The host plant Pinus pinaster exerts specific effects on phosphate efflux and polyphosphate metabolism of the ectomycorrhizal fungus Hebeloma cylindrosporum: a radiotracer, cytological staining and 31P NMR spectroscopy study

Torres‐Aquino, Margarita; Becquer, Adeline; Guernevé, Christine Le; Louche, Julien; Amenc, Laurie; Staunton, Siobhán; Quiquampoix, Hervé; Plassard, Claude

doi:10.1111/pce.12847

Cited by 23 publications

(21 citation statements)

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“…We previously showed that H. cylindrosporum mycelia released greater amounts of 32 P when incubated with P. pinaster (Torres‐Aquino et al ., ). Using the same experimental design, we examined how HcPT2 expression levels affect both 32 P uptake and release capacities by the fungal transgenic lines.…”

Section: Resultsmentioning

confidence: 97%

“…from the Médoc, Landes‐Sore‐Vergé source) were grown first in test tubes, uninoculated or inoculated with 3‐wk‐old wild‐type or transgenic fungi as described previously (Plassard et al ., ; Garcia et al ., ). Mycorrhizal and nonmycorrhizal (NM) plants were watered every week with 15 ml of mineral nutrient solution (Torres‐Aquino et al ., ). All test tubes were placed in a growth chamber under a 16 h : 8 h, light–dark cycle at 25°C/20°C, 80%/100% relative humidity, CO 2 concentration of c .…”

Section: Methodsmentioning

confidence: 97%

“…PolyPs are then translocated via a motile tubular vacuolar system (Ashford & Allaway, ) before being hydrolyzed within the Hartig net (Cairney, ). This provides Pi efflux from fungal cells to the interfacial apoplast (Torres‐Aquino et al ., ). Finally, Pi is taken up by, as yet, uncharacterized plant transporters that are specifically up‐regulated in colonized roots (Loth‐Pereda et al ., ; Kariman et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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The Hebeloma cylindrosporum HcPT2 Pi transporter plays a key role in ectomycorrhizal symbiosis

et al. 2018

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Through a mutualistic relationship with woody plant roots, ectomycorrhizal fungi provide growth-limiting nutrients, including inorganic phosphate (Pi), to their host. Reciprocal trades occur at the Hartig net, which is the symbiotic interface of ectomycorrhizas where the two partners are symplasmically isolated. Fungal Pi must be exported to the symbiotic interface, but the proteins facilitating this transfer are unknown. In the present study, we combined transcriptomic, microscopy, whole plant physiology, X-ray fluorescence mapping, P labeling and fungal genetic approaches to unravel the role of HcPT2, a fungal Pi transporter, during the Hebeloma cylindrosporum-Pinus pinaster ectomycorrhizal association. We localized HcPT2 in the extra-radical hyphae and the Hartig net and demonstrated its determinant role for both the establishment of ectomycorrhizas and Pi allocation towards P. pinaster. We showed that the host plant induces HcPT2 expression and that the artificial overexpression of HcPT2 is sufficient to significantly enhance Pi export towards the central cylinder. Together, our results reveal that HcPT2 plays an important role in ectomycorrhizal symbiosis, affecting both Pi influx in the mycelium and efflux towards roots under the control of P. pinaster.

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Section: Resultsmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

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The Hebeloma cylindrosporum HcPT2 Pi transporter plays a key role in ectomycorrhizal symbiosis

et al. 2018

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“…Long‐chain polyP can be visualized only by staining with toluidine blue (Torres‐Aquino et al ., ), but not by in vivo or in vitro 31 P‐NMR, as can short‐chain polyP (Martin et al ., ; Torres‐Aquino et al ., ). When H. cylindrosporum mycelia, preloaded with Pi to generate long‐chain polyP, were brought into contact with roots of a mycorrhizal host plant ( Pinus pinaster ), a strong short‐chain (average length of 10–30 residues) polyP NMR signal became visible after 6 h. By contrast, no changes were observed in the presence of roots of a non‐host plant ( Zea mays ) or in free‐living mycelia (Torres‐Aquino et al ., ). In addition to this polyP conversion, fungal mycelia in contact with P. pinaster roots also released much larger amounts of 32 P compared with controls.…”

