The Evolving Battle Between Yellow Rust and Wheat: Implications for Global Food Security

doi:10.21203/rs.3.rs-557233/v1

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The Evolving Battle Between Yellow Rust and Wheat: Implications for Global Food Security

https://doi.org/10.21203/rs.3.rs-557233/v1

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published 25 Nov, 2021

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Wheat (Triticum aestivum L.) is a global commodity, and its production is a key component underpinning worldwide food security. Yellow rust, also known as stripe rust, is a wheat disease caused by the fungus Puccinia striiformis f. sp. tritici (Pst), and results in yield losses in most wheat growing areas. Recently, the rapid global spread of genetically diverse sexually derived Pst races, which have now largely replaced the previous clonally propagated slowly evolving endemic populations, has resulted in further challenges for the protection of global wheat yields. However, advances in the application of genomics approaches, in both the host and pathogen, combined with classical genetic approaches, pathogen and disease monitoring, provide resources to help increase the rate of genetic gain for yellow rust resistance via wheat breeding while reducing the carbon footprint of the crop. Here we review key elements in the evolving battle between the pathogen and host, with a focus on solutions to help protect future wheat production from this globally important disease.

Medical Genetics

Wheat fungal pathogens

disease resistance breeding

crop genomics

pathogenomics

cereal genetics

global food security

Wheat (Triticum aestivum L.) is one of the most important staple crops, with global demand predicted to increase to 324 kg/year (per capita) by 2050 (Alexandratos & Bruinsma, 2012). Wheat production faces numerous threats, with 10-16% of global wheat harvests estimated to be lost due to pests and diseases (Oerke, 2006; Strange & Scott, 2005). Yellow rust (YR), also known as stripe rust, is a major disease of wheat caused by the biotrophic fungal pathogen, Puccinia striiformis f. sp. tritici (Pst). YR infection is most commonly noted on wheat leaves, where the resulting damage to photosynthetic tissues leads to reduced light interception and radiation use efficiency, thus lowering yields (Figure 1a-b). However, YR infection can also take place on the structures of the wheat ear such as the glumes, lemma and palea, particularly during moderate to severe epidemics, resulting in reduced grain yield and quality (Bouvet et al. 2021a; Cromey, 1989; Wellings, 2003; 2009) (Figure 1c). Recurrent Pst epidemics have occurred in the majority of wheat growing areas over the past 60 years and can cause significant yield losses and reductions in grain quality if not adequately controlled (Wellings, 2011). Notably, the past two decades have seen the rapid global emergence of more aggressive and genetically diverse Pst populations adapted to warmer temperatures (Hovmøller et al. 2016; Hubbard et al. 2015; Milus et al. 2009), with concomitant impact on the YR resistance ratings of many wheat varieties. YR resistance breeding targets have had to adapt to tackle the rapidly changing Pst threat, and sources of genetic resistance for the development of improved wheat varieties are continually being sought. This is now being aided by advances in wheat genomics approaches, as well as detailed characterisation of Pst population pathotypes, genetic diversity, effector characterisation and field monitoring. Ultimately, efficient control of wheat fungal disease will be via approaches that combine agricultural and agronomic practices, disease monitoring, and varietal genetic improvement (Downie et al. 2020). In this review, we summarise current understanding of the Pst lifecycle, modes of dispersal and genetic diversity, and wheat genetic resistance and highlight some of the challenges facing the efforts to maintain adequate protection against wheat YR infection, with a focus on genetic resistance approaches.

Pst goes through five different spore stages and requires two plant host species for completion of its lifecycle (Figure 1d). The two broad stages of the Pst lifecycle are classified as: (i) the asexual stage which occurs on wheat (the primary host), and (ii) the sexual stage which we now know occurs on Berberis species (the alternate host). In wheat, YR disease occurs during the asexual stage of the Pst lifecycle and is caused by multiple cycles of dikaryotic (i.e. two nuclei in each cell: n + n) Pst urediniospores re-infecting the primary host via wind dispersal. As it is this Pst lifecycle stage that is detrimental to wheat production, the uredinial infection and colonisation processes have been studied extensively. Early phenotypic studies identified the environmental conditions conducive of infection and colonisation by uredinia: free moisture, a 9-13 °C temperature range for sporulation, and low light levels (reviewed in Line, 2002). During the initial infection stage, urediniospores germinate on the leaf surface and eventually form an appressorium from which hyphae develop and enter the leaf tissue via the stomata. Growing hyphae develop into a dense network extending between and inside host mesophyll cells. Among this network, haustoria infection structures will form and specifically develop in host cell walls to extract nutrients from it (Szabo & Bushnell, 2001). On the leaves of mature susceptible plants, disease symptoms are visible 12-14 days after infection, consisting of yellow to orange coloured urediniospores that erupt from pustules arranged in characteristic stripes that follow the veins down the leaf blade (Chen et al. 2014), which can then lead to successive rounds of secondary infections. On resistant to mildly susceptible varieties, symptoms will range from non-sporulating flecks (a sign of hypersensitivity) to necrotic and chlorotic patches with no to limited sporulation. Towards the end of the wheat growth season, diploid teliospores may be produced by some isolates via karogamy. These readily germinate to produce a promycellim of four cells, with meiosis subsequently resulting in a single haploid nucleus that forms a basidiospore able to infect the alternate host (Chen et al. 2014).

