The coincidence of many unpredictable factors resulted in a rare opportunity to illustrate the danger LSD poses to the Brazilian industry and the strategies to adopt to avoid future outbreaks. The first element was the fact that LSD epidemics occurred on RB966928, the most important sugarcane cultivar since 2015 in São Paulo and Mato Grosso do Sul states (responsible for more than 50% of Brazil sugarcane area), when it was the number one to reestablish new sugarcane fields (9). Since then, its popularity remains high as it was the most cultivated sugarcane in the 2021 crop season (10). Moreover, the present data were obtained from a commercial field, it was not a field experiment comparing diseased and disease-free treatments. Therefore, the high disease incidence and severe tonnage decline quantified on this field (Tables 1 and 2) reflected a real-world situation, demonstrating that the damage inflicted by LSD had a serious financial consequence; besides, it shows that a considerable number of other commercial fields of the same cultivar may suffer the same magnitude of damage observed in that particular field. In the 2021 survey, considering the reform and ratoon areas, this single cultivar (RB966928) was responsible for more than a quarter (27.3%) of all sugarcane area of São Paulo and Mato Grosso do Sul states (10).
The second factor was the existence of another field of the same cultivar in close proximity (5 meter apart), grown under similar edaphoclimatic conditions and agronomic practices, and established the same year. The single difference, but paramount for the aim of the present research, was the origin of seedcanes as they were formed from different nurseries, which resulted in fields with different LSD phytosanitary status (one heavily diseased and another, symptomless). The existence of this second field gave a rare chance to assess the effect of LSD epidemics by a method highly appreciated by the sugarcane industry, i.e., on a commercial field by comparing various disease/host components of diseased (field A) and non-diseased field (B); it was assumed that field A would have the same potential yield of field B had the disease not occurred. This approach proved to be correct since the straight comparison of stalk population between stools with different phytosanitary status (asymptomatic and symptomatic stools) from the same field resulted in no significant difference (Table 1). However, when field B was used as gold standard, a significant reduction of stalk population occurred in field A, demonstrating that LSD caused around 50% decrease in number of stalks per stool. Poor cane population can have lasting effect on future ratoon yields since a positive correlation was observed between population density and root biomass production in RB966928, fewer stalk population density resulted in smaller leaf area index and consequently, poorer root system to support the nutrition and development of plants of subsequent yields (11). Other yield components affected by LSD were high number of dead stalks, severe weight reduction of the remaining stalks, and considerable stool weight decline, which resulted in significant yield loss (Table 1). Among these three components, stool weight is of most immediate consequence to the sugarcane industry because it is the major yield factor and thus, directly affects financial return.
Besides the direct impact LSD caused on a commercial sugarcane field, the fact that the epidemic occurred at plant cane stage brings a dilemma of catastrophic consequence, i.e., what would be the best future action to take on this field? Sugarcane in Brazil is cropped over various cycles of harvest and regrowth from a single planting. Consequently, the more harvests, the more profit since the cost of sugarcane reform is diluted over many harvests; reform of sugarcane field includes many distinct phases such as removal of previous crop, soil preparation, fertilization, seedcane nursery, weed control, etc, making it a complicated and costly operation. Therefore, it is understandable the reluctance to reform sugarcane fields at such early stage. On the other hand, keeping a field with history of high LSD incidence is also a very risky decision; although possibility exists that fewer number of stalks be symptomatic in subsequent ratoons with no yield loss as observed in some cultivars in Guadeloupe (5). In the case of RB966928 however, as it had the highest susceptibility among ten cultivars (Table 3), the possibility of LSD outbreak of the same or greater proportion can´t be ruled out because a direct correlation was observed between yield loss and disease severity (5). Even though environmental factors such as extreme weather conditions were mentioned as important trigger to LSD symptom expression (4), there is no scientific data to assist in decision making in situation similar of field A.
