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Ciencia e investigación agraria

versión On-line ISSN 0718-1620

Cienc. Inv. Agr. vol.40 no.2 Santiago mayo 2013

http://dx.doi.org/10.4067/S0718-16202013000200001 

CROP PRODUCTION
LITERATURE REVIEW

 

Fusarium crown rot disease: biology, interactions, management and function as a possible sensor of global climate change

Fusariosis de la corona: biología, interacción, manejo y un posible sensor de cambio climático global

 

Ernesto A. Moya-Elizondo

Departamento de Producción Vegetal, Facultad de Agronomía, Universidad de Concepción, Ave. Vicente Méndez 595, Chillán, Chile.
Corresponding author: emoya@udec.cl


Abstract

E.A. Moya-Elizondo. 2013. Fusarium crown rot disease: biology, interactions, management and function as a possible sensor of global climate change. Cien. Inv. Agr. 40(2):235-252. Wheat crops are commonly affected by the dryland root rot complex (DLRRC) under dry and semiarid conditions. This complex is associated with seedling blight, and rotting of roots, crowns and stems of wheat plants. Several pathogens are associated with this complex, but Fusarium crown rot disease (FCR) is the most common and is of worldwide importance. Increased drought frequency and changes in rainfall regimes associated with global climate change may increase the prevalence of this complex of diseases, especially of FCR, in wheat crop areas. This review discusses the characteristics of the pathogen species involved in DLRRC, the known interactions between the pathogens, and information regarding management strategies. We also discuss the possibility that the activity of FCR pathogens could act as a sensor of global climate change.

Key words: Fusarium crown rot, wheat, climatic change.


Resumen

E.A. Moya-Elizondo. 2013. Fusariosis de la corona: biología, interacción, manejo y un posible sensor de cambio climático global. Cien. Inv. Agr. 40(2):235-252. Bajo condiciones de producción en secano y áreas semiáridas, los cultivos de trigo son comúnmente afectados por el complejo de pudriciones radiculares del secano (DLRRC). Este complejo se asocia con la necrosis de plántulas y pudrición de raíces, coronas y tallos de las plantas de trigo. Varios patógenos están asociados a este complejo, pero la Fusariosis de la corona (FCR) es la enfermedad más comúnmente asociado con DLRRC y tiene importancia en todo el mundo. Incremento en la frecuencia de sequías y los cambios en los regímenes de lluvias asociadas al fenómeno de Cambio Climático Global podría aumentar la prevalencia de este complejo de enfermedades, especialmente de FCR, en las áreas donde se cultiva trigo. Este artículo discute sobre la posible actividad de patógenos asociados con FCR como sensores de este fenómeno global. La presente revisión también analiza las características de las especies de patógenos implicados en esta enfermedad del DLRRC, reporta información sobre la interacción entre los patógenos involucrados, y entrega información sobre las estrategias de manejo de la enfermedad.

Palabras claves: Fusariosis de la corona, trigo, cambio climático.


 

Introduction

The semiarid conditions associated with short or non-existent rotations, and the widespread use of no-till or conservation tillage system practices favor survival of pathogens that cause the dryland root rot complex (DLRRC) in wheat crops. If it is considered that about 32% of the 99 million hectares under wheat cultivation in developing countries experiences varying levels of drought stress (Rajaram et al, 1996), we can expect considerable yield losses caused by the pathogens associated with DLRRC in wheat crops worldwide. Semiarid conditions enhance the expression of the diseases associated with DLRRC because this complex of pathogens reduces the amount of functional root and crown tissue, which is critical under moisture-restricted conditions (Papendick and Cook, 1974; Cook, 1981; Bailey et al, 1989; Burguess et al, 2001; Paulitz et al, 2002). The measurable effects on yield are most apparent when the cereals are subjected to water stress later in the growing season and temperatures are high (Cook, 1981; Paulitz et al, 2002). Moreover, the damage is especially acute when drought occurs during the seedling and post-anthesis growth stages (Smiley et al, 2005a). However, infections by some Fusarium species, such as F. pseudograminearum, can occur in relatively moist soils (Burgess et al, 1981) and in irrigated systems (Paulitz et al, 2010).

Agricultural concerns related to global climate change are associated with the potential threat to the food supply derived from impacts such as changing patterns of rainfall, increasing incidence of extreme weather, and the changing distribution and incidence of diseases and their vectors (Tubiello et al., 2007; Soussana et al., 2010). Nevertheless, modeling studies indicate small beneficial effects on crop yields in temperate regions (resulting from local mean temperature increases of 1-3°C accompanied by CO2 increases and rainfall changes). On the other hand, there is a general agreement among the scientific community that the consequences of global climate change will negatively affect all regions of the world (Soussana et al., 2010), especially subsistence or smallholder farmers, due to the increased likelihood of crop failure (Morton, 2007). Additionally, during the 20th century, the major drought index has increased over a number of regions (Bates et al, 2008), which is expected to increase the frequency of heat stress, droughts, and floods (IPCC, 2007; Beniston et al, 2007). Furthermore, extreme rainfall regimes are expected to increase the duration and severity of soil water stress in temperate areas as intervals between rainfall events increase (Knapp et al., 2008; Soussana et al., 2010). In this context, drought increases and extreme rainfall regime changes associated with climate change may lead to an increase of yield losses, and prevalence of the diseases and pathogens associated with the DLRRC. This provides a basis for further study in this field in order to deepen our knowledge of the biology, interactions and management of the pathogens associated with DLRRC.

