Plant cell wall-mediated disease resistance: Current understanding and future perspectives.

Beyond their function as structural barriers, plant cell walls are essential elements for the adaptation of plants to environmental conditions. Cell walls are dynamic structures whose composition and integrity can be altered in response to environmental challenges and developmental cues. These wall changes are perceived by plant sensors/receptors to trigger adaptative responses during development and upon stress perception. Plant cell wall damage caused by pathogen infection, wounding, or other stresses leads to the release of wall molecules, such as carbohydrates (glycans), that function as damage-associated molecular patterns (DAMPs). DAMPs are perceived by the extracellular ectodomains (ECDs) of pattern recognition receptors (PRRs) to activate pattern-triggered immunity (PTI) and disease resistance. Similarly, glycans released from the walls and extracellular layers of microorganisms interacting with plants are recognized as microbe-associated molecular patterns (MAMPs) by specific ECD-PRRs triggering PTI responses. The number of oligosaccharides DAMPs/MAMPs identified that are perceived by plants has increased in recent years. However, the structural mechanisms underlying glycan recognition by plant PRRs remain limited. Currently, this knowledge is mainly focused on receptors of the LysM-PRR family, which are involved in the perception of various molecules, such as chitooligosaccharides from fungi and lipo-chitooligosaccharides (i.e., Nod/MYC factors from bacteria and mycorrhiza, respectively) that trigger differential physiological responses. Nevertheless, additional families of plant PRRs have recently been implicated in oligosaccharide/polysaccharide recognition. These include receptor kinases (RKs) with leucine-rich repeat and Malectin domains in their ECDs (LRR-MAL RKs), Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE group (CrRLK1L) with Malectin-like domains in their ECDs, as well as wall-associated kinases, lectin-RKs, and LRR-extensins. The characterization of structural basis of glycans recognition by these new plant receptors will shed light on their similarities with those of mammalians involved in glycan perception. The gained knowledge holds the potential to facilitate the development of sustainable, glycan-based crop protection solutions.

Leucine rich repeat-malectin receptor kinases IGP1/CORK1, IGP3 and IGP4 are required for arabidopsis immune responses triggered by ß-1,4-D-Xylo-oligosaccharides from plant cell walls.

Pattern-Triggered Immunity (PTI) in plants is activated upon recognition by Pattern Recognition Receptors (PRRs) of Damage- and Microbe-Associated Molecular Patterns (DAMPs and MAMPs) from plants or microorganisms, respectively. An increasing number of identified DAMPs/MAMPs are carbohydrates from plant cell walls and microbial extracellular layers, which are perceived by plant PRRs, such as LysM and Leucine Rich Repeat-Malectin (LRR-MAL) receptor kinases (RKs). LysM-RKs (e.g. CERK1, LYK4 and LYK5) are needed for recognition of fungal MAMP chitohexaose (ß-1,4-D-(GlcNAc)6, CHI6), whereas IGP1/CORK1, IGP3 and IGP4 LRR-MAL RKs are required for perception of ß-glucans, like cellotriose (ß-1,4-D-(Glc)3, CEL3) and mixed-linked glucans. We have explored the diversity of carbohydrates perceived by Arabidopsis thaliana seedlings by determining PTI responses upon treatment with different oligosaccharides and polysaccharides. These analyses revealed that plant oligosaccharides from xylans [ß-1,4-D-(xylose)4 (XYL4)], glucuronoxylans and α-1,4-glucans, and polysaccharides from plants and seaweeds activate PTI. Cross-elicitation experiments of XYL4 with other glycans showed that the mechanism of recognition of XYL4 and the DAMP 33-α-L-arabinofuranosyl-xylotetraose (XA3XX) shares some features with that of CEL3 but differs from that of CHI6. Notably, XYL4 and XA3XX perception is impaired in igp1/cork1, igp3 and igp4 mutants, and almost not affected in cerk1 lyk4 lyk5 triple mutant. XYL4 perception is conserved in different plant species since XYL4 pre-treatment triggers enhanced disease resistance in tomato to Pseudomonas syringae pv tomato DC3000 and PTI responses in wheat. These results expand the number of glycans triggering plant immunity and support IGP1/CORK1, IGP3 and IGP4 relevance in Arabidopsis thaliana glycans perception and PTI activation. Significance Statement: The characterization of plant immune mechanisms involved in the perception of carbohydrate-based structures recognized as DAMPs/MAMPs is needed to further understand plant disease resistance modulation. We show here that IGP1/CORK1, IGP3 and IGP4 LRR-MAL RKs are required for the perception of carbohydrate-based DAMPs ß-1,4-D-(xylose)4 (XYL4) and 33-α-L-arabinofuranosyl-xylotetraose (XA3XX), further expanding the function of these LRR-MAL RKs in plant glycan perception and immune activation.

