Taxonomy,distribution and biology of lettuce powdery mildew (Golovinomyces cichoracearum sensu stricto)

This paper reviews the taxonomy, biology, importance, host–pathogen interactions and control of lettuce powdery mildew. The main causal agent of this disease, Golovinomyces cichoracearum s.s., is an important powdery mildew pathogen of many members of the family Asteraceae. The pathogen is distributed worldwide and occurs on Lactuca sativa as well as wild Lactuca spp. and related taxa (e.g. Cichorium spp.). Powdery mildew of lettuce can be a major problem in production areas with favourable environmental conditions for disease development (dry, hot weather). The fungus grows ectophytically and appears as white, powdery growth on both the upper and lower sides of leaves. There is rather limited information on the geographic distribution of powdery mildew on wild Lactuca spp. Most L. sativa cultivars have been found to be susceptible. Large variability in virulence was confirmed and existence of different races is supposed. Resistance in L. sativa and some related wild Lactuca spp. is characterized by race‐specificity, but the genetic background of resistance is poorly understood. Sources of resistance are known in L. saligna and L. virosa. Lettuce powdery mildew can be effectively controlled by common fungicides (e.g. sulphur, myclobutanil, quinoline, strobilurins, etc.) and protective compounds (e.g. extract of neem oil, Reynoutria sachaliensis extracts). However, fungicide resistance may arise. Non‐fungicidal activators of plant systemic acquired resistance (SAR) had no direct effect on the causal agent. Future issues regarding lettuce powdery mildew research are summarized.     

The reliability of leaf bioassays for predicting disease resistance on fruit: a case study on grapevine resistance to downy and powdery mildew

This study was designed to assess the reliability of grapevine leaf bioassays for predicting disease resistance on fruit in the field. The efficacy of various grapevine quantitative trait loci (QTLs) for conferring resistance to downy and powdery mildew was evaluated in bioassays and in a 2‐year field experiment for downy mildew. The resistance genes studied were inherited from Muscadinia rotundifolia (Rpv1 and Run1) and from American Vitis species through cv. Regent (QTLRgP and QTLRgD). In bioassays, genotypes carrying Run1 blocked powdery mildew development at early stages. Genotypes combining Run1 with QTLRgP displayed no greater level of resistance. For downy mildew, genotypes carrying Rpv1 and/or QTLRgD were more resistant than the susceptible cv. Merlot, and showed a high level of leaf resistance in the field (<10% severity). Disease levels on bunches were much higher than those on leaves, with a high variability between Rpv1 genotypes (1–48%). A Bayesian decision theory framework predicted that an OIV‐452 threshold of 5 in leaf bioassays allowed accurate selection of grapevine genotypes (P = 0·83) with satisfactory disease severity on bunches. Therefore, this study validates that the use of early bioassays on leaves, as currently performed by grapevine breeders, ensures a satisfactory level of resistance to downy mildew of bunches in the field.     

Quantitative trait loci associated with resistance to a potato isolate of Verticillium albo‐atrum in Medicago truncatula

Verticillium albo‐atrum is responsible for considerable yield losses in many economically important crops, among them alfalfa (Medicago sativa). Using Medicago truncatula as a model for studying resistance and susceptibility to V. albo‐atrum, previous work has identified genetic variability and major resistance quantitative trait loci (QTLs) to Verticillium. In order to study the genetic control of resistance to a non‐legume isolate of this pathogen, a population of recombinant inbred lines (RILs) from a cross between resistant line F83005.5 and susceptible line A17 was inoculated with a potato isolate of V. albo‐atrum, LPP0323. High genetic variability and transgressive segregation for resistance to LPP0323 were observed among RILs. Heritabilites were found to be 0·63 for area under the disease progress curve (AUDPC) and 0·93 for maximum symptom score (MSS). A set of four QTLs associated with resistance towards LPP0323 was detected for the parameters MSS and AUDPC. The phenotypic variance explained by each QTL (R²) was moderate, ranging from 4 to 21%. Additive gene effects showed that favourable alleles for resistance all came from the resistant parent. The four QTLs are distinct from those described for an alfalfa V. albo‐atrum isolate, confirming the existence of several resistance mechanisms in this species. None of the QTLs co‐localized with regions involved in resistance against other pathogens in M. truncatula.     

