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Abstract Local adaptation has been a central theme of eco-evolutionary research for decades. It is generally assumed that plant pathogens are locally adapted due to their standing interactions with biotic and abiotic factors in the ecosystem. Effectors, secreted small proteins encoded by pathogens, play critical roles in host–pathogen interactions, by activating host genotype-specific resistance, suppressing plant immunity, and playing other functions. In this study, we investigated the potential involvement of RXLR effector genes in ecological adaptation by examining the simple sequence repeat (SSR), virulence, and effector profiles in Phytophthora infestans isolates collected from two geographic regions differing in ecological environments. Genotypic analyses with SSR markers and virulence assays showed that the pathogen from the two regions shared genetic background but differed in virulence spectrums. High-throughput sequencing and expression analysis of 24 selected P. infestans isolates further showed variations in the RXLR effector repertoire, ranging from 536 to 548 for each isolate and the expression of effector genes was highly associated with the accumulation of homologous sRNA. Regional specific alleles were detected at 94 RXLR effector genes, and a specific accumulation of homologous 25–26 nt sRNAs was found at 67 RXLR effector genes. Two of the regional specific RXLR effector genes were confirmed to be virulence factors. Taken together, these results suggest that genomic and epigenetic variations in RXLR effector genes contribute significantly to the ecological adaptation of P. infestans populations and that regional specific effector genes will help to understand the adaptive landscape of pathogens and efficient use of host resistance genes.

Space exploration and interstellar migration are important strategies for long-term human survival. However, extreme environmental conditions, such as space radiation and microgravity, can cause adverse effects, including DNA damage, cerebrovascular disease, osteoporosis, and muscle atrophy, which would require prophylactic and remedial treatment en route. Production of oral drugs in situ is therefore critical for interstellar travel and can be achieved through industrial production utilizing microalgae, which offers high production efficiency, edibility, resource minimization, adaptability, stress tolerance, and genetic manipulation ease. Synthetic biological techniques using microalgae as a chassis offer several advantages in producing natural products, including availability of biosynthetic precursors, potential for synthesizing natural metabolites, superior quality and efficiency, environmental protection, and sustainable development. This article explores the advantages of bioproduction from microalgal chassis using synthetic biological techniques, suitability of microalgal bioreactor-based cell factories for producing value-added natural metabolites, and prospects and applications of microalgae in interstellar travel.

Abstract Background Sequence variation produced by mutation provides the ultimate source of natural selection for species adaptation. Unlike nonsynonymous mutation, synonymous mutations are generally considered to be selectively neutral but accumulating evidence suggests they also contribute to species adaptation by regulating the flow of genetic information and the development of functional traits. In this study, we analysed sequence characteristics of ATP6, a housekeeping gene from 139 Phytophthora infestans isolates, and compared the fitness components including metabolic rate, temperature sensitivity, aggressiveness, and fungicide tolerance among synonymous mutations. Results We found that the housekeeping gene exhibited low genetic variation and was represented by two major synonymous mutants at similar frequency (0.496 and 0.468, respectively). The two synonymous mutants were generated by a single nucleotide substitution but differed significantly in fitness as well as temperature-mediated spatial distribution and expression. The synonymous mutant ending in AT was more common in cold regions and was more expressed at lower experimental temperature than the synonymous mutant ending in GC and vice versa. Conclusion Our results are consistent with the argument that synonymous mutations can modulate the adaptive evolution of species including pathogens and have important implications for sustainable disease management, especially under climate change.

Abstract Reproductive systems play an important role in the ecological function of species, but little is known about how climate change, such as global warming, may affect the reproductive systems of microbes. In this study, 116 Phytophthora infestans isolates sampled from five different altitudes along a mountain were evaluated under five temperature regimes to determine the effects of historical and experimental temperature on the reproductive system of the pathogen. Both altitude, a proxy for historical pathogen adaptation to temperature, and temperature used in the experiment affected the sexual reproduction of the pathogen, with experimental temperature, that is, contemporary temperature, playing a role several times more important than historical temperature. Furthermore, the potential of sexual reproduction, measured by the number of oospores quantified, increased with the temperature breadth (i.e., difference between the highest and lowest temperature at which sexual reproduction takes place) of the pathogen and reached the maximum at the experimental temperature of 21°C, which is higher than the annual average temperature in many potato‐producing areas. The results suggest that rising air temperature associated with global warming may increase the potential of sexual reproduction in P. infestans. Given the importance of sexuality in pathogenicity and ecological adaptation of pathogens, these results suggest that global warming may increase the threat of P. infestans to agricultural production and other ecological services and highlight that new epidemiological strategies may need to be implemented for future food security and ecological resilience.

