CIMMYT, Mexico, D.F. Mexico
Protecting South Asian Wheat Production from Stem Rust (Ug99) Epidemic
Rajiv K. Sharma1, Pawan K. Singh2, Vinod3, Arun K. Joshi4, Subhash C. Bhardwaj5, Navtej S. Bains6and
Authors’ addresses:1International Maize and Wheat Improvement Center (CIMMYT), P.O. Box 5291, Kabul, Afghanistan;
2CIMMYT, Apdo. Postal 6-641, Mexico D.F., 06600, Mexico;3Division of Genetics, Indian Agricultural Research Institute,
New Delhi, India;4CIMMYT, P.O. Box 5186, Singha Durbar Plaza Marg Bhadrakali, Kathmandu, Nepal;5Directorate of
Wheat Research, Shimla, India;6Department of Plant Breeding, Punjab Agricultural University, Ludhiana, Punjab, India
(correspondence to S. Singh. E-mail: email@example.com)
Received June 18, 2012; accepted November 28, 2012
Keywords: Ug99, adult plant resistance, Puccinia graminis tritici, race non-specific resistance
The Ug99 group of stem rust races (Puccinia graminis
Pers. f. sp. tritici Eriks. & E. Henn.) has evolved and
migrated. While the original variant overcame the
widely deployed gene Sr31, and Sr21 (in Chinese
Spring background), but not Sr21 in Einkorn, a new
strain of Ug99, virulent on Sr24, was detected in 2006
and caused a severe epidemic in 2007 in Kenya. Forms
virulent on Sr36 and Sr21 were identified in 2007.
Likewise, an Ug99 variant virulent to both Sr21 and
Sr24 was identified in 2008 in Kenya. Simultaneously,
the original strain spread to Yemen and Sudan in
2006. Fears of a spread into Asia were confirmed when
this race was detected in Iran in 2007. This has raised
serious concerns that Ug99 could follow the same
migratory route from Africa to Asia as Yr9 and cause
major epidemics across the epidemiological region of
South Asia. In 2005–06, screening in Kenya and Ethio-
pia of wheat materials from Asian countries revealed a
very low frequency of lines resistant to Ug99 and its
variants. Under the umbrella of the Borlaug Global
Rust Initiative (BGRI), significant efforts have been
made to counter the challenges posed by Ug99 and its
derivative races. Diverse sources of resistance to the
pathogen have been identified and incorporated in
high-yielding wheat backgrounds. The most promising
strategy has been to deploy spring wheat varieties pos-
sessing adult plant resistance (APR) in infested and
bordering areas to decrease inoculum amounts and
slow down the development of new virulence, for
example four CIMMYT genotypes with Sr2+ have
been released in Afghanistan and their seed is also dis-
tributed in region bordering Iran. For an immediate
remedy, race-specific resistance genes can be deployed
in combinations using marker-assisted selection. Sev-
eral Ug99-resistant varieties have already been released
in South Asian countries (Afghanistan, India, Nepal,
Bangladesh and Pakistan), and seed dissemination is
underway. The Ug99 risk in the region can be reduced
to minimum levels by identifying, releasing and provid-
ing seed of high-yielding and resistant cultivars.
Globally, annual wheat production is estimated over
680 million tons (2009 harvest year) from approxi-
mately 225 million hectares. Whilst wheat cultivation
spans from 44°S to 60°N on both sides of the equator
and at altitudes ranging from sea level to 3000 masl,
Asia accounts for approximately 45% of both the area
and yield (Table 1, FAO 2010). Major producers in
Asia include China, India, Pakistan and Iran, which
together account for 34% of global production and
30% of the acreage.
Worldwide, various wheat growing areas are differen-
tially suitable for the development of stem, stripe and
leaf rust diseases (Saari and Prescott 1985). These
pathogens belong to the genus Puccinia and are there-
fore highly specialized with a narrow host range. How-
ever, the rust urediniospores are produced in large
Wheat acreage, production and productivity in different countries of
Asia (FAO 2010)
J Phytopathol 161:299–307 (2013)
© 2012 Blackwell Verlag GmbH
numbers and can travel considerable distance with wind
(Hodson 2011); the long distance transport of stem rust
used to be an annual phenomenon across the North
American Great Plains (800 km; Roelfs 1985) and from
Australia to New Zealand (2000 km; Luig 1985), and it
is understood to have travelled 8000 km from East
Africa to Australia (Luig 1985). The three rusts vary in
their optimum temperature requirements for different
developmental stages. Stem rust can survive the highest
temperatures (15–30°C) and stripe rust requires the
lowest (9–15°C), whereas leaf rust has intermediate tem-
perature requirements (Roelfs et al. 1992).
Since the Green Revolution, stem rust has been
managed through the use of resistant semi-dwarf
spring wheat varieties (Singh et al. 2011). A stem rust
epidemic in 1916 in the USA and Canada triggered
research on the disease, and this was further intensified
when epidemics recurred in following decades. The
adult plant resistance (APR) gene Sr2, transferred to
hexaploid wheat ‘Hope’ and ‘H44-24’ from tetraploid
emmer wheat ‘Yaroslav’ by McFadden (1930), was
shown to confer slow rusting (Sunderwirth and Roelfs
1980). This gene is known to be associated with
pseudo-black chaff and confers insufficient protection
to stem rust when present alone (Kota et al. 2006).
The combination of Sr2 with other unknown slow-
rusting resistance genes (also known as the Sr2 com-
plex) has provided the basis for durable resistance to
stem rust (McIntosh 1988; Rajaram et al. 1988).
Whilst leaf and stripe rusts continued to pose a
major threat to wheat production in many parts of the
world, South Asian and especially Indian wheat germ-
plasm remained resistant to stem rust, mainly due to
the presence of resistance genes Sr31, Sr24 and Sr2
complex. In addition, other genes such as Sr26, Sr36
and Sr38 remained effective against Indian stem rust
races (Joshi et al. 2008). Consequently, stem rust was
often not considered an important threat for wheat
production in India and breeders focused on leaf and
stripe rusts. However, with the current threat of new,
virulent stem rust races, a more proactive approach
must be taken to protect approximately 38 million
hectares of wheat in South Asia, which is now prone
to an Ug99 stem rust attack. This review analyses the
past achievements, current status and future impera-
tives for managing stem rust disease in South Asia, to
safeguard a crucial, life-sustaining crop.
