Robert McIntosh*,Jingmei Mu,Dejun Han,Zhensheng Kang

aPlant Breeding Institute Cobbitty,University of Sydney,Private Bag 4011,Narellan,NSW 2567,Australia

bState Key Laboratory of Crop Stress Biology in Arid Areas,College of Agronomy,Northwest A&F University,Yangling 712100,Shaanxi,China

cCollege of Agronomy,Northwest A&F University,Yangling,712100,Shaanxi,China

dCollege of Plant Protection,Northwest A&F University,Yangling,712100,Shaanxi,China

Keywords:

A B S T R A C T The objective of this review is to describe events in China and elsewhere that are related to the discovery,genetic identification,use,and ultimate break-down of a single wheat gene for resistance to stripe rust,namely Yr24/Yr26.In our retrospective analysis there was an early assumption of at least three genes at or near the locus,which caused an erroneous presumption of genetic diversity for resistance.It is an example of another boom and bust cycle in plant breeding with races virulent to Yr26(V26 races)now being the majority race group in the Chinese Pst population.We have attempted to present our story in a historical and personal context demonstrating research inputs from different national and international groups,as well as some significant contemporary side issues.It covers the period from the late 1980s to 2017,during which significant rapid advances in the molecular biology of host:pathogen genetics occurred.We attempt to describe both successes and drawbacks in our work.

1.Introduction

Stripe or yellow rust(caused by Puccinia striiformis Westend.f.sp.tritici)is a significant wheat disease worldwide.Although many genes for resistance have been documented and a number given permanent designations,there are many more that have been documented and given temporary names because they require either further validation, suitable germplasm to represent a permanent designation,or the stocks carrying them are not internationally accessible.In other cases,resistances have been named as quantitative trait loci(QTL)that span considerable genetic length and again need further work for validation and Mendelization.Nevertheless,resistances in the last two groups can be given temporary names or QTL designations according to the rules of genetic nomenclature for wheat.

Stripe rust,along with Fusarium head blight,are currently the two most important diseases of wheat worldwide.Major stripe rust epidemics in China are infrequent,but can be spectacular in scope and consequence.These well described epidemics,were consequences of the introduction and widespread use of initially effective resistance genes,either in widely grown varieties,or suites of derivatives with the same resistance genes,followed by the emergence of virulent races.This pattern of resistance breeding and subsequent disease epidemics clearly follows the predictable boom-and bust cycle.

Since the 1950s there have been five documented boom and bust stripe rust episodes in China[1].The first occurred in the 1950s with the use of variety Bima 1 that carries gene Yr1[2].The second was in 1964,but in this case there is no documentation relating to any specific source of resistance.The third was due to virulence to Yr9 present in the widely used 1BL.1RS translocation produced in Germany in the 1930s and later distributed worldwide,and mainly derived from successful varieties produced in the former USSR.These varieties then went on to China and CIMMYT,Mexico where they were used further in breeding programs.Virulence for Yr9 in China was first documented in 1987 in a race known as CYR29[3].The fourth major change and subsequent epidemics came with virulence to Fan 6 and its derivatives from 2002.The race involved was CYR32.Fan 6 and derivatives were grown widely in Sichuan province and other stripe rust hots pot regions in the country(Box 1).The genetic basis of resistance in Fan 6 and its derivatives has never been well established.There were reports that its resistance was derived from a complex parentage that included Hybrid 46,which has Yr4,an all-stage resistance gene likely present on chromosome 3BS[4].However,Fan 6 has also been described as lacking all-stage resistance.The major races that overcame Fan 6 and derivatives were CYR31,CYR31,and CYR33,but the avirulence/virulence for mulae based on differential host genotypes with all-stage resistance genes do not directly explain virulence on Fan 6 seedlings and adult plants in the same way as described above for the Yr1 and Yr9 examples.