IntroductionThe macromolecular polysaccharide Inonotus obliquus polysaccharide (IOP) is composed of various monosaccharides, and it could modulate the composition and diversity of intestinal flora. However, its impact on the intestinal flora in rats of different genders remains unclear. Therefore, this study aims to investigate the structural changes of IOP and its effects on the intestinal flora after administration in male and female rats.MethodsIn this study, the molecular weight and purity of IOP were analyzed by high-performance gel permeation chromatography (HPGPC) and phenol sulfuric acid method, and NMR was used to confirm the chemical structure of IOP. Sex hormone [testosterone (T) and estradiol (E2)] levels and intestinal microbial changes were detected by enzyme-linked immunosorbent assay (ELISA) and 16S rRNA, respectively, after gavage of IOP (100 mg/kg) in male and female Sprague Dawley (SD) rats.ResultsHPGPC analysis showed that the average molecular weight (Mw) of IOP was 4,828 Da, and the total sugar content of the purified IOP was 96.2%, indicating that the polysaccharide is of high purity. NMR revealed that IOP is a linear macromolecule with an α-D-type glucose backbone. The results of ELISA and 16S rRNA showed that the IOP increased the abundance of beneficial bacteria, such as Clostridia_UCG-014 and Prevotellaceae_NK3B31, and reduced that of harmful bacteria, such as Colidextribacter and Desulfobacterota in the intestine of both male and female rats, and IOP changed the levels of sex hormones in male and female rats. Further analyses revealed that the increase in alpha diversity was higher in male than female rats. α diversity and β diversity revealed a significant difference in the composition of cecal microbiota between male and female rats in the control group, but IOP intake reduced this difference. Meanwhile, α analysis revealed a change in the composition of bacterial flora was more stable in male than female rats.ConclusionsThis study enhances our comprehension of the IOP structure and elucidates the alterations in intestinal flora following IOP administration in rats of varying genders. Nonetheless, further investigation is warranted to explore the specific underlying reasons for these discrepancies.

Environmental exposure to hazardous materials causes enormous socioeconomic problems due to its deleterious impacts on human beings, agriculture and animal husbandry. As an important hazardous material, cadmium can promote uterine oxidative stress and inflammation, leading to reproductive toxicity. Antioxidants have been reported to attenuate the reproductive toxicity associated with cadmium exposure. In this study, we investigated the potential protective effect of procyanidin oligosaccharide B2 (PC-B2) and gut microbiota on uterine toxicity induced by cadmium exposure in rats. The results showed that the expression levels of glutathione peroxidase (GSH-Px) and superoxide dismutase (SOD) were reduced in utero. Proinflammatory cytokines (including tumor necrosis factor-α, interleukin-1β and interleukin-6), the NLRP3 inflammasome, Caspase-1 and pro-IL-1β were all involved in inflammatory-mediated uterine injury. PC-B2 prevented CdCl2-induced oxidative stress and inflammation in uterine tissue by increasing antioxidant enzymes and reducing proinflammatory cytokines. Additionally, PC-B2 significantly reduced cadmium deposition in the uterus, possibly through its significant increase in MT1, MT2, and MT3 mRNA expression. Interestingly, PC-B2 protected the uterus from CdCl2 damage by increasing the abundance of intestinal microbiota, promoting beneficial microbiota, and inhibiting harmful microbiota. This study provides novel mechanistic insights into the toxicity of environmental cadmium exposure and indicates that PC-B2 could be used in the prevention of cadmium exposure-induced uterine toxicity.

Cadmium (Cd) is a toxic element that can negatively affect both humans and animals. It enters the human and animal bodies through the respiratory and digestive tracts, following which it tends to accumulate in different organs, thereby seriously affecting human and animal health, as well as hampering social and economic development. Cd exposure can alter the composition of intestinal microbiota. In addition, it can damage the peripheral organs by causing the translocation of intestinal microbiota. However, the relationship between translocation-induced changes in the composition of microbiome in the blood and metabolic changes remains unclear. In the present study, we investigated the effects of Cd exposure on microbiota and serum metabolism in rats by omics analysis. The results demonstrated that Cd exposure disrupted the balance between the blood and intestinal flora in Sprague–Dawley (SD) rats, with a significant increase in gut microbiota (Clostridia_UCG_014, NK4A214_group) and blood microbiome (Corynebacterium, Muribaculaceae). However, Cd exposure caused the translocation of Corynebacterium and Muribaculaceae from the gut into the blood. In addition, Cd exposure was associated with the up-regulation of serum indoxyl sulfate, phenyl sulfate, and p-cresol sulfate; down-regulation of δ-tocopherol and L-glutamine; and changes in blood microbiome and metabolites. In conclusion, we identified novel metabolic biomarkers for Cd toxicity, which will also expand our understanding of the role of blood microbiome in Cd-induced injury.

