J. A. Kolmer

Wheat leaf rust caused by Puccinia triticina

UNLABELLED Leaf rust, caused by Puccinia triticina, is the most common rust disease of wheat. The fungus is an obligate parasite capable of producing infectious urediniospores as long as infected leaf tissue remains alive. Urediniospores can be wind-disseminated and infect host plants hundreds of kilometres from their source plant, which can result in wheat leaf rust epidemics on a continental scale. This review summarizes current knowledge of the P. triticina/wheat interaction with emphasis on the infection process, molecular aspects of pathogenicity, rust resistance genes in wheat, genetics of the host parasite interaction, and the population biology of P. triticina. TAXONOMY Puccinia triticina Eriks.: kingdom Fungi, phylum Basidiomycota, class Urediniomycetes, order Uredinales, family Pucciniaceae, genus Puccinia. HOST RANGE Telial/uredinial (primary) hosts: common wheat (Triticum aestivum L.), durum wheat (T. turgidum L. var. durum), cultivated emmer wheat (T. dicoccon) and wild emmer wheat (T. dicoccoides), Aegilops speltoides, goatgrass (Ae. cylindrica), and triticale (X Triticosecale). Pycnial/aecial (alternative) hosts: Thalictrum speciosissimum (= T. flavum glaucum) and Isopyrum fumaroides. IDENTIFICATION Leaf rust is characterized by the uredinial stage. Uredinia are up to 1.5 mm in diameter, erumpent, round to ovoid, with orange to brown uredinia that are scattered on both the upper and the lower leaf surfaces of the primary host. Uredinia produce urediniospores that are sub-globoid, average 20 microm in diameter and are orange-brown, with up to eight germ pores scattered in thick, echinulate walls. DISEASE SYMPTOMS Wheat varieties that are fully susceptible have large uredinia without causing chlorosis or necrosis in the host tissues. Resistant wheat varieties are characterized by various responses from small hypersensitive flecks to small to moderate size uredinia that may be surrounded by chlorotic and/or necrotic zones. USEFUL WEBSITE USDA Cereal Disease Laboratory: http://www.ars.usda.gov/mwa/cdl.

Physiologic Specialization of Puccinia triticina on Wheat in the United States in 2005

Collections of Puccinia triticina were obtained from rust-infected wheat leaves by cooperators throughout the United States and from surveys of wheat fields and nurseries in the Great Plains, Ohio River Valley, southeast, California, and Washington State, in order to determine the virulence of the wheat leaf rust population in 2005. Single uredinial isolates (797 in total) were derived from the collections and tested for virulence phenotype on lines of Thatcher wheat that are near-isogenic for leaf rust resistance genes Lr1, Lr2a, Lr2c, Lr3a, Lr9, Lr16, Lr24, Lr26, Lr3ka, Lr11, Lr17a, Lr30, LrB, Lr10, Lr14a, Lr18, Lr21, Lr28, and winter wheat lines with genes Lr41 and Lr42. In the United States in 2005, 72 virulence phenotypes of P. triticina were found. Virulence phenotype TDBGH, selected by virulence to resistance gene Lr24, was the most common phenotype in the United States, and was found throughout the Great Plains region. Virulence phenotype MCDSB with virulence to Lr17a and Lr26 was the second most common phenotype and was found widely in the wheat growing regions of the United States. Virulence phenotype MFPSC, which has virulence to Lr17a, Lr24, and Lr26, was the third most common phenotype, and was found in the Ohio Valley region, the Great Plains, and California. The highly diverse population of P. triticina in the United States will continue to present a challenge for the development of wheat cultivars with effective durable resistance to leaf rust.

Lr34-Mediated Leaf Rust Resistance in Wheat: Transcript Profiling Reveals a High Energetic Demand Supported by Transient Recruitment of Multiple Metabolic Pathways

The wheat gene Lr34 confers partial resistance to all races of Puccinia triticina, the causal agent of wheat leaf rust. However, the biological basis for the exceptional durability of Lr34 is unclear. We used the Affymetrix GeneChip Wheat Genome Array to compare transcriptional changes of near-isogenic lines of Thatcher wheat in a compatible interaction, an incompatible interaction conferred by the resistance gene Lr1, and the race-nonspecific response conditioned by Lr34 3 and 7 days postinoculation (dpi) with P. triticina. No differentially expressed genes were detected in Lr1 plants at either timepoint whereas, in the compatible Thatcher interaction, differentially expressed genes were detected only at 7 dpi. In contrast, differentially expressed genes were identified at both timepoints in P. triticina-inoculated Lr34 plants. At 3 dpi, upregulated genes associated with Lr34-mediated resistance encoded various defense and stress-related proteins, secondary metabolism enzymes, and transcriptional regulation and cellular-signaling proteins. Further, coordinated upregulation of key genes in several metabolic pathways that can contribute to increased carbon flux through the tricarboxylic cycle was detected. This indicates that Lr34-mediated resistance imposes a high energetic demand that leads to the induction of multiple metabolic responses to support cellular energy requirements. These metabolic responses were not sustained through 7 dpi, and may explain why Lr34 fails to inhibit the pathogen fully but does increase the latent period.

