Rice

2.3.2.1 Introduction

Rice (Oryza sativa L) belongs to the Graminae family and as a cereal grain is the most important food resource for a large part of the world's population. As with maize, rice is grown in most tropical and subtropical regions. Rice is grown in 114 countries throughout the world in Asia, Africa, Central and South America and Northern Australia. Asia accounts for 90% of world rice production with China, India, Indonesia, Bangladesh and Vietnam the five highest rice-producing countries (FAO 2008; Tables 2.1 and 2.3).

There are different systems of cultivating rice that have evolved to suit specific environments, including irrigated, rainfed lowland, deepwater, tidal wetlands and upland. Irrigated rice is the dominant growing system in the world. Plant parasitic nematodes have adapted to each cultivation system with both foliar and root parasites being important.

2.3.2.2 Economic Importance and Distribution

Parasitic nematodes on rice can be divided into two groups: the foliar parasites and the root parasites. The foliar parasites include two well known species. Aph-elenchoides besseyi Christie, 1942 the causal agent of 'white tip disease' in rice is widely spread throughout the rice growing areas of the world. A. besseyi is seed borne in rice and hence the infested seed acts as a primary source of infestation. The characteristic symptom caused by A. besseyi in rice is a whitening of the leaf tip that turns to necrosis, there is also distortion of the flag leaf that encloses the panicle. Infected plants are stunted, have reduced vigour and their panicles contain small and distorted grain (Ou 1985). Two other species, A. nechaleos and A. paranecha-leos have been reported from rice stems in Sierra Leone and Vietnam. Both have a similar morphology and biology to A. besseyi (Hooper and Ibrahim 1994; Ibrahim et al. 1994). However, both species show marked differences in their pathogenicity to rice and the inconsistencies observed in the damage caused by A. besseyi to rice might be due to incorrect nematode identification (Ibrahim et al. 1994). The economic damage threshold density was determined to be 300 live nematodes per 100 seeds (cited by Bridge et al. 2005). Yield losses of up to 60% due to A. besseyi have been widely reported from various infested regions (Bridge et al. 2005). Such high losses are probably rare as the disease is now easily controlled by seed treatment and resistant cultivars (Whitehead 1998).

The other major foliar nematode pest in rice is Ditylenchus angustus, which is mostly limited to the south and southeast of Asia where deepwater and lowland cultivation systems are used (Table 2.3). Although it has been suggested that D. angustus cannot survive severe desiccation (Ibrahim and Perry 1993; Sein 1977), a recent survey indicated the recovery of live nematodes from dried seeds three months after harvest, mainly located in the germ portion (Prasad and Varaprasad 2002). This finding emphasises the importance of seed (and nematode) exchanges between different regions as a source of infection. D. angustus causes 'ufra' disease in rice and the most prominent symptoms of infected plants are chlorosis, twisted leaves and swollen lower nodes. Infected panicles are usually crinkled with empty, shrivelled glumes, especially at their bases, the panicle head and flag leaf are twisted and distorted (Bridge et al. 2005). The annual yield loss due to D. angustus has been estimated at 4% in Bangladesh (Catling et al. 1979) and 10-30% in Assam and West Bengal, India (Rao et al. 1986). However, the importance of D. angustus has reduced as the area sown to deep-water rice has declined (Plowright et al. 2002).

Nematode parasites of rice root systems include migratory endoparasites, sedentary endoparasites (cyst and root knot nematodes) and ectoparasites. Many species of Hirschmanniella, known as the rice root nematodes, have been reported from the majority of rice growing regions which are irrigated, lowland and deep water rice. Seven species are reported to damage rice, with the most commonly reported species being H. oryzae. The symptoms caused by Hirschmanniella species are not specific and include poor growth, leaf chlorosis, reduction of tillering and yield. Nematodes invade roots and migrate through the cortical tissues causing cell necrosis and cavities with infected roots, which turn brown and rot. The crop losses due to Hirschmanniella spp. have been estimated at 25% (Hollis and Keoboonrueng 1984).