Glycogen synthase kinase 3 (GSK3) family members are evolutionally conserved Ser/Thr protein kinases in mammals and plants. In plants, the GSK3s function as signaling hubs to integrate the perception and transduction of diverse signals required for plant development. Despite their role in the regulation of plant growth and development, emerging research has shed light on their multilayer function in plant stress responses. Here we review recent advances in the regulatory network of GSK3s and the involvement of GSK3s in plant adaptation to various abiotic and biotic stresses. We also discuss the molecular mechanisms underlying how plants cope with environmental stresses through GSK3s-hormones crosstalk, a pivotal biochemical pathway in plant stress responses. We believe that our overview of the versatile physiological functions of GSK3s and underlined molecular mechanism of GSK3s in plant stress response will not only opens further research on this important topic but also provide opportunities for developing stress-resilient crops through the use of genetic engineering technology.

Plant disease management plays an important role in achieving the sustainable development goals of the United Nations (UN) such as food security, human health, socio-economic improvement, resource conservation and ecological resilience. However, technologies available are often limited due to different interests between producers and society and lacks of proper understanding of economic thresholds and the complex interactions among ecology, productivity and profitability. A comprehensive synergy and conflict evaluation of economic, sociological and ecological effects with technologies, productions and evolutionary principles as main components should be used to guide sustainable disease management that aims to mitigate crop and economic losses in the short term while maintaining functional farm ecosystem in the long term. Consequently, there should be an increased emphasis on technology development, public education and information exchange among governments, researchers, producers and consumers to broaden the options for disease management in the future.

Effector genes, together with climatic and other environmental factors, play multifaceted roles in the development of plant diseases. Understanding the role of environmental factors, particularly climate conditions affecting the evolution of effector genes, is important for predicting the long-term value of the genes in controlling agricultural diseases. Here, we collected Phytophthora infestans populations from five locations along a mountainous hill in China and sequenced the effector gene Pi02860 from >300 isolates. To minimize the influence of other ecological factors, isolates were sampled from the same potato cultivar on the same day. We also expressed the gene to visualise its cellular location, assayed its pathogenicity and evaluated its response to experimental temperatures. We found that Pi02860 exhibited moderate genetic variation at the nucleotide level which was mainly generated by point mutation. The mutations did not change the cellular location of the effector gene but significantly modified the fitness of P. infestans. Genetic variation and pathogenicity of the effector gene were positively associated with the altitude of sample sites, possibly due to increased mutation rate induced by the vertical distribution of environmental factors such as UV radiation and temperature. We further found that Pi02860 expression was regulated by experimental temperature with reduced expression as experimental temperature increased. Together, these results indicate that UV radiation and temperature are important environmental factors regulating the evolution of effector genes and provide us with considerable insight as to their future sustainable action under climate and other environmental change.

To successfully survive and reproduce, all species constantly modify the structure and expression of their genomes to cope with changing environmental conditions including ultraviolet (UV) radiation. Thus, knowledge of species adaptation to environmental changes is a central theme of evolutionary studies which could have important implication for disease management and social-ecological sustainability in the future but is generally insufficient. Here, we investigated the evolution of UV adaptation in organisms by population genetic analysis of sequence structure, physiochemistry, transcription, and fitness variation in the radiation-sensitive 4 (RAD4) gene of the Irish potato famine pathogen Phytophthora infestans sampled from various altitudes. We found that RAD4 is a key gene determining the resistance of the pathogen to UV stress as indicated by strong phenotype-genotype-geography associations and upregulated transcription after UV exposure. We also found conserved evolution in the RAD4 gene. Only five nucleotide haplotypes corresponding to three protein isoforms generated by point mutations were detected in the 140 sequences analyzed and the mutations were constrained to the N-terminal domain of the protein. Physiochemical changes associated with non-synonymous mutations generate severe fitness penalty to mutants, which are purged out by natural selection, leading to the conserved evolution observed in the gene.

Abstract 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.

Abstract 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.

