摘要
小麦禾谷孢囊线虫病(cereal cyst nematode)在我国北方小麦主要产区发生分布十分广泛,对小麦生产构成了潜在的威胁。河南是我国小麦第一生产大省,种植面积和总产量都居国内首位。近年来小麦孢囊线虫病在河南郑州和许昌两地区危害严重,造成了严重的产量损失。为了给该病防控工作提供理论依据,我们对郑州和许昌地区3个禾谷孢囊线虫群体的种类和致病型进行了鉴定,同时对国内外小麦品种及相关资源材料对孢囊线虫郑州和许昌群体的抗性进行了筛选,初步探索了小麦品种抗禾谷孢囊线虫的分子机理。主要研究结果如下:
通过对郑州和许昌小麦孢囊线虫群体的形态鉴定和分子鉴定,明确了郑州和许昌地区小麦孢囊线虫的种类:郑州须水和荥阳两个群体都属于禾谷孢囊线虫组中的燕麦孢囊线虫(Heterodera avenae Wollenweber, 1924),许昌群体属于禾谷孢囊线虫组中的菲利普孢囊线虫〔H.filipjevi(Madzhidov,1981)Stelter,1984〕。小麦孢囊线虫郑州两个群体成熟孢囊柠檬形,褐色至黑褐色。颈较长,阴门锥显著。阴门膜孔为双膜孔,卵圆形,有阴门桥,但没有下桥。尾锥内不规则分布着大量褐色泡状突。二龄幼虫蠕虫形,口针粗壮,口针基部球锚形。中食道球卵圆形。尾圆锥形,有较长的透明尾。许昌群体成熟孢囊褐色,柠檬形,头部与尾部明显。头部有颈,尾部有尾锥。阴门膜孔为双膜孔,马蹄形。有阴门桥和下桥结构。尾锥内不规则分布着褐色泡状突,泡状突较郑州的两个群体少。二龄幼虫蠕虫形,口针粗壮,口针基部球锚形。中食道球卵圆形。尾圆锥形,有较长的透明尾。
扩增郑州和许昌3个小麦孢囊线虫群体核糖体DNA的ITS区,PCR产物都产生1条大小约为980bp的片段。用TaqⅠ、AluⅠ、HaeⅢ、HinfⅠ、RsaⅠ、PstⅠ、CfoⅠ、Tru9Ⅰ等8种限制性内切酶酶切3个群体的rDNA–ITS–PCR产物,结果表明,郑州须水和荥阳两个群体的酶切图谱相同,它们的ITS属于“B”型;许昌群体的酶切图谱与已报道H. filipjevi的酶切图谱一致;TaqⅠ酶与PstⅠ酶均可将许昌与郑州两地的小麦孢囊线虫区分开来。rDNA-ITS序列聚类分析结果表明,郑州须水和荥阳两个群体的序列与国内过去报道的H.avenae序列亲缘关系较近,与澳大利亚的H. australis序列也有较近的亲缘关系。许昌群体的序列与国外已报道的H. filipjevi序列聚在同一簇。
利用燕麦孢囊线虫致病型国际鉴别寄主对郑州荥阳、须水和许昌3个群体的致病型进行鉴定,结果表明,根据国际鉴别寄主A组的鉴定结果,小麦孢囊线虫荥阳群体与须水群体为同一致病型,它们不同于国际上已命名的13个致病型,与国内已报道的5个燕麦孢囊线虫群体的致病型有较大差异,该致病型与澳大利亚致病型Ha13较为相近。根据致病型命名的原则,郑州地区小麦孢囊线虫应属于第三致病型组,命名为Ha43。
小麦孢囊线虫许昌群体致病型与国际上命名的13个致病型也不相同。小麦孢囊线虫许昌群体致病型与郑州的两个群体存在极大的差异,有5个大麦品种、2个燕麦品种和1个小麦品种对两个群体的反应是不同的。与国内已报道的致病型比较,许昌群体与北京房山和河南新乡群体对国际鉴别寄主的反应是一致的,而与河北定州群体、山西太谷和安徽固镇群体有一定差异。许昌群体致病型与瑞典报道的G(West)有些相近。小麦孢囊线虫郑州两个群体对A组鉴别寄主材料的致病谱大于许昌群体。
采用室内接种和田间病圃鉴定方法测定了黄淮麦区主推小麦品种对小麦孢囊线虫郑州荥阳群体和许昌群体的抗性。结果表明,46个主推小麦品种对荥阳群体的抗性总体较差,多数品种表现为感病(中感、感病或高感),缺乏免疫和高抗品种,只有太空6号、新麦18、中育6号和新麦11等4个品种对燕麦孢囊线虫表现出一定的抗性。对许昌群体的抗性总体表现也较差,室内接种鉴定没有发现抗病品种,全部表现为中感、感病或高感;田间鉴定表现抗病的有中育6号、太空6号、偃展4110、濮麦9号、豫农201、豫农949等6个品种。对来源于CIMMYT的66份小麦品种资源材料和41份小麦近缘材料对小麦孢囊线虫许昌群体或荥阳群体的抗性进行了测定,66份国外小麦品种多数表现感病,6R(6D)、MACKELLER、CP1133842等12个品种表现较好的抗性,具有很好的利用价值。同时,鉴定结果发现,小麦近缘材料中存在着丰富的抗禾谷孢囊线虫资源,三羊草属(Aegilops)、冰草属(Agropyron)、偃麦草属(Elytrigria)、簇毛麦属(Haynaldia)等中的一些材料对H. avenae和H. filipjevi均表现出较好的抗性,在抗禾谷孢囊线虫育种中可加以利用。
以小麦稳定表达的肌动蛋白基因(Actin)为对照,利用半定量RT-PCR技术对接种H.avenae后小麦不同抗性品种、不同时期、不同部位的几丁质酶基因表达进行了分析,结果表明:小麦受到禾谷孢囊线虫侵染后,能够诱导植株体内几丁质酶基因表达的上调,小麦抗、感品种之间几丁质酶基因表达量没有显著差异,说明几丁质酶活性变化不是小麦品种抗禾谷孢囊线虫的主要作用机制。
The cereal cyst nematode (CCN) occurred and distributed widely in the major wheat growing regions which brought a potential menace on the wheat production in China. Henan province was the main wheat production region and its cultivated area and total output of wheat ranked first in China. In recent years, CCN has caused serious yield losses in Zhengzhou and Xuchang, Henan province. In order to provide basis for the disease control, species and pathotypes of CCN from both areas and the resistance of wheat and its relatives to CCN were identified, the disease-resistant mechanism of wheat to Heterodera avenae were preliminarily studied .The main research results presented as follows.