Understanding the Problem
Rust fungi are obligate parasites and therefore survive
on living plants. During the off-season, the fungus sur-
vives on either self-sown (volunteer) wheat plants or
other susceptible grass species. Intensive, year-round
crop cultivation and the existence of suitable environ-
mental conditions in several parts of the world promote
the carry-over of inoculums between seasons/years.
Primary hosts for the stem rust pathogen (Puccinia
graminis Pers. f. sp. tritici Eriks. & E. Henn.) (Pgt)
include wheat, barley, triticale and some other related
species. Alternate hosts are non-functional in the
Indian subcontinent, and rusts spread through uredini-
ospores as a result of wheat and barley being grown
throughout the year in south India and as summer
crops in the hills of India, Nepal and Pakistan. In the
absence of functional alternate hosts, cultivation of
wheat and barley in the hills allows the oversummering
of rusts that then spread to the main crop during the
Rabi/winter season (Nagarajan and Joshi 1985).
The first stem rust epidemic in India was recorded
in 1786 in central India, and more than five major
epidemics have occurred in central India since then
(Gokhle 1952; Nagarajan and Joshi 1975). In 1829,
wheat crops were destroyed completely in an epidemic
of stem rust in Madhya Pradesh (Sleeman 1839), and
20% losses occurred due to stem rust epidemics in cen-
tral India during 1946–47 (Joshi et al. 1986). Due to
throughout the year in the Nilgiri hills (Tamil Nadu).
Tall plants and landraces occurring as varietal mix-
tures in Peninsular India are often infected with stem
and leaf rusts, thereby indicating that the inoculum of
rusts is present in nature. Stem rust is more important
later in the growing period, that is, on late-sown and
New races of rust pathogens may arise through sex-
ual recombination, mutation or somatic hybridization
followed by selection whenever the new race has a selec-
tive advantage (Singh et al. 2002). Being airborne, new
races may also be introduced into a new area through
migration. A P. striiformis race with virulence for resis-
tance gene Yr9 is understood to have migrated from the
Eastern African highlands to South Asia, through West
Asia (Hodson 2011). The last major stem rust epidemic,
in Ethiopia during 1993–94, coincided with global epi-
demics of stripe and leaf rust and caused major losses
to the popular variety ‘Enkoy’. Therefore, if a new viru-
lent race arises anywhere in South Asia, given time and
favourable conditions, it could spread throughout this
epidemiologic region. It is estimated that approximately
18 million hectares of the wheat area in South Asia
have suitable conditions for a stem rust epidemic
(Reynolds and Borlaug 2006). These regions fall along
the potential migration path of the Ug99 race and
account for approximately 25% of global wheat
acreage and 19% of global production.
Appearance of Ug99 and its Spread
Ug99 was first detected in Uganda in 1998 (Pretorius
et al. 2000) and spread to most of the wheat growing
areas of Kenya and Ethiopia by 2003 (Table 2). The
race was reported from eastern Sudan in early 2006
and from western Yemen in late 2006. Aapproximately
90% of existing varieties tested in Kenya were
observed to be susceptible to the Ug99 race (Singh
et al. 2011). Coupled with the past experience of inter-
continental movement of the Yr9 virulence of stripe
rust, the current spread of Ug99 is a warning for the
Middle East and Asian wheat growing areas.
In 2007, Ug99 was detected in a winter wheat sample
from Iran (Nazari et al. 2009). Appropriate environ-
Sharma et al.
mental conditions and the presence of barberry in the
surrounding mountains might be a probable threat to
neighbouring countries such as parts of Afghanistan,
and even further to Pakistan, India, Bangladesh and
Nepal. Together, these countries grow over 40 million
hectares of wheat, producing approximately 110 million
tons; an amount just sufficient to meet the require-
ments of this populous region of the world. This is a
vulnerable region where Ug99 would greatly harm the
already fragile food security situation.
The 1B/1R translocation has been widely used in
wheat breeding throughout the world. This transloca-
tion includes Lr26, Sr31 and Yr9 genes and confers
not only rust resistance to the recipient variety but
also some degree of yield advantage. The stem rust
resistance gene Sr31 present on the translocation pro-
vided protection against all prevalent stem rust races
until the condition was overturned by the appearance
of the Ug99 race of the pathogen (Jin et al. 2008; Pre-
torius et al. 2010). Ug99 and some of its variants are
the only known races of Pgt that have virulence for
Sr31 and were designated as TTKS (Wanyera et al.
2006). The same race was re-designated as TTKSK
when characterized along with a fifth differential set
(Jin et al. 2008). This race is not only virulent to most
Sr genes of wheat origin (Table 3) but also to the alien
gene Sr38 brought into wheat from T. ventricossum
(Singh et al. 2011). This unique virulence of Ug99 ren-
dersmost wheat varietiessusceptibleworldwide.
Another variant of Ug99 with new virulence to Sr24
was detected in 2006 in Kenya (Jin et al. 2008), and
another with virulence to both Sr24 and Sr36 was
detected in 2007 (Jin et al. 2009). More virulent vari-
ants are expected as the race covers wider geographical
regions and is exposed to varying selective pressures.
The International Maize and Wheat Improvement
Center (CIMMYT) has begun screening cultivars for
resistance to Ug99. Initial results reveal that only 5%
of the commercial cultivars grown across 75 million ha
over 22 risk countries, including China, India and
Pakistan, are resistant to Ug99 (Singh et al. 2011).
The potential wheat grain production losses from this
disease could be enormous; a crop of a susceptible vari-
ety can appear healthy 3 weeks before harvest and com-
pletely destroyed by harvest time (Singh et al. 2006,
2011). If just 10% of South Asia’s wheat production
was to be affected by Ug99, there would be a global
wheat reduction of more than 10 million tons annually.
