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Adult plant resistance QTL identified using the QSM DH lines grown in a 2008 field trial in Njoro, Kenya.
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Stem rust (Puccinia graminis f. sp. tritici; Pgt) is a devastating fungal disease of wheat and barley. Pgt race TTKSK (isolate Ug99) is a serious threat to these Triticeae grain crops because resistance is rare. In barley, the complex Rpg-TTKSK locus on chromosome 5H is presently the only known source of qualitative resistance to this aggressive Pg...
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Barley genotypes Hor 1428, Hor 2926, Hor 3209, BBA 2890, Abyssinian 14, Grannelose Zweizeilige, and Stauffers Obersulzer are resistant to all races of Puccinia striiformis f. sp. hordei so far detected in the U.S.A. Heils Franken, Cambrinus, Astrix, Emir, Hiproly, Varunda, Trumpf,Mazurka, Bigo, BBA 2890, and I 5 are resistant to some races and susc...
Powdery mildew pathogens colonize over 9,500 plant species, causing critical yield loss. The Ascomycete fungus, Blumeria graminis f. sp. hordei (Bgh), causes powdery mildew disease in barley (Hordeum vulgare L.). Successful infection begins with penetration of host epidermal cells, culminating in haustorial feeding structures, facilitating delivery...
Citations
... Of the few eQTL studies that have mapped transcriptional responses to disease, only a fraction of these studies compared eQTLs mapped in disease versus non-disease conditions in plant systems. Moscou et al. (2011), using microarrays to assay transcripts in barley following both inoculations with Puccinia graminis and mock inoculation, had findings that differed from this study, with similar numbers of eQTLs mapped in both mock and inoculated samples and the majority classified as cis. Here, the differences in the number of eQTL mapped between treatments, the lack of concordance of the hotspots between the mock and inoculated treatments, the correspondence with phQTLs, and the functional enrichment of genes within hotspots together suggest that the changes in transcription are due to infection by P. sojae through a coordinated transcriptional response of multiple plant defense mechanisms. ...
Expression of quantitative disease resistance in many host–pathogen systems is controlled by genes at multiple loci, each contributing a small effect to the overall response. We used a systems genomics approach to study the molecular underpinnings of quantitative disease resistance in the soybean-Phytophthora sojae pathosystem, incorporating expression quantitative trait loci (eQTL) mapping and gene co-expression network analysis to identify the genes putatively regulating transcriptional changes in response to inoculation. These findings were compared to previously mapped phenotypic (phQTL) to identify the molecular mechanisms contributing to the expression of this resistance. A subset of 93 recombinant inbred lines (RILs) from a Conrad × Sloan population were inoculated with P. sojae isolate 1.S.1.1 using the tray-test method; RNA was extracted, sequenced, and the normalized read counts were genetically mapped from tissue collected at the inoculation site 24 h after inoculation from both mock and inoculated samples. In total, more than 100,000 eQTLs were mapped. There was a switch from predominantly cis-eQTLs in the mock treatment to an almost entirely nonoverlapping set of predominantly trans-eQTLs in the inoculated treatment, where greater than 100-fold more eQTLs were mapped relative to mock, indicating vast transcriptional reprogramming due to P. sojae infection occurred. The eQTLs were organized into 36 hotspots, with the four largest hotspots from the inoculated treatment corresponding to more than 70% of the eQTLs, each enriched for genes within plant–pathogen interaction pathways. Genetic regulation of trans-eQTLs in response to the pathogen was predicted to occur through transcription factors and signaling molecules involved in plant–pathogen interactions, plant hormone signal transduction, and MAPK pathways. Network analysis identified three co-expression modules that were correlated with susceptibility to P. sojae and associated with three eQTL hotspots. Among the eQTLs co-localized with phQTLs, two cis-eQTLs with putative functions in the regulation of root architecture or jasmonic acid, as well as the putative master regulators of an eQTL hotspot nearby a phQTL, represent candidates potentially underpinning the molecular control of these phQTLs for resistance.
