Elements of disease management: breeding for resistance and influence of cultivation methods

Based on lecture presentations by Helge Skinnes and Morten Lillemo

PJH300 2017

Tittel på presentasjon Norwegian University of Life Sciences 1 Elements of disease management: breeding for resistance and influence of cultivation methods: outline

• ( list of Norwegian, English and scientific names of some major cereal fungi diseases) • The disease triangle • Types of disease resistance Principles • Examples of diseases in cereals Elements/major types – air-borne pathogens – residue-borne pathogens – seed-borne pathogens • Disease control strategies Mandatory for JPH300-2017 – Variety mixtures – Integrated control – Risk assessment

2 Diseases in Cereals SYKDOMMER – diseases in cereals. • • BIOTROFE- biotrophic • MJØLDOGG- Mildew (Blumeria graminis) • SVARTRUST – stem rust, black rust (Puccinia graminis) • GULRUST- Yellow rust (Puccinia striiformis)

• NEKROTROFE- necrotrophic • AKSPRIKK- Glume blotch (Stagnospora nodorum) • BLADPRIKK- Leaf blotch (Mycosphaerella graminicola) (Mycosphaerella graminicola) • BYGG BRUNFLEKK- Net blotch (Pyrenophora teres (Drechslera Teres)) • HAVRE BRUNFLEKK- Leaf blotch (Drechslera avenae) • GRÅ ØYEFLEKK- Scald (Rynchosporium secalis) • FUSARIUM- (Fusarium spp.)

Tittel på presentasjon Norwegian University of Life Sciences 3 SYKDOMMER – diseases in cereals. • • • FOTSYKE- foot rot disease • ROTDREPER- Take all (Gaumanomyces graminis) • STRÅKNEKKER- Eyespot/strawbreaker (Pseudocercosporella herpotrichoides) • • FRØ- OVERFØRTE – seed- borne • STRIPESYKE- stripe (Drechslera graminea) • DEKKET SOT- Covered smut (Ustilago hordei) • NAKEN SOT- Loose smut (Ustilago nuda) • STINKSOT- Common bunt (Tilletia caries) • DVERGSTINKSOT- Dwarf bunt (Tilletia contraversa) • KARNAL BUNT- Carnal bunt (Tilletia indica) • • OVERVINTRINGS SOPPER – snow moulds • SNØMUGG- Pink snow mould (Microdocium nivale) • TRÅDKØLLE- Speckled snow mould () • STORKNOLLET RÅTESOPP- snow mould (Sclerotinia borealis).

https://www.plantevernleksikonet.no/

Tittel på presentasjon Norwegian University of Life Sciences 4 Effect of cropping system on severity of cereal pathogens.

Cropping system Dispersion by Epidemic Seed Plant pathogens debris Cereals after cereals and/ ??? or with reduced tillage Conventional with ??? rotation Conventional winter ???

Ecological with rotation ???

Organic Cereals after ??? cereals The disease triangle

Disease

Favourable environment • Epidemic is the result of an interaction between a virulent pathogen on a susceptible host in an environment that favors the pathogen.

6 Diseases in Cereals Disease resistance • Most plants are resistant to most pathogens • Disease is an exception! • What causes this exception is the pathogen’s ability to overcome resistance mechanisms in the plant • Two types of resistance: –Race specific –Race non-specific

7 Diseases in Cereals Race specific resistance • Based on single genes • Gene-for-gene relationship • Often complete protection • Popular among plant breeders –Easy to select for –Simple genetics –Appealing phenotype

8 Diseases in Cereals Race specific resistance • However,… –Based on the plant’s ability to detect a single effector molecule from the pathogen –A single mutation in the pathogen can render the plants completely susceptible • Result: –Short durability

9 Diseases in Cereals Airborne pathogens with high evolutionary potential • Powdery mildew, Blumeria graminis

• Stem rust, Puccinia graminis

• Leaf rust (brown rust), P. triticina

• Stripe rust (yellow rust), P. striiformis

• Average lifetime of race-specific resistance genes: 3-5 years

https://www.plantevernleksikonet.no/ https://www.plantevernleksikonet.no/l/oppslag/1235/

