Multiple disease resistance in wheat: Need of Today
Pooja Sharma1, R. B. Sharma1*,2, Amit K. Singh3, Rakesh Singh3, Sundeep Kumar3
1: Shri Vankateshwara University Vankateshwara Nagar, Gajraula, J.P. Nagar - 244236 (INDIA)
2: Department of Botany, Saraswati (P.G.) College, Hathras, U.P. (India);
3: National Bureau of Plant Genetic Resources, New Delhi-110012 (INDIA)
*: Visiting Professor, Shri Vankateshwara University Vankateshwara Nagar, Gajraula, J.P. Nagar - 244236 (INDIA)
Corresponding author: Pooja Sharma
E-mail: pooja_genome@rediffmail.com
Wheat as staple food of about 35% world population is facing difficulty due to growing problem of multiple biotic stresses under changing climate scenario. Leaf rust, stem rust and spot blotch are the major biotic stresses of wheat (Triticum aestivum L.). According to Park (2007), leaf rust alone can cause up to 60% yield losses while stem rust can cause 100% yield losses in severe conditions. The losses due to rusts can be large and can vary from year to year and region to region (Sawhney, 1995). The average yield losses due to leaf blight (Spot blotch) is about 20% in India (Joshi et al., 2004) however, it may be up to 80% under heavy infection (Joshi et al., 2007). Therefore, development of resistant varieties for single disease is not enough to save plant product and to feed growing population of the world. These all diseases together toll heavy yield losses and put us in the situation to redesign our strategies to fulfill our requirements. The majority of currently grown wheat varieties are susceptible to these diseases, presumably because of high pathogenic variability occurring in these fungi and narrow genetic base for resistance in currently available wheat varieties. Characterization of our existing germplasm for multiple disease resistance varieties may be a vital option in this regard. The grown varieties on the market do carry some known disease resistance genes against rusts and low levels of quantitative resistance against spot blotch diseases. However, most of the resistance genes against rusts are already broken down. Information regarding spot blotch resistance is not well documented. In the sustainable agriculture, which is economical both for the farmer and nature, multiple disease resistance is an essential tool against pathogens attack beside cultural practices, like crop rotation (McIntosh, 1998). With the biotrophic fungi like rusts, the only solution is the durable disease resistance.
During the last 50 years, significant improvement in wheat production and productivity was achieved through exploitation of major genes for traits like dwarfness, photoperiod insensitivity and resistance to biotic stresses (Reynolds and Borlaug, 2006). However, a quantitative jump in wheat production and productivity is still needed to feed the fast expanding human population despite of drastic changes in world climatic conditions. The current major challenges in the successful wheat production are increasing heat stress, dwindling water supplies for irrigation, a growing threat of new virulence of diseases such as wheat rusts (yellow, brown, black and stem), spot blotch, continuous adoption of rice-wheat systems on around 11 million hectares, changes in urbanization patterns, and demand for better quality wheat (Joshi et al., 2007).
Leaf rust caused by Puccinia triticina (=P. recondita Roberage ex Desmaz f. sp. tritici Eriks and E. Henn.), stripe rust caused by P. striiformis Westend f. sp. Tritici, stem rust caused by Puccinia graminis f. sp. Tritici.and spot blotch caused by Bipolaris sorokiniana are considered as most significant diseases in almost all part of the world where wheat is grown (Ginkel and Rajaram, 1998; Singh et al., 1995; Joshi et al., 2007). These are most common disease which causes almost 50% yield loss. Although, reported as early as 1940 by Mehta, it has gained importance after Green Revolution (Singh and Rajaram, 1992). A number of rust resistance genes are known to provide complete protection (McIntosh et al., 1995) but due to higher rate of breakdown of resistant genes and their narrow genetic base enhance the wheat cultivars susceptibility to rust disease. An epidemic of stem rust on wheat caused by race TTKSK (e.g. isolate Ug99) is currently spreading across Africa, Asia and the Middle East and is causing major concern due to the large numbers of people dependent on wheat for sustenance. The strain was named after the country where it was identified (Uganda) and the year of its discovery (1999) (Singh et al., 2011). P. graminis is a member of the Phylum Basidiomycota within the Kingdom Fungi. The characteristic rust color on stems and leaves is typical of a general stem rust as well as any variation of this type of fungus. Different from most fungi, the rust variations have five spore stages and alternate between two hosts. Wheat is the primary host and barberry is the alternate host.