Stronger compensatory thermal adaptation of soil microbial respiration with higher substrate availability.

Ongoing global warming is expected to augment soil respiration by increasing the microbial activity, driving self-reinforcing feedback to climate change. However, the compensatory thermal adaptation of soil microorganisms and substrate depletion may weaken the effects of rising temperature on soil respiration. To test this hypothesis, we collected soils along a large-scale forest transect in eastern China spanning a natural temperature gradient, and we incubated the soils at different temperatures with or without substrate addition. We combined the exponential thermal response function and a data-driven model to study the interaction effect of thermal adaptation and substrate availability on microbial respiration and compared our results to those from two additional continental and global independent datasets. Modeled results suggested that the effect of thermal adaptation on microbial respiration was greater in areas with higher mean annual temperatures, which is consistent with the compensatory response to warming. In addition, the effect of thermal adaptation on microbial respiration was greater under substrate addition than under substrate depletion, which was also true for the independent datasets reanalyzed using our approach. Our results indicate that thermal adaptation in warmer regions could exert a more pronounced negative impact on microbial respiration when the substrate availability is abundant. These findings improve the body of knowledge on how substrate availability influences the soil microbial community-temperature interactions, which could improve estimates of projected soil carbon losses to the atmosphere through respiration.

Arabidopsis immune responses triggered by cellulose- and mixed-linked glucan-derived oligosaccharides require a group of leucine-rich repeat malectin receptor kinases.

The plant immune system perceives a diversity of carbohydrate ligands from plant and microbial cell walls through the extracellular ectodomains (ECDs) of pattern recognition receptors (PRRs), which activate pattern-triggered immunity (PTI). Among these ligands are oligosaccharides derived from mixed-linked ß-1,3/ß-1,4-glucans (MLGs; e.g. ß-1,4-D-(Glc)2 -ß-1,3-D-Glc, MLG43) and cellulose (e.g. ß-1,4-D-(Glc)3 , CEL3). The mechanisms behind carbohydrate perception in plants are poorly characterized except for fungal chitin oligosaccharides (e.g. ß-1,4-d-(GlcNAc)6 , CHI6), which involve several receptor kinase proteins (RKs) with LysM-ECDs. Here, we describe the isolation and characterization of Arabidopsis thaliana mutants impaired in glycan perception (igp) that are defective in PTI activation mediated by MLG43 and CEL3, but not by CHI6. igp1-igp4 are altered in three RKs - AT1G56145 (IGP1), AT1G56130 (IGP2/IGP3) and AT1G56140 (IGP4) - with leucine-rich-repeat (LRR) and malectin (MAL) domains in their ECDs. igp1 harbors point mutation E906K and igp2 and igp3 harbor point mutation G773E in their kinase domains, whereas igp4 is a T-DNA insertional loss-of-function mutant. Notably, isothermal titration calorimetry (ITC) assays with purified ECD-RKs of IGP1 and IGP3 showed that IGP1 binds with high affinity to CEL3 (with dissociation constant KD  = 1.19 ± 0.03 µm) and cellopentaose (KD  = 1.40 ± 0.01 µM), but not to MLG43, supporting its function as a plant PRR for cellulose-derived oligosaccharides. Our data suggest that these LRR-MAL RKs are components of a recognition mechanism for both cellulose- and MLG-derived oligosaccharide perception and downstream PTI activation in Arabidopsis.