10 Diseases in Cereals • Caused by Blumeria Powdery mildew graminis • Different formae speciales attack wheat, barley, oats and • Colonize epidermal cells of the leaf • Obligate biotrophic pathogen that only survives on living plant material

11 Diseases in Cereals Powdery mildew life cycle

Diseases in Cereals 12 Cleistothecium: globose, completely closed ascocarp, filled with asci that contain 4 or 8 ascospores Powdery mildew on wheat in  Hamar area: – Stable snow cover – Sexual reproduction at the end of the season Hamar – Local adapted populations of B. graminis f.sp. tritici survive on winter wheat

 Oslo area: Oslo – Unstable snow cover – New inoculum from Southern Sweden and Denmark every year

Short durability of race- specific resistance Wind direction Skinnes (2002)

13 Diseases in Cereals Recent spring wheat varieties in Norway • Polkka – Released 1992 – susceptible 1992 •Brakar – Released 1995 – susceptible 1996 •Avle – Released 1996 – susceptible 1999 • Zebra – Released 2001 – susceptible 2003 •Bjarne – Released 2002 – susceptible 2004

14 Diseases in Cereals Why short durability • Airborne pathogens – spores can be dispersed over hundreds of km • Short generation time (Polycycle) • Big population size • Sexual reproduction • Same resistance gene deployed in varieties over a large area • Survival of the pathogen between growing seasons

15 Diseases in Cereals Race non-specific resistance • Also called partial or horizontal resistance • Quantitative inheritance – based on several genes with additive effects • Equal effects against all races of the pathogen • Only partially effective, but retards disease development • High durability

16 Diseases in Cereals Genetics of partial resistance

100 Susceptible

1 to 2 minor genes % rust

2 to 3 minor genes

4 to 5 minor genes 0

Time

17 Diseases in Cereals Race specific vs partial resistance Severity (%) of powdery mildew in European spring wheat ringtest 2001:

30 Partial resistance can be highly effective 25 against powdery mildew in wheat Germany 20 France Norway 1 15 Norway 2 10 Finland Switzerland 5

0 NK98523 Naxos

18 Diseases in Cereals Partial resistance is based on different mechanisms

Naxos Saar NK93602

19 Diseases in Cereals Stripe rust on wheat in UK Cultivar Genes Released Susceptible

Rothwell Perdix Yr1, (Yr2, Yr6) 1964 1966

Maris Ranger Yr3a, Yr4a, Yr6 1968 1969

Talent Yr7 1973 (planned) 1972

Clement Yr2, Yr9 1975 1975

Stetson Yr1, Yr9 1983 1983

Hornet Yr2, Yr6, Yr9 1987 1988

Brigadier Yr9, Yr17 1993 1996

Boyd (2005)

20 Diseases in Cereals https://www.plantevernleksikonet.no/l/oppslag/1235/ http://www.cpm-magazine.co.uk/2017/01/07/yellow-rust-quest-quell-shapeshifter/ Last accessed 31/10/2017 Tittel på presentasjon Norwegian University of Life Sciences 21 http://www.cpm-magazine.co.uk/2017/01/07/yellow-rust-quest-quell-shapeshifter/ Last accessed 31/10/2017 Tittel på presentasjon Norwegian University of Life Sciences 22 Stem rust

• Caused by Puccinia graminis • Historically the most important disease on wheat in terms of damage • Can also affect wheat, barley, oats, and rye • Barberry important as alternative host • Severe yield losses in Europe before the 1900s • Big epidemics in USA and Canada in 1916 and 1935

23 Diseases in Cereals Stem Rust

24 Diseases in Cereals Tittel på presentasjon Norwegian University of Life Sciences 25 Stem rust kept under control

Erradication of Barberry (Berberis vulgaris) Breeding of resistant cultivars – partial resistance conferred by Sr2 and other genes – race-specific resistance – Sr31 on the 1B/1R translocation effective for several decades No serious outbreak in Europe and since the 1950s