New biotic stresses like foliar blight (spot blotch) has also emerged a big constraint for the successful production of wheat in South East Asia (Wiese, 1987; Mathur and Coufer, 1993). Work on the spot blotch was initiated long back (Mishra, 1973) to find the answer of this emerging disease in South-Asia. Variation in the pathogen population and aggressiveness which increase over time are the major concerns in case of spot blotch (Chand et al., 2003). Numerous, breeding programs have been under taken to understand the nature of resistance and incorporation of resistance in to commercial cultivars (Adalkha et al., 1984). However, resistance to spot blotch in the commonly grown wheat cultivars of South East Asia is generally unsatisfactory (Joshi et al., 2004). This disease is now expending towards non-traditional cooler regions like North West Plain Zone (NWPZ) of India, which is considered as major contributor of wheat in South Asia. The available literature covering various aspects falling under the scope of the present study is being detailed as under:
Host range of pathogen
Wheat, barley, triticale, and a few related species are the primary hosts for leaf rust (Puccinia recondita), stem rust (P. graminis f.sp. tritici) and spot blotch (Bipolaris sorokiniana). The primary alternate host in nature has been Berberis vulgaris L., a species native to Europe, although other species have been susceptible in greenhouse tests in case of rusts while, spot blotch appears on host species and survives in soil on crop residues during non-crop season. Sprague (1950) reported that B. sorokiniana has a large host range and almost all the plants belonging to family Poaceae come under its host range. Apart from wheat, it infects oat, barley, rye, Phylaris, Agropyron, Pennisetumm, Lollium, Poae, Secale, Setaria etc. (Bakonyi et al., 1998).
Survival
Weather conditions and age of the plants during late October till December are quite favorable for infection by rust fungi. However, in north India initial outbreaks of rust are delayed by 2-3 months, in case of leaf rust. This suggests that there is no local source of primary inoculum of any of the rust of wheat. In the plains of north India due to prevailing high temperatures after harvest of wheat crop, during the summer months, the urediospores and teliospores of the fungus are killed. Leaf rust may survives between crops as mycelium or as uredinia on infected volunteer and/or on early sown and late maturing wheat crops or native grasses until a fresh crop of wheat is available (Chester, 1946; Eversmeyer and Kramer, 2000). Like other Puccinia species, P. graminis is an obligate biotroph and has a complex life cycle featuring alternation of generations. The fungus is heteroecious, requiring two hosts to complete its life cycle - the cereal host and the alternate host (Schumann et al., 2011). There are many species in Berberis and Mahonia that are susceptible to stem rust, but the common barberry is considered to be the most important alternate host (Singh et al., 2008) P. graminis is macrocyclic (exhibits all five of the spore types that are known for rust fungi (Schumann et al., 2011). The pathogen can survive almost any condition the host leaf can survive (Mehta, 1940). In case of spot blotch, a humid cloudy weather condition favours the survival and spread of disease (Chaurasia et al., 1999).
Occurrence
There are several areas worldwide in which each of the rusts can cause severe losses (Saari and Prescott, 1985). Puccinia triticina can survive the same environmental conditions that the wheat leaf survives, provided infection but no sporulation has occurred. The fungus can infect with dew periods of three hours or less at temperatures of about 20oC, however, more infections occur with longer dew periods. At cooler temperatures, longer dew periods are required, for example, at 10oC a 12 hours dew period is necessary. Few if any infections occur where dew period temperatures are above 32oC (Stubbs et al., 1986) or below 2oC. Once the leaf has become infected, temperature dictates the incubation period (Hogg et al., 1966; Eversmeyer et al., 1980). The epidemiology of P. graminis is similar to P. triticina.
Spot blotch is a disease of importance mainly in warm, humid wheat growing Mega environment (ME-5) where the mean temperature of the coolest month is higher than 17.5oC (Dubin et al., 1998). It causes serious yield losses to wheat crop in India (Joshi et al., 2002), South East Asia (Saari, 1998), North and Latin America, Africa (Duczek and Jones-Flors, 1993), China (Chang and Wn, 1998) and Brazil (Mehta, 1993). More recently, spot blotch has also expended into the cooler, non-traditional irrigated rice-wheat production areas (ME-1) (Dubin and Ginkel, 1991; Duveiller and Gilchrist, 1994; Ginkel and Rajaram, 1998).
