Tomato (Solanum lycopersicum L.) belongs to the Solanaceae family and is the second most important fruit or vegetable crop next to potato (Solanum tuberosum L.). It is cultivated for fresh fruit and processed products. Tomatoes contain many health-promoting compounds including vitamins, carotenoids, and phenolic compounds. In addition to its economic and nutritional importance, tomatoes have become the model for the study of fleshy fruit development. Tomato is a climacteric fruit and dramatic metabolic changes occur during its fruit development. In this review, we provide an overview of our current understanding of tomato fruit metabolism. We begin by detailing the genetic and hormonal control of fruit development and ripening, after which we document the primary metabolism of tomato fruits, with a special focus on sugar, organic acid, and amino acid metabolism. Links between primary and secondary metabolic pathways are further highlighted by the importance of pigments, flavonoids, and volatiles for tomato fruit quality. Finally, as tomato plants are sensitive to several abiotic stresses, we briefly summarize the effects of adverse environmental conditions on tomato fruit metabolism and quality.

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Tomato Fruit Development and Metabolism

Biotrophic microbes feeding on plants must obtain carbon from their hosts without killing the cells. The symbiotic Arbuscular mycorrhizal (AM) fungi colonizing plant roots do so by inducing major transcriptional changes in the host that ultimately also reprogram the whole carbon partitioning of the plant. AM fungi obtain carbohydrates from the root cortex apoplast, in particular from the periarbuscular space that surrounds arbuscules. However, the mechanisms by which cortical cells export sugars into the apoplast for fungal nutrition are unknown. Recently a novel type of sugar transporter, the SWEET, able to perform not only uptake but also efflux from cells was identified. Plant SWEETs have been shown to be involved in the feeding of pathogenic microbes and are, therefore, good candidates to play a similar role in symbiotic associations. Here we have carried out the first phylogenetic and expression analyses of the potato SWEET family and investigated its role during mycorrhiza symbiosis. The potato genome contains 35 SWEETs that cluster into the same four clades defined in Arabidopsis. Colonization of potato roots by the AM fungus Rhizophagus irregularis imposes major transcriptional rewiring of the SWEET family involving, only in roots, changes in 22 of the 35 members. None of the SWEETs showed mycorrhiza-exclusive induction and most of the 12 induced genes belong to the putative hexose transporters of clade I and II, while only two are putative sucrose transporters from clade III. In contrast, most of the repressed transcripts (10) corresponded to clade III SWEETs. Promoter-reporter assays for three of the induced genes, each from one cluster, showed re-localization of expression to arbuscule-containing cells, supporting a role for SWEETs in the supply of sugars at biotrophic interfaces. The complex transcriptional regulation of SWEETs in roots in response to AM fungal colonization supports a model in which symplastic sucrose in cortical cells could be cleaved in the cytoplasm by sucrose synthases or cytoplasmic invertases and effluxed as glucose, but also directly exported as sucrose and then converted into glucose and fructose by cell wall-bound invertases. Precise biochemical, physiological and molecular analyses are now required to profile the role of each potato SWEET in the arbuscular mycorrhizal symbiosis.

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Arbuscular mycorrhiza Symbiosis Induces a Major Transcriptional Reprogramming of the Potato SWEET Sugar Transporter Family.