26 Diseases in Cereals Ug99 – a new threat to global wheat production • Most wheat cultivars across the world have resistance based on a single gene – Sr31 • New virulence to this gene appeared in Uganda in 1999 and is now spreading rapidly

An epidemic of stem rust on wheat caused by race TTKSK (e.g. isolate Ug99) is currently spreading across Africa, and the Middle East Wikipedia last assessed 24.10.2016

27 Diseases in Cereals https://en.wikipedia.org/wiki/Ug99 Dissemination of resistant cultivars is urgent!

28 Diseases in Cereals La

Tittel på presentasjon Norwegian University of Life Sciences 29 Last accessed 31/1072017 Residue-borne diseases • All cereals: –Fusarium Head Blight, Fusarium spp. • Wheat: –Septoria Leaf Blotch, Septoria tritici –Stagonospora Glume Blotch, Stagonospora nodorum •Barley: –Barley scald, Rhynchosporioum secalis –Net blotch, Pyrenophora teres

30 Diseases in Cereals Fusarium Head Blight (FHB)

• Caused by Fusarium graminearum, F. culmorum and other Fusarium spp. • A major disease problem in all cereals • Leads to accumulation of mycotoxins in the grain

31 DETTE ER TITTELEN PÅ PRESENTASJONEN Fusarium Head Blight (FHB)

Mycotoxins

32 DETTE ER TITTELEN PÅ PRESENTASJONEN Fusarium Head Blight (FHB) • Has become a major disease worldwide since the 1990s. • Heavy epidemics in the Mid West of the USA (Minnesota, North Dakota) coincided with the introduction of reduced tillage –pathogen survives in the plant residues • Other factors that promote FHB –cultivation of susceptible wheat and barley varieties –crop rotation with maize –warm and humid weather –lodging https://www.plantevernleksikonet.no/l/oppslag/1239/

33 DETTE ER TITTELEN PÅ PRESENTASJONEN FHB in Norway • Pathogen population has changed (I. S. Hofgaard, Bioforsk) –F. avenaceum and F. culmorum dominated in the 1990s –F. graminearum now the dominating species • Worst problems in wheat and oats

34 DETTE ER TITTELEN PÅ PRESENTASJONEN Resistance breeding for FHB • No complete resistance • Resistance is quantitative and pathogen non-specific • Field testing is expensive, labour-intensive and not very reliable • Marker-assisted selection –genes tagged by molecular markers –selection based on DNA samples • A long-term breeding effort

35 DETTE ER TITTELEN PÅ PRESENTASJONEN Fusarium Head Blight (FHB)

• FHB is a good case for integrated control –ploughing –crop rotation (With what?) –resistant cultivars –fungicides

36 DETTE ER TITTELEN PÅ PRESENTASJONEN Fusarium Head Blight (FHB) • What can we do to combat FHB? – Ploughing or stubble burning effectively removes the inoculum but can have other side-effects • air pullution • soil erosion – Avoid crop rotation with other host species •Maize • Wheat, barley, rye, oats – Grow resistant cultivars • No cultivar with complete resistance yet • Partial resistance important in reducing the epidemics – Spray with fungicides • No fungicide with complete effect • Prothioconazole (Proline®) reduces infection levels to half when sprayed at time of flowering • Strobilurins applied at earlier growth stages against foliar diseases promotes FHB! 37 DETTE ER TITTELEN PÅ PRESENTASJONEN Fusarium spp./ mycotoxins in ecological vs. conventional cropping system Read Bernhoft et al. 2012 Influence of agronomic and climatic factors on Fusarium infestation and mycotoxin contamination of cereals in Norway).

