This document summarizes a comparison of stem rust in oats and yellow rust in wheat in Sweden. It finds that stem rust, primarily affecting oats, shows variation expected from a sexually reproducing population, while yellow rust, primarily affecting wheat, can easily survive systemic infection and has a green bridge, allowing it to persist clonally. Sexual reproduction is necessary for stem rust epidemiology but not for yellow rust in the Swedish cropping system. A model is described that could help understand how dominant clones of pathogens appear and are replaced over multiple seasons.

1. A comparison of stem rust in
oats and yellow rust in wheat:
A Swedish example
J. Yuen, A. Berlin, K. Gillen
Department of Forest Mycology and Plant Pathology, SLU
Y. Jin, USDA Cereal Disease Laboratory

2. Disposition
o Comparison of two
rust diseases in
Sweden
o Stem rust (primarily on
oats)
o Stripe rust (primarily
on wheat)

3. Where did he work?

4. The ’Botanical Section’

5. From Eriksson and Henning, Die Getrideroste (1896)

6. Stem rust in oats grown in Sweden
shows the variation expected from a
sexually reproducing population
Photos: Anna Berlin

7. A collection of oat stem rust
samples from Sweden
Population
Location
Variety
Day of
collectiona
N
G/N
Na
FIS
Ho
He
Ia
p
1
Fransåker
Belinda
01.08.08
27
1.00
62
0.487
0.329 (0.062)
0.618 (0.044)
0.509
0.563
2
Ingvasta
Ivory
06.08.08
29
1.00
45
0.333
0.363 (0.074)
0.526 (0.062)
0.341
0.045
3
Evertsholm
Ingeborg
11.08.08
30
0.93
41
0.133
0.472 (0.085)
0.533 (0.057)
0.184
0.145
4
Skarpenberga
Belinda
11.08.08
28
1.00
46
0.250
0.388 (0.061)
0.503 (0.045)
0.129
0.290
5
Bettna
Belinda
13.08.08
28
1.00
44
0.057
0.470 (0.087)
0.487 (0.065)
0.164
0.098
6
Bränne Övregård
Svava
13.08.08
30
0.90
44
0.054
0.436 (0.090)
0.449 (0.074)
-0.003
0.485
7
Pattala
Belinda
13.08.08
27
1.00
38
-0.028
0.501 (0.091)
0.477 (0.058)
0.108
0.125
8
Ultuna
Ivory
22.08.08
22
1.00
44
0.167
0.413 (0.071)
0.481 (0.063)
0.089
0.281
9
Hjälmarsholm
Kerstin
26.08.08
26
1.00
56
0.333
0.350 (0.066)
0.510 (0.062)
0.073
0.832
10
Götala
Ivory
26.08.08
25
1.00
56
0.244
0.443 (0.087)
0.567 (0.054)
-0.215
1.000
11
Skarpenberga
Belinda
30.07.09
28
1.00
60
0.277
0.419 (0.067)
0.564 (0.061)
0.389
0.149
12
Stäholm
Kerstin
04.08.09
28
1.00
50
0.262
0.398 (0.059)
0.524 (0.061)
0.024
0.649
13
Fransåker
Belinda
04.08.09
30
1.00
61
0.306
0.424 (0.050)
0.593 (0.053)
-0.083
0.665
14
Ingvasta
Ivory
05.08.09
26
1.00
55
0.449
0.330 (0.047)
0.578 (0.042)
0.063
0.661
15
Bränne Övregård
Kerstin
06.08.09
29
1.00
55
0.266
0.422 (0.047)
0.560 (0.047)
-0.096
0.584
16
Klostergården
Dala
Belinda
07.08.09
30
1.00
38
0.130
0.421 (0.067)
0.474 (0.066)
0.332
0.002
17
Evertsholm
Belinda
17.08.09
29
1.00
54
0.164
0.438 (0.065)
0.511 (0.067)
-0.049
0.852
Table 2. Details of population genetic diversity in Puccinia graminis f.sp avenae at 11 microsatellite loci
Abbreviations: N, Number of samples; G/N, number of genotypes divided by number of samples; Na, number of observed alleles;
FIS, inbreeding coefficient in relation to subpopulation; Ho, observed heterozygosity (s.e. in parenthesis); He, expected
heterozygosity (s.e. in parenthesis); IA, Index of Association and its p-value.
aDay of collection, dd.mm.yy
Berlin et al, 2012

8. Most variation within fields
Source
df
SS
MS
Est. Var.
%
p-value
Among Populations
16
698.7
43.7
1.3
13%
<0.001
Within Populations
450
3975.3
8.8
8.8
87%
Totala
466
4674.0
10.1
100%
Among Varieties
4
96.2
24.1
0.2
2%
<0.001
Within Varieties
411
3990.4
9.7
9.7
98%
Totala
415
4086.6
9.9
100%
Among Years
1
97.2
97.2
0.4
4%
<0.001
Within Years
438
4315.4
9.9
9.9
96%
Totala
439
4412.6
10.3
100%
Table 4. Analysis of Molecular Variance (AMOVA) within and among Puccinia graminis f.sp avenae populations,
collected from different varieties and collected 2008 and 2009 based on 11 microsatellite markers.
a Clone correction prior to each AMOVA yields different numbers of total observations
Berlin et al, 2012