The species of cereal cyst nematode from Zhengzhou (Xingyang population and Xushui population) and Xuchang (Xuchang population) were definited based on morphological and molecular methods. Xingyang population and Xushui population belonged to Heterodera avenae Wollenweber, 1924and Xuchang population belonged to H. filipjevi( ( Madzhidov,1981 )Stelter,1984. The mature cysts of both populations from Zhengzhou were lemon shaped, with colors from brown to dark brown, long neck, vulval cone, bifenestrate, vulval bridge. Cysts of Zhengzhou population didn′t have underbridge and their vulval cone had many bullae, yet the cysts of Xuchang population had underbridge, their vulval cone had less bullae. Second-stage juveniles of three populations were worm-shaped, with stylet of anchor-shaped basal knobs, ovoid oesophageal bulb, conical tail, hyaline tail.
Amplification of the rDNA-ITS region yielded a single PCR fragment of approximately 1000bp for each of the 3 populations. Eight kinds of restriction enzymes, TaqⅠ、AluⅠ、HaeⅢ、HinfⅠ、RsaⅠ、PstⅠ、CfoⅠ、Tru9Ⅰwere used to digest production of rDNA–ITS–PCR. The result showed restriction patterns of Xingyang population and Xushui population were the same, their ITS type were type B.The restriction pattern of Xuchang population was the same as the roports before. Zhengzhou cereal cyst nematode could be separated from Xuchang cereal cyst nematode using restriction enzymes Taq I and Pst I.
Cluster analysis for rDNA-ITS sequence, the populations of Xingyang and Xushui closely related to the herrings and native to the H. avenae populations from China and H.australis from Australia. The populations of Xuchang was clustered with high bootstrap supported with all H. filipjevi reported from foreign countries.
The pathotypes of three populations of cereal cyst nematodes from Zhengzhou and Xuchang were identified using the International Host Differentials (IHD). According to the reactions of IHD (group A) to the nematodes, the pathotypes of both populations from Zhengzhou were the same, but they were different from ones which had been nominated and reported. The pathotype of Zhengzhou populations were similar to Hal3, which was the dominant pathotype in Australia. Accoding to nomenclature, the two populations of Zhengzhou should belong to pathotype group 3, so the pathotype of Zhengzhou populations were named as Ha43.
The pathotype of Xuchang population was different from ones which had been nominated. It was different from the two populations of Zhengzhou. The resistant reaction of five barley, two oats and a wheat cultivars were different. Compared with other pathotypes in China, the pathotype of Xuchang population was the same as Fangshan population in Beijing and Xinxiang population in Henan, with little difference from Dingzhou population in Hebei, Taigu population in Shanxi and Guzhen population in Anhui. The pathogenicity of Zhengzhou populations was stronger than Xuchang population to IHD (group A).
Resistance of main released wheat cultivars in Huanghuai wheat area was tested to H.avenae and H. filipjevi by inoculation in greenhouse or in diseased field. The results indicated that the reactions of 46 cultivars were not good in general for Xingyang population, most of cultivars were susceptible (moderate susceptible, susceptible or high susceptible), immune and high resistant cultivars were lacking, Taikong 6, Xinmai18, Zhongyu6 and Xinmai11 were resistant to H.avenae. Resistance of 46 cultivars was not good in general for Xuchang population, also. There was no resistant cultivars in greenhouse identification and all cultivars were moderate susceptible, susceptible or high susceptible. Six cultivars were resistant to Xuchang population in the field testing, they were Zhongyu6, Zhongyu6, Yanzhan4110, Pumai9, Yunong201 and Yunong949.
The resistance of 66 wheat variety resources providing by CIMMYT and 41 relatives of wheat were tested to H. filipjevi of Xuchang population or H.avenae of Xingyang population. The results showed that 12 wheat cultivars were resistant to H. filipjevi of Xuchang population, for instance, 6R(6D), MACKELLER, CPI 133842, ect. There were abundant resistant resources in the relatives of wheat to cereal cyst nematode. Some materials in Aegilops, Agropyron, Elytrigria, Haynaldia were resistant to H.avenae and H. filipjevi, and they could be utilized in breeding for cereal cyst nematode disease resistance.
Taking wheat Actin gene as a control, expression of wheat chitinase gene 4(Chi4) were analyzed in the different growing periods, in different positions of different resistant wheat cultivars after inoculating H. avenae by semi-quantitative RT-PCR. The results showed that the expression of Chi4 was up-regulated when wheat plants were infected by H. avenae, no matter the cultivar was resistant or susceptible. There was no significant difference for Upregulation of Chi4 between resistant and susceptible cultivars. The change of Chi4 activities was not the principal mechanism for the resistance of wheat to cereal cyst nematode.
引文
1.陈品三,王明祖,彭德良.我国小麦禾谷孢囊线虫(Heterodera avenae Wollenweber)鉴定研究.植物病理学报,1992,22(4):339-343.
2.邓洪新,杨小娟,余懋群,等.易变山羊草抗禾谷孢囊线虫基因中核苷酸结合区(NBS)的克隆与序列分析.中国生物化学与分子生物学报,2001,17(6):751-755.
3.段玉玺,陈立杰,远方,等.大豆抗大豆孢囊线虫3号生理小种的抗性机制研究.莱阳学院学报,2004,21(2):118-121.
4.刘维志.植物病原线虫学.北京:中国农业出版社,2000.360-365.
5.蒋选利,李振岐,康振生,等。几丁质酶与植物的抗病性.西北农业学报,2002,11(3):71-75.
6.刘淑霞,徐梅,李海燕,等.几丁质酶活性与大豆对胞囊线虫抗性的关系.黑龙江八一农垦大学学报.2009,21(3):31-34.
7.龙海波,彭德良.小麦抗禾谷孢囊线虫基因研究进展.中国线虫学研究(第三卷),2010,3:224-230.
8.欧师琪,彭德良,李玉,等.河南郑州小麦禾谷孢囊线虫(Heterodera avenae)的核糖体基因ITS序列和RFLP分析.植物病理学报,2008,38(4):407-329.
9.彭德良,Subbotin S., Moens M.小麦禾谷孢囊线虫(Heterodera avenae)的核糖体基因(rDNA)限制性片段长度多态性研究.植物病理学报,2003,33(4):323-329.
10.彭德良,李惠霞,王锡锋,等.我国小麦禾谷孢囊线虫的新发生分布地区.中国线虫学研究(第二卷).北京:中国农业科学技术出版社,2008,2:344-345.
11.王明祖,雷智峰,肖炎农.小麦禾谷孢囊线虫(Heterodera avenae)主要寄主范围的研究.湖北植保,1996,(6):2-3.
12.王明祖,彭德良.小麦禾谷孢囊线虫病的研究I.病原鉴定.华中农业大学学报,1991,10(4):352-356.
13.王振跃,高书峰,李洪连,等.不同小麦品种(系)对禾谷孢囊线虫病的抗性鉴定.河南农业科学,2006,(5):50-52.
14.王振跃,李洪连,袁虹霞.小麦孢囊线虫病的发生危害与防治对策.河南农业科学,2005,(12):54-55.
15.吴海燕,段玉玺.几丁质酶与大豆抗孢囊线虫关系初步研究.植物病理学报.2004,34(6):555-557.
16.谢辉.植物线虫分类学(第二版).北京:高等教育出版社,2005.
17.阎乃红,陈静,余懋群.小麦禾谷孢囊线虫及抗线虫性基因研究进展.麦类作物学报,2003.23(1):90-94.
18.颜清上,王连铮.中国小黑豆抗源对大豆孢囊线虫4号生理小种抗性机制研究.大豆科学,1997,16(1):34-37.
