Arbuscular Mycorrhizal Symbiosis Requires a Phosphate Transceptor in the Gigaspora margarita Fungal Symbiont

Xie, Xianan; Hu, Lin; Peng, Xiao-Wei; Xu, Congrui; Sun, Zhongfeng; Jiang, Kexin; Huang, Antian; Wu, Xiaohui; Tang, Nianwu; Salvioli, Alessandra; Bonfante, Paola; Zhao, Bin

doi:10.1016/j.molp.2016.08.011

Cited by 84 publications

(102 citation statements)

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“…However, only limited information has been obtained on the molecular mechanism underlying the symbiosis‐specific Pi metabolism in the fungi, which is at least partially due to the difficulty in genetic manipulation of the fungi. Recently, host‐induced gene silencing (Helber et al ., ; Xie et al ., ) and virus‐induced gene silencing (Kikuchi et al ., ) were applied for functional characterization of AM fungal genes. With these techniques, however, only the genes expressed in intraradical hyphae, but none of those expressed in extraradical hyphae, have successfully been knocked down because small interference RNA (siRNA) is supplied via the host‐silencing pathway.…”

Section: Discussionmentioning

confidence: 99%

How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine‐tuning of phosphate metabolism

2018

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Contents Summary1116I.Introduction1116II.Foraging for phosphate1117III.Fine‐tuning of phosphate homeostasis1117IV.The frontiers: phosphate translocation and export1119V.Conclusions and outlook1120Acknowledgements1120References1120 Summary Arbuscular mycorrhizal fungi form symbiotic associations with most land plants and deliver mineral nutrients, in particular phosphate, to the host. Therefore, understanding the mechanisms of phosphate acquisition and delivery in the fungi is critical for full appreciation of the mutualism in this association. Here, we provide updates on physical, chemical, and biological strategies of the fungi for phosphate acquisition, including interactions with phosphate‐solubilizing bacteria, and those on the regulatory mechanisms of phosphate homeostasis based on resurveys of published genome sequences and a transcriptome with reference to the latest findings in a model fungus. For the mechanisms underlying phosphate translocation and export to the host, which are major research frontiers in this field, not only recent advances but also testable hypotheses are proposed. Lastly, we briefly discuss applicability of the latest tools to gene silencing in the fungi, which will be breakthrough techniques for comprehensive understanding of the molecular basis of fungal phosphate metabolism.

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Section: Discussionmentioning

confidence: 99%

How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine‐tuning of phosphate metabolism

2018

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“…a). Such a role in Pi uptake has already been ascribed to HcPT2 (Tatry et al ., ) as well as for other H + :Pi symporters whose proteins or transcripts were detected in ECM (Garcia et al ., ; Wang et al ., ; Zheng et al ., ) or arbuscular mycorrhizal (AM) (Harrison & van Buuren, ; Xie et al ., ) fungi. The fact that transgenic lines overexpressing HcPT2 were unaffected in their Pi uptake could be due to a saturation of the Pi transport in nonlimiting Pi concentrations.…”

Section: Discussionmentioning

confidence: 99%

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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“…Fungal Pi:H + symporter (PT) homologues of the yeast high‐affinity transporter PHO84 (Bun‐Ya et al ., ), are thought to be responsible for Pi uptake from the soil (Harrison & van Buuren, ; Maldonado‐Mendoza et al ., ; Benedetto et al ., ; Xie et al ., ). Consistent with this, the fungal PT genes are expressed in the extraradical mycelium (ERM).…”

Section: Nutritional and Regulatory Roles For Key Metabolites In The mentioning

confidence: 97%

“…This transport is suggested to be driven by an H + energy gradient produced by an H + ‐ATPase (Krajinski et al ., ; Wang et al ., ). The expression of fungal PT genes in the intraradical mycelium suggests a possible role in Pi reabsorption from the PAS (Benedetto et al ., ; Balestrini et al ., ; Fiorilli et al ., ; Xie et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis

2018

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Contents Summary 1031 I. Introduction 1031 II. Interkingdom communication enabling symbiosis 1032 III. Nutritional and regulatory roles for key metabolites in the AM symbiosis 1035 IV. The plant-fungus genotype combination determines the outcome of the symbiosis 1039 V. Perspectives 1039 Acknowledgements 1041 References 1041 SUMMARY: The evolutionary and ecological success of the arbuscular mycorrhizal (AM) symbiosis relies on an efficient and multifactorial communication system for partner recognition, and on a fine-tuned and reciprocal metabolic regulation of each symbiont to reach an optimal functional integration. Besides strigolactones, N-acetylglucosamine-derivatives released by the plant were recently suggested to trigger fungal reprogramming at the pre-contact stage. Remarkably, N-acetylglucosamine-based diffusible molecules also are symbiotic signals produced by AM fungi (AMF) and clues on the mechanisms of their perception by the plant are emerging. AMF genomes and transcriptomes contain a battery of putative effector genes that may have conserved and AMF- or host plant-specific functions. Nutrient exchange is the key feature of AM symbiosis. A mechanism of phosphate transport inside fungal hyphae has been suggested, and first insights into the regulatory mechanisms of root colonization in accordance with nutrient transfer and status were obtained. The recent discovery of the dependency of AMF on fatty acid transfer from the host has offered a convincing explanation for their obligate biotrophism. Novel studies highlighted the importance of plant and fungal genotypes for the outcome of the symbiosis. These findings open new perspectives for fundamental research and application of AMF in agriculture.

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Arbuscular Mycorrhizal Symbiosis Requires a Phosphate Transceptor in the Gigaspora margarita Fungal Symbiont

Cited by 84 publications

References 84 publications

How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine‐tuning of phosphate metabolism

How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine‐tuning of phosphate metabolism

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

Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis

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