Although much less is known about the sexual stage, Berberis species were long speculated to support the lifecycle of Pst (e.g. Mains, 1933; Straib, 1937; Hart & Becker, 1934), as well as the related rust species, Pucciniagraminis f. sp. tritici (causal agent of stem rust). Historically this resulted in efforts to eradicate Berberis species in many European and North American countries (Barnes et al. 2020). However, it was not until 2010 that Berberis species were formally confirmed to support development of Pst pycnia and aecia (Jin et al. 2010). Curiously, Berberis species infected with Pst are rarely observed in the wild, with only two accounts from China reported to date (Zhao et al. 2011, 2013). This may be due to the difficulty in finding an environment that simultaneously accommodates germination of teliospores (part of the asexual stage; enclosed in telia that form on wheat leaves towards the end of the infection season and produce basidiospores) and basidiospores (part of the sexual stage; forming on barberry leaves and requiring dew for germination), both of which have short viability (Wang & Chen, 2015). A recent study showed Berberis species do not play a role in YR epidemics in the US Pacific Northwest (Wang & Chen, 2015), and an additional alternate host, Mahonia aquifolium (Oregon grape) has been identified (Wang & Chen, 2013). The main importance of the sexual Pst stage on the alternative host to wheat infection is the generation of novel combinations of standing genetic variation that results in new genetically diverse isolates that can cause widespread epidemics and result in rapid changes in wheat resistance profiles.

Over the years, monitoring of virulence changes in Pst populations in the major wheat producing regions has revealed notable changes in pathogen movement and adaptation. These studies were based on pathogenicity surveys, which use sets of differential wheat lines carrying known resistance genes, either near isogenic lines or cultivars, for the characterisation of pathotypes at the seedling stage (Wellings et al. 2009). More recently, molecular and genomics techniques have been used to infer Pst population structure and genetic diversity, confirming patterns of adaptation hypothesised in pathotype-based approaches. Here, we summarise key findings and events from the past three decades, specifically focusing on patterns of spore dispersal and Pst evolution and adaptation.

Blowing in the wind

Pst urediniospores are windborne and can disperse at continental scales. Coupled with the obligate nature of the pathogen (requiring living tissue to survive), this has led to different scenarios for the observed seasonal and geographic patterns of dispersal. One such model is the local extinction and re-colonisation model, illustrated for example in China where regions of the Sichuan and Gansu provinces in which Pst prevails all year round act as a source of inoculum to the more northerly provinces in which wheat is predominantly grown as a winter crop (Brown & Hovmøller, 2002; Zeng & Luo, 2006). In this way, Pst populations re-establish at the beginning of each wheat cropping season in those regions where Pst spores are usually unable to over-winter. A similar pattern of spore movement according to prevailing winds and the seasonality of the cropping seasons has been speculated in North America, with spores migrating from southern central states of USA and Mexico to northern central states of USA and Canada (Chen, 2005). In North Western Europe, Pst spore dispersion appears to follow the continental-island model, first described by Hedrick (1985), and has been the predominant model of Pst spore dispersion in North Western Europe. In this region, urediniospores travel up to 1,700 km with prevailing winds, and migrating between UK, France, Germany and Denmark (Hovmøller et al 2002). Investigations of YR emergence events in countries where it was previously absent provide examples of rapid inter-continental foreign incursion. Australia has been subject to several known incursions, of which two were notably detrimental to the wheat industry due to their rapid spread: (i) the first occurrence of Pst, in 1979 (Wellings et al. 1987), and (ii) the 2002 incursion in Western Australia (Wellings et al. 2003), now known to have originated from the Middle East/East Africa (Ali et al. 2014a) and attributed to a single Pst isolate (Wellings et al. 2003). The more recent arrival of Pst isolates in South Africa in 1996 were related to the Mediterranean and Central Asian populations (Boshoff et al. 2002; Ali et al. 2014a), and was speculated to be due to wind dispersal or human activities (Ali et al. 2014a). In all three cases, human activity, most likely through accidental transport on clothing, has been either demonstrated or strongly speculated, highlighting the increasing role of globalised trade and international travel as a means for Pst urediniospore dispersal.

