Search bioRxiv⌕ Search

Biology subjects

Polle, A.

Publications and source records attributed to Polle, A..

14 recordsLinked to original sources

Divergent Strategies of Mycorrhiza-Mediated Drought Adaptation in Poplar

Mycorrhizal symbiosis shapes plant growth and stress resilience. Here, we compared physiological and molecular responses of poplars colonized by Paxillus involutus (Pi) or Cenococcum geophilum (Cg) under control conditions, drought stress, and recovery. Both fungal species primed distinct local (root) and systemic (leaf) defenses compared to non-inoculated (Ni) plants. Cg-colonized poplars exhibited constitutively elevated transcripts of heat shock proteins (HSPs), galactinol synthase, and aquaporins in roots and leaves, irrespective of drought. Pi colonization enhanced growth and nitrogen-use-efficiency along with transcriptional increases of TOR/RAPTOR complex. Under severe soil moisture decline, Pi and Ni poplars showed reduced water potential, photosynthesis, growth, and leaf shedding, whereas Cg-colonized plants maintained water status, sustained photosynthesis, and retained foliage. These results reveal two contrasting mycorrhiza-mediated drought strategies in poplar: Pi fosters stress acclimation via drought-induced leaf abscission, enabling rapid recovery; Cg suppresses growth even without stress, conferring constitutive tolerance. Ectomycorrhizal species thus occupy different positions on the growth- defense trade-off spectrum. Such species-specific effects have important ecological and applied implications, enabling targeted use of EM fungi in forestry and agriculture depending on whether maximizing productivity or enhancing stress resilience is the primary goal.

plant biology↗

Divergent functions of three Kunitz trypsin inhibitor (KTI) proteins in herbivore defense in poplar

BackgroundClimate warming promotes the expansion of insect pests. Among the inducible defense responses activated by attacked plants, Kunitz trypsin protease inhibitors (KTIs) play an outstanding role. KTIs affect food digestion and thereby control the fitness of herbivorous insects. Poplars contain an expanded family of KTIs, whose distinct intrinsic functions are under investigation. Here, we set out to identify KTIs with anti-herbivore activity and assessed the potential growth trade-off incurred by high KTI expression levels. ResultsWe identified 28 KTIs in the haploid genome of Populus x canescens, 21 of them were responsive to herbivory. The greatest induction was observed for KTI_400, KTI_600 and KTI_0882 (P. trichocarpa orthologues Potri.019G124400, Potri.019G124600, Potri.019G088200), whereas a moderate response was found for KTI_53200 (Potri017G153200 orthologue), a protein mainly localized in the xylem sap. Mechanical wounding and methyl-jasmonate resulted in fast and strong induction of KTI_400 and KTI_600 and moderate or lacking responses in KTI_0882 and KTI_53200. Increased KTI expression levels were associated with upregulation of ALLENE OXIDE SYNTHASE (AOS), whereas exposure to compounds eliciting ethylene or salicylic acid signaling did not affect KTIs. We generated stable CRISPR/Cas12a-mediated knock-out and p35S-mediated overexpression lines of KTI_400, KTI_600 and KTI_53200 in Populus x canescens. Among the wildtype and transgenic lines, only kti_400+kti_600 double knock-out lines produced greater biomass. Larvae of Helicoverpa armigera, a pest expanding in Europe due to a warmer climate, were allowed to feed on wildtype and transgenic poplar lines. Transgenic poplars overexpressing KTI_400 or KTI_600 resulted in reduced and their double knock-out lines in increased weight gain of the larvae. In contrast, overexpressing or knock-out lines of KTI_53200 had no effect on larval weight gain compared with controls. ConclusionKTI_400 and KTI_600 are potent, natural in-planta anti-herbivorous agents. Their expression is associated with larval growth reductions. Modulation of KTI_53200 levels had no direct effects on the fitness of leaf-feeding H. armigera or on plant growth. This study sheds light on the potential application of KTI in plant defenses and biocontrol against herbivores in trees and presents new options to investigate growth-defense theories.