Mining wild barley for powdery mildew resistance

Powdery mildew, caused by Blumeria graminis f. sp. hordei (Bgh), is a worldwide disease problem on barley (Hordeum vulgare) with potentially severe impact on yield. Historically, resistance genes have been identified chiefly from cultivated lines and landraces; however, wild barley (H. vulgare subsp. spontaneum) accessions have proven to be extraordinarily rich sources of powdery mildew resistance. This study describes the characterization of a collection of 316 wild barley accessions, known as the Wild Barley Diversity Collection (WBDC), for resistance to powdery mildew and the genetic location of powdery mildew resistance loci. The WBDC was phenotyped for reaction to 40 different Bgh isolates at the seedling stage and genotyped with 10 508 molecular markers. Accessions resistant to all 40 isolates of Bgh were not found; however, three accessions (WBDC 053, 085 and 089) exhibited resistance to 38 of the isolates. Gene postulation analyses revealed that many accessions, while resistant, contained none of the 12 genes present in the Pallas near‐isogenic lines Mla1, Mla3, Mla6, Mla7, Mla9, Mla12, Mla13, Mlk1, MlLa, Mlg, Mlat and Ml(Ru2), suggesting that the accessions carry novel genes or gene combinations. A genome‐wide association study of powdery mildew resistance in the WBDC identified 21 significant marker‐trait associations that resolved into 15 quantitative trait loci. Seven of these loci have not been previously associated with powdery mildew resistance. Taken together, these results demonstrate that the WBDC is a rich source of powdery mildew resistance, and provide genetic tools for incorporating the resistance into barley breeding programmes.     

Resistance to powdery mildew (Blumeria graminis f.sp. avenae) in oat seedlings and adult plants

In this work, 165 Avena sativa and Avena byzantina accessions were screened for resistance to powdery mildew caused by Blumeria graminis f.sp. avenae and the defence mechanisms of resistant plants were further characterized. Ten resistant and moderately resistant accessions were selected according to macroscopic assessment. A detailed histological study of selected genotypes showed a range of defence mechanisms, acting alone or in combination, that impeded fungal development at different stages. Since the resistance observed in the collection was scarce, a study of adult plant resistance was carried out in 45 genotypes selected from field trials. Nine oat landraces and two commercial varieties showed very high levels of adult plant resistance. A detailed study of the components of the adult plant resistance revealed a high increase of penetration and post‐haustorial resistance in the fifth compared to the first leaves. Identification of the resistance sources and characterization of underlying defence mechanisms will be useful for future breeding programmes and for further cellular and molecular studies to unravel the genetic basis of resistance, in this species in particular and in cereal–powdery mildew interactions in general.     

Identification and characterization of sources of resistance in Avena sativa,A. byzantina and A. strigosa germplasm against a pathotype of Puccinia coronata f.sp. avenae with virulence against the Pc94 resistance gene

An isolate of Puccinia coronata f.sp. avenae with virulence against the oat crown rust resistance gene Pc94 was discovered in oat fields in Córdoba, Spain. In order to identify alternative sources of resistance to this virulent isolate, a collection of 159 Avena accessions, including 107 A. sativa and 29 A. byzantina landraces and 23 commercial A. sativa and A. strigosa cultivars, was screened. Eight resistant landraces and four cultivars were selected according to macroscopic assessment to further characterize the operative defence mechanisms. Histological studies showed a range of defence mechanisms, acting alone or in combination, which impeded fungal development at different stages. Some accessions allowed reduced fungal growth before mesophyll penetration. In others, the fungus was arrested at the penetration stage by mesophyll cell wall strengthening and/or papilla deposition. Mesophyll cells of several accessions were penetrated by the fungus, but then the hypersensitive response (HR) leading to cell death hampered fungal development. In some cases cell death was very fast and colonies aborted early, whereas in other cases necrosis was observed later and associated with numerous secondary hyphae, suggesting a slow HR. Characterization of defence mechanisms will be useful for breeding programmes and for further cellular and molecular studies to unravel the bases of resistance. Commonalities with the resistance of the same oat collection to powdery mildew are discussed.     

