Legumes can enter into symbiotic relationships with both nitrogen-fixing bacteria (rhizobia) and mycorrhizal fungi. Nodulation by rhizobia results from a signal transduction pathway induced in legume roots by rhizobial Nod factors. DMI3 ,a Medicago truncatula gene that acts immediately downstream of calcium spiking in this signaling pathway and is required for both nodulation and mycorrhizal infection, has high sequence similarity to genes encoding calcium and calmodulin-dependent protein kinases (CCaMKs). This indicates that calcium spiking is likely an essential component of the signaling cascade leading to nodule development and mycorrhizal infection, and sheds light on the biological role of plant CCaMKs.

Dependent Protein Kinase Required for Bacterial and Fungal Symbioses

Mycorrhizas are among the most important biological interkingdom interactions, as they involve ~340,000 land plants and ~50,000 taxa of soil fungi. In these mutually beneficial interactions, fungi receive photosynthesis-derived carbon and provide the host plant with mineral nutrients such as phosphorus and nitrogen in exchange. More than 150 years of research on mycorrhizas has raised awareness of their biology, biodiversity and ecological impact. In this Review, we focus on recent phylogenomic, molecular and cell biology studies to present the current state of knowledge of the origin of mycorrhizal fungi and the evolutionary history of their relationship with land plants. As mycorrhizas feature a variety of phenotypes, depending on partner taxonomy, physiology and cellular interactions, we explore similarities and differences between mycorrhizal types. During evolution, mycorrhizal fungi have refined their biotrophic capabilities to take advantage of their hosts as food sources and protective niches, while plants have developed multiple strategies to accommodate diverse fungal symbionts. Intimate associations with pervasive ecological success have originated at the crossroads between these two evolutionary pathways. Our understanding of the biological processes underlying these symbioses, where fungi act as biofertilizers and bioprotectors, provides the tools to design biotechnological applications addressing environmental and agricultural challenges.

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Unique and common traits in mycorrhizal symbioses.

Arbuscular mycorrhizal (AM) fungi are essential elements of soil fertility, plant nutrition and productivity, facilitating soil mineral nutrient uptake. Helianthus annuus is a non-model, widely cultivated species. Here we used an RNA-seq approach for evaluating gene expression variation at early and late stages of mycorrhizal establishment in sunflower roots colonized by the arbuscular fungus Rhizoglomus irregulare. mRNA was isolated from roots of plantlets at 4 and 16 days after inoculation with the fungus. cDNA libraries were built and sequenced with Illumina technology. Differential expression analysis was performed between control and inoculated plants. Overall 726 differentially expressed genes (DEGs) between inoculated and control plants were retrieved. The number of up-regulated DEGs greatly exceeded the number of down-regulated DEGs and this difference increased in later stages of colonization. Several DEGs were specifically involved in known mycorrhizal processes, such as membrane transport, cell wall shaping, and other. We also found previously unidentified mycorrhizal-induced transcripts. The most important DEGs were carefully described in order to hypothesize their roles in AM symbiosis. Our data add a valuable contribution for deciphering biological processes related to beneficial fungi and plant symbiosis, adding an Asteraceae, non-model species for future comparative functional genomics studies.

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Transcriptome changes induced by arbuscular mycorrhizal fungi in sunflower (Helianthus annuus L.) roots