The DLRRC is known by a variety of names including dryland foot rot, Fusarium foot rot, crown rot, dryland root rot, and common root rot (Paulitz et al., 2002). The disease complex is dominated by different pathogens in different areas or even by different pathogens during successive growing seasons in individual fields (Paulitz et al., 2002). This article focuses on the diseases associated with pathogens of the genus Fusarium. Fusarium crown rot (FCR) is the generic name used to refer to the disease caused by different pathogen species of the genera Fusarium. FCR is primarily caused by F. culmorum (W. G. Sm.) Sacc., F. pseudograminearum (O'Donnell & T. Aoki; group I) (= Gibberella coronicola), and F. graminearum Schwabe (group II) (= G. zeae (Schwein.) Petch) (Paulitz et al, 2002; Cook, 2010). In some geographical regions, F. avenaceum (Fr.) Sacc., F acuminatum Ellis & Everh., F. equiseti (Corda) Sacc., Microdochium nivale (Fr.) Samuels & Hallett (= F. nivale (Fr.) Sorauer), and several Fusarium spp. have also been included and reported in the crown rot disease complex in wheat, but these species are considered less virulent and more environmentally or geographically restricted than the first three species listed (Cook, 2010). Although many species are associated with the DLRRC, F. pseudograminearum, F. culmorum, and Bipolaris sorokiniana (anamorph of Cochliobolus sativus (S. Ito & Kurib.) Drechsler ex Dastur [1942]), the last pathogen associated with common root rot disease and the spot blotch disease, are considered to be the most virulent and economically important pathogens (Burguess et al, 2001; Paulitz et al, 2002; Smiley et al., 2005a). FCR causes symptoms such as grain yield loss, stand reductions, and rotting of seeds, seedlings, roots, crowns, subcrowns, and lower stem tissues, and is also associated with the white-head or premature death of wheat tillers (Paulitz et al., 2002). Additionally, some species of Fusarium are also able to infect the heads or spikes, causing Fusarium head blight, which is associated with mycotoxin production (Cook, 2010). Fusarium species cause a soilborne disease of seedlings similar to that caused by soilborne pathogens such as B. sorokiniana, Gaeumannomyces graminis var. tritici, the causal agent of take-all, and Rhizoctonia spp. (Paulitz et al., 2002).

FCR disease on wheat is a perennial problem in cereal agro-ecosystems and causes significant losses in different regions worldwide (Burgess et al., 2001; Paulitz et al., 2002), such as the Pacific Northwest (Cook, 1968; Smiley and Patterson, 1996; Smiley et al, 2005a), the Texas Panhandle (Specht and Rush, 1988), Southeastern Idaho (Strausbaugh et al, 2004); the upper coastal plain area of the Mississippi (González and Trevathan, 2000), the wheat "Golden triangle" of Montana (Moya-Elizondo et al, 2011a), the Canadian Prairies (Bailey et al, 1995; Hall and Sutton, 1998; Fernández and Jefferson, 2004; Fernández et al, 2007a-b; Fernández et al, 2009), eastern Australia (Backhouse et al, 2004); South Australia (Fedel-Moen and Harris, 1987), Queensland Australia (Wildermuth, 1986; Wildermuth et al, 1997), the United Kingdom (Pettitt et al, 2003), Turkey (Tunali et al., 2008), northwest Iran (Saremi et al., 2007); Argentina (De Souza, INTA Parana, Entre Ríos, Argentina, personal communication) and Chile (Madariaga, INIA Quilamapu, Chillán, Chile, personal communication). Scherm (2004) suggests that there are continuing problems with the application of models for predicting the effects of climate change on disease, including the lack of data on the geographic distribution of disease, non-linear relationships and thresholds in the relationship between climatic variables and epidemiological responses, and the potential for adaptation by plants and pathogens, which is often ignored in models. Interestingly, recent publications about DLRRC surveys have associated pathogen distributions with georeferenced geographical distribution and environmental data (Tunali et al, 2008; Moya-Elizondo et al, 2011a), and it has been suggested that some environmental and ecological adaptations of some fusaria could be used in the future to assess changes associated with global warming (Moya-Elizondo et al, 2011a). These studies have shown the impact of agroecological zones on the distribution, incidence and prevalence of different Fusarium species, and have also highlighted the importance of conducting continuous surveys that associate pathogen incidence with their spatial distribution and environmental data. In fact, these surveys could be a useful tool to monitor the effects of global climate change.