Mechanisms of powdery mildew resistance of wheat – a review of molecular breeding

Powdery mildew (Blumeria graminis f. sp. tritici) results in serious economic loss in wheat production. Exploration of plant resistance to wheat powdery mildew over several decades has led to the discovery of a wealth of resistance genes and quantitative trait loci (QTLs). We have provided a comprehensive summary of over 200 powdery mildew genes (permanently and temporarily designated genes) and QTLs reported in common bread wheat. This highlights the diverse and rich resistance sources that exist across all 21 chromosomes. To manage different data for breeders, here we also present a bridged mapping result from previously reported powdery mildew resistance genes and QTLs with the application of a published integrated wheat map. This will provide important insights to empower further breeding of powdery mildew resistant wheat via marker-assisted selection (MAS).     

Resistant accessions of wild Psidium spp. to Meloidogyne enterolobii and histological characterization of resistance

Meloidogyne enterolobii has been reported in some states of Brazil and other countries causing severe damage on commercial guava (Psidium guajava). The use of resistant varieties is the most effective way to manage nematode parasitism. This study screened 51 accessions of Psidium spp. selected from the Psidium Germplasm Collection (Embrapa) to look for resistance against M. enterolobii. Six months after inoculation, nematode reproduction factor (RF) was used to assess resistance. The following species were resistant to M. enterolobii: P. cattleianum (yellow guava), P. friedrichsthalianum (Costa Rican guava), Acca sellowiana (feijoa) and P. rufum (purple guava). All 43 wild accessions of P. guajava were susceptible, as well as three accessions of P. guineense (Brazilian guava), one of P. acutangulum (pear guava) and the susceptible control P. guajava cv. Paluma. When used as rootstocks under greenhouse conditions, P. cattleianum and P. friedrichsthalianum were compatible with cv. Paluma; however, in greenhouse and field conditions only 50% of both scions survived. No apparent hypersensitive response (HR) was seen in the resistant guava P. cattleianum and P. friedrichsthalianum. Juveniles were able to develop normal feeding sites similar to those in susceptible roots 6–13 days after inoculation (dai). From 27 to 32 dai, giant cell deterioration was observed and nematodes showed arrested development. The majority of nematodes failed to reach maturity and did not begin laying eggs in resistant roots. These results suggested that the induction of resistance is relatively late in this pathosystem.     

Induced resistance to foliar diseases by soil solarization and Trichoderma harzianum

The effect of soil solarization and Trichoderma harzianum on induced resistance to grey mould (Botrytis cinerea) and powdery mildew (Podosphaera xanthii) was studied. Plants were grown in soils pretreated by solarization, T. harzianum T39 amendment or both, and then their leaves were inoculated with the pathogens. There was a significant reduction in grey mould in cucumber, strawberry, bean and tomato, and of powdery mildew in cucumber, with a stronger reduction when treatments were combined. Bacillus, pseudomonad and actinobacterial communities in the strawberry rhizosphere were affected by the treatments, as revealed by denaturing gradient gel electrophoresis fingerprinting. In tomato, treatments affected the expression of salicylic acid (SA)‐, ethylene (ET)‐ and jasmonic acid (JA)‐responsive genes. With both soil treatments, genes related to SA and ET – PR1a, GluB, CHI9 and Erf1 – were downregulated whereas the JA marker PI2 was upregulated. Following soil treatments and B. cinerea infection, SA‐, ET‐, and JA‐related genes were globally upregulated, except for the LOX genes which were downregulated. Upregulation of the PR genes PR1a, GluB and CHI9 in plants grown in solarized soil revealed a priming effect of this treatment on these genes' expression. The present study demonstrates the capacity of solarization and T. harzianum to systemically induce resistance to foliar diseases in various plants. This may be due to either a direct effect on the plant or an indirect one, via stimulation of beneficial microorganisms in the rhizosphere.     

