Breeding wheat for resistance to biotic stresses

Please indicate author’s corrections in blue, setting errors in red

154720 EUPH Ordernummer 208284

19Euphytica 100: 19–34, 1998. 1998 Kluwer Academic Publishers. Printed in the Netherlands.

Breeding wheat for resistance to biotic stresses

R.A. McIntoshUniversity of Sydney, Plant Breeding Institute Cobbitty, Private Bag 11, Camden, NSW 2570, Australia

Summary

Although common wheat and durum may be attacked by a large number of diseases and pests, less than 20diseases and about five insect or mite pests are of major significance. Some of these have a global distributionand occur in most wheat-growing areas, whereas others are restricted to certain geographic regions or climaticzones. A small group of diseases and pests, such as Karnal bunt and Russian wheat aphid, are a major threat tocountries and regions in which they are absent. Although there is genetic variation in response to most dis-eases and pests, resources available to national programs limit the number that can be included as breedingobjectives. Ideal sources of resistance are those present in closely related, commercial genotypes, but caremust be exercised to avoid genetic uniformity. Any effort to transfer resistance from related species andgenera should be considered long term. The chance of successful exploitation of resistance based on aliengenetic material declines with reducing genetic relatedness between recipient and donor species. Breedersmust maintain an awareness of potential problems associated with very high levels of resistance controlled bysingle genes. Lower levels of resistance with established durability or resistance based on a number of genesmay be preferred. In many situations, resistance with moderate to low effectiveness will contribute signif-icantly to crop protection. Unusually susceptible genotypes should be avoided irrespective of perceived riskbased on local surveys. Molecular and other markers for genes of interest are having an increasing role in theselection process. Although genetic engineering in wheat is in its infancy, significant contributions to diseaseresistance, starting with virus resistances, can be expected.

Introduction

Common wheat (Triticum aestivum L.) and durum(T. turgidum L.) are vulnerable to attack by manydifferent pathogens and pests (Jones & Clifford1983; Hatchett et al., 1987; Shaner, 1987; Wiese,1987; Zillinsky, 1983). Some of these pathogens andpests have a broad range of occurrence whereasothers may be very localised; some are extremelydamaging to crop production whereas others causerelatively little damage despite widespread occur-rence. To fulfil its global mandate for wheat im-provement, CIMMYT has directed attention to ar-eas of similar environments, mega-environments(ME). Rajaram (1994a) and Rajaram & van Ginkel(1996) summarised the main biotic stresses that cen-tre on each of the 12 MEs. They exemplified about

12 fungal diseases, one virus and three insect pestsas important. Allowing for a few more, such as thefoot rot fungi and nematodes that might be includedunder ‘soil pathogens’ relating to ME12 (i.e., thesemi-arid zones of northern Great Plains USA,Eastern Europe and extending from Turkey to Af-ghanistan) this number totals about 20.

The various diseases caused by fungi, viruses,bacteria, nematodes, insects and mites consideredimportant by the present author are listed in Tables1 to 5 and most are briefly discussed in the followingnotes. All of the biotic stresses mentioned by Raj-aram (1994a) and Rajaram & van Ginkel (1996), ex-cept Sclerotium rolfsii, are included.



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Table 1. Some fungal diseases of wheat

Common name Organism Regions of importance Resistance

Availability Type1

Alternaria leaf blight Alternaria triticina Prasada & Prabhu India Yes MBlack point = kernel smudge Bipolaris sorokiniana (Sacc. in Sorok.) North America, Australia, India Yes –

Alternaria tenuis, many others Yes –Cephalosporium stripe Cephalosporium gramineum Nisikado & Ikata North America Yes –Common root rot Bipolaris sorokiniana (Sacc. in Sorok.) Widespread, semi-arid Yes ACrown rot Fusarium graminearum Widespread Yes A

Schwabe Group IFusarium culmorum(W.G. Smith) Sacc.Fusarium avenaceum (Fr.) SaccFusarium spp.Microdochium (F.) nivale

Eyespot = Strawbreaker footrot Pseudocercosporella High rainfall Yes Mherpotrichoides (Fran)Deighton

Helminthosporium leaf blight Bipolaris sorokiniana Warm areas, South America, Yes A= Spot blotch (Sacc. in Sorok.) south AsiaPowdery mildew Erysiphe graminis DC f. sp. Widespread, high rainfall Yes M,A

tritici E. MarchalRhizoctonia root rot Rhizoctonia solani Kuhn Australia, Europe, South No –

Africa, USA northwestRusts

Leaf rust Puccinia recondita Rob. ex Desm. f. sp. tritici Widespread, high rainfall Yes M,AStem rust Puccinia graminis Pers. f. sp. tritici Widespread, high rainfall/warm Yes MStripe rust Puccinia striiformis West. f. sp. tritici Widespread, high rainfall/cool Yes M,A

Scab = Fusarium head blight Fusarium graminearum Widespread, high rainfall Yes ASchwabe Group 2Fusarium culmorum (W.G. Smith) Sacc. EuropeFusarium avenaceum (Fr.) Sacc. EuropeFusarium spp.