... Thus, it remains unclear if the changes noted in large-effect co-transcriptome studies are transposable to a system in which numerous signals are varying in both the host and pathogen. To decipher the influence of regulatory variation in stem rust resistance, a host-focused transcriptome study on barley (Hordeum vulgare) showed that host transcripts are largely controlled by a plethora of quantitative moderate effect loci involving a diversity of mechanisms and pathways (Druka et al. 2008;Moscou et al. 2011). A transcriptomic study on strains of the wheat pathogen Zymoseptoria tritici, differing in virulence, found conserved and nonconserved gene expression patterns in genes involved in virulence, suggesting that heterogeneity in pathogen transcriptome contributes to quantitative virulence (Palma-Guerrero et al. 2017). ...
Bidirectional flow of information shapes the outcome of the host-pathogen interactions and depends on the genetics of each organism. Recent work has begun to use co-transcriptomic studies to shed light on this bidirectional flow, but it is unclear how plastic the co-transcriptome is in response to genetic variation in both the host and pathogen. To study co-transcriptome plasticity, we conducted transcriptomics using natural genetic variation in the pathogen, Botrytis cinerea, and large effect genetic variation abolishing defense signaling pathways within the host, Arabidopsis thaliana. We show that genetic variation in the pathogen has a greater influence on the co-transcriptome than mutations that abolish defense signaling pathways in the host. Genome wide association mapping using the pathogens genetic variation and both organisms’ transcriptomes allowed an assessment of how the pathogen modulates plasticity in response to the host. This showed that the differences in both organism’s responses were linked to trans-eQTL hotspots within the pathogen’s genome. These hotspots control gene sets in either the host or pathogen and show differential allele sensitivity to the hosts genetic variation rather than qualitative host specificity. Interestingly, nearly all the trans-eQTL hotspots were unique to the host or pathogen transcriptomes. In this system of differential plasticity, the pathogen mediates the shift in the co-transcriptome more than the host.
... For each biosample, total RNA was isolated from cryoground tissue by buffered thiocyanate salts and phenolchloroform extractions as previously described (Moscou, Lauter, Steffenson, & Wise, 2011). mRNA purification, library construction, and barcoding steps were performed by the DNA Facility staff at Iowa State University with Illumina TruSeq Kits (Illumina, San Diego, CA). ...
The extraordinarily long stigmatic silks of corn (Zea mays L.) are critical for grain production but the biology of their growth and emergence from husk leaves has remained underexplored. Accordingly, gene expression was assayed for inbreds ‘B73’ and ‘Mo17’ across five contiguous silk sections. Half of the maize genes (∼20,000) are expressed in silks, mostly in spatiotemporally dynamic patterns. In particular, emergence triggers strong differential expression of ∼1,500 genes collectively enriched for gene ontology terms associated with abiotic and biotic stress responses, hormone signaling, cell–cell communication, and defense metabolism. Further, a meta‐analysis of published maize transcriptomic studies on seedling stress showed that silk emergence elicits an upregulated transcriptomic response that overlaps strongly with both abiotic and biotic stress responses. Although the two inbreds revealed similar silk transcriptomic programs overall, genotypic expression differences were observed for 5,643 B73–Mo17 syntenic gene pairs and collectively account for >50% of genome‐wide expression variance. Coexpression clusters, including many based on genotypic divergence, were identified and interrogated via ontology‐term enrichment analyses to generate biological hypotheses for future research. Ultimately, dissecting how gene expression changes along the length of silks and between husk‐encased and emerged states offers testable models for silk development and plant response to environmental stresses.
... This demonstrates that 1) genes associated with the early steps of QDR belong to diverse functional classes, in line with the idea that QDR does not involve simply perception of pathogenic molecules (3); 2) the major functional class is related to metabolic processes; and 3) these genes are mostly distinct from PTI and ETI gene networks already described (12,18,31) (SI Appendix, Fig. S7). A similar observation was reported by comparative transcriptomic analyses on barley in response to stem rust, indicating that 25% of barley genes are altered in response to infection, but only very few of these genes are controlled by the R locus (37). In line with these observations, we found a small proportion (6%) of genes putatively associated with response to hormones, none of them related to defense phytohormones such as ethylene (ET), jasmonate (JA), or salicylic acid (SA) (31,38). ...
