Arbuscular mycorrhizal (AM) fungi establish probably one of the oldest mutualistic relationships with the roots of most plants on earth. The wide distribution of these fungi in almost all soil ecotypes and the broad range of host plant species demonstrate their strong plasticity to cope with various environmental conditions. AM fungi elaborate fine-tuned molecular interactions with plants that determine their spread within root cortical tissues. Interactions with endomycorrhizal fungi can bring various benefits to plants, such as improved nutritional status, higher photosynthesis, protection against biotic and abiotic stresses based on regulation of many physiological processes which participate in promoting plant performances. In turn, host plants provide a specific habitat as physical support and a favorable metabolic frame, allowing uptake and assimilation of compounds required for the life cycle completion of these obligate biotrophic fungi. The search for formal and direct evidences of fungal energetic needs raised strong motivated projects since decades, but the impossibility to produce AM fungi under axenic conditions remains a deep enigma and still feeds numerous debates. Here, we review and discuss the initial favorable and non-favorable metabolic plant context that may fate the mycorrhizal behavior, with a focus on hormone interplays and their links with mitochondrial respiration, carbon partitioning and plant defense system, structured according to the action of phosphorus as a main limiting factor for mycorrhizal symbiosis. Then, we provide with models and discuss their significances to propose metabolic targets that could allow to develop innovations for the production and application of AM fungal inocula.

Arbuscular mycorrhizal fungi (AMF) are crucial components of fertile soils, able to provide several ecosystem services for crop production. Current economic, social and legislative contexts should drive the so-called “second green revolution” by better exploiting these beneficial microorganisms. Many challenges still need to be overcome to better understand the mycorrhizal symbiosis, among which (i) the biotrophic nature of AMF, constraining their production, while (ii) phosphate acts as a limiting factor for the optimal mycorrhizal inoculum application and effectiveness. Organism fitness and adaptation to the changing environment can be driven by the modulation of mitochondrial respiratory chain, strongly connected to the phosphorus processing. Nevertheless, the role of the respiratory function in mycorrhiza remains largely unexplored. We hypothesized that the two mitochondrial respiratory chain components, alternative oxidase (AOX) and cytochrome oxidase (COX), are involved in specific mycorrhizal behavior. For this, a complex approach was developed. At the pre-symbiotic phase (axenic conditions), we studied phenotypic responses of Rhizoglomus irregulare spores with two AOX and COX inhibitors [respectively, salicylhydroxamic acid (SHAM) and potassium cyanide (KCN)] and two growth regulators (abscisic acid – ABA and gibberellic acid – Ga3). At the symbiotic phase, we analyzed phenotypic and transcriptomic (genes involved in respiration, transport, and fermentation) responses in Solanum tuberosum/Rhizoglomus irregulare biosystem (glasshouse conditions): we monitored the effects driven by ABA, and explored the modulations induced by SHAM and KCN under five phosphorus concentrations. KCN and SHAM inhibited in vitro spore germination while ABA and Ga3 induced differential spore germination and hyphal patterns. ABA promoted mycorrhizal colonization, strong arbuscule intensity and positive mycorrhizal growth dependency (MGD). In ABA treated plants, R. irregulare induced down-regulation of StAOX gene isoforms and up-regulation of genes involved in plant COX pathway. In all phosphorus (P) concentrations, blocking AOX or COX induced opposite mycorrhizal patterns in planta: KCN induced higher Arum-type arbuscule density, positive MGD but lower root colonization compared to SHAM, which favored Paris-type formation and negative MGD. Following our results and current state-of-the-art knowledge, we discuss metabolic functions linked to respiration that may occur within mycorrhizal behavior. We highlight potential connections between AOX pathways and fermentation, and we propose new research and mycorrhizal application perspectives.

Under the field conditions crop plants interact with diverse microorganisms. These include beneficial (symbiotic) and phytopathogenic microorganisms, which jointly affect growth and productivity of the plants. In last decades, production of potato (Solanum tuberosum L.) suffers from increased incidence of potato virus Y (PVY), which is one of most important potato pests. Arbuscular mycorrhizal fungi (AMF) are common symbionts of potato, however the impact of mycorrhizal symbiosis on the progression of PVY-induced disease is scarcely known. Therefore, in the present study we investigated the effect of joint PVY infection and mycorrhizal colonization by Rhizophagus irregularis on growth traits of the host potato plant (cv. Pirol). The tested PVY isolate belonged to N-Wilga strain group, which is considered to be predominant in Europe and many other parts of the world. The viral particles were concentrated in the leaves, but decreased the root growth. Furthermore, the infection with PVY evoked prolonged oxidative stress reflected by increased level of endogenous H 2 O 2. AMF alleviated oxidative stress in PVY-infected host plants by a substantial decrease in the level of shoot-and rootderived H 2 O 2 , but still caused asymptomatic growth depression. It was assumed that mycorrhizal symbiosis of potato might mask infection by PVY in field observations.

Solanaceae, comprising meaningful crops (as potato, tomato, pepper, eggplant, and tobacco), can benefit from a symbiosis with arbuscular mycorrhizal fungi (AMF), which improve plant fitness and support plant defense against pathogens. Currently, those crops are likely the most impacted by Potato virus Y (PVY). Unfortunately, the effects of AM symbiosis on the severity of disease induced by PVY in solanaceous crops remain uncertain, partly because the interplay between AMF and PVY is poorly characterized. To shed some light on this issue, available studies on interactions in tripartite association between the host plant, its fungal colonizer, and viral pathogen were analyzed and discussed. Although the best-documented PVY transmission pathway is aphid-dependent, PVY infections are also observed in the absence of insect vector. We hypothesize the existence of an additional pathway for virus transmission involving AMF, in which the common mycorrhizal network (CMN) may act as a potential bridge. Therefore, we reviewed (1) the significance of AM colonization for the course of disease, (2) the potential of AMF networks to act as vectors for PVY, and (3) the consequences for crop breeding and production of AM biofertilizers.

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