AOBPreview originally published online on June 27, 2006
Annals of Botany 2006 98(6):1117-1128; doi:10.1093/aob/mcl132
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INVITED REVIEW |
Annual Medicago: From a Model Crop Challenged by a Spectrum of Necrotrophic Pathogens to a Model Plant to Explore the Nature of Disease Resistance
1 Institut National de la Recherche Agronomique, Centre de Recherche de Rennes, UMR BiO3P Domaine de la Motte, BP 35327 Le Rheu Cedex, France
2 Institut National de la Recherche Agronomique, Centre de Recherche de Rennes, UMR APBV Domaine de la Motte, BP 35327 Le Rheu Cedex, France
3 School of Earth and Geographical Sciences, The University of Western Australia 35 Stirling Hwy, Crawley, WA 6009, Australia
4 School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia 35 Stirling Hwy, Crawley, WA 6009, Australia
* For correspondence. E-mail mbarbett{at}cyllene.uwa.edu.au
Received: 10 March 2006 Returned for revision: 21 April 2006 Accepted: 22 May 2006 Published electronically: 27 June 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONNECROTROPHIC PATHOGENSHOST RESISTANCE TO NECROTROPHIC...MEDICAGO TRUNCATULA: THE FIRST...CONCLUSIONSLITERATURE CITED |
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• Background Annual Medicago spp., including M. truncatula, play an important agronomic role in dryland farming regions of the world where they are often an integral component of cropping systems, particularly in regions with a Mediterranean or Mediterranean-type climate where they grow as winter annuals that provide both nitrogen and disease breaks for rotational crops. Necrotrophic foliar and soil-borne pathogens dominate these regions and challenge the productivity of annual Medicago and crop legume species.
• Scope This review outlines some of the major and/or widespread diseases these necrotrophic pathogens cause on Medicago spp. It then explores the potential for using the spectrum of necrotrophic pathogen–host interactions, with annual Medicago as the host plant, to better understand and model pathosystems within the diseases caused by nectrotrophic pathogens across forage and grain legume crops.
• Conclusions Host resistance clearly offers the best strategy for cost-effective, long-term control of necrotrophic foliar and soil-borne pathogens, particularly as useful resistance to a number of these diseases has been identified. Recently and initially, the annual M. truncatula has emerged as a more appropriate and agronomically relevant substitute to Arabidopsis thaliana as a model plant for legumes, and is proving an excellent model to understand the mechanisms of resistance both to individual pathogens and more generally to most forage and grain legume necrotrophic pathogens.
Key words: Fungal pathogens, medics, annual Medicago species, Medicago truncatula, Phoma medicaginis, Aphanomyces euteiches, Colletotrichum trifolii, Mycosphaerella pinodes, grain legumes
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONNECROTROPHIC PATHOGENSHOST RESISTANCE TO NECROTROPHIC...MEDICAGO TRUNCATULA: THE FIRST...CONCLUSIONSLITERATURE CITED |
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Annual Medicago spp. play an important agronomic role in dryland farming regions of the world (Walsh et al., 2001) where they are often an integral component of cropping systems, particularly in regions with a Mediterranean-type climate (Piano and Francis, 1992) where they grow as winter annuals (Sheaffer and Lake, 1997). Some annual Medicago spp. have distinct advantages, such as high levels of hard seededness, that make them attractive over other annual forage legume species such as Trifolium subterraneum in many areas.
Annual Medicago spp. provide nitrogen for rotational crops (Zhu et al., 1998; Sheaffer et al., 2001; Walsh et al., 2001), are used as forage legumes (Puckridge and French, 1983; Anon., 1988; Prosperi et al., 1989; Chatterton and Chatterton, 1996), have potential as summer annual forages (Zhu et al., 1996; Shrestha et al., 1998; de Haan et al., 2002), and/or can be used as intercrops with grains (de Haan et al., 1997), can be used as smother crops (de Haan et al., 1997; Sheaffer et al., 2002), are useful as over-winter cover crops (Fisk et al., 2001), or can be used as a ‘disease break’ for rotational crops (Walsh et al., 2001).
