Salinity is a major constraint to crop productivity. Beneficial plant–fungus interactions represent a promising strategy to enhance stress resilience. Here, we investigated fungal endophytes isolated from the roots of Oryza sativa cultivated in saline-prone marshlands of the Guadalquivir River, Spain. From a collection of 38 isolates, five salt-tolerant strains exhibiting plant growth-promoting activity were identified, including a previously uncharacterized Reticulascus sp. strain S5. Co-cultivation assays with the non-native host plant Arabidopsis thaliana demonstrated that S5 increased the root and shoot biomass under salt stress. To elucidate the underlying molecular mechanisms, a comprehensive RNA-Seq analysis of the roots and shoots under control and saline conditions was performed. Fungal colonization induced pronounced transcriptomic changes, particularly in the shoots, including rewiring of the auxin- and abscisic acid-related pathways and the induction of genes associated with cell wall remodeling. Concurrently, defense-related processes, including glucosinolate biosynthesis and ethylene signaling, were broadly repressed, suggesting attenuated stress perception in colonized plants. In the roots, S5 inoculation suppressed the expression of genes involved in root hair development and cell wall organization, indicating a fungus-driven reconfiguration of root development. Moreover, comparative analysis with Fusarium sp. K-23, a fungus that has previously been demonstrated to promote plant growth under salinity stress, revealed distinct root-associated mechanisms but convergence on a shared regulatory module in shoots involving ABA-responsive transcription factors and osmotic stress regulators. Collectively, our findings demonstrate that Reticulascus sp. S5 enhances plant salt stress tolerance through the coordinated transcriptional reprogramming of growth, hormone signaling, and stress responses, highlighting a possible potential of habitat-adapted endophytes for sustainable crop improvement.
Global agricultural productivity is currently challenged by a range of emerging environmental stressors associated with the ongoing climate change scenario. The future of food security is critically reliant on the capacity to mitigate and manage these stresses on crops and trees. Over recent decades, substantial progress has been made in elucidating plant responses to various stresses, including heat, drought, and soil salinity, and in understanding how plant acclimatization to these responses is regulated by a limited number of signalling molecules, known as phytohormones. In response to abiotic stresses, abscisic acid (ABA) plays a pivotal role as it regulates, among other physiological processes, stomatal aperture and, consequently, the gas exchange and water uptake of plants. Therefore, methods for the comprehensive monitoring of changes in ABA levels are of particular significance. In this chapter, we provide a detailed description of a highly sensitive and accurate method for the quantitative analysis in plants using gas chromatography-coupled tandem mass spectrometry (GC-MS/MS). Additionally, we describe an indirect method for estimating ABA contents in Arabidopsis thaliana using ABA signalling reporter lines.
Serendipita indica, a widely studied beneficial root-colonizing fungal endophyte, promotes plant growth under saline conditions by reducing Na+ accumulation in host plants, including Arabidopsis thaliana. This reduction in Na + levels likely contributes to salt detoxification, but the underlying mechanisms remain unclear. Previous studies have demonstrated that SOS1, a key Na+ transporter and major determinant of salt tolerance in plants, is not involved in this reduction. To explore whether other plant transporters might participate in Na+ reduction, we first characterized the full Arabidopsis transportome, with putative substrates and subcellular localizations, and performed a comprehensive transcriptomic analysis of the full set of transporter proteins. In this study, we investigated and excluded the possible contribution of HKT1, another relevant Na+ transporter implicated in salt adaptation in Arabidopsis. By examining differentially expressed transporters under salt stress, we identified a subset of candidate genes potentially involved in Na+ transport. Among these, we evaluated the role of CNGC10 and CNGC13 using mutant lines under both S. indica- and non-colonized conditions. Interestingly, both transporters appeared to be involved in the endophyte-induced decrease in Na+ accumulation although, other, yet-unidentified transporters may also contribute to this phenomenon.