9. Barberry is common
in Sweden since the
repeal of the
’Barberry eradication
law’ in 1994.

10. Puccinia graminis on Berberis vulgaris
Photographs A. Djurle

11. f.sp avenae
f. sp. tritici/
secalis
Puccinia
arrhenatheri
Photos: Anna Berlin
and Iuliia
Kyaschenko

12. The material from the grass
host can be related to the aecia
Berlin et al, 2012

13. From Eriksson and Henning, Die Getrideroste (1896)

14. Photograph Kerstin Gillen

15. Analysis of P. striiformis with
microsatellite markers

16. A comparison of 2
pathosystems in Sweden
o Oat stem rust
o Spring sown crop
o Localized infection
o Hard to survive as
uredinia or
urediniospores
o No green bridge
o Early infections seen after
aecia production
o Early populations are
from sexual reproduction
o Wheat stripe rust
o Both fall and spring sown
o Systemic infection
o Easy to survive in plants
due to systemic infection
o Green bridge
o Earliest infection seen on
fall sown crops
o Early infections are from
clones

17. The role of sexual reproduction
in the disease epidemiology
o For some pathosystems sexual reproduction is required
• White mold on oil-seed rape caused by Sclerotinia
sclerotiorum
o For others, sexual reproduction is not necessary or is
even unknown
• Soybean rust caused Phakopsora pachyrhizi
o For some, sexual reproduction can take place but it can
have a varying effect on disease epidemiology
• Rust diseases in cereals caused by different Puccinia
species
• Phytophthora infestans on potato and tomato

18. Facultative sexual reproduction
o Pathosystems that can have sexual reproduction
o Obligate sexual reproduction?
o Classification has to be based on pathogen biology as
well as cropping system
o Oats is only spring sown in Sweden
o Thus stem rust on oats in Sweden has ’obligate sexual
reproduction’
o Spring sown oats in a warmer climate or fall-sown oats
could have survival as uredinia and thus have ’facultative
sexual reproduction’ if the alternate host was present

19. A model
comparing early
and late infection
shows that the
earlier infections
will dominate in
the population

20. Can we classify P. striiformis?
o Is the alternate host present (??)
o Both fall and spring sown wheat crops in Sweden
o Examination of aecia from barberry in nature has
revealed only P. graminis and P. arrhenatheri
o Facultative sexual reproduction
o How easy would it be to see the immediate results of
sexual reproduction?

21. Can address this question with
mathematical models
o Expand the model previously described (based on a Lotka-
Volterra model for competition)
o Original model addressed early versus late infection
• The individuals that come early will dominate in the epidemic
• Infections from aeciospores of Pst would have difficulty in
competing with the urediniospores from the overwintering crop
o Expand the model to many seasons and many clones
• Varying fitness, introduction of new individuals, and Muller’s
ratchet can duplicate what we see with the appearance (and
subsequent disappearance) of dominant clones

22. Model Multiple seasons and many
clones
o Begin with population of 200 clones with varying fitness
—each randomly drawn from a distribution with fixed
mean and distribution
o Simulate 100 seasons allowing for competition with
Lotka-Volterra
o Muller’s ratchet slightly decreasing the fitness of each
individual each year
o Initial inoculum each year a function of the final clone
population size the previous year
o Add a new individual each year with random fitness
drawn from the original distribution, replacing the least fit
individual.

23. Results of a model that simulates the
appearance, persistence, and displacement
of dominant clones of a plant pathogen

24. Changes in
dominant
clones of P.
striiformis and
P. infestans

25. What would we see with P.
striiformis?
o Can P. striiformis reproduce sexually in Sweden?
• Alternate host present
• Both fall and spring sown wheat crops in Sweden
• Facultative sexual reproduction
o How easy would it be to see the immediate results of sexual
reproduction?
• Difficult to see immediately, but the introduction of a clone with
better fitness (possibly via sexual reproduction) will allow it to
eventually dominate in the population
• It would take several years before the new clone could be
detected
o This more fit clone can also be an immigrant clone!!

26. Söllingen, Niedersachsen 2013
Photograph courtesy Andreas Jacobi, Strube Research

27. Where is stem rust on wheat?
o Stem rust is rarely seen in wheat
o Alternate host of the pathogen is present
o Sexual reproduction of P. graminis s.l. clearly takes place
o Two possible reasons:
• Swedish wheat cultivars have sufficient resistance genes
that stem rust is not a problem
• Pgt has been eliminated from the pathogen population
• The stem rust we see is caused by another f.sp. that has
infected the wrong host....

28. Why no stem rust on wheat in
Sweden?
• Barberry present
• Severe epidemics on oats and natural grasses
• Some stem rust on rye
• Large genotypic variation within and between fields
• P. graminis is clearly completing its sexual cycle
• How closely related are Pgt and Pgs?
• Does wheat grown in Sweden have effective resistance
genes?
• Preliminary tests by the CDL indicates very few stem rust
resistance genes are present in Swedish wheat varieties

29. o How does the pathogen
survive?
o How is the crop grown?
o How do the different
individuals in the
pathogen population
interact (compete) with
each other?
o Understanding these
relationships is the key to
controlling the disease