Contents Summary 1031 I. Introduction 1031 II. Interkingdom communication enabling symbiosis 1032 III. Nutritional and regulatory roles for key metabolites in the AM symbiosis 1035 IV. The plant-fungus genotype combination determines the outcome of the symbiosis 1039 V. Perspectives 1039 Acknowledgements 1041 References 1041 SUMMARY: The evolutionary and ecological success of the arbuscular mycorrhizal (AM) symbiosis relies on an efficient and multifactorial communication system for partner recognition, and on a fine-tuned and reciprocal metabolic regulation of each symbiont to reach an optimal functional integration. Besides strigolactones, N-acetylglucosamine-derivatives released by the plant were recently suggested to trigger fungal reprogramming at the pre-contact stage. Remarkably, N-acetylglucosamine-based diffusible molecules also are symbiotic signals produced by AM fungi (AMF) and clues on the mechanisms of their perception by the plant are emerging. AMF genomes and transcriptomes contain a battery of putative effector genes that may have conserved and AMF- or host plant-specific functions. Nutrient exchange is the key feature of AM symbiosis. A mechanism of phosphate transport inside fungal hyphae has been suggested, and first insights into the regulatory mechanisms of root colonization in accordance with nutrient transfer and status were obtained. The recent discovery of the dependency of AMF on fatty acid transfer from the host has offered a convincing explanation for their obligate biotrophism. Novel studies highlighted the importance of plant and fungal genotypes for the outcome of the symbiosis. These findings open new perspectives for fundamental research and application of AMF in agriculture.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.15230

Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis

Phytohormones play central roles in boosting plant tolerance to environmental stresses, which negatively affect plant productivity and threaten future food security. Strigolactones (SLs), a class of carotenoid-derived phytohormones, were initially discovered as an "ecological signal" for parasitic seed germination and establishment of symbiotic relationship between plants and beneficial microbes. Subsequent characterizations have described their functional roles in various developmental processes, including root development, shoot branching, reproductive development, and leaf senescence. SLs have recently drawn much attention due to their essential roles in the regulation of various physiological and molecular processes during the adaptation of plants to abiotic stresses. Reports suggest that the production of SLs in plants is strictly regulated and dependent on the type of stresses that plants confront at various stages of development. Recently, evidence for crosstalk between SLs and other phytohormones, such as abscisic acid, in responses to abiotic stresses suggests that SLs actively participate within regulatory networks of plant stress adaptation that are governed by phytohormones. Moreover, the prospective roles of SLs in the management of plant growth and development under adverse environmental conditions have been suggested. In this review, we provide a comprehensive discussion pertaining to SL-mediated plant responses and adaptation to abiotic stresses.

Strigolactones in plant adaptation to abiotic stresses: An emerging avenue of plant research.

Arbuscular mycorrhiza (AM) is a mutualistic association between most plant species and the ancient fungal phylum Glomeromycota in roots, and it plays a key role in a plant's nutrient uptake from the soil. Roots synthesize strigolactones (SLs), derivatives of carotenoids, and exude them to induce energy metabolism and hyphal branching of AM fungi. Despite the well-documented roles of SLs in the pre-symbiotic phase, little is known about the role of SLs in the process of root colonization. Here we show that the expansion of root colonization is suppressed in the mutants of rice (Oryza sativa) SL biosynthesis genes, carotenoid cleavage dioxygenase D10 and more severely in D17. Interestingly, most of the colonization process is normal, i.e. AM fungal hyphae approach the roots and cling around them, and epidermal penetration, arbuscule size, arbuscule number per hyphopodium and metabolic activity of the intraradical mycelium are not affected in d10 and d17 mutants. In contrast, hyphopodium formation is severely attenuated. Our observations establish the requirement for SL biosynthesis genes for efficient hyphopodium formation, suggesting that SLs are required in this process. Efficient hyphopodium formation is required for the punctual internalization of hyphae into roots and maintaining the expansion of colonization.

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Strigolactone Biosynthesis Genes of Rice are Required for the Punctual Entry of Arbuscular Mycorrhizal Fungi into the Roots.

The development of arbuscular mycorrhiza (AM) is strongly suppressed under high-phosphate (Pi) conditions. To investigate AM fungal responses during the suppression of AM by high Pi, we performed an RNA-seq analysis of Rhizophagus irregularis colonizing Lotus japonicus roots at different levels of Pi (20, 100, 300, and 500 μM). AM fungal colonization decreased markedly under high-Pi conditions. In total, 163 fungal genes were differentially expressed among the four Pi treatments. Among these genes, a cell cycle-regulatory gene, cyclin-dependent kinase CDK1, and several DNA replication- and mitosis-related genes were repressed under high-Pi conditions. More than 20 genes encoding secreted proteins were also downregulated by high-Pi conditions, including the strigolactone-induced putative secreted protein 1 gene that enhances AM fungal colonization. In contrast, the expression of genes related to aerobic respiration and transport in R. irregularis were largely unaffected. Our data suggest that high Pi suppresses the expression of genes associated with fungal cell cycle progression or that encode secreted proteins that may be required for intercellular hyphal growth and arbuscule formation. However, high Pi has little effect on the transcriptional regulation of the primary metabolism or transport in preformed fungal structures.

