Evaluation of soybean genotypes for resistance against the rust-causing fungus Phakopsora pachyrhizi in East Africa

Soybean rust, caused by the biotrophic fungus Phakopsora pachyrhizi, is the most important foliar disease of soybean (Glycine max) worldwide. Deployment of resistant soybean cultivars is the best option for managing this disease. Genes conferring resistance to P. pachyrhizi have been identified, but pathotypes of the rust fungus overcoming these resistance genes have also been found. To identify novel resistance genes, soybean genotypes from both local and international sources were screened at multiple locations in Tanzania and Uganda in 2016 and 2017. The results from this screening revealed that infection types, disease severities, and sporulation levels varied among the genotypes and locations. The majority of the genotypes had tan-coloured (TAN) lesions and developed moderate sporulation, implying susceptibility, while only seven of the 71 lines had reddish-brown (RB) lesions and showed low disease severities in all of the screening environments. We identified seven genotypes that were the most resistant to rust in the most locations over the two years. These genotypes will be useful for further studies and, ultimately, for rust management, as they show broad resistance to various pathotypes of the rust fungus.     

Soybean production in eastern and southern Africa and threat of yield loss due to soybean rust caused by Phakopsora pachyrhizi

Soybean is a major source of oil and proteins worldwide. The demand for soybean has increased in Africa, driven by the growing feed industry for poultry, aquaculture and home consumption in the form of processed milk, baked beans and for blending with maize and wheat flour. Soybean, in addition to being a major source of cooking oil, is also used in other industrial processes such as in the production of paints and candle wax. The demand for soybean in Africa so far outweighs the supply, hence the deficit is mainly covered through imports of soybean products such as soybean meal. The area under soybean production has increased in response to the growing demand, a trend that is expected to continue in the coming years. As the production area increases, diseases and insect pests, declining soil fertility and other abiotic factors pose a major challenge. Soybean rust disease, caused by the fungus Phakopsora pachyrhizi, presents one of the major threats to soybean production in Africa due to its rapid spread as a result of the ease by which its spores are dispersed by the wind. Disease control by introducing resistant soybean varieties has been difficult due to the presence of different populations of the fungus that vary in pathogenicity, virulence and genetic composition. Improved understanding of the dynamics of rust ecology, epidemiology and population genetics will enhance the effectiveness of targeted interventions that, in turn, will safeguard soybean productivity.     

Relating epidemic progress from a general disease model to seasonal appearance time of rusts in the United States: implications for soybean rust

ABSTRACT Soybean rust, Phakopsora pachyrhizi, has been considered a threat to the production of the U.S. soybean, Glycine max. During the past decade, this disease gradually spread to Africa, South America, and recently to the United States. Previous soybean rust risk assessments with an assumption of availability of spores early in a season showed that weather conditions (dew and temperature) during a growing season, in general, are suitable for disease development in U.S. soybean-growing regions. Predicting the time of rust appearance in a field is critical to determining the destructive potential of rusts, including soybean rust. In this study, comparative epidemiology was used to assess likely rust incipient time in four locations within the U.S. Soybean Belt from south to north: Baton Rouge, LA; Charlotte, NC; Indianapolis, IN; and Minneapolis, MN. Temperature effects on the infection cycle of five rusts occurring in the Midwest were evaluated using a general disease model. The likely incipient times were examined with the modeling results. Among the rusts studied, early-appearing rusts had suitable conditions for development earlier in a season. However, a lag period of several weeks to more than 3 months was found from the time when conditions are suitable for a rust to develop or when hosts are available to the time when the rust was detected in fields. Length of the lag period differed among the rust species examined. If nature of long-distance dispersal is not significantly different among the rusts, implications of our study to the expected seasonal soybean rust incipience in fields lead to two possible scenarios: (i) average appearance time of soybean rust across the Soybean Belt should be somewhere between appearance times of common corn rust and southern corn rust, and (ii) with late appearance of the disease, late-planted soybean in the south has greater risk.     

