence Pinus radiata Cylindrocarpon pauciseptatum ND (Agustí-Brisach et al. 2011) North/Central America Canada 2005 Post-emergence Durum wheat Arthrinium sacchari ND (Mavragani et al. 2007) Mexico 2014 Post-emergence Habanero pepper Phytophthora capsici ND (Sánchez-Borges et al. 2015) USA 2003 Post-emergence Canola Rhizoctonia solani AG 2–1 ND (Paulitz et al. 2006) 2007–2009 Post-emergence Soybean Fusarium commune ND (Ellis et al. 2012) 2011 Post-emergence Indian spinach Rhizoctonia solani 10 (Liao et al. 2011) 2009 Post-emergence Pea Pythium spp. ND (Alcala et al. 2016) 1994 Post-emergence Wild rice Pythium torulosum ND (Marcum and Davis 2006) South America Brazil 2014 Post-emergence Casuarina equisetifolia Fusarium lacertarum 80 (Poletto et al. 2015) Brazil 2008–2011 Pre-emergence Rice Bipolaris oryzae ND (Schwanck et al. 2015) Oceania Australia 1998–1999 Post-emergence Carrot Alternaria radicina 47 (Coles and Wicks 2003) Agron. Sustain. Dev. (2017) 37: 10 Agron. Sustain. Dev. (2017) 37: 10 Page 5 of 25 10 Fig. 2 An overview of soybean a (a) and pea (b) fields affected by damping-off diseases due to Pythium spp. The presence of empty space along the row indicates seed or seedlings affected by pre- and post- emergence damping-off diseases which killed plants. The economic losses in such a situation are severe owing to a direct cost due to damages of seed or seedlings and an indirect cost related to an additional cost of replanting and the consequent lower yields due to the later planting dates (Fig. 1A is photo courtesy of Martin Chilvers while b Fig. 1B is photo courtesy of Lindsey J. du Toit) 2.1 Pre-emergence symptoms to non-uniform seeding of containers or beds, poor seed de- velopment, and seed rot and decay (Landis 2013). They occur when seeds decay prior to emergence. This can occur (i) before seed germination, or when (ii) the germinating seeds are killed by biotic stresses while shoot tissues are still below ground (Fig. 3; Filer and Peterson 1975; Crous 2002; Horst 2013). In the first case, seeds become soft, rotten, and fail to germinate. In the second case, stems of germinating seeds are affected with characteristic water-soaked lesions formed at or below the soil line (Cram 2003; Landis 2013). With the progression of the disease, these lesions may darken to reddish-brown, brown, or black. Expanding lesions quickly girdle young and tender stems. Seedlings may wilt and die soon before emergence. In general, random pockets of poor seedling emergence are an indication of pre-emergence damping-off. Abiotic stresses can be divided into two categories: chem- ical and physical stress. The first notably involves limiting (i) concentrations in carbon dioxide or ethylene (Negm and Smith 1978), (ii) potential of hydrogen (Foy 1984), (iii) os- Fig. 3 Characteristic symptoms of pre-emergence damping-off of pea motic potential (Romo and Haferkamp 1987), and (iv) phyto- (Pisum sativum L.) caused by Pythium spp. Despite the same sowing date, only the first three seeds on the left have emerged. Note non- toxicity (Wang et al. 2001). The second includes (i) extreme emerged seeds with or without root development. Soft, rotten, and temperatures (high or low) (Khan 1977; Wen 2015), extreme decayed seeds prior to germinating or the germinating seeds killed by seedbed humidity (high or low) (Maraghni et al. 2010; Wen biotic stresses while shoot tissues are still below ground are 2015) and (iii) mechanical stresses such as seedbed clods characteristic symptoms of pre-emergence damping-off. The sixth seed from the left had germinated but the stem of germinating seeds was (Dürr and Aubertot 2000), or crusting at the soil surface affected by the disease with characteristic water-soaked lesions below (Aubertot et al. 2002). Other mechanical events, such as re- the soil line. This led to wilting of the seedling soon after emergence moval of mulch or soil by wind and rain, may also contribute (Photo courtesy of Lindsey J. du Toit) 10 Page 6 of 25 Agron. Sustain. Dev. (2017) 37: 10 Fig. 4 Characteristic symptoms of post-emergence damping-off of death of seedlings in groups (a and b). The presence of an empty space soybean (a and b) and corn (c and d). The succulent tissue of sprouts along the row between corn seedlings indicates the lack of emerged with aboveground shoots collapsed, leading to wilting of some seedling seedlings due to damping-off disease (c and d). (Photo courtesy of populations. Soybean seedlings with stem lesions at ground level and the Martin Chilvers) Because biotic and abiotic stresses interact among them, it because the damage owing to heat lesions is generally is important to distinguish which of them are associated with scattered throughout nurseries/seedbeds, which mainly de- the disease symptoms. pend on patterns of shade and heat buildup (Hartley 1921), while that caused by biotic stresses often occurs in expanding patches. Soil crusting is another important abiotic stress that 2.2 Post-emergence symptoms often hinders seedling emergence or leads to stunted seedling growth (Fig. 5). Phytotoxicity caused by chemical fungicides Post-emergence damping-off symptoms occur when seedlings is another abiotic stress. The symptoms of phytotoxicity, how- decay, wilt, and die after