Status of Existing Prevalent Races
Stakman and Piemeisel (1917) demonstrated the exis-
tence of stem rust races in wheat, which led to the
establishment of pathotype surveys and surveillance
programmes in many countries. Simultaneous to this
was the development of trap nurseries and trap plots
to assess the presence/absence of rusts and virulence
for specific genes. These activities, conducted in collab-
oration with breeding programmes, paid dividends in
Detection of Ug99 lineage races of stem rust of wheat
Key virulence (+)
or avirulence (?)
+Sr31, +Sr38, +Sr21
identification Detection in countries (Year)
TTKSKUg99 1999 Uganda (1998/99), Kenya (2001), Ethiopia (2003),
Sudan (2006), Yemen (2006), Iran (2007)
South Africa (2000), Zimbabwe (2009)
South Africa (2007)
Uganda (1998/99), Kenya (2009), Ethiopia (2007)
Ethiopia (2007), Kenya (2008), South Africa (2009)
South Africa (2010), Zimbabwe (2010)
?Sr24, ?Sr31, ?Sr36, +Sr21
+Sr31, +Sr21, +Sr24, ?Sr36
+Sr31, +Sr36, +Sr21, ? Sr24
?Sr31, ?Sr36, +Sr21, +Sr24
+Sr31, +Sr24, ?Sr21
+Sr13, +SrTmp, +Sr1A.1R
Ug99 + Sr24
Ug99 + Sr36
List of stem rust resistance genes
effective against Ug99 and its
SourceIneffective genes (Sr)Effective genes (Sr)
Triticum aestivum5, 6, 7a, 7b, 8a, 8b, 9a, 9b, 9c, 9f, 10,
15, 16, 18, 19, 20, 23, 30, 41,
42, 49, McN, Wld-1
9d, 9e, 9 g, 11, 12, 13, 17
28a, 29b, 48, Tmpa, ND643,
Sha7, Huw234, AC Cadillac,
32, 39, 47
33, 45, 46
25, 26, 43
aIneffective against some other race(s) (Singh et al. 2006, 2011; Jin et al. 2006).
bLevel of field resistance may not be enough.
cOnly in hexaploid background.
The Threat of Ug99 in South Asia301
terms of accelerated availability of new resistance
sources whenever a shift in virulence was detected. Ini-
tial efforts to conduct global surveys faced two major
problems (Luig 1985): firstly, lack of a commonly
accepted and up-to-date pathogen naming and classifi-
cation system dealing with variation in Pgt; and sec-
ondly, quarantine restrictions to introduce rust isolates
from one country to the other for screening purpose.
The first problem makes it difficult to circulate infor-
Therefore, universal naming of the pathotypes is vital
for comparing results and disseminating the relevant
information among countries and programmes.
An internationally accepted common scientific patho-
type naming system is hindered by absence of common
set of differentials and analytical procedure (McIntosh
et al. 1995; Fetch et al. 2009; Pretorius and Nazari
2009). This limitation was overcome (Pretorius et al.
2000) in case of Ug99 by naming if after the country
and year were detected first. Molecular tools like DNA-
based markers can play a vital role in bridging this gap
by defining the genetic relatedness of different patho-
types (Visser et al. 2009). Fetch et al. (2009) proposed a
set of 20 standard international differential testers and
use of the North American system of naming patho-
types of Pgt, which employs alpha characters and was
originally proposed by Roelfs and Martens (1988).
Wanyera et al. (2010) surveyed the occurrence of
stem rust races in Kenya, the region in which TTKSK
and its variants initially spread. Surveillance in 2006–
07 detected variants of TTKS with virulence on Sr24
(TTKST) and Sr36 (TTTSK). The extensive surveil-
lance during 2008 and 2009 revealed a greater fre-
quency of TTKST, and the authors ascribed this to
the large-scale cultivation of a Sr24 carrying variety,
KS Mwamba. Durum accessions resistant to TTKSK
at Njoro, Kenya, were observed to be susceptible at
Debre Zeit, Ethiopia (Olivera et al. 2012). These acces-
sions had been postulated to carry Sr13. The analysis
discovered two isolates JRCQC and TRTTF, both vir-
ulent on Sr13 and Sr9e. This is of concern as these
two genes are sources of stem rust resistance in the
majority of durum cultivar in North America. Olivera
et al. (2012) screened 338 accessions of emmer wheat
and, based on seedling as well as APR screening at
Debre Zeit, Ethiopia, confirmed that 11 genotypes
were useful in breeding.
Epidemiology of Stem Rust in South Asia
Initial scientific investigations into stem rust epidemiol-
ogy in the Indian subcontinent began in the 19th cen-
tury (Sleeman 1839; Barclay 1887; Butler and Hayman
1906). However, systematic studies on wheat rusts
were initiated by Mehta (1925), who ruled out the
role of Berberis and demonstrated that the aecia on
Berberis spp. were not those of Pgt (Mehta 1940).
Wheat rust urediniospores fail to survive the hot,
dry summer of the Indian plains but over summer in
the hills. Mehta (1952) concluded that stem rust
spreads both from the Himalayas in the north and
from the Nilgiri and Palney Hills in the south. How-
ever, subsequent investigations showed that stem rust
is not active in the Himalayan valleys between Novem-
ber and March (Nagarajan and Joshi 1977); instead,
the Nilgiri and Palney Hills in south India act as the
primary foci of stem rust for wheat crops in the plains
(Joshi et al. 1971). The importance of the Nilgiris on
the survival of stem rust was further suggested in other
studies (Nagarajan 1973; Joshi 1976), and the dispersal
route from south to north used to be called the ‘Pucci-
nia Path’ of India (Joshi et al. 2008). Stem rust uredin-
iospores are carried from South Indian Hills by
tropical cyclones in late October and November to
central India, where infection is established under
favourable conditions (Nagarajan 1973). However,
subsequent development of stem rust depends on the
weather conditions in January and February. From
central India, stem rust spreads to the rest of the coun-
try along with western disturbances.