The fifth change and current cycle of events was the discovery and deployment within China of resistance sources carrying a gene that was designated(for reasons explained below)with two,or more,names viz.Yr24 and Yr26.The first Chinese race virulent to this gene,named V26,was documented in 2008(Box 2).By this time there were many winter and spring wheat varieties carrying the resistance gene(or two or more different resistance genes),and a variety known as Guinong 22 was adopted as a potential differential genotype used to identify races.

Box 1

Disease hotspots:These are regions where a disease tends to occur on a more regular basis due to host genotypes favoured by the farmers,favourable geographic and climatic conditions,overlapping cropping cycles and/or agronomic practices,climatic conditions favouring pathogen survival between cropping cycles,and presence of barberry or other alternate hosts permitting survival and sexual recombination of pathogens.Plant pathologists,geneticists and breeders select such regions for testing host materials.However,the reasons for choosing such regions for host screening may differ.In some cases the purpose is to take advantage of the environmental conditions and to artificially inoculate host nurseries with selected races obtained or purchased from research centres.In other situations the purpose is to rely on natural infection,and hence exposure to existing pathogen variation within the region.Hotspots may also refer to localized spots of disease that develop after initial infection of a field.

China and India are the most populous countries.They are also the largest producers of wheat,in each country often slightly exceeding 100 million metric tons.Any threat to wheat production on the planet is a threat to food security,and is far more significant if that threat occurs in either ofthese countries.Thus,widespread damaging epidemics in either country must be averted by breeders ensuring that there is sufficient diversity and durability of disease resistance in farmers' fields to curtail widespread losses following changes in pathogen populations.In order to have some assurance of diversity and durability we need genetic knowledge and breeding tools to meet future challenges to food security.The necessary details are often known only after a resistance source has failed;inevitably too late to avert farm losses,and perhaps to prevent more widespread disaster.

Box 2 When resistance genes are first deployed they are usually effective against all pathogen isolates in a particular region.Regular surveys then detect virulence for part or all of the underlying resistance,but it may take several years for large-scale epidemics to occur.It is therefore important to know which varieties might carry the affected resistance gene and how those varieties are likely to respond in the field.Some may have additional effective all-stage resistance or adult plant resistance.Some significant events are summarized in the following Table.

Each important resistance source has a story.The purpose of this review is to document the story of Yr24/Yr26 with the objective of learning lessons that might be instructive in minimising the impacts of future epidemics.Already we know that discovery and widespread use of a single gene for resistance in a major crop can be a potential source of disaster,and we must find alternative approaches.The first problem is that different sources of resistance may carry the same resistance gene,or at least express the same response specificity.The germplasm origin and putative variety pedigree are not sufficient evidence for predicting that the resistance gene(s)they carry are in fact different.

2.Discovery and naming Yr24 and Yr26

This part of our story covers genetic research and breeding efforts at four primary locations.

2.1.Australia

E.S.Lagudah at CSIRO Canberra produced a series of synthetic wheat lines,one of which was noted to have all-stage stripe rust resistance.The primary interest in developing synthetic wheat was related to the DD genome component.Synthetic wheat has the genome AABBDD and is an amphidiploid,or chromosomally doubled hybrid of tetraploid wheat(AABB)and Aegilops tauschii(DD).Studies on a Meering*2/Triticum durum K733/Aegilops tauschii AUS18911 backcross derivative and K733 clearly showed that the resistance gene was derived from the latter.The resistance gene was located on chromosome 1B[7].Further studies showed that the gene was located in the centromere region and was likely different from the earlier named Yr15,which was derived from wild emmer(T.dicoccoides,also AABB)and mapped to a similar region on chromosome 1B.Thus on the basis of pedigree,infection type(the phenotype of the host:pathogen interaction,see Fig.1)and marker associations,this gene was determined to be new.It was subsequently named Yr24,transferred by backcrossing to the susceptible selection(AvS)S by C.R.Wellings,at the University of Sydney,and distributed internationally as AvSYr24 or AvS+Yr24.