plant biology↗

Volatile-Mediated Plant Defense Networks: Field Evidence for Isoprene as a Short-Distance Immune Signal

Isoprene, the most abundant hydrocarbon emitted by vegetation, protects photosynthesis against oxidative and thermal stress and significantly impacts atmospheric chemistry. While laboratory studies suggest a role for isoprene in plant defense, its function in plant-plant communication under natural conditions remains unclear. Here, we demonstrate that isoprene acts as a signaling molecule, triggering systemic immune responses in neighboring plants against bacterial pathogens under field conditions. We established an experimental system using wild-type and transgenic silver birch (Betula pendula) lines engineered to emit varying levels of isoprene. Over two growing seasons, we examined the effects of birch-emitted volatile organic compounds on neighboring Arabidopsis thaliana, including wild-type and immune signaling mutants (llp1: legume lectin-like protein 1; jar1: jasmonate resistant 1). Isoprene emission rates positively correlated with systemic resistance in receiver plants, with higher emissions enhancing inhibition of Pseudomonas syringae growth. This immune response occurred independently of jasmonate signaling but required functional LLP1, suggesting a specific recognition pathway. By combining Arabidopsis mutant responses with birch volatile profiles, we confirmed that isoprene, rather than other terpenoids, mediates this effect. These findings reveal an unrecognized ecological function of isoprene as an airborne immune signal, establishing transgenic birch as a robust model for studying volatile-mediated plant defense networks in natural environments. Our results provide new insights into the molecular mechanisms underlying plant volatile perception and expand our understanding of chemical communication in terrestrial ecosystems. Significance StatementIsoprene, the most abundant volatile organic compound released by plants, protects against abiotic stress. Here, we demonstrate that isoprene also functions under ambient atmosphere as a short-distance immune signal, enhancing neighboring plants resistance to bacterial pathogens. This finding reveals a putative ecological role of isoprene in plant defense networks and suggests strategies for sustainable agriculture and forest management under environmental stress.

plant biology↗

A single pathogen-secreted protein reprograms plants for drought resilience

Climate change-enforced drought stress conditions and diseases caused by pathogens often co-occur and represent one of the greatest challenges in plant science1-3. Wilt pathogens that colonize water-conducting plant tissues can aggravate the problem and affect a wide range of agricultural crops4,5. However, whilst fungal infections with the vascular pathogen Verticillium dahliae are typically associated with wilt symptoms due to occlusion of xylem tissues, the related V. longisporum induces de novo formation of tracheary elements6,7. This promotes not only its virulence but also enables elevated water storage capacity of the infected host plant and resilience against drought stress conditions6,7. Here, we identified a secreted Verticillium protein, TRANSDIFFERENTIATION EFFECTOR (TRADE), which triggers cell identity switches of bundle sheath cells into tracheary elements. We show that TRADE interacts with the intracellular plant protein VARICOSE (VCS), a conserved component of the mRNA turnover machinery and ortholog of the metazoan protein ENHANCER OF DECAPPING 4 (EDC4/HEDLS/Ge-1)8. The TRADE-VCS interaction induces SUCROSE NON-FERMENTING 1 (SNF1)-related protein kinase (SRK)-dependent phosphorylation and thus dysfunction of VCS. This affects the abundance of mRNAs encoding master regulators of xylem differentiation and demonstrates how a single pathogen effector protein triggers complex tissue-specific developmental reprogramming and thus promotes abiotic stress resilience.

plant biology↗

Land-use changes impact root-fungal network connectivity in a global biodiversity hotspot

