Ug99

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.[1] 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.[2] It can cause up to 100% crop losses and is virulent against many resistance genes which have previously protected wheat against stem rust.

Puccinia graminis
Scientific classification
Kingdom:
Fungi
Phylum:
Basidiomycota
Class:
Pucciniomycetes
Subclass:
Incertae sedis
Order:
Pucciniales
Family:
Pucciniaceae
Genus:
Puccinia
Species:
P. graminis
Subspecies:
P. graminis tritici
Variety:
Ug99

Although Ug99-resistant varieties of wheat do exist,[2] 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.[1]

The original race of Ug99, which is designated as 'TTKSK' under the North American nomenclature system, was first detected in Uganda in 1998[3] and first characterised in 1999[3] (hence the name Ug99) and has since been detected in Kenya, Ethiopia, Eritrea, Sudan, Yemen, Iran, Tanzania, Mozambique, Zimbabwe, South Africa,[4] and Egypt. There are now 15 known races of Ug99.[5] 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.[1]

Genetics

Ug99 is the product of a type of somatic nuclear exchange event which has not been observed in other stem rust races.[6] During this event and thereafter the nuclei have not experienced recombination.[6]

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.[7] These resistant Sr genes, of which 50 are known, give wheat different resistances to stem rust.[3] The virulence in Uganda was virulent against Sr31 and is specific to Ug99.[3] 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.[3] (In the decades since, however, Sr31-virulence has evolved in other strains in other locations.[8] Patpour et al., 2022 finds it in Spain and Siberia.)[8]

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.[9] This resistance was present without the Ug99 pathogen challenge being present in NA to drive its selection.[9] USDA has studied winter wheat land races where resistance is more probable.[10]

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.[11] 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.[11]

There has been a continuous process of development of new resistant cultivars and failure of those cultivars.[12] This demonstrates the need for continuous improvement.[12]

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.[13] These will be needed given the continuing severe, worldwide threat Ug99 poses.[13][1]

Sr35 confers resistance to all other severe Pgt races and the original Ug99.[14] Salcedo et al., 2017 finds its Avr target, AvrSr35.[14] Races virulent on Sr35 benefit from nonfunctionalization of AvrSr35 by insertion of a mobile element.[14]

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+,[4] TTKTT, TTKTK, TTHSK, PTKTK, TTHST, TTKTT+, and TTHTT.[5] They are all closely related and are believed to have evolved from a common ancestor.[1]

TTKSK

Also known as PTKS.[15] The first Ug99 race to be characterised.[16][15] Like most Ug99 races, and unlike other stem rust varieties, it is virulent against the Sr gene Sr31;[16][15] also virulent against Sr38.[15] Avirulent against Sr24.[16][15] It was found in Uganda[15] in 1999, Kenya[16] in 2001,[5] Ethiopia in 2003,[5] Sudan and Yemen in 2006,[5] Iran in 2007,[5] and Tanzania[1] in 2009,[5] Eritrea in 2012,[5] and Rwanda and Egypt in 2014.[5]

TTKSF

First detected in South Africa in 2000,[5] Zimbabwe 2009,[5] and Uganda in 2012.[5] Avirulent on Sr31.[5]

TTKST

Discovered in Kenya in 2006[16] was the first Ug99 race found to be virulent against Sr gene Sr24.[1][16] TTKST is now the predominant stem rust race in Kenya.[1] Virulent on Sr31.[5]

TTTSK

First detected in Kenya in 2007,[5] Tanzania in 2009,[5] Ethiopia in 2010,[5] Uganda in 2012,[5] and Rwanda in 2014.[5] Virulent on Sr31 and Sr36.[5]

TTKSP

First detected by Visser et al., 2011 in South Africa in 2007.[17][5] Avirulent on Sr31 and virulent on Sr24.[5]

PTKSK

First detected in Ethiopia in 2007,[5] Kenya in 2009,[5] Yemen in 2009,[5] and South Africa in 2017.[5][18] Virulent on Sr31 and avirulent on Sr21.[5]