Pathogen evolution and adaptation

Prior to 2000, pathogenicity surveys and molecular studies using isolates collected across the main wheat-producing regions in Europe, Australia and America typically reported Pst populations were clonal in nature, and that pathotypes exhibited close-relatedness and low genetic variation - predominantly underpinned by single step-wise mutations (Hovmøller et al. 2002; Enjalbert et al. 2005; Chen, 2005; Steele et al. 2001; Chen et al. 2010; Ali et al. 2014a; Hubbard et al. 2015; Hovmøller et al. 2016). Such clonally-derived Pst mutations have caused several severe YR epidemics, due to the ‘breakdown’ of specific wheat Yr resistance genes present in large acreages across the agricultural landscape. Notable examples include breakdown of Yr17 in Northern Europe (Bayles et al. 2000), Yr27 in Ethiopia (Solh et al. 2012), and Yr9 in America, the Middle East and the Indian sub-continent (Chen et al. 2010; Singh et al. 2004). Before the year 2000, the only exceptions to such patterns of low Pst genetic variation were observed in isolates from the Himalayan (Nepal and Pakistan) and near Himalayan (China) regions, which exhibited high levels of genetic recombination, high ability for sexual reproduction and high genetic diversity (Duan et al. 2010; Mboup et al. 2009; Ali et al. 2014b). These areas were therefore classified the putative centres of Pst origin (Ali et al. 2014b). However, the last two decades have seen the emergence of unusual virulence profiles and aggressive strains across the world. The most noteworthy event was the rise of two strains, PstS1 and PstS2, across the USA (Chen et al. 2002; Markell & Milus, 2008), Europe (Hovmøller & Justesen, 2007) and Australia (Wellings, 2007) in the space of just three years in the early 2000s. A global study of pre- and post-2000 Pst races combining detailed virulence pathotyping and DNA fingerprinting found these while these two strains were genetically similar to each other, they were highly divergent from previous races in their respective geographic regions (Hovmøller et al. 2008). Their rapid spread was thought to be due to their increased aggressiveness (ability to yield more spores and for disease symptoms to occur more quickly) and high temperature adaptation - which was later demonstrated in the detailed study by Milus et al. (2009). In addition to PstS1 and PstS2, additional atypical occurrences of Pst races have since been reported. Enjalbert et al. (2005) demonstrated high levels of genetic divergence between the Pst population in northern France and a single clone specific to the South. What was atypical was that this single pathotype was maintained for a long time in this region, despite the presence of gene flow between Northern and Southern Pst populations. This isolate was later found to be more closely related to the Central Asian-Mediterranean population (Ali et al. 2014a). Similarly, instances of strong genetic divergence have also been revealed in North Western Europe (Flath & Barthels, 2002; Hovmøller & Justesen 2007a). Two groups of highly divergent pathotypes from the ‘old’ North-Western European population exhibited three to four times higher levels of genetic diversity (Hovmøller et al. 2007). In 2011, two novel Pst races disrupted the European Pst landscape (www.wheatrust.org). Named after the host varieties on which they were first detected, one race was virulent on wheat cv. ‘Warrior’ and the other was virulent on cv. ‘Kranich’. These were later characterised as PstS7 and PstS8 respectively (Ali et al. 2017), and were detected simultaneously across Europe and infected varieties that had exhibited durable adult plant resistance. Both races were distinct from the typical European isolates in that they produced an unusually high number of teliospores (Hubbard et al. 2015; Hovmøller et al. 2016). Additional Pst races have been characterised (PstS10 also known as ‘Warrior (-)’, PstS4 ‘Triticale aggressive’) and together with the other new genetically diverse Pst races, have come to largely dominate within Europe (Ali et al. 2017; Hovmøller et al. 2016; Hubbard et al. 2015). Collectively, these atypical observations, further supported by genetic diversity studies, have led to speculation of an aerial-induced foreign incursion, which would be the first of its kind in Europe since the establishment of Pst in Europe during the 19^th century. Beyond Europe, rapid invasions and the subsequent Pst population changes have been responsible for a number of YR epidemics in Central Asia, North and East Africa (Ali et al. 2017).