The effect of DLRRC infections under drought stress can cause yield loss exceeding 50%, along with detrimental effects on grain quality such as light test weight (Tunali et al, 2008). In the Pacific Northwest (PNW), Paulitz et al (2002) determined that 76% of the plants in winter wheat fields can be infested with FCR, with estimated losses of 18% in heavily infected fields and a negative impact of US$76 ha-1. In a recent survey in the PNW, yield losses associated with DLRRC in commercial winter wheat fields were valued at US$219 ha-1 and US$51 ha-1, considering field losses of 35% and 9.5%, respectively (Smiley et al, 2005b). In that survey, the greatest damage estimated for field yield losses caused by F. pseudograminearum was 13% (US$48 ha-1), while plots inoculated with F. pseudograminearum showed a grain yield loss of 61%, which was valued at US$372 ha-1. In Australia, FCR has been identified as the second most economically important disease in wheat. Present costs caused by this disease throughout Australia are AUS $ 56M per year (Brennan and Murray, 1998, cited by Wildermuth et al, 2001). Burgess et al (1981) reported that F. pseudograminearum caused up to a 26% yield reduction in individual wheat fields in subtropical southern Queensland, Australia. In Montana, USA, Moya-Elizondo et al. (2011a) showed that in nine intensively sampled fields, populations of FCR pathogens expressed as DNA copy number of the trichothecene TRI5 gene were associated with losses of 24.6% and 34.9% for the dryland fields, and 21% for the second year of wheat recrop in an irrigated field.

The pathogens involved in the DLRRC may occur singly, but they typically co-exist in the same field and even within individual plants. Dominant species in the complex at a specific location can vary from year to year, indicating a high level of adaptation as members of this pathogen complex respond to changes in temperature, seasonal moisture distribution, the amount of moisture, and edaphic factors (Smiley et al., 2005a-b; Moya-Elizondo et al., 2011a). In this context, it is important to understand the biology involved in the establishment and disease infection of FCR.

Biology of Fusarium crown rot of wheat

Different fungal species of the genus Fusarium are associated with FCR. F. culmorum, Fpseudograminearum, and F. graminearum are epidemiologically the most important species involved (Paulitz et al, 2002; Cook, 2010). F. culmorum is associated with cooler semiarid wheat growing regions, while F. pseudograminearum and F. graminearum are dominant in slightly warmer regions (Cook, 1981). It has been determined that the proportion of crops in which F. pseudograminearum infection occurs is positively correlated with maximum temperature during the summer months (Moya-Elizondo et al, 2011a). Increases in fungal biomass have been documented with elevated levels of CO2 (Melloy et al, 2010), a condition also associated with climate global change. The importance of F. pseudograminearum is increasing to the extent that a 70% of incidence has been reported in a wheat crop field in Henan, China (Li et al, 2012). F. pseudograminearum has also been associated with barley kernels in Tres Arroyos, Buenos Aires, Argentina (Castañares et al, 2012).

Among the other species of fusaria, F. avenaceum, F. acuminatum, F. oxysporum, and F. equiseti are among the most common and widespread fungi isolated from underground tissues of wheat in Canada, but a low number of tillers are infected (Fernández and Jefferson, 2004). However, F. avenaceum, F. acuminatum, F. equiseti, F. oxysporum, and M. nivale are considered to be species of lesser importance in the FCR complex (Cook, 2010; Paulitz et al., 2002; Smiley and Patterson, 1996) because they are considered to be secondary colonizers rather than primary pathogens in semi-arid regions (Burgess et al, 2001). F. avenaceum, F. acuminatum and M. nivale are more pathogenic in areas with wet and cold weather (Pettitt et al., 2003; Hall and Sutton, 1998) and their infection levels are very dependent on weather conditions (Hall and Sutton, 1998). A survey in progress between the Araucania and Los Lagos Regions in the South of Chile has identified primarily F. avenaceum over F. culmorum and F. pseudograminearum in these rainy and cold areas (E. Moya-Elizondo, unpublished data). Almost all species of FCR can cause Fusarium head blight (FHB). However, F. graminearum is the most common cause of head blight and seedling blight in wheat in the USA (Bai and Shaner, 2004; Cook, 2010), while F. culmorum is more common in Europe (Wagacha and Muthomi, 2007). FHB infections occur under wet or humid conditions at anthesis or shortly thereafter (Burrows et al., 2008), while FCR is favored by water stress late in the growth season (Paulitz et al., 2002). All members of the FCR complex produce, under dryland conditions, a chocolate brown discoloration in the first to the third internodes up the stem, which can be observed when the leaf sheaths are stripped back in the base of the tiller. When those culm internodes are open, a pink mycelium is observed inside and its presence can be considered as a diagnostic symptom of FCR (Cook, 1981, 2010).

Description of causal organisms

The Fusarium species described above are most commonly associated with FCR disease and considered "unspecialized" pathogens because they can attack any plant tissue if conditions at the tissue surface are favorable for infection (Paulitz et al., 2002). In general, the anamorph of the different Fusarium species may or may not produce macroconidia, microconidia, chlamydospores, and conidia borne on mono or polyphyalides. The typical color of the mycelium on potato dextrose agar (PDA) plus the morphological structures mentioned above can be used to identify individual species throughout different synoptic keys (Nelson et al, 1983). Identification to the species level requires both practice and experience. Recently, specific primers have been developed to identify several of the Fusarium species (Scott et al., 2003; Aoki and O'Donnell, 1999; Nicholson et al, 1998; Wildermuth et al, 1997), and they can be useful to confirm the pathogen identified with synoptic keys.

