Novel Insights into Host Receptors and Receptor-mediated Signaling that Regulate Arbuscular Mycorrhizal Symbiosis

2020 ◽  
Author(s):  
Fahad Nasir ◽  
Ali Bahadur ◽  
Xiaolong Lin ◽  
Yingzhi Gao ◽  
Chunjie Tian
Keyword(s):  
Host Plant ◽  
Host Plants ◽  
Agronomic Traits ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Land Plant ◽  
Physical Contact ◽  
Mycorrhizal Symbiosis ◽  
Downstream Signaling ◽  
Am Symbiosis

Abstract More than 80% of land plant species benefit from symbiotic partnerships with arbuscular mycorrhizal (AM) fungi that assist in nutrient acquisition and enhance the ability of host plants to adapt to environmental constraints. Host-generated plasma membrane-residing receptor-like kinases and the α/β-hydrolases, e.g. DWARF14-LIKE (D14L), a putative karrikin receptor, are used to detect the presence of AM fungi prior to physical contact between the host and fungus. Detection induces the activation of symbiosis-related transcriptional programming, enabling the successful establishment of AM symbiosis. In order to prevent hyper-colonization and to maintain a mutually beneficial association, the host plants precisely monitor and control AM symbiosis during the post-symbiotic stage via different molecular strategies. While previous studies have elucidated how host plant receptors and receptor-mediated signaling regulate AM symbiosis, the molecular details underlying these processes remain poorly understood. The recent identification of a rice (Oryza sativa) CHITIN-ELICITOR RECEPTOR-KINASE 1 (OsCERK1) interaction partner MYC FACTOR RECEPTOR 1 (OsMYR1), as well as new insights into D14L-receptor- and SUPER NUMERIC NODULES 1 (SUNN1) receptor-mediated signaling have improved our understanding of how host plant receptors and their corresponding signaling regulate AM symbiosis. The present review summarizes these and other current findings that have increased our limited understanding of receptor-mediated signaling mechanisms involved in the regulation of AM symbiosis. The identified receptors and/or their downstream signaling components could potentially be used to engineer economically-important crops with improved agronomic traits by conferring the ability to control the colonization of AM fungi in a precise manner.

scholarly journals Target of rapamycin, PvTOR, is a key regulator of arbuscule development during mycorrhizal symbiosis in Phaseolus

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Manoj-Kumar Arthikala ◽  
Kalpana Nanjareddy ◽  
Lourdes Blanco ◽  
Xóchitl Alvarado-Affantranger ◽  
Miguel Lara
Keyword(s):  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Target Of Rapamycin ◽  
Mycorrhizal Symbiosis ◽  
Energy Status ◽  
Symbiotic Associations ◽  
Expression Of Genes ◽  
Fungal Symbiosis ◽  
Am Fungus ◽  
Am Symbiosis

AbstractTarget of rapamycin (TOR) is a conserved central growth regulator in eukaryotes that has a key role in maintaining cellular nutrient and energy status. Arbuscular mycorrhizal (AM) fungi are mutualistic symbionts that assist the plant in increasing nutrient absorption from the rhizosphere. However, the role of legume TOR in AM fungal symbiosis development has not been investigated. In this study, we examined the function of legume TOR in the development and formation of AM fungal symbiosis. RNA-interference-mediated knockdown of TOR transcripts in common bean (Phaseolus vulgaris) hairy roots notably suppressed AM fungus-induced lateral root formation by altering the expression of root meristem regulatory genes, i.e., UPB1, RGFs, and sulfur assimilation and S-phase genes. Mycorrhized PvTOR-knockdown roots had significantly more extraradical hyphae and hyphopodia than the control (empty vector) roots. Strong promoter activity of PvTOR was observed at the site of hyphal penetration and colonization. Colonization along the root length was affected in mycorrhized PvTOR-knockdown roots and the arbuscules were stunted. Furthermore, the expression of genes induced by AM symbiosis such as SWEET1, VPY, VAMP713, and STR was repressed under mycorrhized conditions in PvTOR-knockdown roots. Based on these observations, we conclude that PvTOR is a key player in regulating arbuscule development during AM symbiosis in P. vulgaris. These results provide insight into legume TOR as a potential regulatory factor influencing the symbiotic associations of P. vulgaris and other legumes.