Annual Medicago spp. originated in the Mediterranean region, in which the greatest species diversity occurs (Piano and Francis, 1992). Some 33 species of annual Medicago are recognized (Lesins and Lesins, 1979). Of these, M. polymorpha is considered to be ubiquitous; M. truncatula, M. orbicularis and M. littoralis are distributed throughout areas with Mediterranean-type climates; while some species have close associations with specific regions, such as M. murex with central and western Mediterranean regions, M. rigidula with the Irano-Turanian region, M. tornata and M. aculeata with the western Mediterranean, and M. blancheana, M. constricta, M. noeana, M. radiata and M. rotata with the eastern Mediterranean region (Piano and Francis, 1992).
The distribution of annual Medicago spp. is influenced by edaphic factors including: soil type, levels of soil Ca, P, S and NO3, and soil salinity (Andrew, 1977; Robson, 1983; Abdelguerfi et al., 1988; Prosperi et al., 1989; Ehrman and Cocks, 1990; Ewing and Robson, 1990; Piano et al., 1991; Bounjemate et al., 1992); climatic factors such as altitude and annual rainfall (Gintzburger and Blesing, 1979; Francis, 1980, 1987; Cocks and Ehrman, 1987; Abdelguerfi et al., 1988; Ehrman and Cocks, 1990; Piano et al., 1991); biotic factors such as regeneration capacity and levels of hardseededness (Francis, 1987; Thomson et al., 1990); and possibly also by available rhizobial components (Robson and Loneragan, 1970; Robson, 1983; Vincent, 1988). The effects of these factors on the distribution of annual Medicago spp. have previously been reviewed, for example by Piano et al. (1991) and by Piano and Francis (1992).
There are numerous pathogens of forage plants, with some 400 fungal, bacterial, viral, mycoplasma and nematode diseases known to affect forage species on a worldwide basis (Haggar et al., 1984). Although some aspects of forage diseases have been extensively reviewed (e.g. Graham et al., 1979; Haggar et al., 1984; Barnett and Diachun, 1985; Braverman et al., 1986; Edwardson and Christie, 1986; Johnstone and Barbetti, 1987; Raynal et al., 1989; Cook and Yeates, 1993; Lenné, 1994a, b; Barbetti et al., 1996), such reviews cover superficially, if at all, necrotrophic fungal diseases of annual Medicago spp.
This review outlines the major diseases caused by foliar and soil-borne necrotrophic pathogens and explores the potential for using the spectrum of necrotrophic pathogen–host interactions, with annual Medicago as the host plant, to better understand and model pathosystems within the diseases caused by nectrotrophic pathogens across forage and grain legumes. The links between annual and perennial Medicago spp., the model plant M. truncatula, and with grain legume species, in relation to their interactions with one or more related or unrelated necrotrophic pathogens are considered. For this review, we based our definition of ‘necrotrophs’ on that of Agrios (2004), to mean organisms which can have one part of their life cycle on dead host/tissue and which can grow on artificial nutrient media. As much of the existing literature covers one or more annual Medicago spp. in addition to M. truncatula, discussions in this review relate to annual Medicago spp. in general.
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NECROTROPHIC PATHOGENS |
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TOPABSTRACTINTRODUCTIONNECROTROPHIC PATHOGENSHOST RESISTANCE TO NECROTROPHIC...MEDICAGO TRUNCATULA: THE FIRST...CONCLUSIONSLITERATURE CITED |
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There are many foliar and soil-borne necrotrophic pathogens of annual Medicago spp., and an outline of some of the most important and/or frequently occurring diseases in different regions that are caused by necrotrophic fungal pathogens are listed in Table 1. As indicated, some necrotrophic fungal pathogens (e.g. Phoma medicaginis) on annual Medicago spp. are also known to stimulate production of high levels of phyto-oestrogenic compounds, such as coumestrol. These compounds can adversely affect ovulation rates in sheep (Smith et al., 1979; Croker et al., 1994a, b, 1999, 2005). It is noteworthy that production of phyto-oestrogen compounds in response to disease varies between genotypes of annual Medicago spp. (Barbetti and Fang, 1991; Barbetti and Nichols, 1991).
