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Open Access Highly Accessed Research article

From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism

Inès Zouari1, Alessandra Salvioli1, Matteo Chialva1, Mara Novero1, Laura Miozzi2, Gian Carlo Tenore3, Paolo Bagnaresi4 and Paola Bonfante1*

Author Affiliations

1 Department of Life Sciences and Systems Biology, University of Turin, Viale Mattioli 25, 10125 Turin, Italy

2 Institute of Plant Virology-IVV-CNR, Strada Delle Cacce, 73, 10135 Turin, Italy

3 Department of Pharmacy, University of Naples Federico II, via D. Montesano 49, 80131 Naples, Italy

4 Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Genomics Research Centre via S. Protaso, 302 I –29017 Fiorenzuola d’Arda, PC, Italy

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BMC Genomics 2014, 15:221  doi:10.1186/1471-2164-15-221

Published: 21 March 2014

Abstract

Background

Tomato (Solanum lycopersicum) establishes a beneficial symbiosis with arbuscular mycorrhizal (AM) fungi. The formation of the mycorrhizal association in the roots leads to plant-wide modulation of gene expression. To understand the systemic effect of the fungal symbiosis on the tomato fruit, we used RNA-Seq to perform global transcriptome profiling on Moneymaker tomato fruits at the turning ripening stage.

Results

Fruits were collected at 55 days after flowering, from plants colonized with Funneliformis mosseae and from control plants, which were fertilized to avoid responses related to nutrient deficiency. Transcriptome analysis identified 712 genes that are differentially expressed in fruits from mycorrhizal and control plants. Gene Ontology (GO) enrichment analysis of these genes showed 81 overrepresented functional GO classes. Up-regulated GO classes include photosynthesis, stress response, transport, amino acid synthesis and carbohydrate metabolism functions, suggesting a general impact of fungal symbiosis on primary metabolisms and, particularly, on mineral nutrition. Down-regulated GO classes include cell wall, metabolism and ethylene response pathways. Quantitative RT-PCR validated the RNA-Seq results for 12 genes out of 14 when tested at three fruit ripening stages, mature green, breaker and turning. Quantification of fruit nutraceutical and mineral contents produced values consistent with the expression changes observed by RNA-Seq analysis.

Conclusions

This RNA-Seq profiling produced a novel data set that explores the intersection of mycorrhization and fruit development. We found that the fruits of mycorrhizal plants show two transcriptomic “signatures”: genes characteristic of a climacteric fleshy fruit, and genes characteristic of mycorrhizal status, like phosphate and sulphate transporters. Moreover, mycorrhizal plants under low nutrient conditions produce fruits with a nutrient content similar to those from non-mycorrhizal plants under high nutrient conditions, indicating that AM fungi can help replace exogenous fertilizer for fruit crops.

Keywords:
Arbuscular mycorrhizal fungi; Tomato; RNA sequencing; Fruit gene expression; Systemic effects