SWEET genes are a recently identified plant gene family that play an indispensable role in sugar efflux. However, no systematic study has been performed in pear. In this research, 18 SWEET transporters identified in pear, almost twice the number found in woodland strawberry and Japanese apricot, were divided into four clades. Conserved motifs and six exons of the SWEET transporters were found in six species. SWEET transporters contained seven transmembrane segments (TMSs) that evolved from an internal duplication of an ancestral three-TMSs unit, connected by TMS4. This is the first direct evidence identifying internal repeats through bioinformatics analysis. Whole-genome duplication (WGD) or segmental duplication and dispersed duplication represent the main driving forces for SWEET family evolution in six species, with former duplications more important in pear. Gene expression results suggested that PbSWEET15 and PbSWEET17 have no expression in any tissues because of critical lost residues and that 62.5% of PbSWEET duplicate gene pairs have functional divergence. Additionally, PbSWEET6, PbSWEET7 and PbSWEET14 were found to play important roles in sucrose efflux from leaves, and the high expression of PbSWEET1 and PbSWEET2 might contribute to unloading sucrose from the phloem in the stem. Finally, PbSWEET5, PbSWEET9 and PbSWEET10 might contribute to pollen development. Overall, our study provides important insights into the evolution of the SWEET gene family in pear and four other Rosaceae, and the important candidate PbSWEET genes involved in the development of different tissues were identified in pear.

A New Insight into the Evolution and Functional Divergence of SWEET Transporters in Chinese White Pear (Pyrus bretschneideri).

Sugars Will Eventually be Exported Transporters (SWEET) are a novel type of sugar transporter that plays crucial roles in multiple biological processes. From banana, for the first time, 25 SWEET genes which could be classified into four subfamilies were identified. Majority of MaSWEETs in each subfamily shared similar gene structures and conserved motifs. Comprehensive transcriptomic analysis of two banana genotypes revealed differential expression patterns of MaSWEETs in different tissues, at various stages of fruit development and ripening, and in response to abiotic and biotic stresses. More than 80% MaSWEETs were highly expressed in BaXi Jiao (BX, Musa acuminata AAA group, cv. Cavendish), in sharp contrast to Fen Jiao (FJ, M. acuminata AAB group) when pseudostem was first emerged. However, MaSWEETs in FJ showed elevated expression under cold, drought, salt, and fungal disease stresses, but not in BX. Interaction networks and co-expression assays further revealed that MaSWEET-mediated networks participate in fruit development signaling and abiotic/biotic stresses, which was strongly activated during early stage of fruit development in BX. This study provides new insights into the complex transcriptional regulation of SWEETs, as well as numerous candidate genes that promote early sugar transport to improve fruit quality and enhance stress resistance in banana.

Genome-wide analyses of SWEET family proteins reveal involvement in fruit development and abiotic/biotic stress responses in banana.

The sugar content of Solanum lycopersicum (tomato) fruit is a primary determinant of taste and quality Cultivated tomato fruit are characterized by near-equimolar levels of the hexoses glucose and fructose, derived from the hydrolysis of translocated sucrose As fructose is perceived as approximately twice as sweet as glucose, increasing its concentration at the expense of glucose can improve tomato fruit taste Introgressions of the FgrH allele from the wild species Solanum habrochaites (LA1777) into cultivated tomato increased the fructose-to-glucose ratio of the ripe fruit by reducing glucose levels and concomitantly increasing fructose levels In order to identify the function of the Fgr gene, we combined a fine-mapping strategy with RNAseq differential expression analysis of near-isogenic tomato lines The results indicated that a SWEET protein was strongly upregulated in the lines with a high fructose-to-glucose ratio Overexpressing the SWEET protein in transgenic tomato plants dramatically reduced the glucose levels and increased the fructose : glucose ratio in the developing fruit, thereby proving the function of the protein The SWEET protein was localized to the plasma membrane and expression of the SlFgr gene in a yeast line lacking native hexose transporters complemented growth with glucose, but not with fructose These results indicate that the SlFgr gene encodes a plasma membrane-localized glucose efflux transporter of the SWEET family, the overexpression of which reduces glucose levels and may allow for increased fructose levels This article identifies the function of the tomato Fgr gene as a SWEET transporter, the upregulation of which leads to a modified sugar accumulation pattern in the fleshy fruit The results point to the potential of the inedible wild species to improve fruit sugar accumulation via sugar transport mechanisms

https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.14035

Natural genetic variation for expression of a SWEET transporter among wild species of Solanum lycopersicum (tomato) determines the hexose composition of ripening tomato fruit.

Jia Xuan Han

Papers

Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato