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Engineering >> 2018, Volume 4, Issue 4 doi: 10.1016/j.eng.2018.07.006

Aphanomyces euteiches: A Threat to Canadian Field Pea Production

a Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB T6G 2P5, Canada

b Crop Diversification Center North, Alberta Agriculture and Forestry, Edmonton, AB T5Y 6H3, Canada

c Agriculture and Agri-Food Canada, Morden Research and Development Centre, Morden, MB R6M 1Y5, Canada

Received: 2018-02-02 Revised: 2018-05-02 Accepted: 2018-06-08 Available online: 2018-07-17

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Abstract

Field pea (Pisum sativum var. arvense L.) is an important legume crop around the world. It produces grains with high protein content and can improve the amount of available nitrogen in the soil. Aphanomyces root rot (ARR), caused by the soil-borne oomycete Aphanomyces euteiches Drechs. (A. euteiches), is a major threat to pea production in many pea-growing regions including Canada; it can cause severe root damage, wilting, and considerable yield losses under wet soil conditions. Traditional disease management strategies, such as crop rotations and seed treatments, cannot fully prevent ARR under conditions conducive for the disease, due to the longevity of the pathogen oospores, which can infect field pea plants at any growth stage. The development of pea cultivars with partial resistance or tolerance to ARR may be a promising approach to analyze the variability and physiologic specialization of A. euteiches in field pea and to improve the management of this disease. As such, the detection of quantitative trait loci (QTL) for resistance is essential to field pea-breeding programs. In this paper, the pathogenic characteristics of A. euteiches are reviewed along with various ARR management strategies and the QTL associated with partial resistance to ARR.

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References

[ 1 ] Felix M, Perez-Puyana V, Romero A, Guerrero A. Development of thermally processed bioactive pea protein gels: evaluation of mechanical and antioxidant properties. Food Bioprod Process 2017;101:74–83. link1

[ 2 ] Canada: outlook for principal field crops, 2017-12-18 [Internet]. Ottawa: Minister of Agriculture and Agri-Food; 2017 Dec 20 [cited 2018 Jan 15]. Available from: http://www.agr.gc.ca/eng/industry-markets-and-trade/market- information-by-sector/crops/outlook-for-principal-field-crops-in-canada/canada- outlook-for-principal-field-crops-2017-12-18/?id=1513698779109#a4. link1

[ 3 ] Karkanis A, Ntatsi G, Kontopoulou C, Pristeri A, Bilalis D, Savvas D. Field pea in European cropping systems: adaptability, biological nitrogen fixation and cultivation practices. Not Bot Horti Agrobo 2016;44(2):325–36. link1

[ 4 ] FAOSTAT database collections [Internet]. Rome: Food and Agriculture Organization of the United Nations; c2014 [cited 2017 Dec 27]. Available from: http://www.fao.org/faostat/en/#data/QC. link1

[ 5 ] De Cicco A. Dry pulses in EU agriculture—statistics on cultivation, production and economic value [Internet]. Luxembourg: Eurostat Statistics Explained; [updated 2017 Dec 20 cited 2018 Jan 12]. Available from: http://ec.europa. eu/eurostat/statistics-explained/index.php/Dry_pulses_in_EU_agriculture_-_ statistics_on_cultivation,_production_and_economic_value.

[ 6 ] Slinkard AE, van Kessel C, Feindel DE, Aii-Khan ST, Park R. Addressing farmers’ constraints through on-farm research: peas in western Canada. In: Muehlbauer FJ, Kaiser WJ, editors. Expanding the production and use of cool season food legumes. New York: Kluwer Academic Publisher; 1994. p. 877–89. link1

[ 7 ] Chan MYK, Close RC. Aphanomyces root rot of peas: evaluation of methods for assessing inoculum density of Aphanomyces euteiches in soil. New Zeal J Agric Res 1987;30(2):213–7. link1