Recent outbreaks of rust diseases and the importance of basic biological research for controlling rusts

Rust fungi are obligate plant parasites belonging to the order Pucciniales; they comprise about 7,800 species throughout the world. Some species seriously damage crops, vegetables, fruits and trees. Of these species, wheat stem rust (Puccinia graminis f. sp. tritici), Asian soybean rust (Phakopsora pachyrhizi) and myrtle rust (Puccinia psidii) have recently become major concerns worldwide, and this review, discusses recent rust disease outbreaks of Asian soybean rust and myrtle rust. Both rusts have very wide host ranges. Asian soybean rust has spread from its original region of distribution (eastern Asia) to many areas of soybean cultivation around the world. Myrtle rust is a new disease in areas where host plants were first introduced and has spread to other parts of the world including the areas where the host plants are indigenous. New diseases of economically important plants can occur by host shifts from wild host plants or host jumps from phylogenetically unrelated plant species. Recent advances in molecular phylogenetic studies have contributed to a revision of rust taxonomy. Molecular phylogenetic analyses, together with precise morphological observations and inoculation experiments, have identified taxonomic groups among populations that are morphologically very similar. Systematic, ecological and other basic biological studies of rust fungi in both cultivated and wild host plants are very important for developing methods to control rust diseases. Recent changes in the International Code of Botanical Nomenclature will surely affect the systematics of rust fungi.     

Simulation of apparent infection rate to predict severity of soybean rust using a fuzzy logic system

ABSTRACT Few biologically based models to assess the risk of soybean rust have been developed because of difficulty in estimating variables related to infection rate of the disease. A fuzzy logic system, however, can estimate apparent infection rate by combining meteorological variables and biological criteria pertinent to soybean rust severity. In this study, a fuzzy logic apparent infection rate (FLAIR) model was developed to simulate severity of soybean rust and validated using data from field experiments on two soybean cultivars, TK 5 and G 8587. The FLAIR model estimated daily apparent infection rate of soybean rust and simulated disease severity based on population dynamics. In weekly simulation, the FLAIR model explained >85% of variation in disease severity. In simulation of an entire epidemic period, the FLAIR model was able to predict disease severity accurately once initial values of disease severity were predicted accurately. Our results suggest that a model could be developed to determine apparent infection rate and an initial value of disease severity in advance using forecasted weather data, which would provide accurate prediction of severity of soybean rust before the start of a season.     

The use of host resistance in disease management of rust in common bean

Bean rust, caused by Uramyces appendiculatus, is one of the major diseases in dry and snap bean production world-wide. Numerous advancements in disease management have been made to reduce rust losses. Host resistance is an important component of rust management. However, durability of disease resistance has often been short due to the use of single genes for resistance interacting with extremely high virulence diversity of the bean rust fungus. The challenge to increase durability of resistance has led to strategies such as gene pyramiding of race-specific resistance, selection and use of partial resistance, and investigation and discovery of leaf morphological features that may slow the rust epidemic. Germplasm with multiple sources of rust resistance has been developed in specific bean seed classes and released for public and commercial use in intensive production systems such as those in the United States. However, progress to develop rust resistant germplasm for the subsistence agriculture of Latin America and Africa where intercropping and mixed cultivars dominate the production system has been slow. Incorporation of high yielding, disease-resistant components as partial replacement in farmer's mixtures has the potential to reduce severity in the crop and increase yield in the presence of rust. This strategy would not erode the genetic diversity that is historically known to enhance resistance durability and for many years has given stability in production in the subsistent agriculture systems.     