19.叶兴国,程红梅,徐惠君,等.转几丁质酶和β—1,3—葡聚糖酶双价基因小麦的获得和鉴定.作物学报,2005,31(5):583-586.
20.余懋群,田文兰.易变山羊草携抗禾谷类根结线虫基因染色体向普通小麦的转移.西南农业学报,1994,7(3):9-14.
21.袁红旭,许新萍,张建中,等.转几丁质酶基因(RC24)水稻中大2号抗纹枯病特性研究.中国水稻科学,2004,18(1):39-42.
22.翟旭光,余懋群.抗禾谷孢囊线虫基因研究进展.中国线虫学研究(第一卷).北京:中国农业科学技术出版社,2006,1::39-346.
23.郑经武,程瑚瑞,方中达.小麦禾谷孢囊线虫致病型研究.植物病理学报,1997,27:309-314.
24.郑经武,林茂松,程瑚瑞,等.安徽省小麦上两个孢囊线虫群体的鉴定.江苏农业科学,1996,12(1):31-35.
25.郑经武,林茂松,程瑚瑞,等.麦类作物对燕麦孢囊线虫的抗病性.植物保护学报,1999,26:250-255.
26.郑经武.麦类作物对燕麦胞囊线虫抗病性遗传研究进展.沈阳农业大学学报,2001,32(3):224-227.
27.郑经武,林茂松,方中达。寄生麦类作物的孢囊线虫种类、分布及其鉴定特征。植物检疫,1996,10(1):8-11
28. Abidou H.,Valette S., Gauthier J.P., et al. 2005. Molecular polymorphism and morphometrics of species of the Heterodera avenae group in Syria and Turkey. Journal of Nematology, 37: 146-154.
29. Abidou H., Valette S., Gauthier J.P., et al. 2005.Molecular polymorphism and morphometrics of species of the Heterodera avenae group in Syria and Turkey. J. Nematol. 37:146-154.
30. Andersen K., Andersen S.1968. Inheritance of resistance to Heterodera avenae in barley. Nematologica, 14:128-130.
31. Andersen K., Andersen S.1973. Linkage between marker genes on barley chromosome 2 and agene for resistance to Heterodera avenae. Hereditas, 73:271-276.
32. Anderson S., Anderson K. 1982. Suggestions for Determination and Terminology of Pathotypes and Genes for Resistance in Cyst-forming Nematodes, especially Heterodera avenae. EPPO Bull.12(4):379-386
33. Anita Ireholm. 1994. Characterization of pathotypes of cereal cyst nematodes, Heterodera spp.,in Sweden. Nematologica, 40:399-411.
34. Baldwin J.G., and M. Mundo-Ocampo. 1991. Heteroderinae, cyst and non-cyst-forming nematodes. pp. 275–362 in W. R. Nickle, ed. Manual of agricultural nematology. New York: Marcel Dekker.
35. Barker K. R., Noe J. P. 1987. Establishing and using threshold population levels. In J. A. Veech, S. W. Dickson (Eds.), Vistas on Nematology (pp. 75–81). Maryland, USA: Society of Nematologists.
36. Bekal S., Gauthier J. P., Rivoal R. 1997. Genetic diversity among a complex of cereal cyst nematodes inferred from RFLP analysis of the ribosomal internal transcribed spacer region. Genome, 40, 479–486.
37. Broeker K., Fehser S., Moerschbacher B.M. 2006. Survey and expression analysis of five new chitin synthase genes in the biotrophic rust fungus Puccinia graminis. Current Genetics, 50(5):295-230.
38. Brown R.H., 1984. The ecology and control of cereal cyst nematode (Heterodera avenae) in Southern Australia. Journal of Nematology, 16: 216-222.
39. Cooper, B.A.1955.A prelimination key to British species of Heterodera for use in soil examination.Soil Zoology. Butterworth Co.Led., London.pp.269-280.
40. Cronin D., Moenne-Loccoz Y., Dunne C., et al.1997.Inhibition of egg hatch of the potatocyst nematode Globodera rostochiensis by chitinase-producing bacteria. European Journal of Plant Pathology, 103(5):433-440.
41. Delibes A., Romero D., Aguaded S.,et al. 1993. Resistance to the cereal cyst nematode (Heterodera avenae Woll.) transferred from the wild grass Aegilop ventricosa to hexaploid wheat by a stepping-stone procedure. TAG Theoretical and Applied Genetics, 87:402-408.
42. Dundas I.S., Shepherd K.W., Fisher J.M.1992. Transfer of a nematode resistance gene from rye chromosome 6R to wheat and its mapping with deletion mutants. In: Abstr 1st Int Crop Sci Cong Ames Iowa. Crop Science Society of America, Madiso, Wisconsin, 1992, 58.
