Resistance of wheat to Mycosphaerella graminicola involves early and late peaks of gene expression

Large-scale cDNA-AFLP profiling identified numerous genes with increased expression during the resistance response of wheat to the Septoria tritici blotch fungus, Mycosphaerella graminicola. To test whether these genes were associated with resistance responses, primers were designed for the 14 that were most strongly up-regulated, and their levels of expression were measured at 12 time points from 0 to 27 days after inoculation (DAI) in two resistant and two susceptible cultivars of wheat by real-time quantitative polymerase chain reaction. None of these genes was expressed constitutively in the resistant wheat cultivars. Instead, infection of wheat by M. graminicola induced changes in expression of each gene in both resistant and susceptible cultivars over time. The four genes chitinase, phenylalanine ammonia lyase, pathogenesis-related protein PR-1, and peroxidase were induced from about 10- to 60-fold at early stages (3 h–1 DAI) during the incompatible interactions but were not expressed at later time points. Nine other genes (ATPase, brassinosteroid-6-oxidase, peptidylprolyl isomerase, peroxidase 2, 40S ribosomal protein, ADP-glucose pyrophosphorylase, putative protease inhibitor, methionine sulfoxide reductase, and an RNase S-like protein precursor) had bimodal patterns with both early (1–3 DAI) and late (12–24 DAI) peaks of expression in at least one of the resistant cultivars, but low if any induction in the two susceptible cultivars. The remaining gene (a serine carboxypeptidase) had a trimodal pattern of expression in the resistant cultivar Tadinia. These results indicate that the resistance response of wheat to M. graminicola is not completed during the first 24 h after contact with the pathogen, as thought previously, but instead can extend into the period from 18 to 24 DAI when fungal growth increases dramatically in compatible interactions. Many of these genes have a possible function in signal transduction or possibly as regulatory elements. Expression of the PR-1 gene at 12 h after inoculation was much higher in resistant compared to susceptible recombinant-inbred lines (RILs) segregating for the Stb4 and Stb8 genes for resistance. Therefore, analysis of gene expression could provide a faster method for separating resistant from susceptible lines in research programs. Significant differential expression patterns of the defense-related genes between the resistant and susceptible wheat cultivars and RILs after inoculation with M. graminicola suggest that these genes may play a major role in the resistance mechanisms of wheat.     

Studies on the Interaction Between Septoria tritici and Stagonospora nodorum in Wheat

Interactions between Stagonospora nodorum and Septoria tritici were studied. Results from a detached glume experiment indicated that the interaction may be isolate-dependent, as it was shown that the interaction between the two pathogens may be beneficial or antagonistic depending on the isolate of each pathogen present. The number of spores produced by both pathogens was significantly greater when an aggressive isolate of S. tritici was mixed with a non-aggressive isolate of S. nodorum, whereas the number of spores produced by both pathogens was significantly less when two non-aggressive isolates were mixed. There was a significant reduction in disease level when S. tritici was applied prior to S. nodorum, compared to vice versa in the growth chamber. Results from growth chamber and field studies showed that S. nodorum produced significantly more spores when both pathogens were present together. It is concluded that S. tritici has a stimulatory effect on spore production by S. nodorum. However, there was a reduction of S. tritici spores observed in the dual inoculation treatments, suggesting that S. nodorum inhibits S. tritici.     

A predictive model for early-warning of Septoria leaf blotch on winter wheat

Disease–weather relationships influencing Septoria leaf blotch (SLB) preceding growth stage (GS) 31 were identified using data from 12 sites in the UK covering 8 years. Based on these relationships, an early-warning predictive model for SLB on winter wheat was formulated to predict the occurrence of a damaging epidemic (defined as disease severity of 5% or > 5% on the top three leaf layers). The final model was based on accumulated rain > 3 mm in the 80-day period preceding GS 31 (roughly from early-February to the end of April) and accumulated minimum temperature with a 0°C base in the 50-day period starting from 120 days preceding GS 31 (approximately January and February). The model was validated on an independent data set on which the prediction accuracy was influenced by cultivar resistance. Over all observations, the model had a true positive proportion of 0.61, a true negative proportion of 0.73, a sensitivity of 0.83, and a specificity of 0.18. True negative proportion increased to 0.85 for resistant cultivars and decreased to 0.50 for susceptible cultivars. Potential fungicide savings are most likely to be made with resistant cultivars, but such benefits would need to be identified with an in-depth evaluation.     