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As also indicated in Table 1, a number of Fusarium spp. on annual Medicago spp. have been shown to be responsible for the production of deleterious mycotoxins on animal feed material in Australia (Barbetti and Allen, 2005, 2006) and particularly in South Africa, where there is concern about the ability of Fusarium spp. on annual Medicago spp. to produce mycotoxins on animal feed material (Lamprecht et al., 1986).
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HOST RESISTANCE TO NECROTROPHIC PATHOGENS |
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TOPABSTRACTINTRODUCTIONNECROTROPHIC PATHOGENSHOST RESISTANCE TO NECROTROPHIC...MEDICAGO TRUNCATULA: THE FIRST...CONCLUSIONSLITERATURE CITED |
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A range of cultural and chemical strategies have been used to varying degrees for control of diseases in annual Medicago spp. (e.g. Barbetti, 1989a; You et al., 1999; Walsh et al., 2001). However, it is the use of resistant cultivars that offers the most effective long-term control measure for annual forage and grain legume diseases. This approach has been spectacularly successful as the main and most reliable avenue for the successful management of the most important pathogens of annual forage legumes such as Kabatiella on Trifolium spp. (Barbetti, 1996). These same opportunities exist for at least some diseases, such as Phoma blackstem disease, in annual Medicago spp. (Barbetti, 1993) providing large-scale screening of germplasm for resistance is undertaken as has been done for many years against Kabatiella in Australia (Nichols et al., 1996).
A degree of resistance to many diseases is already available in some annual Medicago spp. For example, variation in resistance to stem and leaf disease caused by Phoma medicaginis (Renfro and Sprague, 1959; Barbetti, 1987, 1989a, 1990; O'Neill et al., 2003), by Leptosphaerulina trifolii (Renfro and Sprague, 1959; Martinez and Hanson, 1963; Barbetti and Nichols, 1991), by Colletotrichum trifolii (Parmelee, 1962; Raynal, 1977; Elgin and Ostazeski, 1982; Lamprecht and Knox-Davies, 1984a, b; Lamprecht, 1986b; Troeung and Gosset, 1990; O'Neill and Bauchan, 2000), by Cercospora medicaginis (Berger and Hanson, 1963; Barbetti, 1985), by Pseudopeziza medicaginis (Schmiedeknecht, 1959), by Phytophthora medicaginis (de Haan et al., 2002) and by Leptotrochila medicaginis (Semeniuk and Rumbaugh, 1976) has been reported in annual Medicago spp. Andrew (1962) demonstrated that M. denticulata had much greater resistance to post-emergence by Pythium spp. than did M. minima.
Methods of identifying host resistance: foliar necrotrophic pathogens
Various types of tests have been used to identify host resistance in annual Medicago spp. to necrotrophic foliar pathogens, ranging from laboratory to glasshouse screening tests to evaluations of swards under field conditions as illustrated in Fig. 7. For example, Troeung and Gosset (1990) used laboratory tests to locate resistance to Colletotrichum trifolii in annual Medicago spp. such as M. rigidula and M. truncatula. Lamprecht and Knox-Davies (1984b) tested the reactions of 3- and 6-week-old plants of annual Medicago accessions using C. trifolii spore suspensions at 15–25 °C under glasshouse conditions and assessed disease using the five-point scale of Ostazeski et al. (1969) (immume, resistant, intermediate, susceptible, dead) after 14 d to highlight different accession responses to crown rot. Lamprecht (1986b) used five different C. trifolii spore suspension application techniques and a sand-bran culture application technique on 4- to 6-week-old injured and uninjured M. littoralis, M. tornata, M. truncatula and M. scutellata plants held at 15–28 °C under glasshouse conditions and assessed disease on a 0–4 pointscale, where 4 indicated crown completely rotted, to successfully highlight resistance in M. truncatula. O'Neill and Bauchan (2000) and O'Neill et al. (2003) used standardized environmental conditions in growth chambers to screen separately 201 accessions across 36 annual Medicago spp. for resistance to C. trifolii and Phoma medicaginis. Semeniuk and Rumbaugh (1976) screened 25 annual Medicago spp. for resistance to Leptotrochila medicaginis under glasshouse conditions, identifying a high level of resistance in 22 of the species tested.