The introduction of semi-dwarf varieties during the
Green Revolution also brought resistance to the stem
rust pathogen, which led to the gradual decrease in its
inoculum. Bangladesh is hot and humid and therefore
could be favourable for stem rust, but it has not
reported a significant incidence of stem rust (Joshi
et al. 2008). However, a potent race of stem rust has
been reported in Pakistan in recent years (Joshi et al.
2011). This pathogen reportedly over summers in the
Sulaiman ranges, Hindukush Mountains and Baluchis-
tan area (Mehta 1940, 1952).
Where resistant cultivars are not available, chemicals,
such as some fungicides, have been shown to effectively
protect wheat from stem rust (Wanyera et al. 2009).
Products containing a triazole fungicide have been
found to reduce disease severity (Paul and Booyse
2010), although differences in efficacy have been
observed. Additional local studies may be required to
determine the effectiveness of fungicides, application
time, rate and crop growth stage to derive maximum
benefits from chemical application. A USDA funded
project is currently investigating use of fungicides to
control wheat rusts in Afghanistan. It is also under-
stood that the efficient use of fungicides will depend on
accurate forecasting, knowledge of cultivar and integra-
tion with control of other diseases or insect pests.
Status of Genetic Resistance to Stem Rust
The biggest concern for Ug99 is that it will follow the
same migration path taken by the Yr9 virulent stripe
rust pathogen. Therefore, restriction strategies include
growing resistant varieties in the projected pathway
and endemic regions, viz. East Africa, the Arabian
Peninsula, North Africa, the Middle East and South-
west Asia. A varietal mixture in the identified region
could help restrict the multiplication of inoculum and
spread (Singh et al. 2006, 2011).
A number of high-yielding Ug99-resistant varieties
have now been released in the countries of this region
Sharma et al.
(Table 4), in addition to several varieties already under
cultivation in India that were found to be resistant to
Ug99 (Joshi et al. 2011). In Central and Peninsular
Zones, which are prone to stem rust, a large number
of resistant varieties viz. Lok 1, HI 8498, WH 147,
GW 322, HI 1531, HI 8627, HD 4672, DL 788-2 and
MPO 1215 are under cultivation. It is estimated that
Lok 1 occupies approximately 50% of the cultivated
wheat area in these two zones, and the remaining vari-
eties collectively account for at least 20% of the culti-
vated wheat area. Hence, the total area under Ug99-
resistant varieties in the two zones is approximately
70% of the ~7.0 million hectares, that is, approxi-
mately 4.9–5.0 million hectares. However, this resis-
tance could be overcome with the emergence of new
races of the stem rust pathogen. Therefore, it is impor-
tant to understand the nature of resistance in these
Further sources of resistance need to be identified,
and it was with this objective that global Ug99 stem
rust screening services were established in 2005 under
the Borlaug Global Rust Initiative (BGRI) in Kenya
and Ethiopia. The initiative supports national and
international wheat research by evaluating germplasm
for new sources of resistance to incorporate them into
elite breeding lines (http://www.globalrust.org). More
than 100 000 advanced breeding lines were screened
against Ug99, and diverse sources of resistance, includ-
ing APR, were identified. Of the 40 000 lines screened
in the 2009 main season nursery, less than 20% of
bread wheat lines and less than 10% of durum wheat
lines had an acceptable level of resistance. During test-
ing at Njoro, Kenya, Acevedo et al. (2010) observed
that higher proportions of landraces from Ethiopia
and Iran were resistant to Ug99 and its variants. Sev-
enty-seven accessions showed moderate to high-level
resistance in multiple tests. The doubled haploid (DH)
progeny lines from the cross AC Cadillac/Carberry
showed a high degree of resistance (Knox et al. 2010).
AC Cadillac was thus postulated to possess Sr2 and
SrCad genes for resistance to stem rust. Rouse and Jin
(2011) screened 1061 accessions of T. monococcum and
214 accessions of T. urartu against race Ug99 and
reported a large proportion of the accessions (78.7%
of T. monococcum and 93.0% of T. urartu) were resis-
tant. They also found that 98 (22%) of 456 accessions
of Aegilops tauschii were resistant to the Ug99 race
(Rouse et al. 2011). A new source of resistance to
Ug99 was identified on the short arm of Ae. searsii
chromosome 3S, and three Robertsonian transloca-
tions and one recombinant with stem rust resistance
were identified (Liu et al. 2011).
In post-Green Revolution India, stem rust has been
under control largely due to the cultivation of resistant
cultivars. The stem rust genes commonly postulated in
Indian cultivars are Sr2, Sr5, Sr7b, Sr8a, Sr8b, Sr9e,
Sr24 and Sr31. Most of these genes are not very effec-
tive except Sr24, Sr31 and the APR gene Sr2. Basi-
cally only Sr2 remains effective to Ug99, at best in
combinations. The virulence for Sr24 in India is not
widespread, and no virulence exists for Sr31. However,
some unknown genes might confer resistance in certain
Deployment of Resistance Genes
Resistance conferred by one or few race-specific genes
generally remains effective throughout the lifecycle of
the plant and is easy to transfer through conventional
plant-breeding tools. A large number of these genes
are currently deployed in the region (Sinha et al. 2002;
Joshi et al. 2007a). It is relatively easy to screen for
this type of resistance under artificial conditions at the
seedling stage. Many of these genes originate from
wild relatives and have linked markers, which can be
utilized to pyramid these genes in desirable genotypes
tance also offers the advantage of very high resilience
against environmental factors. The major disadvantage
of seedling resistance genes pertains to their race speci-
ficity and the selection pressure that such genes exert
on pathogens which then evolve to counter these
genes. Durability of these genes has therefore been a
major concern. However, there have been exceptions,
such as Sr31, which have provided resistance against a
large number of races for a long time. Another exam-
ple is the Agropyron elongatum-derived stem rust resis-
tance gene, Sr26, which has remained effective in spite
of its large-scale use in Australia, although it is not
known to be present in cultivars in other countries
(Joshi et al. 2008).