Review of global YR epidemics shows most wheat growing regions document recurrent crop losses of 5-10 %, with occasional losses of up to 25 % (Welling, 2011). However, following the global spread of aggressive Pst races since 2000, surveys highlight an increase in both the number of countries being significantly hit by such races, and the extent of the losses incurred (Beddow et al. 2015). Indeed, the financial implications of this change in Pst race structure estimated that a global average of US$ 158 million was lost annually pre 2000s, compared to US$ 979 million post 2000 (Beddow et al. 2015). Wheat growers have two principal options to protect against the effects of YR on yield: (i) protect their crop with agro-chemicals that limit initial infection and progression of pathogen colonisation, and/or (ii) grow wheat varieties with adequate levels of genetic resistance. Systemic fungicides that are absorbed into the plant became commercially available in the 1980s and have since formed an important part of integrated control measures against YR (Chen, 2005). Several products with different modes of action are available for protection against YR (reviewed by Chen & Kang, 2017), with timely application a key aspect of an effective fungicide programme. Such an approach has, for example, prevented significant financial losses in periods of severe epidemics in the USA (Line, 2002). While fungicide control provides an essential tool in combatting sudden yellow rust epidemics and in situations where growing resistant varieties is not an option, over-dependence on their use comes with negative environmental impacts and notable financial cost to growers. For example, in Australia an estimated A$ 359 million per year is spent on fungicides for YR control (Murray & Brennan, 2009). In the mid-to-long term, regular Pst exposure to fungicides also increases the risk that Pst populations develop resistance to frequently used chemistries. Historically, Pst been classified as being at low-risk of developing fungicide resistance. However, of the three classes of fungicides active against Pst (demethylation inhibitors, DMIs; succinate dehydrogenase inhibitors, SDHIs; quinone outside inhibitors, QoIs), Pst resistance has evolved against two. Low levels of DHI resistance have been reported, and while high proportions of isolates carrying resistance associated mutations have been reported in some countries (Cook et al. 2021), DHI resistance has so far had limited agronomic-scale significance (Oliver, 2014). SDHIs active against rusts have only been introduced relatively recently, giving less time for Pst resistance to evolve. Nevertheless, sets of geographically diverse isolates have been identified that carry a mutation homologous to that linked to SDHI resistance in the related rust species P. pachyrhzi (Cook et al. 2021). In the face of additional considerations such as changing regulation surrounding permissible chemistries, such evidence has led to the suggestion that the Pst risk classification should be upgraded (Oliver, 2014), fungicide resistance management practices be considered, and that systematic monitoring for Pst for fungicide resistance should be implemented (Cook et al. 2021). Lastly, the optimisation of fungicide timing, as well as improved fungicide application technologies, represent areas where additional research and development is required (Carmona et al. 2020).

More than 300 wheat genomic regions conferring YR resistance have been reported (Rosewarne et al. 2013; Wang & Chen, 2017). Of these, ~80 are permanently named yellow rust resistance (Yr) genes (recently summarised by Jamil et al. 2020). Two main classes of YR resistance (R) genes are commonly described. The first is termed ‘all stage resistance’ (or ‘seedling resistance’) and confers qualitative resistance – typically to one or a low number of Pst isolates. The second is termed ‘adult plant resistance’ (APR) and confers quantitative or partial resistance. While these R gene classifications are useful, additional categories are also used, based on criteria such as phenotypic response (infection type, race specificity, resistance levels), temperature sensitivity, durability, the number of genes involved (monogenic versus polygenic) and the size of gene effect (Chen, 2013). One of the issues that comes with defining YR resistance with such a broad range of criteria is the assumptions associated with each of them. For example, APR is typically non-race specific, more durable than seedling resistance and conditioned by genes with minor or partial effect. Nevertheless, some APR genes have been shown to exhibit race specificity, such as Yr11, Yr12, Yr13 and Yr14 (Johnson, 1992; McIntosh et al. 1995).