As a vital element of climate change, elevated temperatures resulting from global warming present new challenges to natural and agricultural sustainability, such as ecological disease management. Mitochondria regulate the energy production of cells in responding to environmental fluctuation, but studying their contribution to the thermal adaptation of species is limited. This knowledge is needed to predict future disease epidemiology for ecology conservation and food security. Spatial distributions of the mitochondrial genome (mtDNA) in 405 Phytophthora infestans isolates originating from 15 locations were characterized. The contribution of MtDNA to thermal adaptation was evaluated by comparative analysis of mtDNA frequency and intrinsic growth rate, relative population differentiation in nuclear and mtDNA, and associations of mtDNA distribution with local geography climate conditions. Significant variation in frequency, intrinsic growth rate, and spatial distribution was detected in mtDNA. Population differentiation in mtDNA was significantly higher than that in the nuclear genome, and spatial distribution of mtDNA was strongly associated with local climatic conditions and geographic parameters, particularly air temperature, suggesting natural selection caused by a local temperature is the main driver of the adaptation. Dominant mtDNA grew faster than the less frequent mtDNA. Our results provide useful insights into the evolution of pathogens under global warming. Given its important role in biological functions and adaptation to local air temperature, mtDNA intervention has become an increasing necessity for future disease management. To secure ecological integrity and food production under global warming, a synergistic study on the interactive effect of changing temperature on various components of biological and ecological functions of mitochondria in an evolutionary frame is urgently needed.

Abstract Temperature plays a multidimensional role in host–pathogen interactions. As an important element of climate change, elevated world temperature resulting from global warming presents new challenges to sustainable disease management. Knowledge of pathogen adaptation to global warming is needed to predict future disease epidemiology and formulate mitigating strategies. In this study, 21 Phytophthora infestans isolates originating from seven thermal environments were acclimated for 200 days under stepwise increase or decrease of experimental temperatures and evolutionary responses of the isolates to the thermal changes were evaluated. We found temperature acclimation significantly increased the fitness and genetic adaptation of P. infestans isolates at both low and high temperatures. Low‐temperature acclimation enforced the countergradient adaptation of the pathogen to its past selection and enhanced the positive association between the pathogen's intrinsic growth rate and aggressiveness. At high temperatures, we found that pathogen growth collapsed near the maximum temperature for growth, suggesting a thermal niche boundary may exist in the evolutionary adaptation of P. infestans. These results indicate that pathogens can quickly adapt to temperature shifts in global warming. If this is associated with environmental conditions favoring pathogen spread, it will threaten future food security and human health and require the establishment of mitigating actions.

Abstract Gene flow is an important evolutionary force that enables adaptive responses of plant pathogens in response to changes in the environment and plant disease management strategies. In this study, we made a direct inference concerning gene flow in the Irish famine pathogen Phytophthora infestans between two of its hosts (potato and tomato) as well as between China and India. This was done by comparing sequence characteristics of the eukaryotic translation elongation factor 1 alpha (eEF‐1α) gene, generated from 245 P. infestans isolates sampled from two countries and hosts. Consistent with previous results, we found that eEF‐1α gene was highly conserved and point mutation was the only mechanism generating any sequence variation. Higher genetic variation was found in the eEF‐1α sequences in the P. infestans populations sampled from tomato compared to those sampled from potato. We also found the P. infestans population from India displayed a higher genetic variation in the eEF‐1α sequences compared to China. No gene flow was detected between the pathogen populations from the two countries, which is possibly attributed to the geographic barrier caused by Himalaya Plateau and the minimum cross‐border trade of potato and tomato products. The implications of these results for a sustainable management of late blight diseases are discussed.

Biodiversity plays multifaceted roles in societal development and ecological sustainability. In agricultural ecosystems, using biodiversity to mitigate plant diseases has received renewed attention in recent years but our knowledge of the best ways of using biodiversity to control plant diseases is still incomplete. In term of in-crop diversification, it is not clear how genetic diversity per se in host populations interacts with identifiable resistance and other functional traits of component genotypes to mitigate disease epidemics and what is the best way of structuring mixture populations. In this study, we created a series of host populations by mixing different numbers of potato varieties showing different late blight resistance levels in different proportions. The amount of naturally occurring late blight disease in the mixture populations was recorded weekly during the potato growing seasons. The percentage of disease reduction (PDR) in the mixture populations was calculated by comparing their observed late blight levels relative to that expected when they were planted in pure stands. We found that PDR in the mixtures increased as the number of varieties and the difference in host resistance (DHR) between the component varieties increased. However, the level of host resistance in the potato varieties had little impact on PDR. In mixtures involving two varieties, the optimum proportion of component varieties for the best PDR depended on their DHR, with an increasing skewness to one of the component varieties as the DHR between the component varieties increased. These results indicate that mixing crop varieties can significantly reduce disease epidemics in the field. To achieve the best disease mitigation, growers should include as many varieties as possible in mixtures or, if only two component mixtures are possible, increase DHR among the component varieties.