Integrating physiological, community, and evolutionary perspectives on the arbuscular mycorrhizal symbiosis

Botany ◽  
2014 ◽  
Vol 92 (4) ◽  
pp. 241-251 ◽  
Author(s):  
Ylva Lekberg ◽  
Roger T. Koide
Keyword(s):  
Evolutionary Biology ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Partner Choice ◽  
Mycorrhizal Symbiosis ◽  
Physiological Processes ◽  
Resource Transfers ◽  
Am Symbiosis ◽  
Controlled Environments ◽  
Natural Settings

Our knowledge of arbuscular mycorrhizal (AM) function is largely based on results from short-term studies in controlled environments. While these have provided many important insights into the potential effects of the symbiosis on the two symbionts and their communities, they may have also inadvertently led to faulty assumptions about the function of the symbiosis in natural settings. Here we highlight the consequences of failing to consider the AM symbiosis from the perspectives of community ecology and evolutionary biology. Also, we argue that by distinguishing between physiological and evolutionary viewpoints, we may be able to resolve controversies regarding the mutualistic vs. parasitic nature of the symbiosis. Further, while most AM research has emphasized resource transfers, primarily phosphate and carbohydrate, our perceptions of parasitism, cheating, bet-hedging, and partner choice would most likely change if we considered other services. Finally, to gain a fuller understanding of the role of the AM symbiosis in nature, we need to better integrate physiological processes of plants and their AM fungi with their naturally occurring temporal and spatial patterns. It is our hope that this article will generate some fruitful discussions and make a contribution toward this end.

scholarly journals Phytohormones Regulate the Development of Arbuscular Mycorrhizal Symbiosis

2018 ◽  
Vol 19 (10) ◽  
pp. 3146 ◽  
Author(s):  
Dehua Liao ◽  
Shuangshuang Wang ◽  
Miaomiao Cui ◽  
Jinhui Liu ◽  
Aiqun Chen ◽  
...  
Keyword(s):  
Early Recognition ◽  
Fungal Growth ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Mycorrhizal Symbiosis ◽  
Dependent Manner ◽  
Terrestrial Plants ◽  
Root Cells ◽  
Della Proteins ◽  
Am Symbiosis

Most terrestrial plants are able to form a root symbiosis with arbuscular mycorrhizal (AM) fungi for enhancing the assimilation of mineral nutrients. AM fungi are obligate symbionts that depend on host plants as their sole carbon source. Development of an AM association requires a continuous signal exchange between the two symbionts, which triggers coordinated differentiation of both partners, to enable their interaction within the root cells. The control of the AM symbiosis involves a finely-tuned process, and an increasing number of studies have pointed to a pivotal role of several phytohormones, such as strigolactones (SLs), gibberellic acids (GAs), and auxin, in the modulation of AM symbiosis, through the early recognition of events up to the final arbuscular formation. SLs are involved in the presymbiotic growth of the fungus, while auxin is required for both the early steps of fungal growth and the differentiation of arbuscules. GAs modulate arbuscule formation in a dose-dependent manner, via DELLA proteins, a group of GRAS transcription factors that negatively control the GA signaling. Here, we summarize the recent findings on the roles of these plant hormones in AM symbiosis, and also explore the current understanding of how the DELLA proteins act as central regulators to coordinate plant hormone signaling, to regulate the AM symbiosis.

scholarly journals Expression Pattern Suggests a Role of MiR399 in the Regulation of the Cellular Response to Local Pi Increase During Arbuscular Mycorrhizal Symbiosis

2010 ◽  
Vol 23 (7) ◽  
pp. 915-926 ◽  
Author(s):  
Anja Branscheid ◽  
Daniela Sieh ◽  
Bikram Datt Pant ◽  
Patrick May ◽  
Emanuel A. Devers ◽  
...  
Keyword(s):  
Cellular Response ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Mycorrhizal Symbiosis ◽  
Pi Homeostasis ◽  
Pi Starvation ◽  
Mycorrhizal Roots ◽  
Am Symbiosis ◽  
Pi Stress