SmutsCommon bunt Tilletia caries (DC) Tul. Semi arid regions, West Asia, Yes M

Tilletia laevis Kuhn USA northwestDwarf bunt Tilletia controversa Kuhn Cooler areas of West Africa, Yes M

USA northwestFlag smut Urocystis agropyri (Preuss) Semi arid, Australia, USA Yes A

Schroet northwest, WANAKarnal bunt Tilletia indica Mitra Indian subcontinent, North America Yes M,ALoose smut Ustilago tritici (Pers.) Rostr. Semi arid Yes M

SeptoriasSeptoria nodorum blotch Leptosphaeria nodorum E. Muller Widespread, moist Yes ASeptoria tritici blotch Mycosphaerella graminicola Widespread, moist Yes M,A

(Fukel) J. Schrot. in CohnSharp eyespot Rhizoctonia cerealis Van Hoeven Europe, North America No –Take-all Gaeumannomyces graminis Widespread, dry No –

(Sacc.) Arx & D. Olivier var. triticiTan (yellow) spot Pyrenophora tritici-repentis (Died.) Drechs. Widespread, moist Yes M

1 Arbitrarily classified major gene or additive.



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Table 2. Some viral diseases of wheat

Name Region of importance Resistance

Availability Type2

Barley yellow dwarf virus Widespread Yes MSoil-borne mosaic virus Widespread Yes MWheat streak mosaic virus Europe, North America Yes MWheat spindle streak mosaic virus North America Yes MWheat yellow mosaic virus Widespread Yes M


Major biotic stresses of wheat

Fungal diseasesAlternaria leaf blight. This serious leaf spot andseed-borne disease is restricted to certain cultivarsgrown in India and is readily controlled by resistantcultivars.

Black point. Caused by a number of pathogens, in-cluding B. sorokiniana and A. tenuis, this disease in-volves the infection, spread and discoloration ofwheat kernels from the embryo end leading to re-duced industrial quality. The disease tends to bemore important in durums.

Cephalosporium stripe. This soil-borne vasculardisease seems to be favoured by low temperature,moist soils of low pH. Outbreaks are most commonin the Pacific northwest states of the USA.

Common root rot. Common root rot is a frequentlyencountered soil-borne disease of wheat and barleyin dry temperate regions. Both simple and complexgenetic control of resistance have been reported(Johnson & Lupton, 1987). Larson & Atkinson(1981, 1982) located a single recessive gene on chro-mosome 5BS. Johnson & Lupton (1987) pointed outthat despite the availability of resistance sources,relatively little progress had been made in breedingfor resistance.

Crown rot, foot rot and seedling blight caused by Fu-sarium spp. Crown rot and foot rot caused by spe-cies of the Fusarium complex are among the mostwidespread of wheat diseases (Nelson et al., 1981).

Seedling blights probably result from seed-borneinoculum, whereas the crown and foot rots resultmore commonly from soil-borne sources. Symp-toms are expressed by the phenomenon of ‘whiteheads’ which become evident with moisture stress.

No cultivar is immune, but cultivaral differenceshave been reported. It is unknown if the same rela-tive resistance/tolerance levels apply over the vari-ous pathogen species. There seems to be no geneticrelationship between resistance/tolerance to crownrot and resistance to head scab caused by the samepathogens. Durums are reputed to be more suscep-tible than common wheats.

Eyespot or strawbreaker foot rot. Occurs in westernEurope, and northwest USA and Great Lakes re-gions. Resistance has been documented in theFrench cultivars Cappelle Desprez and VPM1, a de-rivative of Aegilops ventricosa. This latter resist-ance is present in the UK cultivar Rendezvous andthe USA Pacific northwest cultivars Madsen andHyak.

Helminthosporium leaf blight (HLB) or spot blotch.HLB can be a significant splash-dispersed diseasein south Asia and certain sub-tropical areas, espe-cially those with rice:wheat rotations. In more tem-perate regions however, the same pathogen specieswith a wide host range causes common root rot ofwheat and barley. Severe epidemics of HLB resultin widespread necrosis of the upper crop canopyleading to significant losses with spread to the headand seed. Pathogen isolates from wheat tend to bemore adapted on wheat than on barley (G. Platz &R. Rees, personal communication). Sources of re-



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Table 3. Some bacterial diseases of wheat

Name Organism Region of importance Resistance

Availability Type3

Bacterial stripe = Xanthomonas campestris Eastern Europe, North Yes Mbacterial leaf streak pv. translucens (J.J. & R.) Dye America, South America,= black chaff WANABacterial leaf blight Pseudomonas syringae pv. North America Yes –

syringae Van HallBasal glume rot Pseudomonas syringae pv. Eastern Europe, Yes –

atrofaciens (McCullock) Syria, UkraineYoung et al.

Spike blight = tundu Corynebacterium tritici (ex China, India, WANA – –Huchinson) Carlson & Vidaver


sistance are available among wheats from Brazil,China and Zambia.

Powdery mildew. This disease occurs very widelythroughout wheat-growing areas of the world and ismost damaging in cooler moister regions such asChina, Europe, South America, southeast USA andsome WANA (West Asia and North Africa) coun-tries. It is haploid, and regular sexual recombina-tion provides a mechanism for genetic recombina-tion.

Although controlled by resistant cultivars, mostwell catalogued single gene sources of resistancehave been overcome by virulent pathotypes. Var-ying levels of adult plant resistance are readily rec-ognised and at least some of these are considered tobe durable (Roberts & Caldwell, 1970; Shaner &Finney, 1977). A breeding strategy aimed at theavoidance of highly susceptible genotypes may beas effective as one aimed at complete resistancebased on genes conferring non-durable resistance.

Powdery mildew has increased in incidence andseverity in South America following the breakdownin resistance conferred by Pm8. Attempts werethen made to exploit resistance conferred by Pm6and Pm17, to incorporate resistances from emmersand Haynaldia villosa, and to use slow mildewingsources (Kohli, 1994).

Rusts. The rust diseases are not only among themost important of wheat diseases, but they are also

the diseases that have attracted the most attentionand about which there is most knowledge. Whilerust diseases are readily controlled by resistant cul-tivars, virulent pathotypes are a constant threat.Much of the research effort is directed at identifyingand utilising sources of resistance that are consid-ered to be durable (Simmonds & Rajaram, 1988).Stem (black) rust tends to occur in the warmer,moister regions, whereas stripe (yellow) rust occursin cooler regions. Leaf (brown) rust occurs in allwheat-growing areas with moister climates. Most ofthe documented genes for resistance to rusts, andsome known but not formally documented are de-scribed in McIntosh et al. (1995b).