O_LICross-kingdom associations play a fundamental role in ecological processes. Yet our understanding of plant-fungal co-occurrences in tropical rainforests and the potential impacts of land-use change shaping species connections remains limited. C_LIO_LIBy using amplicon sequencing on DNA from roots and their associated fungal communities, we aim to understand the impact of rainforest transformation on the composition and structure of root-fungal ecological networks in human-modified landscapes in Sumatra, Indonesia. C_LIO_LIEach land-use type supports a distinctive set of indicator species, which are organisms that reflect specific environmental conditions and can signal changes in ecosystem health. We observed a decline in the richness of plant species indicators and plant-fungal associations with increasing land-use intensification. Additionally, there is a turnover in root communities, shifting from native and endemic species in rainforests to non-native, generalist herbaceous species in rubber and oil palm plantations. C_LIO_LIPlant-fungal connectivity significantly declined with increasing land-use intensification, suggesting that managed ecosystems may have weakened root-fungal interactions. Network analysis highlights the distinct responses of various fungal groups. For instance, arbuscular mycorrhizal fungi (AMF) showed fewer connections with modules linked to oil palm and rubber roots, indicating weakened root-fungal associations in monocultures. This aligns with the observed reduction in AMF diversity in converted land-use areas compared to forests, further reinforcing the negative impact of land-use practices in oil palm and rubber monocultures on AMF diversity. C_LIO_LISynthesis. Dimensioning the impacts of rainforest transformations belowground is constrained by our understanding of fungal functional guilds. Highly modified systems exhibited fewer connections, suggesting a dynamic restructuring of root-fungal relationships in response to land-use changes. Understanding the intricate interplay between plants and fungi in the face of land-use change can provide valuable information for conservation efforts, agricultural practices, and ecosystem management strategies aimed at promoting biodiversity, soil health, and ecosystem resilience in the context of changing environmental conditions. Moreover, it underscores the importance of communities networks in land-use planning and management decisions to support plant and fungal diversity in terrestrial ecosystems. C_LI

ecology↗

Wax ester synthase overexpression affects stomatal development, water consumption and growth of poplars

Poplars are important fast-growing biomass crops. Their water-spending lifestyle renders them susceptible to drought and threatens plantations under global climate change with extended periods of water deprivation. The cuticle and stomatal regulation are major traits to protect plants from uncontrolled water loss. Here, we targeted the wax biosynthesis pathway of Populus x canescens by overexpressing jojoba (Simmondsia chinensis) wax ester synthase (ScWS) to improve cuticular properties. ScWS expression caused accumulation of lipid droplets inside the cells, decreased transcript levels of endogenous wax biosynthetic genes, and moderate shifts in surface wax composition but did not affect non-stomatal water loss. During short- and long-term drought scenarios under greenhouse and outdoor conditions, ScWS lines showed decreased stomatal conductance and increased water-use-efficiencies leading to a water-saving phenotype and delayed leaf shedding. This phenotype was caused by a high fraction (80%) of wax-occluded or semi-occluded stomata, and was accompanied by suppression of OCCLUDED STOMATAL PORE1 (OSP1), known to cause abberant wax accumulation at the stomatal ledges as found here. Occluded stomata limited poplar photosynthesis under high but not under low light intensities. Leaf damage and insect scores did not reveal differences compared with wild-type plants. Biomass production of ScWS lines was unaffected in short-term experiments but dropped below that of wild-type poplars at the end of two field seasons, indicating a growth trade-off. In conclusion, our study pinpoints a tight connection between wax biosynthesis and stomatal features and opens a new avenue to improve poplar water consumption by optimizing stomatal ledges with refined biotechnological approaches.