Control of Stagonospora nodorum and Septoria tritici in Wheat by Pre-treatment with Drechslera teres, a Non-host Pathogen

A field study is described which explored the possibility of controlling Stagonospora nodorum and Septoria tritici on wheat using a barley pathogen, Drechslera teres. Pre-treatment of wheat cv. Hussar flag leaves with D. teres resulted in a significant reduction in disease caused by S. nodorum and S. tritici, resulting in a significant increase in grain yield. When cv. Brigadier leaves were treated with D. teres prior to inoculation with S. nodorum there was an initial increase in disease expression whilst D. teres had no effect on symptoms produced by S. tritici on cv. Brigadier. There was significantly less disease on leaves of cvs. Hussar and Brigadier pre-treated with D. teres prior to inoculation with an equal mixture of S. nodorum and S. tritici compared to plants pre-treated with water. It is concluded that D. teres and other non-host pathogens show potential as biological control agents for S. nodorum and S. tritici.     

Survey of cereal diseases and petts in the Netherlands. 5. Occurrence of Septoria spp. in winter wheat

Data of the annual surveys of circa 100 commerical winter wheat fields were compiled to describe epidemics ofSeptoria spp. in the Netherlands during 1974–1986. In May, during the first node stage,S. tritici was dominant whileS. nodorum was virtually absent. In July, during ripening,S. tritici on average dominated overS. nodorum, though in the most continental districts of the countryS. nodorum predominated.In May between 1974 and 1984, on average 56% of the fields showed leaf infections bySeptoria spp., while in July between 1975 and 1986, on average 83% of the fields showed leaf infections. Prevalence ofSeptoria spp. has increased during the surveys. Annual intensity ofSeptoria spp. in winter wheat crops was positively correlated with precipitation and negatively with average monthly sunshine duration during the harvest-month August of the previous growing season. The correlation with sunshine during August could indicate that ascospores play a major role in subsequent epidemics; but whether it is a causal relation remains to be answered.Present address: Center for Agrobiological Research (CABO-DLO), PO Box 14, 6700 AA Wageningen, the Netherlands     

Genetic Structure of Mycosphaerella graminicola Populations from Iran, Argentina and Australia

Restriction fragment length polymorphism (RFLP) markers were used to assess the genetic structure of populations of Mycosphaerella graminicola collected from wheat fields. A total of 585 isolates representing 10 field populations were sampled from Iran, Argentina and Australia. The genetic structure of M. graminicola populations from Iran and Argentina is described for the first time. Results were compared to previously investigated populations from Israel, Uruguay and Australia. Populations from Iran exhibited high clonality and low gene diversity, suggesting an inoculation event. Populations from uninoculated fields in Argentina had gene and genotype diversities similar to previously described European and North American populations. Genotype diversity was high for populations from Australia and tests for multilocus associations were consistent with sexual recombination in these populations. Gene diversity was low and fixed alleles were found for several loci. These findings are consistent with a relatively small founding population for Australia. These 10 new populations were integrated into a genetic distance comparison with 13 global populations that were characterized earlier.     

Effects of nitrogen fertilization and cultivar on the damage relation of powdery mildew (Erysiphe graminis) in winter wheat

The damage relation of powdery mildew in winter wheat was studied in field experiments in 1981 and 1983, in the Netherlands. No firm conclusion was obtained on the effect of nitrogen supply (175 and 235 kg ha^–1 N totally) on the damage relation. The relation was not affected by cultivars (four) and did not differ significantly between both years. The measured relation averaged 0.0125 kg are^–1 damage per pustule-day mildew per leaf, at yields of 70–90 kg are^–1. The effect of the fungicide triadimefon on yield could be ascribed to its effect on diseases. The vertical distribution of mildew in the crop was described.Samenvatting In 1981 en 1983 werd in veldproeven met wintertarwe de relatie tussen schade (in kg are^–1) en meeldauw onderzocht. Of de relatie onafhankelijk is van de stikstofbemesting (175 en 235 kg ha^–1 N totaal), kon niet met zekerheid worden vastgesteld. De schaderelatie werd niet significant beïnvloed door de vier getoetste rassen. In de twee jaren werd een vergelijkbare schade van gemiddeld 0.0125 kg are^–1 per puistdag meeldauw per blad gemeten, bij een opbrengstniveau van 70–90 kg are^–1. Tevens werd de locatie van meeldauw in het gewas beschreven.     