Complex interplay of future climate levels of CO2, ozone and temperature on susceptibility to fungal diseases in barley

Barley (Hordeum vulgare) was grown in different climatic environments with elevated [CO₂] (700 vs 385 ppm), [O₃] (60/90 vs 20 ppb) and temperature (24/19 vs 19/12°C day/night) as single factors and in combinations, to evaluate the impact of these climatic factors on photosynthesis and susceptibility to powdery mildew and spot blotch disease. No significant increase in net CO₂ assimilation rate was observed in barley grown under elevated [CO₂] at ambient temperature. However, this rate was positively stimulated under elevated temperature together with a slightly higher potential quantum efficiency of PSII, both at ambient and elevated [CO₂], suggesting that photosynthesis was not limited by [CO₂] at ambient temperature. When growing under elevated temperature or [O₃], infection by the biotrophic powdery mildew fungus decreased, whereas disease symptoms and growth of the toxin‐secreting hemibiotrophic spot blotch fungus increased compared to ambient conditions, implying that climate‐induced changes in disease severity could be linked to the trophic lifestyle of the pathogens. Elevated [CO₂] decreased powdery mildew infection but had no effect on spot blotch disease compared to ambient condition. However, the effect of elevated [CO₂], [O₃] and temperature did not act in an additive manner when combined. This led to a surprising disease development in the combination treatments, where powdery mildew infection increased despite the individual reducing effect of the climatic factors, and spot blotch disease decreased despite the individual promoting effect of temperature and ozone, emphasizing the importance of conducting multifactorial experiments when evaluating the potential effects of climate change.     

Evaluation of triticale accessions for resistance to wheat bacterial leaf streak caused by Xanthomonas translucens pv. undulosa

The bacterium Xanthomonas translucens pv. undulosa (Xtu) causes bacterial leaf streak (BLS) on wheat and other small grains. Several triticale accessions were reported to possess high levels of resistance to wheat Xtu strains. In this study, a worldwide collection of triticale accessions as well as the major North Dakota hard red spring and durum wheat cultivars were evaluated for reaction to two local Xtu strains. All wheat cultivars showed a susceptible reaction but a wide range of reactions was observed among triticale accessions. Out of the 502 accessions tested, 45 and 10 accessions were resistant to the two virulent strains BLS‐LB10 and BLS‐P3, respectively, with five accessions, PI 428736, PI 428854, PI 428913, PI 542545 and PI 587229, being highly resistant to both strains. Statistical analysis showed significant difference among the accessions, strains, and the accession by strain interaction (P < 0.001). Bacterial population growth in resistant triticale was significantly slower than that in susceptible triticale. Molecular cytogenetic characterization in four representative triticale accessions confirmed the hexaploid level of the species and the presence of 12 or 14 rye chromosomes. The triticale accessions identified are valuable materials for developing wheat germplasm with high levels of BLS resistance.     

Identification and distribution of mating‐type idiomorphs in populations of Podosphaera macularis and development of chasmothecia of the fungus

Podosphaera macularis, the causal agent of hop powdery mildew, is known to produce chasmothecia (formerly cleistothecia) in eastern North America and Europe. Ascocarps have not yet been reported from the Pacific Northwestern region of North America. Reasons for the apparent absence of chasmothecia in the Pacific Northwest were unknown. This study established that P. macularis is heterothallic and ascocarp ontogeny, maturation, dehiscence and ascospore infection proceed similarly to other powdery mildew fungi. Genome sequencing of a MAT1‐1 isolate revealed the structure of the MAT1 locus and presence of MAT1‐1‐3, demonstrating further similarities to other powdery mildew fungi. PCR assays with primers designed from conserved domains of the MAT1 idiomorphs were developed to characterize the frequency of idiomorphs in populations of P. macularis. Amongst 317 samples of P. macularis collected during 2012 and 2013 from the Pacific Northwest only the MAT1‐1 idiomorph was found. In contrast, among 56 samples from the eastern United States and Europe, MAT1‐1 and MAT1‐2 idiomorphs were detected at equivalent frequencies. At temperatures representative of late season conditions in the Pacific Northwest, chasmothecia formed readily when a Pacific Northwest MAT1‐1 isolate was paired with a MAT1‐2 isolate collected from outside the region. Although these findings do not encompass all climatic, geographic or temporal barriers that could inhibit the formation of chasmothecia, the current absence of the ascigerious stage of P. macularis in the Pacific Northwest could be explained by the absence of the MAT1‐2 mating type idiomorph.     