[ 8 ] Tu JC, Findlay WI. The effects of different green manure crops and tillage practices on pea root rots. In: Proceedings of 1986 British Crop Protection Conference. 1986 Nov 17–20; Brighton, UK: Pests and Diseases; 1986. p. 229–36. link1

[ 9 ] Pfender W, Malvick DK, Pfleger FL, Grau CR. Aphanomyces root rot. In: Kraft JM, Pfleger FL, editors. Compendium of pea diseases and pests. St. Paul: APS Press; 2001. p. 9–13. link1

[10] Tu JC. Integrated control of the pea root rot diseases complex in Ontario. Plant Dis 1987;71(1):9–13. link1

[11] Hwang SF, Lopetinsky K, Evans IR. Effects of seed infection by Ascochyta spp., fungicide seed treatment, and cultivar on yield parameters of field pea under field conditions. Can Plant Dis Surv 1991;71:169–72. link1

[12] Bailey KL, Gossen BD, Gugel RK, Morrall RAA, editors. Diseases of field crops in Canada. Saskatoon: Canadian Phytopathological Society; 2003. link1

[13] Chang KF, Bowness R, Hwang SF, Turnbull GD, Howard RJ, Lopetinsky K, et al. Pea diseases occurring in central Alberta in 2004. Can Plant Dis Surv 2005;85:89–90. link1

[14] Chang KF, Hwang SF, Ahmed H, Gossen BD, Turnbull GD, Strelkov SE. Management strategies to reduce losses caused by Fusarium seedling blight of field pea. Can J Plant Sci 2013;93(4):619–25. link1

[15] Chang KF, Hwang SF, Ahmed H, Fu H, Zhou Q, Strelkov SE, et al. First report of Phytophthora sansomeana causing root rot in field pea in Alberta, Canada. Crop Prot 2017;101:1–4. link1

[16] Ondrej M, Dostalova R, Trojan R. Evaluation of virulence of Fusarium solani isolates on pea. Plant Prot Sci 2008;44(1):9–18. link1

[17] Wicker E, Moussart A, Duparque M, Rouxel F. Further contributions to the development of a differential set of pea cultivars (Pisum sativum) to investigate the virulence of isolates of Aphanomyces euteiches. Eur J Plant Pathol 2003;109(1):47–60. link1

[18] Parke JL, Rand RE, Joy AB, King EB. Biological control of Pythium damping-off and Aphanomyces root rot of peas by application of Pseudomonas cepacia or P. fluorescens to seed. Plant Dis 1991;75(10):987–92. link1

[19] Bowers JH, Parke JL. Epidemiology of Pythium damping-off and Aphanomyces root rot of pea after seed treatment with bacterial agents for biological control. Phytopathology 1993;83(12):1466–73. link1

[20] Feng J, Hwang R, Chang KF, Hwang SF, Strelkov SE, Gossen BD, et al. Genetic variation in Fusarium avenaceum causing root rot on field pea. Plant Pathol 2010;59(5):845–52. link1

[21] McLaren DL, Henderson TL, Kim YM, Chang KF, Kerley TD, Thompson MJ. Field pea diseases in Manitoba in 2016. Can Plant Dis Surv 2017;97:200–2.

[22] Hwang SF, Chang KF. Incidence and severity of root rot disease complex of field pea in northeastern Alberta in 1988. Can Plant Dis Surv 1989;69(2):139–41. link1

[23] Tu JC. Effects of soil compaction, temperature, and moisture on the development of the Fusarium root rot complex of pea in southwestern Ontario. Phytoprotection 1994;75(3):125–31. link1

[24] Xue AG. Biological control of pathogens causing root rot complex in field pea using Clonostachys rosea strain ACM941. Phytopathology 2003;93(3):329–35. link1

[25] Pfender WF. Aphanomyces root rot. In: Hagedorn D, editor. Compendium of pea diseases. St. Paul: APS Press; 1984. p. 25–8. link1

