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Root Rots in Pulses Michelle Hubbard, Agriculture and Agri-Food Canada, Swift Current Research Scientist, Pulse Pathology Co-authors: Sabine Banniza, Zakir Hossain, Sherrilyn Phelps, Syama Chatterton, Luke Bainard & Barb Ziesman What is root rot?

Caused by micro-organisms Range of pathogens • species • species • solani • euteiches Pea and do not like wet feet

High soil moisture can cause • ↓ root and shoot growth • yellowing • ↓ nodulation Stressed plants are more susceptible to infection

Normal soil Water- moisture saturated Peas in sterile field soil Root rot is a complex

Fusarium species Pythium species Rhizoctonia solani Aphanomyces euteiches And it is complicated!

Wider host range True fungi • Fusarium spp. (e.g. solani, • Fusarium spp. avenaceum, acuminatum, graminearum) • Rhizoctonia solani • Rhizoctonia solani • Pythium spp. Fungus-like organisms () Attack only specific plants: • Pythium spp. • Fusarium oxysporum f.sp. pisi, f.sp. ciceris or f. sp. • Aphanomyces lentis, F. virgulifome euteiches • Aphanomyces euteiches • Phytophthora spp. • Phytophthora spp Fusarium

Courtesy of S. Chatterton, AAFC Infects many different plants Courtesy of F. Dokken-Bouchard, SMA Aphanomyces Oospores

Infects pea and lentil Oospores = resting spores • More vulnerable after they germinate Zoospores: can swim short distances

Courtesy of S. Chatterton, AAFC

Courtesy of F. Dokken-Bouchard, SMA Aphanomyces

Oospores

EveryInfects time pea aand plant lentil gets infected,Oospores the= resting amount spores of AphanomycesMore vulnerable in after the theysoil ↑germinate Zoospores: can swim short distances

Courtesy of S. Chatterton, AAFC

Courtesy of F. Dokken-Bouchard, SMA https://www.apsnet.org/edcenter/dis andpath/oomycete/pdlessons/Pages /Aphanomyces.aspxd text Aphanomyces vs Fusarium?

Yellowing and Shoots remain wilting of shoots healthy

Pinching of epicotyl, stops Blackened tap root, abruptly at soil starts at seed line attachment Healthy lateral Lateral roots roots watery and honey-brown

decay Courtesy of Dr. Chatterton, Aphanomyces Fusarium AAFC Usually multiple pathogens

More pathogens → worse disease

S. Chatterton, AAFC Lethbridge Environmental preferences …..according to the literature Organism Temperature Optimum Optimum pH optimum (oC) Soil Moisture Aphanomyces 22 to 27 Excessive pH 4.5 to 6.5 Fusarium 25 to 30 Moderate Pythium 17 to 23 Wet Rhizoctonia Can damage Wide range at 18 but of conditions most aggressive at 24 to 30 Aphanomyces survey from 2014-2017

 Widespread

Pea and lentil  Severe in SK: 2015-2017 Elrose area

Chatterton et al. (2018) Can. J. Plant Path. Pea, lentil and chickpea Aphanomyces infects pea and lentil • Usually more severe for pea Aphanomyces doesn’t cause disease in chickpea, but other organisms do S Chatterton Pea root rot 2019, SK Widespread 100% of pea fields had some root rot 3.4 (0-7 scale) average severity Both Fusarium species and Aphanomyces found

Source: Pulse Situations Report 2019, Survey for Root Rot of Field Pea in Saskatchewan in 2019, Chatterton et al. Lentil root rot 2019 in SK 59% prevalence

Number of Region Fields Prevalence (%) surveyed Southwest 23 61 Southeast 12 75 East-central 8 63 West-central 34 50 Northeast 1 100 Overall 78 59

Source: Pulse Situations Report 2019, Lentil Disease Survey, Barb Zeisman, SK ministry of Agriculture Chickpea root rot

In general: Pythium species Rhizoctonia solani Fusarium species Leiso et al. (2011) Can. J. Plant Pathol. 33(3): 400–409

Chickpea root rot 2019 Photo: M Hubbard Sample: S. Phelps Chickpea root rot in SK, 2019 Severe damage to chickpea in far south west of SK in July

Five diseased samples: • Fusarium redolens, • F. solani (possibly forma specialis pisi), • F. avenaceum and • Pea leaf weevil can

increase Fusarium root rot Disease severity Disease

Control Pea leaf Fusarium Fusarium weevil + pea leaf weevil Willsey et al. 2019. Crop Protect. 116: 108-114. Pea leaf weevil and Fusarium root rot are mutualistic

Pea leaf weevil

Fusarium + pea weevil # of pea leaf weevils leaf pea of #

Willsey et al. 2019. Crop Protect. 116: 108-114. What can you do?

Avoid certain fields Crop rotation Field avoidance

Compaction

Poor drainage • Fine-textured soil

History of root rot

Syama Chatterton, AAFC Lethbridge Testing Fields for root rots

 Labs offering testing for root rots (aphanomyces, fusarium?)

