A plant effector‐triggered immunity signaling sector is inhibited by pattern‐triggered immunity

Since signaling machineries for two modes of plant‐induced immunity, pattern‐triggered immunity (PTI) and effector‐triggered immunity (ETI), extensively overlap, PTI and ETI signaling likely interact. In an Arabidopsis quadruple mutant, in which four major sectors of the signaling network, jasmonate, ethylene, PAD4, and salicylate, are disabled, the hypersensitive response (HR) typical of ETI is abolished when the Pseudomonas syringae effector AvrRpt2 is bacterially delivered but is intact when AvrRpt2 is directly expressed in planta. These observations led us to discovery of a network‐buffered signaling mechanism that mediates HR signaling and is strongly inhibited by PTI signaling. We named this mechanism the ETI‐Mediating and PTI‐Inhibited Sector (EMPIS). The signaling kinetics of EMPIS explain apparently different plant genetic requirements for ETI triggered by different effectors without postulating different signaling machineries. The properties of EMPIS suggest that information about efficacy of the early immune response is fed back to the immune signaling network, modulating its activity and limiting the fitness cost of unnecessary immune responses.     

Olfactory antennal responses of the vine weevil Otiorhynchus sulcatus to plant volatiles

Electroantennograms (EAGs) were recorded from the vine weevil, Otiorhynchus sulcatus F. (Coleoptera: Curculionidae) to a broad range of volatile plant compounds. The response profile is restricted to a small number of volatiles that evoke substantial EAGs. Large EAG responses were particularly found among green leaf volatiles (GLV) such as (E)-2-hexenol-1, (Z)-3-hexenol-1, hexanol-1, hexanal, and heptanal. Other plant volatiles eliciting responses in the weevils' antenna are 2,5-dimethylpyrazine, hexylamine, benzylalcohol, 1,2-dimethoxybenzene, o-cresol, myrtenol, 3-methylcyclohexanol, -hexalactone, and -heptalactone. EAG responses to terpenes were generally weak. Many of the monoterpenes are characteristic for the odour of conifers, a group of plants which tend to be avoided by adult vine weevils. The EAG response to several GLV and benzene derivatives in three geographically distinct populations of the vine weevil differed, suggesting between-population variation in receptor sensitivities for several compounds under test. The GLV-composition of the odour profile of potential food plants may be an important criterion for a polyphagous insect like the vine weevil to be used in host-plant selection, since compounds in this odour group dominate so strongly the EAG response profile. In multiple food-choice situations the weevils are known to prefer certain plant species and we hypothesize that they combine GLV information with that of more specific plant volatiles, thereby promoting attraction or avoidance.     

Density‐dependent demographic responses of a semelparous plant to natural variation in seed rain

The link between reproductive and vegetative ecology of flowering plants is rarely explored, despite its importance for understanding population processes and fitness. This link can be studied by using experimental or natural variation in seed input to the soil to assess how reproductive success affects vital rates of offspring. We previously reported for Ipomopsis aggregata that per‐seed probability of germinating is insensitive to density of seeds sown into plots, whereas per capita flower production among adults that grow from the seedlings declines in nonlinear fashion with density. Here we describe a parallel non‐experimental study. We related seedling emergence to estimated natural seed input (‘seed rain’) in three populations across ten summers and monitored seedlings that emerged in the first two summers throughout their life histories. Seedling emergence in 1996 was linearly related to seed rain from plants that flowered in 1995. This density independent seed‐to‐seedling transition recurred over the next nine summers, but the slope varied with springtime precipitation. Total numbers of 1996 seedlings that survived to flower and numbers of flowers they produced increased linearly with seed rain in one population, but did not vary detectably in the other two, consistent with negative density dependence. In consequence λ (the dominant eigenvalue of a population projection matrix) decreased from high values at low densities of seed rain to a relatively constant low value with greater seed rain. We also detected density dependence in the 1995 seedling cohort in survival and flower production. The similarity of results from natural and experimental studies supports a conclusion of nonlinear density dependence and shows that characterizing it requires the full life history. For this plant species and others, studies of pollination and fecundity alone may not suffice to draw conclusions about population change or fitness.     