Many plants improve their phosphate (Pi) availability by forming mutualistic associations with arbuscular mycorrhizal (AM) fungi. Pi-repleted plants are much less colonized by AM fungi than Pi-depleted plants. This indicates a link between plant Pi signaling and AM development. MicroRNAs (miR) of the 399 family are systemic Pi-starvation signals important for maintenance of Pi homeostasis in Arabidopsis thaliana and might also qualify as signals regulating AM development in response to Pi availability. MiR399 could either represent the systemic low-Pi signal promoting or required for AM formation or they could act as counter players of systemic Pi-availability signals that suppress AM symbiosis. To test either of these assumptions, we analyzed the miR399 family in the AM-capable plant model Medicago truncatula and could experimentally confirm 10 novel MIR399 genes in this species. Pi-depleted plants showed increased expression of mature miR399 and multiple pri-miR399, and unexpectedly, levels of five of the 15 pri-miR399 species were higher in leaves of mycorrhizal plants than in leaves of nonmycorrhizal plants. Compared with nonmycorrhizal Pi-depleted roots, mycorrhizal roots of Pi-depleted M. truncatula and tobacco plants had increased Pi contents due to symbiotic Pi uptake but displayed higher mature miR399 levels. Expression levels of MtPho2 remained low and PHO2-dependent Pi-stress marker transcript levels remained high in these mycorrhizal roots. Hence, an AM symbiosis-related signal appears to increase miR399 expression and decrease PHO2 activity. MiR399 overexpression in tobacco suggested that miR399 alone is not sufficient to improve mycorrhizal colonization supporting the assumption that, in mycorrhizal roots, increased miR399 are necessary to keep the MtPho2 expression and activity low, which would otherwise increase in response to symbiotic Pi uptake.

Overexpression of MdIAA24 improves apple drought resistance by positively regulating strigolactone biosynthesis and mycorrhization

2020 ◽  
Author(s):  
Dong Huang ◽  
Qian Wang ◽  
Guangquan Jing ◽  
Mengnan Ma ◽  
Chao Li ◽  
...  
Keyword(s):  
Drought Stress ◽  
Positive Impact ◽  
Growth Parameters ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Land Plant ◽  
Exchange Capacity ◽  
Cortical Cells ◽  
Relative Water ◽  
Am Symbiosis

Abstract Most land plant species have the ability to establish a symbiosis with arbuscular mycorrhizal (AM) fungi. These fungi penetrate into root cortical cells and form branched structures (known as arbuscules) for nutrient exchange. We cloned the MdIAA24 from apple (Malus domestica) following its up-regulation during AM symbiosis. Results demonstrate the positive impact of the overexpression (OE) of MdIAA24 in apple on AM colonization. We observed the strigolactone (SL) synthesis genes, including MdD27, MdCCD7, MdCCD8a, MdCCD8b and MdMAXa, to be up-regulated in the OE lines. Thus, the OE lines exhibited both a higher SL content and colonization rate. Furthermore, we observed that the OE lines were able to maintain better growth parameters under AM inoculation conditions. Under drought stress with the AM inoculation, the OE lines were less damaged, which was demonstrated by a higher relative water content, a lower relative electrolytic leakage, a greater osmotic adjustment, a higher reactive oxygen species scavenging ability, an improved gas exchange capacity and an increased chlorophyll fluorescence performance. Our findings demonstrate that the OE of MdIAA24 in apple positively regulates the synthesis of SL and the formation of arbuscules as a drought stress coping mechanism.

Contribution of arbuscular mycorrhizal symbiosis to in vitro root metal uptake: from trace to toxic metal conditionsThis paper is one of the papers presented at the 50th Annual Meeting of the Canadian Society of Plant Physiologists (CSPP) held at the University of Ottawa, Ontario, in June 2008. Other papers from this meeting are presented in the July 2009 Special Issue of Botany.

Botany ◽  
2009 ◽  
Vol 87 (10) ◽  
pp. 913-921 ◽  
Author(s):  
Patrick Audet ◽  
Christiane Charest
Keyword(s):  
Metal Binding ◽  
Toxic Metal ◽  
In Vitro Study ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Mycorrhizal Symbiosis ◽  
Relative Contribution ◽  
Am Symbiosis ◽  
Metal Contaminant