All-stage resistance

Initially expressed at the seedling stage, all-stage resistance extends throughout the growth of the wheat plant and is characterised by a hypersensitive response. It is generally effective against some, but not all, Pst races and is therefore also referred to as ‘race-specific resistance’. All-stage resistance is underpinned by the gene-for-gene model, first explored by Flor (1956) in the flax-rust pathosystem, whereby the product of an R gene must be recognised by the protein encoded by its corresponding avirulent (Avr) gene in the pathogen, with resistance conferred by an incompatible R-Avr interaction. This results in a qualitative resistance phenotype that can be easily assessed, historically making it a popular selection criterion in breeding programmes, and more recently, for gene cloning. The majority of catalogued YR R genes exhibit this type of phenotype, and many become ineffective against present-day Pst races. This type of resistance has commonly been shown to be a short-term strategy for YR control. Indeed, the deployment of varieties with single or low-numbers of all-stage resistance Yr genes over large acreages inevitably exerts high selective pressure on the pathogen, forcing it to evolve and mutate until host resistance is broken down, and leading to cycles of ‘boom and bust’ (McDonald & Linde, 2002).

Adult Plant Resistance

Adult plant resistance (APR) is characterised by slow rusting (a long period of latent infection, small lesion size) (Guo et al. 2008) or partial resistance, typically manifests at the adult plant stage, and has long been established as a durable source of YR resistance. Two notable examples are Yr18/Lr34/Sr67/Pm38, extensively deployed in spring wheat cultivars through the international breeding programme at CIMMYT (Singh et al. 2005) and Yr16, an APR gene commonly used in early European varieties such as ‘Cappelle Desprez’, a major hub in the European wheat pedigree (Fradgley et al. 2019). While APR is primarily non-race specific, examples of APR specificity to Pst races do exist, such as Yr12 and Yr13 (Johnson, 1992; McIntosh et al. 1995). Such APR race-specificity was initially reported by Johnson (1988) and has recently been observed in Europe following the spread of atypical Pst races (Sørensen et al. 2014). For example, while the APR resistance allele conferred by the founder Claire at the QTL QYr.niab-2D.1 was effective in the UK during the 2015 and 2016 seasons (Bouvet et al. 2021b), it has since broken down (Simon Berry, personal communication). Another example is that of Yr49, which was initially found to be non-race specific against all Australian Pst isolates, but when tested against Chinese races was found to be virulent and thus showed race-specificity (Ellis et al. 2014). These occurrences undermine the durability of APR and puts into question whether this pathotype criteria should be used to describe this type of resistance. It has been suggested that as some APR genes confer resistance against multiple biotrophic pathogens, this characteristic is a good indicator of durability. Examples include Yr18/Lr34/Sr67/Pm38 (Spielmeyer et al. 2005; Lillemo et al. 2008), Yr29/Lr46/Sr58/Pm39 (Lagudah, 2011), Yr30/Lr27/Sr2 (Mago et al. 2011) and Yr46/Lr67/Sr55/Pm46 (Herrer-Foessel et al. 2014). Interestingly, some of these genes are also associated with traits such as leaf tip necrosis (Yr18/Lr34/Sr67/Pm38, Singh et al. 1992; Yr29/Lr46/Sr58/Pm39, Rosewarne et al. 2006; Yr46/Lr67/Sr55/Pm46, Herrera-Foessel et al. 2014) and pseudo-black chaff (Yr30/Lr27/Sr2, Kota et al. 2006). Finally, some APR resistances are more effective at high temperature (usually 25-30 °C), and are termed High Temperature Adult Plant (HTAP) resistance. Yr36 was initially characterised as HTAP (Uauy et al. 2005), with subsequent studies showing resistance was effective over 25 °C at all growth stages (Fu et al. 2009), and that the lower effective temperature range is 18 °C (Bryant et al. 2014).

Nucleotide Binding Sequence Leucine Rich Repeat (NBS-LRR) proteins are the most common class of proteins encoded by plant R genes, and act predominantly by recognising the effector molecules that pathogens produce to inhibit host defence responses (Jones et al. 2016). To help fight against potential infecting pathogens, plant NLR gene families have radiated and diversified, for example via localised gene duplication or mutation within their LRR domains that bind pathogen effectors (Sarris et al. 2016). Furthermore, some NBS-LRRs contain additional ‘integrated’ domains, the most common of which are kinase and DNA-binding domains (Andersen et al. 2020; Steuernagel et al. 2020), and are thought to be involved in receptor activation or downstream signalling (Sarris et al. 2016). Of the 18 genes conferring all-stage resistance to wheat rusts (yellow rust, stem rust, leaf rust) that have been cloned, 17 encode NBS-LRRs (Table 1). Furthermore, all but two of these NBS-LRRs contain coiled coil (CC) domains towards their N-termini; the exceptions being Yr7 and the allelic R genes Yr5/YrSP, each of which contains an N-terminus integrated BED zinc finger domain (Marchal et al. 2018) and Sr60, which is race-specific but confers a partial resistance phenotype and encodes a protein with two putative kinase domains (Chen et al. 2020).

