Ug99#TTKSK

{{Short description|Virulent race of stem rust}}

File:Stem rust close up.jpg

{{Use dmy dates|date=August 2024}}

{{infraspeciesbox special

| image =

| image_alt =

| image_caption =

| genus = Puccinia

| species = graminis

| infraspecies_rank1_name = Forma specialis

| infraspecies_rank1_abbrev = f.sp.

| infraspecies_rank1 = P. g. f. sp. tritici

| infraspecies_rank2_name = Varietas

| infraspecies_rank2_abbrev = var.

| infraspecies_rank2 = Ug99

| authority =

| subdivision_ranks = Races

| subdivision_ref =

| subdivision = see text

}}

Ug99 is a lineage of wheat stem rust (Puccinia graminis f. sp. tritici), which is present in wheat fields in several countries in Africa and the Middle East and is predicted to spread rapidly through these regions and possibly further afield, potentially causing a wheat production disaster that would affect food security worldwide. In 2005 the noted green revolution pioneer Norman Borlaug brought great attention to the problem, and most subsequent efforts can be traced to his advocacy.{{cite journal | last=Gross | first=Michael | title=Pests on the move | journal=Current Biology | publisher=Cell Press | volume=23 | issue=19 | year=2013 | issn=0960-9822 | doi=10.1016/j.cub.2013.09.034 | pages=R855–R857 | pmid=24251330 | s2cid=15559913| doi-access=free | bibcode=2013CBio...23.R855G }} It can cause up to 100% crop losses and is virulent against many resistance genes which have previously protected wheat against stem rust.

Although Ug99-resistant varieties of wheat do exist, a screen of 200,000 wheat varieties used in 22 African and Asian countries found that only 5–10% of the area of wheat grown in these countries consisted of varieties with adequate resistance.

The original race of Ug99, which is designated as 'TTKSK' under the North American nomenclature system, was first detected in Uganda in 1998

{{Unbulleted list citebundle

|{{*}} {{cite journal | last1=Pretorius | first1=Z. A. | last2=Singh | first2=R. P. | last3=Wagoire | first3=W. W. | last4=Payne | first4=T. S. | title=Detection of Virulence to Wheat Stem Rust Resistance Gene Sr31 in Puccinia graminis. f. sp. tritici in Uganda | journal=Plant Disease | publisher=American Phytopathological Society | volume=84 | issue=2 | year=2000 | issn=0191-2917 | doi=10.1094/pdis.2000.84.2.203b | pages=203 | pmid=30841334 | s2cid=73469939}}

|{{*}} {{ Cite journal|year=2012|issue=4|volume=13|publisher=Wiley-Blackwell|first11=Gary|first10=Jeff|first9=Regine|first8=Marty|first7=Jason|first6=Pietro|first5=Antonio|first4=Kim|first3=Zacharias|first2=Jan|first1=Ralph|last11=Foster|last10=Ellis|last9=Kahmann|last8=Dickman|last7=Rudd|last6=Spanu|last5=Pietro|last4=Kosack|last3=Pretorius|last2=Kan|last1=Dean|pages=414–430|title=The Top 10 fungal pathogens in molecular plant pathology|journal=Molecular Plant Pathology |issn=1464-6722|doi=10.1111/j.1364-3703.2011.00783.x|pmc=6638784|pmid=22471698|s2cid=18505064}}

|{{*}} {{ Cite journal

| last1=Singh

| first1=Ravi P.

| last2=Hodson

| first2=David P.

| last3=Huerta-Espino

| first3=Julio

| last4=Jin

| first4=Yue

| last5=Bhavani

| first5=Sridhar

| last6=Njau

| first6=Peter

| last7=Herrera-Foessel

| first7=Sybil

| last8=Singh

| first8=Pawan K.

| last9=Singh

| first9=Sukhwinder

| last10=Govindan

| first10=Velu

| title=The Emergence of Ug99 Races of the Stem Rust Fungus is a Threat to World Wheat Production

| journal=Annual Review of Phytopathology

| publisher=Annual Reviews

| date=8 September 2011

| volume=49

| issue=1

| pages=465–481

| doi=10.1146/annurev-phyto-072910-095423

| pmid=21568701

| s2cid=24770327

| issn=0066-4286

}}

|{{*}} {{ Cite book | last1=Singh | first1=Ravi P. | last2=Hodson | first2=David P. | last3=Huerta-Espino | first3=Julio | last4=Jin | first4=Yue | last5=Njau | first5=Peter | last6=Wanyera | first6=Ruth | last7=Herrera-Foessel | first7=Sybil A. | last8=Ward | first8=Richard W. | title=Advances in Agronomy | chapter=Will Stem Rust Destroy the World's Wheat Crop? | publisher=Elsevier | year=2008 | volume=98 | issn=0065-2113 | doi=10.1016/s0065-2113(08)00205-8 | pages=271–309/xiii+422 | isbn=9780123743558 | s2cid=55174564}}

}}

and first characterised in 1999 (hence the name Ug99) and has since been detected in Kenya, Ethiopia, Eritrea, Sudan, Yemen, Iran, Tanzania, Mozambique, Zimbabwe, South Africa,{{cite web|first1=D. P. |last1=Hodson |first2=J. |last2=Grønbech-Hansen |first3=P. |last3=Lassen |first4=Y. |last4=Alemayehu |first5=J. |last5=Arista |first6=K. |last6=Sonder |first7=P. |last7=Kosina |first8=P. |last8=Moncada |first9=K. |last9=Nazari |first10=R. F. |last10=Park |first11=Z. A. |last11=Pretorius |first12=L. J. |last12=Szabo |first13=T. |last13=Fetch |first14=Y. |last14=Jin|title=Tracking the Wheat Rust Pathogens|url=http://wheatrust.org/fileadmin/www.grcc.au.dk/Publications/Hodson_BGRI2012.pdf|work=2012 Borlaug Global Rust Initiative Technical Workshop Proceedings|publisher=Borlaug Global Rust Initiative|access-date=28 November 2012|archive-url=https://web.archive.org/web/20191005184722/http://wheatrust.org/fileadmin/www.grcc.au.dk/Publications/Hodson_BGRI2012.pdf |archive-date=5 October 2019 |url-status=live}} and Egypt. There are now 15 known races of Ug99.{{cite web |url=http://rusttracker.cimmyt.org/?page_id=22 |title=Pathotype Tracker – Where is Ug99? |publisher=The International Maize and Wheat Improvement Center}} They are all closely related and are believed to have evolved from a common ancestor, but differ in their virulence/avirulence profiles and the countries in which they have been detected.