The teleomorph Gibberella spp. of the complex develop perithecia in clusters on the surface of plant tissues. Perithecia are globose, 125-265 in diameter, rough-walled, and vary from bluff to dark blue in color (Cook, 2010). Perithecia produce clavate asci of 4-10 μm in width x 50-80 μm in length with six to eight spores. Ascospores are hyaline, ellipsoidal, 3.3-6.5 x 13-17 μm, and one- to three-septate (Cook, 2010). The contrasting biology of the most important members of the FCR complex is described in Table 1.

Table 1. Contrasting biological features among the most important members of the Fusarium crown rot complex.
 

Pathogenic variation among isolates is recognized for species associated with the crown rot complex (Smiley et al, 2005a-b). A comparison of pathogenicity of the FCR complex pathogens on hard red spring and durum wheat conducted in Montana showed that F. culmorum caused the greatest seedling blight, while F. pseudograminearum and F. graminearum caused greater crown rot (Dyer et al, 2009).

Disease cycle of Fusarium crown rot

Both seed-borne and soil-borne inoculums are important to the epidemiology of FCR (Cook, 1981). Chlamydospores, macroconidia, and mycelium are common survival structures in the soil and in crop residues (Paulitz, 2006; Cook, 1981). F. culmorum survives adverse conditions and generally remains as viable chlamydospores, while F. pseudograminearum and F. avenaceum most commonly survive as mycelium inside non-decayed plant residues. This is the major reason why the adoption of conservation tillage practices has resulted in an increase of FCR caused by F. pseudograminearum (Sitton and Cook, 1981; Paulitz et al., 2002).

Crown infection initially occurs 2-3 cm below the soil surface, either through openings around emerging secondary roots or by infection of newly emerging crown roots (Cook, 1981; Wiese, 1991). Coleoptile infection also occurs through stomata and between epidermal cells (Malalasekera et al., 1973). Infection of the seedling occurs through epidermal cell layers of the coleoptile and then expands into the parenchyma (Pisi and Innocenti, 2001). During pathogenesis, FCR pathogens produce an array of enzymes to overcome plant defense responses. Both induction of active laccases (Kwon and Anderson, 2002) and enhancement of catalase activity (Ponts et al., 2009) caused by FCR pathogens have been reported. These enzymes have been associated with reducing or inactivating active oxygen species (AOS) produced by the plant in response to necrotroph infection (Mayer et al, 2001). It is also important to note that trichothecene mycotoxin deoxynivalenol (DON), which is a toxin produced during infection by F. graminearum and F. pseudograminearum in the wheat stem base (Mudge et al, 2006), could play an important role in colonization of the wheat stem because DON is an inhibitor of protein synthesis. Thus, DON could suppress the production of host defense enzymes and other compounds, as has been suggested by Mudge et al. (2006). DON also elicits hydrogen peroxide production, programmed cell death and defense responses in wheat (Desmond, 2008b). Additionally, defense responses of the plant during Fusarium colonization could be depleted by ammonization and pH modulation of apoplastic fluids by F. culmorum infection. Ammonization and pH modulation have shown to modulate the activity of the cell-wall-degrading enzymes polygalacturonase and pectin lyase (Aleandri et al., 2007). When FCR pathogens are inside the plant, colonization of the pith cavity is not restricted by the barrier of the lumen at each node (Clement and Parry, 1998). The lumen appears to provide a pathway for vertical growth, while the surrounding parenchyma cells provide a potential nutrient source and a humid environment (Mudge et al., 2006). Similarly, Stephens et al. (2008), working with histological and real-time quantitative polymerase chain reaction (qPCR) analyses, showed that when F. graminearum causes crown rot, three distinct phases of infection can be identified: i) initial spore germination with formation of a superficial hyphal mat at the inoculation point, ii) colonization of the adaxial epidermis of the outer leaf sheath and mycelial growth from the inoculation point to the crown, concomitant with a drop in fungal biomass, and iii) extensive colonization of the internal crown tissue. This study also examined gene expression during each phase using Affymetrix GeneChips. In total, 1,839 F. graminearum genes were significantly up-regulated, including some known FHB virulence genes associated with mycotoxin production (e.g., TRI5 and TRI14), and 2,649 genes were significantly down-regulated in planta compared with axenically cultured mycelia. Plants infected by FCR rarely show obvious symptoms until after heading (Cook, 1981). However, if wheat plants are under drought conditions, plant defenses weaken and the pathogen infection expands in the vascular tissue, disrupts water movement and prevents the recovery of infected plants from water stress (Cook and Christen, 1976; Hare and Parry, 1996).

Antagonistic responses or interactions between fusaria and other pathogens have been studied. The negative relationship between pathogen populations in a field is likely to be regulated by dynamics of competition for colonizing the different wheat tissues or/and displacement between each pathogen, depending on environmental conditions that favor one pathogen or the other. For example, Tinline (1977) reported that prepossession of the internode by B. sorokiniana infection does not prevent subsequent invasion by F. culmorum and F. acuminatum, but that prepossession by fusaria pathogens greatly reduces subsequent infection by B. sorokiniana in studies of single or combined inoculation of wheat. In the same way, Moya-Elizondo et al. (2011b) assessed pathogen populations in the first internode at heading, milk, and harvest stage of wheat development using qPCR. They reported that high and low levels of F. pseudograminearum inoculum colonized lower internodes earlier and reduced B. sorokiniana populations in field trials, but B. sorokiniana inoculations did not affect F. pseudograminearum populations. However, neither of the pathogens prevented infection by the other in the first internode of wheat stems.

