Abstract

Specialised metabolites produced during plant-fungal associations often define how symbiosis between the plant and the fungus proceeds. They also play a role in the establishment of additional interactions between the symbionts and other organisms present in the niche. However, specialised metabolism and its products are sometimes overlooked when studying plant-microbe interactions. This limits our understanding of the specific symbiotic associations and potentially future perspectives of their application in agriculture. In this study, we used the interaction between the root endophyte Serendipita indica and tomato (Solanum lycopersicum) plants to explore how specialised metabolism of the host plant is regulated upon a mutualistic symbiotic association. To do so, tomato seedlings were inoculated with S. indica chlamydospores and subjected to RNAseq analysis. Gene expression of the main tomato specialised metabolism pathways was compared between roots and leaves of endophyte-colonised plants and tissues of endophyte-free plants. S. indica colonisation resulted in a strong transcriptional response in the leaves of colonised plants. Furthermore, the presence of the fungus in plant roots appears to induce expression of genes involved in the biosynthesis of lignin-derived compounds, polyacetylenes, and specific terpenes in both roots and leaves, whereas pathways producing glycoalkaloids and flavonoids were expressed in lower or basal levels.

Highlights

  • Fossils from the Early Devonian period displaying fungal-like structures inside plant cells provide evidence that plant-fungal interactions date back to more than 400 million years ago

  • Our results showed that the presence of S. indica in the roots led to a strong transcriptional response in the leaves of colonised plants, which has not been reported before

  • Plant specialised metabolites are important for adaptation and interaction with the environment, serving as defence compounds against microorganisms or other competing plants, or as signal molecules, attracting pollinators or seed dispersal animals

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Summary

Introduction

Fossils from the Early Devonian period displaying fungal-like structures inside plant cells provide evidence that plant-fungal interactions date back to more than 400 million years ago. It appears that these symbiotic interactions have contributed to the colonisation of land and the emergence of the first terrestrial plants [1–3]. Plant-fungal symbiosis is considered a dynamic interaction, ranging from mutualism and commensalism, to parasitism, depending on the result of the interaction on the plant host [4]. Mutualistic interactions in the soil are usually characterised by exchange of nutrients, during which the fungus acquires carbon from the host and, in return, it facilitates the acquisition and assimilation of essential and scarce soil elements (e.g., nitrogen, phosphorus, and iron) [3,5]. Plants produce defence molecules to fight pathogens or exude a variety of compounds to recruit beneficial fungi, while fungal symbionts synthesise metabolites to reprogram plant signalling and metabolism or antimicrobials to defend themselves

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