[26] Schrum H, Kotcon J, Verlinden S. Organic methods for control of root rot in pea and spinach in northeastern US. In: Neuhoff D, Halberg N, Alfldi T, Lockeretz W, Thommen A, Rasmussen IA, et al., editors. Proceedings of the Second Scientific Conference of the International Society of Organic Agriculture Research; 2008 Jun 18–20; Modena, Italy; 2008. p. 624–7. link1

[27] Lawson HM, Topham PB. Competition between annual weeds and vining peas grown at a range of population densities: effects on the weeds. Weed Res 1985;25(3):221–9. link1

[28] Xi K, Stephens JHG, Hwang SF. Dynamics of pea seed infection by Pythium ultimum and Rhizoctonia solani: effects of inoculum density and temperature on seed rot and pre-emergence damping-off. Can J Plant Pathol 1995;17 (1):19–24. link1

[29] Hwang SF, Gossen BD, Chang KF, Turnbull GD, Howard RJ, Blade SF. Etiology, impact and control of Rhizoctonia seedling blight and root rot of chickpea on the Canadian prairies. Can J Plant Sci 2003;83(4):959–67. link1

[30] Heffer Link V, Powelson ML, Johnson KB. Oomycetes. Plant health instr [Internet]; 2002 [cited 2018 Jan 12]; [about 1 p.]. Available from: https:// www.apsnet.org/edcenter/intropp/LabExercises/Pages/Oomycetes.aspx. link1

[31] Alexopoulos CJ, Mims CW. Introductory mycology. 3rd ed. New York: John Wiley & Sons, Inc.; 1979. link1

[32] Kamoun S. Molecular genetics of pathogenic oomycetes. Eukaryot Cell 2003;2 (2):191–9. link1

[33] Judelson HS, Blanco FA. The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol 2005;3:47–58. link1

[34] Pérez-Jiménez RM. Significant avocado diseases caused by fungi and oomycetes. Eur J Plant Sci Biotechnol 2008;2(1):1–24. link1

[35] Rossman AY, Palm ME. Why are Phytophthora and other Oomycota not true fungi? Outlooks Pest Manage 2006;17(5):217–9. link1

[36] Grünwald NJ. The biology of the genus Aphanomyces. In: Proceedings of the 2nd International Aphanomyces Workshop. Washington, DC: US Department of Agriculture; 2003. p. 9–14. link1

[37] Diéguez-Uribeondo J, García MA, Cerenius L, Kozubíková E, Ballesteros I, Windels C, et al. Phylogenetic relationships among plant and animal parasites, and saprotrophs in Aphanomyces (oomycetes). Fungal Genet Biol 2009;46(5):365–76. link1

[38] Papavizas GC, Ayers WA. Aphanomyces species and their root diseases in pea and sugarbeet: a review. Report. Washington, DC: Agricultural Research Service, US Department of Agriculture; 1974 Sep. Report No.:1485.

[39] Moussart A, Onfroy C, Lesne A, Esquibet M, Grenier E, Tivoli B. Host status and reaction of Medicago truncatula accessions to infection by three major pathogens of pea (Pisum sativum) and alfalfa (Medicago sativa). Eur J Plant Pathol 2007;117(1):57–69. link1

[40] Vandemark GJ, Porter LD. First report of lentil root rot caused by Aphanomyces euteiches in Idaho. Plant Dis 2010;94(4):480. link1

[41] Gaulin E, Jacquet C, Bottin A, Dumas B. Root rot disease of legumes caused by Aphanomyces euteiches. Mol Plant Pathol 2007;8(5):539–48. link1

[42] Malvick DK, Grau CR. Characteristics and frequency of Aphanomyces euteiches races 1 and 2 associated with alfalfa in the Midwestern United States. Plant Dis 2001;85(7):740–4. link1