黄瓜白粉病菌在不同抗性黄瓜材料上的侵染过程

白粉病是黄瓜生产中发生普遍,危害严重的主要病害之一。pm5.1和PM5.2是黄瓜上的2个白粉病抗性位点,本文对7份不同抗病基因型的黄瓜自交系进行了黄瓜白粉病抗性鉴定,并开展了黄瓜白粉病菌侵染过程的研究,对侵染后12、24、72 h的萌发率、菌丝形成率及菌落形成率等进行了分析。结果表明,当基因型为PM5.1PM5.1 pm5.2pm5.2时,黄瓜病情指数最高,表现为高感白粉病;当基因型为PM5.1PM5.1PM5.2 PM5.2和pm5.1pm5.1pm5.2pm5.2时,表现为中感白粉病;当基因型为pm5.1pm5.1PM5.2PM5.2时黄瓜自交系病情指数最低,表现为抗白粉病。分生孢子在抗、感黄瓜自交系植株叶片上均能萌发,但只能在感病黄瓜材料上完成整个无性生长周期,产生分生孢子。此外,黄瓜白粉病菌分生孢子在感病材料上的萌发率、菌丝形成率及菌落形成率均高于抗病材料。     

Differential interactions between strains of Rhizorhapis,Sphingobium, Sphingopyxis or Rhizorhabdus and accessions of Lactuca spp. with respect to severity of corky root disease

Over 100 isolates of Rhizorhapis suberifaciens, Sphingobium (Sb.) sp., Sb. mellinum, Sb. xanthum, Rhizorhabdus sp., and Sphingopyxis sp. (Sphingomonodaceae) were tested for pathogenicity on lettuce (Lactuca sativa) cultivars Salinas and Green Lakes, susceptible and resistant, respectively, or their resistant descendent breeding line (B.L.) 440‐8, to R. suberifaciens type strain CA1^T. Rhizorhabdus sp. CA15 and NL2, R. suberifaciens CA3, and Sphingopyxis CA32 were equally virulent to Green Lakes or B.L. 440‐8 and Salinas. Over 40 accessions from four Lactuca species were tested for resistance to R. suberifaciens CA1^T/CA3 or Rhizorhabdus sp. CA15/NL2. All lettuce accessions with resistance to CA1^T were susceptible to isolates CA15, NL2 and/or CA3. None of the Lactuca lines were highly resistant to all four isolates. There was a significant differential interaction between eight Lactuca lines and ten isolates of Rhizorhapis and related genera with respect to corky root severity. Three strains of isolates were distinguished: (i) isolates with a similar virulence pattern as R. suberifaciens CA1^T, (ii) isolates with a virulence pattern similar to that of R. suberifaciens CA3 and Sphingopyxis sp. CA32, and (iii) isolates of Rhizorhabdus being moderately aggressive to all Lactuca lines. Thus, strains belonging to several genera can cause similar symptoms (a rare phenomenon) but have different virulence patterns on Lactuca species and cultivars.     

Field evaluation of mungbeans for resistance to Cercospora leaf spot and powdery mildew

Abstract

Cercospora leaf spot, caused by Cercospora canescens and powdery mildew, caused by Erysiphe polygoni are two of the most important fungal diseases of mungbeans. Nearly 4000 accessions of the global mungbean collection at the Asian Vegetable Research and Development Center were screened for resistance to these two pathogens. Less than 4% and 12% of the accessions showed resistance to Cercospora leaf spot and powdery mildew, respectively. The level of resistance to Cercospora leaf spot varied and highly resistant lines were not found. A few lines were rated highly resistant to powdery mildew over several years but others were rated moderately resistant or susceptible in other years.     