BDS Laboratoires – Qu’Appelle, SK

BioVision Seed Labs* – Sherwood Park, AB

Discovery Seed Labs** – Saskatoon, SK

20/20 Seed Labs* – Nisku, AB/Winnipeg, MB Quantum Genetix* – Saskatoon, SK Crop Protection Lab – Regina, SK (Visual diagnostic services)  Individual labs may differ in testing methods and sample requirements. Please check with the lab prior to sending samples. *Lab offers DNA test for Aphanomyces. ** Lab offers Bait test & DNA Crop rotation

For Aphanomyces, 6-8 year break between pea or lentil crops Every time you grow pea or lentil, pathogens increase Other possibilities

Specific rotations Herbicides • Resistant pulses Nutrition • Brassicas Mycorrhizae • Oats Antagonistic Green manures bacteria Intercropping Soil pH modification Rotations with a resistant pulse  Chickpea, faba bean, soybean  Theory: oospores germinate → die (do not produce more oospores)

7 Other Pulse Pea SE 6 Rotation± studies take time 5 Study4 runs 2018-2013

severity severity 3 Stay2 tuned….. 1

Disease Disease 0 Chickpea Chickpea Faba bean Faba bean Soybean Soybean Taber Swift Lacombe Sask Lomond Redvers Aphanomyces resistant pulses Aphanomyces  Still get Fusarium 100% 100%

80% 80% Aph = Aphanomyces euteiches, Fred = Fusarium redolens, 60% 60% Fsol = Fusarium solani, Fave = Fusarium avenaceum

40% Aphanomyces 40% Fusarium

20% 20%

Fusarium 0% 0% Soybean Pea Soybean Pea Chickpea Pea Chickpea Pea Lomond Redvers Taber Swift Aph 0.3 325.8 0.1 118.6 Aph 0.1 86.6 1.9 25.7 Fred 2.2 12.0 7 1.2 Fred 37.9 438.6 37 88.0 Fsol 1.78 44.9 0.1 11.0 Fsol 12.5 121.6 129.7 73.5 Fave 0.1 0.1 3.9 1.0 Fave 0.4 356.9 6.9 6.4 Brassicas and root rots

 Potential to “bio-fumigate” soil

Glucosinolates Isothiocyanates

https://lpi.oregonstate.edu/mic/dietary-factors/phytochemicals/isothiocyanates#metabolism-bioavailability Oats and Aphanomyces  Potential to stimulate oospore germination (Shang et al. 2000)

Shang et al. (2000) • After germination, oospores are vulnerable Plant Dis. 84: 994-998.

 Potential to kill zoospores (Deacon and Mitchell 1985) • Possibly due to saponins

Zoospore

Deacon and Mitchell (1985) Trans. Br. Mycol. Soc. 84 (3), 479-487 Green manures May promote breakdown → release of “bio-fumigants” Crops • Oat • Yellow mustard • Forage radish • Durum

Forage radish July 2018, Swift Current M. Hubbard Grain harvest or green manure in 2018 Pea in 2019 30 2018 & 2019 Trial

Swift Current Indian Head Melfort

Dr. Luke Bainard Green manure results No clear impact

Swift Current

7.0

SE ±

) ) 6.0

7 - 5.0

4.0

3.0

Rot Rating (1 Rating Rot 2.0

1.0 Root Root Oats Yellow Mustard Forage Radish Durum Grain harvest Green manure Intercropping  Growing two or more crops together  Insurable starting in 2017

20,000 2018 2019 18,000 16,000 14,000 Pulse/brassica 12,000 intercrops 10,000 8,000 6,000

Insured Acres Insured 4,000 2,000 0 Photo: M Hubbard, Axten Farm Pea/mustard Pea/brassica Intercropping

 Pea/canola is one of the most common intercrops  Remember glucosinolates and isothiocyanates -> soil “fumigation”?

Isothiocyanates

Glucosinolates Pea/brassica Intercropping  2018 results: Disease severity on pea was not significantly different on intercrop compared to monocrop pea roots

6 Taber Saskatoon 5

4

3

2

Disease Severity Disease 1

0 Pea Pea:Can Pea:Can Pea:Mus Pea:Mus 30:70 50:50 30:70 50:50

Chatterton et al. 2019. Can. Phytopath. Society Annual meeting. Pea/brassica Intercropping

 2018 resultsSaskatoon Taber Pea Total Pea Total LER^ LER^ yield yield yield yield Pea 637.7 637.7 1.00 542.7 594.2 1.00 Canola (Can) 1066.2 604.5 Mustard (Mus) 826.3 387.9 Pea:Can 30:70 102.5 1040.0 1.00 287.0 709.7 1.16 Pea:Can 50:50 276.2 1028.0 1.18 250.0 705.8 1.27 Pea:Mus 30:70 227.2 987.6 1.28* 246.5 456.2 0.99 Pea:Mus 50:50 583.9 1083.9* 1.53* 310.0 624.6* 1.35* ^LER = yield crop A in intercrop/ yield crop A in monocrop + yield crop B in

intercrop/ yield crop B in monocrop Chatterton et al. 2019. *significantly different than monocrop yield or LER at P = 0.05 Can. Phytopath. Society Annual meeting. Soil pH Acidic soils may ↑ risk • Pea and lentil don’t like low pH (acid) + Ammonium (NH4 ) N-fert can lower soil pH Calcium may help ↓ root rot Disease (Heyman et al. 2007) Soil Severity Adding lime may help #4 80a • But may not be #4 + CaCO3 73b feasible #4 + CaSO4 11d Heyman et al. (2007) Soil Bio. and Biochem. 39: 2222-2229 Courtesy of S. Phelps, SPG Herbicides Symptoms after herbicide application • Stress can weaken plants Weeds host aphanomyces: • shepherd’s purse, • chickweed, • vetches • (kochia?, lamb’s quarters?) Fusarium species can infect many weeds