Management of Fusarium crown rot

The probable increase of FCR infestation in wheat crops under dryland field conditions, which could be associated with global climate change and adoption of no-till practices worldwide, will force growers and agricultural extensionists to deepen their knowledge of management strategies for this disease complex. Cook (2010) has recommended different control practices, such as the use of clean and chemically disinfected seed, management of seeding dates, proper fertilization, the use of tillage, crop rotations avoiding other cereals, and the use of cultivars with resistance or tolerance and/or with resistance to water stress. No single management strategy has proven effective in eliminating root and crown rots. However, combined practices have proved helpful, even though they do not provide high levels of control.

Chemical disinfection of seed. Fungicide seed treatments are recommended for the management of FCR and other soilborne diseases, combined with healthy seeds. In fact, their capability of reducing seedling blight has been widely observed (Cook, 2010). For example, emergence of winter wheat in fields was superior for seed treated with difenoconazole (Dividend®) alone or mixed with metalaxyl (Apron®) (Smiley and Patterson, 1995). Extension plant pathologists at Montana State University recommend using seed treatment fungicides such as Vitavax Extra (carboxin + imazalil + thiabendazole), Dividend XL or RT (difenoconazole + mefenoxam), Raxil XT or MD (tebuconazole + metalaxyl), Raxil MD Extra (tebuconazole + metalaxyl + imazalil), Baytan (tridimenol), and RR, Flo-pro, NuZone (imazalil) to promote healthy seedling growth (Dyer et al, 2007). However, as fungicides do not maintain their efficiency beyond 2-4 weeks (Balmas et al., 2006), chemical control is limited to the early stages of wheat growth, and later infections can be observed, especially in winter wheat.

Management of planting date. The use of cultivars with high yield potential and following the recommended date of planting in a geographic area can be simple actions that reduce the incidence of DLRRC disease. In general, early planting promotes disease in winter wheat (Cook, 2010). In the PNW, assessment of planting dates showed that FCR was more prevalent in early-planted winter wheat and generally reduced or absent in plantings made later in the fall (Smiley, 2009). Late-autumn seeding of winter wheat also reduces seedling exposure to warm soil and limits the amount of vegetative growth that can lead to premature reduction of soil water and water stress that promotes damage by pathogens (Cook, 2010). Despite the effectiveness of this practice, management of planting date depends on the amount of hectares managed by each farmer and weather conditions associated with each area of production.

Crop rotation with non-cereals. Crop rotation is the most effective method to control soilborne pathogens. Crop rotation also allows growers to limit alternative hosts and to control the more ephemeral Fusarium species (Wiese, 1991), which significantly reduces the pathogenic fitness level of F. graminearum and F. pseudograminearum on wheat (Akinsanmi et al, 2007). However, about half of the inoculum of Fusarium spp. present after harvest is functional a year later, and approximately 10% can survive for nearly two years (Wiese, 1991). Rotation with a broadleaf crop, such as peas or soybeans has proven beneficial to limit damage from both FHB and FCR caused by F. graminearum. In fact, a crop rotation with at least a two-year break from cereal is the most effective way to reduce damage from FCR caused by F. pseudograminearum (Burgess et al., 2001; Cook, 2010). The longevity of chlamydospore inoculum of F. culmorum makes the use of rotation more challenging, as evidenced by experiments that showed that a two-year break did not provide effective control of this species (Cook 1981, 2010). Fernández et al. (2007b) reported that summer-fallow was associated with increased infection by B. sorokiniana, whereas it appeared that relative levels of Fusarium spp., except for F. acuminatum and F. equiseti, consistently decreased when there was summer-fallow in the previous year, or in one of the previous 2 years. Fusarium species have a large host range, which includes numerous grass species; therefore, crop options for the rotations are limited. Additionally, crop rotation options are limited in some areas because low rainfall limits commercial economic alternatives (Strausbaugh et al, 2005).

Cultivar resistance or tolerance. Use of resistant cultivars would be the most effective and efficient measure to reduce the impact of FCR disease. Nevertheless, resistance to FCR pathogens in commercial cultivars is only partial (Cook, 2010) and disease outbreaks are common and can also be severe when climatic conditions are favorable for the pathogens on these partially resistant cultivars (Burgess et al, 2001; Strausbaugh et al, 2005).

Resistance to Fusarium pathogens is associated with FHB resistance (Bai and Shaner, 2004) or direct resistance to crown root rot disease (Smiley et al., 2003). The two most important types of resistance to FHB in wheat have been described as resistance to initial infection (referred as type I) and resistance to spread of FHB symptoms within a spike (referred to as type II). Type II resistance has been found in a number of wheat cultivars and appears to be more stable and less affected by non-genetic factors than type I resistance (Bai and Shaner, 2004). However, while high resistance to FHB has been described (Bai and Shaner, 2004), work performed by Xie et al. (2006) and Li et al. (2010) suggested that FHB resistant germplasm did not offer any resistance to FCR. The idea of resistance inversion has been proposed for the observed phenomenon of differential resistance to FCR and FHB in wheat, where one plant genotype displays a resistant phenotype at one development stage but a susceptible reaction to the same pathogen at another stage (Li et al., 2010). Nevertheless, work conducted by Moya-Elizondo and Jacobsen (unpublished data) have shown dual resistance to FCR and FHB in cv. Volt, and their results contradict the idea of resistance inversion proposed by Li et al. (2010). Cultivar Volt is also considered to have good tolerance to FHB, but this resistance did not originate in the 1B chromosome from the Chinese Sumai 3 cultivar, which gives resistance to FHB. On the other hand, its performance against FCR is similar or worse than other cultivars that are susceptible to FHB and FCR (Xie et al., 2006; Moya-Elizondo and Jacobsen, unpublished data).

