Variation in severity of cashew powdery mildew (Oidium anacardii Noack) disease in Tanzania: Implications for research and extension

Abstract

Cashew trees in farmers’ fields in two contrasting areas in southern Tanzania were surveyed for growth, powdery mildew development, amounts and applications of sulphur, pest damage and nut yield by village‐based extension workers in 1993. There was a wide range of powdery mildew levels on cashew flowers, apples and nuts at both the Tunduru (inland) and Newala (western Makonde plateau). In both Newala and Tunduru application of sulphur dust was associated with reduced severity of blossom powdery mildew. Sulphur usage commenced later in Newala than Tunduru though this was associated with earlier onset of blossoming in the latter district. Farmers in both areas applied similar numbers of rounds of sulphur, however in Newala more sulphur was applied per tree reflecting the bigger trees found in this district. There was a highly significant (P < 0.001) negative association between use of sulphur and severity of blossom powdery mildew irrespective of nut yield. There was a strong positive association (P < 0.01) between use of sulphur and more than one nut per panicle from harvests in October, no significant association in November and a significant negative association (P < 0.05) between use of sulphur and more than one nut per panicle in December. The survey highlighted areas in Newala where there were higher powdery mildew levels, through either lack of sulphur application or poor control by late application of sulphur, with relatively high numbers of nuts per panicle. Conversely, areas were identified where despite control of cashew powdery mildew severity by application of sulphur nut yield remained relatively low. The results suggest that final yield results from an interaction of factors of which cashew powdery mildew is only one. There was a highly significant (P < 0.01) association between the number of sulphur rounds and severity of cashew powdery mildew (Newala data only) but no significant association between number of rounds of sulphur and yield taken during October. Pest damage estimates from cashew nuts showed no consistent pattern in either region. Survey results suggest that there is considerable potential in the optimization of sulphur usage as a strategy for control of powdery mildew.     

Variation in the response of cashew genotypes to the targeted application of fungicide to flower panicles for control of powdery mildew disease

Application of the fungicide triadimenol (Bayfidan) directly to inflorescences of cashew was investigated as a means of controlling powdery mildew disease caused by Oidium anacardii. Disease development and nut production were studied in 12 cashew genotypes that differed in their susceptibility to mildew. Panicle colonization by O. anacardii reached 100% coverage in all genotypes without fungicide treatment, but rates of infection differed significantly. Triadimenol sprays reduced mildew to less than 9%, even in panicles of highly susceptible genotypes. In the absence of disease, particularly good yield responses with more than nine times more nuts set than untreated controls were achieved by AM6 and AC1, which were categorized as highly susceptible and intermediate, respectively, in reaction to powdery mildew. By contrast, the partially resistant genotypes AZA2 and AC6 both produced yield response ratios of less than 3·0. The targeted treatment of flower panicles to control mildew is recommended, rather than the current practice of wastefully treating whole trees on which all mature leaves are naturally immune to infection.     

Morphological,molecular phylogenetic and pathogenic analyses of Erysiphe spp. causing powdery mildew on cashew plants in Brazil

Cashew powdery mildew is presently the most important disease of cashew trees in all Brazilian growing regions. Although it was described over a century ago, it had never threatened the Brazilian cashew industry until the first decade of the 21st century. Morphological and pathogenic evidence indicated the possibility of different pathogen species being involved in early and late types of cashew powdery mildew. This study was designed to elucidate this issue by comparing two different powdery mildew fungi occurring on cashew plants in Brazil according to the morphological characteristics, phylogenetic relationships with closely related powdery mildew fungi and pathogenic relationships. Based on morphology, molecular phylogenetics and pathogenicity on cashew, it was shown that two species of powdery mildew specimens are without question associated with cashew trees. One species, which infects young immature tissues such as shiny leaves, flowers and young fruits, is Erysiphe quercicola, while Erysiphe necator is associated exclusively with mature leaves. This is the first report of both E. quercicola and E. necator causing cashew powdery mildew, and the first detection of E. necator on cashew.     

