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RiPEIP1, a gene from the arbuscular mycorrhizal fungus Rhizophagus irregularis, is preferentially expressed in planta and may be involved in root colonization

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Abstract

Transcriptomics and genomics data recently obtained from the arbuscular mycorrhizal (AM) fungus Rhizophagus irregularis have offered new opportunities to decipher the contribution of the fungal partner to the establishment of the symbiotic association. The large number of genes which do not show similarity to known proteins witnesses the uniqueness of this group of plant-associated fungi. In this work, we characterize a gene that was called RiPEIP1 (Preferentially Expressed In Planta). Its expression is strongly induced in the intraradical phase, including arbuscules, and follows the expression profile of the Medicago truncatula phosphate transporter MtPT4, a molecular marker of a functional symbiosis. Indeed, mtpt4 mutant plants, which exhibit low mycorrhizal colonization and an accelerated arbuscule turnover, also show a reduced RiPEIP1 mRNA abundance. To further characterize RiPEIP1, in the absence of genetic transformation protocols for AM fungi, we took advantage of two different fungal heterologous systems. When expressed as a GFP fusion in yeast cells, RiPEIP1 localizes in the endomembrane system, in particular to the endoplasmic reticulum, which is consistent with the in silico prediction of four transmembrane domains. We then generated RiPEIP1-expressing strains of the fungus Oidiodendron maius, ericoid endomycorrhizal fungus for which transformation protocols are available. Roots of Vaccinium myrtillus colonized by RiPEIP1-expressing transgenic strains showed a higher mycorrhization level compared to roots colonized by the O. maius wild-type strain, suggesting that RiPEIP1 may regulate the root colonization process.

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Acknowledgments

Research was funded by the BIOBIT-Converging Technology project (WP2), the Progetto Ateneo SLEPS and the University grant (60 %) to LL. We thank Maria J. Harrison for the mtpt4-2 mutant, Nuria Ferrol for the RFP yeast strains, Andrea Genre for confocal microscopy observations, Raffaella Balestrini for the help on laser microdissection, and Paola Bonfante and Silvia Perotto for fruitful discussions and critical reading of the manuscript.

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Authors and Affiliations

  1. Department of Life Science and Systems Biology, University of Torino, via Accademia Albertina 13, 10123, Torino, Italy

    Valentina Fiorilli, Simone Belmondo, Hassine Radhouane Khouja, Stefania Daghino & Luisa Lanfranco

  2. Institute for Sustainable Plant Protection (IPSP), CNR, Strada delle Cacce 73, 10135, Torino, Italy

    Simona Abbà & Antonella Faccio

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  1. Valentina Fiorilli
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Correspondence to Valentina Fiorilli.

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Table S1

(DOCX 12 kb)

Figure S1

Nucleotide and deduced amino acid sequences of RiPEIP1. (a) RiPEIP1 genomic DNA sequence showing the presence of five introns. (b) RiPEIP1 protein sequence showing the 4 transmembrane domains (underlined), the typical ER-retention/retrieval motifs (bold) and the predicted phosphorylation sites (red). See text for details (GIF 255 kb)

High Resolution (TIF 2702 kb)

Figure S2

Colonization level of M. truncatula roots at 28 and 60 days post inoculation (dpi) assessed accordingly to Trouvelot et al. (1986). F%: frequency of mycorrhization in the root system (a), a%: arbuscules abundance in mycorrhizal parts of root fragments (b). Different letters indicate statistically significant difference (p < 0.05 ANOVA, Tukey’s post-hoc test) (GIF 17 kb)

High Resolution (TIF 102 kb)

Figure S3

Mycorrhizal phenotype of M. truncatula wt (a, b) and mtpt4-2 (c, d) roots colonized by R. irregularis. Roots were harvested 60 dpi, stained with acid fuchsin and observed with a confocal microscope. Arbuscules in mtpt4-2 are degenerated as described in Javot et al. (Javot et al. 2011). Bars = 25 μm. (GIF 119 kb)

High Resolution (TIF 1438 kb)

Figure S4

Molecular analyses of O. maius transgenic strains expressing RiPEIP1. (a) Gel electrophoresis of PCR products obtained from genomic DNA of wt and transgenic strains using RiPEIP1 specific primers (b) Southern blot of genomic DNA from wt and transgenic strains restricted with BglII enzyme and hybridized with the RiPEIP1 probe. Lanes corresponding to BC6, BA2, BA4 samples exhibited a single genomic insertion. (GIF 114 kb)

High Resolution (TIF 1418 kb)

Figure S5

Phenotype of O. maius free living mycelia from wt and RiPEIP1-expressing strain BA2 as revealed by calcoflour white staining. Laser-scanning microscope observation of one-month-old O. maius wt and transgenic strains stained with calcofluor white. Transmitted light images are shown on the right (b, d) and the corresponding fluorescence images on the left (a, c). Bars: 10 μm (GIF 188 kb)

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Figure S6

Mycorrhizal phenotype of O. maius wt and RiPEIP1-expressing strain BC6. Mycorrhized V. myrtillus roots were stained with acid fuchsin and observed 2 months after fungal inoculation. O. maius transgenic strains showed an increased number of coils (asterisk) in epidermal cells compared to the wt. (GIF 426 kb)

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Fiorilli, V., Belmondo, S., Khouja, H.R. et al. RiPEIP1, a gene from the arbuscular mycorrhizal fungus Rhizophagus irregularis, is preferentially expressed in planta and may be involved in root colonization. Mycorrhiza 26, 609–621 (2016). https://doi.org/10.1007/s00572-016-0697-0

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  • DOI: https://doi.org/10.1007/s00572-016-0697-0

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