APR genes confer resistance at the adult plant stage,
and seedlings are generally susceptible (Kolmer 2001;
Singh et al. 2008, 2011). This type of resistance shows
a continuous variation for disease and is not easy to
Ug99-resistant wheat varieties
released or in an advance stage of
the process in South Asian
VarietyCIMMYT name/cross CountrySr Gene
The Threat of Ug99 in South Asia303
select because it can only be screened at the adult
plant stage and is affected by environmental condi-
tions. However, it is possible to identify molecular
markers for APR for an early and environmentally
independent selection. Distribution of APR-based elite
material by CIMMYT to various countries is expected
to result in deployment of durable, race non-specific
material in the future.
Surveillance and Research Initiatives in South Asia
Surveillance of wheat rusts has been an important part
of wheat research in South Asia for several years and
has been taken up quite effectively by the Indian
wheat programmes as part of India’s coordinated net-
work. With the realization of the threat of Ug99, sev-
eral breeding initiatives were adopted by South Asian
countries in collaboration with CIMMYT and BGRI
(Joshi et al. 2011; Singh et al. 2011). Both advanced
and segregating materials were shuttled to Njoro,
Kenya, and useful material was obtained (Singh et al.
2008). Recently, these efforts paid dividends, and agro-
nomically superior, Ug99-resistant varieties were iden-
tified and released in each of these countries (Joshi
et al. 2011). Additionally, trap nurseries are sown at
several critical locations to detect any change in race
profile. Samples were collected from susceptible hosts
(Agra Local) and analysed on sets of differentials (Ba-
hadur et al. 1985; Bhardwaj 2012) The pathotypes
were designated binomially, and international equiva-
lents given (Bhardwaj et al. 2006). In recent surveys,
pathotype 62G29 (PTH) and 62G29-1 (PTH +Sr24)
were predominant (Bhardwaj et al. 2006). The latest
detailed pathotype situation of wheat rusts is now
available for the Indian subcontinent (Bhardwaj 2012).
Although germplasm exchange has been a regular
practice at the international level, a similar exercise at
the regional level is lacking. The regional political alli-
ance, South Asian Association for Regional Coopera-
tion (SAARC), has developed a SAARC wheat disease
trap nursery. This nursery is planted every year in sev-
eral locations across SAARC countries to understand
the movement and virulence of pathogens. During
2009–10, the nursery was planted at 23 locations and
comprised 20 lines contributed by four SAARC
nations (Prashar et al. 2010). The nursery has also
been sown at Kabul in Afghanistan this year in the
neighbourhood of Iran where Ug99 was detected in
2007. In 2009–10, Afghanistan also benefitted from the
export of 1.5 tons of seed of the Ug99-resistant variety
Misr-1 from Egypt (where it is called Muqawim), fol-
lowed by a further provision of 150 tons of Misr-1 reg-
istered seed in 2011. This resulted in Ug99 resistance
for over 17% of the total certified seed for the 2011–
12 season in Afghanistan.
The nurseries and trials originating from CIMMYT
and the International Center for Agricultural Research
in the Dry Areas (ICARDA) are serving an important
purpose by distributing the relevant genetic material
and the required information to increase wheat pro-
ductivity in the region. These Consultative Group
Centers (CIMMYT and ICARDA) and BGRI, in col-
laboration with national research centres, have devel-
oped high-yielding Ug99-resistant varieties that are
now being distributed in the most vulnerable areas,
with an objective of resistant lines being grown on at
least 5% of the entire wheat area (Joshi et al. 2011).
Accelerated and Precise Breeding Using Molecular
The fastest way to decrease the susceptibility of
important wheat cultivars and the best new germ-
plasm is to systematically incorporate diverse resis-
tance genes through limited backcrossing, a regular
practice at CIMMYT. Because most of these Ug99-
effective genes are of alien origin, co-segregating
molecular markers for some of them are already
available (http://maswheat.ucdavis.edu/index.htm) and
can aid selection. Conventional backcross breeding
can also be combined with molecular approaches to
transfer rust resistance genes. Stem rust resistance
genes Sr25 and Sr36 were transferred in the genetic
background of several rust susceptible cultivars using
both conventional and molecular approaches in India
(Sivasamy et al. 2009). However, these reconstituted
resistant lines are being used as donors to provide
resistance against endemic races as well as the poten-
tial threat of Ug99. Molecular breeding combining
foreground and background selection can accelerate
the resistance gene transfer in popular cultivars by
reducing the number of backcrosses. Effective rust
resistance genes, including those effective against
Ug99 and its variants such as Sr25 and Sr26, are
being transferred in the genetic background of several
popular cultivars, in addition to other leaf and stripe
rust resistance genes, in a network project funded by
the Department of Biotechnology, Government of
India. Furthermore, marker-based introgression has
been combined with doubled haploid production to
produce different combinations of genes Sr2, Sr24,
Sr25 and Sr26 under an Australian Center for Inter-
national Agricultural Research (ACIAR) project.
Molecular markers provide a powerful tool to iden-
tify plants that carry combinations of resistance genes.
Few diagnostic molecular markers that can be used in
marker-assisted breeding are available (http://mas-
wheat.ucdavis.edu/index.htm). Markers for other genes
need to be developed to facilitate their utilization. Two
different approaches are normally followed to transfer
two or more effective resistance genes into an adapted
cultivar. In the first approach, target genes of all
donor parents (two or more) are assembled first in a
single complex F1by inter-crossing of donor parents,
followed by backcrossing with the recipient cultivar as
recurrent parent. In the second approach, individual
target genes are transferred in the genetic background
of recipient cultivar by repeated backcrossing, followed
by inter-crossing of these backcross lines to assemble
the target genes.
Unfortunately, few effective race-specific resistance
genes are available for immediate utilization. Breeding
Sharma et al.
efforts in CIMMYT focus on selecting for minor gene-
based slow-rusting APR, especially for high-risk areas
where favourable environmental conditions and the
presence of susceptible hosts mean that the pathogen
is expected to survive for several years. It is thought
that this strategy will allow other areas of the world,
regions, to use race-specific resistance genes more suc-
cessfully. Durable stem rust resistance of some older
US, Australian and CIMMYT spring wheat is due to
the deployment of Sr2 in conjunction with other
unknown minor additive genes. Sr2 was detected in
several highly resistant, old, tall Kenyan cultivars,
including ‘Kenya Plume’ and CIMMYT-derived semi-
dwarf wheats Pavon 76, Parula, Kritati and Kingbird
(Njau et al. 2010). Kingbird, a new advanced line, is
at present the best known source of APR in CIMMYT
semi-dwarf wheat (Singh et al. 2011).
