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The worldwide Pst population structure and its temporal maintenance in Pakistan
Sajid Ali
The University of Agriculture, Peshawar, Pakistan &
Aarhus University, Denmark
#bgri2014

In the context of invasion Pst: Puccinia striiformis f.sp. tritici
PstS1 &
PstS2
2000
2003
Post-2000
Cases of recent invasions in Pst
Australia
1979
South American
Early 1900s
South African population
1996
“Warrior-Kranich” type strains in Europe
2011-present
North American
Early 1900s
Virulence to Yr9
1986
1998
(Milus et al., 2006, Hovmøller et al., 2008; Wellings et al., 2004; Singh et al., 2004)
Population subdivision for this long distance migrating
pathogen?

Worldwide Pst population structure
Worldwide representative set of 409 isolates, selected from INRA, France and AU, Denmark collection
Genotyped with 20 SSR markers

FST values for geographically spaced populations
NW
Europe
Mediterranean
Region
Central A
sia
East A
frica
Middle E
ast
Nepal
Pakistan
China
NW Europe - 0.420 0.380 0.500 0.380 0.370 0.410 0.390
Mediterranean Region 0.000 - 0.020 0.150 0.009 0.280 0.280 0.390
Central Asia 0.000 0.030 - 0.160 0.040 0.230 0.260 0.340
East Africa 0.000 0.000 0.000 - 0.140 0.380 0.280 0.540
Middle-East 0.000 0.020 0.000 0.000 - 0.260 0.250 0.360
Nepal 0.000 0.000 0.000 0.000 0.000 - 0.220 0.210
Pakistan 0.000 0.000 0.000 0.000 0.000 0.000 - 0.450
China 0.000 0.000 0.000 0.000 0.000 0.000 0.000 -
Non-significant FST values (> 0.01) are shown in bold.
(Ali et al. 2014; PLOS Pathogens)
Worldwide population subdivision

Assignment with STRUCTURE at different K-values
K2
K3
K4
K5
K7
K6
K8
China
Nepal
Pakistan
Middle-‐East
Central Asia
Medite
rranean
region
NW Europe
East Africa
(Ali et al. 2014; PLOS Pathogens)
Worldwide population subdivision

Discriminant analysis of principal components (ADEGENET) Identification six distinct genetic groups of Pst
(Ali et al. 2014; PLOS Pathogens)
Worldwide population subdivision
NW Europe
ChinaNepal
Pakistan
Central Asia-‐Mediterranean
region
Eigen values’ contribution Number of clusters
BIC
CMiddle East-‐East Africa
A
200 300 400 500 600
2 4 6 8 10
B

France G1G2G3G4G5G6HUn
Azerbaijan G1G2G3G4G5G6HUn
France G1G2G3G4G5G6HUn
Kyrgyzstan G1G2G3G4G5G6
Eritrea G1G2G3G4G5G6
Afghanistan G1G2G3G4G5G6
Cyprus G1G2G3G4G5G6
Iran
Israil G1G2G3G4G5G6
Lebanon G1G2G3G4G5G6
Turkey G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Morocco
G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Tunisia G1G2G3G4G5G6
Nepal G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Pakistan G1G2G3G4G5G6
China G1G2G3G4G5G6
- Geographically spaced genetic groups identified
(Ali et al. 2014; PLOS Pathogens)
Worldwide population subdivision and source of recent invasions
Denmark G1G2G3G4G5G6HUn
Sources of these recent invasions?
Early 1900s
1979 1996
2003
2000
Early 1900s

FST Values
NW
Europe
North
Am
erica
South A
merica
Mediterrane
an Region
Central A
sia
South Africa
East A
frica
Middle E
ast
Nepal
Pakistan
China
NW Europe - 0.039 0.001 0.420 0.380 0.498 0.500 0.380 0.370 0.410 0.390 North America 0.100 - 0.046 0.409 0.368 0.485 0.490 0.378 0.364 0.400 0.398 South America 0.410 0.100 - 0.435 0.396 0.514 0.511 0.393 0.379 0.416 0.405 Mediterranean Region 0.000 0.000 0.000 - 0.020 0.109 0.150 0.009 0.280 0.280 0.390 Central Asia 0.000 0.000 0.000 0.030 - 0.044 0.160 0.040 0.230 0.260 0.340 South Africa 0.000 0.000 0.000 0.010 0.190 - 0.229 0.160 0.298 0.314 0.419 East Africa 0.000 0.000 0.000 0.000 0.000 0.006 - 0.140 0.380 0.280 0.540 Middle-East 0.000 0.000 0.000 0.020 0.000 0.000 0.000 - 0.260 0.250 0.360 Nepal 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 - 0.220 0.210 Pakistan 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 - 0.450 China 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 - FST for aggressive strains 0.420 0.408 0.434 0.000 0.010 0.099 0.150 0.010 0.270 0.270 0.390
P-value for aggressive strains 0.000 0.000 0.000 0.860 0.070 0.040 0.000 0.020 0.000 0.000 0.000
Non-significant FST values (> 0.01) are shown in bold.
(Ali et al. 2014; PLOS Pathogens)
Worldwide population subdivision