2.2.Nanjing Agricultural University,China

Work by P.D.Chen's group at Nanjing was focussed on the transfer of Pm21 for resistance to powdery mildew from Dasypyrum villosum(syn.Haynaldia villosa)to wheat[8].Several sister lines with Pm21 were selected and widely distributed in China and elsewhere.Because Pm21 was highly effective the lines were widely used in breeding programs located in both the winter and alternate growth habit wheat production areas in China where powdery mildew is endemic.The original materials were also resistant to stripe rust and breeders selected for stripe rust resistance as well as powdery mildew resistance when opportunities permitted,either in their own local nurseries or in nurseries located in stripe rust hotspot locations in Gansu or Sichuan provinces.It was initially presumed that the stripe rust resistance gene was located in the same alien segment(6AS·6VS)as Pm21.Indeed the gene name Yr26 was proposed and approved on that basis[9].Suggestions then came that Pm21 and Yr26 were not present in the same alien segment.Genetic independence of these genes was confirmed in Australia by C.R.Wellings and R.A.McIntosh(unpublished)by evaluating segregating Avocet S backcross populations for response to stripe rust and powdery mildew.Clearly,the two genes were not associated.The pedigree of the Nanjing materials(Yangmai 5/4/T.durum cv.γ 80-1/Haynaldia villosa//Ningmai6/3/Yangmai)included a somewhat ignored durum parent used as a bridging parent in the original wide cross.However,when the issue of gene identity arose,seed of the durum parent was no longer available and therefore rust and powdery mildew tests on it could not be performed.Yr26 was located in the centromere region of chromosome 1B[10,11].

A different D.villosum derivative was produced and distributed as Guinong 22.The pedigree of this line was D.villosum/T.durum cv.Sauwene,and the subsequent hybrid material was naturally outcrossed with common wheat[12].Genetic analysis of this line located a recessive gene named yrGn22 in the centromere region of chromosome 1B[13].They further suggested that Yr26 and yrGn22 were linked or were possibly the same gene.However this work was published long after races virulent to Guinong 22 had been identified[6]and in 2009 Guinong 22 was still being listed as possessing an unknown resistance gene;at least in regard to race determination up to 2007[5].

Fig.1–Comparisons of seedling stripe rust responses(infection types)on lines carrying Yr24,Yr25,YrCH42,YrGn22,Yr10 and Yr15 with Australian(A)and Chinese(B)Pst races.(A)AvS+Yr15,K733(durum source of Yr2),AvS+Yr26,C07.22(Chuanmai 42),AvS+Yr10,and Avocet S inoculated with races 134 E16A+(culture accession 572)and 150 E16A+(accession 598);(B)AvS+Yr26,AvS+Yr24,Guinong 22,K733,AVS+Yr10,and Mianyang 169 inoculated with races CYR32 and V26.Note for both countries the common virulences for Yr24,Yr26,YrGn22,and AvocetS+Yr10 and the similar necrotic resistant responses(infection types)of all sources of Yr24/Yr26 that are clearly different from the near-immune responses of Yr10 and Yr15.Durum line K733 is also more resistant to race 134 E16A+than the AvSYr24 derivative.Photographs by courtesy of Dr.P.Zhang.

2.3.Sichuan Academy of Agricultural Sciences

In the late 1980s and 1990s there was increasing international interest in the development and use of synthetic wheat germplasms and their hybrid derivatives distributed by CIMMYT.Cultivar Chuanmai 42 was selected from such materials in Sichuan province by Dr.Wuyun Yang and colleagues at the Sichuan Academy of Agricultural Sciences,Chengdu on the basis of superior yield and stripe rust resistance.Sichuan is one of the most stripe rust-prone areas of China and resistance is an obligatory trait for variety release in that province.Once recognised as an outstanding rust resistant variety,Chuanmai 42 was grown widely and utilized as a parent in crossing programs.Genetic analysis revealed a single gene on chromosome 1B,temporarily named YrCH42,and once again located in the centromeric region[14].They also reported that YrCH42 was allelic with Yr24 and Yr26.In Table 1 of that paper there was a strong hint that a Pst isolate from Egypt might be virulent to all three putative genes as well as Yr10.The main reasons for persisting with a notion that three different Yr26/Yr24 alleles were involved were pedigree,reports of different linked markers associated with each source,and possibly the fact that Yr24 and Yr26 had been(erroneously)named as different genes.See also Box 3.