• Generally less mycotoxins in ecological cropping system • Fungicides in conv. system increase Fusarium severity • Herbicides in conv. system increase Fusarium severity • Manure: less problems with toxins than artificial NPK • Low N reduce Fusarium level directly • Low N reduce Fusarium level indirectly with less lodging • More ploughing in ecological system reduse Fusarium severity Septoria tritici leaf blotch (Mycosphaerella graminicola)

• Caused by Mycosphaerella graminicola • Transferred by plant debris from previous season

39 Diseases in Cereals The Septoria life cycle

Septoria is a splash-dispersed pathogen

40 Diseases in Cereals Damage caused by Septoria tritici • Pycnidiospores are dispersed by ‘splashy’ rain from plant debris and infected leaves

Promoted by – warm and humid weather – dense plant canopy – high levels of N fertilization Necrotic lesions destroys the photosynthetic capacity of the leaves Results in poor grain filling and lower yield

41 Diseases in Cereals Resistance to Septoria tritici blotch • Varieties have varying degrees of resistance • Both race specific and race non-specific resistance is important • No complete resistance available, but important in delaying the epidemics • Tall plants tend to get less disease

42 Diseases in Cereals Control of Septoria tritici blotch

• Cultivation of resistant cultivars –delays the epidemic –less inoculum carried over to next year • Crop rotation • Removal of plant residues by proper tillage • Fungicides are effective, but should be used wisely

43 Diseases in Cereals Fungicide resistance is a problem • Septoria quickly developed resistance to MBC fungicides (Benzimidazole) after their introduction in the 1960s • Strobilurins were introduced in 1997 and resistance appeared in 2003 (data from UK):

 The only remaining group of effective fungicides are the azoles (imidazoles and triazoles; DMIs)

44 Diseases in Cereals Seed-borne diseases • Loose smut, Ustilago nuda • Barley stripe, Pyrenophora graminea • Ergot, Claviceps purpurea • Common bunt (stinking smut), Tilletia tritici

45 Diseases in Cereals Loose smut

• Caused by Ustilago nuda • Attacks barley and wheat • Transferred by seeds as dormant mycelium within the embryo • Grows systematically within the plant • Produces teliospores in the head of infected plants instead of flowers

46 Diseases in Cereals Epidemiology of loose smut

• Spread by wind to neighbouring plants at flowering • Dormant mycelia established in the embryo of developing grains • Favoured by warm and humid conditions at flowering

47 Diseases in Cereals Control of loose smut

• Resistance is available in both wheat and barley • Varieties with closed flowers tends to escape infection to a higher degree than open- flowering varieties • Avoid infection by use of clean seed from un- infected fields • Seed treatment with systemic fungicides • Heat treatment of seeds: new method, first investigated due to the need for control of seed borne disease in organic farming. Now (2016) the standard seed treatment at FK

48 Diseases in Cereals Barley stripe • Caused by Pyrenophora graminea / Drechslera graminea) • Transferred by infected seeds • Grows systematically in the plant • Produces toxins that kill the leaf cells • Sporulates in the dead leaf tissue under moist conditions

49 Diseases in Cereals Barley stripe • Spores spread by wind to heads of neighbouring plants at flowering • Germinates and causes infection under moist conditions • Stays as dormant mycelium in infected kernels

50 Diseases in Cereals Control of barley stripe

• Race-specific resistance is present in some varieties • Use of non-infected seed • Seed treatment with fungicide • Heat treatment of seeds: new method, first investigated due to the need for control of seed borne disease in organic farming

51 Diseases in Cereals Disease control strategies

• Fungicides work well for most pathogens, but there are alternatives! • Important to know the biology and life-cycle of the pathogen Disease • Use of variety mixtures • Integrated disease control • Risk assessment Favourable environment

52 Diseases in Cereals Powdery mildew is favoured by high levels of N fertilization Mildew severity in Catrin spring barley as affected by N- application (kg/haa). Experiment from Denmark.

NB: typical response for a biotrophic polycycle diseases

53 Diseases in Cereals Disease control by mixtures • Two types of mixtures –multiline varieties –variety mixtures • The idea is to slow down the epidemic by having a genetically diverse host • Conditions where mixtures are most effective –polycyclic airborne pathogens –gene-for-gene relationships • Less effective for –residue- and seed-borne pathogens –partial resistance

54 Diseases in Cereals How do variety mixtures work?

• Rate of development of pathogen is reduced. – Genotype with different resistance act as barrier – Infection of the same genotype (autoinfection) is reduced • Diversity of inoculum is favoured – Possibility for avirulent isolates to survive - not necessary with new virulences – Reduced selection for new mutant/recombined virulence genes – Reduced selection for fitness of individual pathogen race • Competitive/resistant plant genotypes favored • Non-virulent pathogens induce resistance