The ongoing changes and rapid spread of Pst populations around the world has led to growing interest in more durable sources of resistance. To date, four adult plant YR resistance genes have been cloned. Yr36 encodes a protein with a kinase and a START lipid-binding domain (WHEAT KINASE START 1, WKS1; Fu et al. 2009), and is thought to regulate reactive oxygen species (ROS) via phosphorylation of the thylakoid ascorbate peroxidase protein, resulting in increased levels of ROS during immunity (Gou et al. 2015). More recently, WKS1 has been shown to phosphorylate a protein component of photosystem II, sbO, resulting in reduced photosynthesis, leaf chlorosis and Pst resistance (Wang et al. 2019). Yr18/Lr34 encodes an ABC transporter (Krattinger et al. 2009) involved in the translocation of abscisic acid (Krattinger et al. 2019) while Yr46/Lr67 encodes a hexose transporter (Moore et al. 2015). Finally, the broad-spectrum R gene Yr15 encodes a tandem kinase-pseudokinse protein (Klymiuk et al. 2018) similar to that encoded by the barley stem rust resistance gene Rpg1 (Brueggeman et al .2002), and has recently been shown to be allelic with YrG303/YrH52 (Klymiuk et al. 2020).

Pyramiding multiple resistance genes with additive effects into single genetic backgrounds should help prevent dramatic breakdown of wheat Pst field resistance. This first iteration of resistance gene pyramiding was developed using conventional breeding techniques. Indeed, the CIMMYT wheat breeding programme has made extensive use of the ‘Yr18 complex’ (Yr18 and at least two closely linked resistance genes), which has provided durable resistance against yellow rust (Singh et al. 2005). Tools to help such approaches are available. These include protocols for the use of diagnostic molecular markers for marker-assisted breeding for many of the cloned resistance genes listed above (https://maswheat.ucdavis.edu/), as well as ‘speed breeding’ methods that include the use of extended day lengths and controlled temperatures to shorten the wheat lifecycle (Watson et al. 2018). However, combining numerous unlinked genes via crossing is time-consuming. For example, a recent crossing scheme for the incorporation of 12 resistance genes int a single recurrent background involved 20 generations (Hafeez et al. 2021). Additionally, sources of YR resistance commonly originate from species related to bread wheat (see Table 1), including diploid wheat (e.g. T. monococcum and Aegilops tauschii) and wild or cultivated tetraploid wheats (T. turgidum ssp. dicoccoides and T. turgidum ssp. durum, respectively), resulting in introgression of linked chromosomal regions from the donor progenitor species. Such introgressed regions may have a negative effect on crop performance; for example, while Sr60 has recently been introduced into bread wheat via the introgression of a small T. monococcum segment containing the R gene, it nevertheless contains linked PUROINDOLIN genes which will affect grain texture (Chen et al. 2020). Such considerations mean development of resistance gene cassettes containing multiple R genes could provide a useful breeding tool, providing multiple sources of resistance inherited as a single genetic unit. Assuming their effects will be additive (i.e. show no epistasis), the four cloned APR genes, Yr15, Yr18, Yr36 and Yr46, possibly combined with one or more ASR genes, represent obvious immediate targets. Indeed, a transgene cassette containing four stem rust ASR genes and one APR gene has recently been shown to confer broad-spectrum field resistance (Luo et al. 2021). However, such approaches do not come without their challenges: genetic modification regulations and consumer acceptance remains an important barrier in many parts of the world, relatively low numbers of Yr genes have been cloned, and further work is needed to determine how specific genes work in combination within the context of inbred lines and F₁ hybrids. Towards tackling some of these issues, proposals to generate an R gene atlas for the major diseases of wheat have been made (Hafeez et al. 2021). Such concepts would be aided by the systematic identification and monitoring of the corresponding Pst effectors and their standing variation across the agricultural environment, and should be extended to identify, characterise and eliminate wheat susceptibility (S) genes that act to increase YR susceptibility (e.g. Corredor-Moreno et al. 2021). Underpinning such aims is the availability of new genomic techniques and resources in wheat that complement classical map-based cloning methodologies (recently reviewed by Adamski et al. 2020). For example, candidate gene association mapping using diversity panels of wheat or wheat relatives genotyped via reduced representation sequencing of classes of genes known a priori to be prevalent in disease resistance (such as NBS-LRRs or wall-associated kinases). This method, termed ‘RenSeq’ (Jupe et al. 2013), alongside functional validation via chemical mutagenesis of germplasm containing the functional allele of interest, has been used to identify the wheat stem rust resistance genes Sr46 and SrTA1662 (Arora et al. 2019). Such association mapping approaches can be extended to include more representative coverage across the genome, for example using promotor/exome capture arrays (Gardiner et al. 2019) or whole-genome sequencing at low-coverage combined with imputation of SNPs and haplotypes, aided by the use of reference genome assemblies (e.g. for bread wheat: IWGSC, 2018; Walkowiak et al. 2021). Furthermore, the availability of Pst genome assemblies (e.g. Cantu et al. 2011, 2013; Zheng et al. 2013; Schwessinger et al. 2018, 2020) and mutant populations (Li et al. 2020), as well as gene expression resources and interrogation tools for both species (e.g. Adams et al. 2021) should help identify and characterise pathogen effectors. Detailed knowledge of the specificity of the recognition interactions between wheat R genes and their corresponding Pst effectors could be used, for example, to monitor the functionality of each component of R stacks, and to design synthetic R genes engineered to recognise multiple races (as demonstrated for example by editing of the rice NBS-LRR gene PikP to recognise multiple variants of the effector AvrPik from the rice blast pathogen Magnaporthe oryzae; De La Concepcion et al. 2019). Similarly, identification of wheat S genes would allow their elimination, via marker assisted approaches, mutation breeding or gene editing. Finally, further understanding of the exact developmental stages at which different adult plant resistance genes become effective, how best to deploy these in the agricultural landscape to best protect the crop from infection throughout the key growth stages, and understand which R genes exhibit the lowest yield cost, will further help protect wheat against the effects of YR.