3.Race survey data from iinternational laboratories

3.1.The Avocet S story

An Avocet S near-isogenic line series developed in Australia by C.R.Wellings was widely distributed internationally for stripe rust research in conjunction with local research programs.Avocet was chosen for its widespread stripe rust susceptibility in many countries and environments,as well as day-length insensitivity and a facultative growth habit that made it sufficiently well adapted for autumn-sown field use in most wheat-growing regions worldwide,except for those environments with extremes in day-length or winter cold.It can also be spring-sown in the latter regions.The advantage of choosing Avocet was that it could be used for both greenhouse work with seedlings and for adult plant work in the field.Nevertheless,these advantages were accompanied by some problems as outlined below.Another vision for the Avocet lines was that they might be used to identify races in the field.A line with just one resistance gene will simply tell us whether a virulent race(or races)is present or absent at a particular field location.A limitation of the single gene lines is that they fail to determine race designations that are based on gene combinations.Characterization of a sample for the purpose of assigning a race designation requires a combination of virulences and avirulences on a number of host genotypes.Theoretically,lines(e.g.Avocet S and NILS)with all possible resistance gene combinations are required,but one vision is that lines with two-gene or three-gene combinations strategically chosen for different geographic areas will adequately achieve such an objective.Such lines are under construction at the Plant Breeding Institute,University of Sydney.On the other hand,the current rapid progress in DNA sequencing of pathogens and identification of specific effectors will likely achieve the same objectives before the relevant host gene combinations are widely deployed.

Box 3

Genes completely linked in repulsion should be assumed to be the same until shown to be different on the basis of function or sequence.Even at the sequence level it may be necessary to consider haplotype variation in combination with function.A common attitude among many scientists is that a newly detected resistance gene is a new resistance gene.The evidence provided is usually pedigree,which may not be correct due to human error in recording,errors in germplasm tracking,errors in crossing,and natural outcrossing during the breeding process.

Following widespread testing of the Avocet S NILs set we came to realise that a number of the lines carried Yr18,the adult plant pleiotropic resistance gene more commonly and historically known as Lr34.The lines carrying Yr18 include AvSYr1,AvSYr5,AvSYr10,AvSYr15,and some sources of AvSYr17 in addition to AvSYr18(P.Zhang,personal communication).The origin of the Yr18 adult plant resistance gene was due to its then unknown presence in the lines used as gene donors,some of which were breeding materials involving other putatively susceptible parents.The AvS NILs were produced in the absence of markers and resistant hybrid plants were sequentially backcrossed to Avocet S.It is now well known that Yr18 often enhances the low infection types associated with all-stage resistance and hence some lines were likely unknowingly selected for gene combinations including Yr18.Even in the presence of Yr18 in some lines the AvS NIL set has generated the types of results for which it was originally produced—to enable national(that is,Australia)and international use in providing a conduit for understanding global variability in Pst populations.