Accumulating such complex resistance will be cum-
bersome but not impossible. Molecular markers linked
to the slow-rusting resistance gene Sr2 are known and
can be used in selection (Mago et al. 2010). CIMMYT
has employed a shuttle breeding programme between
Mexico and Kenya to incorporate APR, which has
resulted in the development of high-yielding wheat
lines with high levels of APR (Singh et al. 2011).
Germplasm dissemination can be speeded up by fol-
lowing farmers’ participatory approach (Witcombe
et al. 2001, 2003). Indian research centres have already
worked successfully on this model with CIMMYT and
other partners (Joshi et al. 2007a). This path can be
used effectively for quick dissemination of superior
varieties in areas characterized by weaker linkages (Jo-
shi et al. 2007b). A speedy intervention in the form of
participatory varietal selection (PVS) has recently been
demonstrated in Bangladesh (Pandit et al. 2011).
Farmers’ preferences were judged through PVS by CI-
MMYT-Bangladesh and the Wheat Research Center,
Bangladesh Agricultural Research Institute (BARI),
Dinajpur, from 2006 to 2009. The moderately resistant
variety BAW1064 was accepted by farmers due to its
10% yield superiority over the best check, bolder white
grains, non-lodging behaviour, earliness and resistance
to diseases (Pandit et al. 2011). In this case, farmers
were not involved in breeding but in identifying lines
from a set of advanced lines (including check varieties)
being grown in their fields. In fact, adaptive trials, in
which the best few lines obtained in 2 years of on-sta-
tion multi-location trials are tested in farmers’ fields, is
a routine but mandatory step to get a variety released
for cultivation in Bangladesh. On the other hand, PVS
in farmer’s fields is accepted as a way of evaluating
advanced lines for their release. In India, participatory
seed production is used for rapid dissemination of
released cultivars (Joshi et al. 2007a).
After effective control for nearly 50 years, stem rust
has once again become a threat to global food security
due to the evolution and spread of a highly virulent
Ug99 group of races. However, proper utilization of
race-specific resistance in combination with a focus on
breeding wheat varieties with high levels of APR
should mitigate the Ug99 threat, provided these resis-
tant varieties are successful in displacing the current
popular, but susceptible varieties. Diligent monitoring
can help implement chemical control strategies as
emergency measures where necessary. A strong effort
and investment will be essential to promote resistant
varieties for their fast adoption by millions of farmers
in South Asia.
This work was supported in part by funds provided through a grant
from the Bill & Melinda Gates Foundation to Cornell University for
the Borlaug Global Rust Initiative (BGRI) Durable Rust Resistance
in Wheat (DRRW) Project. We acknowledge the help of Emma
Quilligan, CIMMYT-Mexico, in editing the article.
Acevedo M, Bonman JM, Jackson EW, Bateman AM, Jin Y, Njau
P, Wanyera R, Bockelman H, Goates B, Brown-Guedira G.
(2010) Mining a collection of wheat landraces for resistance to
new races of Puccinia graminis f. sp. tritici. Proceedings, oral
papers and posters, 2010 Technical Workshop, Borlaug Global
Rust Initiative, St. Petersburg, Russia, 30–31 May, 2010, p. 51.
Bahadur P, Nagarajan S, Nayar SK. (1985) A proposed system of
virulence designation in India. II Puccinia graminis f. sp. tritici.
Proc Indian Acad Sci (Plant Sciences) 95:29–33.
Barclay A. (1887) A descriptive list of uredinales occurring in the
neighborhood of Simla (Western Himalaya). J Asiatic Society Ben-
gal 56 (Part II):350–375.
Bhardwaj SC. (2012) Wheat rust pathotypes in Indian subcontinent
then and now. In: Singh SS, Hanchinal RR, Singh G, Sharma
RK, Saharan MS, Sharma I (eds) Wheat-Productivity enhancement
under changing climate. Narosa Publishing House Pvt. Ltd., New
Delhi, pp 227–238.
Bhardwaj SC, Prashar M, Singh S, Datta D. (2006) Physiologic
specialization of Puccinia graminis tritici on wheat in India during
2002–04. Indian J Agric Sci 76:324–426.
Borlaug Global Rust Initiative (2011) Available at: http://www.glob-
alrust.org (accessed 19 February 2011)
Butler EJ, Hayman JM. (1906) Indian wheat rusts with a note on
the relation of weather to rust on cereals. Mem Dept Agric India
Bot Serv 1:1–57.
FAO (2010) Available at: http://faostat.fao.org (accessed October
Fetch T, Jin Y, Nazari K, Park R, Prashar M, Pretorius Z. (2009)
Race nomenclature systems: can we speak the same language? In:
McIntosh R (ed.) Proceedings Oral Papers and Posters, 2009 Tech-
nical Workshop. Obreg? on, Sonora Mexico, Borlaug Global Rust
Initiative, Cd., pp 61–64.
Gokhle VP. (1952) Wheat varieties that are resistant to rust. Farmer
(Bombay) 3: Part 6
Hodson DP. (2011) Shifting boundaries: Challenges for rust moni-
toring. Euphytica 179:93–104.
Jin Y, Pretorius ZA, Singh RP, Fetch T Jr. (2008) Detection of viru-
lence to resistance gene Sr24 within race TTKS of Puccinia
graminis f. sp. tritici. Plant Dis 92:923–926.
Jin Y, Szabo LJ, Rouse M, Fetch T Jr, Pretorius ZA, Wanyere R,
Njau P. (2009) Detection of virulence to resistance gene Sr36
within race TTKS lineage of Puccinia graminis f. sp. tritici. Plant
Joshi LM. (1976) Recent contributions towards epidemiology of
wheat rusts in India. Ind Phytopathology 29:1–16.
Joshi LM, Saari EE, Gera SD. (1971) Epidemiology of wheat rusts
in India. INSA Bull 37B:449–453.