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Frequently, germplasm responses to various diseases are a consequence of opportunistic occurrences of diseases in germplasm trials established for other purposes. A good example of this was the assessment by Lamprecht and Knox-Davies (1984a) of annual Medicago spp. varietal reactions (using a 0–4 disease severity index where 4 represents maximum disease) to a range of necrotrophic pathogens (Phoma medicaginis, Leptosphaerulina trifolii, Colletotrichum trifolii and C. destructivum, Cercospora medicaginis, Pseudopeziza medicaginis and Stemphylium vesicarium) in experimental field plots at 12 locations in South Africa. In Western Australia, a 0–10 point disease assessment scale is frequently used (Barbetti, 1990), and for leaf pathogens such as Phoma, Leptosphaerulina, Pseudopeziza, plots are rated 0, where there was no disease; 1, where there was >0–9 %; 2,
10–19 %; 3, 20–29 %; 4, 30–39 %; 5, 40–49 %; 6, 50–59 %; 7, 60–69 %; 8, 70–79 %; 9, 80–89 %; and 10, 90 % of leaves with lesions. However, depending upon the disease symptoms, especially if multiple diseases are occurring in the same plots, diseases can also be rated using a simplified system where 0 = no disease, 1 = there were >0–10 % of stems with mostly small (<3 mm diameter or length) lesions; 2 = there were >10–20 % of stems with small lesions; 3 = there were >20–30 % of stems with lesions and then ratings 4–10 reflecting an increasing incidence and severity of damage and, ultimately, complete collapse of the sward.
Methods of identifying host resistance: soil-borne necrotrophic pathogens
Various types of tests have been used to identify host resistance in annual Medicago spp. to necrotrophic soil-borne pathogens, ranging from glasshouse screening tests to evaluations under field conditions. For example, de Haan et al. (2002) used field assays on single rows of annual Medicago spp. at a site that had been artificially prior-inoculated using infested soil. They applied irrigation to maximize disease severity and assessed the level of root rot on plants using the 1–6 point disease scoring system described by Thies and Barnes (1991), which defined resistant germplasm as those with disease scores of only 1–2.
It is important that resistance to seedling death, damping-off and root disease all be determined in the search for annual Medicago spp. genotypes with improved field performance against soil-borne pathogens in disease-prone areas. This is because studies with annual Trifolium spp. have clearly indicated that resistance to seedling damping-off is frequently specific and under different genetic control to resistance to root rot (e.g. You et al., 2005), and it is likely that the same will apply for annual Medicago spp.
Sources of host resistance
Identification of host resistance to many necrotrophic pathogens has frequently been a key aim of cultivar development programmes, especially as there is large variability in annual Medicago spp. in relation to disease resistance, for example Phoma blackstem disease (Barbetti, 1989a, 1990, 1993; O'Neill et al., 2003). However, such resistance has rarely been defined (e.g. as complete or partial, under a monogenic or polygenic control, respectively).
In the United States, de Haan et al. (2002) identified three accessions of M. polymorpha that had resistance to Phytophthora medicaginis. O'Neill et al. (2003) identified accessions within M. constricta, M. doliata, M. heyniana, M. laciniata, M. lesinsii, M. murex, M. orbicularis, M. praecox, M. soleirolii and M. tenoreana that exhibited a high level of resistance to Phytophthora medicaginis. O'Neill and Bauchan (2000) identified 14 accessions of the 201 tested that had resistance to Colletotrichum trifolii, including accessions in M. murex, M. muricoliptis, M. polymorpha var. brevispina, M. polymorpha var. polymorpha, M. radiata, M. soleirolii, M. truncatula and M. turbinata.
In South Africa, Lamprecht (1986b) identified M. truncatula cultivars ‘Borung’ and ‘Cyfield’ as the most resistant of nine cultivars tested from across four annual Medicago spp. (M. littoralis, M. tornata, M. truncatula and M. scutellata).
In Australia, a high degree of resistance, particularly to Phoma black stem, has been identified in screening programmes, useful both as parental materials in breeding and in providing resistant cultivars (Barbetti, 1995b). The incorporation of this resistance in commercial cultivars offers a promising long-term control measure for foliar disease in annual Medicago spp. (Barbetti and Nicholas, 1997).