Inoculum Source and Infection
The main methods of inoculation include: dusting or brushing with dry spores, with or without a carrier such as talc or spores of the club moss Lycopodium; spraying with water or isoparaffinic oil-based suspensions; or plant tissue injection using water-based suspensions. Inoculation by uredinia involves regional transport of urediniospores by wind (Hirst and Hurst, 1967; Watson and de Sousa, 1983), may introduce a new virulent race in an area, but probably seldom results in a severe epidemic that season except on the most susceptible cultivars. Aeciospores from the alternate host (sexual) rarely result in an epidemic. The urediospores of Puccinia triticina are brown and spherical, 16-28 microns in diameter and with a minutely echinulate wall furnished with 7-10 germ pores. Infection by germ tubes from urediospores occurs through stomata on either side of the leaf. The germination process requires moisture, and works best at 100% humidity. Optimum temperature for germination is between 15oC-20oC. Before sporulation, wheat plants appear completely asymtomatic. This is because rust pathogens are biotrophic and require living plant cell to survive.
In case of spot blotch, isolates having dark green to green colour were highly sporulating, while those with grey to white colour were poor in sporulation (Chand et al., 2003). Duczek et al. (1996) reported that sporulation of Bipolaris sorokiniana varied from year to year. They observed production of conidia of Bipolaris sorokiniana on the crowns of field grown annual crops; sporulation was highest in crown region of wheat and other grasses.
Symptoms
Rust fungi all produce similar disease symptoms on the host plants and have similar requirements for infection. The diseases get their name from their appearance on the plant. Infection can occur on any above-ground plant part, leading to the production of pustules that contain thousands of dry yellow-orange to reddish-brown or black spores. These pustules give the appearance of “rust” on the plant.
Stem rust occurs primarily on stems but can also be found on leaves, sheaths, glumes, awns and even seed. Symptoms begin as oval to elongate lesions that are generally reddish-brown in color. In the late stages of the disease, erumpent pustules produce numerous black sooty spores. Severe infestations with many stem lesions may weaken plant stems and result in lodging.
Leaf rust is generally found on leaves but may also infect glumes and awns. Symptoms begin as small, circular to oval yellow spots on infected tissue of the upper leaf surface. As the disease progresses, the spots develop into orange colored pustules which may be surrounded by a yellow halo. The pustules produce a large number of spores that are easily dislodged from the pustule resulting in an “orange dust” on the leaf surface or on clothes, hands and equipment. As the disease progresses, black spores may be produced resulting in a mixture of orange and black lesions on the same leaf. Tiny orange lesions may be present on seed heads, but these lesions do not develop into erumpent pustules. This difference helps to distinguish leaf rust from stem rust.
The symptoms of spot blotch appear as small, light brown lesions which are scattered throughout the leaves and increase in size with stage advancement. Later, these lesions coalesce and change to large spots after a week of infection. These spot are of different size and shape (oval to oblong and measuring 0.5 to 10 mm long and 3 to 5 mm wide). Symptoms of spot blotch are also commonly noticed on leaf, sheath, nodes and glumes (Chand et al., 2002).
Yield Loss
Stakman et al. (1962) note that leaf and stripe rust generally do not cause the same level of yield damage as stem rust. However, both typically can become as epidemic as stem rust, and each may cause greater annual damage then stem rust in certain areas. Traditionally, stripe rust is likely to be most destructive in cool, moist seasons; stem and leaf rusts are likely to be most destructive in warm, moist seasons. However, this appears to be changing. In recent years new, higher temperature tolerant, aggressive strains of stripe rust are moving into non-traditional, warmer areas (Hovmøller and Henriksen, 2008; Milus et al., 2009). Hanson et al. (1982) provided a summary of the impacts of rust diseases in developing countries and identified the hot spots for each of the rusts. Table 1 indicates that stem and stripe rusts are more destructive in an epidemic, but that leaf rust is more significant endemically.
Yield losses caused by the spot blotch disease are conciderable in South Asia (Dubin and Ginkel, 1991). Saari (1998) reviewed the losses reported for the wheat leaf blight diseases and concluded that average loss due to leaf blight in South Asia was 19.6% (Table 1).
