Symbiotic synergy: How Arbuscular Mycorrhizal Fungi enhance nutrient uptake, stress tolerance, and soil health through molecular mechanisms and hormonal regulation

Ahmed N., Tu P., Deng L., Chachar S., Chachar Z., Deng L.

Deng L., Tu P., Ahmed N., Zhang G., Cen Y., Huang B., Deng L., Yuan H.

Gebremeskel K., Birhane E., Habtu S., Haile M., Chanyalew S., Tadele Z., Assefa K.

Arbuscular mycorrhizal fungi (AMF) form beneficial partnerships with most plant species, helping to improve crop resilience in tough environmental conditions. This paper analyzed how different genotypes responded to AMF inoculation, focusing on root colonization percentage (RCP) and the impact of AMF on above-ground agronomic traits. However, RCP alone may not fully explain genotype variation, and AMF effects cannot be judged solely on above-ground traits. This research aims to explore the variation in ninety tef genotypes under AMF conditions and assess how AMF and genotypes affect root and shoot morphology traits. Genotypes were sorted into six cluster groups, showing varied responsiveness to AMF, with RCP ranging from 25.03 to 72.29%. Despite similar RCP, variations in morphological traits were observed, and groups with lower RCP exhibited important traits not found in those with higher RCP, indicating RCP alone cannot indicate genotype variability. Wider Mahalanobis distance (D2) between clusters IV and VI, I and VI, and V and VI were crucial for developing different varieties and advancing root traits through hybridization. Among the tested genotypes, Wehni and Tsaeda zezew, followed by Gureaza, exhibited higher scores for plant height (PH), panicle length (PL), shoot biomass yield (SBY), root length (RL), and specific root length (SRL) compared to Simada. However, Wehni, Tsaeda zezew, and Gureaza showed similar results for days to maturity (DM), grain yield (GY), harvest index (HI), root dry weight (RDW), and root depth distribution (RDD) but differed from Simada genotype. Moreover, the inoculated Wehni genotype increased in days to panicle emergence (DPE) by 72%, DM by 84.11%, PH by 73.93%, PL by 73.68%, SBY by 144.17%, GY by 254.58%, HI by 133.33%, RL by 74.16%, RDW by 216.92%, SRL by 220%, and RDD by 93.28% as compared to the non-inoculated Simada. Improved performance of inoculated genotypes despite genotype variability could be because AMF enhances nutrient and water uptake by increasing root and shoot growth and the inherent growth strategy of the genotypes. Small-seeded crops planted shallowly benefit from AMF, which promotes deeper root growth for better nutrient and water uptake.

Wu Y., Chen C., Wang G.

Arbuscular mycorrhizal fungi (AMF) have profound effects on plant growth and nitrogen (N) and phosphorus (P) nutrition. However, a comprehensive evaluation of how plant N and P respond to AMF inoculation is still unavailable. Here, we complied data from 187 original researches and carried out a meta-analysis to assess the effects of AMF inoculation on plant growth and N and P nutrition. We observe overall positive effects of AMF inoculation on plant performance. The mean increases of plant biomass, N concentration, P concentration, N and P uptake of whole plant are 47%, 16%, 27%, 67%, and 105%, respectively. AMF inoculation induces more increases in plant concentrations and storage of P than N. Plant responses to AMF inoculation are substantially higher with single AMF species than with mixed AMF species, in laboratory experiments than in field experiments, and in legumes than in non-legumes. The response ratios of plant N and P nutrition are positively correlated with AMF colonization rate, N addition, P addition, and water condition, while unvaried with experiment duration. The biggest and smallest effect sizes of AMF inoculation on plant performance are observed in the application of nitrate and ammonium, respectively. Accordingly, this meta-analysis study clearly suggests that AMF inoculation improves both plant N and P nutrients and systematically clarifies the variation patterns in AMF effects with various biotic and abiotic factors. These findings highlight the important role of AMF inoculation in enhancing plant N and P resource acquisitions and provide useful references for evaluating the AMF functions under the future global changes.