Variation in resistance to stem and leaf disease caused by Pseudopeziza medicaginis (Renfro and Sprague, 1959; Barbetti, 1987, 1989a, 1990) and L. trifolii (Renfro and Sprague, 1959; Barbetti and Nichols, 1991) has been reported in annual Medicago spp.
It is noteworthy that the Mediterranean region has proved to be a productive source for collecting host germplasm with excellent resistance to one or more foliar and soil-borne necrotrophic pathogens. The value of this region as a source of resistance is highlighted by the example of the four introductions of Trifolium subterraneum germplasm from Sardinia that were directly released as new cultivars in Australia in the early 1990s, namely cultivars ‘Denmark’, ‘Goulburn’, ‘Leura’ and ‘York’. Against important diseases on T. subterraneum in Australia, two of these cultivars had good resistance to both Race 1 and Race 2 of K. caulivora, two had good resistance to Uromyces trifolii-repentis, three had resistance to Cercospora zebrina and all four had outstanding resistance to the original race of Phytophthora clandestina. This is despite the fact that these diseases occurred infrequently (e.g. C. zebrina and U. trifolii-repentis) or have never occurred (e.g. K. caulivora and P. clandestina) in Sardinia, highlighting the value of looking for annual Medicago spp. sources of resistance to necrotrophic pathogens from the Mediterranean centre of origin, even if the particular diseases of interest do not occur there (Barbetti, 1996; Nichols et al., 1996; M. J. Barbetti, unpubl. data). It is interesting that nearly all the major diseases of annual Medicago spp., especially in Australia, are caused by necrotrophic pathogens that are common to other pasture legumes and across several continents, including the centre of origin of these host taxa. Presumably, such wide distribution of many of these pathogens is due to their wide host range and/or to their seed-borne nature. However, some annual Medicago and Trifolium species in Australia can be challenged by a pathogen such as Phytophthora clandestina that is only recorded in Australia and is yet to be recorded in the centre of origin of the host taxa. This can be described as a ‘new encounter disease’ (Buddenhagen, 1977; Allen et al., 1998) for both these legumes. With Phytophthora clandestina, there is clear indication of the existence of allopatric resistance (Allen et al., 1998) in Sardinia. It is also interesting that secondary centres of genetic diversity for annual Medicago and Trifolium spp. in Australia have provided successful sources of naturalized strains with increased resistance to disease for pasture legumes (Barbetti, 1996).
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MEDICAGO TRUNCATULA: THE FIRST MODEL MEDICAGO SP. |
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TOPABSTRACTINTRODUCTIONNECROTROPHIC PATHOGENSHOST RESISTANCE TO NECROTROPHIC...MEDICAGO TRUNCATULA: THE FIRST...CONCLUSIONSLITERATURE CITED |
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M. truncatula: why it is an ideal model for necrotrophic pathogens
Although Medicago spp. are subject to a very large range of foliar as well as soil-borne necrotrophic pathogens, our knowledge of resistance sources, resistance expression, genetic determination and resistance mechanisms is still inadequate. However, annual Medicago spp. are now emerging as appropriate and agronomically relevant plants to study necrotrophic pathogens. Among the annual Medicago spp., M. truncatula is already proving to be an ideal model plant for both functional and structural genomic studies for identifying agronomically important genes and studying pathogen relationships in legumes. Arabidopsis, which to date has been the most valuable model plant to work on genetics and physiology of various aspects of plant biology, is a host of a very restricted range of species of necrotrophic pathogens, and is a less relevant model plant as a result.