This in-vitro study investigated the role of arbuscular mycorrhizal (AM) symbiosis in root metal acquisition and stress tolerance from two experiments using a carrot root-organ culture system, and involving the essential micronutrient zinc as a typical metal contaminant. We demonstrated that the AM symbiosis plays a dual role in root metal acquisition by increasing nutrient uptake via mycorrhizal “enhanced uptake” at low (trace) metal concentrations in the growth medium, but then lessening the uptake through “metal-binding” processes at high (toxic) concentrations. Furthermore, we also observed the relative contribution of hyphal uptake and translocation to roots, which led us to suggest that the enhanced uptake and metal-binding processes likely occur simultaneously and (or) independently. Ultimately, symptoms of metal toxicity toward both the roots and AM fungi at the highest Zn exposure concentrations was observed. From this finding, a critical toxicity burden likely exists arising from conditions ranging from trace to toxic metal extremes.

scholarly journals Addition of high C:N crop residues to a P-limited substrate constrains the benefits of arbuscular mycorrhizal symbiosis for wheat P and N nutrition

Mycorrhiza ◽  
2021 ◽  
Author(s):  
Rosolino Ingraffia ◽  
Sergio Saia ◽  
Antonio Giovino ◽  
Gaetano Amato ◽  
Giuseppe Badagliacca ◽  
...  
Keyword(s):  
Plant Growth ◽  
Nutrient Uptake ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
P Uptake ◽  
Mycorrhizal Symbiosis ◽  
N Recovery ◽  
Positive Effects ◽  
Plant P Uptake ◽  
Am Symbiosis

AbstractMany aspects concerning the role of arbuscular mycorrhizal (AM) fungi in plant nutrient uptake from organic sources remain unclear. Here, we investigated the contribution of AM symbiosis to N and P uptake by durum wheat after the addition of a high C:N biomass to a P-limited soil. Plants were grown in pots in the presence or absence of a multispecies AM inoculum, with (Org) or without (Ctr) the addition of 15N-labelled organic matter (OM). A further treatment, in which 15N was applied in mineral form (Ctr+N) in the same amount as that supplied in the Org treatment, was also included. Inoculation with AM had positive effects on plant growth in both control treatments (Ctr and Ctr+N), mainly linked to an increase in plant P uptake. The addition of OM, increasing the P available in the soil for the plants, resulted in a marked decrease in the contribution of AM symbiosis to plant growth and nutrient uptake, although the percentage of mycorrhization was higher in the Org treatment than in the controls. In addition, mycorrhization drastically reduced the recovery of 15N from the OM added to the soil whereas it slightly increased the N recovery from the mineral fertiliser. This suggests that plants and AM fungi probably exert a differential competition for different sources of N available in the soil. On the whole, our results provide a contribution to a better understanding of the conditions under which AM fungi can play an effective role in mitigating the negative effects of nutritional stresses in plants.

scholarly journals Mycorrhizal symbiosis alleviates plant drought stress within and across plant generations via plasticity

2020 ◽  
Author(s):  
Javier Puy ◽  
Carlos Perez Carmona ◽  
Inga Hiiesalu ◽  
Maarja Opik ◽  
Mari Moora ◽  
...  
Keyword(s):  
Drought Stress ◽  
Phenotypic Plasticity ◽  
Water Availability ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Mycorrhizal Symbiosis ◽  
Fungal Colonization ◽  
Transgenerational Effects ◽  
Two Generations ◽  
Am Symbiosis

Phenotypic plasticity is essential for organisms to adapt to local ecological conditions. Little is known about how mutualistic interactions, such as arbuscular mycorrhizal (AM) symbiosis, mediate plant phenotypic plasticity and to what extent this plasticity may be heritable (i.e. transgenerational effects). We tested for plant plasticity within- and across-generations in response to AM symbiosis and varying water availability in a full factorial experiment over two generations, using the perennial apomictic herb Taraxacum brevicorniculatum. We examined changes in phenotype, performance, and AM fungal colonization of the offspring throughout plant development. AM symbiosis and water availability triggered phenotypic changes during the life cycle of plants. Additionally, both triggered adaptive transgenerational effects, especially detectable during the juvenile stage. Drought stress and absence of AM fungi caused concordant plant phenotypic modifications towards a stress-coping phenotype within- and across-generations. AM fungal colonization of offspring was also affected by the parental environment. AM symbiosis can trigger transgenerational effects, including changes in functional traits related to resource-use acquisition and AM fungal colonization of the offspring, in turn affecting the biotic interaction. Thus, transgenerational effects of mycorrhizal symbiosis are not limited to plant fitness, but also improve plants ability to cope with environmental stress.

scholarly journals Molecular signal communication during arbuscular mycorrhizal formation induces significant transcriptional reprogramming of wheat (Triticum aestivum) roots