Significance
Molecular studies of plant immune responses have mainly focused on qualitative resistance, a form of immunity determined by a few large effect genes. In contrast, very limited information exists about quantitative disease resistance (QDR), although it is extensively observed in wild and crop species. We used systems biology approaches to describe this form of immunity in Arabidopsis thaliana . On the basis of gene regulation studies and search for protein–protein interactions, we report the reconstruction of a highly interconnected and distributed network, organized in five modules with differential robustness to genetic mutations. These studies revealed key functions of QDR, mainly distinct from those previously identified for plant immunity, and shed some light on the complexity of this plant immune response.
... Whereas resistance (R) genes mediating complete disease resistance all belong to the nucleotide-binding site leucine-rich repeat (NLR) family, genes underlying QDR discovered to date span a broad range of molecular functions (Poland et al., 2011;Roux et al., 2014;Corwin and Kliebenstein, 2017). Molecular function of genes associated with QDR include for instance transporters (Krattinger et al., 2009), kinases (Fu et al., 2009;Huard-Chauveau et al., 2013), peptidases (Poland et al., 2011;Badet et al., 2017b), or actin-related proteins (Moscou et al., 2011). NLRs (Debieu et al., 2015;Lee et al., 2016) and signalling components typically associated with R-mediated resistance (Iakovidis et al., 2016) can also mediate QDR, illustrating the tight integration of QDR and R-mediated immunity components. ...
The broad host range necrotrophic fungus Sclerotinia sclerotiorum is a devastating pathogen of many oil and vegetable crops. Plant genes conferring complete resistance against S. sclerotiorum have not been reported. Instead, plant populations challenged by S. sclerotiorum exhibit a continuum of partial resistance designated as quantitative disease resistance (QDR). Because of their complex interplay and their small phenotypic effect, the functional characterization of QDR genes remains limited. How broad host range necrotrophic fungi manipulate plant programmed cell death is for instance largely unknown. Here, we designed a time‐resolved automated disease phenotyping pipeline enabling high‐ throughput disease lesion measurement with high resolution, low footprint at low cost. We could accurately recover contrasted disease responses in several pathosystems using this system. We used our phenotyping pipeline to assess the kinetics of disease symptoms caused by seven S. sclerotiorum isolates on six A. thaliana natural accessions with unprecedented resolution. Large effect polymorphisms common to the most resistant A. thaliana accessions identified highly divergent alleles of the nucleotide‐binding site leucine‐rich repeat gene LAZ5 in the resistant accessions Rubenzhnoe and Lip‐0. We show that impaired LAZ5 expression in laz5.1 mutant lines and in A. thaliana Rub natural accession correlate with enhanced QDR to S. sclerotiorum. These findings illustrate the value of time‐resolved image‐based phenotyping for unravelling the genetic bases of complex traits such as QDR. Our results suggest that S. sclerotiorum manipulates plant sphingolipid pathways guarded by LAZ5 to trigger programmed cell death and cause disease.
... This marker is ;0.7 Mb upstream from the rgp4/Rpg5 resistance complex (640765916 Mb) (Mascher et al. 2017). The proximity of the marker associated with resistance to the rpg4/Rpg5 complex suggests that we were able to detect the effect of this complex in our Cycle II barley population, as was also found in other previous studies (Case et al. 2018b;Hernandez et al. 2019;Moscou et al. 2011;Steffenson et al. 2009). At the adult stage, two QTLs were associated with resistance in MN18. ...
... Case et al. (2018b) reported the same marker associated with resistance at this growth stage. Moscou et al. (2011), using a biparental population from the cross Q21861 × SM89010, detected a resistance QTL on 5H at 74.9 cM, supporting the notion that this region on 5H is important for stem rust resistance at the adult stage. ...