Genetics of resistance
(a) Rust resistance
A complete study of wheat rust genetics demands the genetics of both host and pathogen. Although genetics of the rust pathogens is difficult to study, the genetics of the host (wheat) can be studied from the interaction between host and pathogen which produce incompatible (resistance) and compatible (susceptible) reactions. Majority of already designated stem rust resistance genes are of dominant nature and under monogenic control (McIntosh et al., 1995). In Wheat (Triticum spp.) and leaf rust (Puccinia recondite f. sp. tritici) interaction, additive type of gene action have been reported (Singh et al., 1998). Studies with combining ability analysis expressed both additive and non additive gene effects for resistance to leaf rust in wheat (Chawla et al., 1990). Singh et al. (2004, 2005) also reported two to five more genes for leaf rust and stripe rust resistance from many cultivars in addition to Lr34 and Yr18 that are contributing towards their durable resistance.
(b) Spot blotch resistance
Efforts have been made to reveal the inheritance of resistance to spot blotch. According to Velazquez Cruz (1994), inheritance of spot blotch seems to be polygenic with additive effect. Kumar et al. (2007) reported the involvement of two to three genes in the resistance mechanism of spot blotch. This is in accordance with the previous reports based on Indian wheat genotypes where one or two genes control was reported (Srivastava et al., 1971; Srivastava, 1982; Adlakha et al., 1984). However, these studies did not go beyond F2 generation and utilized limited population size. Further, that time spot blotch was not an important disease of Indian sub-continent and effective pathotypes were also not available for characterization. Later, Joshi et al. (2004) reported the involvement of three genes having additive effect in resistance sources viz., Mon/Ald, Acc. 8206 and Suzhoe-8 based on advanced segregating generations and big size populations.
The heritability estimates for these crosses were of moderate type ranging from 0.65 to 0.8. Sharma et al. (2007) and Joshi et al. (2004) also reported moderate range of heritability with respect to spot blotch resistance. According to Joshi et al. (2004) by creating effective afrificial epiphytotic conditions and proper disease severity recording taking care of the growth stages, environmental effect could be minimized thus, higher estimates of heritability can be obtained.
The evaluation of large number of genotypes (aestivum and durum) and triticale over the year has clearly established that majority of the durum (AB genome) genotypes are highly susceptible to leaf blight pathogen. On the other hand, the aestivum (ABD genomes) genotypes fall under the category of susceptible to moderately resistant. Most of the triticales (ABR genome) seem to be moderately resistant to resistant. These data indicated that in aestivum wheat, resistance is probably located on D genome and in case of triticale on the R genome (Chand et al., 2002).
Breeding progress for multiple disease resistance
It is assumed that resistant genes effective against prevailing races of a particular region, the chances of yield losses is lesser than those varieties which are not carrying these resistance genes. Chances of out breakage of varieties are more if only one or two resistance genes are present. Enhanced resistance can be achieved by adding some other resistance genes in addition to the existing one. Incorporation of 3-4 prominent resistant genes conferring resistance against leaf and stem rusts and spot blotch diseases chances of out breakage of disease is low and the duration of efficient resistance can be increased and multiple disease resistance can be achieved (Singh et al., 2000)
Rust pathogens can mutate to overcome the existing resistant genes. Therefore, breeding for rust resistance needs to focus on maintaining current levels of resistance and on developing new and improved sources of resistance. The maintenance of rust resistance involves a continuing search for, and development of, new forms or combinations of resistance, to ensure that the varieties in farmers’ fields have effective genetic resistance against the current strains of the pathogens. To ensure that rust does not cause economic losses, breeders need to have an understanding of cultivar susceptibility, the rust pathogens and a sense of the resistance genes available for use.
To achieve this, three or four lines carrying different minor genes were crossed (3-way and 4-way crosses), and plants in large segregating populations were selected under artificially created rust epidemics. Races of pathogens that have virulence for race-specific resistance genes present in the parents were used to create the epidemics (Singh et al., 2000). The experience of breeders to achieve partial resistance in breeding populations (Dubin and Ginkel, 1991; Duveiller and Gilchirst, 1994; Dubin and Rajaram, 1996) suggested polygenic type of resistance. Breeding for durable resistance based on minor additive genes has been challenging and often slow, for several reasons:
1) A sufficient number of minor genes may not be present in a single source genotype,
2) A source genotype may be poorly adapted,
3) There may be confounding effects from the segregation of both major and minor genes in the population,
4) Crossing and selection schemes and population sizes are more suitable for selecting major genes,
5) Reliable molecular markers for several minor genes are unavailable, and
6) The cost associated with identifying and utilizing multiple markers, is high.