43. Eastwood R.F., Lagudah E.S., Appels R., et al. 1991.Triticum tauschii:a novel source of resistance to cereal cyst nematode (Heterodera avenae). Aust. J.Agri Res, 42:69-77.
44. Erica E. Davis, Robert C.Venette. Mini risk assessment Mediterranean cereal cyst nematode, Heterodera latipons Franklin (Nematoda: Heteroderidae). CAPS PAR: Heterodera latipons.1-26.
45. Fenwick, D.W.1959.The genus Heterodera. In Plant nematology.Edited by J.F.Southey. Tech.Bull.7, Min.Agric.Fish.Food London, England.pp.61-70.
46. Ferris V. R., Faghihi J. , Ireholm A., et al. 1989. Two- dimensional protein patterns of cereal cyst nematodes. Phytopathology 79:927–933.
47. Ferris V. R.,Subbotin S. A.,Ireholm A,et al. 1999,Ribosomal DNA sequence analysis of Heterodera filipjevi and H.1atipons from Russia and comparisons with other nematode isolates.Russian Journal of Nematology, 2:121-125.
48. Ferris, V. R., J. M. Ferris, J. Faghihi, and A. Ireholm. 1994. Comparisons of isolates of Heterodera avenae using 2-D PAGE protein patterns and ribosomal DNA. Journal of Nematology 26:144–151.
49. Franklin, 1969 on grass stands in Czecholovakia. Helminthologia, 25, 201-206.
50. Gabler C., Sturhan D. , Subbotin S. A., et al. 2000. Heterodera pratensis sp. n., a new cyst nematode of the H. avenae complex (Nematoda: Heteroderidae). Russian Journal of Nematology 8:115-26.
51. Gan Zhongwei, Yang Jinhui, Tao Nan et al.2007. Cloning of the gene Lecanicillium psalliotae chitinase Lpchi1and identification of its potential role in the biocontrol of root-knot nematode Meloidogyne incognita. Appl Microbiol Biotechnol, 1-9.
52. Golden, A. M. 1986. Morphology and identification of cyst nematodes. pp. 23-45 in F. Lamberti and C. E. Taylor, eds. Cyst nematodes.New York: Plenum Press.
53. Greco N., Vovlas N., A.Troccoli, et al.2002.The Mediterranean cereal cyst nematode, Heterodera latipons: a menace to cool season cereals of the United States, Nematology Circular No.221:1-6.
54. Green C.D., 1971.The morphology of terminal area of the round-cyst nematodes, S.G. Heterodera rostochiensis and allied species.Nematologica, 17:34-46.
55. Hajieghrari B.,Mousa T., Waeyenberge L. 2007. Comparative d2/d3 LSU–rDNA sequence study of some Iranian Pratylenchus loosi populations. African Journal of Biotechnology .6 (21), pp: 2458-2466.
56. Hajihasani A., Tanha Maafi Z., Nicol J. M. et al. 2010. Relationships between population densities of the cereal cyst nematode, Heterodera latipons and yield losses of winter wheat in microplots. Australasian Plant Pathology, 39, 530-535
57. Handa D.K., Mathur R. L., Mathur B. N.et al. 1985b. Estimation of losses in barley due to cereal cyst nematode in sandy and sandy loamy soils. Indian Journal of Nematology, 15, 163–166.
58. Handoo Z. A. 2002. A key and compendium to species of the Heterodera avenae Group (Nematoda: Heteroderidae). J. Nematol. 34:250-262.
59. Hesling J.J.1965. Heterodera: Morphology and identification. In Plant nematology.Edited by J.F.Southey.Tech.Bull.7, Min.Agric.Fish.Food London, England.pp.103-130.
60. Hesling J.J.1978.Cyst nematodes: morphology and identification of Heterodera, Globoderaand Punctodera, pp: 125-155. In J.F. Southey (ed.), Plant nematology.
61. Holgado R., Andersson S., Magnusson C. 2006. Management of cereal cyst nematodes, Heterodera spp., in Norway. Commun Agric Appl Biol Sci. 71(3 Pt A):639-45.
62. Holm Nielsen C.H.1972.The test assortment for cereal cyst nematode (Heterodera avenae). (On behalf of the Heterodera group).Ⅺth International Sypmosium of Nemotology, Reading,50-51(abstract).
63. Ibrahim A. A. M., Al-Hazmi A. S., Al-Yahya, F. A., et al.1999. Damage potential and reproduction of Heterodera avenae on wheat and barley under Saudi field conditions. Nematology, 1, 625–630.
64. Jahier J.,Tanguy A.M., Abelard P.,et al. 1996. Utilization of deletion to localize a gene for resistance to the cereal cyst nematode Heterodera avenae on an Aegilop ventricosa chromosome. Plant Breeding, 115:282-284.
