Genome-wide characterization of 2-oxoglutarate and Fe(II)-dependent dioxygenase family genes in tomato during growth cycle and their roles in metabolism

Abstract

Background 2-Oxoglutarate and Fe(II)-dependent dioxygenases (2ODDs) belong to the 2-oxoglutarate-dependent dioxygenase (2OGD) superfamily and are involved in various vital metabolic pathways of plants at different developmental stages. These proteins have been extensively investigated in multiple model organisms. However, these enzymes have not been systematically analyzed in tomato. In addition, type I flavone synthase (FNSI) belongs to the 2ODD family and contributes to the biosynthesis of flavones, but this protein has not been characterized in tomato. Results A total of 131 2ODDs from tomato were identified and divided into seven clades by phylogenetic classification. The Sl2ODDs in the same clade showed similar intron/exon distributions and conserved motifs. The Sl2ODDs were unevenly distributed across the 12 chromosomes, with different expression patterns among major tissues and at different developmental stages of the tomato growth cycle. We characterized several Sl2ODDs and their expression patterns involved in various metabolic pathways, such as gibberellin biosynthesis and catabolism, ethylene biosynthesis, steroidal glycoalkaloid biosynthesis, and flavonoid metabolism. We found that the Sl2ODD expression patterns were consistent with their functions during the tomato growth cycle. These results indicated the significance of Sl2ODDs in tomato growth and metabolism. Based on this genome-wide analysis of Sl2ODDs, we screened six potential FNSI genes using a phylogenetic tree and coexpression analysis. However, none of them exhibited FNSI activity. Conclusions Our study provided a comprehensive understanding of the tomato 2ODD family and demonstrated the significant roles of these family members in plant metabolism. We also suggest that no FNSI genes in tomato contribute to the biosynthesis of flavones.

A Moss 2-Oxoglutarate/Fe(II)-Dependent Dioxygenases (2-ODD) Gene of Flavonoids Biosynthesis Positively Regulates Plants Abiotic Stress Tolerance

“…2-Oxoglutarate/Fe(II)-dependent dioxygenases (2-ODDs), non-heme iron-containing soluble proteins, participate in the synthesis of important plant hormones and diverse secondary metabolites (Farrow and Facchini, 2014;Wei et al, 2021). Flavonoids, the natural products present in plants, possess enormous chemical diversity due to the organization and modifications of the three-ring structure by 2-ODDs, cytochrome P450-dependent oxygenases (CYPs), glycosyltransferase, and O-methyltransferases (Wang et al, 2019).…”

“…Therefore, we concluded that Pn2-ODD1 contributed to the accumulation of anthocyanins and flavonol in Arabidopsis. 2-ODDs in the flavonoids biosynthesis pathway are involved in the growth and development, as well as stress responses of plants (Wei et al, 2021). Salinity stress can adversely hamper plant germination and growth, transpiration, and photosynthesis, which is one of the major threats to plant productivity (Wang et al, 2021a).…”

“…The 2-oxoglutarate/Fe(II)-dependent dioxygenases (2-ODDs) are non-heme iron-containing soluble proteins, which catalyze the oxidation reactions of diverse substrates, including hydroxylation, demethylation, desaturation, halogenation, and epimerization (Wang et al, 2021c;Wei et al, 2021). 2-ODDs mainly participate in the biosynthesis of various metabolic pathways, such as flavonoids, benzylisoquinoline alkaloids, glucosinolates, tropane alkaloids, and plant hormones (Kawai et al, 2014;Wang et al, 2019).…”

The Flavonoid Biosynthesis Network in Plants

“…FNSIs are soluble 2-oxoglutarate- and Fe 2+ -dependent dioxygenases mainly found in members of the Apiaceae [ 62 ]. Meanwhile, FNSII members belong to the NADPH- and oxygen-dependent cytochrome P450 membrane-bound monooxygenases and are widely distributed in higher plants [ 63 , 64 ]. FNS is the key enzyme in flavone formation.…”

Substrates and Loaded Iron Ions Relative Position Influence the Catalytic Characteristics of the Metalloenzymes Angelica archangelica Flavone Synthase I and Camellia sinensis Flavonol Synthase

“…FNS I and FLS belong to the 2-Oxoglutarate-dependent dioxygenase (2ODGs, Kawai et al, 2014 ) superfamily (FNS I into DOXC28 and FLS into DOXC47). Both FNS Ⅰ and FLS can exert catalytic activity in vitro ( Halbwirth et al, 2006 ; Wang Y. et al, 2021 ; Wei et al, 2021 ). The FNS I has a similar structure to the FLS, and the conserved amino acids of FNS I from different sources are also highly conserved in FLS.…”