The wide-ranging spread of new genetically diverse Pst races has meant that YR is likely to become an increasing threat to global wheat production, resulting in lower yields and increased financial and environmental costs. Here, we conclude with a series of recommendations for future research and development in YR management over the next decade:

Host genetics

Systematic programmes to identify and clone known and novel R genes, particularly those conferring adult plant or non-host resistance.
Informed design and development of durable R gene pyramid combinations, via traditional crossing and/or R gene cassettes.
Identification and targeted removal of susceptibility (S) genes from breeders’ germplasm.

Monitoring

Regional and international networks to rapidly monitor the emergence and spread of Pst pathotypes.
Field networks to monitor R gene effectiveness at regional/international scales.

Agronomy

Regional monitoring for the emergence and spread of fungicide resistances.
Innovation in fungicide application to allow more timely, accurate and efficient fungicide application.
The use of variety mixtures, which is becoming increasingly used in some regions.

Ultimately, the success of advances in integrated YR management approaches will depend on timely communication of information to wheat growers. Therefore, trusted grower-facing networks and sources of information that can rapidly and succinctly inform and advise farmers of threats and best practice within each growing season will become increasingly critical in realising future ambitions to better protect wheat yields from diseases such as YR.

Adult plant resistance APR

Demethylation inhibitors DMIs

Genome-wide association scan GWAS

Marker assisted selection MAS

Nucleotide-binding leucine-rich repeat NLR

Puccinia striiformis f. sp. tritici Pst

Quantitative trait locus QTL

Quinone outside inhibitors QoIs

Succinate dehydrogenase inhibitors SDHIs

Yellow rust YR

Author contributions: LB wrote the manuscript with inputs from JC. All authors edited and critically revised the manuscript.

Funding: LB was funded via a Biotechnology and Biological Sciences Research Council (BBSRC) Doctoral Training Partnership PhD award to the University of Cambridge. JC’s time has partly supported by Biotechnology and Biological Research Council grant BB/N00518X/1, funded via the 2^nd call of the ERA-CAPs framework.

Acknowledgements: We thank Prof. Julian Hibberd (University of Cambridge) for administrative supervisory input during LB’s PhD.

Conflict of interest statement: On behalf of all authors, the corresponding author states that there is no conflict of interest.