Genetics

Ug99 is the product of a type of somatic nuclear exchange event which has not been observed in other stem rust races.{{cite journal |last1=Li |first1=Feng |last2=Upadhyaya |first2=Narayana M. |last3=Sperschneider |first3=Jana |last4=Matny |first4=Oadi |last5=Nguyen-Phuc |first5=Hoa |last6=Mago |first6=Rohit |last7=Raley |first7=Castle |last8=Miller |first8=Marisa E. |last9=Silverstein |first9=Kevin A. T. |last10=Henningsen |first10=Eva |last11=Hirsch |first11=Cory D. |last12=Visser |first12=Botma |last13=Pretorius |first13=Zacharias A. |last14=Steffenson |first14=Brian J. |last15=Schwessinger |first15=Benjamin |date=7 November 2019 |title=Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation |journal=Nature Communications |publisher=Nature Portfolio |volume=10 |issue=1 |page=5068 |bibcode=2019NatCo..10.5068L |doi=10.1038/s41467-019-12927-7 |issn=2041-1723 |pmc=6838127 |pmid=31699975 |last16=Dodds |first16=Peter N. |last17=Figueroa |first17=Melania |s2cid=207916981}}

During this event and thereafter the nuclei have not experienced recombination.

Gene resistance

Ug99 and its variants differ from other strains of the Black Stem Rust (BSR) pathogen due to their ability to overcome resistance genes in wheat that have been durable against the BSR pathogen for decades.{{cite web |title=USDA Coordinated Approach to Address Pgt-Ug99 |publisher=ARS (USDA Agricultural Research Service)|date=20 September 2017 |url=https://www.ars.usda.gov/ug99/}} These resistant Sr genes, of which 50 are known, give wheat different resistances to stem rust. The virulence in Uganda was virulent against Sr31 and is specific to Ug99. The massive losses of wheat that have occurred have been devastating, but in recent years the wheat rust epidemic has been effectively controlled through selection and breeding for additional Sr genes. (In the decades since, however, Sr31-virulence has evolved in other strains in other locations. Patpour et al., 2022 finds it in Spain and Siberia.)

{{ Unbulleted list citebundle

|{{*}} {{ Cite journal

| language = English

| year = 2022

| doi-access = free

| publisher = Springer Nature B.V.

| issue = 6

| volume = 14

| pages = 1475–1497

| first7 = Anders

| first6 = Jim

| first5 = Anne

| first4 = Ivar

| first3 = Anna

| first2 = Beth

| first1 = Djurle

| last7 = Kvarnheden

| last6 = Nygren

| last5 = Blomstrom

| last4 = Vågsholm

| last3 = Berlin

| last2 = Young

| last1 = Annika

| title = Addressing biohazards to food security in primary production

| issn = 1876-4517

| eissn = 1876-4525

| journal = Food Security

| s2cid = 250250761

| doi = 10.1007/s12571-022-01296-7

| id = AD {{ORCID|0000-0003-1830-6406}}, AB {{ORCID|0000-0002-9518-5719}}, IV {{ORCID|0000-0002-1661-0677}}, ALB {{ORCID|0000-0003-4455-311X}}, AK {{ORCID|0000-0001-9394-7700}}

}}

|{{*}} {{ Cite journal

| language = English

| year = 2022

| doi-access = free

| publisher = Frontiers Media SA

| volume = 13

| id = 882440

| page = 882440

| first19 = Anne

| first18 = Jens

| first17 = Tine

| first16 = Romain

| first15 = Kevin

| first14 = Les

| first13 = Yue

| first12 = Ekaterina

| first11 = Svetlana

| first10 = Alena

| first9 = Pawel

| first8 = Kerstin

| first7 = Anna

| first6 = Vladimir

| first5 = Dolors

| first4 = Biagio

| first2 = Mogens

| first3 = Julian

| first1 = Mehran

| last19 = Justesen

| last18 = Hansen

| last17 = Thach

| last16 = Valade

| last15 = Meyer

| last14 = Szabo

| last13 = Jin

| last12 = Skolotneva

| last11 = Slikova

| last10 = Hanzalova

| last9 = Czembor

| last8 = Flath

| last7 = Berlin

| last6 = Shamanin

| last5 = Villegas

| last4 = Randazzo

| last3 = Rodriguez

| last2 = Hovmoller

| last1 = Patpour

| journal = Frontiers in Plant Science

| issn = 1664-462X

| oclc = 731659269

| s2cid = 249244042

| pmc = 9202592

| pmid = 35720526

| doi = 10.3389/fpls.2022.882440

| title = Wheat Stem Rust Back in Europe: Diversity, Prevalence and Impact on Host Resistance

}}

}}

United States Department of Agriculture (USDA) researchers are testing genes to determine their Ug99 resistance, which will ultimately aid in the development of wheat varieties that will be able to fight off the rust. Resistance has been identified in a small number of spring wheat land races from North America – 23 out of 250 races with adult plant resistance, 27 out of 23,976 SNPs conveying APR, and only 9 races having seedling resistance.

{{Unbulleted list citebundle

| {{*}} {{cite journal | last1=Bajgain | first1=P. | last2=Rouse | first2=M. N. | last3=Bulli | first3=P. | last4=Bhavani | first4=Sridhar | last5=Gordon | first5=T. | last6=Wanyera | first6=R. | last7=Njau | first7=P.N. | last8=Legesse | first8=W. | last9=Anderson | first9=J. A. | last10=Pumphrey | first10=M. O. | title=Association mapping of North American spring wheat breeding germplasm reveals loci conferring resistance to Ug99 and other African stem rust races | journal=BMC Plant Biology | publisher=BioMed Central | volume=15 | issue=1 | date=14 October 2015 | issn=1471-2229 | doi=10.1186/s12870-015-0628-9 | page=249 | pmid=26467989 | pmc=4606553 | s2cid=54521938 | doi-access=free}}

