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1 Cyst Nematodes – Life Cycle and Economic Importance 1 Cyst Nematodes – Life Cycle and Economic Importance Maurice Moens1,2, Roland N. Perry2,3 and John T. Jones2,4,5 1Flanders Research Institute for Agriculture, Fisheries and Food, Merelbeke, Belgium; 2Ghent University, Ghent, Belgium; 3University of Hertfordshire, Hatfield, Hertfordshire, UK; 4The James Hutton Institute, Invergowrie, Dundee, UK; 5University of St Andrews, St Andrews, UK 1.1 Introduction 1 1.2 Impact 2 1.3 History of the Genus 2 1.4 Distribution 3 1.5 Identification 3 1.6 Life Cycle 4 1.7 Syncytium 7 1.8 Effect of Abiotic Factors 8 1.9 Important Species 8 1.10 Pathotypes and Races 13 1.11 Symptoms 14 1.12 Management 17 1.13 References 18 1.1 Introduction Vittatidera (Subbotin et al., 2010a, b). However, not all genera of the Heteroderinae are cyst Cyst nematodes are remarkable parasites. They forming; for example, Atalodera, Bellodera, Meloi- have highly specialized interactions with plants dodera and Verutus (Evans and Rowe, 1998). and induce the formation of a unique feeding The most economically important species occur structure, the syncytium, within the roots of within the genera Heterodera and Globodera. their hosts. Cyst nematodes are of enormous All cyst nematodes are obligatory endo- economic importance throughout the world and parasites feeding within the roots of their hosts. the various species infect all of the world’s most Following fertilization and production of eggs, important crops (Jones et al., 2013); they also the body wall of the female tans and desiccates. share a unique feature: the ability of the female This generates a long-lasting cyst that holds a to turn her cuticle into a durable, protective cap- large number of embryonated eggs, which can sule for her eggs. Cyst nematodes are classified survive for long periods until a suitable host is within eight genera of the subfamily Heterod- available. This persistence is one of the charac- erinae: Heterodera, Globodera, Cactodera, Dolicho- teristics that explain the economic importance dera, Paradolichodera, Betulodera, Punctodera and of this group. At low nematode densities, © CAB International 2018. Cyst Nematodes (eds R.N. Perry, M. Moens and J.T. Jones) 1 2 M. Moens et al. above-ground symptoms of cyst nematode dam- lifted in 1972 because it was ineffective. It has age may be minimal. When nematode popula- been suggested that the movement of SCN- tions increase, host plants may become stunted infested soil and plant material into new soy- and wilt. These symptoms are often misattrib- bean production areas had already occurred uted to other abiotic factors, such as soil charac- before the quarantine could be established. teristics, mineral nutrition and water availability, or diseases. 1.3 History of the Genus 1.2 Impact Wouts and Baldwin (1998) wrote an excellent review of the taxonomy and identification of the The most damaging species include soybean cyst cyst nematodes, including historical aspects. nematodes (SCN) (Heterodera glycines), potato The following is partly inspired by this review. cyst nematodes (PCN) (including Globodera palli- The first cyst-forming nematode was reported by da and G. rostochiensis) and cereal cyst nema- Schacht (1859) from sugar beets that showed todes (CCN) (including Heterodera avenae and poor development. The nematode was later de- H. filipjevi) (Jones et al., 2013). Losses caused by scribed by Schmidt (1871) as Heterodera schachtii these and other cyst nematodes are difficult to in honour of its discoverer. During the years that define. PCN have been estimated to cause losses followed, further cyst nematodes were reported to of 9% of total potato production worldwide cause similar effects on other crops; it was be- (Turner and Subbotin, 2013). SCN are thought lieved that H. schachtii was the causal agent in all to be responsible for losses in excess of US$1.5 of these cases. However, when cyst nematodes billion each year in the USA alone (Chen et al., collected from peas did not infect oats, a well- 2001). Losses caused by CCN largely depend on known host of H. schachtii, it became clear that environmental conditions but may sometimes other cyst-for ming species were involved. Eventu- exceed 90% (Nicol et al., 2011). ally, Liebscher (1892) described the species as In addition to this direct impact on crop H. goettingiana. Based on the host specificity of yield, cyst nematodes also have an indirect effect cyst nematodes, Wollenweber described the po- due to increased costs incurred by growers for tato cyst nematode (G. rostochiensis) and oat cyst their control and due to a reduction of product nematode (H. avenae) in 1923 and 1924, respect- quality. Control of cyst nematodes uses a number ively (Wollenweber, 1923, 1924). All of these spe- of strategies including host resistance, prolonged cies were detected in Europe; H. punctata was the rotation, chemicals, the action of biological first cyst nematode species to be described from antagonists (which may be stimulated