The effect of temperature on colony growth by Erysiphe sp. infecting Rhododendron

The growth and reproduction of powdery mildew pathogens is generally encouraged by increasing temperatures, up to 25°C. Germination and germ tube extension of Erysiphe sp. on Rhododendron cv. Elizabeth were optimal at 20°C for conidia originally formed at either 10 or 15°C. During a 50-day period of colony growth, the viability of conidia formed at 15°C declined but for those formed at 10°C it increased. The expansion of Erysiphe colonies over an initial 12-day period was favoured by incubation at 15°C compared with 10 or 20°C. In the first 8 to 10 days of growth, secondary and tertiary hyphae formed most rapidly at 20°C. After 12 days, expansion of colonies at 20°C was limited to the area initially infested by primary hyphae, whereas in colonies grown at 10 and 15°C secondary and tertiary hyphae had extended beyond the area first colonized. Small colonies of densely packed hyphae formed at 20°C compared with open spreading colonies observed at 10 and 15°C.     

Comparative analysis of powdery mildew development on leaves, seedlings and flower panicles of different genotypes of cashew

Resistance of cashew ( Anacardium occidentale ) genotypes to powdery mildew ( Oidium anacardii ) was assessed on detached leaves, seedlings and flower panicles. Leaves were more susceptible before the development of a waxy cuticle, which confers a dull appearance. Differences in susceptibility/resistance were observed on detached leaves inoculated in the laboratory. Some genotypes supported dense growth of mildew, whereas on others only slight infection was observed under comparable conditions. Mature leaves were immune to colonization. In the field the rate of mildew infection, as estimated from disease progress curves on both seedlings and flower panicles, varied significantly between genotypes allowing their categorization into susceptible and partially resistant clones. A similar rank order for degree of susceptibility/resistance was determined from studies on detached leaves, seedlings and flower panicles. Brazilian introductions of A. occidentale and the AZA2 and AC6 genotypes proved to be partially resistant, while AM6, ATA19 and AIN62 were highly susceptible. The relationship between leaf and flower mildew infection showed positive and highly significant correlations. It is concluded that each of the three approaches to the assessment of disease susceptibility can be used to screen genotypes against mildew attack. Screening in the laboratory provides a rapid indication of potential resistance providing that leaves are compared at the same stages of maturity.     

宁夏温室瓜菜白粉病菌鉴定及病害流行预测模型构建

为明确宁夏回族自治区温室瓜菜白粉病菌的分类地位,对采自该地区温室的南瓜、黄瓜和甜瓜上的白粉病菌基于ITS序列分析进行分子鉴定;利用孢子捕捉器对温室中甜瓜白粉病菌的孢子量进行监测,分析环境因子、孢子量和病情指数之间的关系,并采用逐步回归分析法构建温室甜瓜白粉病的流行预测模型。结果表明,基于ITS序列的分子鉴定结果,3种瓜菜白粉病的病原菌均为单囊壳白粉菌Podosphaera xanthii。发病期间,每日温室中甜瓜白粉病菌的孢子量在12:00—16:00时段最多,占24 h内总孢子量的34%~81%,20:00—08:00时段最少;白粉病菌孢子的释放与光照强度有关,相关系数为0.602。第t天的病情指数与标准累积温度、标准累积湿度、t-4 d前08:00—12:00时段的累积孢子量、第t-4天16:00—20:00时段的孢子量均具有显著的相关性,相关系数分别为0.935、0.938、0.956和0.921。以标准累积湿度和第t-4天16:00—20:00时段的孢子量为预测变量构建了温室甜瓜白粉病流行预测模型,决定系数为0.962,表明该模型具有较好的实际应用价值。     

Suppression of conidial germination and appressorial formation by silicate treatment in powdery mildew of strawberry