However, such germplasm carrying combinations of minor genes should be very useful in transferring these genes to adapted local cultivars.
Availability for tightly linked DNA markers in the future can be useful in maintaining and diversifying the combinations of additive slow rusting resistance genes in the wheat germplasm and cultivars (Sareen et al., 2012). The actual use of multiple markers in breeding strategy at CIMMYT is likely be limited to the characterization and selection of parents to be used in specific crosses as the field screening is very reliable and cost-effective. However, if such genes need to be incorporated in adapted cultivar that contains an effective race-specific resistance gene, then markers are the only option and will be used despite the cost.
Molecular tools in achieving multiple disease resistance
Molecular tools have opened up new dimensions in the area of crop improvement. In condition of the availability of linked molecular markers, an effective selection strategy can be made for the development of multiple disease resistance varieties. Once, markers are established for different resistant genes conferring resistance against multiple diseases, these markers can be used in selecting multiple disease resistant varieties through marker assisted selection (MAS). There are number of varieties which are not currently being grown due to their susceptibility however, having good in quality and production, can be improved further, through intensive crossing program which following marker assisted selection. The association of leaf tip necrosis with Lr34/Yr18 genes was established by Singh et al. (2000). Later, Joshi et al. (2004) established the linkage of leaf tip necrosis with spot blotch resistance. In addition, stay green trait was also showed positive linkage with spot blotch resistance (Joshi et al., 2007). These morphological markers are successfully being used in markers assisted selection of spot blotch resistance germplasm lines.
Number of molecular markers linked to leaf and stem rusts resistance genes/QTLs have been identified in wheat (Singh et al., 2011). As far as stem rust is concerned, some of them arose in bread wheat (e.g. Sr5 and Sr6), while others have been bred in from other wheat species (e.g. Sr21 from T. monococcum) or from other members of the tribe Triticeae (e.g. Sr31 from rye and Sr44 from Thinopyrum intermedium). None of the Sr genes provide resistance to all races of stem rust. For instance many of them are ineffective against the Ug99 lineage (Singh et al., 2011). Notably Ug99 has virulence against Sr31, which was effective against all previous stem rust races (Singh et al., 2011).
A sequence-tagged-site (STS) marker is reported linked to Lr28, a leaf rust resistance gene in wheat. RAPD (random amplified polymorphic DNA) analysis of near-isogenic lines (NILs) of Lr28 in eight varietal backgrounds was carried out using random primers. Ten microsatellite sequences were found, and three of them were polymorphic in our population and were genetically mapped close to Lr34. Therefore, SWM10 is a highly useful marker to assist selection for Lr34 in breeding programs worldwide (Bossolini et al., 2006). Molecular markers are expected to make an increasing impact on our ability to select gene combinations needed to enhance the durability of resistance. Advances in molecular plant pathology, however, have made marker assisted selection a routine task. With the help of PCR-based DNA markers, number of leaf and yellow rust, powdery mildew and spot blotch resistance gene(s) can be detected.
Although, many reports of tagging and mapping of several disease resistance genes and QTLs are available in wheat (Langridge et al., 2001) however, not many reports are available for spot blotch. For this disease, the association of resistance with microsatellite markers in bulks of susceptible and resistant progeny lines was reported (Sharma et al., 2007). The QTLs for spot blotch resistance in the Chinese wheat variety, ‘Yangmai 6’ were mapped on chromosome 2A, 2B, 5B and 6D (Kumar et al. 2009). However, more information with respect to the identification of QTLs in different genetic background was generated when QTLs were mapped in two other resistance sources (‘Ning 8201’ and ‘Chirya 3’) and to compare the chromosomal locations of QTLs with ‘Yangmai 6’ to identify diagnostic markers that can be used for marker assisted selection and to make an effective breeding program (Kumar et al., 2010). List of markers reported to be linked with leaf and stem rust and spot blotch resistance genes/QTLs are given in table 2.
Future strategies
Identification of exploited and unexploited resistant gene(s) for each disease and combine them together for the development of multiple pest resistant variety should be the aim of future breeding programs. For this purpose, resistance genes especially those which can provide resistance against prominent races of economically important diseases and where linked markers are available to be used in marker assisted selection (MAS). Characterization of wheat germplasm at pathological level followed by their molecular characterization through linked markers for known resistance genes to leaf & stem rusts and spot blotch would be one of the best possible approaches to combat with the growing problem of biotic stresses in wheat.
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