As with any set of materials based on a common genetic background a major problem for many laboratories is maintenance of genetic identity and purity of each line.Because such lines are morphologically very similar,human error in maintenance is difficult to detect,but in host:pathogen investigations the accuracy of deductions made when using the lines depends on the integrity of their true identity.One problem in many laboratories is a lack of adequate seed storage facilities and a need(or habit)to increase seed every year,increasing the likelihood of human errors during line multiplication and maintenance.A range of reliable and simple storage methods are now within reach of most researchers.These range from cool basements(viability for 3—5 years);domestic refrigerators(4 °C,10—15 years)and freezers(?20 °C,20+years).Prior to storage the seed must be dry,free of vermin,and sealed to prevent moisture uptake(e.g.plastic zip bags or aluminium foil pouches—common seed storage technology).With sufficient space large bulks from a single increase can be used as source materials;with lesser space smaller bulks can be maintained from which limited subsampling and one-year increases can serve as the working materials—the objective being to maintain the shortest route to the original source.When the entire AvS NIL set is grown at the same time two lines serve as checks—AvSYr8 is taller and later maturing due to linkage drag imposed by the alien segment containing Yr8;and AvSYr10 has brown chaff colour linked to Yr10 and inherited from the original PI 178383 source.The Avocet NIL set was distributed from the University of Sydney on more than one occasion.In one distribution,a 2007 source of AvSYr26 was a mixture of resistant and susceptible plants and subsequently caused problems in a Sichuan nursery when a decision on whether Yr24 and Yr26 applied to the same gene was critical.

Avocet S has repeatedly been shown to carry a weakly expressed QTL detectable in genetic studies[15].This is seen by transgressive segregation in hybrid populations.A further problem that has emerged in regard to advanced molecular research involving the Avocet NlLs is that Avocet S is genetically impure,a problem that confounds comparisons among lines within the set(C.Uauy,personal communication).This indicates that the original selected line was not derived from a single completely homozygous individual.Despite these drawbacks there are still many reasons to continue to build on the Avocet S base rather than start again only to find other small problems that will likely emerge.That is the nature of biological research.

4.One Yr24/Yr26 gene or more?

Gene location and molecular characterization of the materials described above gradually focussed on the centromeric region of chromosome 1B where other stripe rust resistance genes such as Yr15 and YrH52 were also located[16,17].Yr24 was phenotypically distinguishable from Yr15 on the basis of infection type(Fig.1)and Zakari et al.[18]obtained a recombinant line combining Yr15 and Yr24.Relatively little information is available for YrH52,but it was different from Yr15[17].Reporting of different markers associated with Yr24,Yr26 and YrCh42 led some researchers to believe that the genes were different or perhaps(by wishful thinking)alleles with different specificities;however,different linked markers in different germplasm,each with a different lineage,is not a reliable basis for gene identification(Box 4).

Box 4

Naming resistance genes in wheat:To name a potentially new rust resistance gene a proposal supported by the available evidence is considered by the wheat gene catalogue curators and peer researcher panels.The data includea gene description,pedigree,chromosome location,and where necessary,tests of allelism.Representative germplasm must be available in an internationally accessible gene bank.When Yr26 was named there was a presumption that it was located in the same 6AL.6VS chromosome as gene Pm21 for resistance to powdery mildew.No connection was made with the durum parent,or with the previously named Yr24.

The next and most convincing clue on gene identity came when it became evident that most Pst isolates with virulence to Yr10 in North America were also virulent to Yr24 and Yr26.This observation was followed by the occurrence of similarly combined virulences in Australia(race 150 E16 A+,accession 598,collection no.051877)and China(different V26 races known as V26-CH42 and V26-Gui22 and independently collected from Chuanmai 42 and Guinong 22).Australian race 150 E16 A+was collected in 2005 from a South Australian nursery that included a backcross derivative of Bindawarra carrying Yr10.This is the only Australian race and only isolate identified with virulence to Yr24/Yr26.Wheat varieties with Yr10 or Yr24 were not being cultivated in Australia at that time.In North America the races under discussion likely came from varieties carrying Yr10.

5.Why Yr10?