| {{*}} {{cite journal | last1=Kumar | first1=Jitendra | last2=Gupta | first2=Debjyoti Sen | last3=Gupta | first3=Sunanda | last4=Dubey | first4=Sonali | last5=Gupta | first5=Priyanka | last6=Kumar | first6=Shiv | title=Quantitative trait loci from identification to exploitation for crop improvement | journal=Plant Cell Reports | publisher=Springer Science+Business Media | volume=36 | issue=8 | date=28 March 2017 | issn=0721-7714 | doi=10.1007/s00299-017-2127-y | pages=1187–1213 | pmid=28352970 | s2cid=25627600|url=https://mel.cgiar.org/reporting/download/hash/EseurVAQ }}

| {{*}} {{cite journal|publisher=John Wiley & Sons|id=Society for Experimental Biology (SEB)| last1=Scheben | first1=Armin | last2=Verpaalen | first2=Brent | last3=Lawley | first3=Cynthia T. | last4=Chan | first4=Chon-Kit K. | last5=Bayer | first5=Philipp E. | last6=Batley | first6=Jacqueline | last7=Edwards | first7=David | title=CropSNPdb: a database of SNP array data for Brassica crops and hexaploid bread wheat | journal=The Plant Journal| volume=98 | issue=1 | date=28 January 2019 | issn=0960-7412 | doi=10.1111/tpj.14194 | pages=142–152 | pmid=30548723 | s2cid=56486847}}

| {{*}} {{cite journal|publisher=John Wiley & Sons, Inc.| last1=Bajgain | first1=Prabin | last2=Jin | first2=Yue | last3=Tsilo | first3=Toi J. | last4=Macharia | first4=Godwin K. | last5=Reynolds | first5=Susan E. | last6=Wanyera | first6=Ruth | last7=Anderson | first7=James A. | title=Registration of KUWNSr, a wheat stem rust nested association mapping population | journal=Journal of Plant Registrations| volume=14 | issue=3 | date=14 May 2020 | issn=1936-5209 | doi=10.1002/plr2.20043 | pages=467–473 | s2cid=219423451}}

}}

This resistance was present without the Ug99 pathogen challenge being present in NA to drive its selection. USDA has studied winter wheat land races where resistance is more probable.

{{ Cite report |

language=en|

year=2007|

pages=1–27|

url=https://www.ars.usda.gov/ug99/actionplan.pdf |

title=Action Plan to Minimize Impact of Ug99 Stem Rust in the United States|

author=USDA Agricultural Research Service|

publisher=USDA Agricultural Research Service|

edition=1.01|

archive-url=https://web.archive.org/web/20221020091749/http://www.ars.usda.gov/ug99/actionplan.pdf|

archive-date=20 October 2022}}

In addition to the research being conducted by the USDA, The United Kingdom’s Department for International Development (DFID) along with Bill & Melinda Gates Foundation, announced in February 2011 that they will be granting $40 million to a global project led by Cornell University to combat virulent strains of Ug99.{{ Cite news|url=https://news.cornell.edu/stories/2011/02/40m-grant-fight-wheat-rust-threatens-food-security|title=$40M grant to fight wheat pathogen that threatens global food security|work=Cornell Chronicle|language=en|access-date=5 October 2019|first=Linda|last=McCandless|date=27 February 2011}} The five-year grant to the Durable Rust Resistance in Wheat (DRRW) project supported attempts to identify new resistance genes as well as reproduce and distribute rust resistant wheat seeds to farmers.

There has been a continuous process of development of new resistant cultivars and failure of those cultivars. This demonstrates the need for continuous improvement.

{{Unbulleted list citebundle

|{{*}} {{ Cite journal | last1=Wessels | first1=Elsabet | last2=Prins | first2=Renée | last3=Boshoff | first3=Willem H. P. | last4=Zurn | first4=Jason D. | last5=Acevedo | first5=Maricelis | last6=Pretorius | first6=Zacharias A. | title=Mapping a Resistance Gene to Puccinia graminis f. sp. tritici in the Bread Wheat Cultivar 'Matlabas' | journal=Plant Disease | publisher=American Phytopathological Society | volume=103 | issue=9 | year=2019 | issn=0191-2917 | doi=10.1094/pdis-10-18-1731-re | pages=2337–2344| pmid=31306087 | doi-access=free | s2cid=146090970}}

|{{*}} {{ Cite journal

| language = English

| year = 2021

| publisher = Taylor & Francis

| volume = 43

| first4 = Ronald

| first3 = Zacharias

| first2 = Robert

| first1 = Thomas

| last4 = Depauw

| last3 = Pretorius

| last2 = Park

| last1 = Fetch

| issue = sup2

| pages = S275–S297

| s2cid = 233672540

| journal = Canadian Journal of Plant Pathology

| issn = 0706-0661

| doi = 10.1080/07060661.2021.1902860

| title = Stem rust: its history in Kenya and research to combat a global wheat threat

| bibcode = 2021CaJPP..43S.275F

}}

|{{*}} {{ Cite journal | last1=Pretorius | first1=Zacharias A. | last2=Prins | first2=Renée | last3=Wessels | first3=Elsabet | last4=Bender | first4=Cornel M. | last5=Visser | first5=Botma | last6=Boshoff | first6=Willem H.P. | title=Accomplishments in wheat rust research in South Africa | journal=South African Journal of Science | publisher=Academy of Science of South Africa | volume=116 | issue=11/12 | date=26 November 2020 | issn=1996-7489 | doi=10.17159/sajs.2020/7688 | pages=1–8 | s2cid=229382857}}

}}

{{As of|2020}} modern molecular and molecular genetics techniques are identifying quantitative trait loci (QTLs), particular cellular structures, and individual R genes more efficiently than ever before.{{cite journal | last1=Deng | first1=Yiwen | last2=Ning | first2=Yuese | last3=Yang | first3=Dong-Lei | last4=Zhai | first4=Keran | last5=Wang | first5=Guo-Liang | last6=He | first6=Zuhua | title=Molecular Basis of Disease Resistance and Perspectives on Breeding Strategies for Resistance Improvement in Crops | journal=Molecular Plant | publisher=Cell Press | volume=13 | issue=10 | date=5 October 2020 | issn=1674-2052 | pmid=32979566 | doi=10.1016/j.molp.2020.09.018 | pages=1402–1419| s2cid=221955936 }} These will be needed given the continuing severe, worldwide threat Ug99 poses.

{{Vanchor|Sr35}} confers resistance to all other severe Pgt races and the original Ug99. Salcedo et al., 2017 finds its Avr target, {{Vanchor|AvrSr35}}. Races virulent on Sr35 benefit from nonfunctionalization of AvrSr35 by insertion of a mobile element.

