Biology subjects

Hiruma, K.

Publications and source records attributed to Hiruma, K..

9 recordsLinked to original sources

bioRxiv2026

Iron-dependent reprogramming of damage-associated peptide receptor signaling coordinates immunity and phosphate stress adaptation

Plant adaptation to inorganic phosphate (Pi) limitation entails extensive developmental and metabolic reprogramming, collectively termed the phosphate starvation response (PSR). How plants balance nutrient acquisition with immune competence remains unresolved. Here, we show that PSR selectively remodels pattern-recognition receptor (PRR) signaling in Arabidopsis thaliana. Membrane proteomics reveals increased abundance of the Pep receptor PEPR1 under Pi deficiency, whereas most receptor kinases, including the microbial PRRs FLS2 and CERK1, are reduced. Immunoblotting further shows increased PEPR2 abundance. Consistently, Pep-triggered responses are strongly potentiated under Pi depletion, while flagellin- and chitin-induced responses are not, indicating selective PEPR sensitization rather than global immune suppression. This sensitization requires the PSR-associated ferroxidases LPR1/LPR2, NADPH oxidases RBOHD/RBOHF, and transcription factor WRKY33, linking iron-dependent redox remodeling to immune amplification. Beyond inducible defense, PEPRs promote basal PSR transcriptional reprogramming and growth under Pi limitation. Loss of PEPR1/PEPR2 compromises bacterial resistance and alters root-associated microbiota assembly under nutrient deficiency. Together, Pi depletion selectively sensitizes specific PRR pathways. PEPRs exhibit context-dependent dual functionality, promoting either immunity or nutrient stress adaptation, potentially in response to distinct PROPEP-derived ligands, thereby supporting nutrient acquisition without compromising immune vigilance. These findings provide a framework for how nutritional status selectively remodels PRR signaling to coordinate immunity with nutrient stress adaptation.

plant biology↗

bioRxiv2026

A fungal phosphate starvation regulator gates virulence to prioritize nutrient adaptation in response to host phosphate status

Plant-associated microbes must constantly balance environmental adaptation with virulence to survive in fluctuating ecosystems, yet the molecular mechanisms coupling these processes remain poorly understood. Here, we identify NUTRIENT-DEPENDENT FACILITATOR OF COLONIZATION1 (NFC1), a virulence factor in a conditionally pathogenic Colletotrichum tofieldiae strain, whose expression is tightly regulated by both temperature and phosphate availability. Leveraging plant phosphate starvation response (PSR) mutants and direct phosphate supplementation to host plants, we demonstrate that NFC1 expression is driven by the internal phosphate status of the host rather than environmental availability alone. Notably, the fungal PSR regulator CtPHO4 represses NFC1 and virulence during phosphate starvation, while simultaneously activating canonical fungal PSR-related genes. Conversely, under phosphate sufficiency, NFC1 is strongly induced and promotes infection, potentially by modulating the host circadian clock system. This study uncovers a molecular link between metabolic adaptation and virulence programming, providing a conceptual framework for predicting disease dynamics under changing environments.

microbiology↗

bioRxiv2025

Genetic factors driving multi-host infection in a core member of the root mycobiota

Core members of the fungal root microbiota include pathogens capable of colonizing multiple hosts, yet the underlying genetic determinants remain unknown. We report that Plectosphaerella cucumerina is a core member of the Arabidopsis thaliana root microbiota displaying high pathogenic potential and multi-host colonization capabilities. Establishment of a Plectosphaerella reference culture collection, followed by whole-genome sequencing of 72 strains reveals subtle phenotypic and genotypic variation that associate with fungal phylogeny, but not host plant identity. Transcriptome profiling of a model P. cucumerina isolate in roots of multiple hosts identifies core and host-specific fungal processes linked to carbon catabolism and root cell wall deconstruction of the hosts. A fungal gene encoding a candidate {beta}-1,3-glucanase (GH64) was identified as a key genetic factor driving infection and disease in plants that diverged 110 million years ago. The gene is enriched in plant-colonizing fungi and consistently functions as a disease determinant in the root pathogen Colletotrichum incanum. We conclude that diverse and tunable fungal repertoires of carbohydrate-active enzymes act as disease determinants and drive multi-host compatibility belowground.