The near-universal feature that races virulent to Yr24/Yr26 are also virulent to Yr10 is worthy of detailed discussion.These genes are located in chromosome 1B;Yr24/Yr26 is in the centromeric region and Yr10 is very closely linked(2 cM or less)in coupling with Rg1 for red or brown glume colour and the gliadin locus Gli-B1[16,19,20].The AvSYr10 NIL and all varieties in commercial use with Yr10 have red/brown glume colour,but Bariana et al.[20]reported a T.vavilovii accession(AUS22498)that had Yr10 and white glume colour.There is no evidence that T.vavilovii has been used by wheat breeders as a source of stripe rust resistance.Clearly the Yr24/Yr26 and Yr10 genes are different.

Beginning with Watson[21]a preferred strategy for increasing the durability of rust resistance was to combine effective resistance genes that were not earlier widely deployed as single genes.This assumed that variation in rust pathogens was primarily the result of mutation in otherwise asexually reproducing pathogen populations as was the situation in Australia where the alternate host is not extant.With this strategy in mind,and given that a Yr15Yr24 recombinant was already available,McIntosh[unpublished]set out to pyramid these genes with Yr10 using:1)the highly resistant phenotype(IT 0)conferred by Yr15,2)a molecular marker allele(Xgwm11-1B190)that was introduced into the Yr15Yr24 parent with gene Yr24[18]and 3)the brown glume phenotype associated with Yr10.The occurrence of the mutant pathotype that overcame Yr24/Yr26 and Yr10 simultaneously put a quick stop to that effort.

There is increasing evidence that sexual reproduction in Pst on the alternate barberry host is occurring in the Himalayan Mountain region extending from Pakistan to southwestern China[22—24](Fig.2).If sexual recombination is a regular event then a strategy of gene combinations involving all-stage resistance genes,and very likely,at least some APR genes will be extremely difficult because it is well known that cereal rust pathogens are commonly heterozygous and that novel combinations of multiple avirulence(dominant)/virulence alleles can occur by gene re-assortment during sexual recombination.

Fig.2–(A)Barberry plants overhanging a wheat field near Baoji in Shaanxi province,China;(B)Aecia on a barberry leaf from the same location;(C)Stripe rust infections in the adjacent wheat field.That stripe rust could have been caused by aeciospores from the barberry,or independently by incoming urediniospores from other areas.Photographs by courtesy of Dr.J.Zhao.

Current theory in the study of host:pathogen genetics with particular regard to rust pathogens is that small secreted proteins(some of which may be the products of avirulence alleles)pass through the haustorial/plant membrane barriers into the host cytoplasm where they are specifically recognised and directly or indirectly by host receptors(resistance proteins)to trigger subsequent events that restrict further pathogen development to varying degrees.The result is a wide range of incompatibilities varying from virtual immunity involving necrosis of just a few cells at infection sites(e.g.Yr15)to larger necrotic lesions to small uredinia(e.g.Yr24/Yr26),and larger uredinia that are barely distinguishable from those that are considered to represent compatibility,pathogen virulence,or host susceptibility.One explanation for the co-incident Yr24/Yr26 and Yr10 virulences is that the same effector is recognised by two different host receptors;however,the phenotypic expression(infection type)associated with Yr10 is easily distinguished from that associated with Yr24/Yr26(Fig.1).Alternatively,AvrYr10 and AvrYr24/AvrYr26 could be tightly linked genes in the pathogen and are most commonly lost by deletion of both genes.These observations present a very interesting challenge for stripe rust research,or even for host:pathogen studies in general.Yr10 has been cloned[25];Yr24/Yr26 has not.

McIntosh[26]drew attention to a similar situation in relation to stem rust caused by Puccinia graminis f.sp.tririci(Pgt).Sr21 on chromosome 2A originated from the related AA genome species T.monococcum,and Sr45 on chromosome 1D originated from the DD genome species Ae.tauschii.A range of natural variants in Australia and the USA,and induced Pgt mutants of Australian races with virulence to Sr21 were each virulent to Sr45.After cloning of Sr45[27]it was shown that Sr45 and Sr21 were not the same gene(E.S.Lagudah,personal communication).In addition H.S.Bariana(personal communication)identified a Pgt isolate in the University of Sydney Pgt culture collection that distinguished the two genes.Nevertheless,the close association of combined virulences arising in natural and induced mutant variants,as well as prediction(and later actual evidence)that double virulences might be present in specific pathotypes begs further investigation.