Cucumis metuliferus is resistant to root‐knot nematode Mi1.2 gene (a)virulent isolates and a promising melon rootstock

Pot experiments were carried out to characterize the response of two Cucumis metuliferus accessions (BGV11135 and BGV10762) against Mi1.2 gene (a)virulent Meloidogyne arenaria, M. incognita and M. javanica isolates and to determine the compatibility and the effect on physicochemical properties of fruit melons. In addition, histopathological studies were conducted. One week after transplanting, plants were inoculated with one J2 cm^?3 of sterilized sand (200 cm³ pots) and maintained in a growth chamber at 25 °C for 40 days. The susceptible cucumber cv. Dasher II or melon cv. Paloma were included for comparison. The number of egg masses and number of eggs per plant were assessed, and the reproduction index (RI) was calculated as the percentage of eggs produced on the C. metuliferus accessions compared to those produced on the susceptible cultivars. The compatibility and fruit quality were assessed by grafting three scions, two of Charentais type and one of type piel de sapo, under commercial greenhouse conditions. The resistance level of both C. metuliferus accessions ranged from highly resistant (RI < 1%) to resistant (1% ≤ RI ≤ 10%) irrespective of Meloidogyne isolates. Melon plants grafted onto C. metuliferus accession BGV11135 grew as self‐grafted plants without negatively impacting fruit quality traits. Giant cells induced by Meloidogyne spp. on C. metuliferus were in general poorly developed compared to those on cucumber. Furthermore, necrotic areas surrounding the nematode were observed. Cucumis metuliferus accession BGV11135 could be a promising melon rootstock to manage Meloidogyne spp., irrespective of their Mi1.2 (a)virulence, without melon fruit quality reduction.     

Evaluation of mulberry germplasm for resistance to powdery mildew in the field and greenhouse

Powdery mildew caused by the ascomycete Phyllactinia guttata (syn. P. corylea) is a major foliar disease worldwide of the unique mulberry (Morus spp.) for silkworm feed. Genetic resistance to powdery mildew, the most sustainable and economical strategy for disease control, is still elusive for tropical mulberry. About 147 germplasm sources, representing 18 countries of origin, were screened for resistance to P. guttata in six seasonal fields and greenhouse trials after exposure to natural and artificial inoculum, respectively. In the field, the level of plant responsiveness to disease was assessed from 30 to 62 days after pruning in each season as variations in the disease severity index (DSI), disease incidence (DI%) and area under the disease progress curve (AUDPC). These measures differed significantly among the germplasm. Of 147 germplasm sources, ~6.8% had useful resistance (two high and nine moderately resistant) to the powdery mildew pathogen on the basis of DSI. The AUDPC values were 13.5-fold higher in the most susceptible accession—(Philippines) than the least responsive (Vietnam-2). The results of DSI were strongly correlated with the obtained DI values (r = 0.92; P < 0.01) and AUDPC (r = 0.89; P < 0.01). Moreover, field screening results were highly correlated (R ² = 0.839) with values from the greenhouse evaluation using artificial inoculum. However, the DSI values in field and greenhouse screenings for three sources (Non-nayapati, Nao-khurkul and Tista Valley) varied significantly. A relatively low disease reaction of 09 resources (Vietnam-2, Ankara and 07 others) using different assessment scales after natural and artificial inoculation prove, for the first time, that they have potential in breeding for resistance in tropical mulberry to powdery mildew.     

Crop damage caused by powdery mildew on hop and its relationship to late season management

Powdery mildew of hop (Podosphaera macularis) may cause economic loss due to reductions in cone yield and quality. Quantitative estimates of crop damage from powdery mildew remain poorly characterized, especially the effect of late season disease management on crop yield and quality. Field studies in Washington State evaluated cone yield, bittering acid content and quality factors when fungicide applications were ceased at different stages of cone development. The incidence of cones with powdery mildew was linearly correlated with yield of cones, bittering acids and accelerated cone maturation. In cultivar Galena, the cumulative effect of every 1% increase in cones powdery mildew incidence was to reduce alpha‐acid yield by 0·33%, which was due to direct effects on cone yield but also indirect effects mediated by dry matter. In the more susceptible cultivar Zeus, alpha‐acid yield was increased 20% by controlling powdery mildew through the transition of bloom to early cone development compared to ceasing fungicide applications at bloom: additional applications provided only modest improvements in alpha‐acid yield. In both cultivars, the impact of powdery mildew on aroma characteristics and bittering acid content were less substantial than cone yield. The damage caused by powdery mildew to cone colour and alpha‐acid yield, as well as the effectiveness of fungicide applications made to manage the disease, appears inseparably linked to dry matter content of cones at harvest. Realising achievable yield potential in these cultivars requires control of the disease through early stages of cone development and harvest before maturity exceeds c. 25% dry matter.