[43] Wicker E, Hullé M, Rouxel F. Pathogenic characteristics of isolates of Aphanomyces euteiches recovered from pea in France. Plant Pathol 2001;50 (4):433–42. link1

[44] Jones FR, Drechsler C. Root rot of peas in the United States caused by Aphanomyces euteiches. J Agric Res 1925;30(4):293–325. link1

[45] Kraft JM. Registration of 90-2079, 90-2131 and 90-2322 pea germplasms. Crop Sci 1992;32(4):1076. link1

[46] Chatterton S, Bowness R, Harding MW. First report of root rot of field pea caused by Aphanomyces euteiches in Alberta, Canada. Plant Dis 2015;99(2): 288. link1

[47] Pfender WF, Hagedorn DJ. Disease progress and yield loss in Aphanomyces root rot of peas. Phytopathology 1983;73(8):1109–13. link1

[48] Scharen AL. Germination of oospores of Aphanomyces euteiches embedded in plant debris. Phytopathology 1960;50(4):274–7. link1

[49] Hoch HC, Mitchell JE. The effects of osmotic water potentials on Aphanomyces euteiches during zoosporogenesis. Can J Bot 1973;51(2):413–20. link1

[50] Kerr A. Influence of soil moisture on infection of peas by Pythium ultimum. Aust J Biol Sci 1964;17(3):676–85. link1

[51] Haenseler CM. Studies on the root rot of peas (Pisum sativum) caused by Aphanomyces euteiches Drechsler. NJ Agric Exp Stn Annu Rpt 1926;46:467–84. link1

[52] Smith PG, Walker JC. Certain environmental and nutritional factors affecting Aphanomyces root rot of garden pea. J Agric Res 1941;63:1–20. link1

[53] Burke DW, Mitchell JE. Temperature and moisture effects on infection of pea seedlings by Aphanomyces euteiches in soil [abstract]. Phytopathology 1968;58(8):1045.

[54] Burke DW, Mitchell JE, Hagedorn DJ. Selective conditions for infection of pea seedlings by Aphanomyces euteiches in soil. Phytopathology 1969;59:1670–4. link1

[55] Carlson LE. Studies on the root rot of peas caused by Aphanomyces euteiches Drechs [dissertation]. Minneapolis and Saint Paul: University of Minnesota; 1965.

[56] Gaulin E, Madoui MA, Bottin A, Jacquet C, Mathé C, Couloux A, et al. Transcriptome of Aphanomyces euteiches: new oomycete putative pathogenicity factors and metabolic pathways. PLoS One 2008;3(3):e1723. link1

[57] King EB, Parke JL. Biocontrol of Aphanomyces root rot and Pythium damping- off by Pseudomonas cepacia AMMD on four pea cultivars. Plant Dis 1993;77 (12):1185–8. link1

[58] Kraft JM, Kaiser WJ. Screening for disease resistance in pea. In: Singh KB, Saxena MC, editors. Breeding for stress tolerance in cool-season food legumes. Chichester: John Wiley and Sons; 1993. p. 123–44. link1

[59] Scott WW. A monograph of the genus Aphanomyces. Blacksburg: Virginia Agricultural Experiment Station; 1961. link1

[60] Sekizaki H, Yokosawa R, Chinen C, Adachi H, Yamane Y. Studies on zoospore attracting activity. II. Synthesis of isoflavones and their attracting activity to Aphanomyces euteiches zoospore. Biol Pharm Bull 1993;16(7): 698–701. link1

[61] Mitchell JE, Yang CY. Factors affecting growth and development of Aphanomyces euteiches. Phytopathology 1966;56(8):917.F–22.F. link1

[62] Kjøller R, Rosendahl S. Enzymatic activity of the mycelium compared with oospore development during infection of pea roots by Aphanomyces euteiches. Phytopathology 1998;88(9):992–6. link1

[63] Muehlchen AM, Rand RE, Parke JL. Evaluation of crucifer green manures for controlling Aphanomyces root rot of peas. Plant Dis 1990;74(9):651–4. link1

[64] Chupp C, Sherf AF. Vegetable diseases and their control. New York: Ronald Press Company; 1960.