65. Kerry B.R., de Leij, F.A.A.M. 1992. Key factors in the development of fungal agents for the control of cyst and root-knot nematodes. In Biological control of plant diseases, p: 139-144. London, Plenum.
66. Kort J. 1972. Nematode diseases of cereals of temperate climates. In J. M. Webster (Ed.), Economic Nematology (pp:97–126). London, UK: Academic Press.
67. Krall E.L., H.A., Krall, 1978.Systematic changes of phytonematodes of the family Heteroderidae based on tropic specialization of these parasites and their evolutionary connection with agricultural plants. In Fitogel’mintologicheskie issledovaniya, pp. 39–56. Moscow, USSR: Nauka.
68. Kretschmer M., K. J. Chalmem, S. Manning., et al. 1997. RFLP mapping of the Ha2 cereal cyst nematode resistance gene in barley. Theor Appl Genet, 94:1060-1064.
69. Lagudah E., Moullet O.1997. Appels R.Map-based cloning of a gene sequence encoding anucleotide-binding domain and a leucine-rich region at the Cre3 nematode resistance locus of wheat. Genome, 40:659-665.
70. Lopez-Brana I., M.D. Romero, A.Delibes.1996. Analysis of Heterodera avenae populations by the random amplified polymorphic DNA technique. Genome, 39:118-122.
71. Luc M., A. R. Maggenti, R. Fortuner. 1988. A reappraisal of Tylenchina (Nemata). 9. The family Heteroderidae Filipjev & Schuurmans Stekhoven, 1941. Review of nematology. 11:159–176.
72. Madani M., Vovlas N., Castillo P., et al. 2004. Molecular characterization of cyst nematode species (Heterodera spp.) from the Mediterranean Basin using RFLPs and sequences of ITS-rDNA. J. Phytopathol. 152:229-234.
73. Maqbool M.A., 1988. Present status of research on plant parasitic nematodes in cereals and food and forage legumes in Pakistan. pp. 173-180. In: Nematodes parasitic to cereals and legumes in temperate semi-arid regions (Saxena M.C., Sikora R.A. and Srivastava J.P., eds) Workshop Proceedings, Larnaca, Cyprus, 1-5 March 1987. ICARDA, Aleppo, Syria.
74. McDonald A., Nicol, J. M. 2005. Nematode parasites of cereals. In J. Bridge, R. Sikora & M. Luc (Eds.), Plant parasitic nematodes in tropical and subtropical agriculture (pp: 131-191). CABI Publishing, Wallingford, Oxon, United Kingdom.
75. Mohammad Abdollahi. 2008. Morphology and morphometries of Heterodera filipjevi (Madzhidov, 1981) Steller, 1984 from Kohgiluyeh and Boyer-Ahmad province, Iran.. Pakistan Journal of Biological Sciences, 11 (14): 1864-1867.
76. Mokabli A., Valette S., Gauthier J. P.et al. 2002. Variation in virulence of cereal cyst nematode populations from North Africa and Asia. Nematology, 4, 521-525.
77. Montes M.J., Lopez-Brana I., Delebes A. 2004. Root enzyme activities associated with resistance to Heterodera avenae conferred by gene Cre2 in wheat/ Aegilop triuncialis introgression line. J. Plant Physiol, 161:493-495.
78. Mulvey R. H., A. M. Golden. 1983. An illustrated key to the cyst-forming genera and species of Heteroderidae in the western hemisphere with species morphometrics and distribution. Journal of Nematology 15:1–59.
79. Mulvey R.H. 1972.Identification of Heterodera cysts by terminal and cone top structures. Can.J. Zool.50:1277-1292.
80. Mulvey R.H.1957.Taxonomic value of the cone top and the underbridge in the cyst-forming nematodes Heterodera schachtii, H.schachtii var.trifolii and Heterodera avenae (Nematoda: Hematoderidae). Can.J.Zool.35:421-423.
81. Nicol J., Rivoal R., Valette S., et al. 2002. The frequency and diversity of the cyst and lesion nematode on wheat in the Turkish Central Anatolian Plateau. Journal of Nematology, 4, 272. [Abstract].
82. O, Brien P., Fisher J., Rathjen A.1980. Inheritance of resistance in two wheat cultivars to an Australian population of Heterodera avenae. Nematologica, 26:69-74.
83. Ogbonnaya, F.C., S. Scab, A. Delibes, et al. Malecular-genetie characterization of a new nematode resistance gene in wheat. Theor Appl Genet., 2001, 102:623-629.
84. Peng D.L., Cook R.1996. Observations on pathotypes of cereal cyst nematodes (Heterodera avenae) in China. Afro-Asina Journal of Nematode, 6(2):176-178.