Courtesy of S. Phelps, SPG Atrazine Can make Fusarium root rot worse in pea Photosystem II inhibitor (group 5) In Aatrex (corn)

Percich & Lockwood 1975. Phytopathology. 65: 154-159 Trifluralin, ethalfluralin Mitotic inhibitor, Group 3 • Trifluralin: Bonanza, Rival, Treflan • Broadleaf control • Ethalfuralin: Edge • Broadleaf + grassy ↓ root rot in pea in greenhouse, but not in field Johnston et al. (1980) Plant Disease. 64: 942-943 Trifluralin Minnesota field trials Trifluralin and dinitramine • ↓ growth, zoospore production and movement in lab • slightly ↓ root rot in field No impact found in research in Western Canada so far

Grau and Reiling. 1977. Phytopathology 67:273-276. Nutrition - Nitrogen May cause “woodiness” of roots • Impede pathogen penetration/colonization May improve growth if nodulation is poor Could also have opposite impact • Interfering with nodulation • Promoting disease (?) • Liu et al. (2016) found that Rhizoctonia- diseased soybean came from soils with higher N levels Mycorrhizae In pea, have been shown to reduce • Aphanomyces colonization (Rosendahl 1985; Hilou et al. 2014) or • Aphanomyces-induced growth losses (Thygesen et al. 2004) Have other potential benefits to host plant • Nutrient acquisition • Abiotic stress tolerance

Hilou et al. 2014. Mycorrhiza 24: 45–54 Rosendahl 1985. J Phytopath 114: 31–40 Thygesen et al. 2004. Eur J Plant Path 110: 411–419 43 Treatments AMF: with or without commercial inoculum Nitrogen: • 0 kg/ha actual N, • 60 kg/ha actual N, or • 120 kg/ha actual N CDC Meadow pea CDC Maxim red lentil Cell-Tech, granular rhizobial inoculant Randomized complete block, 4 reps Results - Root rot in Swift Current 44 Pea Lentil 4.0 3.5 a b a a b SE SE a 3.0 ± 3.5 a

± b 7)

- a 5)

- 2.5 3.0 2.0 2.5 1.5 No AMF No AMF AMF2.0 AMF 1.0 1.5 0.5

Root rot severity(1 Rootrot 1.0

Root rot severity (0 rot Root 0.0 0 60 120 0 60 120 Nitrogen rates (kg/ha) Nitrogen rates (kg/ha)  Nitrogen-fertilized crops had lower root rot scores than unfertilized plants • On the “Aphanomyces” (0-5) scale for pea, • On the “Fusarium” (1-7) scale for lentil,  Commercial AMF inoculum had no impact Results – Indian Head & Melfort 45 Indian Head: Melfort: • N-fert helped pea, • Neither N-fert nor AMF but not lentil helped • AMF did not help

10 pea plants 120 kg N/ha + AMF Nitrogen fertilization of pulses

Sometimes “starter” N is recommended • Low rates (~10-15kg/ha)

Pros Cons Might reduce yield losses due to root rot Has costs: • Financial • Nitrogen balance

46 Biologicals

 Compete with pathogens  Stimulate root growth/health  Antimicrobial compounds/activities  Other modes of action  Potential organisms or products: • Pseudomonads – antibiotic compounds • Streptomyces – antibiotic compounds • Trichoderma (RootShield) - competition • Clonostachys rosea - ? • Saponins (HeadsUp) Remember this from the oats? • Others Bacterial antagonists – research ongoing

Bacteria from SK fields Tested in • Petri plates • Greenhouse • Outdoors Aphanomyces growth stopped on Petri plates

Aphanomyces Bacteria Greenhouse

Control Pathogen Pathogen + bacteria

Pea: CDC Meadow

Bacteria added in liquid

Aphanomyces cultured in oatmeal broth 9 bacterial selected from greenhouse

Dr. Zakir Hossain Outdoor experiment 2019

Plants just before flowering Conclusions

Root rots of pulses are serious and complicated Different pulse crops have different pathogens Management: • Crop rotation and • Avoidance of high risk fields • Weaker evidence for other approaches Research continues! Acknowledgements

 We thank C. Vucurevich, A. Erickson, N. Thangam, T. Dubitz, G. Daniels, D. Burke, L. Poppy, L. Syrovy, W. May, R. Davies, G. Peng, S. Ginter, B. Evans, S. Campbell and numerous laborers and students.

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