[65] King TH, Bissonnette HL. Physiologic specialization in Aphanomyces euteiches [abstract]. Phytopathology 1954;44:495.

[66] Beute MK, Lockwood JL. Pathogenic variability in Aphanomyces euteiches. Phytopathology 1967;57:57–60.

[67] Sundheim L, Wiggen K. Aphanomyces euteiches on peas in Norway, isolation technique, physiologic races and soil indexing. Norgres Landbr Hoiskoles Meld 1972;51:17. link1

[68] Manning M, Menzies SA. Pathogenic variability in isolates of Aphanomyces euteiches from New Zealand soils. N Z J Agric Res 1984;27(4):569–74. link1

[69] Malvick DK, Percich JA. Variation in pathogenicity and genotype among single-zoospore strains of Aphanomyces euteiches. Phytopathology 1998;88 (1):52–7. link1

[70] Wicker E, Rouxel F. Specific behaviour of French Aphanomyces euteiches Drechs. populations for virulence and aggressiveness on pea, related to isolates from Europe, America and New Zealand. Eur J Plant Pathol 2001;107 (9):919–29. link1

[71] Malvick DK, Percich JA. Genotypic and pathogenic diversity among pea- infecting strains of Aphanomyces euteiches from central and western United States. Phytopathology 1998;88(9):915–21. link1

[72] Malvick DK, Percich JA. Identification of Pisum sativum germplasm with resistance to root rot caused by multiple strains of Aphanomyces euteiches. Plant Dis 1999;83(1):51–4. link1

[73] Wu LF. Occurrence and management of root rot of field pea cause by Aphanomyces euteiches [dissertation]. Edmonton: University of Alberta; 2018. link1

[74] Scott RE. Root rot and soil compaction problems of pea crops. Agron Soc New Zealand Spec Publ 1987;6:45–50. link1

[75] Manning MA, Menzies SA. Root rot of peas in New Zealand caused by Aphanomyces euteiches. N Z J Agric Res 1980;23(2):263–5. link1

[76] Vandemark GJ, Barker BM, Gritsenko MA. Quantifying Aphanomyces euteiches in alfalfa with a fluorescent polymerase chain reaction assay. Phytopathology 2002;92(3):265–72. link1

[77] Pilet-Nayel L, Muehlbauer FJ, McGee RJ, Kraft JM, Baranger A, Coyne CJ. Quantitative trait loci for partial resistance to Aphanomyces root rot in pea. Theor Appl Genet 2002;106(1):28–39. link1

[78] Pilet-Nayel ML, Muehlbauer FJ, McGee RJ, Kraft JM, Baranger A, Coyne CJ. Consistent quantitative trait loci in pea for partial resistance to Aphanomyces euteiches isolates from the United States and France. Phytopathology 2005;95 (11):1287–93. link1

[79] Hamon C, Baranger A, Coyne CJ, McGee RJ, Le Goff I, L’Anthoëne V, et al. New consistent QTL in pea associated with partial resistance to Aphanomyces euteiches in multiple French and American environments. Theor Appl Genet 2011;123(2):261–81. link1

[80] Hamon C, Coyne CJ, McGee RJ, Lesné A, Esnault R, Mangin P, et al. QTL meta- analysis provides a comprehensive view of loci controlling partial resistance to Aphanomyces euteiches in four sources of resistance in pea. BMC Plant Biol 2013;13(1):45. link1

[81] Lavaud C, Lesné A, Piriou C, Le Roy G, Boutet G, Moussart A, et al. Validation of QTL for resistance to Aphanomyces euteiches in different pea genetic backgrounds using near-isogenic lines. Theor Appl Genet 2015;128(11):2273–88. link1