Stem rust. Probably the most damaging disease ofwheat, stem rust has been largely controlled by ear-lier maturing genotypes and resistance based onsingle genes with established durability, e.g., Sr2,Sr26, Sr31, or gene combinations involving two toseveral resistance genes.

Leaf rust is currently considered the most impor-tant rust disease worldwide. Durable resistancesources are available and, among them, the geneLr34 is probably best known. Singh & Rajaram(1994) identified a number of wheats with combina-tions of adult plant resistance genes which individu-ally contribute to relatively low levels of resistance.These were considered to be potentially durablebecause of their wide effectiveness and the need for



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Table 4. Some nematodes of wheat

Name Organism Region of Importance Resistance

Availability Type4

Cereal cyst nematode Heterodera avenae Woll. Widespread Yes MRoot knot nematode Meloidogyne naasi Frank. Europe, WANA Yes MRoot lesion nematode Pratylenchus neglectus Australia, west Asia, Yes M

(Rensch.) Filip North America,Pratylenchus thornei North AfricaSher & Allen

Seed gall nematode Anguina tritici (Steinb.) Chit. West Asia, south Asia Yes –


the pathogen to undergo several mutational chang-es to overcome them.

Stripe rust continues to be a problem in coolerwheat-growing areas at high elevation or higher lat-itudes. Recent epidemics in areas sown to the pop-ular Mexican cultivar Seri 82 and its derivatives insouth and west Asia have required changes in culti-vars. Considerable variation in disease response isavailable in common wheats, and effective levels ofpotentially durable resistance based on adult plantresistance genes with additive effects are easily pro-duced. The adult plant resistance gene Yr18 is com-pletely associated with Lr34 and is present in a widearray of wheats selected for both leaf rust and striperust resistances. As with Lr34, Yr18 alone may pro-vide inadequate protection in rust-prone regionsand needs to be combined with other resistancegenes to provide increased resistance.

Scab/Fusarium head blight. Scab is a widespreadproblem in humid growing areas of North Amer-ica, China, central and Eastern Europe and SouthAmerica. Mesterhazy (1984) identified 17 speciesamong 4024 Fusarium isolates, the predominanttypes being F. graminearum (59%) and F. culmo-rum (26%). In North America and Europe, F. gra-minearum Group 2 is also a pathogen of maize, butin China the species survives on rice stubbles with-out being an active pathogen of rice. Mesterhazy(1995) reviewed various types of resistance and de-fined an ideotype that would best display featuresof resistance, viz. a plant which is 90-100 cm tall,

awnless and with a peduncle of 15 cm in length. Heagreed with others that the cultivars Nobeoka Bo-zu, Beijing 8 and Sumai-3 represented good sourc-es of resistance. Standard screening tests based onartificial point inoculations of spikes and visualevaluations of spread are now widely used. It is pre-sumed that the best sources of resistance provideprotection to a range of the important pathogenspecies. Wilcoxson et al. (1992) found that the Chi-nese wheats did not produce resistance levels supe-rior to the most resistant USA wheats, but conclud-ed they may provide even better levels when com-bined. Snijders (1990a, 1990b) reported on the ge-netics of resistance to scab caused by F. culmorum,but the genotypes he used as parents had no obvi-ous relationships with those studied in NorthAmerica. The results of Buerstmayr et al. (1996)and Vassilev (1996) indicate that the same resist-ance sources give protection to both F. culmorumand F. graminearum. Durum was noted as highlysusceptible to scab in South America (Kohli et al.,1992).

Septoria nodorum blotch. This stubble-borne andseed-borne, splash-dispersed disease has a largelyoverlapping occurrence with septoria tritici blotch(STB) and can be extremely damaging because, un-like STB, it also affects the spike tissues and therebyprobably competes more actively for photosyn-thates. Most studies have shown that resistance isquantitatively based, but Lewis et al. (1996) report-ed a single gene for resistance in chromosome 5D ofa synthetic wheat. Rajaram (1994b) suggested that



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Table 5. Some insect and mite pests of wheat

Name Organism Region of importance Resistance

Availability Type5

AphidsCorn leaf aphid Rhopalosiphum maidis (Fitch) Asia, USA south – –English grain Sitobion avenae (F.) Europe, Americas Yes –Aphid Sitobion miscenthi (Takahashi) Australia, ChinaGreenbug Schizaphis graminum (Rondani) Eastern Europe, South Yes M

America, USAOat bird cherry aphid Rhopalosiphum padi (L.) Europe, Americas – –Rose wheat aphid Metapolophium dirhodum Europe, South America – –

(Walker)Russian wheat aphid Diuraphis noxia (Mordvilko) South Africa, North Yes M

Africa, North AmericaCereal leaf beetle Oulema melanopus (L.) Asia, Europe, USA Yes M

northeastHessian fly Mayetiola destructor (Say) North Africa, USA Yes MMites

Brown wheat mite Petrobia latens (Muller) USA north – –Wheat curl mite Eriophes tulipae Keifer North America Yes M

Eriophes tosichella Keifer EuropeSawflies

Black grain stem sawfly Trachelus tabidus (F.) Europe, USA east Yes AEuropean wheatstem sawfly

Cephus pigmaeus (L.) Europe, USA east Yes A

Wheat stem sawfly Cephus cinctus Norton North America, WANA Yes ASunni (Sunn) pest Eurygaster integriceps Puton Eastern Europe, WANA – –


useful levels of resistance were present in CIM-MYT germplasm.