The use of ecological principles to manage plant pests has attracted renewed attention, but our knowledge related to the contributions of ecological pest management to social and natural sustainability is fragmented. In this study, we compared the performance and resilience of tea production and the economic benefits of tea ecological management (TEM) and tea conventional management (TCM). We show that TEM significantly improved tea biomass and quality, nutritional efficiency, and beneficial insects, but reduced seasonal variation. As a result, economic return increased by $8045/ha in the TEM mode compared to $6064/ha in the TCM mode. These results confirm that TEM is a promising production mode that can reconcile the conflict between the immediate and long-term service of agriculture. However, environmental improvements associated with organic pest control benefit society, and the government should provide adequate financial support to promote the production system.

Phytophthora infestans, the most damaging oomycete pathogen of potato, is specialized to grow sporangiophore through opened stomata for secondary inoculum production. However, it is still unclear which metabolic pathways in potato are manipulated by P. infestans in the guard cell–pathogen interactions to open the stomata. Here microscopic observations and cell biology were used to investigate antagonistic interactions between guard cells and the oomycete pathogen. We observed that the antagonistic interactions started at the very beginning of infection. Stomatal movement is an important part of the immune response of potato to P. infestans infection and this occurs through guard cell death and stomatal closure. We observed that P. infestans appeared to manipulate metabolic processes in guard cells, such as triacylglycerol (TAG) breakdown, starch degradation, H2O2 scavenging, and NO catabolism, which are involved in stomatal movement, to evade these stomatal defense responses. The signal transduction pathway of P. infestans-induced stomatal opening likely starts from H2O2 and NO scavenging, along with TAG breakdown while the subsequent starch degradation reinforces the opening process by strengthening guard cell turgor and opening the stomata to their maximum aperture. These results suggest that stomata are a barrier stopping P. infestans from completing its life cycle, but this host defense system can be bypassed through the manipulation of diverse metabolic pathways that may be induced by P. infestans effector proteins.

Abstract Background Cross-resistance, a phenomenon that a pathogen resists to one antimicrobial compound also resists to one or several other compounds, is one of major threats to human health and sustainable food production. It usually occurs among antimicrobial compounds sharing the mode of action. In this study, we determined the sensitivity profiles of Alternaria alternata, a fungal pathogen which can cause diseases in many crops to two fungicides (mancozeb and difenoconazole) with different mode of action using a large number of isolates (234) collected from seven potato fields across China. Results We found that pathogens could also develop cross resistance to fungicides with different modes of action as indicated by a strong positive correlation between mancozeb and difenoconazole tolerances to A. alternata. We also found a positive association between mancozeb tolerance and aggressiveness of A. alternata, suggesting no fitness penalty of developing mancozeb resistance in the pathogen and hypothesize that mechanisms such as antimicrobial compound efflux and detoxification that limit intercellular accumulation of natural/synthetic chemicals in pathogens might account for the cross-resistance and the positive association between pathogen aggressiveness and mancozeb tolerance. Conclusions The detection of cross-resistance among different classes of fungicides suggests that the mode of action alone may not be an adequate sole criterion to determine what components to use in the mixture and/or rotation of fungicides in agricultural and medical sects. Similarly, the observation of a positive association between the pathogen’s aggressiveness and tolerance to mancozeb suggests that intensive application of site non-specific fungicides might simultaneously lead to reduced fungicide resistance and enhanced ability to cause diseases in pathogen populations, thereby posing a greater threat to agricultural production and human health. In this case, the use of evolutionary principles in closely monitoring populations and the use of appropriate fungicide applications are important for effective use of the fungicides and durable infectious disease management.

Abstract Expected global changes in environmental conditions underline the need for a better understanding of genetic variation in ecological traits and their strategies of adaptation to the stresses. In this study, evolutionary mechanisms and processes of UV adaptation in plant pathogens were investigated by combining statistical genetics, physiological assays, and common garden experiment approaches in an assessment of the potato late blight pathogen, Phytophthora infestans, sampled from various geographic locations in China. We found spatial divergence caused by diversifying selection in UV tolerance among P. infestans populations. Local UV radiation was the driving force of selection as indicated by a positive correlation between UV tolerance in P. infestans populations and the altitude of collection sites. Plasticity accounted for 68% of population variation while heritability was negligible, suggesting temporary changes in gene expression and/or enzymatic activity play a more important role than permanent modification of gene structure in the evolution of UV adaptation. This adaptation strategy may explain the lack of fitness penalty observed in genotypes with higher UV tolerance.