2019 ◽  
Author(s):  
Hui Tian ◽  
Runze Wang ◽  
Mengjiao Li ◽  
Haiyan Dang ◽  
Zakaria M Solaiman
Keyword(s):  
High Throughput Sequencing ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Physical Contact ◽  
Nitrogen And Phosphorus ◽  
Wheat Roots ◽  
Transcriptional Profiles ◽  
Am Symbiosis ◽  
Molecular Signal ◽  
Pass Through

Abstract Background and Aims Arbuscular mycorrhizal (AM) symbiosis begins with molecular signal communication (MSC) between AM fungi and the roots of the host plant. We aimed to test the hypothesis that the transcriptional profiles of wheat roots can be changed significantly by AM symbiotic signals, without direct contact. Methods Non-mycorrhizal (NM) and MSC treatments involved burying filter membrane bags containing sterilized and un-sterilized inoculum of the AM fungus Rhizophagus irregularis, respectively. The bags physically separated roots and AM structures but allowed molecular signals to pass through. Extracted RNA from wheat roots was sequenced by high-throughput sequencing. Results Shoot total nitrogen and phosphorus content of wheat plants was decreased by the MSC treatment. A total of 2360 differentially expressed genes (DEGs), including 1888 up-regulated DEGs and 472 down-regulated DEGs, were found dominantly distributed on chromosomes 2A, 2B, 2D, 3B, 5B and 5D. The expression of 59 and 121 genes was greatly up- and down-regulated, respectively. Only a portion of DEGs could be enriched into known terms during gene ontology analysis, and were mostly annotated to ‘catalytic activity’, ‘protein metabolic process’ and ‘membrane’ in the molecular function, biological process and cellular component ontology categories, respectively. More than 120 genes that may be involved in key processes during AM symbiosis development were regulated at the pre-physical contact stages. Conclusions The transcriptional profiles of wheat roots can be changed dramatically by MSC. Much of the information provided by our study is of great importance for understanding the mechanisms underlying the development of AM symbiosis.

scholarly journals A Phosphate-Dependent Requirement for Transcription Factors IPD3 and IPD3L During Arbuscular Mycorrhizal Symbiosis in Medicago truncatula

2019 ◽  
Vol 32 (10) ◽  
pp. 1277-1290
Author(s):  
Penelope L. Lindsay ◽  
Brandon N. Williams ◽  
Allyson MacLean ◽  
Maria J. Harrison
Keyword(s):  
Gene Expression ◽  
Signaling Pathway ◽  
Medicago Truncatula ◽  
Lotus Japonicus ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Mycorrhizal Symbiosis ◽  
Wild Type ◽  
Symbiotic Gene ◽  
Am Symbiosis

During arbuscular mycorrhizal (AM) symbiosis, activation of a symbiosis signaling pathway induces gene expression necessary for accommodation of AM fungi. Here, we focus on pathway components Medicago truncatula INTERACTING PROTEIN OF DOES NOT MAKE INFECTIONS 3 (IPD3) and IPD3 LIKE (IPD3L), which are potential orthologs of Lotus japonicus CYCLOPS, a transcriptional regulator essential for AM symbiosis. In the double mutant ipd3 ipd3l, hyphal entry through the epidermis and overall colonization levels are reduced relative to the wild type but fully developed arbuscules are present in the cortex. In comparison with the wild type, colonization of ipd3 ipd3l is acutely sensitive to higher phosphate levels in the growth medium, with a disproportionate decrease in epidermal penetration, overall colonization, and symbiotic gene expression. When constitutively expressed in ipd3 ipd3l, an autoactive DOES NOT MAKE INFECTIONS 3 induces the expression of transcriptional regulators REDUCED ARBUSCULAR MYCORRHIZA 1 and REQUIRED for ARBUSCULE DEVELOPMENT 1, providing a possible avenue for arbuscule development in the absence of IPD3 and IPD3L. An increased sensitivity of ipd3 ipd3l to GA3 suggests an involvement of DELLA. The data reveal partial redundancy in the symbiosis signaling pathway, which may ensure robust signaling in low-phosphorus environments, while IPD3 and IPD3L maintain signaling in higher-phosphorus environments. The latter may buffer the pathway from short-term variation in phosphorus levels encountered by roots during growth in heterogeneous soil environments.

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