55 Diseases in Cereals How to make mixtures • Number of components at least 3-4 • Functional diversity important • Equal amount of components • Uniformity for maturity • Uniformity for quality • Breeding for mixing ability

56 Diseases in Cereals Effect of number of components in mixture of winter barley cultivars on Rhynchosporium infection, and on yield with or without fungicides

(Newton et al., Scottish Crop Res. Inst.) 57 Diseases in Cereals Application of mixtures in practice

• Often used for animal feed from cereals • More difficult, but possible for bread and beer production • High quality coffee without rust • Grassland and forage cereals (species mixtures) • Grass and cereals mixed with legumes • ”Extenso” cereal prod. in Switzerland without fungicides, insecticides and growth regulators supported financially

58 Diseases in Cereals Variety mixtures in spring barley for mildew control in Eastern Germany

Infection Fungicide use Area sown with varity mixtures

59 (Barley GeneticsDiseases in Cereals VI (1992), p. 1063) Critical environment for establishment of pathogen

Powdery mildew Moderate temperature and humidity Yellow rust Mild winter, cool/humid summer Leaf/ glume blotch Cool at early growth phase, diseases then frequent rainfall Barley stripe Cool at vegetative growth phase

Loose smut Humidity during flowering, moderate temp. at germination Common bunt Humidity and low temperature at germination. Dispersion of inoculum of fungal pathogens in cereals. Wind Seeds Plant debris

Mildew X Yellow rust X Net blotch of barley X X Leaf blotch of oats X X Scald (X) X Glume/leaf bl. wheat X X Fusarium spp. XX Pink snow mould XX Barley stripe X Loose smut X Covered smut X Common bunt X Take all X Strawbreaker X Speckled sn. mould Sclerotinia sn. mould Effect of cropping system on severity of cereal pathogens.

Cropping Epidemic Disper- sion by system pathogens Seed Plant debris Cereals after cereals Constant Constant Increase and/ or with reduced tillage Conventional with Constant Constant Reduce rotation Conventional winter Increase Constant Increase wheat Ecological with rotation Reduce * Reduce Organic Cereals after Reduce * Increase cereals * Increased, can now be controlled by thermotreatment Five evolutionary forces to consider (after McDonald & Linde 2002)

1. Mutation • the ultimate source of genetic variation 2. Population size • bigger populations have more mutants 3. Gene flow • Increases the genetic diversity 4. Reproduction system • Sexual reproduction increases genetic diversity • Most damaging pathogens have both sexual and asexual reproduction 5. Selection • Promoted by wide-spread cultivation of varieties with the same race-specific resistance genes

63 DETTE ER TITTELEN PÅ PRESENTASJONEN Risk assessment (McDonald & Linde 2002)

64 DETTE ER TITTELEN PÅ PRESENTASJONEN Strategies for resistance breeding

65 Diseases in Cereals Large scale heat treatment of cereal seeds now in Norway

• It has also a benefitial efffect on germination,

• https://www.youtube.com/watch?v=wFKrP2nbopA

• Unfortunately it does not specify which disease are controlled best • In 2015 seed batch from 2013 that had been thermotreated germinated poorly in 2015 (this regards seeds prepared for 2014, but used in 2015)

Tittel på presentasjon Norwegian University of Life Sciences 66 Learn more – from Youtube • Fusarium • https://www.youtube.com/watch?v=RjDWf8ohj4A

Tittel på presentasjon Norwegian University of Life Sciences 67 Some good films about cereal diseases- in Spanish. • Rusts • https://www.youtube.com/watch?v=pvIqN5towZo • Powdery mildew • https://www.youtube.com/watch?v=N77_i9e4FJc • Septoria • https://www.youtube.com/watch?v=ktOX_2Na3m8 • Fusarium • https://www.youtube.com/watch?v=6Mg428V7H34 • Scald (Barley and Rye) • https://www.youtube.com/watch?v=prkg4KrxvqM

Tittel på presentasjon Norwegian University of Life Sciences 68