Knowledge of pathogen adaptation to global warming is important for predicting future disease epidemics and food production in agricultural ecosystems; however, the patterns and mechanisms of such adaptation in many plant pathogens are poorly understood. Here, population genetics combined with physiological assays and common garden experiments were used to analyze the genetics, physiology, and thermal preference of pathogen aggressiveness in an evolutionary context using 140 Phytophthora infestans genotypes under five temperature regimes. Pathogens originating from warmer regions were more thermophilic and had a broader thermal niche than those from cooler regions. Phenotypic plasticity contributed ~10-fold more than heritability measured by genetic variance. Further, experimental temperatures altered the expression of genetic variation and the association of pathogen aggressiveness with the local temperature. Increasing experimental temperature enhanced the variation in aggressiveness. At low experimental temperatures, pathogens from warmer places produced less disease than those from cooler places; however, this pattern was reversed at higher experimental temperatures. These results suggest that geographic variation in the thermal preferences of pathogens should be included in modeling future disease epidemics in agricultural ecosystems in response to global warming, and greater attention should be paid to preventing the movement of pathogens from warmer to cooler places.

Effector genes play critical roles in the antagonistic interactions between plants and pathogens. However, knowledge of mutation mechanisms and evolutionary processes in effector genes and the contribution of climatic factors to the evolution of effector genes are fragmented but important in sustainable management of plant diseases and securing food supply under changing climates. Here, we used a population genetic approach to explore the evolution of the Avr4 gene in Phytophthora infestans, the causal agent of potato blight. We found that the Avr4 gene exhibited a high genetic diversity generated by point mutation and sequence deletion. Frameshifts caused by a single base-pair deletion at the 194th nucleotide position generate two stop codons, truncating almost the entire C-terminal, which is important for effector function and R4 recognition in all sequences. The effector is under natural selection for adaptation supported by comparative analyses of population differentiation (FST) and isolation-by-distance between Avr4 sequences and simple sequence repeat marker loci. Furthermore, we found that local air temperature was positively associated with pairwise FST in the Avr4 sequences. These results suggest that the evolution of the effector gene is influenced by local air temperature, and the C-terminal truncation is one of the main mutation mechanisms in the P. infestans effector gene to circumvent the immune response of potato plants. The implication of these results to agricultural and natural sustainability in future climate conditions is discussed.

Rhizoctonia solani anastomosis group 3 (AG-3) is the main causative agent of the soil-borne disease known as potato black scurf, which poses a huge threat to potato production. Rapid and accurate identification of R. solani AG-3 isolates in soil and potato seed tubers prior to planting is essential for good production. In this study, a multiplex PCR assay was established for the detection of R. solani AG-3. Two pairs of target-specific primers were designed from sequences for endopolygalacturonase and pyridoxine biosynthesis genes downloaded from GenBank. The main factors influencing PCR amplification, such as annealing temperature and primer concentration, were optimized. Results show that the proposed multiplex PCR assay is highly sensitive and specific for the target genes in the pathogen even when the DNA concentration is reduced to 20 fg/μL. The resulting calibration plot shows a linear relationship between electrophoretic band peaks and genomic DNA concentration (R2 = 0.98). The primer specificity was confirmed by applying them to other R. solani AG groups and plant pathogen species on which no amplicons were produced. Using the primers, we successfully detected small amounts of R. solani AG-3 present in soil and potato tuber samples. Taken together, the detection assay developed in this study has high sensitivity, strong specificity, and accuracy and can be used to detect and identify soil and potato seed tubers infected with Rhizoctonia solani AG-3.

Climate change is triggering similar effects on the incidence and severity of disease for crops in agriculture and wild plants in natural communities. The complexity of natural ecosystems, however, generates a complex array of interactions between wild plants and pathogens in marked contrast to those generated in the structural and species simplicity of most agricultural crops. Understanding the different impacts of climate change on agricultural and natural ecosystems requires accounting for the specific interactions between an individual pathogen and its host(s) and their subsequent effects on the interplay between the host and other species in the community. Ultimately, progress will require looking past short-term fluctuations to multiyear trends to understand the nature and extent of plant and pathogen evolutionary adaptation and determine the fate of plants under future climate change.

Potato Alternaria leaf blight is one of the economically most important disease in potato production worldwide. A recent study reported a quick method to distinguish main Alternaria pathogens A. tenuissima, A. alternata, and A. solani using partial histone H3 gene sequences. Using this method, our collection of 79 isolates from 8 provinces in China were presumably separated into A. tenussima and A. alternata. But in depth morphological and genetic analysis casted doubt on this identification. Culture morphologies of six presumed A. alternata isolates (PresA_alt) and six presumed A. tenuissima isolates (PresA_ten) were not significantly different. PresA_ten isolates also produced conidia in branched chains which supposed to be A. aternata. Phylogenetic analyses were conducted using internal transcribed spacer region (ITS) and five genes commonly used for species identification including glyceraldehyde-3-phosphate dehydrogenase (GPDH), translation elongation factor 1-alpha (TEF1), β-tubulin, plasma membrane ATPase (ATPase), and calmodulin genes. The results showed that GPDH and TEF1 sequences of PresA_alt and PresA_ten isolates were identical. The 12 isolates did not cluster by presumed species neither by individual or concatenated sequence comparisons. The phylogeny-trait association analysis confirmed that the two group isolates were undistinguishable by those molecular markers. Analysis of histone H3 gene sequences revealed variable intron sequences between PresA_ten and PresA_alt isolates, but the amino acid sequences were identical. Our results indicate that the previously published method to distinguish Alternaria species based on histone H3 gene sequence variation is inaccurate and that the prevalence of A. tenuissima isolates in China was likely overestimated.