Four cyst nematodes species are known to affect rice; Heterodera oryzicola, H. elachista, H. oryzae and H. sacchari on upland, lowland and flooded rice in Japan, India, West Africa and Iran. As with Hirschmaniella the infected plants show reduced growth, chlorosis, fewer tillers and a reduction in root growth. The crop losses due to cyst nematodes have been documented by Bridge et al. (2005), H. ela-chista decreases yield by 7-19% and even higher yield losses have been attributed to H. oryzicola in India. In Côte d'Ivoire increasing H. sacchari populations are expanding rapidly with intensive wet season rice cropping, leading to yield losses of up to 50% (Bridge et al. 2005).

Although several species of root knot nematodes have been reported on rice, the key species is M. graminicola which is mainly distributed in South and South East Asia. This species has also been reported from the USA and some parts of South America (Table 2.2). M. graminicola causes damage to upland, lowland, deepwater and irrigated rice. The most prominent symptoms of M. graminicola on the root system are swollen and hooked root tips which are characteristic for M. graminicola and M. oryzae (Bridge et al. 2005). Typical above ground symptoms include stunting and chlorosis leading to reduced tillers and yield. The effects of M. graminicola on grain yield in upland rice has been estimated at 2.6% for every 1,000 nematodes present around young seedlings (Rao and Biswas 1973). The tolerance limit of seedlings has been determined as less than one second stage juvenile/cm3 of soil in flooded rice (Plowright and Bridge 1990).

2.3.2.3 Major Methods of Control

Using clean seed is the most effective means of preventing yield loss due to A. besseyi. Fumigating seed with methyl bromide, gamma radiation, seed dressing with effective nematicides, hot water or chemical seed treatment are the most useful methods for reducing crop losses. There are many reports on seed treatment of rice by hot water but the most effective control requires pre-soaking seed in cold water for 18-24 h followed by immersion in water at 51-53°C for 15 min (Bridge et al. 2005). Using resistant or tolerant cultivars and low seed planting densities are other control measures for reducing the crop losses due to A. besseyi.

There are many different methods to control 'ufra' disease in rice caused by D. angustus. These include destroying or removing the infested stubble or straw, burying crop residues, growing non-host crops such as jute or mustard in rotation with rice, using early maturing cultivars, removing weed hosts and wild rice to prevent the build up of nematodes for the next crop and improving water management to prevent spread of the nematodes. There are good sources of resistance to D. angustus and advanced generation breeding material is available for development of resistant cultivars suitable for lowland and deep-water environments (Plowright et al. 2002).

Management of Hirschmanniella spp. comprises various methods including soil solarisation, fallow, weed control, use of resistant cultivars and rotation with non host plants (Bridge et al. 2005). For H. sacchari, there are good sources of resistance in the African rice O. glaberrima. Flooding of soil reduces the population density of this nematode. Soil solarization and use of resistant cultivars are the main methods used for control of root knot nematodes in rice cultivation (Whitehead 1998).

2.3.3 Wheat 2.3.3.1 Introduction

Wheat (T. aestivum and T. durum) is the third largest cereal staple with production of 633Mt each year. The three largest producers are China, India and the USA (Table 2.1). It is considered the key crop of importance for food security in the regions of West Asia and North Africa. This section will focus on the primary nematodes of global economic importance on wheat: Cereal Cyst Nematode (Heterodera) and Root Lesion Nematode (Pratylenchus). Other important nematode genera including Root Knot (Meloidogyne), Stem (Ditylenchus) and Seed Gall (Anguina) will not be described here. However, further information on all these nematodes can be found in the reviews of Kort (1972), Griffin (1984), Sikora (1988), Swarup and Sosa-Moss (1990), Rivoal and Cook (1993), Nicol (2002) and McDonald and Nicol (2005), Nicol and Rivoal (2007) and Riley et al. (2009).