Jin Q., Chachar M., Ali A., Chachar Z., Zhang P., Riaz A., Ahmed N., Chachar S.

Global warming poses a significant threat to plant ecosystems and agricultural productivity, primarily through heat stress (HS), which disrupts photosynthesis, respiration, and overall plant metabolism. Epigenetic modifications, including DNA methylation, histone modifications, and RNA modifications, enable plants to dynamically and heritably adjust gene expression in response to environmental stressors. These mechanisms not only help plants survive immediate stress but also confer stress memory, enhancing their resilience to future HS events. This review explores the mechanisms underlying plant thermotolerance, emphasizing the critical role of epigenetic regulation in adapting to HS. It also highlights how DNA methylation modulates stress-responsive genes, histone modifications facilitate transcriptional memory, and RNA modifications influence mRNA stability and translation. Recent advancements in genome editing technologies, such as CRISPR-Cas9, have enabled precise modifications of epigenetic traits, offering new avenues for breeding climate-resilient crops. The integration of these modern tools with traditional breeding methods holds significant promise for developing crops with enhanced thermotolerance. Despite the potential, challenges such as the stability and heritability of epigenetic marks and the complex interplay between different epigenetic modifications need to be addressed. Future research should focus on elucidating these interactions and identifying reliable epigenetic markers for selection. By leveraging the insights gained from epigenetic studies, we can develop innovative breeding strategies to improve crop resilience and ensure sustainable agricultural productivity in the face of global warming. This review underscores the importance of epigenetic regulation in plant adaptation to heat stress and its potential to revolutionize crop breeding, offering a pathway to secure food production and sustainability under changing climatic conditions.

Yang D., Wang L., Wang X.

Molybdenum (Mo) is an essential nutrient for leguminous plants, but the effects of Mo exposure on plant growth, especially in relation to soil microorganisms, are not fully understood. This study employed alfalfa (Medicago sativa L.) to evaluate the physiochemical responses to gradient soil Mo variations and explore the potential regulatory role of rhizosphere microorganism - arbuscular mycorrhizal fungi (AMF) in modulating Mo's impact on plant physiology, with a focus on metabolic pathways. The results showed that Mo exerted hormetic effect (facilitation at low doses; inhibition at high doses) on alfalfa growth, promoting biomass (below 90.94 mg/kg, with a 63.98 % maximum increase), root length (below 657.11 mg/kg, with a 39.29 % maximum increase), and plant height (below 304.03 mg/kg, with an 18.4 % maximum increase). Excess Mo (1000 mg/kg) resulted in a reduction in photosynthesis and biomass growth due to increased oxidative stress (p < 0.05). Within the stimulatory zones, AMF enhanced Mo accumulation in alfalfa, augmenting its phytological effects. Exceed the stimulatory zones, AMF enhanced alfalfa Fe uptake and reduced the generation of reactive oxygen species (ROS) induced by excess Mo by shifting the redox homeostasis-controlled enzyme from peroxidase (POD) to superoxide dismutase (SOD), thereby improving alfalfa's tolerance to Mo. Metabolomic analysis further revealed that AMF promoted the biosynthesis of indole acetic acid (IAA) and various amino acids in Mo-stressed alfalfa (p < 0.05), which accelerated alfalfa growth and mitigated Mo-induced phytotoxicity. These insights provide a foundation for developing sustainable management strategies for Mo-exposed soils using AMF inoculants, such as minimizing Mo fertilizer application in Mo-deficient soils and facilitating the reclamation of Mo-contaminated soils.

Jian P., Zha Q., Hui X., Tong C., Zhang D.

Arbuscular mycorrhizal fungi (AMF) are beneficial microorganisms ubiquitous in soil that form symbiotic mycorrhizal structures with plant roots. When the host plant is exposed to temperature stress, arbuscular mycorrhizal fungi can improve the host plant’s resistance by helping regulate the growth of underground and aboveground parts. In recent years, due to climate change, extremely high and low temperatures have occurred more frequently and for longer durations, significantly impacting plant growth, antioxidant systems, osmotic balance, photosynthesis, and related gene expression. Consequently, numerous scholars have used arbuscular mycorrhizal fungi to aid plants, confirming that arbuscular mycorrhizal fungi can help host plants improve their ability to resist temperature stress. In this paper, the quantitative research method of Meta-analysis was used to collate and build a database of 129 relevant works to evaluate the effects of AMF on plant resistance to temperature stress and explore the response mechanism of AMF to host plants subjected to temperature stress, providing a theoretical basis for further exploring arbuscular mycorrhizal fungi in improving plant resistance to temperature stress.