Soils in warmer and less developed countries have less micronutrients globally.

Soil micronutrients are capital for the delivery of ecosystem functioning and food provision worldwide. Yet, despite their importance, the global biogeography and ecological drivers of soil micronutrients remain virtually unknown, limiting our capacity to anticipate abrupt unexpected changes in soil micronutrients in the face of climate change. Here, we analyzed >1300 topsoil samples to examine the global distribution of six metallic micronutrients (Cu, Fe, Mn, Zn, Co and Ni) across all continents, climates and vegetation types. We found that warmer arid and tropical ecosystems, present in the least developed countries, sustain the lowest contents of multiple soil micronutrients. We further provide evidence that temperature increases may potentially result in abrupt and simultaneous reductions in the content of multiple soil micronutrients when a temperature threshold of 12-14°C is crossed, which may be occurring on 3% of the planet over the next century. Altogether, our findings provide fundamental understanding of the global distribution of soil micronutrients, with direct implications for the maintenance of ecosystem functioning, rangeland management and food production in the warmest and poorest regions of the planet.

Trends in soil mercury stock associated with pollution sources on a Mediterranean island (Majorca, Spain).

Hg is a global concern given its adverse effects on human health, food security and the environment, and it requiring actions to identify major local Hg sources and to evaluate pollution. Our study provides the first assessment of Hg stock trends on the entire Majorca surface, identifying major Hg sources by studying the spatiotemporal soil Hg variation at two successive times (2006 and 2016-17). The Hg soil concentration ranged from 14 to 258 µg kg-1 (mean 52 µg kg-1). Higher concentrations (over 100 µg kg-1) were found in two areas: (i) close to the Alcudia coal-fired power plant; (ii) in the city of La Palma. During the 11-year, the total Hg stock in Majorcan soil increased from 432.96 tons to 493.18 tones (14% increase). Based on a block kriging analysis, soil Hg enrichment due to power plant emissions was clearly detectable on a local scale (i.e. a shorter distance than 18 km from the power plant). Nonetheless, a significant island-wide Hg increase due to diffuse pollution was reported. This result could be extrapolated to other popular tourist destinations in the Mediterranean islands where tourism has increased in recent decades In short, more than 60 tons of Hg have accumulated on Majorca island in 11 years.

Functional rarity and evenness are key facets of biodiversity to boost multifunctionality.

The functional traits of organisms within multispecies assemblages regulate biodiversity effects on ecosystem functioning. Yet how traits should assemble to boost multiple ecosystem functions simultaneously (multifunctionality) remains poorly explored. In a multibiome litter experiment covering most of the global variation in leaf trait spectra, we showed that three dimensions of functional diversity (dispersion, rarity, and evenness) explained up to 66% of variations in multifunctionality, although the dominant species and their traits remained an important predictor. While high dispersion impeded multifunctionality, increasing the evenness among functionally dissimilar species was a key dimension to promote higher multifunctionality and to reduce the abundance of plant pathogens. Because too-dissimilar species could have negative effects on ecosystems, our results highlight the need for not only diverse but also functionally even assemblages to promote multifunctionality. The effect of functionally rare species strongly shifted from positive to negative depending on their trait differences with the dominant species. Simultaneously managing the dispersion, evenness, and rarity in multispecies assemblages could be used to design assemblages aimed at maximizing multifunctionality independently of the biome, the identity of dominant species, or the range of trait values considered. Functional evenness and rarity offer promise to improve the management of terrestrial ecosystems and to limit plant disease risks.