Septoria tritici blotch. This stubble-borne splash-dispersed disease has a widespread occurrenceworldwide. Despite demonstration of pathogenicvariation in the pathogen (e.g., Eyal et al., 1973; Gil-christ, 1994; Kema et al., 1996), there are a few re-ports of dramatic cases of break-down in resistance(Kema et al., 1996). Kema et al. (1996) also providedevidence for greater differences between isolatesfrom common wheat and durum than between iso-lates from genotypes within either group. Cunfer(Shaner, 1987) considered quantitative resistanceand tolerance to be the most important means ofachieving protection from this disease. Gilchrist(1994) reported high levels of resistance to STB inemmer wheats.

Smuts. With the exception of Karnal bunt, the seedand soil-borne smuts have been controlled for manyyears by seed steeping and pickling, initially withheavy metal fungicides and hexachlorobenzeneand, more recently, with systemic fungicides. How-ever, use of these procedures is more difficult in de-veloping countries, and in developed countries theprocedures are coming under scrutiny due to in-creased incidence of resistance to systemic chemi-cals in micro-organisms and the trend towards re-duced use of agrochemicals. Sources of resistance toeach of the smut diseases are available but seldomexploited because additional breeding objectivesimpose further constraints to breeding success.

Common bunt (stinking smut) is a soil- and seed-borne disease, common in drier environmentsthroughout south Asia and the WANA region. A



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number of resistance genes have been describedand pathogenic variation is common.

Dwarf bunt, which shares many features with com-mon bunt, occurs in cooler wheat-growing areas ofthe USA Pacific northwest and higher altitude ar-eas of central and west Asia. Some sources of resist-ance effective against common bunt provide pro-tection against dwarf bunt.

Flagsmut is a seed and soil-borne leaf smut found indryland farming areas of Australia, south Asia,WANA and the USA Pacific northwest. Flagsmutcan be controlled with resistance conferred by addi-tive genes, but is seldom thought to be sufficientlyimportant to justify resistance breeding.

Karnal bunt. With recent reports of Karnal bunt(KB) at several locations in the USA, this diseasewill take a higher profile in other countries, espe-cially those with a major dependence on interna-tional wheat trade. Although KB does not pose amajor threat to yield and quality, tolerance levelsfor international trade are fixed at zero (Brennan etal., 1990). Karnal bunt is a soil-borne, seed-borneand possibly air-borne disease with a life cycle thatshares features with a number of smuts and ergot.Using a booted spike injection procedure first de-veloped in India by Aujla et al. (1980), pathologistsat CIMMYT, Mexico, reported several examples ofsingle gene and duplicate gene control of resistancerelative to the highly susceptible cultivar WL711(Morgounov et al., 1994; Singh, 1994). Six non-allel-ic genes for resistance were catalogued by Morgou-nov et al. (1994). Durum wheats are consistentlymore resistant than hexaploids under field condi-tions and some synthetics have shown immunity(Singh, 1994; Villareal, 1994).

Karnal bunt occurs in Mexico, India, Nepal, Pa-kistan and possibly Iraq. Suggestions of its presencein Syria, Lebanon and Turkey by Zillinsky (1983)seem to be unconfirmed. The problem of KB on theIndian subcontinent was probably exacerbated bywidely grown, very susceptible cultivars such asWL711. Given the principle that disease problemsarise as much from unanticipated extreme levels ofsusceptibility of widely grown cultivars as they do

from lack of resistance, it would be of interest fortrading countries, such as Australia, to obtain a pro-file of KB responses for all recommended and wide-ly used cultivars; so that those with extreme suscep-tibility can be identified and discouraged from useeither before or following breaches of quarantine.Such information and measures will allow assess-ment of potential risk and could firstly, reduce therate of spread if the disease is introduced and sec-ondly, would enable easier achievement of any tol-erance levels that may be specified for internationaltrade. To get useful response information, nationalprograms will depend on collaboration with labora-tories in countries that already have the disease. Anassumption of such work would be that there is min-imal pathogenic variation.

Loose smut is a flower infecting, seed-borne smutwhich is widely distributed in wheat-growing areasand considered to be important in south Asia andsome countries of the WANA region. High levels ofresistance are available but the organism is patho-genically variable.

Take-all. A soil-borne crown and root disease ofworld-wide significance, take-all has not been con-trolled with resistant cultivars.

Tan (yellow) spot. Tan spot is a stubble-borne,splash-dispersed disease. Its incidence and distri-bution has increased with recent trends in usingstubble retention as a means of reducing soil deg-radation in countries such as the USA and Austra-lia. However in some regions such as Nepal, tanspot can be a significant problem, even when allstraw is removed from cropping areas (J. Dubin,personal communication). In these circumstancesreservoirs of inoculum presumably survive ingrasses.

Four ‘pathotypes’ of Pyrenophora tritici-repentiswere distinguished by their ability to produce a ne-crotic response on cultivar Glenlea (due to a host-specific toxin) or a chlorotic response on line6B363. Pathotype 3 (nec- chl+) had been isolatedonly once in Canada and came from a durum. Astudy (Lamari et al., 1995) of 39 isolates from durumgrown in Algeria yielded only pathotype 3-like iso-



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lates but the disease levels on 6B363 and cultivarNeepawa were reversed.

Control of tan spot can be achieved by breedingusing seedling screening and selection techniques.Resistance is quantitative and relative and may beovercome with long periods of moisture. The impli-cations for pathogenic variation in the pathogen re-quire further study. Kohli (1994) noted that somewheats such as Milan, are resistant to STB as well astan spot.

Other fungal diseases. A number of minor fungaldiseases are reviewed by Cunfer (Shaner, 1987).