through North America (Thorne, 1928). Being unaware solarization) or trap crops (see Chapters 9 and 13, of the description of H. rostochiensis, a species this volume). To reduce potential costs for control, with a spherical cyst, the author considered the quarantine status is assigned to some species. For spherical shape of the cyst the basis of H. punctata. example, PCN, a group of global importance, are In his review of the genus Heterodera, Filipjev native to South America (Plantard et al., 2008; (1934) recognized seven cyst-forming species. Be- Grenier, 2010) from where they were introduced fore restoration of the earlier generic name Meloi- in Europe along with potatoes (Turner and Evans, dogyne by Chitwood (1949), the genus Heterodera 1998). Because of their substantial impact on contained both cyst-forming species of Heterode- potato production and their ease of dissemin- ridae and various root-knot species under the ation, PCN are listed as quarantine nematodes in name H. marioni (Luc, 1986; Moens et al., 2009). many countries around the world (CABI, 2016a; With her monograph on the genus Heterodera, Chapter 7, this volume). The rapid expansion in Franklin (1951) enabled the identification of ten the area of soybean production in the USA that species. However, the host range remained for sev- started in the mid-1900s served to establish a eral years the standard for the identification of huge reservoir of hosts that permitted a simi- Heterodera species. In 1959, Skarbilovich erected larly large increase in SCN (Davis and Tylka, the subgenus Globodera to group the round cyst 2000). A federal quarantine for SCN was estab- nematode species, including the PCN. Later, Behr- lished in 1957; however, the quarantine was ens (1975) raised Globodera to generic level. Cyst Nematodes – Life Cycle and Economic Importance 3 On the basis of solid morphological charac- Africa, New Zealand, Peru, Canada, the Middle ters the former genus Heterodera was eventually East, North Africa and the USA. Heterodera split into the genera Heterodera, Globodera, Punc- latipons is distributed in the Mediterranean re- todera and Cactodera (Wouts and Baldwin, gion, but has also been detected in the former 1998). The genera Dolichodera, Betulodera, Para- Soviet Union, Iran, Japan and Canada. Heterode- dolichodera and Vittatidera (each represented by ra filipjevi was first reported in the Sverdlovsk one species) were added later (Turner and Sub- region (Russia). Later, it was found in the for- botin, 2013). In 2017, eight genera and a total mer Soviet Union, Europe (Norway, Germany, of 121 species are recognized within the cyst Poland, Spain and Sweden), Turkey, Iran, Syria, nematodes (see Chapter 15, this volume). India, Tajikistan and the USA. Heterodera glycines is a major pest of soybean in regions of the USA, particularly semi-arid areas. The nematode has 1.4 Distribution also been found as a pest of soybean outside the USA (e.g. Argentina, Brazil, Colombia, China, For a long time, cyst nematodes were thought to Egypt, Indonesia, Iran, Italy, Japan, Korea, Para- occur only in temperate areas (Luc, 1986) or to guay and the former Soviet Union) (CABI, 2016b). be largely a pest of temperate regions. The first Both H. schachtii and H. trifolii have a cosmo- report of a cyst nematode in a tropical crop was politan distribution. Other species have a rather on sugarcane in Hawaii (Muir and Henderson, limited distribution: H. cajani is restricted to 1926). When Luc (1961) reported two Heterode- India and neighbouring countries (Pakistan and ra species, one from swamp rice in the Ivory Myanmar; CABI, 2016c); H. oryzicola has only Coast and another from sugarcane in the Congo, been identified in India; H. sacchari in several it became clear that cyst nematodes could occur West African countries, India and Pakistan; in the tropics. The species were described as H. sorghi in India and Pakistan; whilst H. zeae has H. oryzae and H. sacchari, respectively. Later, sev- been identified in India, Pakistan, Egypt and the eral other species were described from tropical USA. The patchy distributions of some species crops and weeds (Fourie et al., 2017; Chapter 15, may reflect a restricted presence in a relatively this volume). Their host range may be large (e.g. small geographical area but may also reflect re- H. cajani) or restricted to a small number of plants distribution due to human activities as well as the (e.g. H. sacchari). lack of thorough sampling in some areas. Within the genus Globodera, three species are of major importance: G. pallida, G. rostochien- sis and G. tabacum. They are found worldwide in 1.5 Identification temperate regions or in temperate areas of trop- ical regions where their hosts are grown. The 1.5.1 Traditional identification range of their economically important hosts is restricted to Solanaceae. The genus Heterodera Species of the Heteroderinae share similar contains many more species of economic import- morphology and are often distinguished from ance.
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