85. Philis J.1988. Occurrence of Hederodera latipons on barley in Cyprus. Nematologia Mediterranea 16, 223.
86. Rivoal R., Cook R. 1993. Nematode pests of cereals. In K. Evans, D. L. Trudgill, J. M. Webster eds., Plant parasitic nematodes in temperate agriculture (pp:259–303). U.K.: CAB International.
87. Rivoal R., Cook R.1993.Nematode pest of cereals.pp.259-303. In K. Kvans, D.L. Trudgill, J.M. Webster (ed.) Plant parasitic nematode in temperate agriculture. CAB int., Wallmyford. UK.
88. Robinson, A. J., A. R. Stone, D. J. Hooper, and J. A. Row. 1996. A redescription of Heterodera arenaria Cooper, 1955, a cyst nematode from marram grass. Fundamental and Applied Nematology 19:109–117.
89. Romero M, Montes M, Sin E, et al. 1998.A cereal cyst nematode (Heterodera avenae Woll.) resistance gene transferred from Aegilop triuncialis to hexaploid wheat.TAG Theoretical and Applied Genetics, 96:1135-1140.
90. Rumpenhorst H. J., D. Sturhan, S. A. Subbotin. 1996. Studies on the Heterodera avenae complex. Russian Journal of Nematology, 4:95–96.
91. Sabo A., Vovlas N., Ferris V.R. 2001.Phylogenetic relationships based on ribosomal DNA data for four species of cyst nematodes from Italy and one from Syria.J.Nematol.33,183-190.
92. Sabova M.,Valocka B., Liskova, M., et al.1988. The first finding of Heterodera latipons Franklin, 1969 on grass stands in Czechoslovakia. Helminthologia, 25:201-206.
93. Scholz U. 2001.Biology, pathogenicity and control of the cereal cyst nematode Heterodera latipons Franklin, on wheat and barley under semiarid conditions, and interactions with common root rot Bipolaris sorokiniana Shoemaker [teleomorph: Cochliobolus sativus (Ito et Kurib.) Drechs. Ex Dastur.]. PhD Thesis, Bonn University,
94. Sergei A., Subbotin D. S., H. J. Rumpenhorst, et al. 2002. Description of the Australian cereal cyst nematode Heterodera australis sp. n. (Tylenchida:Heteroderidae) Russian Journal of Nematology, 10 (2):139– 148.
95. Sergei A., Subbotin S.A, Dieter Sturhan, et al. 2003. Molecular and morphological characterization of the Heterodera avenae species complex (Tylenchida: Heteroderidae). Nematology, 5(4):515-538.
96. Sharma S. B., Swarup, G. 1984. Cyst forming nematodes of India. Cosmo Publication 1, New Delhi, India, 150 pp.
97. Sikora R. A. 1988. Plant parasitic nematodes of wheat and barley in temperate and temperate semi-arid regions- a comparative analysis. In M. C. Saxena, R. A. Sikora & J. P. Srivastava (Eds.), Nematodes Parasitic to Cereals and Legumes in Temperate Semi-arid Regions (pp:46-48). International Centre for Agricultural Research in the Dry Areas (ICARDA),Syria.
98. Slootmaker L., Lange W., Jochemsen G., et al.1974.Monosomic analysis in bread wheat of resistance to cereal root eelworm. Euphytica, 23:497-503.
99. Smiley R. W. 2009. Occurrence, distribution and control of Heterodera avenae and H. filipjevi in the western USA. Pages 35-40 in: Proc. 1st Int.Cereal Cyst Nematodes Initiative. I. T. Riley, J. M. Nicol, and A. A. Dababat, eds. CIMMYT, Ankara, Turkey.
100. Smiley R. W., Whittaker R. G., Gourlie J. A. et al. 2005. Plant-parasitic nematodes associated with reduced wheat yield in Oregon: Heterodera avenae. Journal of Nematology, 37, 297–307.
101. Smiley R. W., Yan, G. P., and Handoo, Z. A. 2008. First record of the cyst nematode Heterodera filipjevi on wheat in Oregon. Plant Dis. 92:1136.
102. Smiley R.W, Nicol J.M. 2009. Nematodes which challenge global wheat production. In‘Wheat science and trade’(Ed. BF Carver) pp. 171-187.(Wiley-Blackwell: Ames, IA)
103. Stone A. R. 1986. Taxonomy and phylogeny of cyst nematodes. Pp.119–131 in F. Lamberti and C. E. Taylor, eds. Cyst nematodes. New York: Plenum Press.
104. Stone A. R., and A. J. Hill. 1982. Some problems posed by the Heterodera avenae complex. Bulletin OEPP 12:317–320.
105. Subbotin S. A., Sturhan D., Rumpenhorst H. J., et al. 2003. Molecular and morphological characterisation of the Heterodera avenae species complex (Tylenchida: Heteroderidae). Nematology, 5:515-538.