emergence (Fig. 4; Boyce 1961; ever, may vary based on the type of chemical used including Horst 2013). In most cases, all symptoms result in the collapse marginal necrosis, chlorotic patches or spots, and malformed and death of at least some seedlings in any given seedling flowers, buds, and young leaves (Dole and Wilkins 2004). For population. In the case of soil-borne pathogen, there could example, fungicides based with benzimidazole can cause re- be the death of seedlings in groups in roughly circular patches duced plant growth and visual damage in bedding plants and the seedlings may have stem lesions at ground level. (Iersel and Bugbee 1996). Seedling stems can become thin and tough (commonly known as “wirestem”), which often leads to reduced seedling vigor. These symptoms can be also accompanied by leaf spotting 2.3 Occurrence of damping-off symptoms and a complete root rot may occur. Overall, the symptoms on the stem of the seedlings include water-soaked, sunken Most damping-off diseases present a single sort of symptom lesion at or slightly below the ground level and sometime also (pre- or post-emergence). However, both sorts of symptoms below ground line (i.e., on the roots), causing the plant to fall are also reported to some extent (Table 1) although the under- over (Wright 1944; Filer and Peterson 1975). Surviving plants lying factors leading to the occurrence of each sort of symp- are stunted, and affected areas often show uneven growth. tom are poorly discussed in the literature. The complexity of Abiotic stresses, such as superficial soil heat, can also lead damping-off symptoms result from interactions between to post-emergence seedling symptoms such as whitish lesions, cropping practices and the production situation (Aubertot which are often located only on one side of the stem in the and Robin 2013). This may explain the relevant lack of infor- early growth stage of seedlings (Hartley 1918). Such symp- mation. This complexity involves synergism among damping- toms can be distinguished from those caused by biotic stresses off pathogens (Al-Hazmi and Al-Nadary 2015), variation of Agron. Sustain. Dev. (2017) 37: 10 Page 7 of 25 10 Fig. 5 Lack of sugar beet (Beta vulgaris L.) seedlings emergence due to such a field is characteristic of abiotic stresses including stunted growth of soil crusting followed by drought. The formation of soil crusts on the soil seedlings without any necrosis of leaves or stems. (Photo courtesy of surface represents a strong mechanical barrier which impedes seedlings Carolyne Dürr) from being emerged. Overall, lack of seed germination and emergence in symptoms according to environmental conduciveness occurrence. To this aim, the list of damping-off diseases we (Schwanck et al. 2015), direct effect of plant density provide in Table 1 constitutes a potential starting point. (Burdon and Chilvers 1975), and many other factors, which are very specific for each damping-off symptom. For instance, the disease cycle components of damping-off are seldom 3 Integrated management of damping-off discussed in a broader sense in the literature, by comparing different diseases. Some factors related to the time/moment of An effective management of damping-off requires the deploy- disease occurrence and timing of disease cycle components ment of a number of strategies, which can be classified into the could determine whether pre- or post-emergence symptoms following four major groups: (i) seed treatment to enhance will occur. In this sense, it is possible that for both pre- and germination and seedling vigor, (ii) deployment of resistant post-emergence damping-off, the infection occurs during seed or tolerant cultivars to damping-off diseases, (iii) adoption of germination but a longer or shorter incubation period may best cropping practices, and (iv) timely treatment interven- implicate in pre- or post-emergence damping-off. In addition, tions of seedlings with effective products (conventional pesti- the effect of individual factors involved on the disease pro- cides as well as biopesticides and/or biocontrol agents). None cesses from the disease cycle and the host cycle (e.g., seed of these strategies is effective in managing damping-off dis- germination), for damping-off symptom development, is rare- ease when applied individually and thus it requires that all of ly discussed in the literature. Taken together, several studies them are combined within the frame of IPM. virtually explore the effect of a given factor (e.g., temperature) on damping-off diseases intensity (Ben-Yephet and Nelson 3.1 Seed treatment to enhance germination and seedling 1999), without specifying whether the factor plays a specific vigor role on the pathogen (e.g., organism metabolism) or on the host (e.g., slow germination process increases time exposure While the use of completely healthy seeds is the most effective underground). Further knowledge on disease cycle features means to prevent and/or contain damping-off diseases, seeds and processes would help better understand damping-off might not be always free from pathogens and thus would symptom occurrence. Although it was out of the focus of this benefit from treatments. Even when there is no risk of con- work, it is worth to mention