The third coincidence observed was the fact that both fields were at plant cane stage, which serves as an illustrating example of how effective the use of clean seedcane can be as a measure to control LSD. Because harvest has not yet occurred in both fields, within field dissemination has not yet taken place. It is documented that LSD transmission by harvester blade occurs when sap of a diseased stalk is deposited on its blades and transmitted to the next plant (7). Therefore, the striking difference in phytosanitary status between these two fields suggested since the first glance on the field that the phytosanitary status of propagating materials employed to establish each field was to be blame; later on, it was confirmed by the grower that seedcanes of field A were formed from different nursery of field B. The fact that canes of field B remained symptomless up to the time of data collection despite been in close proximity during the whole crop season is a clear indication of the importance of clean seedcane to control LSD. Also, it demonstrates that the main (if not, the only one) mechanism of LSD dissemination in Brazil is cutting instruments; the aerial transmission of X. albilineans observed in the Caribbean region during tropical storms and hurricanes (12) was unlikely to occur in the sub-tropical climate of São Paulo state; transmission by the sap-sucking spittle bug (Mahanarva fimbriolata) observed in laboratory assay (13) probably did not play any role in this field.
The adoption of clean seedcane to reestablish new sugarcane fields in Brazil may not be easy since a survey on LSD in prospective sugarcane fields for nursery formation carried out from 2019 to 2022 showed an average level of contamination of 52.2% among 710 fields examined. More worrisome was the drastic increase of LSD contamination along the years from 37.5% across 72 fields in 2019 to an astonishing 70.9% among 289 fields in 2022 (14). The recommended area for sugarcane renovation varies between 14–17% each year (15), which accounted for 188.100 hectares in 2020/21 crop season (16). Due to huge seedcane demand, it is unknown how many sugarcane mills discard these contaminated fields, as recommended, or even worse, how many mills are conscious of the need of laboratory diagnostic analysis of propagating materials before nursery formation, possibility of higher level of contamination in mills that did not perform routine diagnostic test can´t not be ruled out.
The present work also confirmed another LSD trait that reinforces the importance of laboratory based diagnostic test as significant difference occurred between visual and lab-based detection of LSD; only the latter identified materials with latent stage of the disease (Table 2). The impossibility to identify canes with latent infection in the field can have catastrophic consequences as nurseries can be formed by contaminated propagative materials, which was the case of field A; the high incidence measured in the present study reinforces this assumption. Pathogen dissemination by propagative material with latent infection, was the cause of spread of LSD to many new geographical locations (17). Nowadays this mechanism of long-distance dissemination has reduced dramatically thanks to the use of molecular based diagnostic test capable of detecting the latent stage of LSD (18).
Besides the use of clean seedcanes, the knowledge of cultivar reaction is paramount to implement the use of resistant cultivars. This strategy is adopted worldwide to control LSD (4, 8, 19). This essential piece for the success of LSD control is somehow blurred for the Brazilian cultivars because the sugarcane industry is characterized by huge number of cultivars available, but no scientific study on disease resistance of contemporary cultivar; data on cultivar reaction is confined to pathogen aggressiveness analysis (20, 21). Our data confirmed wide range of reaction to X. albilineans where RB966928 stood out as the most susceptible when disease severity was measured on leaves after inoculation by decapitation. Furthermore, other cultivar reaction is of concern because 5 out 10 canes were classified as susceptible or moderately susceptible (Table 3). Importantly, RB92579 showed to be as susceptible as RB966928, it was the fifth most cropped cultivar in São Paulo and Mato Grosso do Sul states occupying 4.7% and 2% of new sugarcane areas, respectively (10). It is well-adapted for the Northeastern Brazil due to its high yield (22), a region distant more than 1880km from the Center-South but where LSD was also detected (3). Therefore, two of most popular cultivars for the most important sugarcane regions of Brazil showed the same susceptibility to LSD, hence it can speculate that commercial fields of RB92579 have the potential to suffer the same yield loss verified in RB966928. Cultivars RB867515, RB975201, RB855156 were the remaining cultivars classified as moderately susceptible. They ranked respectively 2nd, 6th, 14th in preference to establish new sugarcane fields and covered an area of 16.9% of new renovated area in 2021, despite the absence of data on yield loss some degree of damage is expected since large chlorotic area was observed on their leaves after inoculation of X. albilineans (Figura 1, Table 3). In short, our data showed the magnitude of problem LSD could have on the productive sector. Finally, the disease rating scale developed in this work (Fig. 1) to assess host reaction after pathogen inoculation by decapitation method proved valuable and can be quicky adopted in many places because cultivar classification to LSD was obtained in a short period of time in a reliable manner as seen by comparison of assay 1 and assay 2 (Table 3).