STRUCTURE G1 G2 G3 G4 G5 G6
America
China
Nep
al
Pakistan
Middle-‐East
Central A
sia
Med
iterranean
region
NW Europ
e
South Africa
PstS1 and PstS2
PstS3
East Africa
G1 G2 G3 G4 G5 G6 DAPC
Recent invasions
(Ali et al. 2014; PLOS Pathogens)
Source of recent invasion

France G1G2G3G4G5G6HUn
Azerbaijan G1G2G3G4G5G6HUn
France G1G2G3G4G5G6HUn
Kyrgyzstan G1G2G3G4G5G6
Eritrea G1G2G3G4G5G6
Afghanistan G1G2G3G4G5G6
Cyprus G1G2G3G4G5G6
Iran
Israil G1G2G3G4G5G6
Lebanon G1G2G3G4G5G6
Turkey G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Morocco
G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Tunisia G1G2G3G4G5G6
Nepal G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Pakistan G1G2G3G4G5G6
China G1G2G3G4G5G6
- Geographically spaced genetic groups identified - Sources of recent invasions identified
(Ali et al. 2014; PLOS Pathogens)
Worldwide population subdivision and source of recent invasions
Diversity and recombinaIon in the
worldwide populaIons?

Recombination in Pakistan, Nepal and China
(Ali et al. 2014; PLOS Pathogens)
Diversity and recombination in worldwide populations
High genetic and genotypic diversity in Pakistan, Nepal
and China

France G1G2G3G4G5G6HUn
Azerbaijan G1G2G3G4G5G6HUn
France G1G2G3G4G5G6HUn
Kyrgyzstan G1G2G3G4G5G6
Eritrea G1G2G3G4G5G6
Afghanistan G1G2G3G4G5G6
Cyprus G1G2G3G4G5G6
Iran
Israil G1G2G3G4G5G6
Lebanon G1G2G3G4G5G6
Turkey G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Morocco
G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Tunisia G1G2G3G4G5G6
Nepal G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Pakistan G1G2G3G4G5G6
China G1G2G3G4G5G6
- Recombination and diversity in Himalayan and Near Himalayan regions
Diversity and recombination in PST worldwide populations
(Ali et al. 2014; PLOS Pathogens)

0.00
1.00
2.00
3.00
4.00
5.00
6.00
4 5 6 7
Telia
l pro
duct
ion
Weeks after inoculation
China
Nepal
Pakistan
Middle-East
Mediterranean
France
Telial progress curve for 56 PST isolates according to their geographical origin
Reduction in PST sexual reproduction ability in worldwide populations
(Ali et al. 2010; Fungal Genetics and Biology)

France G1G2G3G4G5G6HUn
Azerbaijan G1G2G3G4G5G6HUn
France G1G2G3G4G5G6HUn
Kyrgyzstan G1G2G3G4G5G6
Eritrea G1G2G3G4G5G6
Afghanistan G1G2G3G4G5G6
Cyprus G1G2G3G4G5G6
Iran
Israil G1G2G3G4G5G6
Lebanon G1G2G3G4G5G6
Turkey G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Morocco
G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Tunisia G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Nepal G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Pakistan G1G2G3G4G5G6
China G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Denmark G1G2G3G4G5G6HUn
- Centre of diversity in Himalayan and Near Himalayan - Reduction in sexual reproduction ability during ancestral invasion
(Ali et al. 2014; PLOS Pathogens)
Ancestral relaIonship of worldwide PST populaIons
Reduction in PST sexual reproduction ability in worldwide populations

Ancestral relationship among worldwide populations
Ch Np Pk Ch Np Pk Ch Np Pk Ch Np Pk
Ch Np Pk
(Ali et al. 2014; PLOS Pathogens)
ABC analyses with DIYABC (Cornuet et al., 2008)

The six genetic groups together
Ancestral relationship among worldwide populations
(Ali et al. 2014; PLOS Pathogens)

Mexico G1G2G3G4G5G6
Nepal G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Pakistan G1G2G3G4G5G6
China G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Azerbaijan G1G2G3G4G5G6HUn
France G1G2G3G4G5G6HUn
Kyrgyzstan G1G2G3G4G5G6
Eritrea G1G2G3G4G5G6
Afghanistan G1G2G3G4G5G6
Cyprus G1G2G3G4G5G6
Iran
Israil G1G2G3G4G5G6
Lebanon G1G2G3G4G5G6
Turkey G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
Yemen G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Morocco
G1G2G3G4G5G6
France G1G2G3G4G5G6HUn
Tunisia G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Early 1900s
1979 1996
Denmark G1G2G3G4G5G6HUn
2000
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
Mexico G1G2G3G4G5G6
?
- The worldwide spread with population subdivision and loss of sexual reproduction - PST possibly originated in the Himalayan and Near Himalayan region
- Re-emergence linked with the recent invasions
Overall conclusions on worldwide populations
(Ali et al. 2014; PLOS Pathogens)