that from the extensive literature taminated seeds from seed-borne pathogens, seed treatments review, we did not perceive any pattern on the sort of can be an effective means to increase seedling emergence, damping-off symptom (pre- or post-) according to the region, particularly when done on seeds of low vigor and when the the pathogen genus, or crop species affected. Therefore, a seed coat has been damaged (Mancini and Romanazzi 2014). meta-analytical approach to test hypotheses associated with Chemical seed treatments still represent a major practice in damping-off diseases would be highly valuable to better ex- agriculture to manage damping-off diseases (Rhodes and plain the factors involved in damping-off symptoms Myers 1989; Babadoost and Islam 2003; Howell 2007; 10 Page 8 of 25 Agron. Sustain. Dev. (2017) 37: 10 Table 2 Examples of literature reports highlighting the efficacy of non-chemical seed treatments to suppress damping-off diseases. The tested formulations are most often reported to suppress both pre- and post-emergence damping-off although their effectiveness may vary in terms of disease suppressiveness Crop Pathogen Formulation/product Reference Alfalfa Pythium spp. Mineral seed coating (Samac et al. 2014) Canola Pythium spp. Rhizosphere bacteria (Bardin et al. 2003) Corn Pythium and Fusarium spp Several biocontrol agents (Mao et al. 1997; Mao et al. 1998) Cotton Pythium spp. Enterobacter cloacae and (Nelson 1988) Erwinia herbicola Cotton Pythium spp., Rhizopus oryzae Trichoderma spp. (Howell 2007) Cucumber Pythium ultimum Ethanol extracts of Serratia (Roberts et al. 2016) marcescens and Trichoderma spp. Cucumber Pythium spp. Phosphonate (Abbasi and Lazarovits 2005; Abbasi and Lazarovits 2006) Sunflower Rhizoctonia solani Spermine (El-Metwally and Sakr 2010) Lentil, pea, Pythium spp. Rhizobium leguminosarum (Bardin et al. 2004b; Huang and Erickson 2007) sugar beet Pea Pythium spp. Rhizosphere bacteria (Bardin et al. 2003) Safflower Pythium spp. Rhizosphere bacteria (Bardin et al. 2003) Sesame Soil-borne pathogens Paenibacillus polymyxa (Ryu et al. 2006) Sugar beet Pythium spp. Rhizosphere bacteria, crop straw powders (Bardin et al. 2003; Bardin et al. 2004a) Tomato and hot pepper Pythium spp. Fluorescent Pseudomonads (Ramamoorthy et al. 2002) Bradley 2007; Leisso et al. 2009; Dorrance et al. 2009; 3.2 Deployment of host-plant resistance and/or tolerance Rothrock et al. 2012; Kandel et al. 2016). Several chemicals including bleach, hydrogen peroxide, ethanol, and fungicides Overall, host-plant resistance as a management tactic is com- can be applied to remove pathogen inoculum from seed coats posed of the following two strategies: (i) deployment of resis- (Dumroese and James 2005; Mancini and Romanazzi 2014). tant and/or tolerant plant varieties, which support lower path- Generally, chemical treatments are effective but they can also ogen populations or better tolerate injury caused by them; and negatively affect seed germination and cause phytotoxicity (ii) the integration of such varieties with other management (Axelrood et al. 1995; du Toit 2004) besides negative impacts tactics within the frame of IPM. Unfortunately, for many plant to human health and the environment (Lamichhane et al. pathogens, including those causing damping-off diseases, no 2016). In addition to chemical treatments, physical seed treat- plant cultivar with measurable resistance is available ment can be applied including hot water, hot air, and electron (Babadoost and Islam 2003). Therefore, the only way to better treatments (Mancini and Romanazzi 2014). Finally, a number use the available crop varieties with tolerance to pathogens is of biological seed treatment methods are being developed and through their adequate integration with other disease manage- used in recent years with a satisfactory level of damping-off ment measures. Nevertheless, insufficient focus has been paid disease suppression (Table 2). to date to the integration of plant resistance with other IPM Because seed germination and emergence are often tactics, and to quantifying the benefits of plant resistance in influenced by site-specific soil and climate conditions, multi-tactic IPM programs (Stout and Davis 2009). an in-depth knowledge of a specific site in question is a On the other hand, the breeding approach used to date to prerequisite for an effective decision-making process for develop resistant and/or tolerant crop varieties should be seed treatments. An experiment on pesticide-free revisited if we want to focus on sustainable crop protection agroecosystems conducted in 2014 across eight experi- based on IPM. This is particularly true taking into account the mental sites in France, with non-treated seeds, showed fact that most, if not all, crop varieties bred to date are based that the percentage of emergence rates markedly differs on a market-driven approach focused on high-yielding and for the same seeds across the sites (Fig. 3). In particu- most profitable crop varieties. This trend has boosted adoption lar, while the rate of emergence of soft wheat was of short rotations or monoculture practices, on one hand, and 100% in the Le Rheu and Grignon sites, it was lower ignored the potential that minor crops may