Salinity is a major constraint to crop productivity. Beneficial plant–fungus interactions represent a promising strategy to enhance stress resilience. Here, we investigated fungal endophytes isolated from Oryza sativa cultivated in saline-prone marshlands of the Guadalquivir River, Spain. From a collection of 38 isolates, five salt-tolerant strains exhibiting plant growth-promoting activity were identified, including a previously uncharacterized Reticulascus sp. strain S5. Co-cultivation assays with Arabidopsis thaliana demonstrated that S5 increased root and shoot biomass under salt stress. To elucidate the underlying mechanisms, a comprehensive RNA-seq analysis of roots and shoots under control and saline conditions was performed. Fungal colonization induced pronounced transcriptomic changes, particularly in shoots, including the rewiring of auxin- and abscisic acid-related pathways and the induction of genes associated with cell wall remodelling. Concurrently, defence-related processes, including glucosinolate biosynthesis and ethylene signalling, were broadly repressed, suggesting attenuated stress perception in colonized plants. In roots, S5 infection suppressed genes involved in root hair development and cell wall organization, indicating a fungus-driven reconfiguration of root development. Comparative analysis with the growth-promoting Fusarium sp. K-23 revealed distinct root-associated mechanisms but convergence on a shared regulatory module in shoots involving ABA-responsive transcription factors and osmotic stress regulators. Collectively, our findings demonstrate that Reticulascus sp. S5 enhances plant salt stress tolerance through coordinated transcriptional reprogramming of growth, hormone signalling, and stress responses, highlighting the potential of habitat-adapted endophytes for sustainable crop improvement.
Arsenic (As) contamination severely compromises plant growth and agricultural productivity, particularly in environments affected by mining or industrial activities. Microbial symbionts adapted to metalliferous soils represent a promising yet underexploited resource for enhancing plant tolerance to As toxicity. In this study, we isolated root-associated fungal endophytes from three plant species thriving on As-rich tailings of the Mónica mine (Bustaviejo, Spain) and identified Penicillium sp. strain D7 as a highly As-tolerant symbiont with pronounced plant growth–promoting effects. When co-cultivated with Arabidopsis thaliana, D7 significantly enhanced shoot biomass under As(III) stress and mitigated characteristic toxicity symptoms. Transcriptome profiling revealed that D7 reprograms plant hormone signalling of the host in a tissue-specific manner: the fungus suppresses abscisic acid (ABA) biosynthesis and ABA-responsive stress pathways in roots, while simultaneously inducing auxin biosynthesis and signalling in shoots, consistent with improved growth performance. Furthermore, D7 elicited the coordinated induction of key components of the plant’s intrinsic As detoxification machinery, including ARQ1, PCS1, and the vacuolar transporters ABCC1 and ABCC2. Functional analyses using the abcc1 abcc2 double mutant demonstrated that vacuolar sequestration of As(III) in roots is essential for D7-mediated stress tolerance, indicating that fungal colonisation enhances the host’s capacity for intracellular detoxification rather than reducing As uptake. Together, these results demonstrate that Penicillium sp. D7 reinforces plant resilience to As(III) by simultaneously attenuating stress perception, promoting growth-related hormonal programs, and stimulating vacuolar sequestration of As. This study highlights D7 as a promising microbial tool for supporting vegetation establishment and phytostabilisation efforts in As-contaminated environments.
Global climate change is linked to an increased occurrence of heat waves and droughts, which alter plant growth and development, and thus threaten food security. By associating with generalist root fungal endophytes that are adapted to harsh environments, crop plants can improve productivity under adverse conditions. Here, we examined the effects of two root endophytes isolated from Antarctica plants (Penicillium chrysogenum and P. brevicompactum) on mechanisms of tolerance to heat and drought in strawberry (Fragaria x ananassa). We found that inoculated plants exhibited better water retention, increased photosynthesis, reduced proline content and lipid peroxidation, and modulated antioxidative enzymatic activity. Transcriptomic and cis-element/transcription factor analyses revealed that differentially expressed genes (DEGs) were associated with abscisic acid (ABA) signaling, including dehydrins, as well as with cellular water homeostasis, such as aquaporins. These DEGs reveal mechanisms that enhance the physiological performance of endophyte-inoculated plants under drought and high-temperatures. This study highlights the novel role of Antarctic fungi in modulating ABA signaling and aquaporin expression, offering potential agricultural applications to enhance plant stress tolerance, which is crucial for improving food security.