:{{cite journal|issue=1|volume=10|year=2019|publisher=Nature Portfolio|last1=Li|first1=Feng|last2=Upadhyaya|first2=Narayana|last3=Sperschneider|first3=Jana|last4=Matny|first4=Oadi|last5=Nguyen-Phuc|first5=Hoa|last6=Mago|first6=Rohit|last7=Raley|first7=Castle|last8=Miller|first8=Marisa|last9=Silverstein|first9=Kevin|last10=Henningsen|first10=Eva|last11=Hirsch|first11=Cory|last12=Visser|first12=Botma|last13=Pretorius|first13=Zacharias|last14=Steffenson|first14=Brian|last15=Schwessinger|first15=Benjamin|last16=Dodds|first16=Peter|last17=Figueroa|first17=Melania|journal=Nature Communications|s2cid=207916981|bibcode=2019NatCo..10.5068L|pmid=31699975|pmc=6838127|doi=10.1038/s41467-019-12927-7|title=Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation|page=5068|issn=2041-1723|id=(FL {{ORCID|0000-0001-8528-4249}}.) (NMU {{ORCID|0000-0002-3052-0416}}.) (OM {{ORCID|0000-0002-8447-2886}}.) (HNP {{ORCID|0000-0001-9329-4287}}.) (KATS {{ORCID|0000-0002-4955-3218}}.) (EH {{ORCID|0000-0001-9619-3705}}.) (CDH {{ORCID|0000-0002-3409-758X}}.) (BJS {{ORCID|0000-0001-7961-5363}}.) (PND {{ORCID|0000-0003-0620-5923}}. GS [http://scholar.google.com/citations?user=N3w9QUUAAAAJ N3w9QUUAAAAJ]. RID [http://researcherid.com/rid/D-1181-2009 D-1181-2009].) (MF {{ORCID|0000-0003-2636-661X}}. (RID [http://researcherid.com/rid/R-7696-2017 R-7696-2017]) }}

:

:This review cites this research.

:

:{{cite journal|year=2017|publisher=American Association for the Advancement of Science (AAAS)|journal=Science|issn=0036-8075|last1=Salcedo|first1=Andres|last2=Rutter|first2=William|last3=Wang|first3=Shichen|last4=Akhunova|first4=Alina|last5=Bolus|first5=Stephen|last6=Chao|first6=Shiaoman|last7=Anderson|first7=Nickolas|last8=De Soto|first8=Monica|last9=Rouse|first9=Matthew|last10=Szabo|first10=Les|last11=Bowden|first11=Robert|last12=Dubcovsky|first12=Jorge|last13=Akhunov|first13=Eduard|pages=1604–1606|volume=358|issue=6370|s2cid=206664159|doi=10.1126/science.aao7294|title=Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99|pmid=29269474 |pmc=6518949 |bibcode=2017Sci...358.1604S }}

Races

There are 15 races of Ug99, which (under the North American nomenclature system) have the designations TTKSK, TTKSF, TTKST, TTTSK, TTKSP, PTKSK, PTKST, TTKSF+, TTKTT, TTKTK, TTHSK, PTKTK, TTHST, TTKTT+, and TTHTT. They are all closely related and are believed to have evolved from a common ancestor.

{{anchor|PTKS}}

= TTKSK =

Also known as PTKS.{{ Cite journal | last1=Nagarajan | first1=Subrahmaniam | last2=Kogel | first2=Hans J. | last3=Zadoks | first3=Jan C. | author-link3=Jan Zadoks | title=Epidemiology of Puccinia graminis f.sp. tritici-Ug99 in the Rift Valley "Flyway" from Uganda-Kenya to Yemen | journal=Plant Health Progress | publisher=American Phytopathological Society | volume=13 | issue=1 | year=2012 | issn=1535-1025 | doi=10.1094/php-2012-1114-01-rv | page=31 | s2cid=88243732}} The first Ug99 race to be characterised. Like most Ug99 races, and unlike other stem rust varieties, it is virulent against the Sr gene Sr31;

{{Unbulleted list citebundle

|{{*}} {{ Cite journal | last1=Jin | first1=Yue | last2=Szabo | first2=Les J. | last3=Pretorius | first3=Zacharias A. | last4=Singh | first4=Ravi P. | last5=Ward | first5=R. | last6=Fetch | first6=T. | title=Detection of Virulence to Resistance Gene Sr24 Within Race TTKS of Puccinia graminis f. sp. tritici | journal=Plant Disease | publisher=American Phytopathological Society | volume=92 | issue=6 | year=2008 | issn=0191-2917 | doi=10.1094/pdis-92-6-0923 | pages=923–926| pmid=30769714 | doi-access=free | s2cid=55431333}}

|{{*}} {{ Cite journal

| last1=Singh

| first1=Ravi P.

| last2=Hodson

| first2=David P.

| last3=Huerta-Espino

| first3=Julio

| last4=Jin

| first4=Yue

| last5=Bhavani

| first5=Sridhar

| last6=Njau

| first6=Peter

| last7=Herrera-Foessel

| first7=Sybil

| last8=Singh

| first8=Pawan K.

| last9=Singh

| first9=Sukhwinder

| last10=Govindan

| first10=Velu

| title=The Emergence of Ug99 Races of the Stem Rust Fungus is a Threat to World Wheat Production

| journal=Annual Review of Phytopathology

| publisher=Annual Reviews

| date=8 September 2011

| volume=49

| issue=1

| pages=465–481

| doi=10.1146/annurev-phyto-072910-095423

| pmid=21568701

| s2cid=24770327

| issn=0066-4286

}}

| {{*}} {{ Cite book | last=Sparks | first=Donald L. | title=Advances in Agronomy | volume=98 | publication-place=London | isbn=978-0-08-088814-9 | oclc=302357009 | pages=xiii+422 | issn=0065-2113 | publisher=Elsevier | year=2008}} {{RP|page=281}}

| {{*}} {{cite journal | last1=Singh | first1=Ravi P. | last2=Hodson | first2=David P. | last3=Jin | first3=Yue | last4=Lagudah | first4=Evans S. | last5=Ayliffe | first5=Michael A. | last6=Bhavani | first6=Sridhar | last7=Rouse | first7=Matthew N. | last8=Pretorius | first8=Zacharias A. | last9=Szabo | first9=Les J. | last10=Huerta-Espino | first10=Julio | last11=Basnet | first11=Bhoja R. | last12=Lan | first12=Caixia | last13=Hovmøller | first13=Mogens S. | title=Emergence and Spread of New Races of Wheat Stem Rust Fungus: Continued Threat to Food Security and Prospects of Genetic Control | journal=Phytopathology | publisher=American Phytopathological Society | volume=105 | issue=7 | year=2015 | issn=0031-949X | doi=10.1094/phyto-01-15-0030-fi | pages=872–884 | pmid=26120730 | s2cid=205345605}}

}}

also virulent against Sr38. Avirulent against Sr24. It was found in Uganda in {{pslink||1999}}, Kenya in {{pslink||2001}}, Ethiopia in {{pslink||2003}}, Sudan and Yemen in {{pslink||2006}}, Iran in {{pslink||2007}}, and Tanzania in {{pslink||2009}}, Eritrea in {{pslink||2012}}, and Rwanda and Egypt in {{pslink||2014}}.