Variation of the seed endophytic bacteria among plant populations and their plant growth‐promoting activities in a wild mustard plant species,Capsella bursa‐pastoris

Recent studies have revealed that some bacteria can inhabit plant seeds, and they are likely founders of the bacterial community in the rhizosphere of or inside plants at the early developmental stage. Given that the seedling establishment is a critical fitness component of weedy plant species, the effects of seed endophytic bacteria (SEB) on the seedling performance are of particular interest in weed ecology. Here, we characterized the SEB in natural populations of Capsella bursa‐pastoris, a model species of weed ecology. The composition of endophytic bacterial community was evaluated using deep sequencing of a 16S rDNA gene fragment. Additionally, we isolated bacterial strains from seeds and examined their plant growth‐promoting traits. Actinobacteria, Firmicutes, Alpha‐, and Gammaproteobacteria were major bacterial phyla inside seeds. C. bursa‐pastoris natural populations exhibited variable seed microbiome such that the proportion of Actinobacteria and Alphaproteobacteria differed among populations, and 60 out of 82 OTUs occurred only in a single population. Thirteen cultivable bacterial species in six genera (Bacillus, Rhodococcus, Streptomyces, Staphylococcus, Paenibacillus, Pseudomonas) were isolated, and none of them except Staphylococcus haemolyticus were previously reported as seed endophytes. Eight isolates exhibited plant growth‐promoting traits like phosphate solubilization activity, indole‐3‐acetic acid, or siderophore production. Despite the differences in the bacterial communities among plant populations, at least one isolated strain from each population stimulated shoot growth of either C. bursa‐pastoris or its close relative A. thaliana when grown with plants in the same media. These results suggest that a weedy plant species, C. bursa‐pastoris, contains bacterial endophytes inside their seeds, stimulating seedling growth and thereby potentially affecting seedling establishment.     

Structural and functional responses of plant communities to climate change‐mediated alterations in the hydrology of riparian areas in temperate Europe

The hydrology of riparian areas changes rapidly these years because of climate change‐mediated alterations in precipitation patterns. In this study, we used a large‐scale in situ experimental approach to explore effects of drought and flooding on plant taxonomic diversity and functional trait composition in riparian areas in temperate Europe. We found significant effects of flooding and drought in all study areas, the effects being most pronounced under flooded conditions. In near‐stream areas, taxonomic diversity initially declined in response to both drought and flooding (although not significantly so in all years) and remained stable under drought conditions, whereas the decline continued under flooded conditions. For most traits, we found clear indications that the functional diversity also declined under flooded conditions, particularly in near‐stream areas, indicating that fewer strategies succeeded under flooded conditions. Consistent changes in community mean trait values were also identified, but fewer than expected. This can have several, not mutually exclusive, explanations. First, different adaptive strategies may coexist in a community. Second, intraspecific variability was not considered for any of the traits. For example, many species can elongate shoots and petioles that enable them to survive shallow, prolonged flooding but such abilities will not be captured when applying mean trait values. Third, we only followed the communities for 3 years. Flooding excludes species intolerant of the altered hydrology, whereas the establishment of new species relies on time‐dependent processes, for instance the dispersal and establishment of species within the areas. We expect that altered precipitation patterns will have profound consequences for riparian vegetation in temperate Europe. Riparian areas will experience loss of taxonomic and functional diversity and, over time, possibly also alterations in community trait responses that may have cascading effects on ecosystem functioning.     

Demographic responses to climate‐driven variation in habitat quality across the annual cycle of a migratory bird species

The demography and dynamics of migratory bird populations depend on patterns of movement and habitat quality across the annual cycle. We leveraged archival GPS‐tagging data, climate data, remote‐sensed vegetation data, and bird‐banding data to better understand the dynamics of black‐headed grosbeak (Pheucticus melanocephalus) populations in two breeding regions, the coast and Central Valley of California (Coastal California) and the Sierra Nevada mountain range (Sierra Nevada), over 28 years (1992–2019). Drought conditions across the annual cycle and rainfall timing on the molting grounds influenced seasonal habitat characteristics, including vegetation greenness and phenology (maturity dates). We developed a novel integrated population model with population state informed by adult capture data, recruitment rates informed by age‐specific capture data and climate covariates, and survival rates informed by adult capture–mark–recapture data and climate covariates. Population size was relatively variable among years for Coastal California, where numbers of recruits and survivors were positively correlated, and years of population increase were largely driven by recruitment. In the Sierra Nevada, population size was more consistent and showed stronger evidence of population regulation (numbers of recruits and survivors negatively correlated). Neither region showed evidence of long‐term population trend. We found only weak support for most climate–demographic rate relationships. However, recruitment rates for the Coastal California region were higher when rainfall was relatively early on the molting grounds and when wintering grounds were relatively cool and wet. We suggest that our approach of integrating movement, climate, and demographic data within a novel modeling framework can provide a useful method for better understanding the dynamics of broadly distributed migratory species.     