2.3.3.2 Economic Importance and Distribution

The most globally recognized and economically important nematode on wheat is the Cereal Cyst Nematode (CCN). The CCN complex is represented by a group of twelve valid and several undescribed species. Three main species, Heterodera avenae, H. filipjevi and H. latipons, are thought to be the most economically important. One of the complexities of the CCN is the presence of pathotypes, making the use of genetic control challenging. The above ground symptoms caused by CCN occur early in the season as pale green patches, which may vary in size from 1 to more than 100 m2, with the lower leaves of the plant being yellow and in which plants generally have few tillers. The symptoms can easily be confused with nitrogen deficiency or poor soils and the root damage caused by CCN exacerbates the effect of any other abiotic stress, e.g. water or nutrient stress. The below ground symptoms may vary depending on the host. Wheat attacked by H. avenae shows increased root production such that roots have a 'bushy-knotted' appearance, usually with several females visible at each root. The cysts are glistening white-grey initially and dark brown when mature. Root symptoms are recognisable within one to two months after sowing in Mediterranean environments and often later in more or less temperate climates (Tables 2.1 and 2.3).

As reviewed by Nicol and Rivoal (2007), H. avenae is the most widely distributed and damaging species on cereals cultivated in more or less temperate regions. H. avenae has been detected in many countries, including Australia, Canada, South Africa, Japan and most European countries, as well as India, China and several countries within North Africa and Western Asia, including Morocco, Tunisia, Libya and Pakistan, Iran, Turkey, Algeria, Saudi Arabia and Israel. Het-erodera latipons is essentially only Mediterranean in distribution, being found in Syria, Cyprus, Turkey, Iran, Italy and Libya. However, it is also known to occur in Northern Europe, and Bulgaria. Another species with an increasingly wide distribution is H. filipjevi, formerly known as Gotland strain of H. avenae, which appears to be found in more continental climates such as Russia, Tadzhikistan, Sweden, Norway, Turkey, Iran, India, Pacific North West USA and Greece. A relatively new report also decribes this species from Himachal Pradesh in India (SP Bishnoi, pers. com.). There are also several other species of Heterodera reported on wheat but these are not considered to be of major economic importance (Nicol and Rivoal 2007).

In terms of economic importance the review of Nicol and Rivoal (2007) provides a long list of published yield loss studies. Interpretation of the damage threshold between specific nematological studies should be done with extreme caution, as very few studies are truly comparable, with inherent differences in sampling protocol, extraction procedure and nematode quantification. Several authors have reported that water stress is one of the key environmental conditions that can exacerbate damage caused. Yield losses due to H. avenae on wheat are reported to be 15-20% in Pakistan, 40-92% in Saudi Arabia, 23-50% in Australia, 24% in the Pacific North West of the USA and 26-96% in Tunisia. It has been calculated that H. avenae is responsible for annual yield losses of 3 million pounds sterling in Europe and 72 million Australian dollars in Australia (Wallace 1965; Brown 1981). The losses in Australia are now greatly reduced due to their control with resistant and tolerant cultivars.

Little is known about the economic importance of the species H. latipons. As reviewed by Nicol and Rivoal (2007) there is one report from Cyprus on barley that indicated 50% yield loss. Recent studies in Iran in field microplots reported yield losses of up to 55% on winter wheat (Hajihasani et al. in press). Because the cysts of H. avenae and H. latipons are similar in size and shape it is possible that damage caused by this recently described nematode species has previously been attributed to H. avenae (Kort 1972). Similarly, H. filipjevi is most likely an economically important nematode on cereals due to its widespread distribution but has previously been misidentified as H. avenae in the former USSR and Sweden. In Turkey significant yield losses (average 42%) in several rainfed winter wheat locations have been reported. In Iran under microplot field trials yield losses of 48% were found on common winter wheat over two wheat seasons (Hajihasani et al. 2010). Natural field trials conducted over several seasons have clearly indicated greater losses under drought conditions. Given increased recognition and incidence, H. filipjevi and H. latipons are now being identified as a constraint to cereal production (Philis 1988; Ozturk et al. 2000; Scholz 2001).