Differential Expression of Fungal Genes Determines the Lifestyle of Plectosphaerella Strains During Arabidopsis thaliana Colonization.

The fungal genus Plectosphaerella comprises species and strains with different lifestyles on plants, such as P. cucumerina, which has served as model for the characterization of Arabidopsis thaliana basal and nonhost resistance to necrotrophic fungi. We have sequenced, annotated, and compared the genomes and transcriptomes of three Plectosphaerella strains with different lifestyles on A. thaliana, namely, PcBMM, a natural pathogen of wild-type plants (Col-0), Pc2127, a nonpathogenic strain on Col-0 but pathogenic on the immunocompromised cyp79B2 cyp79B3 mutant, and P0831, which was isolated from a natural population of A. thaliana and is shown here to be nonpathogenic and to grow epiphytically on Col-0 and cyp79B2 cyp79B3 plants. The genomes of these Plectosphaerella strains are very similar and do not differ in the number of genes with pathogenesis-related functions, with the exception of secreted carbohydrate-active enzymes (CAZymes), which are up to five times more abundant in the pathogenic strain PcBMM. Analysis of the fungal transcriptomes in inoculated Col-0 and cyp79B2 cyp79B3 plants at initial colonization stages confirm the key role of secreted CAZymes in the necrotrophic interaction, since PcBMM expresses more genes encoding secreted CAZymes than Pc2127 and P0831. We also show that P0831 epiphytic growth on A. thaliana involves the transcription of specific repertoires of fungal genes, which might be necessary for epiphytic growth adaptation. Overall, these results suggest that in-planta expression of specific sets of fungal genes at early stages of colonization determine the diverse lifestyles and pathogenicity of Plectosphaerella strains.

Contrasting mechanisms underlie short- and longer-term soil respiration responses to experimental warming in a dryland ecosystem.

Soil carbon losses to the atmosphere through soil respiration are expected to rise with ongoing temperature increases, but available evidence from mesic biomes suggests that such response disappears after a few years of experimental warming. However, there is lack of empirical basis for these temporal dynamics in soil respiration responses, and for the mechanisms underlying them, in drylands, which collectively form the largest biome on Earth and store 32% of the global soil organic carbon pool. We coupled data from a 10 year warming experiment in a biocrust-dominated dryland ecosystem with laboratory incubations to confront 0-2 years (short-term hereafter) versus 8-10 years (longer-term hereafter) soil respiration responses to warming. Our results showed that increased soil respiration rates with short-term warming observed in areas with high biocrust cover returned to control levels in the longer-term. Warming-induced increases in soil temperature were the main drivers of the short-term soil respiration responses, whereas longer-term soil respiration responses to warming were primarily driven by thermal acclimation and warming-induced reductions in biocrust cover. Our results highlight the importance of evaluating short- and longer-term soil respiration responses to warming as a mean to reduce the uncertainty in predicting the soil carbon-climate feedback in drylands.

Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally.

The degree to which climate warming will stimulate soil organic carbon (SOC) losses via heterotrophic respiration remains uncertain, in part because different or even opposite microbial physiology and temperature relationships have been proposed in SOC models. We incorporated competing microbial carbon use efficiency (CUE)-mean annual temperature (MAT) and enzyme kinetic-MAT relationships into SOC models, and compared the simulated mass-specific soil heterotrophic respiration rates with multiple published datasets of measured respiration. The measured data included 110 dryland soils globally distributed and two continental to global-scale cross-biome datasets. Model-data comparisons suggested that a positive CUE-MAT relationship best predicts the measured mass-specific soil heterotrophic respiration rates in soils distributed globally. These results are robust when considering models of increasing complexity and competing mechanisms driving soil heterotrophic respiration-MAT relationships (e.g., carbon substrate availability). Our findings suggest that a warmer climate selects for microbial communities with higher CUE, as opposed to the often hypothesized reductions in CUE by warming based on soil laboratory assays. Our results help to build the impetus for, and confidence in, including microbial mechanisms in soil biogeochemical models used to forecast changes in global soil carbon stocks in response to warming.