Identification of a residue responsible for UDP‐sugar donor selectivity of a dihydroxybenzoic acid glycosyltransferase from Arabidopsis natural accessions

UDP‐glycosyltransferase (UGT) plays a major role in the diversity and reactivity of plant specialized metabolites by catalyzing the transfer of the sugar moiety from activated UDP‐sugars to various acceptors. Arabidopsis UGT89A2 was previously identified from a genome‐wide association study as a key factor that affects the differential accumulation of dihydroxybenzoic acid (DHBA) glycosides in distinct Arabidopsis natural accessions, including Col‐0 and C24. The in vitro enzyme assays indicate that these distinct metabolic phenotypes reflect the divergence of UGT89A2 enzyme properties in the Col‐0 and C24 accessions. UGT89A2 from Col‐0 is highly selective toward UDP‐xylose as the sugar donor, and the isoform from C24 can utilize both UDP‐glucose and UDP‐xylose but with a higher affinity to the glucose donor. The sequences of the two isozymes only differ at six amino acid residues. Examination of these amino acid residues in more natural accessions revealed a strong correlation between the amino acid polymorphism at position 153 and the DHBA glycoside accumulation pattern. Site‐directed mutagenesis that swapped residue 153 between UGT89A2 from Col‐0 and C24 reversed the UDP‐sugar preferences, indicating that residue 153 plays an important role in determining sugar donor specificity of UGT89A2. This study provides insight into the key amino acid changes that confer sugar donor selectivity on UGTs, and demonstrates the usefulness of natural variation in understanding the structure–function relationship of enzymes involved in specialized metabolism.     

Geographic variation in adaptation at the molecular level: a case study of plant immunity genes

Natural selection imposed by interacting species frequently varies among geographic locations and can lead to local adaptation, where alternative phenotypes are found in different populations. Little is known, however, about whether geographically variable selection acting on traits that mediate species interactions is consistent or strong enough to influence patterns of nucleotide variation at individual loci. To investigate this question, we examined patterns of nucleotide diversity and population structure at 16 plant innate immunity genes, with putative functions in defending plants against pathogens or herbivores, from six populations of teosinte (Zea mays ssp. parviglumis). Specifically, we tested whether patterns of population structure and within-population diversity at immunity genes differed from patterns found at nonimmunity (reference) loci and from neutral expectations derived from coalescent simulations of structured populations. For the majority of genes, we detected no strong evidence of geographically variable selection. However, in the wound-induced serine protease inhibitor (wip1), which inhibits the hydrolysis of dietary proteins in insect herbivores, one population showed unusually high levels of genetic differentiation, very low levels of nucleotide polymorphism, and was fixed for a novel replacement substitution in the active site of the protein. Taken together, these data suggest that wip1 experienced a recent selective sweep in one geographic region; this pattern may reflect local adaptation or an ongoing species-wide sweep. Overall, our results indicate that a signature of local adaptation at the molecular level may be uncommon-particularly for traits that are under complex genetic control.     

Intra‐specific variation affects the structure of the natural enemy assemblage attacking pea aphid colonies

Abstract 1. Intra‐specific variation in plant defence traits has been shown to profoundly affect herbivore community structure. Here we describe two experiments designed to test whether similar effects occur at higher trophic levels, by studying pea aphid–natural enemy interactions in a disused pasture in southern England. 2. In the first experiment, the numbers and identity of natural enemies attacking different monoclonal pea aphid colonies were recorded in a series of assays throughout the period of pea aphid activity. 3. In the summer assay, there was a significant effect of clone on the numbers of aphidophagous hoverfly larvae and the total number of non‐hoverfly natural enemies recruited. Clone also appeared to influence the attack rate suffered by the primary predator in the system, the hoverfly Episyrphus balteatus, by Diplazon laetatorius, an ichneumonid parasitoid. Colonies were generally driven to extinction by hoverfly attack, resulting in the recording of low numbers of parasitoids and entomopathogens, suggesting intense intra‐guild predation. 4. To further examine the influence of clonal variation on the recruitment of natural enemies, a second experiment was performed to monitor the temporal dynamics of community development. Colonies were destructively sampled every other day and the numbers of natural enemies attacking aphid colonies were recorded. These data demonstrated that clonal variation influenced the timing, abundance, and identity of natural enemies attacking aphid colonies. 5. Taken together, these data suggest that clonal variation may have a significant influence on the patterns of interactions between aphids and their natural enemies, and that such effects are likely to affect our understanding of the ecology and biological control of these insect herbivores.     

The contribution of the mitochondrial genome to sex‐specific fitness variance

Maternal inheritance of mitochondrial DNA (mtDNA) facilitates the evolutionary accumulation of mutations with sex‐biased fitness effects. Whereas maternal inheritance closely aligns mtDNA evolution with natural selection in females, it makes it indifferent to evolutionary changes that exclusively benefit males. The constrained response of mtDNA to selection in males can lead to asymmetries in the relative contributions of mitochondrial genes to female versus male fitness variation. Here, we examine the impact of genetic drift and the distribution of fitness effects (DFE) among mutations—including the correlation of mutant fitness effects between the sexes—on mitochondrial genetic variation for fitness. We show how drift, genetic correlations, and skewness of the DFE determine the relative contributions of mitochondrial genes to male versus female fitness variance. When mutant fitness effects are weakly correlated between the sexes, and the effective population size is large, mitochondrial genes should contribute much more to male than to female fitness variance. In contrast, high fitness correlations and small population sizes tend to equalize the contributions of mitochondrial genes to female versus male variance. We discuss implications of these results for the evolution of mitochondrial genome diversity and the genetic architecture of female and male fitness.     

