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While arbuscular mycorrhizal (AM) fungi are known for providing host plants with improved drought tolerance, we know very little about the fungal response to drought in the context of the fungal-plant relationship. In this study, we evaluated the drought responses of the host and symbiont, using the fungus Rhizophagus irregularis with carrot ( Daucus carota ) as a plant model. Carrots inoculated with spores of R. irregularis DAOM 197198 were grown in a greenhouse. During taproot development, carrots were exposed to a 10-day water restriction. Compared with well-watered conditions, drought caused diminished photosynthetic activity and reduced plant growth in carrot with and without AM fungi. Droughted carrots had lower root colonization. For R. irregularis , 93% of 826 differentially expressed genes (DEGs) were upregulated during drought, including phosphate transporters, several predicted transport proteins of potassium, and the aquaporin RiAQPF2 . In contrast, 78% of 2,486 DEGs in AM carrot were downregulated during drought, including the symbiosis-specific genes FatM , RAM2 , and STR , which are implicated in lipid transfer from the host to the fungus and were upregulated exclusively in AM carrot during well-watered conditions. Overall, this study provides insight into the drought response of an AM fungus in relation to its host; the expression of genes related to symbiosis and nutrient exchange were downregulated in carrot but upregulated in the fungus. This study reveals that carrot and R. irregularis exhibit contrast in their regulation of gene expression during drought, with carrot reducing its apparent investment in symbiosis and the fungus increasing its apparent symbiotic efforts. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license., Competing Interests: J.-M. Ané provides consulting services to Valent BioSciences. The other authors declare no conflict of interest.

Plant-growth-promoting bacteria (PGPB) stimulate plant growth through diverse mechanisms. In addition to biological nitrogen fixation, diazotrophic PGPB can improve nutrient uptake efficiency from the soil, produce and release phytohormones to the host, and confer resistance against pathogens. The genetic determinants that drive the success of biological nitrogen fixation in nonlegume plants are understudied. These determinants include recognition and signaling pathways, bacterial colonization, and genotype specificity between host and bacteria. This review presents recent discoveries of how nitrogen-fixing PGPB interact with cereals and promote plant growth. We suggest adopting an experimental model system, such as the Setaria -diazotrophic bacteria association, as a reliable way to better understand the associated mechanisms and, ultimately, increase the use of PGPB inoculants for sustainable agriculture.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Legumes form endosymbiotic associations with nitrogen-fixing bacteria and arbuscular mycorrhizal (AM) fungi which facilitate nutrient uptake. Both symbiotic interactions require a molecular signal exchange between the plant and the symbiont, and this involves a conserved symbiosis (Sym) signaling pathway. In order to identify plant genes required for intracellular accommodation of nitrogen-fixing bacteria and AM fungi, we characterized Medicago truncatula symbiotic mutants defective for rhizobial infection of nodule cells and colonization of root cells by AM hyphae. Here, we describe mutants impaired in the interacting protein of DMI3 (IPD3) gene, which has been identified earlier as an interacting partner of the calcium/calmodulin-dependent protein, a member of the Sym pathway. The ipd3 mutants are impaired in both rhizobial and mycorrhizal colonization and we show that IPD3 is necessary for appropriate Nod-factor-induced gene expression. This indicates that IPD3 is a member of the common Sym pathway. We observed differences in the severity of ipd3 mutants that appear to be the result of the genetic background. This supports the hypothesis that IPD3 function is partially redundant and, thus, additional genetic components must exist that have analogous functions to IPD3. This explains why mutations in an essential component of the Sym pathway have defects at late stages of the symbiotic interactions.

Arbuscular mycorrhizal (AM) fungi stimulate root development and induce expression of mycorrhization-specific genes in both eudicots and monocots. Diffusible factors released by AM fungi have been shown to elicit similar responses in Medicago truncatula. Colonization of roots by AM fungi is inhibited by ethylene. We compared the effects of germinating spore exudates (GSE) from Glomus intraradices in monocots and in eudicots, their genetic control, and their regulation by ethylene. GSE modify root architecture and induce symbiotic gene expression in both monocots and eudicots. The genetic regulation of root architecture and gene expression was analyzed using M. truncatula and rice symbiotic mutants. These responses are dependent on the common symbiotic pathway as well as another uncharacterized pathway. Significant differences between monocots and eudicots were observed in the genetic control of plant responses to GSE. However, ethylene inhibits GSE-induced symbiotic gene expression and root development in both groups. Our results indicate that GSE signaling shares similarities and differences in monocots versus eudicots, that only a subset of AM signaling pathways has been co-opted in legumes for the establishment of root nodulation with rhizobia, and that regulation of these pathways by ethylene is a feature conserved across higher land plants.

Many higher plants establish symbiotic relationships with arbuscular mycorrhizal (AM) fungi that improve their ability to acquire nutrients from the soil. In addition to establishing AM symbiosis, legumes also enter into a nitrogen-fixing symbiosis with bacteria known as rhizobia that results in the formation of root nodules. Several genes involved in the perception and transduction of bacterial symbiotic signals named "Nod factors" have been cloned recently in model legumes through forward genetic approaches. Among them, DMI3 (Doesn't Make Infections 3) is a calcium- and calmodulin-dependent kinase required for the establishment of both nodulation and AM symbiosis. We have identified, by a yeast two-hybrid system, a novel protein interacting with DMI3 named IPD3 (Interacting Protein of DMI3). IPD3 is predicted to interact with DMI3 through a C-terminal coiled-coil domain. Chimeric IPD3::GFP is localized to the nucleus of transformed Medicago truncatula root cells, in which split yellow fluorescent protein assays suggest that IPD3 and DMI3 physically interact in Nicotiana benthamiana. Like DMI3, IPD3 is extremely well conserved among the angiosperms and is absent from Arabidopsis. Despite this high level of conservation, none of the homologous proteins have a demonstrated biological or biochemical function. This work provides the first evidence of the involvement of IPD3 in a nuclear interaction with DMI3.

The DMI1, DMI2, and DMI3 genes of Medicago truncatula, which are required for both nodulation and mycorrhization, control early steps of Nod factor signal transduction. Here, we have used diverse approaches to pave the way for the map-based cloning of these genes. Molecular amplification fragment length polymorphism markers linked to the three genes were identified by bulked segregant analysis. Integration of these markers into the general genetic map of M. truncatula revealed that DMI1, DMI2, and DMI3 are located on linkage groups 2, 5, and 8, respectively. Cytogenetic studies using fluorescent in situ hybridization (FISH) on mitotic and pachytene chromosomes confirmed the location of DMI1, DMI2, and DMI3 on chromosomes 2, 5, and 8. FISH-pachytene studies revealed that the three genes are in euchromatic regions of the genome, with a ratio of genetic to cytogenetic distances between 0.8 and 1.6 cM per microm in the DMI1, DMI2, and DMI3 regions. Through grafting experiments, we showed that the genetic control of the dmi1, dmi2, and dmi3 nodulation phenotypes is determined at the root level. This means that mutants can be transformed by Agrobacterium rhizogenes to accelerate the complementation step of map-based cloning projects for DMI1, DMI2, and DMI3.