Reconstructing the history of Maize streak virus ... - RUN-Emerge

The emergence and spread of MSV in Africa
Darren Martin
University of Cape Town, South Africa

The history of maize streak disease
Maize introduced to West Africa by the
Portuguese in the early 1500s
Leaf chlorosis
Deformed cobs
Stunting
Yield losses of up to 100%
It reached southern Africa in the mid
1600s with the Dutch East India
Company
Maize streak disease was first described
in 1901 in southern Africa
It had affected maize there since at least
the 1870s suggesting that the maizeadapted
MSVs had already evolved by
the mid 1800s

MSV-A: The maize adapted MSV
There are 11 known MSV strains - they
are named MSV-A through MSV-K
MSV-K
MSV-A 4
MSV-C
MSV-A 6
MSV-D
MSV-E
MSV-A 3
MSV-B MSV-A 2
Other MSV strains
MSV-J
0.025 substitutions
MSV-I
per site
0.05 substitutions
per site
MSV-A
MSV-F
MSV-G
MSV-H
Other African streak viruses
MSV-A 1
Only MSV-A is known to cause serious
disease in maize
MSV-B to -K, collectively referred to as
“grass infecting” or non-maize adapted
MSVs – produce very mild symptoms in
even the most MSV-sensitive maize
genotypes
MSV-A classified into 5 subtypes/variants
Species > 75% identity
Strain > 89% identity
Subtype > 98% identity Digitaria sp.
Maize

Where did MSV-A come from?
Large-scale cataloguing of inter-strain MSV
recombination
Revealed clear evidence of recombination
hot-spots in non-coding regions
MSV-A variants are all descendants of the
recombinant progeny of ancestral MSV-B
and MSV-G/-F variants

Distributions of African streak viruses
African streak viruses
MSV
MSV-A
A 6
MSV
PanSV-G
MSV-A
A 3
AfSVs like PanSV display
strong geographical
clustering
PanSV-F
PanSV-E
A 1
Are MSVs more mobile
than PanSVs?
MSV-B
PanSV-B
PanSV-C
Is MSV-A more mobile
than other MSVs?
PanSV-A
PanSV-D
PanSV-H
PanSV-I
0.2 substitutions per site
MSV-G
MSV-F
MSV-H
MSV-E
MSV-I
MSV-J
MSV-C
MSV-K
MSV-D
A 4
A 2
If all these viruses are
evolving at the same
rates then Yes x 2
Indian Ocean islands
Southern Africa
West Africa
East Africa

Evolution experiments
How fast are AfSVs Mutating?
Transmission from Coix back
to sugarcane sometime
between 1977 and 1986
Natural virus populations
SSRV - A (32 years)
MSV - F (6 years)
Transmission from
sugarcane to Coix in 1976
Sugarcane plants split into
MSV - A – three Maize lineages adapted in strain 1984
SSRV - A (32 years)
2008 (Sugarcane)
2008 ( Coix )
1989 MSV (Sugarcane) - A 1
(All across Africa)
1991 MSV (Sugarcane)
- A 2 (West Africa)
1997 MSV (Sugarcane)
- A 3 (East Africa)
1987 MSV (Sugarcane)
- A 4 (Southern Africa)
MSV - B (6 years)
MSV - B (5 years)
MSV - F (6 years)
1991
1997
WDV –
Wheat adapted strain
MSV - B (6 years)
European WDV
Chinese WDV
1991
1997
0.004 subs/site
0.004 subs/site
Diversity arising during evolution experiments is comparable to that seen Chinawide
for Wheat dwarf virus or Southern-Africa wide MSV-A 4 populations

How fast are AfSVs Mutating?
SSRV and MSV in 5-32 year
long evolution experiments
evolve very fast
Using substitution rate
inference methods in
programs such as BEAST we
could accurately date events
during the 32 year SSRV
experiment
This is an important
validation of these
techniques

Is MSV evolving so fast in the field?
~1924
Found and sequenced some
field isolates sampled between
the late 1970s and the early
1990s
~1904
~1967
~1969
A 4
A 3
A 2
Taking recombination into
account estimated substitution
rates with BEAST
1870-1904
~1922
A 1
Most recent common ancestor of
all sampled MSVs existed in the
late 1800s at around the time
MSD was first reported in
southern Africa
Date
Years ago
Southern Africa
East Africa
West Africa
La Réunion island
1860 1900 1910 1920
150
110
1930
1940
1950
1960
1970
1980
1990
2000
100 90 80 70 60 50 40 30 20 10 0
2010
A 6

Is MSV really evolving so fast?
Substitution rate estimates are very similar when using experimental
populations and field isolates

What is the cause of high basal mutation rates?
Substitution matrices are “imbalanced”
indicating strand specific mutational
processes
Imbalance suggests mutational
processes acting on ssDNA (e.g. in
double stranded DNA the rates of G to T
and C to A mutations should be the
same)
High rates of G to T, G to A and C to T
mutations suggest viral ssDNA is
particularly sensitive to oxidative
stresses

When did MSV-A emerge?
* best supported
model sets
The recombination event that generated MSV-A probably occurred after
maize was introduced by the Dutch to southern Africa
The MRCA of all MSV-As probably existed within 20 years of the
recombination event taking place