Viral diseasesBarley yellow dwarf (BYDV). BYDV is one of themost widespread and most damaging diseases ofwheat. The BYDVs – several serologically differentluteoviruses (Lister & Ranieri, 1995) – are transmit-ted by at least 23 species of aphids and infect morethan 80 grass species (Brakke, 1987). Combinationsof viruses, vectors and grass hosts allow for a greatcomplexity of specificities, even before individualwheat cultivars are considered. The most importantvectors include several species of Sitobion, notablyS. avenae, Rhopalosiphum padi and Metapolophi-um dirhodum.

The disease symptoms of yellowing and dwarfingare not as highly expressed in wheat compared toother cereals such as oats and barley, but breedingfor resistance, and especially tolerance, is largelybased on differences in symptom development infield nurseries where emphasis is given to lack ofsymptoms, ‘slow yellowing’ and ‘stay-green’ char-acteristics (Burnett et al., 1995). Burnett et al.(1995) reviewed a host response scale and outlinedfeatures of nursery management to enhance oppor-tunities of selecting for reduced BYDV losses.Sources of resistance/tolerance were also de-scribed. The most widely distributed source is theBdv1 gene which is closely linked with Lr34/Yr18 inchromosome 7D (Singh et al., 1993), but this sourceis reported to be ineffective in China.

A number of Agropyron spp. are resistant toBYDV, and various resistant partial amphiploidsand wheat alien addition lines have been produced(Larkin et al., 1995; Sharma et al., 1995). Banks et al.

(1995) described several alien translocation linesproduced by homoeologous chromosome pairingand cell culture that involved a 7Ag chromosomefrom Agropyrum intermedium. Most of these trans-locations involved exchanges with wheat chromo-some 7D (Hohmann et al., 1996). These are current-ly being used in breeding programs in Australia,China and Mexico. Other alien wheat addition lineswith resistance from the same source species havebeen identified, viz. 2Ag (Banks et al., 1995) and adifferent 7Ag chromosome (Sharma et al., 1995).An advantage of these sources is that they provideresistance to increases in virus particles withinplants and therefore can be monitored by serolog-ical assays. When a suitable transformation systemis available for wheat, concerted attempts to genet-ically engineer resistance to BYDV can be expected(Miller & Young, 1995).

Soil-borne wheat mosaic virus. This sometimes seri-ous disease of winter wheat in Europe, Japan andUSA is vectored by the fungus Polymyxa graminiswhich infects wheat roots, but is not a damagingpathogen. Effective resistance is not available inwheat, but has been identified in related species.

Wheat yellow mosaic virus. Also vectored by P. gra-minis, WYMV has been reported in Canada,France, India, Japan and the USA (Brakke, 1987).This disease can be readily controlled by resistantcultivars.

Wheat spindle streak mosaic virus. WSSMV is con-sidered to be a North American variant of WYMV.

Wheat streak mosaic virus. WSMV is vectored bythe eriophyid mite Eriophyes tulipae in NorthAmerica and France and by E. tosichella in Yugos-lavia (Brakke, 1987).

Bacterial diseasesBacterial stripe. Bacterial stripe is an importantdisease in North America, South America andWANA. Tesemma & Mitiku (1992) especiallymention that bacterial stripe is mostly prevalenton ‘wheat varieties’ (durums?) of Mexican originand that Ethiopian durum landraces are almost



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immune. Five genes for resistance in commonwheats were named by Duveiller et al. (1993). Du-rums were noted as susceptible in Brazil (Kohli etal., 1992).

Bacterial leaf blight. This disease, which follows pe-riods of heavy driving rainfall, has been reportedfrom northern USA and Canada.

Basal glume rot. BGR is considered an importantdisease in eastern Europe and the Ukraine. Prior to1940 it was important in Canada, but is now con-trolled presumably with resistance (Shaner, 1987).

Spike blight (tundu). This disease, usually associat-ed with the gall nematode Anguina tritici with whichit is transmitted, is a major problem in India.

Nematode diseasesMany nematode-infested soils, especially in devel-oping countries, are still being identified due to lackof adequate surveys. Crop protection is achieved byresistance or tolerance. Tolerant genotypes conferno benefits in reducing nematode populations.

Root lesion nematode. Symptoms caused by root le-sion nematodes include yellowing and unthriftin-ess, which are symptoms often associated withother diseases. Areas infested with Pratylenchusspp. are often identified by the superior relativeperformance of barley compared with wheat and byreduced symptoms of wheat genotypes known to beresistant or tolerant.

Cereal cyst nematode. CCN is a recognised problemin parts of Europe, WANA and southern Australia,but is likely to occur over much wider areas. All ce-reals are affected. Resistance is available and somebiotype variability has been identified. In additionto gene Cre1 in chromosome 2B of wheat cv. Loros,a second gene (Cre2) was identified in an Aegilopsventricosa derivative and a third gene (Cre3 in chro-mosome 2D) was described in an amphiploid in-volving Triticum tauschii. Braun (1994) suggested arelationship between the incidence of CCN andzinc deficiency.

Insect and mite pestsAphids. More than 30 species of aphid can coloniseand cause damage to growing wheat crops. Moreimportantly, several of the species most importantto wheat are vectors of BYDV. Greenbug and Rus-sian wheat aphid are most damaging to crops be-cause they secrete toxins which affect plant growth.

English grain aphid. Yield losses due to this aphidare associated mainly with spike infestations. Lowlevels of resistance were reported by Lowe (1983).Cultivars with leaf pubescence are resistant (Hatch-ett et al., 1987).

Greenbugs are reported to cause more damage inrelation to insect numbers than most of the otheraphid species. There are many biotypes of this in-sect specialised to both crops and to cultivars withincrops. A number of sources of resistance have beenused to control greenbug (Hatchett et al., 1987).

Oat bird cherry aphid is one of the most effectivevectors of BYDV. Cultivars with leaf pubescenceare resistant (Hatchett et al., 1987).