Seedling and adult plant tolerance (partial resistance) to some members of the FCR complex, such as F. pseudograminearum, has been reported (Collard et al, 2005; Bovill et al, 2006; Li et al, 2010; Cook, 2010) and is associated with reduced damage to stem base tissue and increased wheat yield (Wildermuth et al, 2001). Seedling resistance, but not adult-plant resistance, has been associated with the phenotypic expression of a genetically determined trait, the depth at which crown tissue is formed for each wheat cultivar or breeding line (Wildermuth et al, 2001). Collar et al. (2005) used molecular markers associated with partial seedling resistance to FCR disease in populations of double haploid lines constructed from crosses between '2-49' (partially resistant) and 'Janz' (susceptible) parents. The authors demonstrated that the trait is quantitatively inherited and that none of the QTLs identified as conferring resistance to FCR were located in the same region as resistance QTLs that were identified as segregating for FHB caused by F. graminearum in other populations. Seedling resistance has been linked to QTLs located on chromosomes 2B, 2D and 5D in progenies obtained from a cross between 'W21MMT70' (partial resistance) x 'Mendos' (susceptible) (Bovill et al., 2006). These loci are different from those associated with crown rot resistance in other wheat populations that were examined by Collar et al. (2005), who determined that resistant QTL's were located on chromosomes 1D and 1A. Bovill et al. (2006) suggested that these loci may represent an opportunity for pyramiding QTL to provide stronger resistance to FCR. Recent studies on the effects of plant height on FCR disease severity in near-isogenic lines (NILs) have shown that dwarf isolines had better FCR resistance when compared with their respective tall counterparts and that this resistance was not associated with enhanced defense gene induction (Liu et al., 2010). These authors suggested that the difference in FCR severity between the tall and dwarf isolines might be due to their height difference per se or to some physiological and structural consequences of reduced height.

According to Smiley et al. (2003), genetic tolerance to FCR is important during years when disease pressure is moderate, and it is ineffective when disease pressure is high. In the PNW, Smiley and Yan (2009) conducted a study with winter wheat cultivars, and screened for tolerance to FCR in naturally infested and inoculated soils. The phenotypic tolerance response in individual cultivars was highly variable over years and test sites. In addition, these authors - in a cooperative effort between Australian and USA researchers - have identified significant differences among spring wheat entries in the PNW (Smiley and Yan, 2009).

Losses caused by FCR pathogens are significant. Therefore, active wheat screening and breeding programs for dryland root rot resistance and tolerance have been actively initiated in different locations worldwide with the support of CIM-MYT (Nicol et al, 2004; Smiley et al, 2003; Phil Bruckner, Montana State University, Bozeman, USA, personal communication).

Effect of crop nutrition. Soil fertility must be adequate to support vegetative growth but it needs to be balanced with water supplies to avoid FCR. Excessive nitrogen under low-rainfall conditions promotes vegetative growth and especially tiller formation that could be sustained by the remaining water stored in the soil. These conditions favor water stress on the plants during heading and grain fill, which predisposes the crop to severe foot and crown rot caused by FCR (Papendick and Cook, 1974; Cook, 1980; Burgess et al.,, 2001; Cook, 2010). Cook (1980) recommended nitrogen application rates to be based on a soil test for residual nitrogen. Nitrogen fertility should not exceed 60-75 kg ha-1 in areas with <240 mm average annual precipitation. Moreover, zinc deficiency has been linked with higher levels of infection caused by F. pseudograminearum on wheat in glasshouse trials (Sparrow and Graham, 1988). In addition, wheat genotypes with a more efficient capacity to extract zinc from soils with poor zinc availability have been associated with a reduction of FCR severity as well as increased plant vigor (Grewal et al., 1996).