have for IPM, on across other sites ranging from 43% in Auzeville to the other (Messéan et al. 2016). The limited range of available 75% in Lusignan (Fig. 6). This means that while seed minor crop varieties has been reported as one of the major treatments may result essential across some sites, due to obstacles to crop diversification, thereby confining certain unfavorable soil and climatic conditions, which are con- beneficial practices such as multiple cropping or intercropping ducive to disease development, it may not be the case (Enjalbert et al. 2016; Messéan et al. 2016). Therefore, breed- in other areas. ing for IPM should be based on a different approach than the Agron. Sustain. Dev. (2017) 37: 10 Page 9 of 25 10 irrigation, growing environment, crop sequence and intercropping, cover crops, soil residue management, soil solarization, and tillage (Table 3). Therefore, understand- ing combined effects of abiotic and biotic stresses and factors influencing them are a prerequisite towards effec- tive IPM strategies of damping-off. Once these critical factors have been identified, which might differ from one region to another, best cropping practices should be put in place and adopted. One of the most important practices that allow to the best management of damping-off and root diseases is fer- tilization. Adequate availability of nutrients in the soil can ensure higher vigor, with earlier emergence that limit the period of time where pathogens can infect seeds and seed- lings during the autotrophic stage. In particular, the ad- vantages of fertilizer placement on seed germination and seedling emergence have been previously demonstrated (Cook et al. 2000). The placement of fertilizers, directly under or slightly to one side of the seed, at the time of Fig. 6 Percentage of seed emergence (non-treated seeds) observed across planting or sowing results in an increased level of seed different experimental sites managed under the “Res0Pest” network in germination and emergence (Fig. 7). This is because rel- France in 2014. Res0Pest is a “pesticide-free” trial network launched in 2011 by the INRA/CIRAD IPM network to address objectives of the atively immobile nutrients, such as phosphorus, are not French National Action Plan Ecophyto to develop and demonstrate the readily available for plants especially for those species feasibility of pesticide-free cropping systems (Deytieux et al. 2014). Eight having no or a few lateral roots. Therefore, field fertiliza- experimental sites, comprised of five arable cropping systems (in brown) tion, where damping-off diseases are important, requires and three mixed crop/husbandry systems (in green) are ongoing across the sites. DW durum wheat, SW soft wheat, MSW mixed of soft wheat that the nutrients be made easily accessible to the roots to varieties, SB spring barley. Different percentages of emergence across the increase growth rate. Although these nutrients do not al- experimental sites highlight how soil and climate and cropping practices ways reduce seedling infection, they often enhance seed affect seed germination and the seedling emergence process through germination and seedling vigor (Smiley et al. 1990; biotic and abiotic stress. Low percentages of emerged seedlings are highlighted in red Patterson et al. 1998). Indeed, higher seedling vigor al- lows seedlings to rapidly escape from the soil surface even in the presence of a high soil population density of the pathogen(s). traditional one given the strategic role of breeding in the com- petitiveness of crops and their adaptation to more diversified 3.4 Timely treatment interventions of seedlings cropping systems (Enjalbert et al. 2016). with effective products The strategies described above are mainly of preventive nature 3.3 Adoption of best cropping practices as they can be developed and adopted before the occurrence of damping-off diseases. Once the infection occurs on seedlings Once the causal agent of damping-off has been identified, and there is a high risk of epidemic development, growers all available cropping practices could be adapted to dis- have to attempt for an effective control of the disease. courage the development of the pathogen. Indeed, any Overall, there are two key measures available for damping- technique that allows to reduce the time between seed off control as described below. germination and emergence helps reduce effects of biotic stresses on seedlings. Overall, many pathogens involved 3.4.1 Biological control in damping-off are relatively weak pathogens, which re- quire favorable environmental conditions for infection to Because of their adverse effects on human health and the occur (Table 1). In addition to the susceptibility of host environment, the use of conventional pesticides, including and aggressiveness of pathogen populations, the severity fungicides, has come under increasing public scrutiny in of damping-off is highly dependent on some critical fac- many countries especially in the European Union tors including seedbed preparation, soil pH management, (Bourguet and Guillemaud 2016; Lamichhane et al. seeding date and rate, growing density, nutrition, 2016). In addition, increasing reports of pest resistance 10 Page 10 of 25 Agron. Sustain. Dev. (2017) 