The role of the cell wall compartment in mutualistic symbioses of plants

Rich, Mélanie K.; Schorderet, Martine; Reinhardt, Didier

doi:10.3389/fpls.2014.00238

Cited by 61 publications

(51 citation statements)

References 163 publications

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“…In agreement with previous studies underlining an active role of plant cells in accommodating AM fungi (Hogekamp and Küster 2013;Rich et al 2014), a large number of proteins that display an increased abundance in the PM fraction of mycorrhizal roots were related to protein turnover and cell wall construction (Table 1). Among the candidate proteins mediating cell wall loosening in the cells accommodating fungal structures (Balestrini and Bonfante 2014), the secreted enzymes glucosidase II and xylose isomerase were only detected in symbiotic roots (Table 1).…”

Section: Am-responsive Proteins As Related To Interface Biogenesis Ansupporting

confidence: 91%

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

Aloui¹,

Recorbet²,

Lemaître‐Guillier³

et al. 2017

Mycorrhiza

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In arbuscular mycorrhizal (AM) roots, the plasma membrane (PM) of the host plant is involved in all developmental stages of the symbiotic interaction, from initial recognition to intracellular accommodation of intra-radical hyphae and arbuscules. Although the role of the PM as the agent for cellular morphogenesis and nutrient exchange is especially accentuated in endosymbiosis, very little is known regarding the PM protein composition of mycorrhizal roots. To obtain a global overview at the proteome level of the host PM proteins as modified by symbiosis, we performed a comparative protein profiling of PM fractions from Medicago truncatula roots either inoculated or not with the AM fungus Rhizophagus irregularis. PM proteins were isolated from root microsomes using an optimized discontinuous sucrose gradient; their subsequent analysis by liquid chromatography followed by mass spectrometry (MS) identified 674 proteins. Cross-species sequence homology searches combined with MS-based quantification clearly confirmed enrichment in PM-associated proteins and depletion of major microsomal contaminants. Changes in protein amounts between the PM proteomes of mycorrhizal and non-mycorrhizal roots were monitored further by spectral counting. This workflow identified a set of 82 mycorrhiza-responsive proteins that provided insights into the plant PM response to mycorrhizal symbiosis. Among them, the association of one third of the mycorrhiza-responsive proteins with detergent-resistant membranes pointed at partitioning to PM microdomains. The PM-associated proteins responsive to mycorrhization also supported host plant control of sugar uptake to limit fungal colonization, and lipid turnover events in the PM fraction of symbiotic roots. Because of the depletion upon symbiosis of proteins mediating the replacement of phospholipids by phosphorus-free lipids in the plasmalemma, we propose a role of phosphate nutrition in the PM composition of mycorrhizal roots.

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Section: Am-responsive Proteins As Related To Interface Biogenesis Ansupporting

confidence: 91%

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

Aloui¹,

Recorbet²,

Lemaître‐Guillier³

et al. 2017

Mycorrhiza

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“…The development of this specialized perifungal compartment is prefigured by the formation of the transient cytoplasmic PPA, which links the migrating cell nucleus to the site of AM fungal attachment via the hyphopodium (Genre et al, 2005(Genre et al, , 2008. In addition, Rich et al (2014) have recently proposed that host cell-driven modifications to the cell wall at the site of hyphopodium contact would precede Rhizophagus irregularis entry into the Petunia hybrida root. Thus, by analogy with the creation of the IT precursor within the enclosed space formed by RH curling, it is possible that hyphopodium attachment also creates an enclosed environment within which host secretion and associated wall remodeling generates a specialized compartment, thus allowing the AM hyphae to cross the host cell wall.…”

Section: Plant-microsymbiont Signal Exchange During the Two Stages Ofmentioning

confidence: 99%

Remodeling of the Infection Chamber before Infection Thread Formation Reveals a Two-Step Mechanism for Rhizobial Entry into the Host Legume Root Hair

et al. 2015

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“…The highly branched arbuscules appear ideally suited for lipid absorption, in particular, because the symbiotic interface is extremely narrow and essentially comprises only a thin fungal cell wall between the membranes of the two partners [71]. The periarbuscular space is acidified by H + [ 2 0 8 _ T D $ D I F F ] -ATPases which energize mineral nutrient uptake by the plant [72][73][74][75].…”

Section: The Missing Link: Lipid Uptake By the Fungusmentioning

confidence: 99%

Diet of Arbuscular Mycorrhizal Fungi: Bread and Butter?

Rich

Nouri

Courty

et al. 2017

Trends in Plant Science

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152

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Most plants entertain mutualistic interactions known as arbuscular mycorrhiza (AM) with soil fungi (Glomeromycota) which provide them with mineral nutrients in exchange for reduced carbon from the plant. Mycorrhizal roots represent strong carbon sinks in which hexoses are transferred from the plant host to the fungus. However, most of the carbon in AM fungi is stored in the form of lipids. The absence of the type I fatty acid synthase (FAS-I) complex from the AM fungal model species Rhizophagus irregularis suggests that lipids may also have a role in nutrition of the fungal partner. This hypothesis is supported by the concerted induction of host genes involved in lipid metabolism. We explore the possible roles of lipids in the light of recent literature on AM symbiosis. Carbohydrates in AM Fungal NutritionAM fungi are strictly biotrophic, in other words they depend on their host to complete their life cycle. Although the basis of biotrophy is poorly understood, it has been suggested that it is due to the dependency of AM fungi on some essential nutritional factor(s) from the host [1]. Direct uptake measurements revealed that intraradical mycelium (IRM) can take up carbohydrates, whereas extraradical mycelium (ERM) did not acquire significant amounts of carbohydrates [2,3]. Perhaps this is because AM fungal genes involved in nutrient uptake are expressed only in the host, which would explain their biotrophy. Tracer studies on mycorrhizal roots, and respirometric analysis on isolated intraradical hyphae have established glucose as a central substrate for AM fungi [3][4][5], and indeed a monosaccharide transporter has been identified in the fungal partner [6]. Mycorrhizal roots represent strong carbon sinks [2,4,7], suggesting that they attract sucrose from photosynthetic source tissues. Sucrose is thought to be cleaved in the vicinity of the fungus by invertases and sucrose synthase [8], resulting in monosaccharides (glucose and fructose) that are released to the fungus and taken up by its IRM [5,6]. However, in the fungal storage compartments -the spores and the vesicles -carbon is stored primarily in the form of lipids, with minor amounts of the glucose polymer glycogen. We discuss here salient issues relating to carbohydrate and lipid metabolism in AM fungi and their significance for fungal nutrition during symbiosis. Lipid Metabolism in AM Fungi -Open Questions and SurprisesAlthough the aforementioned carbon fluxes in AM fungi have been firmly established, several questions remain open. AM fungi store and transport most of their carbon in the form of lipids [9][10][11][12]. However, AM fungi cannot produce the basic fatty acid (FA) palmitate (C16) in the absence of their host (as shown in two distantly related species, Rhizophagus irregularis and Gigaspora rosea), while FA elongation and desaturation can occur independently of the plant [13]. This and similar results suggested that AM fungi can only synthesize C16 in the IRM [3,13]. Taken together, the available evidence suggests that AM fungi take up sugars (...

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The role of the cell wall compartment in mutualistic symbioses of plants

Cited by 61 publications

References 163 publications

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

Remodeling of the Infection Chamber before Infection Thread Formation Reveals a Two-Step Mechanism for Rhizobial Entry into the Host Legume Root Hair

Diet of Arbuscular Mycorrhizal Fungi: Bread and Butter?

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