plant biology↗

Planting diversity begets multifaceted tree diversity in oil palm landscapes

Optimizing restoration outcomes is crucial for enhancing multifaceted diversity, resilience, and ecosystem functioning in monoculture-dominated landscapes globally. Here, we experimentally tested the performance of passive and active restoration strategies to recover taxonomic, phylogenetic, and functional diversity by establishing 52 tree islands in an oil palm landscape. Tree diversity via natural regeneration was shaped by local rather than landscape properties, with the diversity of planted tree species and tree island size driving higher multifaceted diversity. We show that large tree islands with higher initial planted diversity catalyze the recovery of multifaceted diversity at both the local and landscape level, including forest-associated species. Our results demonstrate that planted diversity begets regenerating diversity, overcoming major limitations of natural regeneration in highly modified landscapes. By elucidating the contribution of experimental, local, and landscape drivers to natural regeneration, these findings provide practical insights to make oil palm landscapes more biodiversity-friendly by enhancing functional and phylogenetic diversity within plantations.

ecology↗

Scale-dependent landscape-biodiversity relationships shape multi-taxa diversity in an oil palm monoculture under restoration

Enhancing biodiversity in monoculture-dominated landscapes is a pressing restoration challenge. Tree islands can enhance biodiversity locally, but the role of scale-dependent processes on local biodiversity remains unclear. Using a multi-scale approach, we explored how scale-dependent processes influence the diversity of seven taxa (woody plants, understory arthropods, birds, herbaceous plants and soil bacteria, fauna, and fungi) within 52 experimental tree islands embedded in an oil palm landscape. We show that local, metacommunity (between islands), and landscape properties shaped above- and below-ground taxa diversity, with the stronger effects on above-ground taxa. The spatial extent that best-predicted diversity ranged from 150 m for woody plants to 700 m for understory arthropods with below-ground taxa responding at large spatial extents. Our results underscore the need for multi-scale approaches to restoration. Additionally, our findings contribute to understanding the complex processes shaping multi-taxa diversity and offer insights for targeted conservation and restoration strategies.

ecology↗

Landscape heterogeneity and soil biota are central to multi-taxa diversity for landscape restoration

How to enhance biodiversity in monoculture-dominated landscapes is a key sustainability question that requires considering the spatial organization of ecological communities (beta diversity). Here, we experimentally tested if increasing landscape heterogeneity - through tree islands - is a suitable landscape restoration strategy when aiming to enhance multi-taxa diversity. We found that multi-taxa diversity resulted from islands fostering unique species (turnover: between 0.18 - 0.73) rather than species losses and gains (nestedness: between 0.03 - 0.34), suggesting that tree islands enhance diversity at the landscape scale. Through partial correlation networks, we revealed that landscape heterogeneity is associated with multi-taxa diversity (strength = 0.84). Soil biota were also central to the overall community by connecting beta diversity patterns across taxa. Our results show that increasing landscape heterogeneity enhances multi-taxa diversity in monoculture-dominant landscapes. Furthermore, we highlight that strategies aiming to enhance multi-taxa diversity should consider that spatial distributions of above- and below-ground communities are associated.

ecology↗

Forest tree species composition and abiotic site conditions drive soil fungal communities and functional groups

Soil fungi, especially the functional guilds of saprotrophic and mycorrhizal fungi, play a central role in ecosystem processes by degrading litter, mining for mineral nutrients and linking above- and belowground nutrient fluxes. Fungal community structures are influenced by abiotic habitat filters and management decisions such as tree species selection. Yet, the implications of the enrichment of temperate forests consisting of tree species in their natural range with non-native tree species on soil fungal diversity and their functional groups are unknown. Here, we studied fungal communities in 40 plots located in two regions differing in site conditions (nutrient content and soil moisture) in forests composed of European beech, Norway spruce and Douglas-fir (non-native) and mixtures of beech with either spruce or Douglas-fir. We hypothesized that fungal community structures are driven by soil resources and tree species composition, generally resulting in higher fungal diversity in mixed than in mono-specific forests. We further hypothesized that Douglas-fir has a negative effect on ectomycorrhizal fungal species richness compared to native species, whereas saprotrophic fungal richness is unaffected. We found strong separation of fungal communities between nutrient-rich and nutrient-poor sites and taxonomic divergence between beech and conifer fungal communities and an intermediate pattern in mixed forests. Mycorrhizal species richness did not vary with forest type, but the relative abundance of mycorrhizal species was lower in Douglas-fir and in mixed beech-Douglas-fir forests than in spruce or beech- spruce mixture. Conifer forests contained higher relative abundances of saprotrophic fungi than mono-specific beech forests. Among 16 abundant fungal orders in soil, two containing saprotrophic fungi (Tremellales, Hymenochaetales) were enriched in conifer forests, regardless of site conditions and tree species mixture. The other fungal orders, including those dominated by mycorrhizal fungi (Russulales, Boletales, Atheliales, Cantharellales) showed variable patterns depending on site conditions and tree species. In conclusion, Douglas-fir mono-specific or mixed forests show no loss of fungal species richness, but a shift in functional composition towards saprotrophic fungi.