The mode of action of soluble silicon against strawberry powdery mildew (Sphaerotheca aphanis var. aphanis) was investigated in four experiments. First, silicon-treated leaves from plants grown with silicate (Si+) and control leaves were excised, inoculated with conidia, and subsequent germination and formation of appressoria in a petri dish was assessed after 24 h. The germination rate was 49.7% on Si+ leaves, and was 67.2% on control leaves (t-test, P < 0.01). Second, we soaked cellulose membranes in various solvents and then placed the membranes on 4% water agar, dusted the membranes with conidia, and examined after 12 h. No difference was apparent between any treatment and the control (distilled water). Third, strawberries growing hydroponically with additional silicon in the medium were inoculated with conidia, and leaves were observed with a scanning electron microscope 1–2 days after inoculation. Germ tubes and secondary hyphae were shorter and had fewer branches on Si+ leaves than on the control. Moreover, penetration appeared to be inhibited. Fourth, the cuticle was separated from leaves from plants grown as in the third experiment, placed on water agar, and dusted with conidia. Germination of conidia, observed with a light microscope, on Si+ leaves was suppressed markedly to 40%–60% of that of the control. These results suggested that soluble silicon induced physiological changes in the cuticle layer after absorption by the plant. In addition, soluble silicate reduced germination of conidia, formation of appressoria, and possibly the penetration of powdery mildew.     

Effects of temperature and leaf age on conidial germination and disease development of powdery mildew on rubber tree

Powdery mildew is an important disease of rubber trees worldwide. To assess the effects of temperature and leaf age on conidial germination and disease development, conidia were inoculated onto rubber tree seedlings with leaves at three phenological stages (copper bronze, colour-changing, and light green) and then incubated at six constant temperatures (10, 15, 20, 25, 30, and 35°C). Leaf age did not affect conidial germination (p = .296) whilst temperature did (p < .0001), although conidia were able to germinate at all tested temperatures. The estimated optimal temperature for conidial germination was 23.2°C. Leaf age, temperature, and their interactions had significant effects on conidial infection and hypha number (p < .0001). At 10 and 35°C, more than 2 and 4 days were needed for infection to complete, respectively, compared to <2, 1, 0.5, and 0.5 days for 15, 20, 25, and 35°C, respectively. Sporulation and mildew symptoms were only observed on those inoculated leaves of all stages at 20 and 25°C, and at the copper bronze stage only at 15°C. The latent period on the copper bronze leaves at 15°C was longer (9 days) than at 20 and 25°C (4 days). The latent period at 20 and 25°C increased from 4 to 7 days as the leaf development stage increased from copper bronze to light green. Therefore, temperature affected germination and postgermination growth of rubber tree powdery mildew, whereas leaf age primarily affected postgermination growth of the pathogen.     

Coincidence of maximum severity of powdery mildew on grape leaves and the carbohydrate sink‐to‐source transition

Grapevine leaves infected with powdery mildew are a source of inoculum for fruit infection. Leaves emerging on a single primary shoot of Vitis vinifera cv. Cabernet Sauvignon were exposed to average glasshouse temperatures of 18°C (0·23 leaves emerging/day) or 25°C (0·54 leaves emerging/day). All leaves on 8–10 shoots with approximately 20 leaves each were inoculated with Erysiphe necator conidia to assess disease severity after 14 days in the 25°C glasshouse. Two photosynthetic ‘source’ leaves per shoot on the remaining 8–10 shoots were treated with ¹⁴CO₂ to identify, by autoradiography, the leaf position completing the carbohydrate sink‐to‐source transition. There was a clear association between the mean modal leaf position for maximum severity of powdery mildew (position 3·7 for 18°C; position 4·4 for 25°C) and the mean position of the leaf completing the sink‐to‐source transition (position 3·8 for 18°C; position 4·7 for 25°C). The mean modal leaf position for the maximum percentage of conidia germinating to form secondary hyphae was 4·2 for additional plants grown in the 25°C glasshouse. A higher rate of leaf emergence resulted in a greater proportion of diseased leaves per shoot. A Bayesian model, consisting of component models for disease severity and leaf ontogenic resistance, had parameters representing the rate and magnitude of pathogen colonization that differed for shoots developing in different preinoculation environments. The results support the hypothesis that the population of leaves in a vineyard capable of supporting substantial pathogen colonization will vary according to conditions for shoot development.     