Medicago truncatula is being used as a model plant for use in both molecular and classical genetic studies because of its ideal characteristics, such as its small, diploid genome, rapid generation time, self-fertility and ease of seed production (Cook, 1999). M. truncatula has proven to be an easily transformed species, ensuring its role as an ideal model system for investigating and elucidating gene function in legume species (Trieu et al., 2000). There are now several large-scale international projects that have been initiated in relation to M. truncatula genomics, including the complete sequence description through an international consortium. Databases considering whole genome sequencing and annotation, expressed sequence tags (ESTs), structural genomics and comparative mapping, bacterial artificial chromosome (BAC) libraries and physical maps, gene expression, metabolic profiling and bioinformatic tools are accessible through the http://www.medicago.org/ website, which offers adequate links to other sites dealing with M. truncatula genomic resources, and legume phylogeny, protocols and publications. There is no resource specifically dedicated to disease resistance in M. truncatula as yet, apart from some reported EST libraries constructed while submitting plants to various biotic stresses (Torregrossa et al., 2006).
The close phylogenetic relationship of M. truncatula to perennial cultivated Medicago spp. such as alfalfa, and other legumes such as pea (Pisum sativum), lentil (Lens culinaris), chickpea (Cicer arietinum) and faba bean (Vicia faba) increases the attractiveness of utilizing M. truncatula to improve our understanding of important agronomic traits in related grain and forage legume species (Dénarié, 2002). Large crop losses in these grain legumes are due to various necrotrophic pathogens (Tivoli et al., 2006). Use of M. truncatula as a model system offers the first real opportunity for understanding the complex genetic and physiological basis of host–pathogen interactions, including secondary metabolite signalling, as has been done earlier for Arabidopsis thaliana (Bouwmeester et al., 2003). It can also be used for transferring these insights to other annual Medicago spp., to grain legumes and to perennial cultivated Medicago spp. In addition, being a field crop species (unlike Arabidopsis) it could be readily used directly in the field where appropriate.
M. truncatula: a host of most necrotrophic pathogens affecting Medicago spp.
Large-scale screening was recently undertaken of M. truncatula, using the significant natural variation in the Australian Medicago spp. collection, to assess differential responses to over 25 necrotrophic pathogens including those causing foliar diseases such as Ascochyta blight, Botrytis grey mould, Colletotrichum anthracnose and Phoma black stem, and root diseases including those caused by Fusarium and Rhizoctonia (Ellwood et al., 2001, 2004, 2005a, b). This clearly shows that M. truncatula is suitable as a host for a very large range of necrotrophic pathogens and that variation for resistance can be identified for some of these pathogens within the Australian Medicago spp. germplasm resources. The United States Department of Agriculture houses a Medicago spp. core collection. Within this, of 201 accessions of annual Medicago species, studied by O'Neill and Bauchan (2000) and O'Neill et al. (2003), most were observed to be susceptible to Phoma black stem and leaf spot caused by P. medicaginis and also to anthracnose caused by C. trifolii. No source with a high level of resistance could be found against P. medicaginis, but accessions with a high level of resistance to C. trifolii were identified (O'Neill and Bauchan, 2000). The screening of four M. truncatula lines by Torregrossa et al. (2004) identified cultivar ‘Jemalong’ and line DZA315.16 as resistant to C. trifolii Race 1. Therefore, M. truncatula can be used as a model for most necrotrophic pathogens affecting annual and perennial Medicago spp. Disease screening studies involving diseases currently associated with losses in other grain and forage legume species and/or genera have also been undertaken. For example, screenings within Medicago spp. have provided key leads in relation to resistance to the fungus Mycosphaerella pinodes, which is responsible for ascochyta blight (black spot) on pea (Moussart et al., 2006). From a core collection of 131 natural populations (Prosperi et al., 2002), 34 M. truncatula ecotypes and nine ecotypes belonging to other Medicago spp. were screened for My. pinodes resistance either on plantlets or on detached leaves. High levels of resistance to My. pinodes with reduced variability between M. truncatula accessions have now been identified (Tivoli et al., 2005; Moussart et al., 2006), where although some flecks were observed on leaves on all the screened accessions, most accessions showed significant restriction of lesion development. Slowly progressing lesions with fructifications were observed on only a few accessions. Three different resistance reactions were noted, including absence of lesions, restricted fungal development to the site of inoculum application and cessation of progressive lesion development (Moussart et al., 2006). These resistance reactions have also been confirmed in another set of M. truncatula accessions (D. Rubiales, pers. comm.).
