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The concept of durable resistance was introduced by Dr Roy Johnson about 40 years ago, following a breakdown in the slow rusting or adult plant resistance of several English winter wheats to stripe rust, including Joss Cambier, and continued effectiveness of resistance in several other cultivars including Cappelle Desprez and Hybrid de Bersee. The resistance in the latter was referred to as durable, and durable resistance defined as “resistance that remains effective when a cultivar is grown widely in environments favouring disease development”. Durable resistance is a descriptive term; it does not provide any explanation of the causes underlying long lasting resistance. It does, however, contain two conceptual elements, one being that there may be any of several underlying causes for durable resistance and the other that resistance that has remained effective for a long period of widespread use may not necessarily continue to do so in the future. This paper will discuss the role of durable resistance in achieving sustained control of cereal rust diseases. In view of the complexity of host : pathogen interactions, genetic diversity must be seen as a key ingredient in large scale sustained control of plant diseases. It has been argued that even where specific or major resistance genes are used, genetic diversity can be used as insurance against lack of durability and hence as a means of reducing genetic vulnerability. Above all, responsible use of resistance genes depends upon an understanding of the resistance genes present in cultivars and breeding populations, and monitoring pathogen populations with respect to deployed resistances, are crucial in ensuring that the genetic bases of resistances are not narrowed.
The identification of R-genes using traditional map-based approaches is a long, laborious process, not to mention the time required for subsequent development of cultivars incorporating the new resistances. Breeders seek to reduce the length of breeding cycles, and researchers require new tools to accelerate discovery and understanding of mechanisms associated with durable resistance, especially adult plant resistance (APR). A new method for rapid generation advancement, known as ‘speed breeding’, significantly reduces the length of breeding cycles, provide increased recombination during line development and enable selection in early generations. The speed breeding protocol uses controlled temperature regimes and 24h light to accelerate plant growth and development. Phenotyping methods adapted for use in the speed breeding system permit year-round evaluation of APR to rust pathogens within 5 weeks from time of sowing. RNA sequencing (RNA-Seq) technology has revolutionized gene expression profiling in plants. We previously used RNAseq to identify novel transcripts and miRNAs associated with seedling resistance (Lr28) leading to identification of transcription factors and miRNA families (e.g. miR36, miR37 and miR39) involved in signalling and defense response (Kumar et al. J. Nuc. Acids 2014:570176). In this study we report the application of speed breeding and RNAseq technologies for the purpose of rapidly identifying transcripts and miRNA associated with APR. Wheat landraces harbouring novel sources of resistance were grown under speed breeding conditions and sampled for RNA at key growth stages, before and after inoculation, which enabled discovery of differentially expressed miRNAs. Our next steps are aimed at validating these genetic factors associated with APR in order to better understand the signalling pathways and deliver tools to assist the assembly of robust wheat cultivars for the future.
Stem rust (SR) resistance is required for CIMMYT durum germplasm to keep relevance in Ethiopia, where Ug99 and other Pgt races are a major yield-limiting constraint, and in countries along the possible dissemination paths of these races. Resistance to Ug99 is widespread in most durum germplasm groups when tested in Kenya, but resistance is lost when exposed to Ethiopian races; hence selection at the Debre Zeit site in Ethiopia is essential for durum wheat. Due to difficulties with shuttling segregating populations between Mexico and Ethiopia, we have adopted a strategy involving the identification of resistant/moderately resistant lines at Debre- Zeit, and inter-crossing in Mexico followed by selection for resistance to leaf rust and agronomic type and finally screening for SR reaction in the resulting F6 lines at Debre-Zeit at the same time as they are tested for yield and quality in preliminary yield trials in Mexico. This has generated a significant increase in the proportion of resistant and moderately resistant genotypes within outgoing CIMMYT germplasm, from less than 3% at the onset of the initiative in 2008 to 16% in 2011, and 38% in 2013. SR-resistant germplasm was characterized by similar frequency distributions to other traits in the overall germplasm such as yield potential, drought tolerance and industrial quality parameters. Advances have also been realized using marker-assisted selection (MAS) to introgress Sr22 from bread wheat and to combine it with Sr25, producing advanced lines with 2-gene stacks with confirmed outstanding resistance and superior quality attributes. Since the two genes are closely linked but from different sources bringing them together required a very rare recombination event finally detected via MAS among thousands of plants. They are now essentially inherited together with a very low likelihood of generating recombinant individuals with either gene. The yield potential and stability of these lines are under evaluation in Ethiopia and the best lines are being used in a second round of breeding.