Penetration and establishment of Phakopsora pachyrhizi in soybean leaves as observed by transmission electron microscopy

For over 30 years, it has been known that Phakopsora pachyrhizi is unusual in that it penetrates from urediniospores directly through the leaf cuticle without entering stomates. This unusual mode of penetration suggests that disease resistance mechanisms might exist for soybean rust that do not exist for most rust diseases. As a result, we decided to conduct a histological study using transmission electron microscopy to further elucidate the mechanisms of penetration and early establishment of P. pachyrhizi in soybean leaves. Based on our study, it was concluded that P. pachyrhizi utilizes primarily mechanical force, perhaps with the aid of digestive enzymes, to penetrate the cuticle on the leaf surface. However, the lack of deformation lines in micrographs indicated that digestive enzymes, without mechanical force, are used by the penetration hypha to penetrate the outer and inner epidermal cell walls. Digestive enzymes, again indicated by the lack of deformation lines, are used by haustorial mother cells to breach the walls of mesophyll cells to form haustoria. The possibility exists for eventual determination of the precise roles of pressure and digestive enzymes in the development of soybean rust and elucidation of some of the determinants of resistance and susceptibility to this important plant disease.     

Systemic properties of myclobutanil in soybean plants, affecting control of Asian soybean rust (Phakopsora pachyrhizi)

BACKGROUND: The demethylation inhibitor (DMI) fungicide myclobutanil can be an effective component of spray programmes designed to control the highly destructive plant pathogen Phakopsora pachyrhizi Syd. & P. Syd., causal agent of Asian soybean rust. Myclobutanil is known from previous studies in grapevines to be xylem mobile. This study investigates the mobility profile of myclobutanil in soybean as an important component of its effective field performance. RESULTS: Over a 12 day period under greenhouse conditions, a constant uptake of myclobutanil from leaflet surfaces into the leaflet tissue was observed. Once in the leaflet, myclobutanil was seen to redistribute throughout the tissue, although no movement out of leaflets occurred owing to a lack of phloem mobility. The ability of myclobutanil to redistribute over distance within the soybean plant was revealed when visualizing movement of the compound to foliage above the point of application on the plant stem. An efficacy bioassay demonstrated that the systemic properties of myclobutanil allow control of disease at a point remote from the initial site of compound application. CONCLUSION: It is suggested that the high degree of xylem systemicity displayed by myclobutanil in soybean foliage is a contributory factor towards its commercial effectiveness for control of Asian soybean rust. Copyright © 2008 Society of Chemical Industry     

Predicting severity of asian soybean rust epidemics with empirical rainfall models

ABSTRACT Although Asian soybean rust occurs in a broad range of environmental conditions, the most explosive and severe epidemics have been reported in seasons with warm temperature and abundant moisture. Associations between weather and epidemics have been reported previously, but attempts to identify the major factors and model these relationships with field data have been limited to specific locations. Using data from 2002-03 to 2004-05 from 34 field experiments at 21 locations in Brazil that represented all major soybean production areas, we attempted to identify weather variables using a 1-month time window following disease detection to develop simple models to predict final disease severity. Four linear models were identified, and these models explained 85 to 93% of variation in disease severity. Temperature variables had lower correlation with disease severity compared with rainfall, and had minimal predictive value for final disease severity. A curvilinear relationship was observed between 1 month of accumulated rainfall and final disease severity, and a quadratic response model using this variable had the lowest prediction error. Linear response models using only rainfall or number of rainy days in the 1-month period tended to overestimate disease for severity <30%. The study highlights the importance of rainfall in influencing soybean rust epidemics in Brazil, as well as its potential use to provide quantitative risk assessments and seasonal forecasts for soybean rust, especially for regions where temperature is not a limiting factor for disease development.     

Fungicide sensitivity and monocyclic parameters related to the Phakopsora pachyrhizi–soybean pathosystem from organic and conventional soybean production systems