Effect of tillage practices and stubble management. Preceding cropping sequences and agronomic practices can affect the level of inoculum of the FCR pathogens and its distribution in the field, thus defining the incidence of infected plants by FCR (Burgess et al., 2001). FCR has shown higher incidence and severity where stubble is retained than where it is removed (Wildermuth et al, 1997; Paulitz et al, 2002; Cook, 2010). Management of infected stubble through post-harvest burning, fire plus harrowing in the fall season, stubble incorporation by disc cultivators that invert the soil and surface residue, or stubble retirement from the field will greatly reduce the sources of inoculum for FCR (Burgess et al., 2001). On the other hand, plowing that promotes the fragmentation and decomposition of stubble reduces infection by FCR pathogens, such as F. pseudograminearum or F. graminearum (Burgess et al., 2001; Steinkellner and Langer, 2004), but has a lesser effect on the persistent chlamydospores of F. culmorum (Windels and Wiersma, 1992). In dryland agriculture, the use of summer fallow to conserve soil moisture and release organic nitrogen has caused widespread adoption of moisture-conserving minimum tillage systems (Padbury et al., 2002). The use of no-till and conservation tillage system practices in a wheat-fallow production system has been associated with higher levels of Fusarium infections (Smiley et al, 1996; Bailey et al, 2001) and a population change from F. culmorum to F. pseudograminearum (Sitton and Cook, 1981; Paulitz et al., 2002). It has also been suggested that F. pseudograminearum is more aggressive than F. culmorum, which may explain the increase in FCR severity under conservation tillage systems (Paulitz et al, 2002; Smiley et al, 2005a). F. pseudograminearum is strictly a residue-born pathogen that depends on infesting late season tillers for survival between cropping periods (Sitton and Cook, 1981; Pereyra and Dill-Macky, 2004). This fact could increase the selection pressure on the pathogen to capture residues in order to survive a prolonged non-cropping period (Dyer et al, 2009). According to Bailey (1996), prior to the adoption of conservation tillage, the impact of these factors on FCR was largely unknown and could not have been properly considered in making predictions about the impact of conservation tillage practices on this disease. Studies conducted for six years by Paulitz et al. (2010) in an irrigated cropping systems experiment in east-central Washington State determined that inoculum concentration of F. pseudograminearum was higher than that of F. culmorum after three continuous years of winter wheat cultivation; in one of three years, the former was higher after treatments with standing stubble and mechanical straw removal compared to burned treatments. However, burning stubble is a very controversial practice due to the pressure to reduce CO2 emissions to prevent global climate change.

Effect of other cropping practices. Cook (1980) recommended increasing the distance between rows to reduce crown and root rot infection in semiarid areas. The wide-row spacing results in a reduced seedling density and hence a slower rate of soil water use per unit of field area (Papendick and Cook, 1974; Cook, 1980). Cultural practices to reduce moisture loss from the soil would logically be associated with a reduction of crown and root rot diseases (Papendick and Cook, 1974). Improving infiltration and reducing water runoff during precipitation or snow melt by working the field with a chisel plow is thought to reduce crown and root rot diseases by making more water available (Cook, 1981). Controlling weeds in summer fallow land and during crop development should also reduce infection by these diseases, because weeds deplete soil moisture that predisposes plant roots to infection in fall. However, studies conducted in the Northern Great Plain of Canada have determined that previous glyphosate applications in summer-fallow were associated with lower B. sorokiniana and higher Fusarium spp. levels in barley and wheat grown under minimum-till management (Fernández et al, 2005; Fernández et al. 2007a-b, Fernández et al, 2008; Fernández et al, 2009).

New strategies for the control of crown and root rot diseases

The management cropping practices previously discussed make controlling the crown and root rot complex challenging and emphasize the need for other control alternatives. Wildermuth et al. (1997) have suggested that some form of biological suppression may be operating to limit the maximum incidence of crown and root rot infections in Australia. Biological control agents (BCAs) have shown promise in the control of FCR disease (Huang and Wong, 1998; Dal Bello et al, 2002; Johansson et al., 2003; Luongo et al., 2005; Khan et al, 2006; Singh et al, 2009). Two approaches have been considered: 1) Manipulation of microbial antagonists to increase the rate of mortality of Fusarium spp. in cereal residues (Wong et al, 2002; Luongo et al, 2005; Singh et al, 2009), and 2) seed treatment with BCAs (Dal Bello et al, 2002; Khan et al, 2006). Assessment of saprophytic fungi obtained from cereal tissues or necrotic tissues of other crops have shown that isolates of Clonostachys rosea consistently suppressed sporulation of F. culmorum and F. graminearum on wheat straw (Luongo et al., 2005), while Trichoderma harzianum, F. equiseti, and F. nygamai showed strong antagonism in dual culture interactions with F. pseudogramineraum (Singh et al, 2009). These data have been validated in bio-assays conducted under controlled conditions, but results have been variable for different Fusarium spp. (Luongo et al, 2005). In addition, BCA performance was strongly affected by temperature and water potential (Singh et al, 2009). Seed bio-based treatment has proven promising for enhancing biological control of plant diseases. Huang and Wong (1998), working with Burkholderia cepacia (A3R), significantly reduced crown rot symptoms caused by F. pseudograminearum on wheat in glasshouse and field experiments and significantly increased grain yield in one of two field experiments. Johansson et al. (2003) tested the action of 164 bacterial isolates against both F. culmorum and M. nivale as causal agents of wheat seedling blight in field experiments during five consecutive growing seasons. Their research determined that three fluorescent pseudomonads and Pantoea sp. isolate MF 626 were able to increase the number of established wheat plants under field conditions, when wheat seeds were coinoculated with F. culmorum. Del Bello et al. (2002) assessed fifty-two bacterial strains and six Trichoderma spp. isolated from the wheat rhizosphere for biocontrol of seedling blight of wheat caused by F. graminearum. Among isolates tested, Stenotrophomonas maltophilia, three strains of Bacillus cereus and one isolate of T. harzianum increased the plant stand, height and dry weight in different wheat cultivars, but did not cause a significant decrease in the percentage of diseased plants. Khan et al. (2006), working with pseudomonads and chitosan against F. culmorum, reported the induction of a wheat class III plant peroxidase gene, which suggested that part of the biocontrol activity of these bacteria and chitosan might be due to the induction of systemic acquired resistance (SAR) in host plants.