Khyber PeshawarNowshera
HaripurAbbottabad
TanawalMansehra
Attarshisha
BalakotSiran
Battal
Oghi
Skardu
Battagram
Islamabad
KASHMIR
PAKISTAN
Berberis zone
Non-Berberis zone
Sampled in 2010
Sampled in 2011
Off-seasonBerberis zone
200 km
Pakistani PST population; a high genetic diversity
Temporal maintenance of Pakistani PST populaIons

Development of rapid genotyping DNA extraction à Directly from infected lesion
(Ali et al. 2011; BMC Research Notes)
Pakistani PST population; a high genetic diversity

ns
ns
ns ns
ns ns
ns ns ns ns ns ns
ns
ns
0
0.1
0.2
0.3
0.4
0.5
Heterozygosity
Geographical region
He Ho
Year Location Sample
size MLGs
Genotypic diversity
2010
Khyber 35 25 0.971 Peshawar 12 9 0.939 Nowshera 19 8 0.673 Haripur 42 20 0.864 Abbottabad 34 31 0.993 Mansehra 28 27 0.997 Battal 46 33 0.967 Battagram 9 9 1 Attarshisha 30 22 0.966 Balakot 24 18 0.975 Skardu 63 54 0.991
2011
Peshawar 33 23 0.973 Nowshera 16 10 0.825 Abbottabad 18 9 0.706 Mansehra 61 54 0.991 Tanawal 22 19 0.983 Siran 51 33 0.939 Oghi 19 16 0.977 Battal 35 30 0.99 Battagram 20 17 0.984 Attarshisha 40 31 0.953 Balakot 27 21 0.977
A high genotypic diversity and non-significant FIS
across all locations
(Ali et al. 2014; Molecular Ecology)
Pakistani PST population; a high genetic diversity

A high pathotypic diversity à 53 pathotypes out of 127 isolates tested With varying virulence frequencies across locations
Location Number of isolates
pathotyped No. of different
pathotypes detected No. of different
virulences detected Khyber 18 14 16 Peshawar 4 2 13 Nowshera 5 3 15 Haripur 20 13 15 Abbottabad 14 10 15 Mansehra 5 5 15 Battal 24 18 17 Battagram 6 6 15 Attarshisha 16 11 12 Balakot 11 11 16 Skardu 4 4 17
Maximum no. of virulences tested - 26 Maximum no. of pathotypes observed 53 -
- Vr2, Vr6, Vr7, Vr8, Vr9 and VrSu in a high frequency - Vr5, Vr15 detected - AvrVicto detected
Pakistani PST population; a high genetic diversity

Comparison of eight temporally sampled populations
Locations
Sample size FST between
2010 and 2011 Number of resampled MLGs and their frequency over two years*
Peshawar 45 0.0719 1 (5:3)
Nowshera 35 0.0863 1 (13:1)
Abbottabad 52 0.2375 1 (1:11)
Mansehra 89 0.0522 2 (2:2) (1:6)
Battal 81 0.0740 0
Battagram 29 0.0661 0
Attarshisha 70 0.1359 0
Balakot 51 0.0609 1 (1:5)
(Ali et al. 2014; Molecular Ecology)
Pakistani PST population; a high genetic diversity

- Resistance genes deployment considering the information on worldwide population subdivision and diversity
- Worldwide virulence structure to be re-analyzed
Overall conclusions and perspectives
- Future invasion risks assessment and management
- Broader perspective for breeders, considering invasions
- Role of sexual reproduction in PST biology in Pakistan and China
- What strategy to adapt while considering the Berberis spp.?

Current work: - Wheat sampling in 2013 in all
major PST regions
- To be SSR genotyped
- Berberis sampling from the Berberis zone
- Sequence characterization to identify the species (and f.sp.)
HEC-Start-up Research Grant
Rust-Fight Danish Council for Strategic Research
The University of Agriculture, Peshawar, Pakistan
Pakistani PST population; a high genetic diversity Current work

Thanks to all those who contributed to the
worldwide yellow rust collection
French project: EMERFUNDIS, ANR 07-BDIV-003 European Integrated Project: BIOEXPLOIT, FOOD-CT-2005-513959 Higher Education Commission, Pakistan

Thank you
Picture provided by Tarnab Agricultural Research Station, Peshawar, Pakistan