The failure of chemical control of soybean rust has been related to the selection of less sensitive isolates, and the infection capacity of such isolates could have implications for the management of the disease. The aims of the present study were to compare the sensitivity to tebuconazole and azoxystrobin and the monocycle of soybean rust using isolates of Phakopsora pachyrhizi from two soybean fields with different production systems (organic and conventional) in 2012/13 and 2013/14 seasons, and to monitor mutations in the CYP51 gene. To assess the sensitivity to tebuconazole and azoxystrobin, detached leaf tests and in vitro germination, respectively, were used. To evaluate the monocycle, detached leaves were inoculated with a urediniospore suspension and evaluated daily by counting the number of uredia. The occurrence of the mutations in CYP51 was investigated by a pyrosequencing assay. In both 2012/13 and 2013/14 seasons, the EC₅₀ to tebuconazole was lower for the population from the organic system (0.41 and 0.10 μg mL^?1, respectively) compared to the conventional system (1.60 and 4.44 μg mL^?1, respectively), while the EC₅₀ to azoxystrobin was similar for both populations. The lower sensitivity to tebuconazole and azoxystrobin was associated with F120L + Y131H mutations in CYP51, and the F129L mutation in CYTB, respectively. The monomolecular model fitted to monocycle data and parameters related to the maximum asymptote and the AUDPC were superior for organic than the conventional system.     

A long‐term study of burning effects on a plant pathogen in tallgrass prairie

Tallgrass prairie species have evolved with regular exposure to fire. However, burning has been used as a management tool for reducing plant disease in agricultural systems, posing the question of how plant pathogens of tallgrass prairie would be affected by burning. The rust fungus Puccinia dioicae, infecting Erigeron strigosus (Asteraceae), was studied for 8 years in long‐term experiments to evaluate the effects of burning in native tallgrass prairie. This experiment also allowed evaluation of the effects of nutrient additions, although E. strigosus was rare in the plots with added nutrients in most years. Burning reduced rust severity in most years, but effects from additions of nutrients were rarely observed. There was high interannual variation in rust severity within a location, suggesting that weather may be the most important of these three abiotic factors in determining infection. An analysis of weather variables associated with disease severity found that solar radiation in the month prior to sampling was associated with severity in unburned plots; temperature approximately 2 months prior to sampling was also associated with severity in burned plots. High interannual variation also suggests that the effects of this pathogen on its host would be sporadic and difficult to study in short‐term experiments.     

Quantitative aspects of the spread of asian soybean rust in the southeastern United States, 2005 to 2006

ABSTRACT The regional dynamics of soybean rust, caused by Phakopsora pachyrhizi, in six southeastern states (Florida, Georgia, Alabama, South Carolina, North Carolina, and Virginia) in 2005 and 2006 were analyzed based on disease records collected as part of U.S. Department of Agriculture's soybean rust surveillance and monitoring program. The season-long rate of temporal disease progress averaged approximately 0.5 new cases day(1) and was higher in nonsentinel soybean (Glycine max) plots than in sentinel soybean plots and kudzu (Pueraria lobata) plots. Despite the early detection of rust on kudzu in January and/or February each year (representing the final phase of the previous year's epidemic), the disease developed slowly during the spring and early summer on this host species and did not enter its exponential phase until late August, more than 1 month after it did so on soybean. On soybean, cases occurred very sporadically before the beginning of July, after which their number increased rapidly. Thus, while kudzu likely provides the initial inoculum for epidemics on soybean, the rapid increase in disease prevalence on kudzu toward the end of the season appears to be driven by inoculum produced on soybean. Of 112 soybean cases with growth stage data, only one occurred during vegetative crop development while approximately 75% occurred at stage R6 (full seed) or higher. The median nearest-neighbor distance of spread among cases was approximately 70 km in both years, with 10% of the distances each being below approximately 30 km and above approximately 200 km. Considering only the epidemic on soybean, the disease expanded at an average rate of 8.8 and 10.4 km day(1) in 2005 and 2006, respectively. These rates are at the lower range of those reported for the annual spread of tobacco blue mold from the Caribbean Basin through the southeastern United States. Regional spread of soybean rust may be limited by the slow disease progress on kudzu during the first half of the year combined with the short period available for disease establishment on soybean during the vulnerable phase of host reproductive development, although low inoculum availability in 2005 and dry conditions in 2006 also may have reduced epidemic potential.     