= TTKSF =

First detected in South Africa in {{pslink||2000}}, Zimbabwe {{pslink||2009}}, and Uganda in {{pslink||2012}}. Avirulent on Sr31.

= TTKST =

Discovered in Kenya in {{pslink||2006}} was the first Ug99 race found to be virulent against Sr gene Sr24. TTKST is now the predominant stem rust race in Kenya. Virulent on Sr31.

= TTTSK =

First detected in Kenya in {{pslink||2007}}, Tanzania in {{pslink||2009}}, Ethiopia in {{pslink||2010}}, Uganda in {{pslink||2012}}, and Rwanda in {{pslink||2014}}. Virulent on Sr31 and Sr36.

= TTKSP =

First detected by Visser et al., 2011 in South Africa in {{pslink||2007}}. Avirulent on Sr31 and virulent on Sr24.

= PTKSK =

First detected in Ethiopia in {{pslink||2007}}, Kenya in {{pslink||2009}}, Yemen in {{pslink||2009}}, and South Africa in {{pslink||2017}}.{{cite journal | last1=Terefe | first1=T. | last2=Pretorius | first2=Z. A. | last3=Visser | first3=B. | last4=Boshoff | first4=W. H. P. | title=First Report of Puccinia graminis f. sp. tritici Race PTKSK, a Variant of Wheat Stem Rust Race Ug99, in South Africa | journal=Plant Disease | publisher=American Phytopathological Society | volume=103 | issue=6 | year=2019 | issn=0191-2917 | doi=10.1094/pdis-11-18-1911-pdn | pages=1421| doi-access=free }} Virulent on Sr31 and avirulent on Sr21.

= PTKST =

First detected in Ethiopia in {{pslink||2007}}, Kenya in {{pslink||2008}}, South Africa in {{pslink||2009}} by Visser et al., 2011, Eritrea and Mozambique and Zimbabwe in {{pslink||2010}}. Virulent on Sr31 and Sr24, but avirulent on Sr21.

= TTKSF+ =

First detected in both South Africa and Zimbabwe in {{pslink||2010}}. Virulent against Sr9h.{{ Cite journal|publisher=Frontiers Media| last1=Randhawa | first1=Mandeep S. | last2=Singh | first2=Ravi P. | last3=Dreisigacker | first3=Susanne | last4=Bhavani | first4=Sridhar | last5=Huerta-Espino | first5=Julio | last6=Rouse | first6=Matthew N. | last7=Nirmala | first7=Jayaveeramuthu | last8=Sandoval-Sanchez | first8=Maricarmen | title=Identification and Validation of a Common Stem Rust Resistance Locus in Two Bi-parental Populations | journal=Frontiers in Plant Science| volume=9 | date=30 November 2018 | page=1788 | issn=1664-462X | doi=10.3389/fpls.2018.01788 | pmid=30555507 | pmc=6283910 | doi-access=free}}{{ Cite journal | last1=Pretorius | first1=Z. A. | last2=Szabo | first2=Les J. | last3=Boshoff | first3=W. H. P. | last4=Herselman | first4=L. | last5=Visser | first5=B. | title=First Report of a New TTKSF Race of Wheat Stem Rust (Puccinia graminis f. sp. tritici) in South Africa and Zimbabwe | journal=Plant Disease | publisher=American Phytopathological Society | volume=96 | issue=4 | year=2012 | issn=0191-2917 | doi=10.1094/pdis-12-11-1027-pdn | pages=590| pmid=30727416 | doi-access=free}}{{ Cite journal|publisher=Springer Science+Business Media| last1=Rouse | first1=Matthew N. | last2=Nirmala | first2=Jayaveeramuthu | last3=Jin | first3=Yue | last4=Chao | first4=Shiaoman | last5=Fetch | first5=Thomas G. | last6=Pretorius | first6=Zacharias A. | last7=Hiebert | first7=Colin W. | title=Characterization of Sr9h, a wheat stem rust resistance allele effective to Ug99|journal=Theoretical and Applied Genetics |volume=127 | issue=8 | date=10 June 2014 | issn=0040-5752 | doi=10.1007/s00122-014-2330-y | pages=1681–1688| pmid=24913360 | s2cid=2598581 }} Avirulent on Sr31 but virulent on Sr9h.

= TTKTT =

First detected in Kenya in {{pslink||2014}}. Also detected in Iraq in 2019, the first such detection in the country. Found in Nepal in 2023.{{Cite web |title=Successful surveillance results in early first detection of Ug99 in South Asia |url=https://news.agropages.com/News/Detail-49760.htm |access-date=22 April 2024 |website=Grainews |language=en}} Virulent on Sr31, Sr24, and SrTmp.