Russian wheat aphid. Described originally in Rus-sia, this aphid emerged as a serious pest in SouthAfrica in 1978. Following its discovery in Mexico in1980, RWA has become a serious pest throughoutNorth America and there has been an increasingawareness of its presence in southern and centralEurope, north and east Africa, south Asia andSouth America. Australia is considered highly vul-nerable to damage if the aphid is introduced(Hughes & Maywald, 1990). Barley and durum arealso highly vulnerable to this pest, whereas rye andtriticale tend to be more resistant (Burnett et al.,1991).

Resistance is available in common wheats fromIran, Russia and Turkey, certain accessions of T. di-coccum and various related species, but durum isconsidered highly susceptible (Burnett et al., 1991).Six genes for resistance have been catalogued(McIntosh et al., 1995a; Fuentes-Davila et al., 1995).

Cereal leaf beetle. This pest can be controlled withpubescent leafed cultivars (Webster et al., 1982), an



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example of antixenosis. However, pubescent leavesmay lead to higher incidences of leaf curl mites andWSMV.

Hessian fly. Infestation by the larvae of this gall-midge can be highly destructive. Although readilycontrolled by resistant cultivars, the high rate atwhich new biotypes emerge matches the rusts andpowdery mildew diseases. Twenty six genes havebeen designated (McIntosh et al., 1995a; Cox &Hatchett, 1994), of which several occur in chromo-some 5A (Ohm et al., 1995).

Mites. Brown wheat mite. Infestation of this mitecan lead to plant damage in northern USA from Ne-braska to Utah.

Wheat curl mite. Not particularly damaging itself,this mite is more important as a vector of wheatstreak mosaic virus. Sources of resistance are avail-able in species closely related to wheat.

Sawflies. These insects are best controlled using cul-tivars with solid stems, especially the lower inter-nodes, although stem solidness is probably not theonly mechanism of resistance (Nachit, 1994).

Breeding for resistance

Identifying the important diseases and pestsNational breeding programs of limited size will usu-ally need to prioritise the essential objectives oftheir programs along with certain non-essential, butadvantageous, targets that might be achieved. Eachadded objective (trait or gene) reduces the numberof potential genotypes that can be selected within afixed population. The particular diseases or pests tobe targeted will be determined by recent events,personal opinion, data from surveys of disease/pestincidence and severity and crop loss assessments.Changes in agronomic practices and cultivars overtime can have a significant influence on diseasesand pests. For example, the move to shorter geno-types was followed by increased levels of diseasescaused by splash-dispersed pathogens and crop re-sidue retention on the soil surface as a soil conserva-

tion measure led to increased incidence and sever-ity of crown rot, the septorias and tan spot. In-creased levels of a particular disease/pest may beassociated with the widespread cultivation of a cul-tivar with previously unrecognised extreme suscep-tibility in a region where that disease or pest waspreviously given a lower priority. Finally, a new dis-ease/pest (pathotype/biotype) may evolve or be in-troduced. Each of these factors can influence the di-rection and rate of progress of breeding programs.

Each disease/pest will require unique selectionapproaches based on the level of knowledge of theparticular pathogen/pest, its life cycle, and the avail-ability and heritability of resistance. The breeder ofrust resistance can choose among single genes, oli-gogenic resistance or partial (call it what you will)resistance because of the wealth of knowledge andexperience available for the rusts; the breeder ofcrown rot resistance will proceed with the bestavailable sources on an empirical ‘suck it and see’approach.

With the increased global movement of grain(both commercial product and germplasm) and ofpeople (both agricultural and non-agricultural) inrecent years and the associated risk of breeches ofquarantine, there has been an increasing need forbreeders to undertake anticipatory action in orderto be able to respond more rapidly to new threats.For example, Russian wheat aphid and Karnalbunt are potential threats to the Australian wheatindustry. Both are currently absent from that coun-try, but the likelihood of susceptible cultivars and afavourable environment indicate major problemsif either is introduced. To prepare for such threats,the national programs need to undertake researchin a locally established quarantine facility, conductresearch in countries where the pathogen/pest isalready present or contract foreign researchers toproduce the type of germplasm that might be re-quired at the time of introduction. Clearly, interna-tional centres can contribute to such activities.

Sources of resistanceThe raw materials required by breeders are thegermplasm sources carrying the resistance genesthat will confer protection to the level required bythe prevailing production system. Where high lev-



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els of resistance are not available, the raw materialsrequired are those that confer protection resultingin losses lower than those which occurred with pre-existing cultivars. For some diseases/pests, thosegenes will be present in local cultivars or in exoticcultivars of similar phenology and quality; forothers there will be a need to use different types ofwheats as parents; for yet others, related speciesmay be the only sources of satisfactory levels of re-sistance. As one moves away from local germplasm,the probability of successful transfer will decreaseand the time needed to execute the process will in-crease. Transfer of resistances from related specieswhose chromosomes are not homologous withthose of common wheat must not only be consid-ered long term endeavours, but the likelihood ofsuccess will be relatively small. Very few ‘successful’alien transfers (Friebe et al., 1996) have made signif-icant contributions in international agriculture, de-spite the considerable investment in wide crossingand chromosome engineering. Part of this is due toa continuing gap between the scientists involved inthe transfer process and the conventional breeder.

Defining a tolerable level of resistanceAcute disease and pest problems may be associatedwith rapid changes in agronomic practice, release ofone or more widely accepted but ultra-susceptiblecultivars, the introduction of new pathogen or pestspecies from outside the zone of interest or with theintroduction or evolution and increase of new path-otypes/biotypes. There are numerous examples ofeach of these types of change. A further, but not soreadily recognised problem, is chronic disease orpest infestations that go unnoticed because they areaccepted as part of the environment. Many of thebelow soil level problems fall into this category. Insuch situations, farmers accept generally low yieldlevels or disband wheat cultivation in favour ofother crops. There may also be a relationship be-tween the biotic and non-biotic constraints to pro-duction. Braun (1994) drew attention to the likeli-hood that wheat grown under zinc deficient condi-tions could be more pre-disposed to crown rot, rhi-zoctonia foot rot and cereal cyst nematode, usingthe Anatolian Plateau of Turkey as an example. Ifthis is confirmed, then amelioration of soil zinc lev-

els could significantly reduce the breeding effort re-quired to control the biological threats.

