Anti- and pro-microbial roles of autophagy in plant-bacteria interactions

Macroautophagy/autophagy and the ubiquitin-proteasome system (UPS) are major proteolytic pathways that are increasingly recognized as battlegrounds during host-microbe interactions in eukaryotes. In plants, the UPS has emerged as central component of innate immunity and is manipulated by bacterial pathogens to enhance virulence. Autophagy has been ascribed a similar importance for anti-bacterial immunity in animals, but the contribution of autophagy to host-bacteria interactions remained elusive in plants. Here, we present and discuss our recent findings that revealed anti- and pro-bacterial roles of autophagy pathways during bacterial infection in the model plant Arabidopsis thaliana. We discovered that selective autophagy mediated by the autophagy cargo receptor AT4G24690/NBR1 limits growth of Pseudomonas syringae pv. tomato DC3000 (Pst) by suppressing the establishment of an aqueous extracellular space (‘water-soaking’). In turn, Pseudomonas employs the effector protein HopM1 to activate autophagy and proteasome degradation (‘proteaphagy’), thereby enhancing its pathogenicity. Thus, our study demonstrates that distinct selective autophagy pathways contribute to host immunity and bacterial pathogenesis during Pst infection and provide evidence for an intimate crosstalk between the proteasome and autophagy system in plant-bacterial interactions.     

Signal perception during plant-bacteria interactions: from chemicals to physical signals

正During interactions between host plants and microbes, discrimination between "self" and "nonself" is at the center of many biological relationships and determines the success of infection by microbial pathogens or immunity of the hosts.     

Conditional outcomes in mutualistic interactions

Interspecific interactions are traditionally displayed in a grid in which each interaction is placed according to its outcome (positive, negative or neutral) for each partner. However, recent field studies consistently find the costs and benefits that determine net effects to vary greatly in both space and time, inevitably causing outcomes within most interactions to vary as well. Interactions show 'conditionality' when costs and benefits, and thus outcomes, are affected in predictable ways by current ecological conditions. The full range of natural outcomes of a given association may reveal far more about its ecological and evolutionary dynamics than does the average outcome at a given place and time.     

Commensal and mutualistic interactions among terrestrial vertebrates

Although overlooked in many field studies, commensal and mutualistic interactions occur frequently between species of terrestrial vertebrates. Potential advantages for individuals in mixed-species associations are very diverse, and include reduction in parasite load, reduced risk of predation, and increased access to food and other resources. Recent theoretical and experimental studies reveal the prevalence of such interactions among terrestrial vertebrates, and also confirm their importance within communities thought previously to be dominated by interspecific competition.     

Insects as vectors of plant pathogens: mutualistic and antagonistic interactions

Interactions between plants and their herbivores and pathogens are mostly analysed separately, thereby neglecting mutualistic or antagonistic interactions between these antagonists and possible joint effects on the host. We studied interactions between the weed Cirsium arvense, the rust fungus Puccinia punctiformis and three herbivorous insects, the aphids Aphis fabae ssp. cirsiiacanthoidis and Uroleucon cirsii, and the beetle Cassida rubiginosa. All three insect species mechanically transported spore material and significantly increased rates of P. punctiformis infection in healthy thistles. The interaction between C. rubiginosa and the fungus was antagonistic. Although C. rubiginosa transferred spores, biomass of adults was significantly reduced, development of adults tended to be prolonged and mortality increased when feeding on plants infected with P. punctiformis. In contrast, the relationship between the aphid U. cirsii and P. punctiformis was mutualistic: U. cirsii profited by fungal infection and formed significantly larger colonies on fungus-infected plants. Although the differences in insect performance suggest that aphids may be better vectors than the beetle, infection rates were similar. This is the first study to demonstrate that the relationship between herbivores, which increase the dispersal of a pathogen, and the pathogen itself can be mutualistic or antagonistic, depending on the species.     

It pays to be sweet: sugars in mutualistic interactions

It is common knowledge that many flowering plants produce nectar to reward pollinators. Not so well known is the fact that plants, fungi and insects also employ sugar-rich solutions to obtain transport or defensive services. However, not all of these interactions are honest. In many cases, cheaters use tricks instead of treats.     

Modeling the mutualistic interactions between tubeworms and microbial consortia

The deep-sea vestimentiferan tubeworm Lamellibrachia luymesi forms large aggregations at hydrocarbon seeps in the Gulf of Mexico that may persist for over 250 y. Here, we present the results of a diagenetic model in which tubeworm aggregation persistence is achieved through augmentation of the supply of sulfate to hydrocarbon seep sediments. In the model, L. luymesi releases the sulfate generated by its internal, chemoautotrophic, sulfide-oxidizing symbionts through posterior root-like extensions of its body. The sulfate fuels sulfate reduction, commonly coupled to anaerobic methane oxidation and hydrocarbon degradation by bacterial–archaeal consortia. If sulfate is released by the tubeworms, sulfide generation mainly by hydrocarbon degradation is sufficient to support moderate-sized aggregations of L. luymesi for hundreds of years. The results of this model expand our concept of the potential benefits derived from complex interspecific relationships, in this case involving members of all three domains of life.     

Recognition of muramic acid and N-acetylmuramic acid by Leguminosae lectins: possible role in plant-bacteria interactions

Abstract Interaction of 24 different seed lectins/ isolectins from the Leguminosae with muramic acid (MurAc), N-acetylmuramic acid (MurNAc) and muramyl-dipeptides (MDP), was studied by hapten-inhibition of haemagglutination. Although many lectins were shown to interact, irrespective of their monosaccharide-specificity or systematic position, glucose/mannose-specific lectins from the tribe Vicieae exhibited the best affinity for these components of the bacterial cell wall. The discrepancies observed in the binding of the muramyl-dipeptide diastereo-isomers to lectins suggest that the binding is somewhat conformation-dependent. These interactions could be possibly involved in the recognition of bacteria by plants.     