The shortage of stem rust resistance genes effective against the Ug99 group prompted recent efforts to increase the number of resistance genes available to breeders. We are fortunate that many new and/or cytogenetically improved rust resistance genes are now being shared with the global wheat breeding community by their developers. If we are poor stewards of these resources, the new resistance genes will eventually be defeated, and we will waste the efforts and investments that have been made. However, if we are good stewards, we should have enough resistance to achieve sustainable, durable resistance. Stewardship can be defined as the careful and responsible management of something entrusted to one’s care. What should we do to safeguard the new resistance genes? Diversification of resistance is often suggested as a way to reduce the risk of large scale epidemics. Although diversification is generally a good idea, it cannot be at the expense of leaving new genes exposed and vulnerable. A durable combination (pyramid) must be designed so that the component genes protect each other. They should reduce the probability of simultaneous pathogen mutations to virulence and they should avoid stepwise erosion of the pyramid by preventing significant reproduction of any new race that is virulent on component genes. We need pyramids to be immune or nearly immune not only to current races, but to anticipated mutants. This objective should be achievable with three or more major genes or a combination of major and minor genes. Successful gene stewardship will depend on several things. On the technical side, we will need very good markers for each gene. Each breeding program will require strong genotyping support to assemble and then validate pyramids. Most importantly, successful stewardship will require that we organize our user community to cooperate more closely. We will need to decide which genes require special stewardship and which do not. Every user of the stewardship pool resource will need to participate in earnest. It only takes one cultivar with an unprotected gene to give the pathogen a stepping stone to greater virulence. As they say, a chain is only as strong as the weakest link
The Lr34/Yr18 gene has been used in agriculture for more than 100 years. In contrast to many other resistance sources against leaf rust and stripe rust, it has remained effective and no virulence has been reported. This makes Lr34 a unique and highly valuable resource for rust resistance breeding. The pleiotropic nature of the gene conferring partial resistance to different pathogen species, the associated leaf tip necrosis and its durability suggest a molecular mechanism that is different from major gene resistance. This is supported by the molecular nature of Lr34 which was recently found to encode an ABC transporter. Interestingly, all tested wheat lines contain an allele of the Lr34 gene on chromosome 7DS. In its susceptible form, the gene does not confer resistance. The difference between the encoded resistant and susceptible LR34 isoforms consists of only two amino acid changes, whereas the rest of the proteins are identical. These two changes must change the biochemical properties of the resistant LR34 transporter in such a way that the plant becomes resistant. We speculate that there is a slight conformational change in the resistant form of the protein, resulting either in modified specificity or kinetics of the transported molecule, or that the binding properties to an unknown second protein interacting with LR34 are changed, resulting in altered function. While the molecular nature of the molecule(s) transported by the LR34 protein remains unclear, it is likely that a physiological change related to Lr34 activity is at the basis of resistance. We are currently establishing transgenic approaches in heterologous grass species to further investigate the molecular activity of Lr34 and to better understand a physiological mechanisms resulting in disease resistance.
The number of designated stem rust resistance genes has increased by ~10 over the past four years. Translocations involving several broadly-effective alien resistance genes with limited or no previous agricultural deployment were enginneered to reduce the likelihood of linkage drag, and the foundations of adult plant resistance were established. This progress resulted from international collaboration, increased global coordination, and critical financial support. By buidling on these initial accomplishments and improving genetic and genomic resources over the next four years we expect to achieve: 1. more than 10 additional formally designated stem rust resistance genes conferring resistance to Ug99-complex races, 2. robust/diagnostic DNA marker haplotypes identified for most sources of resistance, 3. multiple linkage blocks of two or more resistance genes to enhance gene pyramiding efforts, and 4. knowledge of numerous additional sources of resistance complelely or partially identified. Never before have so many resources and supporting tools been available to combat the wheat rusts. It is an opportune time for the international community to strategically deploy and responsibly steward our genetic resources for durable control of wheat stem rust.