Stripe rust (incited by Puccinia striiformis f. sp. hordei) and stem rust (incited by Puccinia graminis f. sp. tritici) are two of the most important diseases affecting barley. Building on prior work involving the introgression of the resistance genes rpg4/Rpg5 into diverse genetic backgrounds and the discovery of additional QTLs for stem rust resistance, we generated an array of germplasm in which we mapped resistance to stripe rust and stem rust. Stem rust races TTKSK and QCCJB were used for resistance mapping at the seedling and adult plant stages, respectively. Resistance to stripe rust, at the adult plant stage, was determined by QTLs on chromosomes 1H, 4H, and 5H that were previously reported in the literature. The rpg4/Rpg5 complex was validated as a source of resistance to stem rust at the seedling stage. Some parental germplasm, selected as potentially resistant to stem rust or susceptible but having other positive attributes, showed resistance at the seedling stage, which appears to be allelic to rpg4/Rpg5. The rpg4/Rpg5 complex, and this new allele, were not sufficient for adult plant resistance to stem rust in one environment. A QTL on 5H, distinct from Rpg5 and a previously reported resistance QTL, was required for resistance at the adult plant stage in all environments. This QTL is coincident with the QTL for stripe rust resistance. Germplasm with mapped genes/QTLs conferring resistance to stripe and stem rust was identified and is available as a resource to the research and breeding communities.
... The barley research community has developed a number of genome marker-based systems, initially using sequences from expressed sequence tags (ESTs) generated by the international consortium using regional donor cultivars of barley. The first comprehensive polymorphism detection system was Affymetrix GeneChip Barley1 (Close et al., 2004;Luo et al., 2007;Chen et al., 2010;Moscou et al., 2011), which uses hybridization probe sequences chosen to avoid the polymorphic regions of transcripts, and enables the simultaneous detection of gene expression and polymorphisms. Transcript sequence polymorphisms were used to develop the Illumina GoldenGate Assay SNP detection system, which included 2,943 mapped SNPs (Close et al., 2009), and other high-density marker systems were also created for the Illumina iSelect platform (Bayer et al., 2017). ...
Marker-assisted selection of crop plants requires DNA markers that can distinguish between the closely related strains often used in breeding. The availability of reference genome sequence facilitates the generation of markers, by elucidating the genomic positions of new markers as well as of their neighboring sequences. In 2017, a high quality genome sequence was released for the six-row barley (Hordeum vulgare) cultivar Morex. Here, we developed a de novo RNA-Seq-based genotyping procedure for barley strains used in Japanese breeding programs. Using RNA samples from the seedling shoot, seedling root, and immature flower spike, we mapped next-generation sequencing reads onto the transcribed regions, which correspond to ∼590 Mb of the whole ∼4.8-Gbp reference genome sequence. Using 150 samples from 108 strains, we detected 181,567 SNPs and 45,135 indels located in the 28,939 transcribed regions distributed throughout the Morex genome. We evaluated the quality of this polymorphism detection approach by analyzing 387 RNA-Seq-derived SNPs using amplicon sequencing. More than 85% of the RNA-Seq SNPs were validated using the highly redundant reads from the amplicon sequencing, although half of the indels and multiple-allele loci showed different polymorphisms between the platforms. These results demonstrated that our RNA-Seq-based de novo polymorphism detection system generates genome-wide markers, even in the closely related barley genotypes used in breeding programs.
... Moreover, there are few sources of resistance to TTKSK: of 1,924 barley accessions screened for seedling resistance, <5% were highly or moderately resistant . Although several QTLs have been reported that confer varying degrees of resistance to TTKSK, only rpg4/ Rpg5 provides high levels of resistance at the seedling and adult stages (Mamo et al. 2015;Moscou et al. 2011;Steffenson et al. 2009). Jin et al. (1994b) first reported line Q21861, originally from the International Center for Agricultural Research in the Dry Areas (ICARDA)/CIMMYT program in Mexico, as a source of resistance to race QCC (now designed QCCJB) of stem rust. ...
... Mamo et al. (2015) reported a seedling-stage resistance QTL at 88.8 cM (;561 Mb) as determined using the same consensus mapping process. Moscou et al. (2011), using a biparental doubled haploid population, reported an adult plant resistance QTL at 74.9 cM. Case et al. (2018a), using a Fig. 2. Coefficients of infection (CIs) in the TTKSK Cycle I population classified according to multilocus haplotype at Rpg5 and minor quantitative trait locus regions on chromosomes 5H and 7H; + and _ refer to resistance and susceptibility alleles, respectively. ...
