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

Abstract

BackgroundTomato (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.ResultsFruits 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.ConclusionsThis 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.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-221) contains supplementary material, which is available to authorized users.

Gr and hp-1 tomato mutants unveil unprecedented interactions between arbuscular mycorrhizal symbiosis and fruit ripening

“…5). In WT, PSY gene was similarly expressed in MYC and NM conditions, even though a trend towards down-regulation under MYC treatment was observed in a previous RNA-seq experiment using the Moneymaker cultivar (Zouari et al 2014). Lastly, no expression differences were detected between MYC and NM conditions in the mutant backgrounds.…”

“…By contrast, in the hp-1 mutant where there was enhanced pigment production and overall light sensitivity due to the mutation, the AM symbiosis acted as a positive regulator. The enhanced flower and fruit productivity under MYC conditions was probably favored by the synergy between the mutation itself (high light-sensibility in leaves, higher photosynthesis) and mycorrhization, which stimulates photosynthesis both in leaves (Wright et al 1998;Kaschuk et al 2009;Schweiger and Muller 2015) and in fruits, at least as predicted on the basis of transcriptomic analysis (Zouari et al 2014). ICP-OES analysis showed that while the fruits from the WT mycorrhizal plants possessed 30 % more phosphate than those from non-mycorrhizal plants, no differences were detected in the fruits produced by the mutant mycorrhizal plants.…”

“…The scheme illustrates how mutations in Gr (green fruits) and hp-1 (dark red fruits) genes do not impact the AM establishment and the fungal colonization. By contrast, the mutations have an impact not only on the fruit color at the fully ripe stage, but also on the systemic AM effects which are described in WT tomato at fruit level, also according to Zouari et al (2014) …”

“…In addition, they possess a higher anti-oestrogenic power and no in vitro genotoxic effects (Giovannetti et al 2012), as well as an enhanced expression of allergen-encoding genes that do not match with a higher allergenic potential for humans (Schwarz et al 2011). A deeper mRNA-seq transcriptome analysis (Zouari et al 2014) provided a more exhaustive molecular framework for fruits from tomato MYC plants. This study highlighted a fruit systemic ''signature'' consisting of climacteric fleshy fruit-specific genes as well as of transcripts commonly regulated by symbiosis.…”

“…Pathways associated with cell wall metabolism were downregulated, including genes coding for polygalacturonase, which is directly involved in fruit ripeningassociated cell wall remodeling. Since genes involved in ethylene (ET) metabolism were also repressed, Zouari et al (2014) suggested that AM may also increase tomato shelf-life. The use of several tomato ripening mutants has shed light on the genetics behind fleshy fruit ripening mechanisms and their implications in plant hormone and light signal reception (Klee and Giovannoni 2011).…”