Soil microbial respiration adapts to ambient temperature in global drylands.

Heterotrophic soil microbial respiration-one of the main processes of carbon loss from the soil to the atmosphere-is sensitive to temperature in the short term. However, how this sensitivity is affected by long-term thermal regimes is uncertain. There is an expectation that soil microbial respiration rates adapt to the ambient thermal regime, but whether this adaptation magnifies or reduces respiration sensitivities to temperature fluctuations remains unresolved. This gap in understanding is particularly pronounced for drylands because most studies conducted so far have focused on mesic systems. Here, we conduct an incubation study using soil samples from 110 global drylands encompassing a wide gradient in mean annual temperature. We test how mean annual temperature affects soil respiration rates at three assay temperatures while controlling for substrate depletion and microbial biomass. Estimated soil respiration rates at the mean microbial biomass were lower in sites with higher mean annual temperatures across the three assayed temperatures. The patterns observed are consistent with expected evolutionary trade-offs in the structure and function of enzymes under different thermal regimes. Therefore, our results suggest that soil microbial respiration adapts to the ambient thermal regime in global drylands.

Pathways regulating decreased soil respiration with warming in a biocrust-dominated dryland.

A positive soil carbon (C)-climate feedback is embedded into the climatic models of the IPCC. However, recent global syntheses indicate that the temperature sensitivity of soil respiration (RS ) in drylands, the largest biome on Earth, is actually lower in warmed than in control plots. Consequently, soil C losses with future warming are expected to be low compared with other biomes. Nevertheless, the empirical basis for these global extrapolations is still poor in drylands, due to the low number of field experiments testing the pathways behind the long-term responses of soil respiration (RS ) to warming. Importantly, global drylands are covered with biocrusts (communities formed by bryophytes, lichens, cyanobacteria, fungi, and bacteria), and thus, RS responses to warming may be driven by both autotrophic and heterotrophic pathways. Here, we evaluated the effects of 8-year experimental warming on RS , and the different pathways involved, in a biocrust-dominated dryland in southern Spain. We also assessed the overall impacts on soil organic C (SOC) accumulation over time. Across the years and biocrust cover levels, warming reduced RS by 0.30 µmol CO2  m-2  s-1 (95% CI = -0.24 to 0.84), although the negative warming effects were only significant after 3 years of elevated temperatures in areas with low initial biocrust cover. We found support for different pathways regulating the warming-induced reduction in RS at areas with low (microbial thermal acclimation via reduced soil mass-specific respiration and ß-glucosidase enzymatic activity) vs. high (microbial thermal acclimation jointly with a reduction in autotrophic respiration from decreased lichen cover) initial biocrust cover. Our 8-year experimental study shows a reduction in soil respiration with warming and highlights that biocrusts should be explicitly included in modeling efforts aimed to quantify the soil C-climate feedback in drylands.

Differential responses of carbon-degrading enzyme activities to warming: Implications for soil respiration.

Extracellular enzymes catalyze rate-limiting steps in soil organic matter decomposition, and their activities (EEAs) play a key role in determining soil respiration (SR). Both EEAs and SR are highly sensitive to temperature, but their responses to climate warming remain poorly understood. Here, we present a meta-analysis on the response of soil cellulase and ligninase activities and SR to warming, synthesizing data from 56 studies. We found that warming significantly enhanced ligninase activity by 21.4% but had no effect on cellulase activity. Increases in ligninase activity were positively correlated with changes in SR, while no such relationship was found for cellulase. The warming response of ligninase activity was more closely related to the responses of SR than a wide range of environmental and experimental methodological factors. Furthermore, warming effects on ligninase activity increased with experiment duration. These results suggest that soil microorganisms sustain long-term increases in SR with warming by gradually increasing the degradation of the recalcitrant carbon pool.