Epidemics of apple powdery mildew (Podosphaera leucotricha) in a mixed cultivar orchard

Epidemics of apple powdery mildew were monitored on leaves of vegetative extension shoots in a mixed-cultivar orchard in 1979. 1980 and 1981. Cultivars Cox's Orange Pippin. Golden Delicious. Ida Red and Suntan were very susceptible but little mildew developed on cv. Discovery in any year. Results with cvs Crispin and Spartan were less consistent due, in part, to differing patterns of vegetative growth. The rankings of cultivars for disease incidence (proportion of leaves with mildew), number of colonies and mildewed area were similar, and were also consistent on fungicide-sprayed and unsprayed trees in 1981. Less disease occurred on fungicide-treated Golden Delicious than on Cox's Orange Pippin. Most infections occurred on the rolled leaves at the shoot tip. Spore production was greatest on leaves at positions -1 to -4 where leaf 0 was the youngest and leaf - 1 the adjacent and older unrolled leaf.     

Deposits of the mildew fungicide binapacryl on the leaves of apple trees of differing sizes after mist blower spraying

Trials in 1975 and 1976 showed that deposit levels of the fungicide binapacryl, on the leaves of bush trees of Cox's Orange Pippin (Cox) after mist blower spraying, varied inversely with tree spread. Deposit levels were measured on young mildew-susceptible leaves from a well-sprayed zone around the periphery of the tree canopy at a height of 1.5 m. Low deposit levels in large, dense trees were associated with poor mildew control. Leaves from the smallest trees had deposit levels considerably greater than those found for larger trees (in another nearby orchard) which had adequate mildew control. Fungicide deposit levels on leaves from up to five different zones of trees of three different sizes (the largest trees were of the variety Bramley's Seedling) were measured in 1977. The smallest trees had significantly higher deposit levels than the larger trees in the lower centre and lower outside zones of the trees, whereas both orchards of Cox had the same (commercially acceptable) level of mildew infection at the end of the season. Leaves from zones less accessible to spray had lowerdeposit levels than those nearer the sprayer.     

Spatial pattern of black spot incidence within citrus trees related to disease severity and pathogen dispersal

Guignardia citricarpa , the causal agent of citrus black spot, forms airborne ascospores on decomposing citrus leaves and water-spread conidia on fruits, leaves and twigs. The spatial pattern of diseased fruit in citrus tree canopies was used to assess the importance of ascospores and conidia in citrus black spot epidemics in São Paulo State, Brazil. The aggregation of diseased fruit in the citrus tree canopy was quantified by the binomial dispersion index ( D ) and the binary form of Taylor's Power Law for 303 trees in six groves. D was significantly greater than 1 in 251 trees. The intercept of the regression line of Taylor's Power Law was significantly greater than 0 and the slope was not different from 1, implying that diseased fruit was aggregated in the canopy independent of disease incidence. Disease incidence ( p ) and severity ( S ) were assessed in 2875 citrus trees. The incidence-severity relationship was described ( R ² = 88·7%) by the model ln( S ) = ln( a ) +  b CLL( p ) where CLL = complementary log-log transformation. The high severity at low incidence observed in many cases is also indicative of low distance spread of G. citricarpa spores. For the same level of disease incidence, some trees had most of the diseased fruit with many lesions and high disease severity, whereas other trees had most of the fruit with few lesions and low disease severity. Aggregation of diseased fruit in the trees suggests that splash-dispersed conidia have an important role in increasing the disease in citrus trees in Brazil.     

Cytological events in tomato leaves inoculated with conidia of <Emphasis Type="Italic">Blumeria graminis</Emphasis> f. sp. <Emphasis Type="Italic">hordei</Emphasis> and <Emphasis Type="Italic">Oidium neolycopersici</Emphasis> KTP-01

Leaves of tomato and barley were inoculated with conidia of Blumeria graminis f. sp. hordei race 1 (R1) or Oidium neolycopersici (KTP-01) to observe cytological responses in search of resistance to powdery mildew. Both conidia formed appressoria at similar rates on tomato or barley leaves, indicating that no resistance was expressed during the prepenetration stage of these fungi. On R1-inoculated tomato leaves, appressoria penetrated the papillae, but subsequent haustorium formation was inhibited by hypersensitive necrosis in the invaded epidermal cells. On the other hand, KTP-01 (pathogenic to tomato leaves) successfully developed functional haustoria in epidermal cells to elongate secondary hyphae, although the hyphal elongation from some conidia was later suppressed by delayed hypersensitive necrosis in some haustorium-harboring epidermal cells. Thus, the present study indicated that the resistance of tomato to powdery mildew fungi was associated with a hypersensitive response in invaded epidermal cells but not the prevention of fungal penetration through host papilla.     