The second group of nematodes considered economically important on wheat production systems is the migratory endoparasitic genus Pratylenchus. At least eight species infect small grains and the four most important species P. thornei, P. neglectus, P. penetrans and P. crenatus are polyphagous and have a worldwide distribution (Rivoal and Cook 1993). P. thornei is the most extensively studied of these species on wheat and has been found in Syria, Yugoslavia, Mexico, Australia, Canada, Israel, Iran, Morocco, Tunisia, Turkey, Pakistan, India, Algeria, Italy and the USA (Nicol and Rivoal 2007). P. neglectus has been reported in Australia, North America, Europe, Iran and Turkey while the other species have only been reported from local studies.

In terms of economic importance P. thornei, causes yield losses in wheat from 38 to 85% in Australia, 12-37% in Mexico, 70% in Israel and has also recently been reported to cause losses on wheat in the Pacific North West of the USA. P. neglectus and P. penetrans appear to be less widespread and damaging on cereals compared to P. thornei. In Southern Australia, losses in wheat caused by P. neglectus ranged from 16 to 23% while at sites infested with both P. thornei and P. neglectus yield losses of 56-74% were reported. In North America and Germany, P. neglectus has been shown to be a weak pathogen to cereals. Sikora (1988) identified P. neglectus and P. penetrans in addition to P. thornei on wheat and barley in Northern Africa, and all these as well as P. zeae in Western Asia. Further work is necessary to determine the significance of these species in these regions.

The life cycle of Pratylenchus is variable between species and environment and ranges from 45 to 65 days (Agrios 1988). Eggs are laid in the soil or inside plant roots. The nematode invades the tissues of the plant root, migrating and feeding as it moves. Feeding and migration of Pratylenchus causes destruction of roots, resulting in characteristic dark brown or black lesions on the root surface, hence their name 'lesion' nematodes. Secondary attack by fungi frequently occurs in these lesions. Aboveground symptoms of Pratylenchus on cereals, like other cereal root nematodes are non-specific, with infected plants appearing stunted and unthrifty, sometimes with reduced numbers of tillers and yellowed lower leaves.

2.3.3.3 Major Methods of Control

The major method of control for both Cereal Cyst Nematode and Root Lesion Nematode is the use of non-hosts in rotation with wheat and also genetic host resistance. Since CCN is host specific, rotation with non-cereals offers good potential to reduce nematode density. However, as Pratylenchus is largely polyphagous, rotational options for these nematodes are far fewer (Nicol and Rivoal 2007). Successful use of rotation requires a thorough understanding of the effectiveness of a particular rotation and, in the case of Pratylenchus, a clear understanding of the host status of the other plants used in the rotation.

Resistance is one of the most cost effective and straightforward methods for nematode control. Many sources have been reported and reviewed for CCN and Pratylenchus (Nicol and Rivoal 2007). Genetic resistance is favoured with the addition of genetic tolerance (the ability of the plant to yield despite attack by the nematode). The progress in understanding and locating resistance sources in cereals is more advanced for cyst (H. avenae) than lesion (Pratylenchus spp.) nematodes, in part due to the specific host-parasite relationship that cyst nematodes form with their hosts (Cook and Evans 1987). In contrast, the relationship of migratory lesion nematodes with their hosts is less specialized and therefore less likely to follow a gene for gene model. The identified sources of resistance to H. avenae have been found predominantly in wild relatives of wheat in the Aegil-ops genus and have already been introgressed into hexaploid wheat backgrounds for breeding purposes. Unlike cereal cyst nematode, no commercially available sources of cereal resistance are available to P. thornei, although sources of tolerance have been used by cereal farmers in Northern Australia for several years (Thompson and Haak 1997).

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