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.

Effectors, a group of small proteins secreted by pathogens, play a central role in antagonistic interactions between plant hosts and pathogens. The evolution of effector genes threatens plant disease management and sustainable food production, but population genetic analyses to understand evolutionary mechanisms of effector genes are limited compared to molecular and functional studies. Here we investigated the evolution of the Avr1 effector gene from 111 Phytophthora infestans isolates collected from six areas covering three potato cropping regions in China using a population genetic approach. High genetic variation of the effector gene resulted from diverse mechanisms including base substitution, pre-termination, intragenic recombination and diversifying selection. Nearly 80% of the 111 sequences had a point mutation in the 512th nucleotide (T512G), which generated a pre-termination stop codon truncating 38 amino acids in the C-terminal, suggesting that the C-terminal may not be essential to ecological and biological functions of P. infestans. A significant correlation between the frequency of Avr1 sequences with the pre-termination and annual mean temperature in the collection sites suggests that thermal heterogeneity might be one of contributors to the diversifying selection, although biological and biochemical mechanisms of the likely thermal adaptation are not known currently. Our results highlight the risk of rapid adaptation of P. infestans and possibly other pathogens as well to host resistance, and the application of eco-evolutionary principles is necessary for sustainable disease management in agricultural ecosystems.

Evolution of fungicide resistance in plant pathogens is one of major concerns in sustainable plant disease management. In this study, the genetics and potential of developing resistance to a demethylation inhibitor (DMI) fungicide, difenoconazole, in the fungal pathogen Alternaria alternata was investigated using a comparative analysis of genetic variation in molecular (Single Sequence Repeats, SSR) and phenotypic (fungicide tolerance) markers. No difenoconazole resistance was found in the 215 A. alternata isolates sampled from seven different ecological zones in China despite the widespread use of the fungicide for more than 20 years. This result suggests that the risk of developing resistance to difenoconazole in A. alternata is low and we hypothesize that the low risk is likely caused by fitness penalties incurred by resistant mutants and the multiple mechanisms involving in developing resistance. Heritability and plasticity account for ∼24 and 3% of phenotypic variation, respectively, indicating that genetic adaptation by sequence variation plays a more important role in the evolution of difenoconazole resistance than physiological adaptation by altering gene expression. Constraining selection in the evolution of A. alternata resistance to difenoconazole was documented by different patterns of population differentiation and isolate-by-distance between SSR markers and difenoconazole tolerance. Though the risk of developing resistance is low, the findings of significant differences in difenoconazole tolerance among isolates and populations, and a skewing distribution toward higher tolerance suggests that a stepwise accumulation of tolerance to the fungicide might be occurring in the pathogen populations. As a consequence, dynamic management programs guided by evolutionary principles such as spatiotemporal rotations of fungicides with different modes of action are critical to prevent the continued accumulation of tolerance or the evolution of resistance to difenoconazole and other DMI fungicides.

Climate change is considered a major threat to society and nature. UV irradiation is the most important environmental genotoxic agent. Thus, how elevated UV irradiation may influence human health and ecosystems has generated wide concern in the scientific community, as well as with policy makers and the public in general. In this study, we investigated patterns and mechanisms of UV adaptation in natural ecosystems by studying a gene-specific variation in the potato late blight pathogen, Phytophthora infestans. We compared the sequence characteristics of radiation sensitive 23 (RAD23), a gene involved in the nucleotide excision repair (NER) pathway and UV tolerance, in P. infestans isolates sampled from various altitudes. We found that lower genetic variation in the RAD23 gene was caused by natural selection. The hypothesis that UV irradiation drives this selection was supported by strong correlations between the genomic characteristics and altitudinal origin (historic UV irradiation) of the RAD23 sequences with UV tolerance of the P. infestans isolates. These results indicate that the RAD23 gene plays an important role in the adaptation of P. infestans to UV stress. We also found that different climatic factors could work synergistically to determine the evolutionary adaptation of species, making the influence of climate change on ecological functions and resilience more difficult to predict. Future attention should aim at understanding the collective impact generated by simultaneous change in several climate factors on species adaptation and ecological sustainability, using state of the art technologies such as experimental evolution, genome-wide scanning, and proteomics.