Niche construction initiates the evolution of mutualistic interactions

Niche construction theory explains how organisms' niche modifications may feed back to affect their evolutionary trajectories. In theory, the evolution of other species accessing the same modified niche may also be affected. We propose that this niche construction may be a general mechanism driving the evolution of mutualisms. Drosophilid flies benefit from accessing yeast‐infested fruits, but the consequences of this interaction for yeasts are unknown. We reveal high levels of variation among strains of Saccharomyces cerevisiae in their ability to modify fruits and attract Drosophila simulans. More attractive yeasts are dispersed more frequently, both in the lab and in the field, and flies associated with more attractive yeasts have higher fecundity. Although there may be multiple natural yeast and fly species interactions, our controlled assays in the lab and field provide evidence of a mutualistic interaction, facilitated by the yeast's niche modification.     

Instability of a hybrid module of antagonistic and mutualistic interactions

Mutualistic and antagonistic interactions coexist in nature. However, little is understood about their relative roles and interactive effects on multispecies coexistence. Here, using a three-species population dynamics model of a resource species, its exploiter, and a mutualist species, we show that a mixture of different interaction types may lead to dynamics that differ completely from those of the isolated interacting pairs. More specifically, a combination of globally stable antagonistic and mutualistic subsystems can lead to unstable population oscillations, suggesting the potential difficulty in the coexistence of antagonism and mutualism. Mutualism-induced instability arises from the indirect positive effect of mutualism on the exploiter. Furthermore, for a three-species system with a stronger mutualistic interaction to persist stably, a weaker antagonistic interaction is required. Network studies of communities composed of one type of interaction may not capture the dynamics of natural communities.     

Ant aggression and evolutionary stability in plant-ant and plant-pollinator mutualistic interactions

Mutualistic partners derive a benefit from their interaction, but this benefit can come at a cost. This is the case for plant-ant and plant-pollinator mutualistic associations. In exchange for protection from herbivores provided by the resident ants, plants supply various kinds of resources or nests to the ants. Most ant-myrmecophyte mutualisms are horizontally transmitted, and therefore, partners share an interest in growth but not in reproduction. This lack of alignment in fitness interests between plants and ants drives a conflict between them: ants can attack pollinators that cross-fertilize the host plants. Using a mathematical model, we define a threshold in ant aggressiveness determining pollinator survival or elimination on the host plant. In our model we observed that, all else being equal, facultative interactions result in pollinator extinction for lower levels of ant aggressiveness than obligatory interactions. We propose that the capacity to discriminate pollinators from herbivores should not often evolve in ants, and when it does it will be when the plants exhibit limited dispersal in an environment that is not seed saturated so that each seed produced can effectively generate a new offspring or if ants acquire an extra benefit from pollination (e.g. if ants eat fruit). We suggest specific mutualism examples where these hypotheses can be tested empirically.     

Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions

Early evolution of mutualism is characterized by big and predictable adaptive changes, including the specialization of interacting partners, such as through deleterious mutations in genes not required for metabolic cross-feeding. We sought to investigate whether these early mutations improve cooperativity by manifesting in synergistic epistasis between genomes of the mutually interacting species. Specifically, we have characterized evolutionary trajectories of syntrophic interactions of Desulfovibrio vulgaris (Dv) with Methanococcus maripaludis (Mm) by longitudinally monitoring mutations accumulated over 1000 generations of nine independently evolved communities with analysis of the genotypic structure of one community down to the single-cell level. We discovered extensive parallelism across communities despite considerable variance in their evolutionary trajectories and the perseverance within many evolution lines of a rare lineage of Dv that retained sulfate-respiration (SR+) capability, which is not required for metabolic cross-feeding. An in-depth investigation revealed that synergistic epistasis across pairings of Dv and Mm genotypes had enhanced cooperativity within SR− and SR+ assemblages, enabling their coexistence within the same community. Thus, our findings demonstrate that cooperativity of a mutualism can improve through synergistic epistasis between genomes of the interacting species, enabling the coexistence of mutualistic assemblages of generalists and their specialized variants.Subject terms: Microbial ecology, Population genetics, Symbiosis, Population dynamics, Molecular evolution     

Genetic variation in mutualistic and antagonistic interactions in an invasive legume

Oecologia - Mutualists may play an important role in invasion success. The ability to take advantage of novel mutualists or survive and reproduce despite a lack of mutualists may facilitate...     

Structure–stability relationships in networks combining mutualistic and antagonistic interactions

The relationship between the structure of ecological networks and community stability has been studied for decades. Recent developments highlighted that this relationship depended on whether interactions were antagonistic or mutualistic. Different structures promoting stability in different types of ecological networks, i.e. mutualistic or antagonistic, have been pointed out. However, these findings come from studies considering mutualistic and antagonistic interactions separately whereas we know that species are part of both types of networks simultaneously. Understanding the relationship between network structure and community stability, when mutualistic and antagonistic interactions are merged in a single network, thus appears as the next challenge to improve our understanding of the dynamics of natural communities. Using a theoretical approach, we test whether the structural characteristics known to promote stability in networks made of a single interaction type still hold for network merging mutualistic and antagonistic interactions. We show that the effects of diversity and connectance remain unchanged. But the effects of nestedness and modularity are strongly weakened in networks combining mutualistic and antagonistic interactions. By challenging the stabilizing mechanisms proposed for networks with a single interaction type, our study calls for new measures of structure for networks that integrate the diversity of interaction.