Fan L., Zhang P., Cao F., Liu X., Ji M., Xie M.

This study aimed to investigate the effects of applying arbuscular mycorrhizal fungi (AMF) on maize root growth and yield formation under different soil conditions. This study was conducted under sandy soil (S) and saline–alkali soil (Y), with treatments of AMF application (AM) and no AMF application (CK). The root characteristics, yield, and quality of maize were measured. High-throughput sequencing technology was employed to assess the impact of AMF on the soil microbial community structure, and the correlation between soil microbes and soil physicochemical properties was elucidated. The results show that under both sandy and saline–alkali soil conditions, AMF application significantly enhanced maize root growth, yield, grain quality, and soil available nitrogen (AN), available phosphorus (AP), and available potassium (AK) contents compared to the CK treatment. Soil microbial Alpha diversity analysis indicated that AMF application effectively increased soil microbial diversity and richness. Principal coordinate analysis (PCoA) and microbial community structure analysis revealed significant differences in bacterial communities between AM treatment in sandy soil (SAM) and CK in sandy soil (SCK), and significant differences in both bacterial and fungal communities between AM treatment in saline–alkali soil (YAM) and CK in saline–alkali soil (YCK). Furthermore, significant correlations between microbial communities and soil physicochemical properties were found, such as AN, AP, AK, soil salinity (SS), and organic matter (OM) content. AMF application had a greater impact on bacterial communities than on fungal communities. This study demonstrated that the use of AMF as a bio-fungal fertilizer was effective in improving spring maize yields, especially in terms of yield increase and quality stability in sandy and saline soils, thereby contributing to safe and sustainable cropping practices.

Giese E.C., Santos L.S., Santana A.C.

Ahmed N., Deng L., Wang C., Shah Z., Deng L., Li Y., Li J., Chachar S., Chachar Z., Hayat F., Bozdar B., Ansari F., Ali R., Gong L., Tu P.

The role of modified biochar in enhancing phosphorus (P) availability is gaining attention as an environmentally friendly approach to address soil P deficiency, a global agricultural challenge. Traditional phosphatic fertilizers, while essential for crop yield, are costly and environmentally detrimental owing to P fixation and leaching. Modified biochar presents a promising alternative with improved properties such as increased porosity, surface area, and cation exchange capacity. This review delves into the variability of biochar properties based on source and production methods and how these can be optimized for effective P adsorption. By adjusting properties such as pH levels and functional groups to align with the phosphate’s zero point of charge, we enhance biochar’s ability to adsorb and retain P, thereby increasing its bioavailability to plants. The integration of nanotechnology and advanced characterization techniques aids in understanding the structural nuances of biochar and its interactions with phosphorus. This approach offers multiple benefits: it enables farmers to use phosphorus more efficiently, reducing the need for traditional fertilizers and thereby minimizing environmental impacts, such as greenhouse gas emissions and P leaching. This review also identifies existing research gaps and future opportunities for further biochar modifications. These findings emphasize the significant potential of modified biochar in sustainable agriculture.

Zhang Y., Han X., Ren W., Zhang H., Tang M.

