The Full-Size ABCG Transporter of Medicago truncatula Is Involved in Strigolactone Secretion, Affecting Arbuscular Mycorrhiza.

Joanna Banasiak,Lorenzo Borghi,Enrico Martinoia,Natalia Stec,Michał Jasiński

doi:10.3389/fpls.2020.00018

Abstract

Strigolactones (SLs) are plant-derived signaling molecules that stimulate the hyphal branching of arbuscular mycorrhizal fungi (AMF), and consequently promote symbiotic interaction between the fungus and the plant. Currently, our knowledge on the molecular mechanism of SL transport is restricted to the Solanaceae family. In the Solanaceae family, SL translocation toward the rhizosphere occurs through the exodermis via hypodermal passage cells and involves a member of the G subfamily, of the ATP-binding cassette (ABC) membrane transporters. Most Fabaceae species, including those that are agriculturally important, have a different root anatomy compared to most angiosperm plants (i.e., lacking an exodermis). Thus, we have investigated how SL transport occurs in the model legume Medicago truncatula. Here, we show that overexpression of a SL transporter from petunia (PaPDR1) enhances AMF colonization rates in M. truncatula. This result demonstrates the importance of ABCG proteins for the translocation of orobanchol-type molecules to facilitate arbuscular mycorrhiza, regardless of root anatomy and phylogenetic relationships. Moreover, our research has led to the identification of Medicago ABCG59, a close homologue of Petunia PDR1, that exhibits root specific expression and is up-regulated by phosphate starvation as well as in the presence of rac-GR24, a synthetic SL. Its promoter is active in cortical cells, root tips, and the meristematic zone of nodules. The mtabcg59 loss-of-function mutant displayed a reduced level of mycorrhization compared to the WT plants but had no impact on the number of nodules after Sinorhizobium meliloti inoculation. The reduced mycorrhization indicates that less SLs are secreted by the mutant plants, which is in line with the observation that mtabcg59 exudates exhibit a reduced stimulatory effect on the germination of the parasitic plant Phelipanche ramosa compared to the corresponding wild type.

Highlights

Arbuscular mycorrhiza (AM) represents an ancient and widespread beneficial association, established between most terrestrial plants and filamentous fungi from the subphylum Glomeromycotina (Parniske, 2008; Spatafora et al, 2016)
It has been shown that the secretion of SLs in petunia, belonging to the Solanaceae family, occurs through the hypodermal passage cells (HPCs), located within the exodermis (Kretzschmar et al, 2012)
SLs have been shown to be translocated and secreted into the rhizosphere by the membrane transporter PDR1, which belongs to the full-size ABCG (PDR) subfamily of ATP-binding cassette (ABC) transporters (Kretzschmar et al, 2012)

Summary

Introduction

Arbuscular mycorrhiza (AM) represents an ancient and widespread beneficial association, established between most terrestrial plants and filamentous fungi from the subphylum Glomeromycotina (Parniske, 2008; Spatafora et al, 2016). Plants supply the fungi with sugars (Doidy et al, 2012) and lipids (Jiang et al, 2017; Luginbuehl et al, 2017; Rich et al, 2017) This nutrient transfer between symbionts occurs via highly branched, fungus-derived structures called arbuscules, formed inside root cortical cells (Parniske, 2008; Luginbuehl and Oldroyd, 2017). SLs, released into the rhizosphere upon phosphate deficiency, stimulate fungal mitochondrial metabolism, and promote hyphal branching (Akiyama et al, 2005; Besserer et al, 2006) These signaling molecules contribute to the transcriptional reprogramming of AMF (Tsuzuki et al, 2016) and induce the extrusion of chitin oligosaccharides, the so-called “myc factors”, responsible for the activation of nuclear Ca2+ spikes in the host root epidermis (Genre et al, 2013). It has recently been shown that in rice this process is severely attenuated in the SL biosynthetic mutants (Kobae et al, 2018)

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Discussion

Conclusion