= TTKTK =

First detected in Kenya,

{{Unbulleted list citebundle

|{{*}} {{cite journal | last1=Patpour | first1=M. | last2=Hovmøller | first2=M. S. | last3=Justesen | first3=A. F. | last4=Newcomb | first4=M. | last5=Olivera | first5=P. | last6=Jin | first6=Y. | last7=Szabo | first7=Les J. | last8=Hodson | first8=D. | last9=Shahin | first9=A. A. | last10=Wanyera | first10=R. | last11=Habarurema | first11=I. | last12=Wobibi | first12=S. | title=Emergence of Virulence to SrTmp in the Ug99 Race Group of Wheat Stem Rust, Puccinia graminis f. sp. tritici, in Africa | journal=Plant Disease | publisher=American Phytopathological Society | volume=100 | issue=2 | year=2016 | issn=0191-2917 | doi=10.1094/pdis-06-15-0668-pdn | pages=522 | doi-access=free | s2cid=83728264}}

|{{*}} {{ Cite journal | last1=Prasad | first1=Pramod | last2=Savadi | first2=Siddanna | last3=Bhardwaj | first3=S. C. | last4=Gangwar | first4=O. P. | last5=Kumar | first5=Subodh | title=Rust pathogen effectors: perspectives in resistance breeding | journal=Planta | publisher=Springer Science+Business Media | volume=250 | issue=1 | date=12 April 2019 | issn=0032-0935 | doi=10.1007/s00425-019-03167-6 | pages=1–22 | s2cid=111390872 | pmid=30980247| bibcode=2019Plant.250....1P }}

|{{*}} {{ Cite book | last1=Kang | first1=Zhensheng | last2=Chen | first2=Xianming | title=Stripe rust | publication-place=Dordrecht | isbn=978-94-024-1111-9 | oclc=1006649931 | pages=vii+719 | publisher=Springer Netherlands | s2cid=30527470 | doi=10.1007/978-94-024-1111-9 | date=2017}} {{isbn|978-94-024-1491-2}}. {{isbn|978-94-024-1109-6}}. Page 609.

|{{*}} {{ Cite journal | last1=Figueroa | first1=Melania | last2=Upadhyaya | first2=Narayana M. | last3=Sperschneider | first3=Jana | last4=Park | first4=Robert F. | last5=Szabo | first5=Les J. | last6=Steffenson | first6=Brian | last7=Ellis | first7=Jeff G. | last8=Dodds | first8=Peter N. | title=Changing the Game: Using Integrative Genomics to Probe Virulence Mechanisms of the Stem Rust Pathogen Puccinia graminis f. sp. tritici | journal=Frontiers in Plant Science | publisher=Frontiers Media | volume=7 | date=24 February 2016 | page=205 | issn=1664-462X | doi=10.3389/fpls.2016.00205 | s2cid=12619852 | pmid=26941766 | pmc=4764693| doi-access=free }}

}} Rwanda, Uganda, Eritrea, and Egypt in {{pslink||2014}}. Virulent on Sr31 and SrTmp.

= TTHSK =

First detected in Kenya in {{pslink||2014}}. Differs from the original (TTKSK) by avirulence against Sr30. Similar to TTHST. Virulent on Sr31 but avirulent on Sr30.

= PTKTK =

First detected in Kenya in {{pslink||2014}}. Differs from PTKSK by virulence against SrTmp. Differs from TTKTK by avirulence against Sr21. Virulent on Sr31 and Sr24, but avirulent on Sr21.

= TTHST =

First detected in Kenya in {{pslink||2013}}. Virulent on Sr31 and Sr24, but avirulent on Sr30.

= TTKTT+ =

First detected in Kenya in {{pslink||2019}}. Virulent to Sr31, Sr24, SrTmp, and Sr8155B1.

= TTHTT =

First detected in Kenya in {{pslink||2020}}. Virulent to Sr31, Sr24, and SrTmp, avirulent to Sr30.

Timeline

{{prose|date=August 2024}}

= 1993 =

  • There is some evidence that race TTKSK may have been present in Kenya.{{Cite journal |last=Singh |first=Ravi P. |last2=Hodson |first2=David |last3=Huerta-Espino |first3=Julio |last4=Jin |first4=Yue |last5=Njau |first5=Peter |last6=Wanyera |first6=Ruth |last7=Herrera-Foessel |first7=Sybil |last8=Ward |first8=Richard W. |year=2008 |title=Will Stem Rust Destroy The World's Wheat Crop? |url=https://naldc-legacy.nal.usda.gov/naldc/download.xhtml?id=36520&content=PDF |url-status=dead |journal=Advances in Agronomy |publisher=Elsevier B. V. |volume=98 |pages=272–309 |doi=10.1016/S0065-2113(08)00205-8 |isbn=9780123743558 |archive-url=https://web.archive.org/web/20201108063602/https://naldc-legacy.nal.usda.gov/naldc/download.xhtml?id=36520&content=PDF |archive-date=8 November 2020 |access-date=29 December 2018}}

= 1998 =

  • Severe stem rust infections observed in Uganda. Ug99 identified, characterised as having virulence on Sr31 and named.

= 2000 =

= 2001 =

  • TTKSK detected in Kenya.

= 2003 =

= 2006 =

  • TTKSK detected in Sudan and Yemen.
  • TTKST, a new variant of Ug99 with virulence to Sr24, detected in Kenya.

= 2007 =

= 2008 =

  • FAO announced the presence of Ug99 in Iran.{{Cite journal |last=Singh |first=Ravi P. |last2=Hodson |first2=David P. |last3=Huerta-Espino |first3=Julio |last4=Jin |first4=Yue |last5=Bhavani |first5=Sridhar |last6=Njau |first6=Peter |last7=Herrera-Foessel |first7=Sybil |last8=Singh |first8=Pawan K. |last9=Singh |first9=Sukhwinder |last10=Govindan |first10=Velu |date=8 September 2011 |title=The Emergence of Ug99 Races of the Stem Rust Fungus is a Threat to World Wheat Production |journal=Annual Review of Phytopathology |publisher=Annual Reviews |volume=49 |issue=1 |pages=465–481 |doi=10.1146/annurev-phyto-072910-095423 |issn=0066-4286 |pmid=21568701 |s2cid=24770327}}
  • PTKST detected in Kenya.
  • Present in Yemen.