The model plant Arabidopsis thaliana has provided unique opportunities to explore and unravel many key biological features of plant biology including disease resistance. However, the inability of rust fungi of the genus Puccinia to infect Arabidopsis has prevented its use in exploring grass-rust interactions. The model plant Brachypodium distachyon is a member of the same grass subfamily as the principal cool-season grain crops, and can be infected with various Puccinia species. We have focused our efforts on establishing Brachypodium as a model for exploring grass - Puccinia graminis interactions. Brachypodium can be successfully infected by different formae speciales of the stem rust pathogen, including P. graminis f. sp. tritici. A wide range of response to stem rust occurs in Brachypodium and efforts are underway to decipher the genetic basis for this variation using recombinant inbred populations from parents with differing levels of response. Similarly, induced mutants with compromised stem rust resistance have been identified and are now being employed within a program to understand the molecular biology of stem rust resistance and susceptibility. Our results to date suggest that Brachypodium holds promise as a model plant for advancing our understanding of stem rust resistance.
Stripe rust of wheat, caused by Puccinia striiformis f. sp. tritici, continues to cause severe damage worldwide. Durable resistance is a key for sustainable control of the disease. High-temperature adult-plant (HTAP) resistance, which expresses when the weather becomes warm and plants grow old, has been demonstrated to be durable. We have conducted numerous of studies for understanding molecular mechanisms of different types of stripe rust resistance using a transcriptomics approach. Through comparing gene expression patterns with racespecific, all-stage resistance controlled by various genes, we found that a greater diversity of genes is involved in HTAP resistance. The genes involved in HTAP resistance are induced more slowly and their expression induction is less dramatic than genes involved in all-stage resistance. The high diversity of genes and less dramatic expression induction may explain the durability and incomplete level of HTAP resistance. Identification of transcripts may be helpful in identifying resistance controlled by different genes and in selecting better combinations of genes for pyramiding to achieve adequate and more durable resistance.
Full nonhost resistance can be defined as immunity, displayed by an entire plant species against all genotypes of a plant pathogen. The genetic basis of (non)host-status of plants is hard to study, since identification of the responsible genes would require interspecific crosses that suffer from sterility and abnormal segregation. There are some plant/potential pathogen combinations where only 10% or less of the accessions are at most moderately susceptible. These may be regarded as marginal host or near-nonhost, and can provide insights into the genes that determine whether a plant species is a host or a nonhost to a would-be pathogen. Barley (Hordeum vulgare L.) is a near-nonhost to several rust pathogens (Puccinia) of cereals and grasses. By crossing and selection we developed an experimental line, SusPtrit, with high susceptibility to at least nine different heterologous rust taxa such as the wheat and Agropyron leaf rusts (caused by P. triticina and P. persistens, respectively). On the basis of SusPtrit and several regular, fully resistant barley accessions, we developed mapping populations. We established that the near-nonhost resistance to heterologous rusts inherits polygenically (QTLs). The QTLs have different and overlapping specificities. In addition, an occasional R-gene is involved. In each population, different sets of loci were implicated in resistance. Very few resistance genes were common between the populations, suggesting a high redundancy in barley for resistance factors. Selected QTLs have been introduced into near-isogenic lines to be fine-mapped. Our results show that the barley- Puccinia system is ideal to investigate the genetics of host-status to specialized plant pathogens.
With the TTKS family of races virulent on most genes currently providing protection against stem rust worldwide, identifying, mapping, and deploying resistance genes effective against these races has become critical. We present here a genetic map of Sr35. Both parents of our diploid mapping population (DV92/G3116, 142 SSD lines) are resistant to TTKSK, but the population segregates for resistance to TRTTF (Yemen) and RKQQC (US). Race analysis suggests that G3116 carries Sr21 and DV92 both Sr21 and Sr35. Resistance to TRTTF and RKQQC was mapped to a 6 cM interval on chromosome 3AmL between markers BF483299 and CJ656351. This interval corresponds to a 178-kb region in Brachypodium which contains only 16 annotated genes and exhibits a small inversion (including 2 genes) and a putative insertion (2 genes) relative to rice and sorghum. This map contains closely-linked markers to Sr35 and provides the initial step for this gene's positional cloning.