Pathogenic fungi neutralize plant-derived ROS via Srpk1 deacetylation.

In response to infection, plants can induce the production of reactive oxygen species (ROS) to restrict pathogen invasion. In turn, adapted pathogens have evolved a counteracting mechanism of enzymatic ROS detoxification, but how it is activated remains elusive. Here, we show that in the tomato vascular wilt pathogen Fusarium oxysporum f. sp. lycopersici (Fol) this process is initiated by deacetylation of the FolSrpk1 kinase. Upon ROS exposure, Fol decreases FolSrpk1 acetylation on the K304 residue by altering the expression of the acetylation-controlling enzymes. Deacetylated FolSrpk1 disassociates from the cytoplasmic FolAha1 protein, thus enabling its nuclear translocation. Increased accumulation of FolSrpk1 in the nucleus allows for hyperphosphorylation of its phosphorylation target FolSr1 that subsequently enhances transcription of different types of antioxidant enzymes. Secretion of these enzymes removes plant-produced H2 O2 , and enables successful Fol invasion. Deacetylation of FolSrpk1 homologs has a similar function in Botrytis cinerea and likely other fungal pathogens. These findings reveal a conserved mechanism for initiation of ROS detoxification upon plant fungal infection.

A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis.

Establishment of root nodule symbiosis is initiated by the perception of bacterial Nod factor ligands by the plant LysM receptor kinases NFR1 and NFR5. Receptor signaling initiating the symbiotic pathway depends on the kinase activity of NFR1, while the signaling mechanism of the catalytically inactive NFR5 pseudokinase is unknown. Here, we present the crystal structure of the signaling-competent Lotus japonicus NFR5 intracellular domain, comprising the juxtamembrane region and pseudokinase domain. The juxtamembrane region is structurally well defined and forms two α-helices, αA and αA', which contain an exposed hydrophobic motif. We demonstrate that this "juxtamembrane motif" promotes NFR5-NFR5 and NFR1-NFR5 interactions and is essential for symbiotic signaling. Conservation analysis reveals that the juxtamembrane motif is present throughout NFR5-type receptors and is required for symbiosis signaling from barley RLK10, suggesting a conserved and broader function for this motif in plant-microbe symbioses.

Rapid dissemination of host metabolism-manipulating genes via integrative and conjugative elements.

Integrative and conjugative elements (ICEs) are self-transmissible mobile elements that transfer functional genetic units across broad phylogenetic distances. Accessory genes shuttled by ICEs can make significant contributions to bacterial fitness. Most ICEs characterized to date encode readily observable phenotypes contributing to symbiosis, pathogenicity, and antimicrobial resistance, yet the majority of ICEs carry genes of unknown function. Recent observations of rapid acquisition of ICEs in a pandemic lineage of Pseudomonas syringae pv. actinidae led to investigation of the structural and functional diversity of these elements. Fifty-three unique ICE types were identified across the P. syringae species complex. Together they form a distinct family of ICEs (PsICEs) that share a distant relationship to ICEs found in Pseudomonas aeruginosa. PsICEs are defined by conserved backbone genes punctuated by an array of accessory cargo genes, are highly recombinogenic, and display distinct evolutionary histories compared to their bacterial hosts. The most common cargo is a recently disseminated 16-kb mobile genetic element designated Tn6212. Deletion of Tn6212 did not alter pathogen growth in planta, but mutants displayed fitness defects when grown on tricarboxylic acid (TCA) cycle intermediates. RNA-seq analysis of a set of nested deletion mutants showed that a Tn6212-encoded LysR regulator has global effects on chromosomal gene expression. We show that Tn6212 responds to preferred carbon sources and manipulates bacterial metabolism to maximize growth.

Plant microbiota controls an alternative root branching regulatory mechanism in plants.

The establishment of beneficial interactions with microbes has helped plants to modulate root branching plasticity in response to environmental cues. However, how the plant microbiota harmonizes with plant roots to control their branching is unknown. Here, we show that the plant microbiota influences root branching in the model plant Arabidopsis thaliana. We define that the microbiota's ability to control some stages in root branching can be independent of the phytohormone auxin that directs lateral root development under axenic conditions. In addition, we revealed a microbiota-driven mechanism controlling lateral root development that requires the induction of ethylene response pathways. We show that the microbial effects on root branching can be relevant for plant responses to environmental stresses. Thus, we discovered a microbiota-driven regulatory pathway controlling root branching plasticity that could contribute to plant adaptation to different ecosystems.