[82] Lavaud C, Baviere M, Le Roy G, Hervé MR, Moussart A, Delourme R, et al. Single and multiple resistance QTL delay symptom appearance and slow down root colonization by Aphanomyces euteiches in pea near isogenic lines. BMC Plant Biol 2016;16(1):166. link1

[83] Desgroux A, L’Anthoëne V, Roux-Duparque M, Rivière JP, Aubert G, Tayeh N, et al. Genome-wide association mapping of partial resistance to Aphanomyces euteiches in pea. BMC Genomics 2016;17(1):124. link1

[84] Kraft JM, Haware MP, Jiménez-Diaz RM, Bayaa B, Harrabi M. Screening techniques and sources of resistance to root rots and wilts in cool season food legumes. Euphytica 1994;73(1–2):27–39. link1

[85] Thygesen K, Larsen J, Bodker L. Arbuscular mycorrhizal fungi reduce development of pea root-rot caused by Aphanomyces euteiches using oospores as pathogen inoculum. Eur J Plant Pathol 2004;110(4):411–9. link1

[86] Jones FR, Linford MB. Pea disease survey in Wisconsin. Madison: Agricultural Experiment Station of the University of Wisconsin; 1925. link1

[87] Allmaras RR, Fritz VA, Pfleger FL, Copeland SM. Impaired internal drainage and Aphanomyces euteiches root rot of pea caused by soil compaction in a fine-textured soil. Soil Tillage Res 2003;70(1):41–52. link1

[88] Conner RL, Chang KF, Hwang SF, Warkentin TD, McRae KB. Assessment of tolerance for reducing yield losses in field pea caused by Aphanomyces root rot. Can J Plant Sci 2013;93(3):473–82. link1

[89] Oyarzun P, Gerlagh M, Hoogland A, Vos I. Seed treatment of peas with fosetyl-Al against Aphanomyces euteiches. Neth J Plant Pathol 1990;96(5): 301–11. link1

[90] Xue AG. Efficacy of Clonostachys rosea strain ACM941 and fungicide seed treatments for controlling the root rot complex of field pea. Can J Plant Sci 2003;83(3):519–24. link1

[91] Kraft JM, Marcinkowsha J, Muehlbauer FJ. Detection of Aphanomyces euteiches in field soil from Northern Idaho by a wet-sieving/baiting technique. Plant Dis 1990;74(9):716–8. link1

[92] Vandemark GJ, Kraft JM, Larsen RC, Gritsenko MA, Boge WL. A PCR based assay by sequence-characterized DNA markers for the identification and detection of Aphanomyces euteiches. Phytopathology 2000;90(10): 1137–44. link1

[93] Garrett SD. Root disease fungi: a treatise on the epidemiology of soil-borne disease in crop plants, and a first exposition of the principles of root disease control. Waltham: Chronica Botanica; 1944. link1

[94] Temp MV, Hagedorn DJ. Influence of cropping practice on Aphanomyces root rot potential of Wisconsin pea fields. Phytopathology 1967;57:667–70.

[95] Olofsson J. Root rot of canning and freezing peas in Sweden. Acta Agr Scand 1967;17(2–3):101–7. link1

[96] Hossain S, Bergkvist G, Berglund K, Glinwood R, Kabouw P, Mårtensson A, et al. Concentration- and time-dependent effects of isothiocyanates produced from Brassicaceae shoot tissues on the pea root rot pathogen Aphanomyces euteiches. J Agric Food Chem 2014;62(20):4584–91. link1

[97] Williams-Woodward JL, Pfleger FL, Fritz VA, Allmaras RR. Green manures of oat, rape and sweet corn for reducing common root rot in pea (Pisum sativum) caused by Aphanomyces euteiches. Plant Soil 1997;188(1):43–8. link1

[98] Krupinsky J, Bailey K, McMullen M, Gossen B, Kelly Turkington T. Managing plant disease risk in diversified cropping systems. Agron J 2002;94(2): 198–209. link1

