Candeia (Eremanthus erythropappus
(DC.) McLeish), is an important native species for wood production and the potential for essential oil extraction [1
]. Candeia occurs naturally in South America and can be found in northeastern Argentina, Northern and Eastern Paraguay [2
], and in several regions of Brazil, mainly in the Cerrado Biome [2
]. The oil extracted from this tree contains the compound alpha-bisabolol, which has been used in the pharmaceutical and cosmetic industries worldwide [4
]. Approximately 200 products contain alpha-bisabolol [5
] due to its anti-inflammatory, anti-irritant, and antimicrobial properties [4
]. Several plants produce this compound, but the essential oil of candeia has higher quality and concentration of this substance (70%), giving it greater economic viability [4
]. In addition, after extraction of the oil, candeia wood residue is an excellent option for use in the production of particle board, which has higher added value than lumber [6
Because of that and other characteristics, such as its ability to grow in difficult locations where it is not possible to grow other forest species or agricultural crops, candeia is an attractive option for forest cultivation [7
]. The exploitation of this forest species has intensified in recent years. In many areas, candeia is grown exclusively, providing environments that favor the emergence of several diseases. Among them, rust caused by Puccinia velata
] may become a limiting factor for the production of candeia due to the expansion of its planted area. This is because rusts in forest species are known to cause severe and premature defoliation, and the physiological damage reduces wood yield [9
]. P. velata
is described as occurring in trees over three years old and in adult leaves in the field [10
], which may decrease plant growth due to nutrient removal and leaf area reduction resulting from the formation of signs of the pathogen’s fungal structures and early leaf drop [11
]. Consequently, the photosynthetic area is reduced, delaying development of the plant resulting in reduced wood quality and yield.
In this context, despite the knowledge about the negative effect of rusts on hosts, there are no studies on the etiology or epidemiology of P. velata
on candeia trees. The characteristics that hinder the study of rusts include their biotrophic parasitism strategy because they grow only on their specific living hosts [12
]. After the first report of P. velata
in E. erythropappus
in 1897 by Dietel in Ouro Preto, Minas Gerais, few studies have been conducted on this pathogen. There is a report of its incidence in naturally occurring candeia forests [13
]. However, due to the increase in planted area, which favors the incidence of the disease in the field, the pathogen may become a problem for producers, necessitating studies on its behavior and control.
Thus, to identify management strategies for the disease, it is important to study the pathogen, the host and the environment [14
]. The environment is a determinant of the increase in disease severity, as it influences other factors. Environmental variables affect infection, colonization, sporulation, pathogen survival, and host physiological processes [15
]. The factors typically correlated with disease progress are temperature, humidity, and light intensity [16
], though each pathogen is differently affected by these variables. Thus, studying how these variables influence the severity and temporal dynamics of candeia rust can assist in the development of alternative measures for adequate management, as well as in the screening of more resistant genetic materials.
In addition, to understand the disease epidemiology, it is necessary to analyze the damage caused by the disease and its relationship with pathogen, host, and environmental variables [15
]. In such studies, it is common to use statistical models to describe these phenomena [14
]. Vanderplank [18
] quantified disease using the progress rate (r
), maximum disease intensity, and initial inoculum (y0
), demonstrating how statistically calculated variable values could help compare management tactics. Currently, the disease progress is studied fitting the best empiric model to the observed disease incidence and severity data. The choice of the model most representative of the pathosystem is based on the analysis of the coefficient of determination (R2
), the value of the mean square deviation and the plot of the standardized residuals as a function of the dependent variable [14
The objectives of this study were to analyze temporal progress of candeia rust in E. erythropappus clones in the field; correlate disease severity with meteorological variables; select rust-resistant clones; and fit empirical models to describe the candeia rust progress.
This study presents the first temporal analysis under field conditions of candeia rust in E. erythropappus, which is the main disease in plantations to date. The climatic variables influenced the incidence and severity of rust throughout the evaluation period. Candeia rust occurred throughout the year, but an increase in severity was observed only after March. In addition, the evaluated clones presented different levels of resistance to rust.
All clones showed incidence of the disease, but seven clones were considered resistant to rust (C40, C37, C33, C12, C24, C20, and C35), having lower AUDPC values, eight clones were considered moderately resistant (C7, C4, C49, C35, C19, C36, C6, and C26), one was moderately susceptible (C25), and one was susceptible (C27). Clones C27 and C25 presented the highest disease intensity, showing even under conditions not favorable to its occurrence, indicating that the disease progress depends not only on the climatic conditions but also on the physiology of the host.
The resistance and susceptibility of clones to pathogens have been frequently studied using the AUDPC in other forest species. However, due to the relatively recent recognition of candeia as a promising forest species for exploitation [7
], data on the productivity of clones and damage caused by diseases to this pathosystem are lacking. Consequently, studies correlating the incidence and severity of the disease with the development of resistant candeia clones are necessary. Considering that the regions where candeia plantations are established can offer climatic conditions favorable to the disease and that its incidence can cause damage to the physiological development of the plant, the best control option is the use of resistant varieties. Thus, the results of this study suggest that knowledge about genetic resistance can assist in screening clones for disease management.