37: 10 Table 3 Critical factors affecting damping-off and best cropping practices which help discourage its development Critical factors Best cropping practices References Seed quality Use of clean, healthy, and sterile seeds, treatments with (Mao et al. 1998; Babadoost and Islam 2003; Jensen non-chemical products including beneficial microbes to et al. 2004; Abbasi and Lazarovits 2006; Howell enhance seed health and resilience and to promote rapid 2007; Gwinn et al. 2010; Mastouri et al. 2010; germination and emergence and control pre-emergence Samac et al. 2014; Roberts et al. 2016) damping-off, and chemical treatment to control post-emergence damping-off Seedbed preparation Utilize pest-free soil or growing medium through incorporation of (Kassaby 1985; Ben-Yephet and Nelson 1999; Dürr and compost, plant residues, or microbial amendments into soil or Aubertot 2000; Diab et al. 2003; Deadman et al. growing medium which suppress soil-borne pathogens, 2006; Njoroge et al. 2008; Pane et al. 2011; He et al. perform soil solarization, bio-fumigation, adopt mixture of 2011; Landis 2013; Bahramisharif et al. 2013a; particle sizes and good porosity to avoid soil crusting, improve Vitale et al. 2013) soil drainage by subsoiling, crowning the beds, installing drainage tiles, and incorporating composted organic matter to improve soil texture, water-holding capacity, nutrient availability, and cation exchange capacity Adjustment of soil pH Use relatively acidic soils with a low pH (4.5–6.0), increase soil (Russell 1990; Davey 1996; Cram 2003) pH with organic amendments, with applications of aluminum sulfate, sulfur, or acid peat Seeding date Perform sowing neither too early nor too late, avoid warm or wet (Hwang et al. 2000; Cram 2003) weather for sowing, well irrigate soils to the depth of the growing roots without flooding the soil Growing density Avoid over-sowing or excessive plant densities, use crop varieties (Burdon and Chilvers 1975; Neher et al. 1987; Landis with asynchronous germination 2013) Nutrition Apply well-balanced fertilization especially microelements (Gladstone and Moorman 1989; James 1997; (phosphorus, potassium, and calcium) El-Metwally and Sakr 2010; Landis 2013) Growing environment Maintain moderate humidity, escape application of high water (Beech 1949; Duniway 1983b; Wong et al. 1984; volume to avoid waterlogging and adopt frequent and light Yitbarek et al. 1988; Hwang et al. 2000; Schmidt applications, maintain adequate light and optimal temperatures et al. 2004; Kiyumi 2009; Landis 2013; Li et al. 2014) Crop sequence and Avoid monoculture and adopt long rotation schemes to lower (Hwang et al. 2008; Abdel-Monaim and Abo-Elyousr intercropping down pathogen populations, introduce Brassica crops as their 2012) root exudates contain soil-borne pathogen populations Cover crops and soil residue While cover crops are overall useful to produce organic matters (Hansen et al. 1990; Russell 1990; Davey 1996; Bailey management and protect the soil from erosion and leaching, their benefit can and Lazarovits 2003) vary with the type of species selected. Certain leguminous cover crops even favor greater populations of damping-off pathogens than graminaceous plants Tillage Perform tillage to incorporate plant residues into the soil to reduce (Tachibana 1983; Workneh et al. 1998; Bailey and soil-borne pathogen populations although the effect of tillage Lazarovits 2003) may differ from the type of pathogen to be managed development to pesticides have become an issue, thereby products to control damping-off worldwide and most of increasing risks of pest management failure with potential them are based on antagonist fungi, including threats of economic losses for farmers (Onstad 2013; Trichoderma spp. and Gliocladium spp. or bacteria such Bourguet and Guillemaud 2016; Lamichhane et al. as Pseudomonas spp. and Bacillus spp. (Table 5). 2016). Chemical fungicides can also cause phytotoxicity However, not all of them are registered and marketed on crops and foliage plants, which is another drawback of as biocontrol agents nor they are used as plant growth their use (Dias 2012). promoters, plant strengtheners (or biostimulants), or soil The application of biocontrol agents/formulations is conditioners (Paulitz and Bélanger 2001). Numerous an important substitute to conventional fungicides, with studies conducted on biocontrol research in the last lower negative impacts. Often, biocontrol is widely 15 years clearly suggest the increasing concern of the practiced as an alternative disease management strategy scientific community to generate knowledge on an alter- to conventional fungicides especially when the latter are native to chemical solutions (Table 5). Most of these not effective or cause secondary problems such as seed studies have also demonstrated a good effectiveness of phytotoxicity from fungicides (Burns and Benson 2000). biocontrol products in managing the disease. Individual beneficial organisms used as biocontrol Accordingly, the biocontrol industry has become very agents can prevent damping-off pathogens through five dynamic in recent years especially in terms of using mechanisms (Table 4). There are dozens of biocontrol the available scientific knowledge to develop and