106. Subbotin S. A., Waeyenberge L., Molokanova I., et al.1999. Identification of Heterodera avenae group species by morphometrics and rDNA-RFLPs. Nematology 1:195-207.
107. Subbotin S.A., Sturhan D., Chizhov V.N.,et al. 2006. Phylogenetic analysis of Tylenchida Thorne, 1949 as inferred from D2 and D3 expansion fragments of the 28S rRNA gene sequences. Nematology, 8: 455-474
108. Subbotin S.A., Waeyenberge L.and Moens M.2000. Identication of cyst forming nematodes of the genus Heterodera (Nematoda: Heteroderidae) based on the ribosomal DNA-RFLP. Nematology, 2:153-164.
109. Tanha M. Z., Subbotin S. A., Moens M. 2003. Molecular identification of cyst-forming nematodes (Heteroderidae) from Iran and a phylogeny based on ITS-rDNA sequences. Nematology, 5, 99–111.
110. Taylor C., Shepherd .K, Langridge P.1998.A Molecular genetic map of the long arm of the long arm of chromosome 6R of rye incorporating the cereal cystnematode resistance gene,CreR.Therr Appl Genet, 97:1000-1012
111. Vovlas N. 1985. Morphology and histopathology of the cereal cyst nematode (Heterodera avenae Woll.) attacking wheat, oats, and barley in Italy. Nematologica Mediterranea 13:87–96.
112. Vrain T. C., Wakarchuk D.A.,Levesque A.C., et al.1992.Intraspecific rDNA restriction fragment polymorphism in the Xiphinema americanum group. Fundamental and Applied Nematology, 15(6):563-573.
113. Waeyenberge L,Ryes A.,Moens M., et al., 2000. Molecular characterisation of 18 Pratylenchus species using rDNA restriction frangement length polymorphism. Nematology, 2(2):135-142.
114. Wendt K. R.,Vrain T. C.,Webster J. M. 1993. Separation of three species of Ditylenchus and some host races of D.dipsaci by restriction fragment length polymorphism.Journal of Nematology,25(4):555-563.
115. Williams K. J., Lewis J. G., Bogacki P., et al.2003. Mapping of a QTL contributing to cereal cyst nematode tolerance and resistance in wheat. Aust J Agric Res 54:731-737.
116. Williams K. J., Willsmore K. L., Olson S., et al. 2006. Mapping of a novel QTL for resistance to cereal cyst nematode . Theor Appl Genet, 107.
117. Williamson V. M., Gleason C.A. 2003. Plant nematode interactions. Curr. Opin. Plant Biol. 6:327-333.
118. Wouts W. M. 1985. Phylogenetic classification of the family Heteroderidae (Nematoda: Tylenchida). Systematic Parasitology, 7:295–328
119. Wouts W. M., J.G. Baldwin.1998.Taxonomy and identification of cyst-forming nematodes. pp:
83-122. In: The Cyst-forming Nematodes, S.B. Sharma (ed.), Kluwer Academic Publishers, Boston.
120. Wouts W. M., Sturhan D. 1995. Heterodera aucklandica sp. n. (Nematoda: Heteroderidae) from a New Zealand native grass, with notes on the species of the H. avenae group. New Zealand Journal of Zoology, 22:199–207.
121. Wouts W.M., Schoemaker A., Sturhan D., et al. 1995. Heterodera spinicaoda sp.n. (Nematoda: Hematoderidae) from mud flats in the Netherlands, with a key to the species of the H. avenae group. Nematology.41:575-583.
122. Yan Guiping, Richard W. Smiley.2010. Distinguishing Heterodera filipjevi and H.avenae using polymerase chain reaction-restriction fragment length polymorphism and cyst morphology. Phytopathology, 100(3):216-224.
123. Yu M.Q., Jahier J., Dedryver F. 1992. Genetics of two mechanisms of resistance to Meloidogyne nassi in an Aepilobs variabilis accession. Eunhvtica, 58:267-273.
124. Zafar A. Handoo1. 2002. A key and compendium to species of the Heterodera avenae group (Nematoda: Heteroderidae). Journal of Nematology 34(3):250–262.
125. Zhai X., Zhao T., Liu Y., et al.2008.Characterization and expression profiling of a novel cereal cyst nematode resistance gene analog in wheat. Molecular Biology, 42:960-965.
126. Zheng J., Subbotin S.A., Waeyenberge L.et al. 2000. Molecular characterisation of Chinese Heterodera glycines and H. avenae populations based on RFLPs and sequences of rDNA-ITS regions. Russian Journal of Nematology, 8: 109-113.
127. Zijlstra C., Lever A.E., Uenk B.J., et al. 1995. Differences between ITS regions of isolates of root-knot nematodes Meloidogyne hapla and M.chitwoodi. Phytopathology, 85:1231-1237.