Contrasting effects of plant inter‐ and intraspecific variation on community trait responses to restoration of a sandy grassland ecosystem

Changes in plant community traits along an environmental gradient are caused by interspecific and intraspecific trait variation. However, little is known about the role of interspecific and intraspecific trait variation in plant community responses to the restoration of a sandy grassland ecosystem. We measured five functional traits of 34 species along a restoration gradient of sandy grassland (mobile dune, semi‐fixed dune, fixed dune, and grassland) in Horqin Sand Land, northern China. We examined how community‐level traits varied with habitat changes and soil gradients using both abundance‐weighted and non‐weighted averages of trait values. We quantified the relative contribution of inter‐ and intraspecific trait variation in specific leaf area (SLA), leaf dry matter content (LDMC), leaf carbon content (LCC), leaf nitrogen content (LNC), and plant height to the community response to habitat changes in the restoration of sandy grassland. We found that five weighted community‐average traits varied significantly with habitat changes. Along the soil gradient in the restoration of sandy grassland, plant height, SLA, LDMC, and LCC increased, while LNC decreased. For all traits, there was a greater contribution of interspecific variation to community response in regard to habitat changes relative to that of intraspecific variation. The relative contribution of the interspecific variation effect of an abundance‐weighted trait was greater than that of a non‐weighted trait with regard to all traits except LDMC. A community‐level trait response to habitat changes was due largely to species turnover. Though the intraspecific shift plays a small role in community trait response to habitat changes, it has an effect on plant coexistence and the maintenance of herbaceous plants in sandy grassland habitats. The context dependency of positive and negative covariation between inter‐ and intraspecific variation further suggests that both effects of inter‐ and intraspecific variation on a community trait should be considered when understanding a plant community response to environmental changes in sandy grassland ecosystems.     

HSPRO acts via SnRK1-mediated signaling in the regulation of Nicotiana attenuata seedling growth promoted by Piriformospora indica

Nicotiana attenuata HSPRO (NaHSPRO) is a negative regulator of seedling growth promoted by the fungus Piriformospora indica. Homologs of NaHSPRO in Arabidopsis thaliana (i.e., AtHSPRO1 and AtHSPRO2) are known to physically interact with the AKINβγ subunit of the SnRK1 complex.² To investigate whether NaHSPRO is associated with SnRK1 function during the stimulation of seedling growth by P. indica, we studied N. attenuata plants silenced in the expression of NaGAL83 (as-gal83 plants)—a gene that encodes for the regulatory β-subunit of SnRK1—and plants silenced in the expression of both NaHSPRO and NaGAL83 (ir-hspro/as-gal83 plants). The results showed that P. indica differentially stimulated the growth of both as-gal83 and ir-hspro/as-gal83 seedlings compared with control seedlings, with a magnitude similar to that observed in ir-hspro seedlings. Thus, we showed that, similar to NaHSPRO, NaGAL83 is a negative regulator of seedling growth stimulated by P. indica. We propose that the effect of NaHSPRO on seedling growth is associated with SnRK1 signaling.     

BAK1 is required for the attenuation of ethylene‐inducing xylanase (Eix)‐induced defense responses by the decoy receptor LeEix1

Elicitor recognition plays a key role in the reaction of plants to pathogens and the induction of plant defense responses. Furthermore, plant–microbe interactions involve numerous regulatory systems essential for plant defense against pathogens. Ethylene‐inducing xylanase (Eix) is a potent elicitor of plant defense responses in specific cultivars of tobacco (Nicotiana tabacum) and tomato (Solanum lycopersicum). The Eix receptors (LeEix1 and LeEix2) belong to a superclade of leucine‐rich repeat receptor‐like proteins (RLP) with a signal for receptor‐mediated endocytosis, which was shown to be essential for proper induction of defense responses. Both receptors are able to bind Eix, while only LeEix2 mediates defense responses. Here we demonstrate that LeEix1 heterodimerizes with LeEix2 upon application of the Eix elicitor. We show that LeEix1 attenuates Eix‐induced internalization and signaling of the LeEix2 receptor. Furthermore, we demonstrate, using yeast two‐hybrid and in planta bimolecular fluorescence complementation assays, that the brassinosteroid co‐receptor, BAK1, binds LeEix1 but not LeEix2. In BAK1‐silenced plants, LeEix1 was no longer able to attenuate plant responses to Eix, indicating that BAK1 is required for this attenuation. We suggest that LeEix1 functions as a decoy receptor for LeEix2, a function which requires BAK1.