[99] Oyarzun PJ, Dijst G. Zoon FC, Maas PW. Comparison of soil receptivity to Thielaviopsis basicola, Aphanomyces euteiches, and Fusarium solani f. sp. pisi causing root rot in pea. Phytopathology 1997;87(5):534–41. link1

[100] Heyman F, Lindahl B, Persson L, Wikstrom M, Stenlid J. Calcium concentrations of soil affect suppressiveness against Aphanomyces root rot of pea. Soil Biol Biochem 2007;39(9):2222–9. link1

[101] Papavizas GC. Suppression of Aphanomyces root rot of peas by cruciferous soil amendments. Phytopathology 1966;56:1071–5. link1

[102] Papavizas GC. Comparison of treatments suggested for control of Aphanomyces root rot of peas. Plant Dis Res 1967;51:125–9.

[103] Papavizas GC, Lewis JA. Effect of amendments and fungicides on Aphanomyces root rot on peas. Phytopathology 1971;61(2):215–20.

[104] Davey CV, Papavizas GC. Aphanomyces root rot of peas as affected by organic and mineral soil amendments. Phytopathology 1961;51:131–2.

[105] Tu JC. Effect of soil pH on pea root rots, yield and soil biology. Med Fac Landbouww Rijksuniv Gent 1990;55:827–34. link1

[106] Tu JC. Management of root rot diseases of peas, beans, and tomatoes. Can J Plant Pathol 1992;14(1):92–9. link1

[107] Fritz VA, Allmaras R, Pfleger FL, Davis DW. Oat residue and soil compaction influences on common root rot (Aphanomyces euteiches) of peas in a fine- textured soil. Plant Soil 1995;171(2):235–44. link1

[108] Wilkins D, Darnell T, Kraft J. Integrated conservation tillage system for control of pea root rot disease. In: Proceedings of the 1998 ASAE Annual International Meeting; 1998 Jul 11–16; Orlando, FL, USA; 1998.

[109] Sherwood RT, Hagedorn DJ. Determining the common root rot potential of pea fields. Madison: Agricultural Experiment Station, University of Wisconsin; 1958. link1

[110] Reiling TP, King TH, Fields RW. Soil indexing for pea root rot and the effect of root rot on yield. Phytopathology 1960;50:287–90. link1

[111] Sauvage H, Moussart A, Bois F, Tivoli B, Barray S, Laval K. Development of a molecular method to detect and quantify Aphanomyces euteiches in soil. FEMS Microbiol Lett 2007;273(1):64–9. link1

[112] Vandemark GJ, Grünwald NJ. Use of real-time PCR to examine the relationship between disease severity in pea and Aphanomyces euteiches DNA content in roots. Eur J Plant Pathol 2005;111(4):309–16. link1

[113] Armstrong-Cho C, Tetreault M, Banniza S, Bhadauria V, Morrall RAA. Reports of Aphanomyces euteiches in Saskatchewan. Can Plant Dis Surv 2014;94:193–4.

[114] Cohen M. Environmental toxins and health—the health impact of pesticides. Aust Fam Physician 2007;36(12):1002–4. link1

[115] Deberdt P, Mfegue C, Tondje P, Bon M, Ducamp M, Hurard C, et al. Impact of environmental factors, chemical fungicide and biological control on cacao pod production dynamics and black pod disease (Phytophthora megakarya) in Cameroon. Biol Control 2008;44(2):149–59. link1

[116] Kotova VV, Tsvetkova NA. Effectiveness of chemical control measures against Aphanomyces root rot of peas [abstract]. Rev Plant Pathol 1980;59:342.