Joshi LM, Singh DV, Srivastava KD. (1986) Wheat and wheat
diseases in India. Joshi LM, Singh DV, Srivastava KD. (eds)
The Threat of Ug99 in South Asia 305
I Problems and progress of wheat pathology in South Asia. New
Delhi, Malhotra Publishing House, pp 41–68.
Joshi AK, Mishra B, Chatrath R, Ortiz Ferrara G, Singh RP.
(2007a) Wheat improvement in India: present status, emerging
challenges and future prospects. Euphytica 157:431–446.
Joshi AK, Chand R, Arun B, Singh RP, Ortiz R. (2007b) Breeding
crops for reduced-tillage management in the intensive, rice-wheat
systems of South Asia. Euphytica 153:135–151.
Joshi AK, Mishra B, Prashar M, Tomar SMS, Singh RP. (2008)
Ug99 race of stem rust pathogen: challenges and current status
of research to sustain wheat production in India. Indian J Genet
Joshi AK, Azab M, Mosaad M et al. (2011) Delivering rust resistant
wheat to farmers: a step towards increased food security. Euphy-
Knox RE, DePauw RM, Singh D, Fetch T, Singh AK. (2010) Cumula-
tive resistance to Ug99 stem rust variants in wheat cultivar AC
Cadilac. Proceedings, oral papers and posters, 2010 Technical
Workshop, Borlaug Global Rust Initiative, St. Petersburg, Russia,
30–31 May, 2010, 45 p.
Kolmer JA. (2001) Early research on the genetics of Puccinia gramin-
is stem rust resistance in wheat in Canada and the United States.
In: Peterson PD. (ed.) Stem rust of wheat: From ancient enemy to
modern foe. St. Paul, MN, APS Press, pp 51–82.
Kota R, Spielmeyer W, McIntosh RA, Lagudah ES. (2006) Fine
genetic mapping fails to dissociate durable stem rust resistance
gene Sr2 from pseudo?black chaff in common wheat (Triticum
aestivum L.). Theor Appl Genet 112: 492–499.
Liu W, Yue J, Matthew R, Bernd F, Gill B, Pumphrey MO. (2011)
Development and characterization of wheat-Ae. searsii Robertso-
nian translocations and a recombinant chromosome conferring
resistance to stem rust. Theor Appl Genet 122:1537–1545.
Luig NH. (1985) Epidemiology in Australia and New Zealand. In:
Roelfs AP, Bushnell WR. (eds) Cereal Rusts Vol. II; Diseases, Dis-
tribution, Epidemiology, and Control. Orlando, Academic Press, pp
Mago R, Brown-Guedira G, Dreisigacker S, Breen J, Jin Y, Singh
R, Appels R, Lagudah ES, Ellis J, Spielmeyer W. (2010) An accu-
rate DNA marker assay for stem rust resistance gene Sr2 in wheat.
Theor Appl Genet 122:735–744.
MASWheat (2012) Marker assisted selection in wheat. Available at:
McFadden ES. (1930) A successful transfer of emmer characters to
vulgare wheat. J A Soc Agron 22:1020–1034.
McIntosh RA. (1988) The role of specific genes in breeding for dura-
ble stem rust resistance in wheat and triticale. In: Simmonds NW,
Rajaram S. (eds) Breeding Strategies for Resistance to the Rust of
Wheat. Mexico, D.F., CIMMYT, pp 1–9.
McIntosh RA, Wellings CR, Park RF. (1995) Wheat rusts: An atlas
of resistance genes. Victoria, Australia, CSIRO Publications.
Mehta KC. (1925) Yellow and brown rusts of wheat. A preliminary
note on their annual recurrence. Proc. Indian Sci. Congr., 12th,
1925, p. 191.
Mehta KC. (1940) Further Studies on Cereal Rusts in India, Sci.
Monogr. No. 14. Ind Counc Agric Res Delhi
Mehta KC. (1952) Further studies on cereal rusts in India. Part II.
Sci. Monogr. No. 18 Ind Counc Agril Res pp. 385.
Nagarajan S. (1973) Studies on the urediospores transport of Puccinia
graminis tritici and epidemiology of stem rust of wheat in India.
PhD thesis, India, University of Delhi, pp 125.
Nagarajan S, Joshi LM. (1975) An historical account of wheat rust
epidemics in India and their significance. Cereal Rust Bulletin
Nagarajan S, Joshi LM. (1977) Sources of primary inoculum of
wheat stem rust in India. Plant Dis Report 61:454–457.
Nagarajan S, Joshi LM. (1985) Epidemiology in the Indian subconti-
nent (Chapter12). In: Roelfs AP, Bushnell WR. (eds) The Cereal
Rusts Vol. II. Orlando, Florida, Academic Press, Inc., pp 371–402.
Nazari K, Mafi M, Yahyaoui A, Singh RP, Park RF. (2009) Detec-
tion of wheat stem rust (Puccinia graminis f. sp. tritici) race
TTKSK (Ug99) in Iran. Plant Dis 93:317.
Njau PN, Jin Y, Huerta-Espino J, Keller B, Singh RP. (2010) Identi-
fication and evaluation of sources of resistance to stem rust race
Ug99 in wheat. Plant Dis 94:413–419.
Olivera PD, Jin Y, Rouse M, Badebo A, Fetch T Jr, Singh RP,
Yahyaoui A. (2012) Races of Puccinia graminis f. sp. tritici with
combined virulence to Sr13 and Sr9e in a field stem rust screening
nursery in Ethiopia. Plant Dis 96:623–628.
Pandit DB, Mandal MSN, Hakim MA, Barma NCD, Tiwari TP,
Joshi AK. (2011) Farmers’ preference and informal seed dissemi-
nation of first Ug99 tolerant wheat variety in Bangladesh. Czech J
Genet Plant Breed 47:S160–164.
Paul I, Booyse M. (2010) Evaluation of the cost effectiveness of fun-
gicide application for control of fungal diseases of wheat in the
Western Cape, South Africa. Proceedings, oral papers and posters,
2010 Technical Workshop, Borlaug Global Rust Initiative, St.
Petersburg, Russia, 30–31 May, 2010, p 13.
