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Symbioses with beneficial microbes are widespread in plants, but these relationships must balance the energy invested by the plants with the nutrients acquired. Symbiosis with arbuscular mycorrhizal (AM) fungi occurs throughout land plants, but our understanding of the genes and signals that regulate colonization levels is limited, especially in non-legumes. Here, we demonstrate that in tomato, two CLV3/EMBRYO-SURROUNDING REGION (CLE) peptides, SlCLE10 and SlCLE11, act to suppress AM colonization of roots. Mutant studies and overexpression via hairy transformation indicate that SlCLE11 acts locally in the root to limit AM colonization. Indeed, SlCLE11 expression is strongly induced in AM-colonized roots, but SlCLE11 is not required for phosphate suppression of AM colonization. SlCLE11 requires the FIN gene that encodes an enzyme required for CLE peptide arabinosylation to suppress mycorrhizal colonization. However, SlCLE11 suppression of AM does not require two CLE receptors with roles in regulating AM colonization, SlFAB (CLAVATA1 ortholog) or SlCLV2. Indeed, multiple parallel pathways appear to suppress mycorrhizal colonization in tomato, as double mutant studies indicate that SlCLV2 and FIN have an additive influence on mycorrhizal colonization. SlCLE10 appears to play a more minor or redundant role, as cle10 mutants did not influence intraradical AM colonization. However, the fact that cle10 mutants had an elevated number of hyphopodia and that ectopic overexpression of SlCLE10 did suppress mycorrhizal colonization suggests that SlCLE10 may also play a role in suppressing AM colonization. Our findings show that CLE peptides regulate AM colonization in tomato and at least SlCLE11 likely requires arabinosylation for activity.

The mutualistic symbiosis between plants and arbuscular mycorrhizal (AM) fungi is based on a balanced nutrient exchange between both partners, with the plant achieving improved nutrition and stress tolerance. The symbiosis is finely-tuned according to plant's needs and surrounding conditions, usually through phytohormonal signaling. Thus, environmental conditions or stress factors modulating phytohormone signaling may influence the symbiosis. This study compares the colonization abilities of 2 AM fungal species, Funneliformis mosseae and Rhizophagus irregularis, independently or in combination, in tomato plants subjected to different stress conditions. These included salt stress and systemic defense activation by aboveground application of the defense-related hormones methyl jasmonate, abscisic acid and salicylic acid. The results show that root colonization by the two fungal species differs depending on the stress treatment. Nutrient and transcriptional analyses revealed that changes in colonization correlated with differential regulation of nutrient exchange, plant defensive responses, and symbiosis regulatory genes. Specifically, under salt stress R. irregularis colonization decreased, while F. mosseae colonization was promoted. These differential regulation of colonization under stress positively correlated with changes in the functionality of the symbiosis. Overall, the results support that the benefits provided by each AM fungi influence carbon reward and determines the control of root colonization by the host plant.

For the establishment of the Arbuscular Mycorrhiza (AM) symbiosis it is essential that epidermis and cortical cells from plant roots suffer a strong reorganization to allow the penetration of intracellular fungal hyphae. In the same manner, the new formation of a periarbuscular membrane and a symbiotic interface with specific compositions are required for a functional symbiosis. It is believed that the cytoskeleton of the plant host plays an essential role in these processes, particularly the microtubule (MT) cytoskeleton, as huge modifications have been observed in the MT array of root cells accompanying the establishment of the AM symbiosis. Recent research has established a link between microtubule rearrangements and arbuscule functioning. However, further research is required to elucidate the specific functions of MT cytoskeleton along the different stages of the arbuscule life cycle and to unravel the signals triggering these changes.

Aims: Many studies have reported beneficial effects of yeasts on the colonization and development of arbuscular mycorrhizae, thought a few studies have also shown neutral effects. All these studies have in common that the mechanism, by which yeasts and mycorrhizae interact, is little understood. Here, we explore how plant growth-promoting yeasts affect the colonization of tomato plants by beneficial mycorrhizal fungi. Methods: We tested the influence of the soil yeasts Candida saitoana, Tausonia pullulans, and Saccharomyces eubayanus on colonization of tomato roots by the mycorrhizal fungus Rhizophagus irregularis. We analyzed mycorrhizal parameters and the expression pattern of mycorrhiza-specific genes. In plants co-inoculated with S. eubayanus and R. irregularis, we measured the root accumulation pattern of jasmonic acid, oxo-phytodienoic acid, abscisic acid and salicylic acid, and the expression of genes related to plant hormone signaling and metabolism. Results: The three yeasts had distinct effects on mycorrhizal colonization: C. saitoana had no effect on mycorrhizal parameters, T. pullulans delayed mycorrhizal colonization at an early stage, and S. eubayanus slowed colonization down throughout the entire trial. In plants co-inoculated with S. eubayanus and R. irregularis, we observed a sustained increase in jasmonic acid and up-regulation of the JA biosynthesis related genes LOXD, OPR3, and AOS1. Conclusion: Co-inoculation with yeast affected mycorrhizal colonization and altered the expression pattern of mycorrhizal and plant defense-related genes. In particular, the yeast S. eubayanus modified plant defense hormones such as jasmonic acid, which is linked to mycorrhizal-induced resistance in tomato plants.

Plant-microorganism interactions at the rhizosphere level have a major impact on plant growth and plant tolerance and/or resistance to biotic and abiotic stresses. Of particular importance for forestry and agricultural systems is the cooperative and mutualistic interaction between plant roots and arbuscular mycorrhizal (AM) fungi from the phylum Glomeromycotina, since about 80% of terrestrial plant species can form AM symbiosis. The interaction is tightly regulated by both partners at the cellular, molecular and genetic levels, and it is highly dependent on environmental and biological variables. Recent studies have shown how fungal signals and their corresponding host plant receptor-mediated signalling regulate AM symbiosis. Host-generated symbiotic responses have been characterized and the molecular mechanisms enabling the regulation of fungal colonization and symbiosis functionality have been investigated. This review summarizes these and other recent relevant findings focusing on the molecular players and the signalling that regulate AM symbiosis. Future progress and knowledge about the underlying mechanisms for AM symbiosis regulation will be useful to facilitate agro-biotechnological procedures to improve AM colonization and/or efficiency.

Arbuscular mycorrhiza (AM) is a mutualistic symbiotic interaction between plant roots and AM fungi (AMF). This interaction is highly beneficial for plant growth, development and fitness, which has made AM symbiosis the focus of basic and applied research aimed at increasing plant productivity through sustainable agricultural practices. The creation of AM requires host root cells to undergo significant structural and functional modifications. Numerous studies of mycorrhizal plants have shown that extensive transcriptional changes are induced in the host during all stages of colonization. Advances have recently been made in identifying several plant transcription factors (TFs) that play a pivotal role in the transcriptional regulation of AM development, particularly those belonging to the GRAS TF family. There is now sufficient experimental evidence to suggest that GRAS TFs are capable to establish intra and interspecific interactions, forming a transcriptional regulatory complex that controls essential processes in the AM symbiosis. In this minireview, we discuss the integrative role of GRAS TFs in the regulation of the complex genetic re-programming determining AM symbiotic interactions. Particularly, research being done shows the relevance of GRAS TFs in the morphological and developmental changes required for the formation and turnover of arbuscules, the fungal structures where the bidirectional nutrient translocation occurs.