Biological Control of Plant Diseases: An Evolutionary and Eco-Economic Consideration.

Biological control is considered as a promising alternative to pesticide and plant resistance to manage plant diseases, but a better understanding of the interaction of its natural and societal functions is necessary for its endorsement. The introduction of biological control agents (BCAs) alters the interaction among plants, pathogens, and environments, leading to biological and physical cascades that influence pathogen fitness, plant health, and ecological function. These interrelationships generate a landscape of tradeoffs among natural and social functions of biological control, and a comprehensive evaluation of its benefits and costs across social and farmer perspectives is required to ensure the sustainable development and deployment of the approach. Consequently, there should be a shift of disease control philosophy from a single concept that only concerns crop productivity to a multifaceted concept concerning crop productivity, ecological function, social acceptability, and economical accessibility. To achieve these goals, attempts should make to develop "green" BCAs used dynamically and synthetically with other disease control approaches in an integrated disease management scheme, and evolutionary biologists should play an increasing role in formulating the strategies. Governments and the public should also play a role in the development and implementation of biological control strategies supporting positive externality.

Increasing temperature elevates the variation and spatial differentiation of pesticide tolerance in a plant pathogen.

Climate change and pesticide resistance are two of the most imminent challenges human society is facing today. Knowledge of how the evolution of pesticide resistance may be affected by climate change such as increasing air temperature on the planet is important for agricultural production and ecological sustainability in the future but is lack in scientific literatures reported from empirical research. Here, we used the azoxystrobin-Phytophthora infestans interaction in agricultural systems to investigate the contributions of environmental temperature to the evolution of pesticide resistance and infer the impacts of global warming on pesticide efficacy and future agricultural production and ecological sustainability. We achieved this by comparing azoxystrobin sensitivity of 180 P. infestans isolates sampled from nine geographic locations in China under five temperature schemes ranging from 13 to 25°C. We found that local air temperature contributed greatly to the difference of azoxystrobin tolerance among geographic populations of the pathogen. Both among-population and within-population variations in azoxystrobin tolerance increased as experimental temperatures increased. We also found that isolates with higher azoxystrobin tolerance adapted to a broader thermal niche. These results suggest that global warming may enhance the risk of developing pesticide resistance in plant pathogens and highlight the increased challenges of administering pesticides for effective management of plant diseases to support agricultural production and ecological sustainability under future thermal conditions.

Evidence for a synergistic effect of post-translational modifications and genomic composition of eEF-1α on the adaptation of Phytophthora infestans.

Genetic variation plays a fundamental role in pathogen's adaptation to environmental stresses. Pathogens with low genetic variation tend to survive and proliferate more poorly due to their lack of genotypic/phenotypic polymorphisms in responding to fluctuating environments. Evolutionary theory hypothesizes that the adaptive disadvantage of genes with low genomic variation can be compensated for structural diversity of proteins through post-translation modification (PTM) but this theory is rarely tested experimentally and its implication to sustainable disease management is hardly discussed. In this study, we analyzed nucleotide characteristics of eukaryotic translation elongation factor-1α (eEF-lα) gene from 165 Phytophthora infestans isolates and the physical and chemical properties of its derived proteins. We found a low sequence variation of eEF-lα protein, possibly attributable to purifying selection and a lack of intra-genic recombination rather than reduced mutation. In the only two isoforms detected by the study, the major one accounted for >95% of the pathogen collection and displayed a significantly higher fitness than the minor one. High lysine representation enhances the opportunity of the eEF-1α protein to be methylated and the absence of disulfide bonds is consistent with the structural prediction showing that many disordered regions are existed in the protein. Methylation, structural disordering, and possibly other PTMs ensure the ability of the protein to modify its functions during biological, cellular and biochemical processes, and compensate for its adaptive disadvantage caused by sequence conservation. Our results indicate that PTMs may function synergistically with nucleotide codes to regulate the adaptive landscape of eEF-1α, possibly as well as other housekeeping genes, in P. infestans. Compensatory evolution between pre- and post-translational phase in eEF-1α could enable pathogens quickly adapting to disease management strategies while efficiently maintaining critical roles of the protein playing in biological, cellular, and biochemical activities. Implications of these results to sustainable plant disease management are discussed.

Human-Mediated Gene Flow Contributes to Metapopulation Genetic Structure of the Pathogenic Fungus Alternaria alternata from Potato.

Metapopulation structure generated by recurrent extinctions and recolonizations plays an important role in the evolution of species but is rarely considered in agricultural systems. In this study, generation and mechanism of metapopulation structure were investigated by microsatellite assaying 725 isolates of Alternaria alternata sampled from potato hosts at 16 locations across China. We found a single major cluster, no isolate-geography associations and no bottlenecks in the A. alternata isolates, suggesting a metapopulation genetic structure of the pathogen. We also found weak isolation-by-distance, lower among than within cropping region population differentiation, concordant moving directions of potato products and net gene flow and the highest gene diversity in the region with the most potato imports. These results indicate that in addition to natural dispersal, human-mediated gene flow also contributes to the generation and dynamics of the metapopulation genetic structure of A. alternata in China. Metapopulation structure increases the adaptive capacity of the plant pathogen as a result of enhanced genetic variation and reduced population fragmentation. Consequently, rigid quarantine regulations may be required to reduce population connectivity and the evolutionary potential of A. alternata and other pathogens with a similar population dynamics for a sustainable plant disease management.

Viruliferous rate of small brown planthopper is a good indicator of rice stripe disease epidemics.

Rice stripe virus (RSV), its vector insect (small brown planthopper, SBPH) and climatic conditions in Jiangsu, China were monitored between 2002 and 2012 to determine key biotic and abiotic factors driving epidemics of the disease. Average disease severity, disease incidence and viruliferous rate of SBPH peaked in 2004 and then gradually decreased. Disease severity of RSV was positively correlated with viruliferous rate of the vector but not with the population density of the insect, suggesting that the proportion of vectors infected by the virus rather than the absolute number of vectors plays an important role in RSV epidemics and could be used for disease forecasting. The finding of a positive correlation of disease severity and viruliferous rate among years suggests that local infection is likely the main source of primary inoculum of RSV. Of the two main climatic factors, temperature plays a more important role than rainfall in RSV epidemics.