Prashar M, Bhardwaj SC, Sharma YP, Jain SK. (2010) Information
on rust virulences and SAARC disease screening nursery. Pre-
sented at 49th Wheat Worker’s Meeting, PAU, Ludiana, Punjab,
India Aug. 27–30, 2012.
Pretorius ZA, Nazari K. (2009) Global stem rust surveillance in
practice. In: McIntosh R. (ed.) Proceedings, Oral Papers and Post-
ers, 2009 Technical Workshop. Obreg? on, Sonora, Mexico, Borlaug
Global Rust Initiative, Cd., pp 55–59.
Pretorius ZA, Singh RP, Wagoire WW, Payne TS. (2000) Detection
of virulence to wheat stem rust resistance gene Sr31 in Puccinia
graminis f. sp. tritici in Uganda. Plant Dis 84:203.
Pretorius ZA, Bender CM, Visser B, Terefe T. (2010) First report
of a Puccinia graminis f. sp. tritici race virulent to the Sr24 and
Sr31 wheat stem rust resistance genes in South Africa. Plant Dis
Rajaram S, Singh RP, Torres E. (1988) Current CIMMYT
approaches in breeding wheat for rust resistance. In: Simmonds
NW, Rajaram S (eds) Breeding Strategies for resistance to the Rust
of Wheat. Mexico, D.F., CIMMYT, pp 101–18.
Reynolds MP, Borlaug NE. (2006) Applying innovations and new
technologies from international collaborative wheat improvement.
J Agric Sci 144:95–110.
Roelfs AP. (1985) Wheat and rye stem rust. In: Roelfs AP, Bushnell
WR. (eds) The Cereal Rusts, Vol. 2. Orlando, FL, Academic Press,
Roelfs AP, Martens JW. (1988) An international system of nomen-
clature for Puccinia graminis f. sp. tritici. Phytopathology 78:526–
Roelfs AP, Singh RP, Saari EE. (1992) Rust Diseases of Wheat:
Concepts and Methods of Disease Management. Mexico, D.F.,
Rouse M, Jin Y. (2011) Stem rust resistance in A-genome diploid
relatives of wheat. Plant Dis 95:941–944.
Rouse M, Olson E, Gill B, Pumphrey M, Jin Y. (2011) Stem
rustresistance in Aegilops tauschii germplasm. Crop Sci 51:2074–
Saari EE, Prescott JM. (1985) World distribution in relation to eco-
nomic losses. In: Roelfs AP, Bushnell WR. (eds) The Cereal Rusts
Vol. II; Diseases, Distribution, Epidemiology, and Control. Orlando,
Academic Press, pp. 259–98.
Singh RP, Huerta-Espino J, Roelfs AP. (2002) The wheat rusts. In:
Curtis BC, Rajaram S, Go′mez Macpherson H (eds) Bread wheat:
Improvement and production, plant production and protection series
no. 30. Rome, FAO, pp 227–249.
Singh RP, Hodson DP, Jin Y, Huerta-Espino J, Kinyua MG,
Wanyera R, Njau P, Ward RW. (2006) Current status, likely
migration and strategies to mitigate the threat of wheat production
from Ug99 (TTKS) of stem rust pathogen. In CAB Reviews:
Perspect Agric, Vet Sci Nutr and Nat Res 1:1–13.
Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Njau P, Wanyera
R, Herrera-Foessel SA, Ward RW. (2008) Will stem rust destroy
the world’s wheat crop? Adv Agron 98:71–309.
Singh RP, Hudson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P,
Herrera-Foessel S, Singh PK, Singh S, Govindan V. (2011) The
emergence of Ug99 races of the stem rust fungus is a threat to
world wheat production. Ann Rev Phytopathology 49:465–481.
Sharma et al.
Sinha VC, Bhardwaj SC, Sharma RK. (2002) Stem rust resistance Download full-text
genes in Indian wheat breeding programme. Ind Phytopathology
Sivasamy M, Vinod, Tiwari S, Tomar RS, Singh B, Sharma JB,
Tomar SMS, Chand S. (2009) Introgression of useful linked genes
for resistance to stem rust, leaf rust and powdery mildew and their
molecular validation in wheat (Triticum aestivum L.). Ind J Genet
Sleeman WH. (1839) Extracts from Major Sleeman’s diary. Trans
Agric Hortic Soc India 6:77–79.
Stakman EC, Piemeisel FJ. (1917) A new strain of Puccinia graminis.
Sunderwirth SD, Roelfs AP. (1980) Greenhouse characterization of
the adult plant resistance of Sr2 to wheat stem rust. Phytopathol-
Visser B, Herselman L, Pretorius Z. (2009) Genetic comparison of
Ug99 with selected South African races of Puccinia graminis f. sp.
tritici. Mol Plant Pathol 10:213–22.
Wanyera R, Kinyua MG, Jin Y, Singh RP. (2006) The spread of
stem rust caused by Puccinia graminis f. sp. tritici, with virulence
on Sr31 in wheat in Eastern Africa. Plant Dis 90:113.
Wanyera W, Macharia JK, Kilonzo SM, Kamundia JW. (2009)
Foliar fungicides to control wheat stem rust race TTKS (Ug99) in
Kenya. Plant Dis 93:929–932.
Wanyera W, Singh D, Njau P, Fetch T, Jin Y, Hodson D, Kilonzo
S. (2010) Surveillance and race analysis of stem rust in Kenya for
the years 2008 and 2009, Proceedings, oral papers and posters,
2010 Technical Workshop, Borlaug Global Rust Initiative, St.
Petersburg, Russia, 30–31 May, 2010, 18 p.
Witcombe JR, Joshi KD, Rana RB, Virk DS. (2001) Increasing
genetic diversity by participatory varietal selection in high poten-
tial production systems in Nepal and India. Euphytica 122:575–88.
Witcombe JR, Joshi A, Goyal SN. (2003) Participatory plant breed-
ing in maize: a case study from Gujarat, India. Euphytica 130:413–
The Threat of Ug99 in South Asia 307