There is variability in host response to most dis-eases and pests of wheat. However, depending onthe particular disease or pest, the response rangemay be narrow or vary widely from early death toapparent immunity. With a narrow range of host re-sponse, experience or sophisticated tests may be re-quired to detect differences. The constraints ofmost breeding programs are such that resistancewill be sought only if selection is simple, reliable andcheap, preferably requiring only a single observa-tion. Selection will be easier when there is a widerange in response.

As shown by many researchers, very high levelsof resistance may not be necessary to prevent mostof the potential losses. Indeed, high levels of protec-tion conferred by single genes may serve only to de-lay future problems. The use of more durable resist-ances with less effectiveness has been proposed as asafer alternative. However, single genes conferringintermediate levels of resistance are also likely to bevulnerable to changes in pathogenicity. The best as-surance is some measure of durability (Johnson,1981) and an indication that genetic control is morecomplex than a single gene. For example, workers atCIMMYT (Singh & Rajaram, 1994; Singh et al.,1994) and at PBI Cobbitty (R.A. McIntosh, H.S.Bariana & C.R. Wellings, unpublished) found thathighly effective sources of adult plant resistance(APR) to stripe rust invariably possessed two ormore resistance genes which usually behaved in anadditive manner. Single genes conferring high lev-els of APR were not encountered. It is assumed thatthese additive gene combinations that are essentialto providing adequate protection would also con-tribute to durability. Provided the resistances arebased on additive gene effects, there is probably nolimit to the actual level of resistance that might beobtained; the more effective the resistance, themore robust the response over environments andpathotypes.

Singh et al. (1994) demonstrated the beneficial ef-fects of the partially effective gene Lr34 in Jupateco’R’ relative to the near-isogenic selection, Jupateco’S’. In the presence of rust, Lr34 in Jupateco ’R’ re-duced the potential loss measured in Jupateco ’S’ by



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60%. Because this work was conducted in a rustnursery with high levels of disease, the protectionconferred by the gene would be greater in mostfarming situations. With autumn sown springwheats in Australia, Lr34 appears to delay the de-velopment of leaf rust in spring, but terminal leafrust levels can be high. D. Singh (unpublished) hasshown that wheats possessing Lr34 fail to carry rustthrough the winter months; an observation that ap-pears to be consistent with reports that this gene ismore effective at low temperatures (Drijepondt &Pretorius, 1989; Pretorius et al., 1994).

When a very narrow range of disease/pathogenresponse is available, the breeding strategy is morelikely to focus on avoidance of unduly susceptiblegenotypes. Provided genotype ranking is possible,agreed maximum disease levels for cultivar releaseare a useful strategy for preventing unwanted in-creases in disease/pest susceptibility and the emer-gence of new disease problems.

Methods of selection. Ongoing research on selectionmethods aims to reduce and minimise the space,time and costs needed to screen segregating pop-ulations. The use of seedling rust tests in the green-house did much to simplify the screening process,but if the breeder requires only adult plant resist-ance of a certain type, then such procedures canonly be used to remove unwanted germplasm rath-er than to select the desired plants. Greenhouse/growth chamber selection assays for Russian wheataphid, Hessian fly and CCN and the developmentof the boot injection technique for Karnal bunt andthe point injection method for scab are all relativelysimple innovations that improve the efficiency ofselection for these biotic stresses.

The ultimate simplified method for selection is alaboratory test that can be performed in the ab-sence of the disease, especially if the screening pro-cedure is time consuming and costly. However, thismust be preceded by a fairly accurate genetic corre-lation and in most instances selection will be for asingle gene. The concept of molecular markers isnot new; phenotypic associations have been knownand used for many years. Examples of such associ-ations include resistance to sawfly and solid stem,the association of Yr9, Lr26, Sr31 and often Pm8 in

1BL.1RS derivatives, Lr24 and Sr24 in wheat:Agro-pyron translocation lines, the association of Lr37,Yr17 and Sr38 and of eyespot resistance and anα-amylase allele in VPM1 derivatives, the associ-ation of Sr2 and pseudo-black chaff, the associationof Lr34, Yr18, Bdv1 and Ltn and the linkage of Yr10and Rg1. All of these associations have been andwill continue to be used in selection for rust resist-ance.

Rajaram (1994a) extended the shuttle breedingprocess to encompass the use of disease hotspotsthroughout Mexico and key international locationsfor testing responses to specific diseases and pestsor specific combinations of them. The use of hot-spots ensures reliability of infection/infestation andhence the high probability of useful results in eachtesting cycle. There is an assumption that hotspotsrepresent centres of genetic variability of patho-gens or pests. This needs careful monitoring overtime, especially when worldwide distribution ofgermplasm is involved. Such monitoring can beachieved with selected indicator lines of known ge-notype or by sampling for subsequent typing in thelaboratory. In the CIMMYT program, there is com-pensation for possible lack of pathogen/pest varia-bility at hotspots as the selected germplasm is pro-moted to internationally distributed nurserieswhere it is exposed to a wider range of global varia-bility. At ICARDA, Syria, attempts are made torepresent various mega-environments and biotichotspots through differential planting dates at TelHadya and other sites within Syria and key loca-tions throughout the WANA region (Nachit, 1994).