ecology↗

Transcriptional Landscape of Ectomycorrhizal Fungi and Their Host Provide Insight into N Uptake from Forest Soil

Mineral nitrogen (N) is a major nutrient showing strong fluctuations in the environment due to anthropogenic activities. Acquisition and translocation of N to forest trees is achieved by highly diverse ectomycorrhizal fungi (EMF) living in symbioses with their host roots. Here, we examined colonized root tips to characterize the entire root-associated fungal community by DNA metabarcoding-Illumina sequencing of the fungal ITS2 molecular marker and used RNA sequencing to target metabolically active fungi and the plant transcriptome after N application. The study was conducted with beech (Fagus sylvatica L), a dominant tree species in central Europe, grown in native forest soil. We demonstrate strong enrichment of 15N from nitrate or ammonium in the ectomycorrhizal roots by stable isotope labeling. The relative abundance of the EMF members in the fungal community was correlated with their transcriptional abundances. The fungal metatranscriptome covered KEGG and KOG categories similar to model fungi and did not reveal significant changes related to N metabolization but species-specific transcription patterns, supporting trait stability. In contrast to the resistance of the fungal metatranscriptome, the transcriptome of the host exhibited dedicated nitrate- or ammonium-responsive changes with upregulation of transporters and enzymes required for nitrate reduction and drastic enhancement of glutamine synthetase transcript levels, indicating channeling of ammonium into the pathway for plant protein biosynthesis. Our results support that self-composed fungal communities associated with tree roots buffer nutritional signals in their own metabolism but do not shield plants from high environmental N. IMPORTANCEAlthough EMF are well known for their role in supporting tree N nutrition, the molecular mechanisms underlying N flux from the soil solution into the host through the ectomycorrhizal pathway remain widely unknown. Furthermore, ammonium and nitrate availability in the soil solution is subject to constant oscillations that create a dynamic environment for the tree roots and associated microbes during N acquisition. Therefore, it is important to understand how root-associated mycobiomes and the tree roots handle these fluctuations. We studied the response of the symbiotic partners by screening their transcriptomes after a sudden environmental flux of nitrate or ammonium. We show that the fungi and the host respond asynchronously, with the fungi displaying resistance to increased nitrate or ammonium, and the host dynamically metabolizing the supplied N sources. This study provides insights into the molecular mechanisms of the symbiotic partners operating under N enrichment in a multidimensional symbiotic system.

microbiology↗

Multi-omics analysis of xylem sap uncovers dynamic modulation of poplar defenses by ammonium and nitrate