Arbuscular mycorrhizal (AM) fungi can establish a mutualistic relationship with the roots of most terrestrial plants to increase plant nutrient uptake. The effects of potassium uptake and transport by AM symbiosis are much less reported compared to other nutrients. In this research, a heterologous yeast system was used to verify that the LbHAK has capacity for potassium uptake. The split-roots system implemented using seedlings of Lycium barbarum confirmed that R. irregularis locally induced LbHAK expression, which means that LbHAK is only expressed in mycorrhizal roots. Furthermore, the impacts of overexpression of LbHAK on the growth, nutrients and water uptake, and transport of mycorrhizal tobacco (inoculation with Rhizophagus irregularis) at 0.2 mM and 2 mM K conditions were assessed. The mycorrhizal tobacco growth and potassium accumulation were significantly enhanced through LbHAK overexpression in tobacco. In addition, overexpression of LbHAK substantially enhanced phosphorus content, while stimulating the expression of NtPT4, Rir-AQP1, and Rir-AQP2 in mycorrhizal tobacco. Moreover, LbHAK overexpression greatly promoted AM colonization. LbHAK has a potential role in facilitating potassium absorption through the mycorrhizal pathway, and overexpression of LbHAK in tobacco may promote the transport of potassium, phosphorus, and water from AM fungi to tobacco. These data imply the important roles played by the LbHAK in AM-fungi-induced potassium uptake in L. barbarum and in improving plant nutrients and AM colonization.

Zhang J., Sun J., Chiu C.H., Landry D., Li K., Wen J., Mysore K.S., Fort S., Lefebvre B., Oldroyd G.E., Feng F.

Summary Plants establish symbiotic associations with arbuscular mycorrhizal fungi (AMF) to facilitate nutrient uptake, particularly in nutrient-limited conditions. This partnership is rooted in the plant's ability to recognize fungal signaling molecules, such as chitooligosaccharides (chitin) and lipo-chitooligosaccharides. In the legume Medicago truncatula, chitooligosaccharides trigger both symbiotic and immune responses via the same lysin-motif-receptor-like kinases (LysM-RLKs), notably CERK1 and LYR4. The nature of plant-fungal engagement is opposite according to the outcomes of immunity or symbiosis signaling, and as such, discrimination is necessary, which is challenged by the dual roles of CERK1/LYR4 in both processes. Here, we describe a LysM-RLK, LYK8, that is functionally redundant with CERK1 for mycorrhizal colonization but is not involved in chitooligosaccharides-induced immunity. Genetic mutation of both LYK8 and CERK1 blocks chitooligosaccharides-triggered symbiosis signaling, as well as mycorrhizal colonization, but shows no further impact on immunity signaling triggered by chitooligosaccharides, compared with the mutation of CERK1 alone. LYK8 interacts with CERK1 and forms a receptor complex that appears essential for chitooligosaccharides activation of symbiosis signaling, with the lyk8/cerk1 double mutant recapitulating the impact of mutations in the symbiosis signaling pathway. We conclude that this novel receptor complex allows chitooligosaccharides activation specifically of symbiosis signaling and helps the plant to differentiate between activation of these opposing signaling processes.

Jin Z., Wang G., George T.S., Zhang L.

Arbuscular mycorrhizal (AM) fungi engage in symbiosis with more than 80% of terrestrial plants, enlarging root phosphorus (P) absorption volume by producing extensive extraradical hyphae (ERH) in the soil. In addition, AM fungi recruit and cooperate with soil bacteria to enhance soil organic P mobilization and improve fungal and plant fitness through hyphal exudates. However, the role of the dominant compounds in the hyphal exudates in enhancing organic P mobilization in the mycorrhizal pathway is still not well understood. In this study, we added sugars, i.e., glucose, fructose, and trehalose, which are detected in the hyphal exudates, to the hyphal compartments (HCs) that allowed the ERH of the AM fungus to grow or not. The results showed that in AM fungus-inoculated pots, adding three sugars at a concentration of 2 mmol C kg−1 soil significantly increased the phosphatase activity and facilitated the mobilization of organic P in the HCs. The addition of fructose at a concentration of 2 mmol C kg−1 soil was the most efficient in increasing the phosphatase activity and enhancing organic P mobilization. The released inorganic P was then absorbed by the ERH of the AM fungus. The enhanced mobilization of organic P was correlated with the increase in phoD gene number and the changing bacterial community in the presence of fungal hyphae. The sugar addition enriched the relative abundance of some bacterial taxa, e.g., Betaproteobacteriales. Our study suggested that the addition of the sugars by mycorrhizae could be a pivotal strategy in managing P uptake in agricultural production, potentially directing future practices to optimize plant–fungi–bacteria interactions for improved P use efficiency.