A quantitative synthesis of soil microbial effects on plant species coexistence.

Soil microorganisms play a major role in shaping plant diversity, not only through their direct effects as pathogens, mutualists, and decomposers, but also by altering the outcome of plant interactions. In particular, previous research has shown that the soil community often generates frequency-dependent feedback loops among plants that can either stabilize or destabilize species interactions and thereby promote or hinder species coexistence. However, recent insights from modern coexistence theory have shown that microbial effects on plant coexistence depend not only on these stabilizing or destabilizing effects, but also on the degree to which they generate competitive fitness differences. While many previous experiments have generated the data necessary for evaluating microbially mediated fitness differences, these effects have rarely been quantified in the literature. Here, we present a meta-analysis of data from 50 studies, which we used to quantify the microbially mediated (de)stabilization and fitness differences derived from a classic plant-soil feedback model. We found that across 518 plant species pairs, soil microbes generated both stabilization (or destabilization) and fitness differences, but also that the microbially mediated fitness differences dominated. As a consequence, if plants are otherwise equivalent competitors, the balance of soil microbe­generated (de)stabilization and fitness differences drives species exclusion much more frequently than coexistence or priority effects. Our work shows that microbially mediated fitness differences are an important but overlooked effect of soil microbes on plant coexistence. This finding paves the way for a more complete understanding of the processes that maintain plant biodiversity.

Exploiting breakdown in nonhost effector-target interactions to boost host disease resistance.

Plants are resistant to most microbial species due to nonhost resistance (NHR), providing broad-spectrum and durable immunity. However, the molecular components contributing to NHR are poorly characterised. We address the question of whether failure of pathogen effectors to manipulate nonhost plants plays a critical role in NHR. RxLR (Arg-any amino acid-Leu-Arg) effectors from two oomycete pathogens, Phytophthora infestans and Hyaloperonospora arabidopsidis, enhanced pathogen infection when expressed in host plants (Nicotiana benthamiana and Arabidopsis, respectively) but the same effectors performed poorly in distantly related nonhost pathosystems. Putative target proteins in the host plant potato were identified for 64 P. infestans RxLR effectors using yeast 2-hybrid (Y2H) screens. Candidate orthologues of these target proteins in the distantly related non-host plant Arabidopsis were identified and screened using matrix Y2H for interaction with RxLR effectors from both P. infestans and H. arabidopsidis. Few P. infestans effector-target protein interactions were conserved from potato to candidate Arabidopsis target orthologues (cAtOrths). However, there was an enrichment of H. arabidopsidis RxLR effectors interacting with cAtOrths. We expressed the cAtOrth AtPUB33, which unlike its potato orthologue did not interact with P. infestans effector PiSFI3, in potato and Nicotiana benthamiana. Expression of AtPUB33 significantly reduced P. infestans colonization in both host plants. Our results provide evidence that failure of pathogen effectors to interact with and/or correctly manipulate target proteins in distantly related non-host plants contributes to NHR. Moreover, exploiting this breakdown in effector-nonhost target interaction, transferring effector target orthologues from non-host to host plants is a strategy to reduce disease.

Environmental alkalization suppresses deployment of virulence strategies in Pseudomonas syringae pv. tomato DC3000.

Plant pathogenic bacteria encounter a drastic increase in apoplastic pH during the early stages of plant immunity. The effects of alkalization on pathogen-host interactions have not been comprehensively characterized. Here, we used a global transcriptomic approach to assess the impact of environmental alkalization on Pseudomonas syringae pv. tomato DC3000 in vitro. In addition to the Type 3 Secretion System, we found expression of genes encoding other virulence factors such as iron uptake and coronatine biosynthesis to be strongly affected by environmental alkalization. We also found that the activity of AlgU, an important regulator of virulence gene expression, was induced at pH 5.5 and suppressed at pH 7.8, which are pH levels that this pathogen would likely experience before and during pattern-triggered immunity, respectively. This pH-dependent control requires the presence of periplasmic proteases, AlgW and MucP, that function as part of the environmental sensing system that activates AlgU in specific conditions. This is the first example of pH-dependency of AlgU activity, suggesting a regulatory pathway model where pH affects the proteolysis-dependent activation of AlgU. These results contribute to deeper understanding of the role apoplastic pH has on host-pathogen interactions.IMPORTANCEPlant pathogenic bacteria, like Pseudomonas syringae, encounter many environmental changes including oxidative stress and alkalization during plant immunity, but the ecological effects of the individual responses are not well understood. In this study, we found that transcription of many previously characterized virulence factors in P. syringae pv. tomato DC3000 is downregulated by the level of environmental alkalization these bacteria encounter during the early stages of plant immune activation. We also report for the first time the sigma factor AlgU is post-translationally activated by low environmental pH through its natural activation pathway, which partially accounts for the expression Type 3 Secretion System virulence genes at acidic pH. The results of this study demonstrate the importance of extracellular pH on global regulation of virulence-related gene transcription in plant pathogenic bacteria.