Xylem sap is the major transport route for nutrients from roots to shoots. Here, we investigated how variations in nitrogen (N) nutrition affected the metabolome and proteome of xylem sap, growth of the xylem endophyte Brennaria salicis and report transcriptional re-wiring of leaf defenses in poplar (Populus x canescens). We supplied poplars with high, intermediate or low concentrations of ammonium or nitrate. We identified 288 unique proteins in xylem sap. About 85% of the xylem sap proteins were shared among ammonium- and nitrate-supplied plants. The number of proteins increased with increasing N supply but the major functional categories (catabolic processes, cell wall-related enzymes, defense) were unaffected. Ammonium nutrition caused higher abundances of amino acids and carbohydrates, while nitrate caused higher malate levels in xylem sap. Pipecolic acid and N-hydroxy-pipecolic acid increased whereas salicylic acid and jasmonoyl-isoleucine decreased with increasing N nutrition. Untargeted metabolome analyses revealed 2179 features in xylem sap, of which 863 were differentially affected by N treatments. We identified 122 metabolites, mainly from specialized metabolism of the groups of salicinoids, phenylpropanoids, phenolics, flavonoids, and benzoates. Their abundances increased with decreasing N. Endophyte growth was stimulated in xylem sap of high N- and suppressed in that of low N-fed plants. The drastic changes in xylem sap composition caused massive changes in the transcriptional landscape of leaves and recruited defense pathways against leaf feeding insects and biotrophic fungi, mainly under low nitrate. Our study uncovers unexpected complexity and variability of xylem composition with consequences for plant defenses. Significance statementThis study reports the largest, currently available plant xylem sap proteome and metabolome databases and highlights novel discoveries of specialized metabolites and phytohormones in the xylem sap. This is the first multi-omics study linking differences in nitrogen supply with changes xylem sap composition, endophyte growth and transcriptional defenses in leaves.

plant biology↗

Impact of nitrogen and phosphorus addition on resident soil and root mycobiomes in beech forests

In forest soils, the pools of N and P available for microbes and plants are strongly dependent on soil properties. Here, we conducted a P and N fertilization experiment to disentangle the effects of nutrient availability on soil-residing, root-associated and ectomycorrhizal fungi in beech (Fagus sylvativa) forests differing in P availability. We tested the hypothesis that in P-poor forests, P fertilization leads to enhanced fungal diversity in soil and roots, resulting in enhanced P nutrition of beech and that N fertilization aggravates P shortage, shifting the fungal communities towards nitrophilic species. In response to fertilizer treatments (1x 50 kg ha-1 P, 5x 30 kg ha-1 N within 2 years), the labile P fractions increased in soil and roots, regardless of plant-available P in soil. Root total P decreased in response to N fertilization and root total P increased at the low P site in response to P addition. The relative abundances of ectomycorrhizal fungi, but not their species richness, increased in response to P or N addition in comparison with that of saprotrophic fungi. While some fungal orders (Trechisporales, Atheliales, Cantharellales) were moderately decreased in response to fertilizer treatments, Boletales increased in response to P and Russulaes to N addition. N or P fertilization resulted in functional trade-off, shifting away from saprotrophic towards symbiotrophic potential. Our results suggest that chronic exposure of forest ecosystems to increased nutrient inputs may overcome the resistance of the resident mycobiome structures resulting in nutritional imbalance and loss of forest ecosystem services.

ecology↗

Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Below-ground microbes can induce systemic resistance (ISR) against foliar pests and pathogens on diverse plant hosts. The prevalence of ISR among plant-microbe-pest systems raises the question of host specificity in microbial induction of ISR. To test whether ISR is limited by plant host range, we tested the ISR-inducing ectomycorrhizal (ECM) fungus Laccaria bicolor on the non-mycorrhizal plant Arabidopsis. We found that root inoculation with L. bicolor triggered ISR against the insect herbivore Trichoplusia ni and induced systemic susceptibility (ISS) against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Pto). We found that L. bicolor-triggered ISR against T. ni was dependent on jasmonic acid (JA) signaling and salicylic acid (SA) biosynthesis and signaling. We found that heat killed L. bicolor and chitin are sufficient to trigger ISR against T. ni and ISS against Pto and that the chitin receptor CERK1 is necessary for L. bicolor-mediated effects on systemic immunity. Collectively our findings suggest that some ISR responses might not require intimate co-evolution of host and microbe, but rather might be the result of root perception of conserved microbial signals.

plant biology↗