One promising strategy to control diseases is induced resistance. In the broadest sense, induced resistance means the control of parasites or pests by activation of genetically programmed plant defense pathways before infection or infestation (Kogel and Langen, 2005). Induced resistance to microbial pathogens, resembling the SAR response, can be obtained by applying defense-signaling compounds that activate the defense signaling pathways (Kogel and Langen, 2005). In cereals, pathways for SAR induction are regulated by salicylic acid (SA) and jasmonic acid (JA) and their cellular targets (Kogel and Langen, 2005). Downstream signaling components, such as nonexpressor of pathogenesis-related gene 1 (NPR1), are deployed during SA-dependent defense and orchestrate cross-talk between the SA and JA pathways (Spoel et al., 2003). The antagonistic SA and JA pathways elicit the accumulation of distinct subsets of defense-related proteins. SA-dependent pathways are associated with Pathogenesis-Related proteins (PR-proteins), such as peroxidase, chitinase, β-glucanase and PR-1 (Durrant and Dong, 2004). The JA pathway is associated with production of thionins, defensins and proteinase inhibitors (Xu et al., 2001). Almost all classes of PR-proteins induced in plants in response to attack by microbial or insect pests have been identified in wheat (Muthukrishnan et al., 2001).

Few studies have been conducted to explore the response to infection with crown rot pathogens in wheat. Desmond et al. (2006), studying the molecular host-interaction between F. pseudograminearum and wheat, showed the induction and expression of eight defense genes in a susceptible and a partially resistant cultivar of wheat when plants were infected by the pathogen. Additionally, they were able to show that the induction of those genes by methyl jasmonate and benzo (1,2,3)thiadiazole-7-carbothionic acid-S-methyl ester (BTH, Bion) treatments delayed disease development caused by infection of F. pseudograminearum. In two gene expression research projects, induction of chitinase gene expression in wheat seedling has been observed in response to F. pseudograminearum (Desmond et al, 2006) and F. asiaticum (Li et al., 2010) infection.

Over-expression of the chitinase gene and chitin-binding (PR-4) gene in wheat seedlings has been associated with seedling resistance to F. asiaticum infection. High expression of a plant cytochrome P450 gene CYP709C1, which is involved in detoxification of exogenous compounds, has also been associated with seedling resistance to F. asiaticum infection (Li et al, 2010). Pathogenesis-related proteins of the PR-4 family have been shown to have distinct antifungal activities in coleoptiles and roots against F. culmorum (Caruso et al., 2001; Bertini et al, 2003). PR 4 has chitin-binding activity and it has been demonstrated to possess RNAse activity, which may be part of a mechanism for inhibiting invading pathogens (Caruso et al., 2001). Moreover, Desmond et al. (2006) also showed that in response to FCR, thaumatin-like proteins (PR-5) were highly expressed after inoculation with F. pseudograminearum.

By using a GeneChip® Wheat array, Desmond et al. (2008a) showed that after one day of stem base inoculation of 2-week-old wheat seedlings with F. pseudograminearum, 1248 unique genes were induced compared to mock-controls. Among these genes, the largest classes of induced genes were associated with anti-microbial proteins, such as chitinase, β-1, 3-glucanase, PR-1, PR-10, PR-5, peroxidases, germin-like proteins, and detoxifying proteins such as glucosyltransferase or cytochrome P450. This array of genes involved in the response of the plant to crown rot pathogens indicates that process of resistance to this necrotrophic disease is complex, and demonstrates the necessity of going in depth in the study of genes that correspond to different sources of disease resistance.

In conclusion, FCR disease is an endemic disease in wheat crops caused by different pathogens of the genera Fusarium. Predictions associated with global climate change suggest considerable yield loss and widespread distribution of the pathogens associated with this crown and root rot complex on worldwide cereal agro-ecosystems. This concern is especially high due to the changing patterns of rainfall and increasing drought over different regions of the world, which could increase yield losses and the prevalence of the diseases and the pathogens. Field surveys of pathogen species associated with FCR in different wheat crop regions could be an adequate tool to assess changes associated with climate change, especially considering the impact of agroecological zones on the distribution, incidence and prevalence of different Fusarium species. Based on the diverse biology involved in the establishment and disease infection of the pathogens of the FCR complex, management strategies are required. The use of certified and chemically disinfected seed, management of seeding date, proper fertilization, the use of tillage, crop rotations avoiding other cereals, the use of cultivars with resistance or tolerance, and/or with resistance to water stress are useful tools to reduce the impact of this disease. However, new practices such as the use of biological control and induction of resistance with chemicals and BCAs could be new alternatives to control this problem.

Acknowledgements

The author would like to thank Dr. Barry J. Jacobsen at Montana State University for his time, useful comments and assistance in the preparation of this review article. This work was partially funded by the Comisión Nacional de Investigación Científica y Tecnológica de Chile (CONICYT) through FONDECYT grant No. 11110105.

 

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Received October 23, 2012.
Accepted April 9, 2013.

 

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