Immune activation during Pseudomonas infection causes local cell wall remodeling and alters AGP accumulation.

The plant cell boundary generally comprises constituents of the primary and secondary cell wall (CW) that are deposited sequentially during development. Although it is known that the CW acts as a barrier against phytopathogens and undergoes modifications to limit their invasion, the extent, sequence, and requirements of the pathogen-induced modifications of the CW components are still largely unknown, especially at the level of the polysaccharide fraction. To address this significant knowledge gap, we adopted the compatible Pseudomonas syringae-Arabidopsis thaliana system. We found that, despite systemic signaling actuation, Pseudomonas infection leads only to local CW modifications. Furthermore, by utilizing a combination of CW and immune signaling-deficient mutants infected with virulent or non-virulent bacteria, we demonstrated that the pathogen-induced changes in CW polysaccharides depend on the combination of pathogen virulence and the host's ability to mount an immune response. This results in a pathogen-driven accumulation of CW hexoses, such as galactose, and an immune signaling-dependent increase in CW pentoses, mainly arabinose, and xylose. Our analyses of CW changes during disease progression also revealed a distinct spatiotemporal pattern of arabinogalactan protein (AGP) deposition and significant modifications of rhamnogalacturonan sidechains. Furthermore, genetic analyses demonstrated a critical role of AGPs, specifically of the Arabinoxylan Pectin Arabinogalactan Protein1, in limiting pathogen growth. Collectively, our results provide evidence for the actuation of significant remodeling of CW polysaccharides in a compatible host-pathogen interaction, and, by identifying AGPs as critical elements of the CW in plant defense, they pinpoint opportunities to improve plants against diverse pathogens.

Drought stress-mediated differences in phyllosphere microbiome and associated pathogen resistance between male and female poplars.

Phyllosphere-associated microbes play a crucial role in plant-pathogen interactions while their composition and diversity are strongly influenced by drought stress. As dioecious plant species exhibited secondary dimorphism between the two sexes in response to drought stress, whether such difference will lead to sex-specific differences in phyllosphere microbiome and associated pathogen resistance between male and female conspecifics is still unknown. In this study, we subjected female and male full siblings of a dioecious poplar species to a short period of drought treatment followed by artificial infection of a leaf pathogenic fungus. Our results showed that male plants grew better than females with or without drought stress. Female control plants had more leaf lesion area than males after pathogen infection, whereas drought stress reversed such a difference. Further correlation and in vitro toxicity tests suggested that drought-mediated sexual differences in pathogen resistance between the two plant sexes could be attributed to the shifts in structure and function of phyllosphere-associated microbiome rather than the amount of leaf main defensive chemicals contained in plant leaves. Supportively, the microbiome analysis through high-throughput sequencing indicated that female phyllosphere enriched a higher abundance of ecologically beneficial microbes that serve as biological plant protectants, while males harbored abundant phytopathogens under drought-stressed conditions. The results could provide potential implications for the selection of suitable poplar sex to plants in drought or semi-drought habitats.

Time-dependent interaction modification generated from plant-soil feedback.

Pairwise interactions between species can be modified by other community members, leading to emergent dynamics contingent on community composition. Despite the prevalence of such higher-order interactions, little is known about how they are linked to the timing and order of species' arrival. We generate population dynamics from a mechanistic plant-soil feedback model, then apply a general theoretical framework to show that the modification of a pairwise interaction by a third plant depends on its germination phenology. These time-dependent interaction modifications emerge from concurrent changes in plant and microbe populations and are strengthened by higher overlap between plants' associated microbiomes. The interaction between this overlap and the specificity of microbiomes further determines plant coexistence. Our framework is widely applicable to mechanisms in other systems from which similar time-dependent interaction modifications can emerge, highlighting the need to integrate temporal shifts of species interactions to predict the emergent dynamics of natural communities.