Molecular characterization of durum and common wheat recombinant lines carrying leaf rust resistance (Lr19) and yellow pigment (Y) genes from Lophopyrum ponticum

Chromosome 7E from Lophopyrum ponticum carries a valuable leaf rust resistant gene designated Lr19. This gene has not been widely used in common wheat breeding because of linkage with the yellow pigment gene Y. This gene tints flour yellow, reducing its appeal in bread making. However, a high level of yellow pigment is desirable in durum wheat breeding. We produced 97 recombinant chromosomes between L. ponticum transfer 7D.7E#1 and its wheat homoeologues, using the ph1b mutation that promotes homoeologous pairing. We characterized a subset of 37 of these lines with 11 molecular markers and evaluated their resistance to leaf rust and the abundance of yellow pigment. The Lr19 gene was mapped between loci Xwg420 and Xmwg2062, whereas Y was mapped distal to Xpsr687, the most distal marker on the long arm of chromosome 7. A short terminal 7EL segment translocated to 7A, including Lr19 and Y (line 1-23), has been transferred to durum wheat by backcrossing. The presence of this alien segment significantly increased the abundance of yellow pigment. The Lr19 also conferred resistance to a new durum leaf rust race from California and Mexico that is virulent on most durum wheat cultivars. The new durum lines with the recombinant 7E segment will be useful parents to increase yellow pigment and leaf rust resistance in durum wheat breeding programs. For the common wheat breeding programs, we selected the recombinant line 1-96, which has an interstitial 7E segment carrying Lr19 but not Y. This recombinant line can be used to improve leaf rust resistance without affecting flour color. The 7EL/7DL 1-96 recombinant chromosome did not show the meiotic self-elimination previously reported for a 7EL/7BL translocation.

Identification of novel QTLs for seedling and adult plant leaf rust resistance in a wheat doubled haploid population

Pyramiding of genes that confer partial resistance is a method for developing wheat (Triticum aestivum L.) cultivars with durable resistance to leaf rust caused by Puccinia triticina. In this research, a doubled haploid population derived from the cross between the synthetic hexaploid wheat (SHW) (×Aegilotriticum spp.) line TA4152-60 and the North Dakota breeding line ND495 was used for identifying genes conferring partial resistance to leaf rust in both the adult plant and seedling stages. Five QTLs located on chromosome arms 3AL, 3BL, 4DL, 5BL and 6BL were associated with adult plant resistance with the latter four representing novel leaf rust resistance QTLs. Resistance effects of the 4DL QTL were contributed by ND495 and the effects of the other QTLs were contributed by the SHW line. The QTL on chromosome arm 3AL had large effects and also conferred seedling resistance to leaf rust races MJBJ, TDBG and MFPS. The other major QTL, which was on chromosome arm 3BL, conferred seedling resistance to race MFPS and was involved in a significant interaction with a locus on chromosome arm 5DS. The QTLs and the associated molecular markers identified in this research can be used to develop wheat cultivars with potentially durable leaf rust resistance.

Genome Wide Association Study of Seedling and Adult Plant Leaf Rust Resistance in Elite Spring Wheat Breeding Lines

Leaf rust is an important disease, threatening wheat production annually. Identification of resistance genes or QTLs for effective field resistance could greatly enhance our ability to breed durably resistant varieties. We applied a genome wide association study (GWAS) approach to identify resistance genes or QTLs in 338 spring wheat breeding lines from public and private sectors that were predominately developed in the Americas. A total of 46 QTLs were identified for field and seedling traits and approximately 20–30 confer field resistance in varying degrees. The 10 QTLs accounting for the most variation in field resistance explained 26–30% of the total variation (depending on traits: percent severity, coefficient of infection or response type). Similarly, the 10 QTLs accounting for most of the variation in seedling resistance to different races explained 24–34% of the variation, after correcting for population structure. Two potentially novel QTLs (QLr.umn-1AL, QLr.umn-4AS) were identified. Identification of novel genes or QTLs and validation of previously identified genes or QTLs for seedling and especially adult plant resistance will enhance understanding of leaf rust resistance and assist breeding for resistant wheat varieties. We also developed computer programs to automate field and seedling rust phenotype data conversions. This is the first GWAS study of leaf rust resistance in elite wheat breeding lines genotyped with high density 90K SNP arrays.

The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus.

We identify the wheat stem rust resistance gene Sr50 (using physical mapping, mutation and complementation) as homologous to barley Mla, encoding a coiled-coil nucleotide-binding leucine-rich repeat (CC-NB-LRR) protein. We show that Sr50 confers a unique resistance specificity different from Sr31 and other genes on rye chromosome 1RS, and is effective against the broadly virulent Ug99 race lineage. Extensive haplotype diversity at the rye Sr50 locus holds promise for mining effective resistance genes.

