Puccinia graminis f. sp. tritici race TTKSK

Taxonomy

Domain	Eukarya
Kingdom	Fungi
Phylum	Basidiomycota
Subphylum	Pucciniomycotina
Class	Pucciniomycetes
Order	Pucciniales
Suborder	Uredinineae
Family	Pucciniaceae
Genus	Puccinia

Scientific Name

Puccinia graminis

Common Name

wheat stem rust

Author: Leticia Kumar, University of Florida

Reviewed by: Jeffrey Rollins, University of Florida

Pathogen

Puccinia graminis f. sp. tritici (Pgt) has significantly impacted worldwide wheat (Triticum aestivum L.) production throughout human history. The most recent wheat stem rust outbreak in the United States was reported around 1953 - 1954, with an estimated 40% yield loss (13, 14). The loss in yield is attributable to several factors associated with colonization of Pgt on its poaceous hosts. These include competition with the fungus for nutrients, lodging due to weakened stems, and reduced metabolic efficiency.

Telial host range includes wheat, (Triticum aestivum), barley (Hordeum vulgare), goatgrass (Aegilops spp.) and wild rye (Elymus spp.). Aecial host range includes common barberry (Berberis vulgaris), additional Berberis spp., Mahoberberis spp., and Mahonia spp.

Prolific spore generation, wind-borne dispersal, and viability of spores over thousands of miles are characteristics that have made this an efficiently destructive pathogen (3). Until the late 1990s, successful mitigation of the disease was largely attributable to deployment of wheat resistance genes (11) and alternate host eradication programs (9). In 1998, observations revealed a virulent form of Pgt on wheat lines armed with the Sr31 resistance gene in Uganda. In 1999, further analyses confirmed existence of a new race of the pathogen, which was subsequently termed “Ug99” in reference to the country and year in which it was first reported (Pgt-Ug99; 7). In accordance with the nomenclature system of North America, the new virulent race was designated TTKSK (10). It may be noted that although often referred to as such, Ug99 is not a race but rather an individual of the TTKSK race.

The significance of the new pathogen on global wheat production was underscored with a report (4) that laid the foundation for international collaborative efforts addressing the threat of Pgt-Ug99 (7). Of the wheat currently in production across the globe, approximately 90% is considered Ug99 stem rust susceptible (12). Since 1999, Pgt-Ug99 has rapidly altered genetically, giving rise to eight known variants, and has migrated deeper into the African continent as well as the Middle East (5). Due to the highly mobile nature of the fungus, Ug99 stem rust is expected to arrive in North America, although as of April 2014 there have not yet been reports. Anticipation of its arrival has been the impetus of current research objectives and development of action plans (6).

Symptoms and Signs

Early symptoms of the disease on poaceous crops include chlorotic specks and blisters. However, it is the signs of the pathogen that are more often visualized. Blisters on the plant tissue rupture to reveal oval-shaped, elongated pustules of red-orange urediniospores on the stem, leaf sheath, both abaxial and adaxial sides of the leaves, and spikes. Teliospores may be found on the sheaths and stems of the poaceous hosts at growing season’s end. As telia develop, the reddish-orange pustules darken into black lesions (11).

On the alternate host, symptoms include chlorosis and blisters. Signs of the pathogen on barberry are observed as aggregated cup-shaped, orange-pink aecia on leaves, petioles, flowers, and fruit (11).

Ecology and Spread

This pathogen is a heteroecious rust (i.e., requiring separate host organisms for life cycle completion). In presence of the alternate host, genera Berberis, Mahoberberis, and Mahonia, the pathogen spreads to wheat as aeciospores (formed on barberry, which infect wheat). In the absence of the alternate host, the fungus infects the plant in the form of urediniospores (formed on wheat, which infect wheat). Disease inception and progression occur similarly whether introduced as aeciospores or urediniospores: germination on the wheat host through stomata, colonization of plant tissue, and formation of the reproductive structures, uredinium, observed as pustules producing rust-colored, asexual urediniospores. The black-colored, overwintering spores, teliospores, develop at late stages in the wheat growing cycle, inspiring the pathogen’s alternate moniker “black rust.” Under favorable conditions associated with spring time, the teliospores develop basidiospores, which are the spore type pathogenic on the alternate barberry host. The disease cycle continues as the fungus produces the pycnia. Upon mating between different pycniospores, aeciospores are developed in aecia, which infect the grass hosts and complete the life cycle (11).

In the United States, airborne urediniospores travel along the “Puccinia Pathway,” a route stretching from wheat fields in the southern Gulf Coast regions to northern wheat-growing regions. As the wheat growing season progresses northward, the pathogen also follows the host along this northbound path. Perpetual cycles of urediniospore generation, coupled with wind-born dispersal, is the primary cause of localized wheat stem rust epidemics (11).

In the milder climate of the southern United States, the pathogen can overwinter as uredinia. In less favorable climates, the pathogen can overwinter as telia near the end of the wheat harvesting season and develop into basidiospores ready to infect the alternate host when environmental conditions are favorable. For both spore types, an environment conducive to disease progression is characterized by warm, wet weather. The optimal infection temperature range is 15-24°C (59-75°F) while the optimal disease development range of temperature is 24–30°C (75-86°F). Free water on leaf surfaces for six hours, in addition to light, is critical for infection. The first generation of urediniospores occurs between one and two weeks. Subsequent generations of urediniospores form every 4–7 days. Symptoms become progressively more severe as the growing season continues due to maintained environmental conditions favorable to disease. Although spores can be spread by wind and rain, wind dispersal is the primary mechanism. Splash range of spores is relatively short distance, at less than 0.9 m (2).