Roots selectively decompose litter to mine nitrogen and build new soil carbon.

Plant-microbe interactions in the rhizosphere shape carbon and nitrogen cycling in soil organic matter (SOM). However, there is conflicting evidence on whether these interactions lead to a net loss or increase of SOM. In part, this conflict is driven by uncertainty in how living roots and microbes alter SOM formation or loss in the field. To address these uncertainties, we traced the fate of isotopically labelled litter into SOM using root and fungal ingrowth cores incubated in a Miscanthus x giganteus field. Roots stimulated litter decomposition, but balanced this loss by transferring carbon into aggregate associated SOM. Further, roots selectively mobilized nitrogen from litter without additional carbon release. Overall, our findings suggest that roots mine litter nitrogen and protect soil carbon.

Microbial symbionts buffer hosts from the demographic costs of environmental stochasticity.

Species' persistence in increasingly variable climates will depend on resilience against the fitness costs of environmental stochasticity. Most organisms host microbiota that shield against stressors. Here, we test the hypothesis that, by limiting exposure to temporally variable stressors, microbial symbionts reduce hosts' demographic variance. We parameterized stochastic population models using data from a 14-year symbiont-removal experiment including seven grass species that host Epichloë fungal endophytes. Results provide novel evidence that symbiotic benefits arise not only through improved mean fitness, but also through dampened inter-annual variance. Hosts with "fast" life-history traits benefited most from symbiont-mediated demographic buffering. Under current climate conditions, contributions of demographic buffering were modest compared to benefits to mean fitness. However, simulations of increased stochasticity amplified benefits of demographic buffering and made it the more important pathway of host-symbiont mutualism. Microbial-mediated variance buffering is likely an important, yet cryptic, mechanism of resilience in an increasingly variable world.

Nutrient requirements shape the preferential habitat of Allorhizobium vitis VAR03-1, a commensal bacterium, in the rhizosphere of Arabidopsis thaliana.

A diverse range of commensal bacteria inhabit the rhizosphere, influencing host plant growth and responses to biotic and abiotic stresses. While root-released nutrients can define soil microbial habitats, the bacterial factors involved in plant-microbe interactions are not well characterized. In this study, we investigated the colonization patterns of two plant disease biocontrol agents, Allorhizobium vitis VAR03-1 and Pseudomonas protegens Cab57, in the rhizosphere of Arabidopsis thaliana using Murashige and Skoog (MS) agar medium. VAR03-1 formed colonies even at a distance from the roots, preferentially in the upper part, while Cab57 colonized only the root surface. The addition of sucrose to the agar medium resulted in excessive proliferation of VAR03-1, similar to its pattern without sucrose, whereas Cab57 formed colonies only near the root surface. Overgrowth of both bacterial strains upon nutrient supplementation inhibited host growth, independent of plant immune responses. This inhibition was reduced in the VAR03-1 ΔrecA mutant, which exhibited increased biofilm formation, suggesting that some activities associated with the free-living lifestyle rather than the sessile lifestyle may be detrimental to host growth. VAR03-1 grew in liquid MS medium with sucrose alone, while Cab57 required both sucrose and organic acids. Supplementation of sugars and organic acids allowed both bacterial strains to grow near and away from Arabidopsis roots in MS agar. These results suggest that nutrient requirements for bacterial growth may determine their growth habitats in the rhizosphere, with nutrients released in root exudates potentially acting as a limiting factor in harnessing microbiota.

Profiling sorghum-microbe interactions with a specialized photoaffinity probe identifies key sorgoleone binders in Acinetobacter pittii.