Ji C., Ge Y., Zhang H., Zhang Y., Xin Z., Li J., Zheng J., Liang Z., Cao H., Li K.

Background and aimsSoil salinity negatively affects crop development. Halotolerant nitrogen-fixing bacteria (HNFB) and arbuscular mycorrhizal fungi (AMF) are essential microorganisms that enhance crop nutrient availability and salt tolerance in saline soils. Studying the impact of HNFB on AMF communities and using HNFB in biofertilizers can help in selecting the optimal HNFB-AMF combinations to improve crop productivity in saline soils.MethodsWe established three experimental groups comprising apple plants treated with low-nitrogen (0 mg N/kg, N0), normal-nitrogen (200 mg N/kg, N1), and high-nitrogen (300 mg N/kg, N2) fertilizer under salt stress without bacteria (CK, with the addition of 1,500 mL sterile water +2 g sterile diatomite), or with bacteria [BIO, with the addition of 1,500 mL sterile water +2 g mixed bacterial preparation (including Bacillus subtilis HG-15 and Bacillus velezensis JC-K3)].ResultsHNFB inoculation significantly increased microbial biomass and the relative abundance of beta-glucosidase-related genes in the rhizosphere soil under identical nitrogen application levels (p &lt; 0.05). High-nitrogen treatment significantly reduced AMF diversity and the relative abundance of beta-glucosidase, acid phosphatase, and urea-related genes. A two-way analysis of variance showed that combined nitrogen application and HNFB treatment could significantly affect soil physicochemical properties and rhizosphere AMF abundance (p &lt; 0.05). Specifically, HNFB application resulted in a significantly higher relative abundance of Glomus-MO-G17-VTX00114 compared to that in the CK group at equal nitrogen levels.ConclusionThe impact of HNFB on the AMF community in apple rhizospheres is influenced by soil nitrogen levels. The study reveals how varying nitrogen levels mediate the relationship between exogenous HNFB, soil properties, and rhizosphere microbes.

Arifuzzaman M., Bagchi R., Hasan M.R., Rahman M.A., Rahman M.M., Rahman M.A., Kabir A.H.

Zinc (Zn) is an essential micronutrient for plant growth and development, and its deficiency in soil can be a significant problem for broccoli (Brassica oleracea L.) production. While the genetic efforts to breed Zn-efficient broccoli are complex, harnessing microbiomes is an emerging way to induce mineral efficiency in crops. In this study, broccoli, a non-host mycorrhizal species, was cultivated with or without zinc deficiency in the presence or absence of arbuscular mycorrhizal fungi (AMF), confirmed by the colonization efficiency in roots. Zn deficiency caused a significant decrease in morphological parameters and photosynthetic attributes being consistent with the decreased Zn levels in root and shoot relative to Zn-sufficient plants. However, the broccoli plants inoculated with AMF showed a substantial improvement in morphological and photosynthetic parameters in Zn-deficient conditions due to the significant increase in Zn levels. In addition, AMF-inoculated plants under Zn deficiency showed a significant decrease in cell death (%), electrolyte leakage, and H2O2 levels compared to Fe-deficient plants, which further suggests the improvements in cellular status due to the AMF colonization. The real-time PCR experiments showed a significant induction in the expression of BoZIP1 and BoNRAMP1 genes in the roots of Zn-deficient broccoli inoculated with AMF, suggesting that AMF may be associated with the induction of these genes responsible for Zn-uptake and transport. We further observed the induction of POD (peroxidase), APX (ascorbate peroxidase) and SOD (superoxide dismutase), and S-metabolites (cysteine and glutathione) predominantly in the roots of Zn-starved broccoli inoculated with AMF which may confer tolerance to Zn-deficiency induced oxidative damage. This is the first report on the role of AMF in mitigating Zn-deficiency in broccoli which may promote the microbiome-aided improvement of plants suffering from Zn-deficiency in broccoli and other vegetable crops.