PTKST

First detected in Ethiopia in 2007,[5] Kenya in 2008,[5] South Africa in 2009 by Visser et al., 2011,[17][5] Eritrea and Mozambique and Zimbabwe in 2010.[5] Virulent on Sr31 and Sr24, but avirulent on Sr21.[5]

TTKSF+

First detected in both South Africa and Zimbabwe in 2010.[5] Virulent against Sr9h.[19][20][21] Avirulent on Sr31 but virulent on Sr9h.[5]

TTKTT

First detected in Kenya in 2014.[5] Also detected in Iraq in 2019, the first such detection in the country.[5] Virulent on Sr31, Sr24, and SrTmp.[5]

TTKTK

First detected in Kenya,[5][22] Rwanda,[5][22] Uganda,[5][22] Eritrea,[5] and Egypt[5][22] in 2014. Virulent on Sr31 and SrTmp.[5]

TTHSK

First detected in Kenya in 2014.[23] Differs from the original (TTKSK) by avirulence against Sr30.[23] Similar to TTHST.[23] Virulent on Sr31 but avirulent on Sr30.[5]

PTKTK

First detected in Kenya in 2014.[23] Differs from PTKSK by virulence against SrTmp.[23] Differs from TTKTK by avirulence against Sr21.[23] Virulent on Sr31 and Sr24, but avirulent on Sr21.[5]

TTHST

First detected in Kenya in 2013.[5] Virulent on Sr31 and Sr24, but avirulent on Sr30.[5]

TTKTT+

First detected in Kenya in 2019.[5] Virulent to Sr31, Sr24, SrTmp, and Sr8155B1.[5]

TTHTT

First detected in Kenya in 2020.[5] Virulent to Sr31, Sr24, and SrTmp, avirulent to Sr30.[5]

Timeline

1993
  • There is some evidence that race TTKSK may have been present in Kenya.[24]

1998
  • Severe stem rust infections observed in Uganda. Ug99 identified, characterised as having virulence on Sr31 and named.[24]

2000

2001

2003

2006

2007

2008

2009

2010

2013

2014

2017
  • PTKSK confirmed in South Africa.[5]

2019

2020

Geographic spread

Because stem rust (as with many fungi) spreads its spores across long distances with the help of natural air currents, containment is difficult.[26] Advances in fluid mechanics which are commonly used for meteorology have also aided Ug99 dispersal prediction.[26] This is especially important for inter-continental, intermittent spread, such as from Eastern South Africa to Western Australia.[26]

China

Although Ug99 has not yet reached China,[27] other stem rust races already have,[27] and an effort is under way to marry resistance against present races with future needs for resistance against Ug99 whenever it arrives.[27]

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.[28]

Iraq

Detected in Iraq in 2019.[5]

South Asia

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.[29] However as of April 2021 South Asia remains unaffected.[5]