Agron. Sustain. Dev. (2017) 37: 10 Page 11 of 25 10 Fig. 7 Effect of fertilizer placement on germination and emergence of emergence (the middle of the plot). The same field practices were oilseed rape. While the placement of micronutrients (zinc and applied in the field, including the same date of sowing and cultivar. In phosphorous) at the time of sowing allowed seeds to readily germinate addition to oilseed rape, the cultivated field presents annual weed Poa and emerge (the three lateral sides of the plot), the lack of nutrient annua and Vulpia myuros (light green color). (Photo courtesy of Jean- placement has resulted in markedly reduced seed germination and Pierre Sarthou) commercialize formulations. However, most of these for the management of damping-off, particularly for post- formulations are based on individual biocontrol agents emergence ones. This trend is clear also in the literature where and they specifically target a specific pathogen. most recent research efforts are on the development of biocon- trol solutions rather than focusing on the chemical ones 3.4.2 Chemical control (Tables 2 and 5). This happens due to the general concerns with regards to conventional pesticides, but also because pri- While alternative tactics to chemical control are the priority vate and public sectors can design new solutions for the so- for IPM to manage damping-off diseases, such measures called “biocontrol market.” However, even with biocontrol available on the market are not always effective in controlling solutions, diagnosis of the involved pathogens along with damping-off diseases and/or their effectiveness is variable. the analysis of treatment opportunity is still required. Therefore, a judicious use of fungicides maybe needed to combine with other IPM tactics especially when the disease infection has already occurred (Harman 2000). 4 Key challenges and future priorities Chemical control of damping-off as foliar application, for damping-off management however, is restricted to a few active ingredients due to the high cost of fungicides and the small number of products In order to tackle the complex and multifaceted nature of registered for some crops including those for ornamental use damping-off diseases and a range of factors that affect their (Garzón et al. 2011). Among the most frequently used fungi- occurrence and development, we propose five research prior- cides, there are etridiazole and metalaxyl, active against ities, which are essential towards a better understanding and Phytopthora and Pythium spp.; benomyl and thiophanate management of damping-off diseases. methyl, active against Fusarium and Rhizoctonia spp.; mancozeb and maneb, active against Fusarium and 4.1 Correct identification of damping-off pathogens Phythium spp.; and captan, active against common including non-secondary colonizers and anastomosis damping-off pathogens. A rapid decrease in market availabil- groups ity of many previously available fungicides further limits ac- cess to chemical treatments in many countries especially in the An accurate identification of the causal agent(s) associated European Union (Lamichhane et al. 2016). On the other hand, with damping-off is imperative for understanding the etiology resistance to commonly used fungicides developed by several of damping-off outbreaks and thus represents a cornerstone strains of pathogens has challenged the long-term sustainabil- for the decision-making process to IPM. This involves ity of chemical control (Taylor et al. 2002; Allain-Boulé et al. confirming the pest, learning how it spreads, and then identi- 2004; Moorman and Kim 2004; Reeleder et al. 2007; Weiland fying critical points for its management, including develop- et al. 2014). All these new scenarios clearly highlight that non- ment of preventive measures based on adapted cropping prac- chemical measures will be increasingly developed and used tices. Most often, the specific pathogen causing damping-off 10 Page 12 of 25 Agron. Sustain. Dev. (2017) 37: 10 Table 4 Key mechanisms involved in biocontrol activities and list of selected references Mechanism Description References Antibiosis A biocontrol microorganism produces antibiotics which is toxic to one or (Shang et al. 1999; Wright et al. 2001; Koumoutsi et al. 2004; more pathogens Kloepper et al. 2004; Islam et al. 2005; Leclere et al. 2005; Pal and McSpadden 2006; Gerbore et al. 2014) Parasitism A biocontrol organism parasitizes one or more pathogens. This is a typical (Benhamou and Chet 1997; Kiss 2003; Milgroom and Cortesi example of Trichoderma spp. which winds around the hyphae of 2004; Pal and McSpadden 2006; Gerbore et al. 2014) soil-borne fungi and oomycetes by puncturing their cell wall Competition for nutrients A biocontrol organism produces and releases many substances that have (van Dijk and Nelson 2000; Kageyama and Nelson 2003; Pal suppressive effects towards pathogens. This help a biocontrol agent to and McSpadden 2006; Liu et al. 2013; Gerbore et al. 2014) effectively colonize plant environments Production of lytic enzymes or other A biocontrol organism produces metabolites that can interfere with (Bull et al. 2002; Kilic-Ekici and Yuen 2003; Benhamou 2004; chemical signals pathogen growth and/or activities via