= 2009 =

{{Cite journal |last=Singh |first=Ravi P. |last2=Hodson |first2=David P. |last3=Huerta-Espino |first3=Julio |last4=Jin |first4=Yue |last5=Bhavani |first5=Sridhar |last6=Njau |first6=Peter |last7=Herrera-Foessel |first7=Sybil |last8=Singh |first8=Pawan K. |last9=Singh |first9=Sukhwinder |last10=Govindan |first10=Velu |date=8 September 2011 |title=The Emergence of Ug99 Races of the Stem Rust Fungus is a Threat to World Wheat Production |journal=Annual Review of Phytopathology |publisher=Annual Reviews |volume=49 |issue=1 |pages=465–481 |doi=10.1146/annurev-phyto-072910-095423 |issn=0066-4286 |pmid=21568701 |s2cid=24770327}}

...cites this study:

{{ Cite journal | last1 = Visser | first1 = B | last2 = Herselman | first2 = L | last3 = Park | first3 = RF | last4 = Karaoglu | first4 = H | last5 = Bender | first5 = CM | last6 = Pretorius | first6 = Z | year = 2010 | title= Characterization of two new Puccinia graminis f. sp. tritici races within the Ug99 lineage in South Africa | journal=Euphytica | volume = 179 | pages = 119–127 | doi = 10.1007/s10681-010-0269-x | s2cid = 6176783 }}

= 2010 =

= 2013 =

  • TTHST confirmed in Kenya

= 2014 =

  • TTKTK confirmed in Egypt,{{ Unbulleted list citebundle

|{{*}} {{cite journal | last1=Patpour | first1=M. | last2=Hovmøller | first2=M. S. | last3=Shahin | first3=A. A. | last4=Newcomb | first4=M. | last5=Olivera | first5=P. | last6=Jin | first6=Y. | last7=Luster | first7=D. | last8=Hodson | first8=D. | last9=Nazari | first9=K. | last10=Azab | first10=M. | title=First Report of the Ug99 Race Group of Wheat Stem Rust, Puccinia graminis f. sp. tritici, in Egypt in 2014 | journal=Plant Disease | publisher=American Phytopathological Society | volume=100 | issue=4 | year=2016 | issn=0191-2917 | doi=10.1094/pdis-08-15-0938-pdn | pages=863 | doi-access=free }}

|{{*}} This study is cited by the following reviews & books:

|{{*}} {{cite journal | last1=Prasad | first1=Pramod | last2=Savadi | first2=Siddanna | last3=Bhardwaj | first3=S. C. | last4=Gangwar | first4=O. P. | last5=Kumar | first5=Subodh | title=Rust pathogen effectors: perspectives in resistance breeding | journal=Planta | publisher=Springer Science+Business Media | volume=250 | issue=1 | date=12 April 2019 | issn=0032-0935 | doi=10.1007/s00425-019-03167-6 | pages=1–22 | s2cid=111390872 | pmid=30980247| bibcode=2019Plant.250....1P }}

|{{*}} {{ Cite journal|last1=Bhavani|first1=Sridhar|last2=Hodson|first2=David P.|last3=Huerta-Espino|first3=Julio|last4=Randhawa|first4=Mandeep S.|last5=Singh|first5=Ravi P.|title=Progress in breeding for resistance to Ug99 and other races of the stem rust fungus in CIMMYT wheat germplasm|journal=Frontiers of Agricultural Science and Engineering|publisher=Engineering Sciences Press|volume=6|issue=3|year=2019|issn=2095-7505|doi=10.15302/j-fase-2019268|page=210|s2cid=202011907}}

|{{*}} {{cite journal|publisher=Elsevier| last1=Abdelmageed | first1=Kishk | last2=CHANG | first2=Xu-hong | last3=WANG | first3=De-mei | last4=WANG | first4=Yan-jie | last5=YANG | first5=Yu-shuang | last6=ZHAO | first6=Guang-cai | last7=TAO | first7=Zhi-qiang | title=Evolution of varieties and development of production technology in Egypt wheat: A review | journal=Journal of Integrative Agriculture | volume=18 | issue=3 | year=2019 | issn=2095-3119 | doi=10.1016/s2095-3119(18)62053-2 | pages=483–495 | bibcode=2019JIAgr..18..483A | s2cid=92749147}}

|{{*}} {{Cite book |last=Awaad |first=Hassan Auda |title=Mitigating Environmental Stresses for Agricultural Sustainability in Egypt |last2=El-Naggar |first2=Doaa Ragheb |publisher=Springer International Publishing |year=2021 |isbn=978-3-030-64322-5 |series=Springer Water |publication-place=Cham, Switzerland |pages=311–370 |chapter=Developing Rust Resistance of Wheat Genotypes Under Egyptian Conditions |doi=10.1007/978-3-030-64323-2_12 |issn=2364-6934 |s2cid=234309678}} Page 327.

}} Kenya, Eritrea, Rwanda, and Uganda.

  • TTHSK confirmed in Kenya{{Unbulleted list citebundle

|{{*}} {{cite journal | last1=Fetch | first1=T. | last2=Zegeye | first2=T. | last3=Park | first3=R. F. | last4=Hodson | first4=D. | last5=Wanyera | first5=R. | title=Detection of Wheat Stem Rust Races TTHSK and PTKTK in the Ug99 Race Group in Kenya in 2014 | journal=Plant Disease | publisher=American Phytopathological Society | volume=100 | issue=7 | year=2016 | issn=0191-2917 | doi=10.1094/pdis-11-15-1356-pdn | pages=1495 | doi-access=free | s2cid=87136095}}

|{{*}} This study is cited by the following reviews & books:

|{{*}} {{cite journal | last1=Prasad | first1=Pramod | last2=Savadi | first2=Siddanna | last3=Bhardwaj | first3=S. C. | last4=Gangwar | first4=O. P. | last5=Kumar | first5=Subodh | title=Rust pathogen effectors: perspectives in resistance breeding | journal=Planta | publisher=Springer Science+Business Media | volume=250 | issue=1 | date=12 April 2019 | issn=0032-0935 | doi=10.1007/s00425-019-03167-6 | pages=1–22 | s2cid=111390872 | pmid=30980247| bibcode=2019Plant.250....1P }}

|{{*}} {{cite journal | last1=Bhavani | first1=Sridhar | last2=Hodson | first2=David P. | last3=Huerta-Espino | first3=Julio | last4=Randhawa | first4=Mandeep S. | last5=Singh | first5=Ravi P. | title=Progress in breeding for resistance to Ug99 and other races of the stem rust fungus in CIMMYT wheat germplasm | journal=Frontiers of Agricultural Science and Engineering | publisher=Engineering Sciences Press | volume=6 | issue=3 | year=2019 | issn=2095-7505 | doi=10.15302/j-fase-2019268 | page=210 | s2cid=202011907}}

|{{*}} {{Cite book |last=Awaad |first=Hassan Auda |title=Mitigating Environmental Stresses for Agricultural Sustainability in Egypt |last2=El-Naggar |first2=Doaa Ragheb |publisher=Springer International Publishing |year=2021 |isbn=978-3-030-64322-5 |series=Springer Water |publication-place=Cham, Switzerland |pages=311–370 |chapter=Developing Rust Resistance of Wheat Genotypes Under Egyptian Conditions |doi=10.1007/978-3-030-64323-2_12 |issn=2364-6934 |s2cid=234309678}} Page 327.