See also

References
  1. Singh, Ravi P.; Hodson, David P.; Huerta-Espino, Julio; Jin, Yue; Bhavani, Sridhar; Njau, Peter; Herrera-Foessel, Sybil; Singh, Pawan K.; Singh, Sukhwinder; Govindan, Velu (8 September 2011). "The Emergence of Ug99 Races of the Stem Rust Fungus is a Threat to World Wheat Production". Annual Review of Phytopathology. Annual Reviews. 49 (1): 465–481. doi:10.1146/annurev-phyto-072910-095423. ISSN 0066-4286. PMID 21568701. S2CID 24770327.
  2. Gross, Michael (2013). "Pests on the move". Current Biology. Cell Press. 23 (19): R855–R857. doi:10.1016/j.cub.2013.09.034. ISSN 0960-9822. PMID 24251330. S2CID 15559913.
  4. Hodson, D. P.; Grønbech-Hansen, J.; Lassen, P.; Alemayehu, Y.; Arista, J.; Sonder, K.; Kosina, P.; Moncada, P.; Nazari, K.; Park, R. F.; Pretorius, Z. A.; Szabo, L. J.; Fetch, T.; Jin, Y. "Tracking the Wheat Rust Pathogens" (PDF). 2012 Borlaug Global Rust Initiative Technical Workshop Proceedings. Borlaug Global Rust Initiative. Archived (PDF) from the original on October 5, 2019. Retrieved 28 November 2012.
  5. "Pathotype Tracker – Where is Ug99?". The International Maize and Wheat Improvement Center.
  6. Li, Feng; Upadhyaya, Narayana M.; Sperschneider, Jana; Matny, Oadi; Nguyen-Phuc, Hoa; Mago, Rohit; Raley, Castle; Miller, Marisa E.; Silverstein, Kevin A. T.; Henningsen, Eva; Hirsch, Cory D.; Visser, Botma; Pretorius, Zacharias A.; Steffenson, Brian J.; Schwessinger, Benjamin; Dodds, Peter N.; Figueroa, Melania (2019-11-07). "Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation". Nature Communications. Nature Portfolio. 10 (1): 5068. Bibcode:2019NatCo..10.5068L. doi:10.1038/s41467-019-12927-7. ISSN 2041-1723. PMC 6838127. PMID 31699975. S2CID 207916981.
  7. "USDA Coordinated Approach to Address Pgt-Ug99". ARS (USDA Agricultural Research Service). September 20, 2017.
  10. USDA Agricultural Research Service (2007). Action Plan to Minimize Impact of Ug99 Stem Rust in the United States (PDF) (Report) (1.01 ed.). USDA Agricultural Research Service. pp. 1–27. Archived from the original (PDF) on 2022-10-20.
  11. McCandless, Linda (February 27, 2011). "$40M grant to fight wheat pathogen that threatens global food security". Cornell Chronicle. Retrieved October 5, 2019.
  13. Deng, Yiwen; Ning, Yuese; Yang, Dong-Lei; Zhai, Keran; Wang, Guo-Liang; He, Zuhua (2020-10-05). "Molecular Basis of Disease Resistance and Perspectives on Breeding Strategies for Resistance Improvement in Crops". Molecular Plant. Cell Press. 13 (10): 1402–1419. doi:10.1016/j.molp.2020.09.018. ISSN 1674-2052. PMID 32979566. S2CID 221955936.
  14. Li, Feng; Upadhyaya, Narayana; Sperschneider, Jana; Matny, Oadi; Nguyen-Phuc, Hoa; Mago, Rohit; Raley, Castle; Miller, Marisa; Silverstein, Kevin; Henningsen, Eva; Hirsch, Cory; Visser, Botma; Pretorius, Zacharias; Steffenson, Brian; Schwessinger, Benjamin; Dodds, Peter; Figueroa, Melania (2019). "Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation". Nature Communications. Nature Portfolio. 10 (1): 5068. Bibcode:2019NatCo..10.5068L. doi:10.1038/s41467-019-12927-7. ISSN 2041-1723. PMC 6838127. PMID 31699975. S2CID 207916981. (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 N3w9QUUAAAAJ. RID D-1181-2009.) (MF ORCID 0000-0003-2636-661X. (RID R-7696-2017).
    This review cites this research.
    Salcedo, Andres; Rutter, William; Wang, Shichen; Akhunova, Alina; Bolus, Stephen; Chao, Shiaoman; Anderson, Nickolas; De Soto, Monica; Rouse, Matthew; Szabo, Les; Bowden, Robert; Dubcovsky, Jorge; Akhunov, Eduard (2017). "Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99". Science. American Association for the Advancement of Science (AAAS). 358 (6370): 1604–1606. doi:10.1126/science.aao7294. ISSN 0036-8075. PMC 6518949. PMID 29269474. S2CID 206664159.