Cropping systems greatly impact the productivity and resilience of agricultural ecosystems. However, we often lack an understanding of the quantitative interactions among social, economic and ecological components in each of the systems, especially with regard to crop rotation. Current production systems cannot guarantee both high profits in the short term and social and ecological benefits in the long term. This study combined statistic and economic models to evaluate the comprehensive effects of cropping systems on rice production using data collected from experimental fields between 2017 and 2018. The results showed that increasing agricultural diversity through rotations, particularly potato–rice rotation (PR), significantly increased the social, economic and ecological benefits of rice production. Yields, profits, profit margins, weighted dimensionless values of soil chemical and physical (SCP) and heavy metal (SHM) traits, benefits and externalities generated by PR and other rotations were generally higher than successive rice cropping. This suggests that agricultural diversity through rotations, particularly PR rotation, is worth implementing due to its overall benefits generated in rice production. However, due to various nutrient residues from preceding crops, fertilizer application should be rationalized to improve the resource and investment efficiency. Furthermore, we internalized the externalities (hidden ecological and social benefits/costs) generated by each of the rotation systems and proposed ways of incenting farmers to adopt crop rotation approaches for sustainable rice production.

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.

Understanding how habitat heterogeneity may affect the evolution of plant pathogens is essential to effectively predict new epidemiological landscapes and manage genetic diversity under changing global climatic conditions. In this study, we explore the effects of habitat heterogeneity, as determined by variation in host resistance and local temperature, on the evolution of Zymoseptoria tritici by comparing the aggressiveness development of five Z. tritici populations originated from different parts of the world on two wheat cultivars varying in resistance to the pathogen. Our results show that host resistance plays an important role in the evolution of Z. tritici. The pathogen was under weak, constraining selection on a host with quantitative resistance but under a stronger, directional selection on a susceptible host. This difference is consistent with theoretical expectations that suggest that quantitative resistance may slow down the evolution of pathogens and therefore be more durable. Our results also show that local temperature interacts with host resistance in influencing the evolution of the pathogen. When infecting a susceptible host, aggressiveness development of Z. tritici was negatively correlated to temperatures of the original collection sites, suggesting a trade-off between the pathogen’s abilities of adapting to higher temperature and causing disease and global warming may have a negative effect on the evolution of pathogens. The finding that no such relationship was detected when the pathogen infected the partially resistant cultivars indicates the evolution of pathogens in quantitatively resistant hosts is less influenced by environments than in susceptible hosts.

Host resistance and synthetic antimicrobials such as fungicides are two of the main approaches used to control plant diseases in conventional agriculture. Although pathogens often evolve to overcome host resistance and antimicrobials, the majority of reports have involved qualitative host - pathogen interactions or antimicrobials targeting a single pathogen protein or metabolic pathway. Studies that consider jointly the evolution of virulence, defined as the degree of damage caused to a host by parasite infection, and antimicrobial resistance are rare. Here we compared virulence and fungicide tolerance in the fungal pathogen Mycosphaerella graminicola sampled from wheat fields across three continents and found a positive correlation between virulence and tolerance to a triazole fungicide. We also found that quantitative host resistance selected for higher pathogen virulence. The possible mechanisms responsible for these observations and their consequences for sustainable disease management are discussed.

Fitness cost associated with pathogens carrying unnecessary virulence alleles is the fundamental assumption for preventing the emergence of complex races in plant pathogen populations but this hypothesis has rarely been tested empirically on a temporal and spatial scale which is sufficient to distinguish evolutionary signals from experimental error. We analyzed virulence characteristics of ≈ 1000 isolates of the barley pathogen Rhynchosporium secalis collected from different parts of the United Kingdom between 1984 and 2005. We found a gradual increase in race complexity over time with a significant correlation between sampling date and race complexity of the pathogen (r(20) = 0.71, p = 0.0002) and an average loss of 0.1 avirulence alleles (corresponding to an average gain of 0.1 virulence alleles) each year. We also found a positive and significant correlation between barley cultivar diversity and R. secalis virulence variation. The conditions assumed to favour complex races were not present in the United Kingdom and we hypothesize that the increase in race complexity is attributable to the combination of natural selection and genetic drift. Host resistance selects for corresponding virulence alleles to fixation or dominant frequency. Because of the weak fitness penalty of carrying the unnecessary virulence alleles, genetic drift associated with other evolutionary forces such as hitch-hiking maintains the frequency of the dominant virulence alleles even after the corresponding resistance factors cease to be used.