Strawberries (Fragaria x ananassa) are valued worldwide for their aroma among other quality traits. Pyruvate decarboxylase (PDC) is a key enzyme in aroma, initiating the conversion of pyruvate into acetaldehyde. This process produces precursors for esters and aromatic compounds that enhance strawberry aroma. Additionally, alcohol acyltransferases (AATs) are essential for catalyzing acyl group transfers, further enriching fruit aroma diversity. However, strawberries are highly vulnerable to drought, which affects product quality. Plant root-associated fungi offer a novel approach to mitigate water deficiency stress. This study investigates the effect of Antarctic fungal inoculation on the gene expression of FaPDC, and the FaAAT gene family, related to the accumulation of volatile organic compounds (VOCs) in strawberries. Fruits of fungi-inoculated plants under drought stress showed significant changes in gene expression, leading to increased total volatile ester production, primarily in acetate esters, which are important for strawberry aroma. These findings underscore the role of Antarctic fungi in modulating the metabolic pathway of volatile esters by inducing the expression of FaPDC and FaAAT genes. Beyond elucidating the molecular mechanisms underlying aromatic compound biosynthesis in fruits, this study highlights the potential of Antarctic microorganisms as valuable tools to restore and maintain the sensory attributes of agricultural products under water deficiency stress.
Plants orchestrate their developmental processes and responses to environmental stimuli through a sophisticated network of small signaling molecules, termed phytohormones. Among these, auxins are recognized for their role in promoting plant growth. However, indole-3-acetamide (IAM), an auxin precursor, has been observed to inhibit primary root elongation. The molecular mechanism underlying this inhibitory effect remains largely unexplored. A comprehensive genome-wide association study (GWAS) conducted on a highly diverse collection of 166 wild Arabidopsis accessions from the Iberian Peninsula has identified several genomic regions associated with reduced IAM sensitivity under controlled in vitro conditions. This study highlighted ABA3 and GA2ox2 as possible candidate genes. Molecular and structural analyses suggest that the inhibition of primary root elongation induced by IAM is intricately associated with the enhanced production of abscisic acid (ABA) involving ABA3. Studies employing mutant and reporter lines have confirmed that IAM activates ABA signaling, thereby revealing a novel interaction between the auxin precursor IAM and ABA and suggesting an independent role for IAM as a signaling molecule in plant hormone crosstalk.
Plants regulate their developmental programs and their responses to environmental changes through a complex network of small signaling compounds, known as phytohormones. The role of auxins in promoting plant growth has been extensively investigated. Furthermore, previous studies have demonstrated that the accumulation of indole-3-acetamide (IAM), an auxin precursor, results in the suppression of plant growth, particularly primary root elongation. This observation led to the hypothesis that IAM or an IAM derivative exerts negative growth regulatory effects. However, the molecular mechanism by which IAM inhibits plant growth remains largely unelucidated. To gain deeper insight into the molecular mode of action of IAM, we conducted a comprehensive genome-wide association study (GWAS) using a highly diverse collection of 166 wild Arabidopsis accessions from the Iberian Peninsula. Consequently, we identified several genomic regions associated with a reduced response to IAM under controlled in vitro conditions, which included ABA3 and GA2ox2 as candidate genes. Sequence analyses, transcriptomics studies, and comparison of three-dimensional models generated for ABA3 proteins encoded by the two major natural alleles identified in the collection of wild accessions suggested that IAM-triggered inhibition of primary root elongation is closely associated with the formation of abscisic acid (ABA) in Arabidopsis thaliana seedlings. Finally, physiological characterization of mutants for those candidate genes further corroborated that IAM activates ABA signaling. Our results demonstrate that IAM is intricately linked with ABA biosynthesis and signaling, thereby elucidating a novel node in plant hormone crosstalk. ### Competing Interest Statement The authors have declared no competing interest. Ministerio de Ciencia e Innovación, https://ror.org/05r0vyz12, BFU2017-82826-R, PID2020-119441RB-100, PID2022-136893NB-I00, RED2022-134917-T, SEV-2016-0672
Plant–microbe interactions exert a significant influence on host stress responses; however, the molecular mechanisms underlying these effects remain inadequately understood. In this study, we characterize FaMAN8, an α-mannosidase from Fragaria × ananassa, to explore its role in adaptation to heat waves and water deficit, as well as its modulation by fungal endophytes. Transcriptomic analysis identified FaMAN8 as the sole α-mannosidase isoform highly conserved across reported sequences, with root-specific induction under conditions of heat stress, deficient irrigation, and endophytic colonization. Structural modeling revealed that FaMAN8 exhibits the canonical domain organization of glycoside hydrolase family 38 (GH38) enzymes, featuring a conserved catalytic architecture and metal-binding site. Molecular docking and dynamics simulations with the Man3GlcNAc2 ligand indicated a stable binding pocket involving key catalytic residues and strong electrostatic complementarity. MM-GBSA and free energy landscape analyses further supported the thermodynamic stability of the protein–ligand complex. Cavity analysis revealed a larger active site in FaMAN8 compared to its homolog JbMAN, suggesting broader substrate accommodation. Collectively, these findings identify FaMAN8 as a stress-responsive glycosidase potentially involved in glycan remodeling during beneficial root–fungus interactions. This work provides molecular insights into plant–microbe symbiosis and lays the groundwork for microbiome-informed strategies to enhance crop stress resilience.