Stem rust (incited by Puccinia graminis f. sp. tritici) is a devastating disease of wheat and barley in many production areas. The widely virulent African P. graminis f. sp. tritici race TTKSK is of particular concern, because most cultivars are susceptible. To prepare for the possible arrival of race TTKSK in North America, we crossed a range of barley germplasm-representing different growth habits and end uses-with donors of stem rust resistance genes Rpg1 and rpg4/Rpg5. The former confers resistance to prevalent races of P. graminis f. sp. tritici in North America, and the latter confers resistance to TTKSK and other closely related races from Africa. We produced doubled haploids from these crosses and determined their allele type at the Rpg loci and haplotype at 7,864 single-nucleotide polymorphism loci. The doubled haploids were phenotyped for TTKSK resistance at the seedling stage. Integration of genotype and phenotype data revealed that (i) Rpg1 was not associated with TTKSK resistance, (ii) rpg4/Rpg5 was necessary but was not sufficient for resistance, and (iii) specific haplotypes at two quantitative trait loci were required for rpg4/Rpg5 to confer resistance to TTKSK. To confirm whether lines found resistant to TTKSK at the seedling resistance were also resistant at the adult plant stage, a subset of doubled haploids was evaluated in Kenya. Additionally, adult plant resistance to leaf rust and stripe rust (incited by Puccinia hordei and Puccinia striiformis f. sp. hordei, respectively) was also assessed on the doubled haploids in field trials at three locations in the United States over a 2-year period. Doubled haploids were identified with adult plant resistance to all three rusts, and this germplasm is available to the research and breeding communities.
... One of the major tools of disease resistance functional genomics will be RNASeqbased transcriptome profiling. Comparison of transcriptome profiles from barley lines after pathogen infection will give insights into gene expression differences involved in resistance and tolerance (Moscou et al., 2011). Expression QTLs (eQTLs), as identified by transcriptome profiling, will be useful in connecting phenotypic variation to genotypic diversity, thus leading to a hypothetical regulatory network based on the location of eQTLs and phenotypic QTLs, for example, eQTL analysis of partial resistance to P. hordei in barley (Chen et al., 2010). ...
... Several authors have demonstrated that BPM is highly efficient in identifying known and novel QTLs associated with resistance to P. hordei (Hickey et al. 2011;Singh et al. 2015Singh et al. , 2017Ziems et al. 2017), P. graminis f. sp. tritici (Moscou et al. 2011), and P. striiformis f. sp. hordei (Esvelt Klos et al. 2016). ...
We assembled an international barley panel comprising 282 entries from 26 countries with various levels of field resistance to leaf rust caused by Puccinia hordei. The panel was screened for leaf rust response with an array of pathotypes at the seedling stage, and at the adult plant stage in multiple environments (2013-2015) in Aus-tralia and Uruguay, and genotyped using > 13 K polymor-phic DArT-Seq markers. Multipathotype testing in the greenhouse postulated the presence of seedling resistance genes Rph1, Rph2, Rph3, Rph4, Rph7, Rph9.am, Rph12, Rph14, Rph15, Rph19, and Rph25. Genome-wide association studies (GWAS) based on field data identified 13 QTLs significantly associated with DArT-Seq markers on chromosomes 2H (Rph_G_Q1, Rph_G_Q2, Rph_G_Q3, and Rph_G_Q4), 4H (Rph_G_Q5), 5H (Rph_G_Q6, Rph_G_Q7, Rph_G_Q8), 6H (Rph_G_Q9 and Rph_G_Q10), and 7H (Rph_G_Q11, Rph_G_Q12, and Rph_G_Q13). Three QTLs (Rph_G_Q3, Rph_G_Q5, and Rph_G_Q6) were detected under all environments, whereas the other ten were variable, being detected in 1-4 environments; Rph_G_Q1 and Rph_G_Q13 being detected only in Uruguay. Among the three QTLs detected under all environments, Rph_G_Q6 on chromosome 5H had the largest effect and corresponded to a region where the cataloged APR gene Rph20 is located. Rph_G_Q3 and Rph_G_Q5 detected on chromosome 2H and 4H aligned with QTLs reported in at least three previous studies. The studies provide useful information towards better understanding of the genetic architecture of seedling and adult plant resistance to leaf rust in diverse global barley germplasm.