These approaches to identifying and buildingadapted germplasm with acceptable levels of resist-ance to targeted biotic stresses using field-basednurseries can be contrasted with the National Cere-al Rust Control Program in Australia where knowl-edge gained from pathotype surveys and ongoinghost genetics programs allow gene combinations tobe planned and assembled on-site. The approach isto assess international germplasm in greenhouseand field tests with a few carefully chosen localpathotypes and to select as parents, lines, pheno-types or genes considered to add to those in currentuse. The isolated field nurseries are inoculated withpathotypes that are currently in farmers’ fields or



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are considered likely to increase in the future. Thestrategy is to add to current resistances and to havereplacement genotypes for the future; the purposeof resistance is to minimise inoculum levels. Lowrust incidence seems to be associated with low lev-els of variation.

Coping with pathogenic variation. Pathogenic vari-ation in some pathogens and pests of wheat consti-tutes a major problem that must be addressed bybreeders. In some situations, the role of pathogen/pest specialisation is probably under-rated especial-ly where those pathogens and pests affect more spe-cies than wheat, including weed species. TakingPuccinia recondita as an example, it is known thatpathotypes occurring on common wheat, durumand some Aegilops species may be different. Hence,the role of any one group of hosts in influencing epi-demics on a different group must be carefully as-sessed. Moreover, attention must be given to thesource of inoculum used in breeding nurseriesaimed at improvement of both durum and commonwheat. In contrast to this level of specialisation inthe leaf rust system, the likelihood of a common setof genes giving resistance to scab caused by differ-ent Fusarium species has already been mentioned.Mamluk (1990) drew attention to the likely differ-ential specialisation of the common bunt pathogensto durum and common wheat. This type of special-isation probably occurs for many other disease/pestsituations, e.g., leaf rust (Roelfs & Huerta-Espino,1992).

Pathogenic specialisation reaches its greatest lev-el of complexity and concern for breeders in the air-borne rust and powdery mildew pathogens. Hessianfly is also highly variable, but the spread of biotypesis not as rapid as with the rust pathogens. In order tounderstand the structure and variability of rustpathogens, many national programs undertake col-lection surveys throughout the wheat growing re-gions. Samples are pathotyped in seedling tests ofestablished differential genotypes. The results,made available to breeders and others and ex-pressed in frequencies of pathotypes or as frequen-cies of virulence for each tester or gene if known,provide information on distribution over large ar-eas. If commercial cultivars are used as differen-

tials, or if the genotypes of differentials and culti-vars are known and are similar, relevant deductionscan be made to the farm situation. However, manysurveys only partially achieve a relationship be-cause the survey is based on seedling resistancegenes which are not present in the national culti-vars.

With increased emphasis on durable adult plantresistances based on the Sr2 complex, Lr34 andother slow rusting adult plant factors for leaf rustresistance and on adult plant resistances to striperust, traditional rust surveys will continue to fail toprovide knowledge of useful genetic relationshipsbetween the pathogen flora and host cultivars. In-clusion of adult plant tests in such surveys will partlyrectify the situation. In order to gain knowledge ofpathogen variation for adult plant resistances, D.Singh (unpublished) has developed an inoculationtechnique for adult plants using inoculated seg-ments of adhesive tape. These small segmentsplaced on flag leaves enable infection without needfor humidity chambers. A well-tillered plant can beinoculated with many different pathogen isolates.This technique can also be used very efficiently forselection in accelerated backcross breeding pro-grams.

For national programs that lack facilities for tra-ditional pathotype surveys, there is considerablemerit in assembling sets of indicator genotypes forplanting in strategic locations throughout the agri-cultural regions. The responses of the indicator ge-notypes provide information on pathotype distribu-tion. Wellings et al. (1996) propose the develop-ment of a set of near-isogenic lines for internationaluse in stripe rust research.

The use of molecular markers in pathogen and hostidentification and screening. Molecular biology willplay an increasing role in pathogen identificationand the study of variation in pathogens and pests;isozyme markers, RFLPs (restriction fragmentlength polymorphism), PCR (polymerase chain re-action) and other techniques will be used to supple-ment information gained from traditional patho-genicity surveys.

Molecular markers should have an increasingrole in resistance breeding. At present, there are



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relatively few examples in wheat where markerscan be applied for selection in practical breedingprograms. Eastwood et al. (1994) reported com-plete linkage between Cre3 (Ccn-D1) for cereal cystnematode resistance and a RAPD marker in chro-mosome 2D. Although resistance sources involvinggenes in alien segments can be identified with mole-cular markers that distinguish the alien segmentsfrom wheat chromatin, few of the segments havebeen successfully exploited in cultivars. Wherealien transfers involve undesirable yield or qualitycharacteristics, selection for recombination eventsthat reduce the amounts of alien chromatin andhence increase the likelihood of more desirabletransfers can be aided by selection against markersthat were previously present. Clearly, if such mark-ers are very closely linked, or co-incident with thewanted resistance gene(s), the desired recombina-tion events will be rare or impossible.

Transformation/genetic engineering. Transforma-tion as a breeding tool for wheat is in its infancy.Meanwhile, resistance genes involving a number ofdiseases and a range of host species have beencloned and at least partially sequenced. Despitecommon features among many of the cloned resist-ance genes, there is still no understanding of host-:pathogen specificity. The genes appear to be in-volved in signal-transduction pathways. An under-standing of resistance genes and avirulence genes inpathogens, their products and their roles shouldprovide opportunities for the construction of novelresistance genes. If known resistance genes, espe-cially those in species that are related to wheat, canbe efficiently cloned, and if an efficient transforma-tion system is developed, it should be possible tocarry out the types of alien transfer now being at-tempted by chromosome engineering. When this isachieved by transformation, the alien segmentsshould be very small and should not involve the cur-rent problems of undesirable traits associated withalien transfers.

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Breeding wheat for resistance to biotic stresses