Abstract

To investigate the regulation of seed metabolism and to estimate the degree of metabolic natural variability, metabolite profiling and network analysis were applied to a collection of 76 different homozygous tomato introgression lines (ILs) grown in the field in two consecutive harvest seasons. Factorial ANOVA confirmed the presence of 30 metabolite quantitative trait loci (mQTL). Amino acid contents displayed a high degree of variability across the population, with similar patterns across the two seasons, while sugars exhibited significant seasonal fluctuations. Upon integration of data for tomato pericarp metabolite profiling, factorial ANOVA identified the main factor for metabolic polymorphism to be the genotypic background rather than the environment or the tissue. Analysis of the coefficient of variance indicated greater phenotypic plasticity in the ILs than in the M82 tomato cultivar. Broad-sense estimate of heritability suggested that the mode of inheritance of metabolite traits in the seed differed from that in the fruit. Correlation-based metabolic network analysis comparing metabolite data for the seed with that for the pericarp showed that the seed network displayed tighter interdependence of metabolic processes than the fruit. Amino acids in the seed metabolic network were shown to play a central hub-like role in the topology of the network, maintaining high interactions with other metabolite categories, i.e., sugars and organic acids. Network analysis identified six exceptionally highly co-regulated amino acids, Gly, Ser, Thr, Ile, Val, and Pro. The strong interdependence of this group was confirmed by the mQTL mapping. Taken together these results (i) reflect the extensive redundancy of the regulation underlying seed metabolism, (ii) demonstrate the tight co-ordination of seed metabolism with respect to fruit metabolism, and (iii) emphasize the centrality of the amino acid module in the seed metabolic network. Finally, the study highlights the added value of integrating metabolic network analysis with mQTL mapping.

Highlights

  • Tomato is one of the most important crops worldwide (FAO Statistical Database; last updated 2011), being used mainly for human consumption

  • To understand the genetic basis of seed metabolism—a strategic need in the improvement of seed crops—we studied a collection of offspring plants stemming from the cross between a domesticated tomato cultivar Solanum lycopersicum cv M82 and its distant wild relative S. pennellii

  • Metabolic profiling of seeds in a tomato introgression lines (ILs) population identifies 46 metabolite quantitative trait loci (mQTL) and suggests strong posttranscriptional regulation To identify the potential quantitative trait loci (QTL) involved in the regulation of the level of metabolites in the tomato seed, we used a set of 76 ILs resulting from crosses between the domesticated Solanum lycopersicum and its distant relative S. pennellii, with each IL carrying a small chromosomal portion (5 cM to 75 cM) of the distant relative within the chromosomal background of the domesticated tomato [59]

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Summary

Introduction

Tomato is one of the most important crops worldwide (FAO Statistical Database; last updated 2011), being used mainly for human consumption. Strategies based on the exploitation of natural variation are being extensively employed [16,18,19,20,21] in an effort to reintroduce the lost genetic variation into cultivated species, including tomato [7], rapeseed [22], wheat [23], rice [24,25], barley [26], soybean [27], maize [28], the common bean [29], and pepper [30] This approach has led to the generation of mapping populations, facilitating the identification of a vast array of quantitative trait loci (QTL), including loci for yieldrelated traits, flowering time, fruit quality (in terms of BRIX) and plant-specific organ relations [11,31,32,33,34,35]. Numerous QTL associated with seed size, dormancy [36,37,38] seedling vigor [39,40], and tolerance to salt [41] has been identified and mapped

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