Temperature Dependent Seed Transmission of Stagonospora nodorum in Wheat

The transmission of Stagonospora nodorum from four naturally infected winter wheat seedlots was quantified in controlled environment germination chambers at 9, 13, 17, 21, and 25 °C. Seedlings were harvested when the second leaf began to emerge. Coleoptiles and first seedling leaves were examined for the presence of lesions caused by S. nodorum. First leaves were incubated on Bannon's medium for 2 weeks, after which they were examined for pycnidia of S. nodorum. Transmission to the coleoptile occurred at all temperatures, but decreased from 100% to 72% as temperature increased from 9 to 25 °C. Transmission to the first leaf was less, dropping from 37% to 2% as temperature increased from 9 to 25 °C. At least 44% of infected first leaves were symptomless at all temperatures, with 96% of infected leaves showing no symptoms at 25 °C. Transmission to seedling leaves occurred over a broad temperature range. Under the high densities at which wheat is sown, a significant number of infected seedlings per unit area may originate from relatively low initial seed infection levels and transmission efficiencies.     

Studies on the origin,spread, and evolution of an important group ofPuccinia recondita f. sp.tritici pathotypes in Australasia

Wheat brown rust pathotype (pt) 104-2,3,(6),(7), 11 was first detected in Australasia in Victoria during 1984. Although it appeared similar to a pre-existing pathotype, 104-2,3,6,(7), detailed greenhouse test revealed nine pathogenic differences between the two rusts. Six differences involved contrasting virulence/avirulence for the resistance genes/specificitiesLr12, Lr27+Lr31 andLr16, and three uncharacterised genes, present in the wheat cultivars Gaza and Harrier, and in triticale cultivar Lasko. Differences in partial virulence between the pathotypes were found for the genesLr2a, Lr13 andLr26. A comparison of the phenotypes for 13 isozyme systems in the two pathotypes revealed two differences, including aPgm2 allele in pt 104-2,3,(6),(7),11 not found in other contemporary AustralasianPuccinia recondita f. sp.tritici pathotypes. On the basis of these differences, it was concluded that pt 104-2,3,(6),(7),11 was introduced into the Australasian region before or during 1984.Seven variants of pt 104-2,3,(6),(7),11, that differed by single virulences, were detected during 1984–1992. Pt 104-2,3,(6),(7),11 and a derivative pathotype with virulence forLr20 underwent rapid increases in frequency, largely displacing pathotypes which predominated before 1984. Although first detected in eastern Australia, both pathotypes spread to New Zealand, and the derivative pathotype appeared in Western Australia. The rapid spread and increase of these pathotypes could not be explained by host selection. Pt 104-2,3,(6),(7),11 and derivatives may therefore be more aggressive than other contemporary Australasian pathotypes.Abbreviations NSW New South Wales - Prt Puccinia recondita f. sp.tritici - Qld Queensland - SA South Australia - WA Western Australia     

Genetic variation in partial resistance to leaf rust in winter wheat: disease progress,foliage senescence and yield reduction

Relations between leaf rust progress, foliage senescence and yield reduction were studied for seven winter wheat genotypes, differing in their partial resistance to leaf rust. Leaf rust accelerated leaf and ear senescence. Photosynthesis measurements showed, however, that the photosynthetic capacity of the remaining green surface was not affected. Differences between genotypes in yield reduction were largely explained by differences in leaf senescence and, therefore, in cumulative light interception (r=0.83) and crop photosynthesis. Reduction in cumulative light interception was closely related to the area under the disease-progress-curve (r=0.85), which was also closely associated with yield reduction (r=0.88). However, the time taken to reach a 50% reduction of green leaf area and the pustule density on 1 July (i.e. halfway through the epidemic) were just as good predictors of yield reduction as cumulative light interception and area under disease-progress-curve, suggesting that the former are useful criteria in the selection for partial resistance to leaf rust.Samenvatting De relatie stussen de epidemiologie van bruine roest, bladveroudering en oprengstderving werden bestudeerd bij zeven wintertarwegenotypen die verschilden in partiële resistentie tegen bruine roest. Bruine roest versnelde de veroudering van blad en aar. Fotosynthesemetingen wezen echter uit dat de fotosynthesecapaciteit van het resterende groene oppervlak niet werd beïnvloed. Verschillen tussen de genotypen in opbrengstderving werden voornamelijk veroorzaakt door verschillen in bladveroudering en daarmee in cumulatieve lichtinterceptie (r=0.83) en gewasfotosynthese. De reductie in cumulatieve lichtinterceptie was nauw gerelateerd aan de cumulatieve ziektedruk (in puistdagen) (r=0.85), welke ook nauw was geassocieerd met de opbrengstderving (r=0.88). De opbrengstreductie werd echter even goed voorspeld door de tijdsduur tot 50% reductie van het groene bladoppervlak en de puistdichtheid halverwege de epidemie als door cumulatieve lichtinterceptie en cumulatieve ziektedruk, waardoor beide eerste criteria gebruikt kunnen worden in de selectie voor partiële resistentie tegen bruine roest.     

