Genetic and physiological analysis of tomato fruit weight and composition: influence of carbon availability on QTL detection

Abstract

Throughout tomato domestication, a large increase in fruit size was associated with a loss of dry matter and sugar contents. This study aims to dissect the contributions of genetic variation and the physiological processes underlying the relationships between fruit growth and the accumulation of dry matter and sugars. Fruit quality traits and physiological parameters were measured on 20 introgression lines derived from the introgression of Solanum chmielewskii into S. lycopersicum, under high (HL, unpruned trusses) and low (LL, trusses pruned to one fruit) fruit load conditions. Inter- and intra-genotypic correlations among traits were estimated and quantitative trait loci (QTL) for size, composition, and physiological traits were mapped. LL increased almost all traits, but the response of sugar content was genotype-dependent, involving either dilution effects or differences in carbon allocation to sugars. Genotype x fruit load interactions were significant for most traits and only 30% of the QTL were stable under both fruit loads. Many QTL for fresh weight and cell or seed numbers co-localized. Eleven clusters of QTL for fresh weight and dry matter or sugar content were detected, eight with opposite allele effects and three with negative effects. Two genotypic antagonistic relationships, between fresh weight and dry matter content and between cell number and cell size, were significant only under HL; the second could be interpreted as a competition for carbohydrates among cells. The role of cuticular conductance, fruit transpiration or cracking in the relationship between fruit fresh weight and composition was also emphasized at the genetic and physiological levels.

Fig. 1.

Effect of fruit load on several traits. (A) Groups of genotypes according to fruit load effects on (B) fruit fresh weight (FW), (C) pericarp dry weight (DW), (D) pericarp dry matter content (DMC), (E) pericarp sugar content relative to fresh weight (SUGfw), and (F) pericarp sugar content relative to dry weight (SUGdw). Arrows indicate significant increase or decrease and (–) no change from high load (HL) to low load (LL). According to the different combinations among trait variations, genotypes were ordered into five groups (Gr 1–Gr 5). Each point is the mean of the two years of measurements. Triangles refer to group 1, circles to group 2, diamonds to group 3, squares to group 4, and inverted triangles to group 5. On each graph, black symbols indicate significant difference between HL and LL and white symbols refer to non-significant differences at the 0.05 probability level. On each graph, a linear regression was fitted to all genotypes, and values of determination coefficients (R²) and P-value (p) are shown on each figure. Dotted lines refer to bisecting lines.

Fig. 2.

Linkage map showing the locations of the 110 COS markers whose names begin with ‘C2_At’ and the three SSR markers. Numbers on the right of the marker names indicate the genetic distances in cM from the top of the chromosome. Map distances are based on the tomato-EXPEN F2.2000 mapping population (S. lycopersicum LA925×S. pennellii LA716 type F2.2000) (http://www.sgn.cornell.edu/). At the bottom of each chromosome, the total genetic length is mentioned. If the genotype carried a single homozygous introgression, its location is black-filled (for example C1a). If the genotype carried a single heterozygous introgression, its location is grey-filled (C4c). If the genotype carried multiple homozygous introgressions, its name refers to the largest introgression and the locations of all the introgressions are white-filled. The locations of the other introgressions are indicated at the bottom of the fragment. For example, the C3c carried its main introgression on chromosome 3 and a smaller one on chromosome 2. If the genotype carried multiple heterozygous introgressions, introgressions are hatched.

Fig. 3.

Genetic map of the QTL detected on genotypes carrying a single introgressed fragment, and at least one QTL for fruit weight or composition. QTL for fruit weight and composition are circled; QTL only detected under high fruit load (HL) are on the left of the chromosome; QTL only detected under low fruit load (LL) are on the right of the chromosome; QTL detected whatever the fruit load are at the middle of the chromosome. (–) and (+) indicate if the S. chmielewskii alleles had negative or positive effects on the trait, respectively.