The availability of germplasm showing various resistance levels towards necrotrophic pathogens within the M. truncatula collections opens the way to (1) isolate the genes controlling resistance to legume necrotrophic pathogens, and (2) study host–pathogen interactions at the histological, biochemical and physiological levels.
M. truncatula: provides for the isolation of genes controlling resistance in Medicago and grain legume species
A cross between cultivar ‘Jemalong’ and the line F83005.5 allowed genetic analysis of resistance in an F2 population, indicating that resistance to C. trifolii was dominant and controlled either by a major resistance gene showing a distorted segregation or by more than one gene (Torregrossa et al., 2004). Ellwood et al. (2005b) have developed and genetically mapped 80 polymorphic markers in a different F2 population from a cross segregating for resistance to P. medicaginis and showed that resistance is under the control of a major gene. Therefore, a rather simple genetic control has been shown in M. truncatula for resistance to two major necrotrophic pathogens of Medicago spp., namely C. trifolii and P. medicaginis. This opens up the way not only for gene isolation based on genomic resources developed in M. truncatula but also for comparative analysis of resistance expression, genetic control and resistance mechanisms between M. truncatula and other Medicago spp. and grain legumes.
The model plant M. truncatula can constitute an efficient bridge between grain and forage legumes. Synteny between Medicago spp. as well as between Medicago and grain legumes such as pea (Gualtieri et al., 2002; Kalo et al., 2004) should allow a comparative analysis of genes or quantitative trait loci involved in resistance to necrotrophic pathogens in these species, including the number of genes involved, genomic localization, contribution to variation, etc. This same perspective could easily be applied where pathogens are common to certain other species (such as C. trifolii and P. medicaginis between different Medicago spp., and probably also P. medicaginis var. pinodella and My. pinodes and between M. truncatula and P. sativum). The suitability of such an approach is illustrated by a study by Kamphuis et al. (2005) in which they were able to conduct disease screening and genetic analyses in M. truncatula for resistance to different Phoma species taken from different legume crops.
M. truncatula: boosts understanding of host–pathogen interactions in both Medicago spp. and grain legumes
During pathogenic interactions between annual Medicago spp. and C. trifolii, O'Neill and Bauchan (2000) observed resistant reactions that were similar to those found in incompatible interactions between this pathogen and alfalfa, with fungal development severely restricted to host tissues at the point of inoculation. They suggested a hypersensitive response, possibly involving phytoalexins, as in the M. sativa–C. trifolii pathosysten (O'Neill, 1996). Cytological observations by Torregrossa et al. (2004, 2006) also showed that resistance was linked to a hypersensitive reaction. Subsequent microarray analysis showed that a strong correlation existed between the number of up-regulated genes and the resistance phenotype. Large differences appeared at 48 h post-inoculation and a large number of defence genes were involved.
Toyoda et al. (2004) described the M. truncatula–My. pinodes interaction and suggested it as a new pathosystem for genetic dissection of susceptibility to fungal pathogens. They observed that as on peas, attenuation or suppression of host defences contributes to establishment of susceptibility. In the case of ascochyta blight resistance on chickpea, Muehlbauer et al. (2005) compared the sequences from selected chickpea BAC clones with M. truncatula genome sequences. They successfully identified several orthologous contigs. The same approach, based on comparative genomics and synteny analyses, was developed by Ford et al. (2005) for ascochyta blight resistance on lentils.