Phylogenetic and morphological analyses of Pythium graminicola and related species

Isolates of Pythium graminicola and related species were differentiated using restriction fragment length polymorphism (RFLP) analyses of the internal transcribed spacer (ITS) regions of rDNA and the cytochrome c oxidase subunit II (COX II) gene. These sequences were used in subsequent phylogenetic analyses. Finally, the phylogenetic placement of species was compared to that determined from morphological characteristics. The 62 isolates tested were divided into seven groups, A–G, based on RFLP analysis of the rDNA-ITS region. In the RFLP analysis of the COX II gene, isolates were divided into groups similar to those based on ITS-RFLP. Groups A and B were each separated into two additional subgroups. Grouping of isolates based on RFLP analyses agreed with the morphological differentiation. Groups A, B, D, E, F, and G were identified as P. graminicola, P. arrhenomanes, P. aphanidermatum, P. myriotylum, P. torulosum, and P. vanterpoolii, respectively. Group C was closely related to group B based on phylogenetic analysis of the rDNA-ITS region and the COX II gene and is similar to P. arrhenomanes. Each of the other species occupied their own individual clades. Although P. arrhenomanes is morphologically similar to P. graminicola, our phylogenetic analyses revealed that it was evolutionarily distant from P. graminicola and more closely related to P. vanterpoolii. Our analysis also revealed that P. torulosum with smaller oogonia is more closely related to P. myriotylum with large oogonia than to P. vanterpoolii, which forms smaller oogonia and is morphologically similar to P. torulosum. P. aphanidermatum with large oogonia and aplerotic oospores was not related to the morphologically similar species P. myriotylum. Results suggest that P. graminicola and related species are phylogenetically distinct, and molecular analyses, in addition to morphological analyses, are necessary for the accurate taxonomic placement of species in this complex.     

Assessing Four-Way Mixtures of Winter Wheat Cultivars from the Performances of their Two-Way and Individual Components

Seven four-way bread wheat mixtures were compared to their components (individual cultivars and two-way mixtures) for septoria tritici blotch severity, grain protein content, and grain yield. Four-way mixtures and two-way mixtures performed better than the average of individual pure line components. Disease severity and protein content were most influenced by mixtures, with mixture efficiencies being greater in the four-way than in the two-way mixtures. Performances of four-way mixtures in terms of diseased leaf area reduction, grain yield, 1000-grain weight, and grain protein content were better predicted by performances of two-way mixtures than by those of pure lines. Our results suggest that two-way mixtures should be screened to remove unfavourable cultivar pairs and those binary mixtures that show complementarity should be selected in order to construct four-way mixtures.     

Early stages of septoria tritici blotch epidemics of winter wheat: build‐up,overseasoning, and release of primary inoculum

Septoria tritici blotch (STB), caused by Mycosphaerella graminicola, is the most prevalent disease of wheat worldwide. Primary inoculum and the early stages of STB epidemics are still not fully understood and deserve attention for improving management strategies. The inoculum build‐up and overseasoning involves various fungal structures (ascospores, pycnidiospores, mycelium) and plant material (wheat seeds, stubble and debris; wheat volunteers; other grasses). Their respective importance is assessed in this review. Among the mechanisms involved in the early stages of epidemics and in the year‐to‐year disease transmission, infection by ascospores wind‐dispersed from either distant or local infected wheat debris is the most significant. Nevertheless, infection by pycnidiospores splash‐dispersed either from neighbouring wheat debris or from senescent basal leaves has also been inferred from indirect evidence. Mycosphaerella graminicola has rarely been isolated from seeds so that infected seed, although suspected as a source of primary inoculum for a long time, is considered as an epidemiologically anecdotal source. Mycosphaerella graminicola can infect a few grasses other than wheat but the function of these grasses as alternative hosts in natural conditions remains unclear. Additionally, wheat volunteers are suspected to be sources of STB inoculum for new crops. This body of evidence is summarized in a spatio‐temporal representation of a STB epidemic aimed at highlighting the nature, sources and release of inoculum in the early stages of the epidemic.     