This initial step in the selection of candeia rust-resistant genetic materials is important, because the development of clonal tests for the selection of desirable characteristics are still scarce for candeia. The implementation of new commercial plantations is recommended in areas where the species occurs naturally. Thus, since the area of natural occurrence extends to different regions with different climatic conditions, the use of resistant clones selected in one region may be susceptible in others. Thus, the selection of candeia rust resistant clones must be carried out in the respective planting regions. Our study was based on the evaluation of disease that occurred naturally in a candeia population. However, the selection of resistant clones can be accessed in the early stages of plant development through artificial inoculation of the pathogen, thus facilitating the identification and selection of resistant progenies in the future. A protocol for this has not yet been developed for phenotyping, as there is a need for studies involving controlled conditions of humidity and temperature, which is in phase of development.
During the experimental period, the incidence and severity of candeia rust were correlated with environmental variables. The evapotranspiration, rainfall, and temperature were inversely correlated with disease progress. This relationship is negative because the evaluations were based on the presence of symptoms of the pustules containing signs (urediniospores) under the abaxial face of the leaves. However, lesions with yellow edges were commonly observed on the adaxial face as well as dead leaves on the plant. Rust sporulation is favored by adverse environmental conditions, such as low temperature, without rain, and low air humidity. Water and leaf wetness are important for germination and infection, and these occur before April in Brazil. Once environmental conditions become unfavorable for sporulation of the pathogen, it is still possible to visualize disease symptoms.
Thus, the negative correlation observed between disease severity and monthly mean temperature shows that mild temperatures favor the incidence of fungal sporulation. Sales et al. [9
] stated that low temperatures can favor the disease because they increase the stress experienced by the plant, thus increasing its susceptibility to the pathogen, since these conditions favor the sporulation of the pathogen. In addition, Ruiz et al. [22
] observed correlations between the severity of P. psidii
in Eucalyptus grandis
and temperatures between 18 and 25 °C and high humidity.
In the present study, relative humidity did not influence the disease severity, but the microclimatic conditions of the leaf surface were not considered. These conditions directly affect disease severity. The influence of microclimatic factors on the release of urediniospores from the pustules of P. psidii
for new infections was well explained in a study conducted by Zauza et al. [23
], where it was observed that variations in irradiance, temperature, relative humidity, and leaf wetness influenced the release of P. psidii
spores in eucalyptus. Along these lines, our results suggest that the high mean insolation and temperature in January, a month in which one of the lowest mean disease severities was observed, contributed to the inhibition of P. velata
spore germination. This behavior was explained by Ruiz et al. [24
], who observed that exposure to light and to high temperatures inhibits the germination of P. psidii
In addition, a negative correlation between rainfall and disease severity was observed. However, in the months before the beginning of disease progression, such as February and March, there was high rainfall. In this case, the high rainfall combined with the high relative humidity observed before the increase in disease severity in the field favored the establishment of the pathogen in the area, since these conditions contribute to the germination of urediniospores to initiate infection [9
]. In turn, the highest mean rainfall, recorded in December, coincided with the lowest mean disease severity. This is due to the reduction in the number of spores in the air thanks to the increased rainfall, which washes away the pustules and deposits the urediniospores in the soil, preventing the release of these spores into the air [25
]. This information is important because it contributes to the selection of adverse climatic regions to rust infection for the establishment of new plantations of candeia, based on the principle of controlling the evasion or escape of the pathogen.
Regarding disease progression over time, the Gompertz model showed the best fit to the data for candeia rust. This model was described by Vanderplank [18
] for modeling diseases, who showed that the infection rate increases during the epidemic because it is not limited by factors such as the amount of host tissue. Sales et al. [9
] studied the temporal progression of teak rust and observed that the Gompertz model had the best fit to the data, indicating that control measures to reduce the disease progress rate are the most effective. In addition, Oliveira et al. [26
] obtained the best fit to bacterial leaf blight (Xanthomonas axonopodis
) progression data with the Gompertz model for most of their studied clones. This indicates the better efficiency of the Gompertz model than others to describe disease progression in several pathosystems [27
], especially polycyclic diseases, as observed by Bergamin Filho et al. [11
The incidence of candeia rust reached 90% of the evaluated trees in May, and there were no changes in the number of infected trees after this period. My-de Mio et al. [28
] observed the same behavior in relation to the incidence of poplar rust, since the incidence of the disease did not serve as a discriminatory resistance variable, as quickly 100% of the evaluated leaves showed symptoms, regardless of the resistance level of the clone. Zauza et al. [23
] also observed a small variation in the incidence of P. psidii
throughout the experimental period in eucalyptus, but the annual seasonal effect within a region and climatic variations in distinct regions should be noted. These variations were referred to as “ecological zoning” of eucalyptus rust by Masson et al. [29
]. Thus, there may be differences in disease intensity between years due to natural climatic variations [23
], so the results obtained in the present study are intrinsic to the region and the experimental period in which they were evaluated.
In contrast to the incidence of candeia rust, the severity of the disease continued to increase until July due to environmental conditions. The high incidence of rust in the experimental field is a worrisome factor for growing because the disease has rapid dissemination and increased severity under favorable conditions. In the field, the constant production of inoculum and its dispersion by wind and rainwater, added to a favorable environment, can accelerate disease progress if the host is susceptible [23
]. Thus, it is important to select genotypes resistant to P. velata
for planting in new areas and for renewal of established plantations, such as the clones classified as resistant in this study, in order to contain the spread of the disease in regions of commercial or naturally occurring candeia forests.