Interactions between plants and soil microbial communities that benefit plant growth and enhance nutrient acquisition are driven by the selective release of metabolites from plant roots, or root exudation. To investigate these plant-microbe interactions, we developed a photoaffinity probe based on sorgoleone (sorgoleone diazirine alkyne for photoaffinity labeling, SoDA-PAL), a hydrophobic secondary metabolite and allelochemical produced in Sorghum bicolor root exudates. We applied SoDA-PAL to the identification of sorgoleone-binding proteins in Acinetobacter pittii SO1, a potential plant growth-promoting microbe isolated from sorghum rhizosphere soil. Competitive photoaffinity labeling of A. pittii whole cell lysates with SoDA-PAL identified 137 statistically enriched proteins, including putative transporters, transcriptional regulators, and a subset of proteins with predicted enzymatic functions. We performed computational protein modeling and docking with sorgoleone to prioritize candidates for experimental validation and then confirmed binding of sorgoleone to four of these proteins in vitro: the α/ß fold hydrolase SrgB (OH685_09420), a fumarylacetoacetase (OH685_02300), a lysophospholipase (OH685_14215), and an unannotated hypothetical protein (OH685_18625). Our application of this specialized sorgoleone-based probe coupled with structural bioinformatics streamlines the identification of microbial proteins involved in metabolite recognition, metabolism, and toxicity, widening our understanding of the range of cellular pathways that can be affected by a plant secondary metabolite.IMPORTANCEHere, we demonstrate that a photoaffinity-based chemical probe modeled after sorgoleone, an important secondary metabolite released by sorghum roots, can be used to identify microbial proteins that directly interact with sorgoleone. We applied this probe to the sorghum-associated bacterium Acinetobacter pittii and showed that probe labeling is dose-dependent and sensitive to competition with purified sorgoleone. Coupling the probe with proteomics and computational analysis facilitated the identification of putative sorgoleone binders, including a protein implicated in a conserved pathway essential for sorgoleone catabolism. We anticipate that discoveries seeded by this workflow will expand our understanding of the molecular mechanisms by which specific metabolites in root exudates shape the sorghum rhizosphere microbiome.

Microbial terroir: associations between soil microbiomes and the flavor chemistry of mustard (Brassica juncea).

Here, we characterized the independent role of soil microbiomes (bacterial and fungal communities) in determining the flavor chemistry of harvested mustard seed (Brassica juncea). Given the known impacts of soil microbial communities on various plant characteristics, we hypothesized that differences in rhizosphere microbiomes would result in differences in seed flavor chemistry (glucosinolate content). In a glasshouse study, we introduced distinct soil microbial communities to mustard plants growing in an otherwise consistent environment. At the end of the plant life cycle, we characterized the rhizosphere and root microbiomes and harvested produced mustard seeds for chemical characterization. Specifically, we measured the concentrations of glucosinolates, secondary metabolites known to create spicy and bitter flavors. We examined associations between rhizosphere microbial taxa or genes and seed flavor chemistry. We identified links between the rhizosphere microbial community composition and the concentration of the main glucosinolate, allyl, in seeds. We further identified specific rhizosphere taxa predictive of seed allyl concentration and identified bacterial functional genes, namely genes for sulfur metabolism, which could partly explain the observed associations. Together, this work offers insight into the potential influence of the belowground microbiome on the flavor of harvested crops.

Microbial responses to stress cryptically alter natural selection on plants.

Microbial communities can rapidly respond to stress, meaning plants may encounter altered soil microbial communities in stressful environments. These altered microbial communities may then affect natural selection on plants. Because stress can cause lasting changes to microbial communities, microbes may also cause legacy effects on plant selection that persist even after the stress ceases. To explore how microbial responses to stress and persistent microbial legacy effects of stress affect natural selection, we grew Chamaecrista fasciculata plants in stressful (salt, herbicide, or herbivory) or nonstressful conditions with microbes that had experienced each of these environments in the previous generation. Microbial community responses to stress generally counteracted the effects of stress itself on plant selection, thereby weakening the strength of stress as a selective agent. Microbial legacy effects of stress altered plant selection in nonstressful environments, suggesting that stress-induced changes to microbes may continue to affect selection after stress is lifted. These results suggest that soil microbes may play a cryptic role in plant adaptation to stress, potentially reducing the strength of stress as a selective agent and altering the evolutionary trajectory of plant populations.

Populus MYC2 orchestrates root transcriptional reprogramming of defence pathway to impair Laccaria bicolor ectomycorrhizal development.

The jasmonic acid (JA) signalling pathway plays an important role in the establishment of the ectomycorrhizal symbiosis. The Laccaria bicolor effector MiSSP7 stabilizes JA corepressor JAZ6, thereby inhibiting the activity of Populus MYC2 transcription factors. Although the role of MYC2 in orchestrating plant defences against pathogens is well established, its exact contribution to ECM symbiosis remains unclear. This information is crucial for understanding the balance between plant immunity and symbiotic relationships. Transgenic poplars overexpressing or silencing for the two paralogues of MYC2 transcription factor (MYC2s) were produced, and their ability to establish ectomycorrhiza was assessed. Transcriptomics and DNA affinity purification sequencing were performed. MYC2s overexpression led to a decrease in fungal colonization, whereas its silencing increased it. The enrichment of terpene synthase genes in the MYC2-regulated gene set suggests a complex interplay between the host monoterpenes and fungal growth. Several root monoterpenes have been identified as inhibitors of fungal growth and ECM symbiosis. Our results highlight the significance of poplar MYC2s and terpenes in mutualistic symbiosis by controlling root fungal colonization. We identified poplar genes which direct or indirect control by MYC2 is required for ECM establishment. These findings deepen our understanding of the molecular mechanisms underlying ECM symbiosis.