Note: Occurrence and distribution ofCucumber mosaic virus infecting danshen (Salvia miltiorrhiza) in China

Cucumber mosaic virus (CMV) has resulted in much damage to Danshen (Salvia miltiorrhiza Bunge) crops in China. A 5-year survey was conducted in Hebei, Shandong, Sichuan, Shanxi, Henan and Gansu Provinces, all major Danshen-growing areas. A total of 156 Danshen plant samples with CMV symptoms were collected and tested for the presence of CMV by a double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA) using polyclonal antibodies against CMV and a positive control, according to the supplier’s instructions (Agdia). They were confirmed to be CMV by amplification of complete coat protein gene and analysis of the gene sequence. The results showed that 122 samples were infected by CMV and all of these CMV isolates belonged to subgroup IB. http://www.phytoparasitica.org posting May 19, 2008. Joint first authors.     

The relationship of leaf wetness duration and disease progress of glume blotch,caused byStagonospora nodorum,in winter wheat to standard weather data

Almost 50% of the variation in leaf wetness duration can be explained by maximum and minimum temperatures, rainfall and hours with relative humidity above 90% on a daily basis. All of these parameters can be estimated from a standard weather station. If variables related to wind are added the level of explanation increases to 69–76%. Leaf wetness duration explained up to 42% of the rate of disease increase (RDI) forS. nodorum. Leaf wetness duration was accumulated over a 5-day window period and correlated with rate of disease increase after a 7-day lag period. Standard weather variables could explain 20–34% of the disease increase. The relevance of these statistical models to disease prediction is discussed.     

Use of carbendazim and carbendazim-resistant yeasts to create different yeast densities on wheat leaves for field studies on biological control

Phyllosphere yeasts may play an important role in suppressing necrotrophic pathogens. In a randomized block design, yeast densities on flag leaves and second leaves of field-grown wheat were left unchanged (D), or were lowered by sprayings with carbendazim (A), or were raised by sprayings with a mixture ofSporobolomyces roseus, Cryptococcus laurentii var.flavescens and nutrients (B), or with carbendazim, carbendazim-resistantS. roseus andC. laurentii var.flavescens and nutrients (C). The application of carbendazim to plots A and C would avoid a biased interference of carbendazim due to other effects than reducing the natural yeast population. Prolonged differences in yeast density would be reflected in differences in severity of diseases caused by carbendazim-insensitive necrotrophic pathogens.Both treatments B and C enhanced the yeast density about 10-fold at the beginning of leaf colonization, 2 to 3 weeks after leaf emergence. Untreated leaves (D), however, were rapidly leaves. Initially, the yeasts were suppressed by carbendazim (A). However, progressively the yeast population consisted of carbendazim-resistant strains which made the carbendazim sprayings ineffective. Therefore, the substantial differences in yeast density were of limited duration. The effect of the treatments on naturally occurringMycosphaerella graminicola (anam.Septoria tritici), Puccinia recondita f. sp.tritici and the total necrotic leaf area (D-value) is discussed.Samenvatting Fyllosfeergisten kunnen misschien een belangrijke rol spelen in de onderdrukking van necrotrofe pathogenen. In een blokkenproef werd de dichtheid van gisten op vlagbladeren en tweede bladeren niet beïvvloed (D) of verlaagd door bespuitingen met carbendazim (A), of verhoogd door bespuitingen met een mengsel van gisten (Sporobolomyces roseus enCryptococcus laurentii var.flavescens en voedingsstoffen (B), of met een mengsel van carbendazim, carbendazim-resistenteS. roseus enC. laurentii var.flavescens en voedingsstoffen (C). De grootste verschillen in dichtheden van de gistpopulaties werden verwacht tussen de behandelingen A en B of C. Door alle veldjes A en C met carbendazim te behandelen wordt een eenzijdig effect van carbendazim, berustend op andere eigenschappen dan de onderdrukking van de natuurlijke gistpopulatie, voorkomen. Langdurige verschillen in de populatiedichtheden van de gisten zouden weerspiegeld kunnen worden in verschillen in aantasting door carbendazimongevoelige necrotrofe pathogenen.Aan het begin van de bladkolonisatie door gisten, 2 tot 3 weken na het verschijnen van het blad, leidde zowel behandeling B als C tot, een 10-voudige verhoging van de gistdichtheid. De onbehandelde bladeren (D) werden echter spoedig door de van nature voorkomende gisten gekoloniseerd en het verschil tussen de onbehandelde en met gist bespoten bladeren werd snel kleiner. Aanvankelijk werden de gisten door carbendazim (A) onderdrukt. Geleidelijk bestond de gistpopulatie echter uit carbendazim-resistente stammen, zodat de carbendazim bespuitingen nauwelijks meer effect hadden. Hierdoor werden grote verschillen in gistdichtheden niet langdurig gerealiseerd. Het effect van de behandelingen op de natuurlijke infectie doorMycosphaerella graminicola (anam.Septoria tritici), Puccina recondita f. sp.tritici en op het totale dode bladoppervlak (D-waarde) wordt besproken.     