AbstractPlants share their habitats with a multitude of different microbes. This close vicinity promoted the evolution of inter-organismic interactions between plants and many different microorganisms that provide mutual growth benefits both to the plant and the microbial partner. The symbiosis ofArabidopsis thalianawith the beneficial root colonizing endophyteSerendipita indicarepresents a well-studied system. Co-colonization of Arabidopsis roots withS. indicasignificantly promotes plant growth. Due to the notable phenotypic alterations of fungus-infected root systems, the involvement of a reprogramming of plant hormone levels, especially that of indole-3-acetic acid, has been suggested earlier. However, until now, the molecular mechanism by whichS. indicapromotes plant growth remains largely unknown. This study used comprehensive transcriptomics, metabolomics, reverse genetics, and life cell imaging to reveal the intricacies of auxin-related processes that affect root growth in the symbiosis betweenA. thalianaandS. indica. Our experiments revealed the essential role of tightly controlled auxin conjugation in the plant–fungus interaction. It particularly highlighted the importance of twoGRETCHEN HAGEN 3(GH3) genes,GH3.5andGH3.17, for the fungus infection-triggered stimulation of biomass production, thus broadening our knowledge about the function of GH3s in plants. Furthermore, we provide evidence for the transcriptional alteration of thePIN2auxin transporter gene in roots of Arabidopsis seedlings infected withS. indicaand demonstrate that this transcriptional adjustment affects auxin signaling in roots, which results in increased plant growth.
Plants share their habitats with a multitude of different microbes. This close vicinity promoted the evolution of interorganismic interactions between plants and many different microorganisms that provide mutual growth benefits both to the plant and the microbial partner. The symbiosis of Arabidopsis thaliana with the beneficial root colonizing endophyte Serendipita indica represents a well-studied system. Colonization of Arabidopsis roots with S. indica promotes plant growth and stress tolerance of the host plant. However, until now, the molecular mechanism by which S. indica reprograms plant growth remains largely unknown. This study used comprehensive transcriptomics, metabolomics, reverse genetics, and life cell imaging to reveal the intricacies of auxin-related processes that affect root growth in the symbiosis between A. thaliana and S. indica. Our experiments revealed the sustained stimulation of auxin signalling in fungus infected Arabidopsis roots and disclosed the essential role of tightly controlled auxin conjugation in the plant-fungus interaction. It particularly highlighted the importance of two GRETCHEN HAGEN 3 (GH3) genes, GH3.5 and GH3.17, for the fungus infection-triggered stimulation of biomass production, thus broadening our knowledge about the function of GH3s in plants. Furthermore, we provide evidence for the transcriptional alteration of the PIN2 auxin transporter gene in roots of Arabidopsis seedlings infected with S. indica and demonstrate that this transcriptional adjustment affects auxin signalling in roots, which results in increased plant growth.