[117] Bruin GCA, Edgington LV. Chemical control of diseases caused by zoosporic fungi: a many-sided problem. In: Buczacki ST, editor. Zoosporic plant pathogens: a modern perspective. London: Academic Press; 1983. p. 193–223. link1

[118] Gossen BD, Conner RL, Henriquez MA, Chang KF, Hwang SF, Pasche J, et al. Identifying and managing root rot of pulses on the northern Great Plains. Plant Dis 2016;100(10):1965–78. link1

[119] Jermyn WA, Banfield RA, Hedley J, Russell AC. Effect of seed treatment on Aphanomyces root rot of peas. Proc Agron Soc New Zealand 1982;12:15–8. link1

[120] Gritton ET, Parke JL, Percich JA, Fritsz YA, Kraft JM, Grau CR, et al. Integrated control of Aphanomyces root rot of pea (Pisum sativum L.). In: Improving production and utilisation of grain legumes. Proceedings of the 2nd European Conference on Grain Legumes; 1995 Jul 9–13; Copenhagen, Denmark. Paris: AEP; 1995. p. 148–9. link1

[121] Wakelin S, Walter M, Jaspers M, Stewart A. Biological control of Aphanomyces euteiches root-rot of pea with spore-forming bacteria. Australas Plant Pathol 2002;31(4):401–7. link1

[122] Bødker L, Kjøller R, Kristensen K, Rosendahl S. Interactions between indigenous arbuscular mycorrhizal fungi and Aphanomyces euteiches in field-grown pea. Mycorrhiza 2002;12(1):7–12. link1

[123] Katan J. Soil solarization. In: Chet I, editor. Innovative approaches to plant disease control. New York: John Wiley and Sons; 1987. p. 77–105. link1

[124] Ramierz-Villapudua J, Munnecke DE. Effect of solar heating and soil amendment of cruciferous residues on Fusarium oxysporum f. sp. conglutinans and other organisms. Phytopathology 1988;78(3):289–95. link1

[125] Davis DW, Fritz VA, Pfleger FL, Percich JA, Malvick DK. MN 144, MN 313 and MN 314: garden pea lines resistant to root rot caused by Aphanomyces euteiches Drechs. HortSci 1995;30(3):639–40. link1

[126] Pilet-Nayel ML, Coyne C, Hamon C, Lesne A, Le Goff I, Esnault R, et al. Understanding genetics of partial resistance to Aphanomyces root rot in pea for new breeding prospects. Proceedings of the Third International Aphanomyces Workshop on Legumes, 2007.

[127] Marx GA, Schroeder WT. Provvidenti R, Mishance W. A genetic study of tolerance in pea (Pisum sativum L.) to Aphanomyces root rot. J Am Soc Hortic Sci 1972;97:619–21. link1

[128] Rao A, Gritton ET, Grau CR, Peterson LA. Aeroponics chambers for evaluating resistance to Aphanomyces root rot of peas (Pisum sativum). Plant Dis 1995;79 (2):128–32. link1

[129] Xue AG. Effect of seed-borne Mycosphaerella pinodes and seed treatments on emergence, foot rot severity, and yield of field pea. Can J Plant Pathol 2000;22 (3):248–53. link1

[130] Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ. Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 2009; 14(1):21–9. link1

[131] Kou Y, Wang S. Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 2010;13(2):181–5. link1

[132] Loridon K, McPhee K, Morin J, Dubreuil P, Pilet-Nayel ML, Aubert G, et al. Microsatellite marker polymorphism and mapping in pea (Pisum sativum L.). Theor Appl Genet 2005;111(6):1022–31. link1

[133] Bao Y, Vuong T, Meinhardt C, Tiffin P, Denny R, Chen S, et al. Potential of association mapping and genomic selection to explore PI 88788 derived soybean cyst nematode resistance. Plant Genome 2014;7(3):1–13. link1

[134] Cheng P, Holdsworth W, Ma Y, Coyne CJ, Mazourek M, Grusak MA, et al. Association mapping of agronomic and quality traits in USDA pea single plant collection. Mol Breed 2015;35(2):75. link1

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