microbiology↗

bioRxiv2025

Nitrogen acquisition and selective bacterial attraction through fungal hyphae promote plant growth and health under nitrogen limitation

Plants alleviate nitrogen (N) deficiency through interactions with beneficial microbes, yet mechanisms underlying plant-fungus-bacterium mediated plant growth promotion (PGP) remain poorly understood. Here, we show that the root endophytic fungus Colletotrichum tofieldiae (Ct) enhances the growth of diverse plant species beyond the Brassicaceae under N deficient field and lab conditions. Optimal Ct-mediated PGP requires Arabidopsis thaliana nitrate transporters (AtNRT2.1/2.2/2.4/2.5), as well as the fungal N utilization regulator CtAREA. Isotopic tracing with 15NO3- reveals that Ct transfers N to hosts via CtAREA-dependent yet AtNRT2s-independent route, implicating distinct, parallel pathways in PGP. Moreover, Ct attracts the beneficial bacterium Paraburkholderia monticola through its hyphae, which metabolizes organic N sources and additively enhances plant growth with Ct. Notably, P. monticola suppressed the pathogenic transition of Ct in plant mutants defective in Brassicaceae-specific tryptophan-derived metabolism, potentially accounting for Cts broad beneficial activities. This plant-fungus-bacteria interaction may secure consistent PGP across varied agricultural settings.

plant biology↗

bioRxiv2024

A fungal transcription factor BOT6 facilitates the transition of a beneficial root fungus into an adapted anthracnose pathogen

The infection strategies employed by plant endophytes are attributed to their ability to overcome durable nonhost resistance and adapt to the host environment. However, the regulatory genetic background underlying how they adapt to the host and determine their lifestyles remains enigmatic. Here, we show that the CtBOT6, a cluster-residing transcription factor in the root-associated fungus Colletotrichum tofieldiae (Ct), plays a pivotal role in regulating virulence-related gene expression and in producing metabolites both not only within and but unexpectedly outside of the cluster. Genetic manipulation of CtBOT6 toward activation alone is sufficient to transition a root beneficial Ct along the mutualist-pathogen continuum even toward a leaf pathogen capable of overcoming nonhost resistance, partly dependent on the host abscisic acid and ethylene pathways. Our findings indicate that the status of CtBOT6 serves as a critical determinant for the endophytic fungus to adapt to the plant different environments and manifest diverse infection strategies.

plant biology↗

bioRxiv2023

Defense-related callose synthase PMR4 promotes root hair callose deposition and adaptation to phosphate deficiency in Arabidopsis thaliana

Plants acquire phosphorus (P) primarily as inorganic phosphate (Pi) from the soil. Under Pi deficiency, plants induce an array of physiological and morphological responses, termed phosphate starvation response (PSR), thereby increasing Pi acquisition and use efficiency. However, the mechanisms by which plants adapt to Pi deficiency remain to be elucidated. Here, we report that deposition of a {beta}-1,3-glucan polymer called callose is induced in Arabidopsis thaliana root hairs under Pi deficiency, in a manner independent of PSR-regulating PHR1/PHL1 transcription factors and LPR1/LPR2 ferroxidases. Genetic studies revealed PMR4 (GSL5) callose synthase being required for the callose deposition in Pi-depleted root hairs. Loss of PMR4 also reduces Pi acquisition in shoots and plant growth under low Pi conditions. The defects are not recovered by simultaneous disruption of SID2, mediating defense-associated salicylic acid (SA) biosynthesis, excluding SA defense activation from the cause of the observed pmr4 phenotypes. Grafting experiments and characterization of plants expressing PMR4 specifically in root hair cells suggest that a PMR4 pool in the cell type contributes to shoot growth under Pi deficiency. Our findings thus suggest an important role for PMR4 in plant adaptation to Pi deficiency. Significance statementWe reveal that PMR4 callose synthase mediates callose deposition in root hairs under phosphate (Pi) deficiency, without requiring Pi starvation response regulators PHR1/PHL1 or LPR1/LPR2. The loss of the callose deposition is accompanied by decreases in Pi acquisition and plant growth in pmr4. Root hair cell-specific PMR4 expression restores callose deposition in root hairs and shoot growth under Pi deficiency, indicating a critical role for root hair callose in plant adaptation to Pi deficiency.

