Nutrient Exchange and Regulation in Arbuscular Mycorrhizal Symbiosis

Wang, Wanxiao; Shi, Jincai; Xie, Qi; Jiang, Yan‐Yi; Yu, Nan; Wang, Ertao

doi:10.1016/j.molp.2017.07.012

Cited by 365 publications

(279 citation statements)

References 140 publications

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“…Recently it has been shown that fatty acids are transported from the host to the fungus, likely serving as a major nutritive carbon source Keymer et al, 2017;Luginbuehl et al, 2017). However, previously it has been shown that the host also provides sugars as carbon source, although the mechanism by which sugars are transported to the fungus is unclear (Rich et al, 2017;Roth & Paszkowski, 2017;Wang et al, 2017). Therefore, in this study we investigated the role of SWEET sugar transporters.…”

Section: Introductionmentioning

confidence: 99%

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

Zeng

et al. 2019

New Phytologist

105

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Summary Plants form a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula. We show that M. truncatula SWEET1b transporter is strongly upregulated in arbuscule‐containing cells compared to roots and localizes to the peri‐arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule‐specific overexpression of MtSWEET1bY57A/G58D, which are considered to act in a dominant‐negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for MtSWEET1b in the transport of glucose across the peri‐arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.

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Section: Introductionmentioning

confidence: 99%

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

Zeng

et al. 2019

New Phytologist

105

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“…For example, it has been proposed previously that the plant sugar transporters should be regulated in response to the plant's intracellular phosphate level (Schott et al ., ). Indeed, different experimental evidence points to diverse nutrient status‐dependent regulation cascades (Roth & Paszkowski, ; Wang et al ., ). Our analyses indicate that the release of C sources in an electroneutral manner, albeit not optimal in terms of energetics and C use efficiency, could be beneficial in terms of P acquisition. Interestingly, SWEETs involved in the export of sugars, and homologs of adenosine triphosphate‐binding cassette (ABC) transporters, putatively involved in the export of fatty acids, have been found to be essential for, or upregulated during, arbuscule formation (Zhang et al ., ; Gutjahr et al ., ; Manck‐Götzenberger & Requena, ).…”

Section: Discussionmentioning

confidence: 97%

“…Our approach concludes with a transporter network (Fig. ) which is not in conflict with those that were sketched according to experimentally verified transporter expression data (Parniske, ; Bonfante & Genre, ; Smith & Smith, ; Behie & Bidochka, ; Wang et al ., ; Chen et al ., ). This fact validates our assumption and, moreover, our approach sheds light on the question marks that were still assigned to several transport pathways.…”

Section: Discussionmentioning

confidence: 99%

Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view

et al. 2019

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Summary To obtain insights into the dynamics of nutrient exchange in arbuscular mycorrhizal ( AM ) symbiosis, we modelled mathematically the two‐membrane system at the plant–fungus interface and simulated its dynamics. In computational cell biology experiments, the full range of nutrient transport pathways was tested for their ability to exchange phosphorus (P)/carbon (C)/nitrogen (N) sources. As a result, we obtained a thermodynamically justified, independent and comprehensive model of the dynamics of the nutrient exchange at the plant–fungus contact zone. The predicted optimal transporter network coincides with the transporter set independently confirmed in wet‐laboratory experiments previously, indicating that all essential transporter types have been discovered. The thermodynamic analyses suggest that phosphate is released from the fungus via proton‐coupled phosphate transporters rather than anion channels. Optimal transport pathways, such as cation channels or proton‐coupled symporters, shuttle nutrients together with a positive charge across the membranes. Only in exceptional cases does electroneutral transport via diffusion facilitators appear to be plausible. The thermodynamic models presented here can be generalized and adapted to other forms of mycorrhiza and open the door for future studies combining wet‐laboratory experiments with computational simulations to obtain a deeper understanding of the investigated phenomena.

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“…In a field split‐plot experiment, N‐deficient plots were strongly colonized by AM fungi when compared with N efficiency plants, despite high soil and tissue P concentrations ( Blanke et al., ). This may indicate that both P and N regulate this symbiosis and are delivered to the host through this plant‐fungus interaction ( Wang et al., ). The availability of essential soil resources, e.g ., soil N : P ratio, was an important force in the formation of geographic mosaics of symbiotic function in mycorrhizae; including N : P ratio of soil availability, and the AM fungi increased the uptake of the nutrient that was most limiting in the soil ( Johnson et al., ).…”

Section: Introductionmentioning

confidence: 99%

Effects of nitrogen feeding for extraradical mycelium of Rhizophagus irregularis maize symbiosis incorporated with phosphorus availability

Ngwene

Hong

et al. 2019

J. Plant Nutr. Soil Sci.

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In terrestrial ecosystems, plants are frequently in symbiosis with arbuscular mycorrhizal fungi (AMF) with mineral nutrients and photosynthesis carbon exchanges in between. This research sought to identify the effects of phosphorus (P) levels on the nitrogen (N) uptake via extraradical mycelium (ERM) and the mycorrhizal growth response (MGR) of maize plants within the AMF symbiosis. Pots were separated into root compartments and hyphae compartments (HCs) with two layers of a 30‐μm mesh membrane and an air gap in between, where only hyphae could pass through, to avoid both N diffusion and root growth effects. Maize plants were inoculated with Rhizophagus irregularis with different N fertilization in HCs under two different P fertilization levels. Our results indicated that a strong increase in MGR with low‐P fertilization. The same tendency was not observed with high‐P fertilization, although both had a large increase in P concentration as a potential source of growth in shoot tissue of mycorrhizal plants. Substantial effects (10.5% more N) were observed in the case of high‐P availability for the host plants from ERM fed with N, whereas under low‐P conditions ERM may prioritize P uptake rather than N uptake. The AM fungi increase the uptake of N and P, which are most limiting in the soil with fewer forces from soil resources. In addition, there was still more P accumulated than N due to the high N for ERM with high‐P supply. Low N in HCs corresponded with a lower colonization rate in roots but with high hyphae density in HCs; this result suggest that N and P availability might change the ratio of extraradical to intraradical hyphae length.

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Nutrient Exchange and Regulation in Arbuscular Mycorrhizal Symbiosis

Cited by 365 publications

References 140 publications

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view

Effects of nitrogen feeding for extraradical mycelium of Rhizophagus irregularis maize symbiosis incorporated with phosphorus availability

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