|{{*}} {{cite journal | last1=Kenis | first1=Marc | last2=Agboyi | first2=Lakpo Koku | last3=Adu-Acheampong | first3=Richard | last4=Ansong | first4=Michael | last5=Arthur | first5=Stephen | last6=Attipoe | first6=Prudence Tonator | last7=Baba | first7=Abdul-Salam Mahamud | last8=Beseh | first8=Patrick | last9=Clottey | first9=Victor Attuquaye | last10=Combey | first10=Rofela | last11=Dzomeku | first11=Israel | last12=Eddy-Doh | first12=Mary Akpe | last13=Fening | first13=Ken Okwae | last14=Frimpong-Anin | first14=Kofi | last15=Hevi | first15=Walter | last16=Lekete-Lawson | first16=Emmanuellah | last17=Nboyine | first17=Jerry Asalma | last18=Ohene-Mensah | first18=Godfried | last19=Oppong-Mensah | first19=Birgitta | last20=Nuamah | first20=Hannah Serwaa Akoto | last21=van der Puije | first21=Grace | last22=Mulema | first22=Joseph | title=Horizon scanning for prioritising invasive alien species with potential to threaten agriculture and biodiversity in Ghana | journal=NeoBiota | publisher=Pensoft Publishers | volume=71 | date=8 February 2022 | issn=1314-2488 | doi=10.3897/neobiota.71.72577 | pages=129–148 | s2cid=246821009 | doi-access=free }}

|{{*}} {{cite journal | last1=Fetch | first1=Thomas G. | last2=Park | first2=Robert F. | last3=Pretorius | first3=Zacharias A. | last4=Depauw | first4=Ronald M. | title=Stem rust: its history in Kenya and research to combat a global wheat threat | journal=Canadian Journal of Plant Pathology | publisher=Agriculture and Agri-Food Canada (T&F) | volume=43 | issue=sup2 | date=27 September 2021 | issn=0706-0661 | doi=10.1080/07060661.2021.1902860 | pages=S275–S297 | bibcode=2021CaJPP..43S.275F | s2cid=233672540}}

}}

  • PTKTK confirmed in Kenya
  • TTKTT confirmed in Kenya.
  • TTKST detected in Egypt.
  • TTKSK detected in Egypt.

= 2017 =

  • PTKSK confirmed in South Africa.

= 2019 =

  • TTKTT detected in Iraq.
  • TTKTT+ confirmed in Kenya.

= 2020 =

  • TTHTT confirmed in Kenya.

= 2023 =

  • TTKTT confirmed in Nepal.

Geographic spread

{{expand section|date=November 2020}}

Because stem rust is very series disease (as with many fungi) spreads its spores across long distances with the help of natural air currents, containment is difficult. Advances in fluid mechanics which are commonly used for meteorology have also aided Ug99 dispersal prediction. This is especially important for inter-continental, intermittent spread, such as from Eastern South Africa to Western Australia.

{{ Cite journal |

language=en|

year=2015|

issue=1|

volume=53|

publisher=Annual Reviews|

first2=Shane|

first1=David|

last2=Ross|

pages=591–611|

last1=Schmale|

journal=Annual Review of Phytopathology|

title=Highways in the Sky: Scales of Atmospheric Transport of Plant Pathogens|

doi=10.1146/annurev-phyto-080614-115942|

pmid=26047561}}

= China =

Although Ug99 has not yet reached China,{{cite journal | last1=Wu | first1=Xian Xin | last2=Lin | first2=Qiu Jun | last3=Ni | first3=Xin Yu | last4=Sun | first4=Qian | last5=Chen | first5=Rong Zhen | last6=Xu | first6=Xiao Feng | last7=Qiu | first7=Yong Chun | last8=Li | first8=Tian Ya | title=Characterization of Wheat Monogenic Lines with Known Sr Genes and Wheat Lines with Resistance to the Ug99 Race Group for Resistance to Prevalent Races of Puccinia graminis f. sp. tritici in China | journal=Plant Disease | publisher=American Phytopathological Society | volume=104 | issue=7 | year=2020 | issn=0191-2917 | doi=10.1094/pdis-12-19-2736-re | pages=1939–1943| pmid=32396054 | doi-access=free }} other stem rust races already have, and an effort is under way to marry resistance against present races with future needs for resistance against Ug99 whenever it arrives.

= Lebanon =

Although Sr5, Sr21, Sr9e, Sr7b, Sr11, Sr6, Sr8a, Sr9g, Sr9b, Sr30, Sr17, Sr9a, Sr9d, Sr10, SrTmp, Sr38, and SrMcN are no longer effective in Lebanon, Sr11, Sr24, and Sr31 still are which is diagnostic for the absence of Ug99 from Lebanon.{{Cite AV media|url=http://youtube.com/watch?v=9ksaCvAy_XQ&t=2677 |archive-url=https://ghostarchive.org/varchive/youtube/20211215/9ksaCvAy_XQ |archive-date=15 December 2021 |url-status=live|publisher=International Institute of Tropical Agriculture + CGIAR |series=CGIAR Germplasm Health Webinar series|volume=Phytosanitary Awareness Week |title=(DAY 2) – Phytosanitary Safety for Transboundary pest prevention – Yellow and Black rust population variability|date=9 November 2020|time-caption=Slide at|time=00:44:37|editor-first1=Rola | editor-last1=El Amil | last=Kumari | first=Safaa | author-link=Safaa Kumari}}{{cbignore}}

= Iraq =

Detected in Iraq in 2019.

= South Asia =

Low-levels of TTKTT were detected in Nepal in 2023, but surveillance has not revealed any propagation in the region. {{As of|2013}} it was the US Director of National Intelligence's assessment that Ug99 would arrive in South Asia soon, in the following few years. This was expected to cause worldwide supply disruptions because, although productivity was growing in Eastern Europe and could theoretically fill that gap, governments worldwide had shown a readiness to forbid exports.{{cite web |url=http://www.dni.gov/files/documents/Intelligence%20Reports/2013%20ATA%20SFR%20for%20SSCI%2012%20Mar%202013.pdf | title=Statement for the Record | publisher=Senate Select Committee on Intelligence | first=James | last=Clapper | author-link=James Clapper | date=12 March 2013 | website=Director of National Intelligence}}

See also

References

{{Reflist}}