Section: N/p Storage and Remobilizationmentioning

confidence: 99%

Nitrogen and phosphate metabolism in ectomycorrhizas

Nehls

Plassard

2018

New Phytologist

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1047 I. Introduction 1047 II. Mobilization of soil N/P by ECM fungi 1048 III. N/P uptake 1048 IV. N/P assimilation 1049 V. N/P storage and remobilization 1049 VI. Hyphal N/P efflux at the plant-fungus interface 1052 VII. Conclusion and research needs 1054 Acknowledgements 1055 References 1055 SUMMARY: Nutrient homeostasis is essential for fungal cells and thus tightly adapted to the local demand in a mycelium with hyphal specialization. Based on selected ectomycorrhizal (ECM) fungal models, we outlined current concepts of nitrogen and phosphate nutrition and their limitations, and included knowledge from Baker's yeast when major gaps had to be filled. We covered the entire pathway from nutrient mobilization, import and local storage, distribution within the mycelium and export at the plant-fungus interface. Even when nutrient import and assimilation were broad issues for ECM fungi, we focused mainly on nitrate and organic phosphorus uptake, as other nitrogen/phosphorus (N/P) sources have been covered by recent reviews. Vacuolar N/P storage and mobilization represented another focus point of this review. Vacuoles are integrated into cellular homeostasis and central for an ECM mycelium at two locations: soil-growing hyphae and hyphae of the plant-fungus interface. Vacuoles are also involved in long-distance transport. We further discussed potential mechanisms of bidirectional long-distance nutrient transport (distances from millimetres to metres). A final focus of the review was N/P export at the plant-fungus interface, where we compared potential efflux mechanisms and pathways, and discussed their prerequisites.

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“…The symbiosis of ectomycorrhizae has been well documented (Hogberg et al , ; Torres‐Aquino et al , ). Ectomycorrhizal fungi have been well studied, which could increase plant primary biomass and increase plant tolerance to stress (Abiala et al , ; Bell et al , ).…”

Section: Discussionmentioning

confidence: 99%

Root‐tip cutting and uniconazole treatment improve the colonization rate of Tuber indicum on Pinus armandii seedlings in the greenhouse

Zhu

et al. 2020

Microbial Biotechnology

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Summary The Chinese black truffle Tuber indicum is commercially valuable. The main factors influencing the success or failure of a truffle crop include the mycorrhizal colonization rate and host plant quality. The effects of a plant growth regulator (uniconazole) and plant growth management technique (root‐tip cutting) on T. indicum colonization rate and Pinus armandii seedling growth were assessed under greenhouse conditions. The results indicated that 10 mg l−1 uniconazole or the combination of 5 mg l−1 uniconazole and root‐tip cutting constitutes an effective method for ectomycorrhizal synthesis based on an overall evaluation of colonization rate, plant biomass, plant height, root weight, stem circumference and antioxidant enzyme activities (SOD and POD) of P. armandii. The abundance of Proteobacteria in the rhizosphere of colonized seedlings might serve as an indicator of stable mycorrhizal colonization. This research inspires the potential application of uniconazole and root‐tip cutting treatments for mycorrhizal synthesis and truffle cultivation.

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The host plant Pinus pinaster exerts specific effects on phosphate efflux and polyphosphate metabolism of the ectomycorrhizal fungus Hebeloma cylindrosporum: a radiotracer, cytological staining and ³¹P NMR spectroscopy study

Cited by 23 publications

References 59 publications

The Hebeloma cylindrosporum HcPT2 Pi transporter plays a key role in ectomycorrhizal symbiosis

The Hebeloma cylindrosporum HcPT2 Pi transporter plays a key role in ectomycorrhizal symbiosis

Nitrogen and phosphate metabolism in ectomycorrhizas

Root‐tip cutting and uniconazole treatment improve the colonization rate of Tuber indicum on Pinus armandii seedlings in the greenhouse

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