Formation of satellite uredinia as an important trait related to grapevine colonization by Phakopsora meliosmae-myrianthae

Phakopsora meliosmae-myrianthae, the causal agent of Asian grapevine leaf rust, significantly reduces the photosynthetic efficiency of grapevine leaves in green symptomless tissues surrounding lesions. This study took a close look at grapevine leaf colonization kinetics by P. meliosmae-myrianthae and compared it to P. pachyrhizi–soybean and Uromyces appendiculatus–bean colonization. It is already known from the literature that soybean rust, similar to grapevine rust, has a negative effect on leaf photosynthesis greater than would be expected based on visual lesions. However, in contrast to soybean and grapevine rusts, the effect of bean rust on leaf photosynthesis is proportional to the diseased leaf area. Colonization progress was monitored by fungal biomass assessed via histological staining and quantitative polymerase chain reaction (qPCR). Individual lesions of P. meliosmae-myrianthae on grapevine, P. pachyrhizi on soybean and U. appendiculatus on common bean leaves were evaluated every 3–4 days, and the number of uredinia was counted. Staining showed that mycelial colonization did not extend beyond the lesion border. The number of P. pachyrhizi and P. meliosmae-myrianthae uredinia within the lesions increased over time (on average 14-fold), whereas the number of U. appendiculatus uredinia remained the same. These findings were corroborated by qPCR, which revealed a greater increase in fungal biomass for Phakopsora spp. than for U. appendiculatus until 12 days post-inoculation. The high number of satellite uredinia within lesions might be directly related to the impact of this pathogen in photosynthetic efficiency on symptomless areas of diseased grapevine leaves. This study identified accelerated formation of satellite uredinia as an important feature of grapevine colonization by P. meliosmae-myrianthae.     

A unique race of the wheat stem rust pathogen with virulence on Sr31 identified in Spain and reaction of wheat and durum cultivars to this race

Wheat stem rust, caused by Puccinia graminis f. sp. tritici, is a re-emerging disease, posing a threat to wheat production. In Spain, stem rust has been rarely detected since the 1970s, but infection was observed in wheat fields in 2018. We analysed six stem rust samples collected in Rota, Cádiz province and one from Monteagudo del Castillo, Teruel province. All the samples from Rota were typed as race TKTTF, whereas the sample from Monteagudo del Castillo, collected in a wheat field adjacent to barberry bushes, was typed as race TKHBK. This race has a unique and significant virulence combination that includes virulence to Sr31, Sr33, Sr53 and Sr59, and is avirulent to Rusty, a durum line developed for universal susceptibility to the wheat stem rust pathogen. TKHBK is the first race outside the Ug99 race group with virulence to Sr31 and the first known race with virulence to Sr59. Genotyping studies indicate that race TKHBK does not belong to the Ug99 or TKTTF race groups and constitutes a previously unknown lineage. Two hundred bread and durum wheat cultivars and breeding lines from Spain were evaluated against TKHBK, TKTTF, and six additional races. Resistance was observed to all the races evaluated. Molecular markers confirmed the presence of Sr7a, Sr24, Sr31, Sr38 and Sr57 in bread wheat, and Sr13 in durum wheat. The re-emergence of wheat stem rust in Spain and the occurrence of unique virulences underscore the need to continue surveying and monitoring this disease.     

Molecular mapping of Asian soybean rust resistance in soybean landraces PI 594767A,PI 587905 and PI 416764

Asian soybean rust (ASR), caused by Phakopsora pachyrhizi, is one of the most serious diseases of soybean. The soybean landraces PI 594767A, PI 587905 and PI 416764 previously showed high levels of resistance to a wide range of ASR fungus, while the genetic basis of the resistance has yet to be understood. In this study, the ASR resistance loci were mapped using three independent mapping populations, POP‐1, POP‐2 and POP‐3 derived from crosses BRS184 × PI 594767A, BRS184 ×  PI 587905 and BRS184 × PI 416764, respectively. In each population, the resistance to ASR segregated as a single gene, but the resistance was dominant in PI 594767A and PI 587905 and incompletely dominant in PI 416764. The resistance genes from both PI 594767A and PI 587905 were mapped on chromosome 18 corresponding to the same location as known resistance locus Rpp1. Quantitative trait locus (QTL) analysis performed on POP‐3 identified the putative ASR resistance locus in PI 416764 on the defined region of chromosome 6 where Rpp3 was located. The QTLs detected by the mapping explained about 67–72% of the phenotypic variation in POP‐3. Cluster analysis based on disease reactions to 64 ASR populations demonstrated the presence of at least two types of functional resistant Rpp1 alleles: strong and weak allele(s), e.g. soybean accession PI 594767A and PI 587905 carry the strong resistant Rpp1 allele(s). Introducing or pyramiding strong Rpp1 allele(s) in elite soybean cultivars is expected to be useful against the South American rust population.     

