Unraveling the Initial Plant Hormone Signaling, Metabolic Mechanisms and Plant Defense Triggering the Endomycorrhizal Symbiosis Behavior

Abstract

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.

Keywords: carbon partitioning; mycorrhizal fungi; phosphorus; physiology; phytohormones; plant defense; plant priming; signaling.

FIGURE 1

Overview of the metabolic crosstalk directions discussed in this review. Solid lines indicate state of the art according to the bibliographic survey. Dashed lines indicate perspectives based on interpretation of the metabolic crosstalk. P, phosphorus; H, plant hormone; E, energetic system (carbon partitioning, respiration, and REDOX potential); AMF, arbuscular mycorrhizal fungi.

FIGURE 2

Overview of the methodologies used and the fungal phenotypic parameters analyzed to investigate hormone response in endomycorrhizal symbiosis. The percentage of publication studying each hormone (A) indicates that SL and ET are likely the most studied while SA and BR are the least investigated. Most of assays were conducted in planta (in greenhouse or growth chambers), (B) but few works were conducted under contrasting P levels (C). The use of mutant plants is the most common method, but pharmacological approaches were also done with hormones (mostly by application on soil/root, in presence of mycorrhizal propagules) and inhibitors (D). Less studies were conducted under monoxenic conditions or by hormonal plant pretreatment (which allow to limit direct interaction between hormones and AM inoculum) (D). Hormone deficient mutants are most often used while hypersensitive mutant plants are less exploited (E). Then, several AM phenotypic parameters were investigated, mostly root colonization and arbuscule abundance, but less data are available regarding other structures, in particular spore germination, extraradical hyphal growth and sporulation (F). ABA, abscisic acid; JA, jasmonate; GA, gibberellins; SA, salicylic acid; SL, strigolactones; ET, ethylene; CK, cytokinins; IAA, auxins; BR, brassinosteroids. Note that more than one phytohormone was studied in some publications, creating redundancies which were counted to calculate the percentages presented in the figures (see Supplementary Material).

FIGURE 3

Plant metabolic orientation of hormone interplay, carbon partitioning and responses on mycorrhizal development under low available P. Box and arrow color indicate repression (red), or promotion (green). Orange boxes and black arrows are used for uncertain conditions. Based on the literature survey, mycorrhizal colonization is enhanced under low available P which goes together with the action of AM-promoting hormones (such as ABA, SL, and JA). This hormonal interplay is connected to a favorable metabolic frame which involves lower phytosynthetic activity, higher translocation of photosynthetats from shoots to roots, accumulation of sugars (reduced glycolysis flow and enhanced lipid oxidation), enhanced plant fermentation activity, cytosolic reductive potential (elevated NADH pool), electron partitioning which is orientated toward the alternative oxidase pathway, reduced ATP formation and ISR implementation. Root exudation of several sugars, aminoacids, some carboxylic acids and hormones (such as SL) participate to the molecular dialog with mycorrhizal fungi present in the rhizosphere. This can support physical contact with the root by stimulating hyphal branching and to induce plant responses by promoting Myc factor release from germative spore exudates. It is questioned if this metabolic flux is accompanied by lower oxygen consumption by plant cells, which may become more available for the fungus (as aerobic organism) under low P. ABA, abscisic acid; JA, jasmonate; GA, gibberellins; SA, salicylic acid; SL, strigolactones; ET, ethylene; CK, cytokinins; IAA, auxins; BR, brassinosteroids; PR, pathogenesis related protein; ISR, induced systemic response; SAR, systemic acquired resistance; AOX, alternative oxidase; COX, cytochrome oxidase; CytC, cytochrome C; TCA, Krebs cycle; NADPH ox., NADPH oxydase; polyamine ox., polyamine oxydase; GSE, germinative spore exudate; G3P, Glycerol 3-phosphate.

FIGURE 4

Plant metabolic orientation of hormone interplay, carbon partitioning and responses on mycorrhizal development under high available P. Box and arrow color indicate repression (red), or promotion (green). Orange boxes and black arrows are used for uncertain conditions. Based on the literature survey, high available P affects mycorrhizal performances mainly due to the activity of mycorrhiza-inhibiting hormones (such as GA, SA, and ET), and in which SAR is potentialized. This goes together with a non-favorable metabolic frame which seems connected to an enhanced photosynthesis activity, lower translocation of photosynthetats from shoots to roots, a continuous flow of sugars processed via glycolysis, lipogenesis, and TCA, but also reduced fermentation activity and higher oxidative potential (reduced NADH⁺H⁺ cytosolic pool). In this system, lower free amounts of compounds (sugars, aminoacids, SL, and carboxylate acids) are released in the root exudate, thus reducing possible molecular dialog between AM fungi and plant root. In addition, high P favors electron partitioning toward the plant COX pathway, thus participating to ATP formation. It is questioned if this metabolic flux is accompanied by higher oxygen consumption by plant cells, which may become less available for the fungus (as aerobic organism) under high P. ABA, abscisic acid; JA, jasmonate; GA, gibberellins; SA, salicylic acid; SL, strigolactones; ET, ethylene; CK, cytokinins; IAA, auxins; BR, brassinosteroids; PR, pathogenesis related protein; ISR, induced systemic response; SAR, systemic acquired resistance; AOX, alternative oxidase; COX, cytochrome oxidase; CytC, cytochrome C; TCA, Krebs cycle; NADPH ox., NADPH oxydase; polyamine ox., polyamine oxydase; GSE, germinative spore exudate; G3P, Glycerol 3-phosphate.

FIGURE 5

Theoretical scheme of the oligosaccharides signaling on alternative oxydase pathway, via ABA-dependant and independent regulation.