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Table 1. Cloned wheat rust resistance (R) genes. ASR = all-stage resistance. APR = adult plant resistance. Lr = leaf rust, Sr = stem rust, Yr = yellow rust. TKP = tandem kinase-pseudokinase. Chr. = chromosome. ^†Yr5/YrSP and Yr7 are listed using their RefSeq v1.1 gene model accession numbers. ^‡In bread wheat, the Sr50 locus from rye has been translocated to chromosome 1D. ^*See also Yuan et al. (2018), who indicate the CC-NBS-LRR gene identified by Liu et al. (2014) may not be the underlying gene.

Cloned YR resistance genes	Original source	Chr.	R gene class	NCBI protein accession number	Gene functional annotation	Reference
Lr1	T. aestivum	5D	ASR	ABS29034	CC-NBS-LRR	Cloutier et al. 2007
Lr10	T. aestivum	1A	ASR	AAQ01784	CC-NBS-LRR	Feuillet et al. 2003
Lr21	Ae. tauschii	1D	ASR	ACO53397	NBS-LRR	Huang et al. 2003
Lr22a	Ae. tauschii	2D	ASR	ARO38244	CC-NBS-LRR	Thind et al. 2017
Sr13	T. turgidum ssp. durum	6A	ASR	ATE88995	CC-NBS-LRR	Zhang et al. 2017
Sr21	T. monococcum	1D	ASR	AVK42833	CC-NBS-LRR	Chen et al. 2018
Sr22	T. monococcum	7A	ASR	CUM44200	CC-NBS-LRR	Steuernagel et al. 2016
Sr33	Ae. tauschii	1D	ASR	AGQ17384	CC-NBS-LRR	Periyannan et al. 2013
Sr35	T. monococcum	3A	ASR	AGP75918	CC-NBS-LRR	Saintenac et al. 2013
Sr45	Ae. tauschii	1D	ASR	CUM44213	CC-NBS-LRR	Steuernagel et al. 2016
Sr46	Ae. tauschii	2D	ASR	AYV61514	CC-NBS-LRR	Arora et al. 2019
Sr50	Secale cereale	1R^‡	ASR	ALO61074	CC-NBS-LRR	Mago et al. 2015
Sr60	T. monococcum	5A	ASR	LRRK123	Tandem kinase	Chen et al. 2020
SrTA1662	Ae. tauschii	1D	ASR	Not listed	CC-NBS-LRR	Arora et al. 2019
Yr5/YrSP	T. spelta album	2B	ASR	TraesCS2B02G488000^†	BED-NBS-LRR	Marchal et al. 2018
Yr7	T. aestivum	2B	ASR	TraesCS2B02G488600^†	BED-NBS-LRR	Marchal et al. 2018
Yr10^*	T. aestivum	1B	ASR	AAG42168	CC-NBS-LRR	Liu et al. 2014
Yr15/YrG303/YrH52	T. turgidum ssp. dicoccoides	1B	APR	AXC33067	TKP	Klymiuk et al. 2018
Yr18/Lr34	T. aestivum	7D	APR	ACN41354	ABC transporter	Krattinger et al. 2009
Yr36	T. turgidum ssp. dicoccoides	6B	APR	ACF33187	Kinase-START	Fu et al. 2009
Yr46/Lr67	T. aestivum	4D	APR	ALL26331	Hexose transporter	Moore et al. 2015
YrAS2388	Ae. tauschii	4D	ASR	QDW65446	CC-NBS-LRR	Zhang et al. 2019

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published 25 Nov, 2021

Read the published version in Theoretical and Applied Genetics →

Reviews received at journal
30 May, 2021
Reviewers invited by journal
28 May, 2021
Editor assigned by journal
24 May, 2021
First submitted to journal
24 May, 2021

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The Evolving Battle Between Yellow Rust and Wheat: Implications for Global Food Security

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Journal Publication

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Abstract

Figures

1. Introduction

2. The Complex Pathogen Lifecycle

3. Pathogens On The Move: Patterns Of Pst Dispersal And The Rise Of Divergent Lineages And Aggressive Races

4. Chemical Control Of Yellow Rust

5. Genetic Control Of Yellow Rust

6. Cloned Yellow Rust Resistance Genes

7. Designing Yellow Rust Resistant Wheat

8. Future Perspectives

Abbreviations

Declarations

References

Tables

Status:

Journal Publication

Version 1