Transcriptional profiling of arbuscular mycorrhizal roots exposed to high levels of phosphate reveals the repression of cell cycle-related genes and secreted protein genes in Rhizophagus irregularis

Arbuscular mycorrhizal (AM) fungi form symbiotic associations with diverse plant species. The AM fungi enhance mineral uptake from the soil, which benefits the growth of the host plants. Previous microarray and RNA-seq analyses have identified a large number of AM-responsive plant genes. However, little is known whether the gene expression profile of mycorrhiza is different among genetically distant plant species. The aim of this study was to assess the conservation and divergence of AM-responsive genes between two different hosts, Solanum lycopersicum L. and Lotus japonicus L., during AM development using RNA-seq data. In each host plant, gene expression was compared between AM roots and non-mycorrhizal (NM) roots. Potential orthologs of AM-responsible genes between S. lycopersicum and L. japonicus were identified with reciprocal BLAST searches. Only one quarter to one third of the AM-inducible genes in each plant species were co-upregulated in both species. The co-upregulated genes included thos...

https://www.tandfonline.com/doi/pdf/10.1080/00380768.2017.1280378

Comparative transcriptome analysis between Solanum lycopersicum L. and Lotus japonicus L. during arbuscular mycorrhizal development

Plants have evolved diverse strategies for foraging, e.g., mycorrhizae, modification of root system architecture, and secretion of phosphatase. Despite extensive molecular/physiological studies on individual strategies under laboratory/greenhouse conditions, there is little information about how plants orchestrate these strategies in the field. We hypothesized that individual strategies are independently driven by corresponding genetic modules in response to deficiency/unbalance in nutrients. Roots colonized by mycorrhizal fungi, leaves, and root-zone soils were collected from 251 maize plants grown across the United States Corn Belt and Japan, which provided a large gradient of soil characteristics/agricultural practice and thus gene expression for foraging. RNA was extracted from the roots, sequenced, and subjected to gene coexpression network analysis. Nineteen genetic modules were defined and functionally characterized, from which three genetic modules, mycorrhiza formation, phosphate starvation response (PSR), and root development, were selected as those directly involved in foraging. The mycorrhizal module consists of genes responsible for mycorrhiza formation and was upregulated by both phosphorus and nitrogen deficiencies. The PSR module that consists of genes encoding phosphate transporter, secreted acid phosphatase, and enzymes involved in internal-phosphate recycling was regulated independent of the mycorrhizal module and strongly upregulated by phosphorus deficiency relative to nitrogen. The root development module that consists of regulatory genes for root development and cellulose biogenesis was upregulated by phosphorus and nitrogen enrichment. The expression of this module was negatively correlated with that of the mycorrhizal module, suggesting that root development is intrinsically an opposite strategy of mycorrhizae. Our approach provides new insights into understanding plant foraging strategies in complex environments at the molecular level.

Yusaku Sugimura

Papers

Strigolactone Biosynthesis Genes of Rice are Required for the Punctual Entry of Arbuscular Mycorrhizal Fungi into the Roots.

Transcriptional profiling of arbuscular mycorrhizal roots exposed to high levels of phosphate reveals the repression of cell cycle-related genes and secreted protein genes in Rhizophagus irregularis

Comparative transcriptome analysis between Solanum lycopersicum L. and Lotus japonicus L. during arbuscular mycorrhizal development

Plant Foraging Strategies Driven by Distinct Genetic Modules: Cross-Ecosystem Transcriptomics Approach