  15. Nagarajan, Subrahmaniam; Kogel, Hans J.; Zadoks, Jan C. (2012). "Epidemiology of Puccinia graminis f.sp. tritici-Ug99 in the Rift Valley "Flyway" from Uganda-Kenya to Yemen". Plant Health Progress. American Phytopathological Society. 13 (1): 31. doi:10.1094/php-2012-1114-01-rv. ISSN 1535-1025. S2CID 88243732.
  17. This review... Singh, Ravi P.; Hodson, David P.; Huerta-Espino, Julio; Jin, Yue; Bhavani, Sridhar; Njau, Peter; Herrera-Foessel, Sybil; Singh, Pawan K.; Singh, Sukhwinder; Govindan, Velu (8 September 2011). "The Emergence of Ug99 Races of the Stem Rust Fungus is a Threat to World Wheat Production". Annual Review of Phytopathology. Annual Reviews. 49 (1): 465–481. doi:10.1146/annurev-phyto-072910-095423. ISSN 0066-4286. PMID 21568701. S2CID 24770327. ...cites this study: Visser, B; Herselman, L; Park, RF; Karaoglu, H; Bender, CM; Pretorius, Z (2010). "Characterization of two new Puccinia graminis f. sp. tritici races within the Ug99 lineage in South Africa". Euphytica. 179: 119–127. doi:10.1007/s10681-010-0269-x. S2CID 6176783.
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  19. Randhawa, Mandeep S.; Singh, Ravi P.; Dreisigacker, Susanne; Bhavani, Sridhar; Huerta-Espino, Julio; Rouse, Matthew N.; Nirmala, Jayaveeramuthu; Sandoval-Sanchez, Maricarmen (2018-11-30). "Identification and Validation of a Common Stem Rust Resistance Locus in Two Bi-parental Populations". Frontiers in Plant Science. Frontiers Media. 9: 1788. doi:10.3389/fpls.2018.01788. ISSN 1664-462X. PMC 6283910. PMID 30555507.
  20. Pretorius, Z. A.; Szabo, Les J.; Boshoff, W. H. P.; Herselman, L.; Visser, B. (2012). "First Report of a New TTKSF Race of Wheat Stem Rust (Puccinia graminis f. sp. tritici) in South Africa and Zimbabwe". Plant Disease. American Phytopathological Society. 96 (4): 590. doi:10.1094/pdis-12-11-1027-pdn. ISSN 0191-2917. PMID 30727416.
  21. Rouse, Matthew N.; Nirmala, Jayaveeramuthu; Jin, Yue; Chao, Shiaoman; Fetch, Thomas G.; Pretorius, Zacharias A.; Hiebert, Colin W. (2014-06-10). "Characterization of Sr9h, a wheat stem rust resistance allele effective to Ug99". Theoretical and Applied Genetics. Springer Science+Business Media. 127 (8): 1681–1688. doi:10.1007/s00122-014-2330-y. ISSN 0040-5752. PMID 24913360. S2CID 2598581.
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  26. Schmale, David; Ross, Shane (2015). "Highways in the Sky: Scales of Atmospheric Transport of Plant Pathogens". Annual Review of Phytopathology. Annual Reviews. 53 (1): 591–611. doi:10.1146/annurev-phyto-080614-115942. PMID 26047561.
  27. Wu, Xian Xin; Lin, Qiu Jun; Ni, Xin Yu; Sun, Qian; Chen, Rong Zhen; Xu, Xiao Feng; Qiu, Yong Chun; Li, Tian Ya (2020). "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". Plant Disease. American Phytopathological Society. 104 (7): 1939–1943. doi:10.1094/pdis-12-19-2736-re. ISSN 0191-2917. PMID 32396054.
  28. Kumari, Safaa (2020-11-09). El Amil, Rola (ed.). (DAY 2) - Phytosanitary Safety for Transboundary pest prevention - Yellow and Black rust population variability. CGIAR Germplasm Health Webinar series. Vol. Phytosanitary Awareness Week. International Institute of Tropical Agriculture + CGIAR. Slide at 00:44:37. Archived from the original on 2021-12-15.
  29. Clapper, James (March 12, 2013). "Statement for the Record" (PDF). Director of National Intelligence. Senate Select Committee on Intelligence.
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