Soil salinity is a significant abiotic stress factor that impedes plant growth and crop yield, particularly in arid and semi-arid regions. Recent reports indicate that 8.7
Global climate change exacerbates abiotic stresses, as drought, heat, and salt stresses are anticipated to increase significantly in the coming years. Plants coexist with a diverse range of microorganisms. Multiple inter-organismic relationships are known to confer benefits to plants, including growth promotion and enhanced tolerance to abiotic stresses. In this study, we investigated the mutualistic interactions between three fungal endophytes originally isolated from distinct arid environments and an agronomically relevant crop, Solanum lycopersicum. We demonstrated a significant increase in shoot biomass under drought conditions in co-cultivation with Penicillium chrysogenum isolated from Antarctica, Penicillium minioluteum isolated from the Atacama Desert, Chile, and Serendipita indica isolated from the Thar Desert, India. To elucidate plant gene modules commonly induced by the different endophytes that could explain the observed drought tolerance effect in tomato, a comprehensive transcriptomics analysis was conducted. This analysis led to the identification of a shared gene module in the fungus-infected tomato plants. Within this module, gene network analysis enabled us to identify genes related to abscisic acid (ABA) signaling, ABA transport, auxin signaling, ion homeostasis, proline biosynthesis, and jasmonic acid signaling, providing insights into the molecular basis of drought tolerance commonly mediated by fungal endophytes. Our findings highlight a conserved response in the mutualistic interactions between endophytic fungi isolated from unrelated environments and tomato roots, resulting in improved shoot biomass production under drought stress.
Plants are sessile organisms that face environmental threats throughout their life cycle, but increasing global warming poses an even more existential threat. Despite these unfavorable circumstances, plants try to adapt by developing a variety of strategies coordinated by plant hormones, resulting in a stress-specific phenotype. In this context, ethylene and jasmonates (JAs) present a fascinating case of synergism and antagonism. Here, Ethylene Insensitive 3/Ethylene Insensitive-Like Protein1 (EIN3/EIL1) and Jasmonate-Zim Domain (JAZs)-MYC2 of the ethylene and JAs signaling pathways, respectively, appear to act as nodes connecting multiple networks to regulate stress responses, including secondary metabolites. Secondary metabolites are multifunctional organic compounds that play crucial roles in stress acclimation of plants. Plants that exhibit high plasticity in their secondary metabolism, which allows them to generate near-infinite chemical diversity through structural and chemical modifications, are likely to have a selective and adaptive advantage, especially in the face of climate change challenges. In contrast, domestication of crop plants has resulted in change or even loss in diversity of phytochemicals, making them significantly more vulnerable to environmental stresses over time. For this reason, there is a need to advance our understanding of the underlying mechanisms by which plant hormones and secondary metabolites respond to abiotic stress. This knowledge may help to improve the adaptability and resilience of plants to changing climatic conditions without compromising yield and productivity. Our aim in this review was to provide a detailed overview of abiotic stress responses mediated by ethylene and JAs and their impact on secondary metabolites.
The pre-exposure of plants to a potentially stressful condition can stimulate tolerance to subsequent stresses, a phenomenon associated with memory in plants. When the stimuli have different natures, a cross-tolerance phenomenon can take place. The objective of this study was to investigate whether the pre-exposure of rice plants to a saline stimulus at the vegetative stage has the potential to mitigate the effects of a drought event during grain-filling. By evaluating the transcriptional and physiological (e.g. hormones, gas exchange, growth parameters) responses, this study seek to identify likely long-term memory mechanisms. Therefore, rice plants were exposed to a pre-treatment in the vegetative stage induced by 150 mM NaCl solution for four days and then subjected to 16 days of water deficit in the reproductive stage. Physiological parameters were evaluated and the endogenous levels of the plant hormones abscisic acid (ABA), salicylic acid (SA) and jasmonic acid (JA) and RNA-sequencing (RNA-Seq) was measured to investigate transcriptional profiles of rice plants subjected to cross-stress. The results demonstrated that primed plants challenged by water stress during the grain-filling stage showed less electrolyte leakage, less damage to the photosynthetic apparatus and increased root growth. The higher ABA concentration in leaves was closely related to the above physiological responses. Along with JA and SA, ABA can be a determinant of long-term stress memory in rice. The annotation of specific cross-tolerance genes pointed to signaling and synthesis of hormones, photosynthesis, stomatal conductance, antioxidant system, glyoxylate cycle and transcription factors. It is concluded that priming with salt in the vegetative stage can mitigates the effects of drought during the reproductive stage at the transcriptional, physiological and hormonal levels.
EDITORIAL article Front. Ecol. Evol., 30 March 2023Sec. Coevolution Volume 11 - 2023 | https://doi.org/10.3389/fevo.2023.1183310