6.Addressing virulence to Yr24/Yr26 in the field

Given the availability of races with contrasting pathogenicity to Yr24/Yr26 in China,including two that are virulent for Yr24/Yr26,it is possible to conduct seedling tests to identify lines that carry the gene.Many of the lines originated from institutes that were focusing heavily on using Chuanmai 42 and other CIMMYT synthetic derivatives,or Nanjing Pm21 materials,or Guinong 22and respective derivatives as crossing parents in their breeding programs.The next step is to test previously resistant cultivars and current breeding lines in nurseries with V26 races or at sites where V26 races are present in significant proportions.Given the wide range of adult plant resistance(APR)in wheat populations it is expected that not all varieties/lines with Yr24/Yr26 will be equally susceptible.Indeed some lines may have sufficient APR to allow continued evaluation and commercialisation(J.M.Mu unpublished).Excessively susceptible cultivars can be recommended for withdrawal from further recommendation.

7.Disease samples,pathogen isolates,races and storage

The general procedure in international cereal rust laboratories is to collect samples from the field by means of formal surveys undertaken by laboratory members,or by samples collected and sent to the laboratory by collaborators.Various types of information such as date of sampling,location(now possible with GPS co-ordinates),variety if known,and various other details documented with the samples will accurately identify sample collection details.Sample isolates are then made from collections.These can be derived from single urediniospores,single pustules,or they may be bulk isolates.Actual procedures will vary between laboratories based on local experience or projected use of such samples in future research.Race identification is normally conducted only on seedlings and is performed by testing the sampled isolates on sets of differential genotypes that may vary between different countries or geographic regions.Each genotype in a differential set usually,but not always,carries a single all-stage resistance gene.A race is therefore defined by its assessed avirulence or virulence on a chosen set of genetic materials.Isolates that are determined to be new or unique races are then permanently stored,and from time to time separate isolates of predominant races may be made and stored for future research.Because a race is defined by a fixed set of differentials at a point in time,and any variation in pathogenicity to genes not included in the differential set is not documented,different isolates with the same race designation may vary in location and time.This will be even more important in areas where an alternate host is implicated as a source of variation.For example,Wang et al.[24]identified race CYR32 in aecial progenies from barberry.If sexual reproduction is a common event it will be difficult to distinguish clonal and sexual derivatives and much greater within-race variation will be expected over time and space.Hence for host genetic studies and inoculated nurseries where inoculum is obtained from source pathology laboratories on an annual basis the actual isolate identity of races should be clearly identified.Such information is not currently evident in published information from some countries.With the increasing application of molecular biology and genomics to pathogens and pathogen populations the availability of well documented historic culture collections of the pathogen(as urediniospores)is equally as valuable as a well documented host collection(usually in the form of seed)as should be predictable by the gene-for-gene model.

8.Future projections and conclusions

This paper is a retrospective view of several significant events in wheat stripe rust research and is a reminder of how resistance genes can be mis-identified and become overexploited in breeding.Other examples can be obtained from the international literature and pathologists and breeders must be made aware of the potential vulnerabilities of individual resistance sources,especially in regard to the possibility of the same gene being present in putatively unrelated resistance sources.The problem can be minimised by increased genetic diversity and greater collaboration between researchers both nationally and internationally.This will be possible only with exchange of genetic resources and information.

Acknowledgments

RAM acknowledges many helpful discussions and the kind hospitality of several Chinese institutions and many scientists during numerous visits.The information assembled here would not be possible without those visits.Valuable suggestions on drafts of the manuscript from Gordon Cisar,Jeff Ellis,Robert Park,Qinlin Wang,Colin Wellings,Jianhui Wu,and Jie Zhao,were greatly appreciated.

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