degradation of essential Palumbo et al. 2005; de los Santos-Villalobos et al. 2013; compounds needed for soil-borne pathogens to develop and start the Gerbore et al. 2014) infection process Induced systemic resistance (ISR) A beneficial organism stimulates the plant’s immune system thereby (Chen et al. 2000; Hammond-Kosack and Jones 2000; protecting plants from pathogens. ISR is a different mechanism from Bargabus et al. 2002; Bargabus et al. 2004; Ongena et al. systemic acquired resistance (SAR). The latter occurs following an 2004; Kloepper et al. 2004; Meziane et al. 2005; Pal and exposition of a plant to a low level of a specific pathogen which allows McSpadden 2006; Gerbore et al. 2014; Pieterse et al. 2014) plants to acquire resistance to that specific pathogen in the future cannot be determined based on the visual inspections of symp- present within a sample (Zinger et al. 2012; James 2012b; Bik toms. Therefore, their correct identification is essential. It is et al. 2016). Culture-independent methods, such as next gen- generally performed using both culture-based and culture- eration sequencing, on the other hand, allow to identify the independent methods. However, both of these techniques overall species diversity present in a given sample but their have their advantages and drawbacks and hence are comple- limit is that they do not allow to determine the virulence and mentary to each other. For example, culture-based techniques fungicide resistance of the microbes associated with the dis- allow for the characterization of important traits such as viru- ease (Lamichhane and Venturi 2015). lence or fungicide resistance. Not only are they time consum- Although many modern PCR techniques allow a rapid de- ing, but they also underestimate the true diversity of species tection and identification of one or more specific pathogens, Table 5 List of selected studies reporting the use of microbial antagonists for biological control of major damping-off pathogens worldwide since 2001. These biological control agents were either applied to seedlings or to soil to achieve disease suppression Pathogen(s) Host Biological control agent(s) References Pythium spp. Tomato Different bacteria (Gravel et al. 2005) Pythium aphanidermatum Cucumber Paenibacillus spp. with organic compounds; (Punja and Yip 2003; Li et al. 2011) Streptomyces griseoviridis, Trichoderma spp., Gliocladium catenulatum Pythium aphanidermatum Tomato Trichoderma harzianumstrain (Jayaraj et al. 2006) Pythium ultimum Cucumber Different bacterial and fungal isolates (Georgakopoulos et al. 2002; Carisse et al. 2003) Pythium ultimum and Bedding plants Gliocladium catenulatum (Mcquilken et al. 2001) Rhizoctonia solani Rhizoctonia spp. Chinese mustard Endomycorrhizal Rhizoctonia (Jiang et al. 2015) Rhizoctonia solani Cucumber Bacillus pumilus SQR-N43; Glomus mosseae and (Jung et al. 2003; Chandanie et al. plant growth-promoting fungi; Paenibacillus 2009; Huang et al. 2012) illinoisensis Rhizoctonia solani Pepper Fluorescent pseudomonads with resistance inducers (Rajkumar et al. 2008) Rhizoctonia solani Radish Peony root bark with Trichoderma harzianum (Lee et al. 2008) Rhizoctonia solani Tomato Streptomyces (Sabaratnam and Traquair 2002) Rhizoctonia solani Different crops Trichoderma spp. (Lewis and Lumsden 2001) Rhizoctonia solani and Tomato Olive mill waste water and its indigenous bacteria (Yangui et al. 2008) Fusarium solani Rhizoctonia spp. Cotton Nonpathogenic Binucleate Rhizoctonia spp. (Jabaji-Hare and Neate 2005) Several soil-borne pathogens Cucumber Several antagonist bacteria (Roberts et al. 2005) Agron. Sustain. Dev. (2017) 37: 10 Page 13 of 25 10 including those reported to cause damping-off diseases independent methods may often lead to inconsistencies in di- (Weiland and Sundsbak 2000; Lievens et al. 2006; Ishiguro versity estimates of Pythium species associated with damping- et al. 2013), the timely identification of the overall species off diseases. Nevertheless, culture-based techniques are the diversity involved in the disease occurrence process still only means to demonstrate, for example, the presence of po- remains a challenge. In addition, such techniques re- tential pathogens even in fields with no previous history of quire DNA purification, the availability of more expen- damping-off diseases. Indeed, based on culture-based tech- sive and sophisticated equipment, and more highly niques, several studies have isolated Pythium species from trained technical personnel to perform the test symptomatic and asymptomatic plants and demonstrated their (Schroeder et al. 2012), which is a strong limit to their pathogenicity on a large number of plant species wider adoption. Therefore, we still need to develop (Bahramisharif et al. 2013b; Coffua et al. 2016). Further, techniques, which could simplify the detection, on one culture-based methods and morphological observations may still hand, and be economically sustainable, on the other. result essential in confirming the presence of novel or unexpected All four soil-borne pathogens dealt in this paper are char- species within a sampling location and thus have to be consid- acterized by a complex of genetically distinct species, with a ered for identification purposes (Zitnick-Anderson and Nelson wide host range or virulence preference for certain hosts. For 2014). example, Rhizoctonia solani species Kühn (teleomorph: The complexity in terms of taxonomy is even more accen- Thanatephorus cucumeris; A. B. Frank; Donk) is a multinu- tuated for the genus Phytophthora with many studies over cleate species that has been divided into 14 anastomosis recent years recognizing different Phytophthora as a species groups (AGs; AG1 to AG13 and AG B1; (Sneh et al. 1991; complex. Often, the taxonomic status of the related species is Carling and Summer 1992; Carling et al. 2002). Binucleate also a matter of controversy or the presence of several distinct Rhizoctonia spp. (teleomorph: Ceratobasidium) are divided lineages perhaps representing as yet undescribed species into 19 AGs (AG A to AG S). Finally, R. oryzae and R. zeae (Safaiefarahani et al. 2015). Many new species of are multinucleate with the teleomorphs Waitea circinata var. Phytophthora are constantly proposed and the taxonomy of circinata and W. circinata var. zeae, respectively (Sneh et al. this genus has been evolving very dynamically (Henricot et al. 1991). Given its variable nature within- and between-AG var- 2014). Consequently, development of rapid and reliable diag- iation in virulence and host range, a correct and timely iden- nostic methods is a challenging task for this genus too. tification of the specific genetic lines associated with Because most damping-off pathogens are either soil- damping-off diseases is still a challenge, which calls for fur- or water-borne, instead of airborne, adoption of good ther research efforts. phytosanitary practices generally allows to manage Fusarium spp. are characterized by a wide genetic diversity damping-off diseases. This is especially the case if a and their taxonomy has been afflicted by changing species proper detection of the causal agent(s) is timely made. concepts, with as few as 9 to over 1000 species being recog- This helps understand also critical management points nized by different taxonomists during the past 100 years that allow pathogens to enter into the field and/or nurs- (Summerell et al. 2003). Indeed, the complexity and the rec- ery. The mode of transmission maybe different for each ognized difficulty of rapidly identifying cultures to species pathogen although spread in infected soil or growing have been reported as the major reason hindering effective medium is common to all species (Table 6). Because disease management (Summerell et al. 2003). The challenge most of these pathogens are common in agricultural within the Fusarium species complex is also to determine the soils, they can be spread via contaminated soil, introduc- specific role of secondary colonizers in occurrence and devel- tion of infected plants (mainly in case of seed-borne opment of damping-off diseases since they are characterized pathogens), improperly sanitized equipment and green- by a high variability and complexity in terms of host range and house, and the use of contaminated irrigation water virulence. (Zappia et al. 2014). In particular, Pythium spp. and Similar problems exist also for Pythium species with most Phytophthora spp. have motile zoospores, which are plant-pathogenic lines having a wide host range. For example, most commonly spread by water leading to epidemic Pythium ultimum is reported to attack over 719 host plants developments (Hong and Moorman 2005; Zappia et al. (Farr and Rossman 2012). Other species such as Pythium 2014). Therefore, the potential presence of these patho- graminicola and Pythium arrhenomanes are restricted only gens in irrigation water should be timely determined to Poaceae family (Schroeder et al. 2012). Traditional baiting using appropriate bioassays such as in-situ baiting or other culture-based techniques are still widely used for the (Ghimire et al. 2009) or PCR techniques (Martin et al. identification of Pythium species although culture- 2012; Schroeder et al. 2012). Appropriate treatments of independent methods, such as cytochrome oxidase subunit 1 the water should be implemented if their presence is pyrosequencing, are also used (Coffua et al. 2016). The chal- confirmed in irrigation water. Detection and management lenge is that methodological biases inherent to culture- approaches of plant pathogens in irrigation water have 10 Page 14 of 25 Agron. Sustain. Dev. (2017) 37: 10 Table 6 Mode of transmission of major causal agents of damping-off and soild and climate conditions favorable to their development. Any IPM approach should consist in the adoption of cropping practices, including cultivar choice and chemical control which could discourage factors favoring damping-off Pathogen Mode of transmission Optimal pedo-climatic conditions for damping-off References Pythium spp. Irrigation water, soil High soil moisture, pH >5.8, the effect of temperature (Roth and Riker 1943; Leach 1947; is variable based on the type of damping-off. While Wright 1957) pre-emergence damping-off may occur at low temperatures (12 °C), the post-emergence one is favored by relatively high temperature (18 to 30 °C) Phytophthora Irrigation water, infected soil Water-saturated soils and higher soil pH levels (Lambert 1936; Duniway 1983b; spp. (