Using transcription of six Puccinia triticina races to identify the effective secretome during infection of wheat

Wheat leaf rust, caused by the basidiomycete Puccinia triticina, can cause yield losses of up to 20% in wheat producing regions. During infection, the fungus forms haustoria that secrete proteins into the plant cell and effect changes in plant transcription, metabolism, and defense. It is hypothesized that new races emerge as a result of overcoming plant resistance via changes in the secreted effector proteins. To understand gene expression during infection and find genetic differences associated with races, RNA from wheat leaves infected with six different rust races, at 6 days post inoculation, was sequenced using Illumina. As P. triticina is an obligate biotroph, RNA from both the host and fungi were present and separated by alignment to the P. triticina genome and a wheat EST reference. A total of 222,571 rust contigs were assembled from 165 million reads. An examination of the resulting contigs revealed 532 predicted secreted proteins among the transcripts. Of these, 456 were found in all races. Fifteen genes were found with amino acid changes, corresponding to putative avirulence effectors potentially recognized by 11 different leaf rust resistance (Lr) genes. Twelve of the potential avirulence effectors have no homology to known genes. One gene had significant similarity to cerato-platanin, a known fungal elicitor, and another showed similarity to fungal tyrosinase, an enzyme involved in melanin synthesis. Temporal expression profiles were developed for these genes by qRT-PCR and show that the genes expression patterns were consistent between races from infection initiation to just prior to spore eruption.

Physiologic Specialization of Puccinia triticina on Wheat in the United States in 2003

Collections of Puccinia triticina were obtained from rust infected wheat leaves by cooperators throughout the United States and from surveys of wheat fields and nurseries in the Great Plains, Ohio Valley, Southeast, California, and the Pacific Northwest, in order to determine the virulence of the wheat leaf rust fungus in 2003. Single uredinial isolates (580 in total) were derived from the wheat leaf rust collections and tested for virulence phenotype on lines of Thatcher wheat that are near-isogenic for leaf rust resistance genes Lr1, Lr2a, Lr2c, Lr3, Lr9, Lr16, Lr24, Lr26, Lr3ka, Lr11, Lr17, Lr30, LrB, Lr10, Lr14a, and Lr18. In the United States in 2003, 52 virulence phenotypes of P. triticina were found. Virulence phenotype MBDS, which has been selected by virulence to resistance gene Lr17, was the most common phenotype in the United States. MBDS was found in the Southeast, Great Plains, the Ohio Valley, and California. Virulence phenotype THBJ, which has been selected by virulence to genes Lr16 and Lr26, was the second most common phenotype, and was found in the southern and northern central Great Plains region. Phenotype MCDS, which has been selected by virulence to genes Lr17 and Lr26, was the third most common phenotype and occurred in the same regions as MBDS. The use of wheat cultivars with leaf rust seedling resistance genes has selected leaf rust phenotypes with virulence to genes Lr9, Lr16, Lr17, Lr24, and Lr26. The population of P. triticina in the United States is highly diverse for virulence phenotypes, which will continue to present a challenge for the development of wheat cultivars with effective durable resistance.

Physiologic Specialization of Puccinia triticina on Wheat in the United States in 2007

In 2007, leaf rust of wheat was severe throughout the Great Plains region of North America. Yield losses in wheat due to leaf rust were estimated to be 14% in Kansas. Collections of Puccinia triticina were obtained from rust-infected leaves provided by cooperators throughout the United States and from surveys of wheat fields and nurseries in the Great Plains, Ohio River Valley, southeast, California, and Washington State in order to determine the virulence of the wheat leaf rust population in 2007. Single uredinial isolates (868 in total) were derived from the collections and tested for virulence phenotype on lines of Thatcher wheat that are near-isogenic for leaf rust resistance genes Lr1, Lr2a, Lr2c, Lr3a, Lr9, Lr16, Lr24, Lr26, Lr3ka, Lr11, Lr17a, Lr30, LrB, Lr10, Lr14a, Lr18, Lr21, and Lr28, and on winter wheat lines with genes Lr41 and Lr42. Fifty-two virulence phenotypes were found. Virulence phenotypes TDBJG, MFPSC, and TDBJH were among the four most common phenotypes and were all virulent to resistance gene Lr24. These phenotypes were found throughout the Great Plains region. Phenotype MLDSD, with virulence to Lr9, Lr17, and Lr41, was also widely distributed in the Great Plains. In the soft red winter wheat region of the southeastern states, phenotypes TCRKG, with virulence to genes Lr11, Lr26, and Lr18, and MFGJH, with virulence to Lr24, Lr26, and Lr11, were among the common phenotypes. Virulence phenotypes with virulence to Lr16 were most frequent in the spring wheat region of the northern Great Plains. Virulence phenotypes with virulence to Lr11, Lr18, and Lr26 were most common in the soft red winter areas of the southeastern states and Ohio Valley. Virulence to Lr21 was not found in any of the tested isolates.