A comparative study of resistance to powdery mildew in wild emmer wheat in the seedling and adult plant stage

An isometric virus was isolated from cucumber plants growing in a plastic house in Crete and showing stunting and bright yellow mosaic of the leaves. Based on host range, properties in crude sap, behaviour during purification, electron microscopy and serology, the virus was identified as an isolate of artichoke yellow ringspot nepovirus. Ecological data corroborate transmission of the virus via the soil.Samenvatting Uit komkommerplanten in plastic-foliekassen op Kreta werd een bolvormig virus geïsoleerd; de aangetaste komkommerplanten vertoonden dwerggroei en helder geel mozaïek op de bladeren. Gebaseerd op de resultaten verkregen uit onderzoek met het virus naar de waardplantenreeks, de eigenschappen in perssap, zuivering, elektronen-microscopie en serologie kon het virus worden geïdentificeerd als een strain van het artichoke yellow ringspot nepovirus. Waarnemingen op het gebied van de ecologie wijzen op overdracht van het virus via de grond.     

Simulation of yield reduction by leaf rust in winter wheat,applied to the analysis of genetic variation in partial resistance

Differences in yield reduction among seven winter wheat genotypes due to leaf rust, as observed in a field experiment, were analysed using a simulation model. In this model, the effects of the disease on crop growth and yield were described on the basis of light interception, photosynthesis, respiration and assimilate partitioning. The model properly described the observed yield difference between the genotypes, both in the absence and in the presence of leaf rust. According to the model, 66% of total yield reduction was due to an accelerated decrease in green leaf area and 18% was due to light capture by dead leaf tissue at the top of the canopy. Genetic variation in yield reduction was, therefore, mainly explained by variation in leaf senescence. Leaf rust did not affect the photosynthetic rate of the remaining green leaf area. Opportunities of selection for individual damage components were assessed from their simulated effect on grain yield, together with their estimated genetic and environmental variance.Samenvatting Verschillen tussen zeven wintertarwegenotypen in opbrengstderving door bruine roest, zoals waargenomen in een veldexperiment, werden geanalyseerd met een simulatiemodel. In dit model werd het effect van de ziekte op gewasgroei en opbrengst beschreven op basis van lichtinterceptie, fotosynthese, ademhaling en assimilatenverdeling. Het model gaf een goede beschrijving van de waargenomen opbrengstverschillen tussen de genotypen, zowel bij aanwezigheid als bij afwezigheid van bruine roest. Van de totale opbrengstreductie werd, volgens modelberekeningen, 66% veroorzaakt door versnelde afname van groen bladoppervlak en 18% door het wegvangen van licht door dood bladweefsel boven in het gewas. De genetische variatie in opbrengstreductie werd zodoende vooral verklaard uit de waargenomen verschillen in bladveroudering tussen de genotypen. De fotosynthese per eenheid resterend groen bladoppervlak werd niet beïnvloed door bruine roest. Respectieven voor selectie op afzonderlijke schadecomponenten werden geëvalueerd op basis van hun gesimuleerde effect op korrelopbrengst, in combinatie met hun genetische en toevalsvariatie.