PUCREC/PUCTRI – a decision support system for the control of leaf rust of winter wheat and winter rye*

During a three‐year project from 2003 to 2006, two models have been developed to predict leaf rust (Puccinia recondita and P. triticina) occurrence and to simulate disease incidence progress curves on the upper leaf layers of winter rye (PUCREC) and winter wheat (PUCTRI). As input parameters the models use air temperature, relative humidity and precipitation. PUCREC and PUCTRI firstly calculate daily infection favourability and a cumulative infection pressure index and, in a second step, disease incidence is estimated. An ontogenetic model (SIMONTO) is used to link disease predictions to crop development. PUCREC and PUCTRI have been validated with data from 2001 to 2005. Both models give satisfactory results in simulating leaf rust epidemics and forecasting dates when action thresholds for leaf rust control are exceeded.     

The origin and genetic diversity of the causal agent of Asian soybean rust,Phakopsora pachyrhizi,in South America

A sequence‐based approach was used to investigate molecular genetic variations in Phakopsora pachyrhizi, an obligate biotrophic pathogen that causes Asian soybean rust. In Argentina, the samples came from uredinium‐bearing leaves taken from 11 soybean fields; in Brazil, the samples comprised urediniospores from leaves of 10 soybean genotypes that had been grown in three experimental stations during two growing seasons. PCR‐based cloning techniques were used to generate DNA sequences for two gene regions and alignments were supplemented with data from GenBank. A total of 575 sequences for the internal transcribed spacer region (18 ribotypes) and 160 partial sequences for a housekeeping gene encoding ADP‐ribosylation factor (10 haplotypes) were obtained. Ribotype accumulation curves predicted that about 20 bacterial clones would recover 5–6 ribotypes (c. 70–80% of the total molecular variation) per locality. The samples from the three experimental stations in Brazil displayed most (14 out of 16) ribotypes found worldwide; the lack of genetic structure and differentiation at a diverse geographic scale suggests that both local and distant sources provide airborne inoculum during disease establishment. Soybean genotypes with resistance genes for the Asian soybean rust did not decrease the molecular genetic variation of fungal populations.     

First report of rust disease on ohia and the causal fungus, <Emphasis Type="Italic">Puccinia psidii</Emphasis>, in Japan

In 2007, a rust disease of ohia (Metrosideros polymorpha) was found in Japan. We identified this pathogen as Puccinia psidii based on its morphological characters and the internal transcribed spacer (ITS) sequence of the ribosomal DNA. This pathogen was pathogenic on Eucalyptus amplifolia and E. rudis in addition to previously reported host species. This is the first report in Japan of a rust disease on ohia and the occurrence of its causal fungus, P. psidii.     

小麦条锈病菌和白粉病菌多重TaqMan Real-time PCR方法的建立

<正>小麦条锈病(Puccinia striiformis f.sp.tritici,Pst)和小麦白粉病(Blumeria graminis f.sp.tritici,Bgt)是我国小麦生产上的重要病害。条锈病主要发生在西北、华北、长江中下游和西南各省、自治区;白粉病则在西南各省和河南、山东、湖北、江苏、安徽等省发生较重,且西北、东北麦区也日趋严重[1]。条锈病菌依靠夏孢子造成小麦初侵染和再侵染并随气流远距离传播导致大区流行,白粉病菌则依赖于分生孢子或子囊孢子进行初侵染和再侵染。二者作为典型的气传病害,空中的接种体在