Domestication and Genetic Improvement Alter the Symbiotic Microbiome Structure and Function of Tomato Leaf and Fruit Pericarp

Abstract

Many studies have attempted to explore the changes in the structure and function of symbiotic microbiomes, as well as the underlying genetic mechanism during crop domestication. However, most of these studies have focused on crop root microbiomes, while those on leaf and fruit are rare. In this study, we generated a comprehensive dataset including the metagenomic (leaf) and metatranscriptomic (fruit pericarp in the orange stage) data of hundreds of germplasms from three tomato clades: Solanum pimpinellifolium (PIM), cherry tomato (S. lycopersicum var. cerasiforme) (CER), and S. lycopersicum group (BIG). We investigated the effect of domestication and improvement processes on the structure of the symbiotic microbiome of tomato leaf and fruit pericarp, as well as its genetic basis. We were able to obtain the composition of the symbiotic microbiome of tomato leaf and fruit pericarp, based on which the tomato clade (PIM, CER, or BIG) was predicted with high accuracy through machine learning methods. In the processes of tomato domestication and improvement, changes were observed in the relative abundance of specific bacterial taxa, Bacillus for example, in the tomato leaf and fruit pericarp symbiotic microbiomes, as well as in the function of these symbiotic microbiomes. In addition, SNP loci that were significantly associated with microbial species that are characteristic of tomato leaf were identified. Our results show that domestication and genetic improvement processes alter the symbiotic microbiome structure and function of tomato leaf and fruit pericarp. We propose that leaf and fruit microbiomes are more suitable for revealing changes in symbiotic microbiomes during the domestication process and the underlying genetic basis for these changes due to the exclusion of the influence of environmental factors such as soil types on the microbiome structure.