plant biology↗

bioRxiv2022

A fungal secondary metabolism gene cluster enables mutualist-pathogen transition in root endophyte Colletotrichum tofieldiae

Plant-associated fungi show diverse lifestyles from pathogenic to mutualistic to the host; however, the principles and mechanisms through which they shift the lifestyles require elucidation. The root fungus Colletotrichum tofieldiae (Ct) promotes Arabidopsis thaliana growth under phosphate limiting conditions. We reveal a Ct strain, designated Ct3, that severely inhibits plant growth. Ct3 pathogenesis occurs through activation of host abscisic acid (ABA) pathways via a fungal secondary metabolism gene cluster related to sesquiterpene ABA and botrydial (BOT) biosynthesis. ABA-BOT cluster activation during root infection suppresses host nutrient uptake-related genes and changes the mineral contents, suggesting its role in manipulating host nutrition states. Conversely, disruption or environmental suppression of the cluster renders Ct3 beneficial for plant growth, in a manner dependent on host phosphate starvation response regulators. Our findings indicate that a fungal metabolism cluster provides a means by which infectious fungi modulate lifestyles along the parasitic-mutualistic continuum in fluctuating environments.

microbiology↗

bioRxiv2021

Synergistic and offset effects of fungal species combinations on plant performance

In natural and agricultural ecosystems, survival and growth of plants depend substantially on microbes in the endosphere and rhizosphere. Although numerous studies have reported the presence of plant-growth promoting bacteria and fungi in below-ground biomes, it remains a major challenge to understand how sets of microbial species positively or negatively affect plants performance. By conducting a series of single- and dual-inoculation experiments of 13 endophytic and soil fungi targeting a Brassicaceae plant species, we here evaluated how microbial effects on plants depend on presence/absence of co-occurring microbes. The comparison of single- and dual-inoculation experiments showed that combinations of the fungal isolates with the highest plant-growth promoting effects in single inoculations did not yield highly positive impacts on plant performance traits (e.g., shoot dry weight). In contrast, pairs of fungi including small/moderate contributions to plants in single-inoculation contexts showed the greatest effects on plants among the 78 fungal pairs examined. These results on the offset and synergistic effects of pairs of microbes suggest that inoculation experiments of single microbial species/isolates can result in the overestimation or underestimation of microbial functions in multi-species contexts. Because keeping single-microbe systems in outdoor conditions is impractical, designing sets of microbes that can maximize performance of crop plants is an important step for the use of microbial functions in sustainable agriculture.

microbiology↗

bioRxiv2020

Host-dependent fungus-fungus competition suppresses fungal pathogenesis in Arabidopsis thaliana

Like animals, plants accommodate a rich diversity of microbes, typically without discernible disease symptoms. How their pathogenesis is prevented in the host remains obscure. Here, we show that the root-infecting fungus Colletotrichum fructicola of the C. gloeosporioides clade (CgE), isolated from field-grown healthy Brassicaceae plants, inhibits growth of pathogenic fungi in Arabidopsis thaliana, in a phosphate status-dependent manner. Loss of host ethylene signaling or phytoalexins, camalexin or indole glucosinolates, however, allows CgE to display pathogenesis, suggesting host contributions to endophytic CgE colonization and benefit. Compared to a closely-related C. gloeosporioides pathogen (CgP), CgE is characterized by genome expansion and >700 fungal genes (4.34%) specifically induced in the host roots when co-inoculated with CgP, including genes related to fungal secondary metabolism. This may underlie antimicrobial tolerance of CgE and its dominance over pathogenic fungi within the host, pointing to a role for fungus-fungus competition in asymptomatic fungal colonization in plants.

plant biology↗