Culture in vitro of Rhododendron and Erysiphe sp.

Successful dual cultures of a powdery mildew pathogen and Rhododendron ponticum plantlets were achieved using a tissue culture technique. Sporulation was observed within 1 week of inoculation. Comparative in vitro cultures were grown at 10, 15 and 20°C with host tissue transferred to fresh media at 2-monthly intervals. Viable conidia capable of infecting host tissue in vivo were obtained from cultures maintained at 10 and 15°C after culture for more than 6 months. Isolates from three sources (Auchincruive, Benmore and Perth) were introduced into culture. Cultures inoculated with Perth and Benmore isolates exhibited increased host growth at 10 and 15°C, respectively compared with control plantlets. These effects may result from pathogen-induced changes to host regulatory metabolism. The culture technique allows the long-term maintenance of pathogen cultures under sterile conditions without requiring subculture.     

Effects of impacting rain drops on the growth and development of powdery mildew fungi

The effects of rain on different stages of powdery mildew development were investigated quantitatively for Erysiphe graminis on barley, Erysiphe pisi on pea and Sphaerotheca pannosa on rose. Water drops 4 mm in diameter released from a height of 2·5 m onto target leaves reduced the numbers of conidia on the impacted surfaces and inhibited subsequent mildew development, the effects declining as the interval between inoculation and impaction increased. Simulated rainfall applied after inoculation reduced the numbers of conidia on leaves and inhibited mildew development, the effect declining as the interval between inoculation and treatment lengthened. Simulated rainfall applied to infected plants reduced their capacity to inoculate other plants, the effect declining as the interval between treatment and use as inoculum lengthened. Controlled exposure of infected peas and roses to natural rain reduced the numbers of conidia on leaves and inhibited subsequent mildew development, especially on upper leaf surfaces.     

Effect of aerated compost tea on grapevine powdery mildew, botrytis bunch rot and microbial abundance on leaves

Aerated compost tea (ACT), prepared from immature compost, was applied to foliage and fruit of grapevines (Vitis vinifera) to assess its potential for suppressing two important diseases: botrytis bunch rot, caused by Botrytis cinerea, and powdery mildew, caused by Erysiphe necator. An ACT applied to leaves of Cabernet Sauvignon vines in pots 7 days before inoculation with E. necator conidia reduced mean powdery mildew severity on the three youngest expanded leaves (at inoculation) to less than 1 %; mean severity on non-treated, inoculated leaves was 15 %. Multiple applications of ACTs at two vineyards in different growing seasons suppressed powdery mildew to <1 % mean severity on Chardonnay leaves (non-treated 79 % severity) and bunches (non-treated 77 % severity), and on Riesling leaves (non-treated 24 % severity). The same treatments reduced the incidence of Chardonnay bunches with latent B. cinerea and Riesling bunches with sporulating B. cinerea, although the level of botrytis bunch rot in both experiments was not economically damaging. The numbers of culturable bacteria, fungi and yeasts on Chardonnay leaves were higher than pre-treatment levels 10 days after ACT application, as were fungal numbers on Riesling leaves 21 days after treatment. Suppression by ACTs of two fruit and foliar pathogens of grapevine with different biology and epidemiology indicated potential for their use as a tactic in integrated disease management. Further testing of ACTs in a range of viticultural environments and application regimes will contribute to a better understanding of the impact of this tactic on disease, grape and wine quality.     