An instructive view of the relevance of M. truncatula as a model species for Medicago spp. as well as for grain legume pathogens is presented by the example of Aphanomyces euteiches, a pathogen causing severe root rot and important yield losses on grain legumes (pea, lentil, vetch, etc.) as well as on alfalfa. The screening of the French core collection (Prosperi et al., 2002) showed that there is a large variation within M. truncatula ecotypes for resistance to a pea A. euteiches isolate, and that the M. truncatula resistant ecotypes present a much higher level of resistance than that observed on pea (Pilet-Nayel et al., 2005; Tivoli et al., 2005; Moussart et al., 2006). Such variation was previously reported in the US by Vandemark and Grunwald (2004) for M. truncatula accessions evaluated for resistance to A. euteiches Race 2, which is pathogenic to alfalfa. Genetic studies (Jacquet et al., 2005a, b; Pilet-Nayel et al., 2005), as well as cytological and transcriptomic studies (Jacquet et al., 2005a, b), have been developed using susceptible and resistant lines of M. truncatula. In order to gain insight into molecular and physiological changes in diseased legume roots, a transcriptomic approach of M. truncatula during infection by A. euteiches was developed by Nyamsuren et al. (2003), which demonstrated that classical mechanisms of pathogenesis as well as new specific gene regulations are involved in root rot disease development caused by A. euteiches. Recently, Colditz et al. (2005) conducted a comparative proteomic analysis of the interaction formed between three lines of M. truncatula and a single A. euteiches strain. Several proteins were identified to be differentially induced after infection of the susceptible or resistant lines. This example shows that through complementary genetic and genomic-based strategies, such a pathosystem can be dissected within M. truncatula and comparative analysis subsequently carried out between this model species and other Medicago spp. and grain legumes to provide a better understanding of the nature of both resistance and susceptibility to necrotrophic fungal pathogens.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONNECROTROPHIC PATHOGENSHOST RESISTANCE TO NECROTROPHIC...MEDICAGO TRUNCATULA: THE FIRST...CONCLUSIONSLITERATURE CITED |
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Host resistance clearly offers the best strategy for cost-effective, long-term control of nectrotrophic foliar and soil-borne pathogens, particularly as useful resistance to a number of these diseases has been identified in annual Medicago germplasm collections. Previously, Arabidopsis had been the most valuable model plant to work on genetics and physiology of various aspects of plant biology, including host–pathogen relationships. However, recently and initially, the annual plant Medicago truncatula has emerged as a more appropriate and agronomically relevant substitute as a model plant for legumes. Because it is both a host of foliar and soil-borne fungal necrotrophic pathogens of numerous Medicago spp. in addition to several necrotrophic fungal pathogens of other grain legumes, M. truncatula is proving an excellent model upon which to dissect and to understand the mechanisms of resistance to necrotrophic pathogens of legumes in general. For example, the genetic and genomic resources now available in relation to M. truncatula will boost genetic analyses in grain legume species and therefore contribute to improved understanding of the structure and function of host resistance genes in relation to necrotrophic fungal pathogens across forage and grain legumes.
Important reasons for annual Medicago spp. proving to be ideal model crops include the following. First, these species are at the ‘meeting point’ between the model plant M. truncatula, other annual Medicago spp., perennial M. sativa and various grain legumes species, with several necrotrophic fungal pathogens able to attack more than one of annual or perennial Medicago and grain legume species (e.g. A. euteiches, C. trifolii and P. medicaginis). Secondly, genetic studies undertaken in relation to identification of resistance genes to fungal necrotrophic pathogens can be easily transferred to M. truncatula not only from other annual or perennial Medicago spp., but also from grain legumes. Parallel approaches can now be undertaken across both annual and perennial Medicago species and grain legumes to provide better understanding of the nature of resistance, particularly for related necrotrophic fungal pathogens such as P. medicaginis and My. pinodes, the former a pathogen on annual and perennial Medicago spp. and pea, the latter a pathogen only on pea. In future, closer consideration of the common links between M. truncatula, other annual and perennial Medicago spp., and other grain legumes will not only enable wider application of genetic and genomic approaches to be undertaken on legumes, but also hasten transfer of relevant knowledge on necrotrophic pathogens between Medicago as the model genus, M. truncatula as the model plant and grain legumes. For example, improved understanding of key plant–pathogen interactions has already been demonstrated in relation to resistance against A. euteiches and C. trifolii. Clearly, modelling of host–pathogen interactions in annual Medicago spp., including M. truncatula, will greatly improve our understanding of the nature of both resistance and susceptibility to necrotrophic fungal pathogens across forage and grain legumes. This will undoubtedly help in the development of new forms of resistance in legumes to a variety of necrotrophic pathogens.
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TOPABSTRACTINTRODUCTIONNECROTROPHIC PATHOGENSHOST RESISTANCE TO NECROTROPHIC...MEDICAGO TRUNCATULA: THE FIRST...CONCLUSIONSLITERATURE CITED |
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