Geographic Distribution

This pathogen can be found in Africa and the Middle East. Countries include Eritrea, Ethiopia, Iran, Kenya, Mozambique, South Africa, Sudan, Tanzania, Uganda, Yemen, and Zimbabwe (12).

Management

The primary form of managing this disease has historically been development of stem rust resistant cultivars of wheat. However, durable resistance to Pgt-Ug99 has been elusive due to the rapid genetic shifting of the pathogen (2).

Removal of alternate hosts is still highly recommended in order to curtail sexual reproduction of the pathogen and subsequently slow the rate of new virulent genotype generation (2).

Although fungicides have been approved for use against the stem rust pathogen, efficacy of this chemical method is debatable due to: 1) increased selection for fungicide-resistant Pgt populations; 2) inadequate supplies and efficiency under heavy disease pressure; and 3) potential cost to growers and environment (2).

Diagnostic Procedures

This fungus is an obligate pathogen; it cannot be cultured on media.

Differentiating Wheat Rusts

Macroscopically- Characteristics that differentiate stem rust from leaf rust or stripe rust include the shape and color of pustules and which plant parts are affected.

Stem (Black) Rust (Puccinia graminis f. sp. tritici)

Pustules: Elongated, red-orange

Tissue: All aerial parts of the plant during wheat growing season

Pustules: Elongated, black

Tissue: Stems at late stages in wheat maturity

Leaf (Brown) Rust (Puccinia recondita f. sp. tritici)

Pustules: Round, brown

Tissue: Leaf blades and sheaths

Stripe (Yellow) Rust (Puccinia striiformis f. sp. tritici)

Pustules: Round, yellow, aggregate to form straight lines

Tissue: Leaf blades (1)

Microscopically- Key characteristics that distinguish stem rust from leaf rust or stripe rust include fresh urediniospore shape and protoplasm behavior when mounted in 36.5% HCl.

Stem (Black) Rust (Puccinia graminis f. sp. tritici)

Urediniospores are globose. In 36.5% HCl, the protoplasm forms many small aggregates.

Leaf (Brown) Rust (Puccinia recondita f. sp. tritici)

Urediniospores are globose. In 36.5% HCl, the protoplasm forms one large aggregate.

Stripe (Yellow) Rust (Puccinia striiformis f. sp. tritici)

Urediniospores are elongated. In 36.5% HCl, the protoplasm forms one large aggregate in the majority of spores; the remainder have protoplasm formation into many small aggregates (15).

Resources and References

1. ARS-USDA. Cereal Disease Lab. Identifying Rust Diseases of Wheat and Barley. Online, www.ars.usda.gov/SP2UserFiles/ad_hoc/36400500Cerealrusts/Rust_Diseases_National.pdf Last Modified: 02/12/2010

2. ARS-USDA. Cereal Disease Lab. Recovery Plan for Stem Rust of Wheat caused by Puccinia graminis f. sp. tritici Ug99 (race TTKSK) and its derivatives. Online, http://www.ars.usda.gov/sp2UserFiles/Place/00000000/opmp/Wheat%20Stem%20Rust%20Ug99%20101016.pdf Last Modified: 3/31/2010

3. Brown, J.K.M. and M.S. Hovmøller. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297: 537-541.

4. Expert Panel. 2005. Sounding the alarm on global stem rust: An assessment of race Ug99 in Kenya and Ethiopia and the potential for impact on neighboring regions and beyond. Expert Panel on the Stem Rust Outbreak in Eastern Africa, CIMMYT, Mexico.

5. Hodson, D.P., J. Grønbech-Hansen, P. Lassen, Y. Alemayehu, J. Arista, K. Sonder, P. Kosina, P. Moncada, K. Nazari, R.F. Park, Z.A. Pretorius, L.J. Szabo, T. Fetch and Y. Jin. 2012. Tracking the wheat rust pathogens. Proceedings Borlaug Global Rust Initiative 2012 Technical Workshop, China, pp. 11-22.

6. http://www.ars.usda.gov/ug99/

7. http://www.wheatrust.cornell.edu/index.html

8. Pretorius, Z.A., R.P. Singh, W.W. Wagoire, and T.S. Payne. 2000. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Disease 84: 203.

9. Roelfs, A.P. 1982. Effects of barberry eradication on stem rust in the United States. Plant Disease 66: 177-181.

10. Roelfs, A.P. and J.W. Martens. 1988. An International System of Nomenclature for Puccinia graminis f. sp. tritici. Phytopathology 78: 526 – 533.

11. Schumann, G.L., and K.L. Leonard. 2000. Stem rust of wheat (black rust). The Plant Health Instructor Online, DOI: 10.1094/PHI-I-2000-0721-01.

12. Singh, R.P., D.P. Hodson, J. Huerta-Espino, Y. Jin, S. Bhavani, P. Njau, S. Herrera-Foessel, P. K. Singh, S. Singh, and V. Govindan. 2011. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annual Review of Phytopathology 49: 465-81.

13. Stakman, E.C. 1954. Observational post: Rust, a persistent threat to wheat. Journal of Agricultural and Food Chemistry 2: 748.

14. Tsilo, T.J., Yue J., and J.A. Anderson. 2010. Identification of Flanking Markers for the Stem Rust Resistance Gene in Wheat. Crop Science 50: 1967-1970.

15. Wang, Yang. 2009. A Simple Diagnostic Technique for Identification of Three Wheat Rust Fungi. National Plant Diagnostic Network News 4: 3- 4.

Acknowledgements

• National Institute of Food and Agriculture, U.S. Department of Agriculture, under Agreement No. 2011-41530-30708 as part of "Diagnostic Image Series Development for Supporting IPM in the Southern Region" (USDA-NIFA-RIPM-003351)