Where did MSV-A emerge?
Haplotype Classification
Legend
MSV-A 1
MSV-A 3
MSV-A 2
MSV-A 4
MSV-A 2 , -A 3 , -A 4 like variant
MSV-A 2 , -A 4 like variant
MSV-A 2 , -A 7 like variant
MSV-A 6
year
2000 – 2008
Using >350 MSV full genomes with
known sampling coordinates we
looked at the contemporary (2000-
2008) distributions of 10 MSV-A 1
and 2 MSV-A 4 lineages (groups of
viruses all sharing the same
recombination mosaics)
MSV-A 1 s have a pan-African
distribution MSV-A 4 is found only in
southern Africa

Where did MSV-A emerge?
1863
1933
(1809-1935)
(1867-1950)
Root probability
0.35
0.30
0.25
0.20
0.15
0.10
0.05
0.00
0.35
0.30
0.25
0.20
0.15
0.10
0.05
0.00
Root probability
Full-genome dataset
Recombination-free dataset
Discrete phylogeography models (taking only countries of origin into account)

Where did MSV-A emerge?
Continuous phylogeography models (taking actual GPS coordinates into account)
Full genome dataset
(80% HPD)
1887(1842-1939)
Recombination free
dataset (80% HPD)
1901 (1828-1941)

What are the most obvious movements?
Age of migration (years before 2008)
BF
TD
BE
NG
CAR
CM
UG
KE
Bayes Factor
0
10
20
30
ZM
ZW
RE
< 3.2
> 3.2
> 10
> 100
40
50
60
70
80
90
ZA
LS
MZ
Dataset
Both
Recombination free
Full genome

A
Are there hotspots of recombinant genesis?
B C D
1995
1975
1994
E
(1997 -
2002)
MSV-A 1 I
F
(1970 -
1980)
MSV-A 1 II
G
(1988 -
1998)
MSV-A 1 III
Every one of the 12 main MSV-A 1
and MSV-A 4 lineages are inferred to
have arisen in either southern Africa
or East Africa
1993
1977
1960
(1987 -
1999)
MSV-A 1 IV
H
(1967 -
1985)
MSV-A 1 V
I
(1949 -
1971)
MSV-A 1 VI
J
The geographical origins of these
lineages are supported by analyses
of both full- genome and
recombination-free datasets
1975
1998
1996
(1967 -
1983)
MSV-A 1 VII
K
(1996 -
2000)
MSV-A 1 VIII
L
(1992 -
1999)
MSV-A 1 XI
M
Remember that these lineages are
defined by the recombination
patterns they carried
1960
(1950 -
1968)
MSV-A 1 XV
1993
(1981 -
2000)
MSV-A 4 I
1947
(1934 -
1958)
MSV-A 4 V
Full-genome
Recombination-free
Sample location

Do different subtypes display the same
movement dynamics?
There may be differences in the
mobility of MSV-A 1 and MSV-A 4
MSV-A 1 lineages that emerge in
southern Africa frequently (in ¾
cases) move to East and/or West
Africa
Both MSV-A 4 lineages that emerged
in southern Africa stayed in
southern Africa

Wave-like east to west movements
3.2
6.0
3.2
< 4.8
2.6
5.9
91.0
7.1
30.0
< 3.7
1975
(1967-1983)
MSV-A 1 VII
< 4.4
< 3.2
< 3.9
< 3.5

Wave-like east to west movements of MSV-A 1
D
76.2
64.0
72.0
76.2
73.7
74.1
2.3
71.4
9.1
< 3.7
1994
(1988-1998)
MSV-A 1 III
< 4.4
< 3.2
< 3.9
< 3.5

Dispersal rate (km per yr)
How fast does MSV move across Africa?
Recombination- free
Continuous model
Dispersal rates may have varied
slightly over he last 100 years
BUT detected differences are
not significant
60
Dispersal rates
50
40
30
20
On average over the past ~100
years MSV has been moving at
an average rate of 33Km/year
(HPD = 15.6-51.6)
10
0
Recombination
free
Full genome

Edward Rybicki - University of Cape Town, South Africa
Aderito Monjane - University of Cape Town, South Africa
Eric van der Walt - University of Cape Town, South Africa
Betty Owor - University of Cape Town, South AfrIca
Gordon Harkins - SANBI, South Africa
Tania van Antwerpen - SASRI, South Africa
Bradley Flett - ARC. South Africa
Moses Ramusi - ARC, South Africa
Darren Martin
Dionne Shepherd
Arvind Varsani
Sunday Oluwafemi - Bowen University, Nigeria
Innocent Zinga - University of Bangui, Central African Republic
Appolinaire Tange - IRAD Yaounde, Cameroon
Fidèle Tiendrebeogo, - Université de Ouagadougou, Burkina Faso
Salem Samtally - MSIRI, Mauritius
Pierre Lefeuvre - CIRAD, La Reunion
Jean-Michel Lett - CIRAD, La Reunion
Michel Peterschmitt - CIRAD, France
Oliver Windram - University of Warwick, England
Peter Markham - ex John Innes Centre, England
Phillipe Lemey - Katholieke Universiteit Leuven, Leuven, Belgium
Rob Briddon - NIBGE, Pakistan
Siobhan Duffy - Rutguers University, USA
Jane Polston - University of Florida, USA

Acknowledgements
Arvind Varsani
Carnegie Corporation of New York, USA
Darren Martin
Sydney Brenner Foundation
Harry Oppenheimer Foundation, South Africa
Wellcome trust research foundation, UK
Dionne Shepherd
Claude Leon Foundation and PANNAR (Pty) Ltd
National Research Foundation, South Africa
Harry Oppenheimer Foundation, South Africa
University of Cape Town block grant, South Africa
Wellcome trust research foundation, UK
Marsden Fund, New Zealand
University of Canterbury Early career research grant, New Zealand
Bimolecular interaction centre seed grant, New Zealand