The mycorrhizal symbiosis: research frontiers in genomics, ecology, and agricultural application.

Mycorrhizal symbioses between plants and fungi are vital for the soil structure, nutrient cycling, plant diversity, and ecosystem sustainability. More than 250 000 plant species are associated with mycorrhizal fungi. Recent advances in genomics and related approaches have revolutionized our understanding of the biology and ecology of mycorrhizal associations. The genomes of 250+ mycorrhizal fungi have been released and hundreds of genes that play pivotal roles in regulating symbiosis development and metabolism have been characterized. rDNA metabarcoding and metatranscriptomics provide novel insights into the ecological cues driving mycorrhizal communities and functions expressed by these associations, linking genes to ecological traits such as nutrient acquisition and soil organic matter decomposition. Here, we review genomic studies that have revealed genes involved in nutrient uptake and symbiosis development, and discuss adaptations that are fundamental to the evolution of mycorrhizal lifestyles. We also evaluated the ecosystem services provided by mycorrhizal networks and discuss how mycorrhizal symbioses hold promise for sustainable agriculture and forestry by enhancing nutrient acquisition and stress tolerance. Overall, unraveling the intricate dynamics of mycorrhizal symbioses is paramount for promoting ecological sustainability and addressing current pressing environmental concerns. This review ends with major frontiers for further research.

Interactions between root hairs and the soil microbial community affect the growth of maize seedlings.

Root hairs are considered important for rhizosphere formation, which affects root system functioning. Through interactions with soil microorganisms mediated by root exudation, root hairs may affect the phenotypes and growth of young plants. We tested this hypothesis by integrating results from two experiments: (1) a factorial greenhouse seedling experiment with Zea mays B73-wt and its root-hairless mutant, B73-rth3, grown in live and autoclaved soil, quantifying 15 phenotypic traits, seven growth rates, and soil microbiomes and (2) a semi-hydroponic system quantifying root exudation of maize genotypes. Possibly as compensation for lacking root hairs, B73-rth3 seedlings allocated more biomass to roots and grew slower than B73-wt seedlings in live soil, whereas B73-wt seedlings grew slowest in autoclaved soil, suggesting root hairs can be costly and their benefits were realized with more complete soil microbial assemblages. There were substantial differences in root exudation between genotypes and in rhizosphere versus non-rhizosphere microbiomes. The microbial taxa enriched in the presence of root hairs generally enhanced growth compared to taxa enriched in their absence. Our findings suggest the root hairs' adaptive value extends to plant-microbe interactions mediated by root exudates, affecting plant phenotypes, and ultimately, growth.

Cytoskeleton remodeling: a central player in plant-fungus interactions.

The eukaryotic cytoskeleton is a complex scaffold consisting of actin filaments, intermediate filaments, and microtubules. Although fungi and plants lack intermediate filaments, their dynamic structural network of actin filaments and microtubules regulates cell shape, division, polarity, and vesicular trafficking. However, the specialized functions of the cytoskeleton during plant-fungus interactions remain elusive. Recent reports demonstrate that the plant cytoskeleton responds to signal cues and pathogen invasion through remodeling, thereby coordinating immune receptor trafficking, membrane microdomain formation, aggregation of organelles, and transport of defense compounds. Emerging evidence also suggests that cytoskeleton remodeling further regulates host immunity by triggering salicylic acid signaling, reactive oxygen species generation, and pathogenesis-related gene expression. During host invasion, fungi undergo systematic cytoskeleton remodeling, which is crucial for successful host penetration and colonization. Furthermore, phytohormones act as an essential regulator of plant cytoskeleton dynamics and are frequently targeted by fungal effectors to disrupt the host's growth-defense balance. This review discusses recent advances in the understanding of cytoskeleton dynamics during plant-fungus interactions and provides novel insights into the relationship between phytohormones and cytoskeleton remodeling upon pathogen attack. We also highlight the importance of fungal cytoskeleton rearrangements during host colonization and suggest directions for future investigations in this field.