Overwintering of Ampelomyces mycoparasites on apple trees and other plants infected with powdery mildews

Apple shoots and aerial parts of 13 other plant species infected with powdery mildews during the previous season were collected in late winter and early spring between 1998 and 2003 at a total of 34 sample sites in Hungary. Samples were examined for the presence of overwintering structures of Ampelomyces, common mycoparasites of powdery mildews. Pycnidia and resting hyphae resembling those of Ampelomyces were found on six plant species, including apple. Their viability and subsequent mycoparasitic activity of the hyphae emerging from the overwintered fungal structures were studied in vitro to determine whether they can serve as sources of primary inocula of Ampelomyces in the spring. Overwintered pycnidia of Ampelomyces collected in the spring, and produced in both the ascomata and the conidiophores of powdery mildews during the previous season, initiated the life cycle of these mycoparasites when placed close to fresh powdery mildew colonies in vitro. Similarly, thick-walled resting hyphae, found in the dried powdery mildew mycelia which covered the overwintered aerial parts of the host plants, also germinated and gave rise to new intracellular pycnidia of Ampelomyces when powdery mildew colonies were inoculated with them in vitro. On apple trees, Ampelomyces mycoparasites overwintered as resting hyphae in the dried powdery mildew mycelia covering the shoots and in the parasitized ascomata of Podosphaera leucotricha on the bark and the scales of the buds. Approximately 31% of the field samples collected from apple trees in spring between 1998 and 2003 contained overwintered structures of Ampelomyces. Artificial bursting of apple buds in the laboratory showed that both P. leucotricha and Ampelomyces start their life cycle during or soon after bud burst, but Ampelomyces can only slowly follow the spread of its mycohost on infected leaves. Most probably, the mycoparasites did not overwinter in the dormant hyphae of P. leucotricha in the buds, but only on the bark and the bud scales, as their hyphae were not found in the young hyphae of apple powdery mildew that appeared on the leaf tissues during bud burst. This study demonstrated that Ampelomyces mycoparasites can survive the winter in the field as pycnidia and as resting hyphae in the dried mycelia of their mycohosts.     

Susceptibility of grapevine buds to infection by powdery mildew Erysiphe necator

Bud colonization and perennation of powdery mildew ( Erysiphe necator ) was studied by inoculating shoots of grapevine ( Vitis vinifera cv. Carignane) at different phenological stages. Disease incidence and severity assessments indicated that buds were most susceptible at the three- to six-unfolded-leaf stage. Incidence of powdery mildew colonies on the surface of buds collected from these shoots 7 weeks postinoculation was highest at these stages (68 and 62%, respectively), which indicates that colonization of the bud interior via the infected bud surface is likely to occur within this period. Histological analyses of buds revealed hyphae with haustoria, conidiophores and conidia on all parts of the bud interior except for the meristems. In particular, trichomes were frequently parasitized by haustoria. In total, 13·2% of all buds analysed, and 32·3% of all buds originating from shoots inoculated at the three-unfolded-leaf stage, were infected by E. necator . In the spring of the following year, buds from inoculated shoots yielded 18 flag shoots (1·6% of all emerging shoots). These primary infections caused an epidemic 28 days after the appearance of the first flag shoot. A linear regression analysis on the frequency of infections of the bud exterior, bud interior and flag shoots revealed that incidence of external bud infection in the first season is strongly correlated with flag shoot incidence in the following season ( R ² = 0·94). Hence predictions of flag shoot incidence may be reliably based on the incidence of infection on the outer bud scales in the preceding season.     

The effect of humidity on the expression of partial resistance to powdery mildew in barley

Seedling leaves of four cultivars of barley, three of which express partial resistance, were inoculated with powdery mildew ( Erysiphe graminis f.sp. hordei ) and enclosed in an apparatus which enabled accurate control of humidity, air speed and temperature. Infection frequency was always greater at high humidity (>95%) than at low humidity (40–50%). Cultivar 7204 (Ethiopian) showed a greater reduction in infection frequency at both 12 and 16°C, and more reduction in biomass per colony at 16°C under low humidity than the other cultivars. The potential for exploiting such differences in barley breeding is discussed.