The genus Solanum comprises three food crops (potato, tomato, and eggplant), which are consumed on daily basis worldwide and also producers of notorious anti-nutritional steroidal glycoalkaloids (SGAs). Hydroxylated SGAs (i.e. leptinines) serve as precursors for leptines that act as defenses against Colorado Potato Beetle (Leptinotarsa decemlineata Say), an important pest of potato worldwide. However, SGA hydroxylating enzymes remain unknown. Here, we discover that 2-OXOGLUTARATE-DEPENDENT-DIOXYGENASE (2-ODD) enzymes catalyze SGA-hydroxylation across various Solanum species. In contrast to cultivated potato, Solanum chacoense, a widespread wild potato species, has evolved a 2-ODD enzyme leading to the formation of leptinines. Furthermore, we find a related 2-ODD in tomato that catalyzes the hydroxylation of the bitter α-tomatine to hydroxytomatine, the first committed step in the chemical shift towards downstream ripening-associated non-bitter SGAs (e.g. esculeoside A). This 2-ODD enzyme prevents bitterness in ripe tomato fruit consumed today which otherwise would remain unpleasant in taste and more toxic.

Halophytes are able to thrive in salt concentrations that would kill 99% of other plant species, and identifying their salt-adaptive mechanisms has great potential for improving the tolerance of crop plants to salinized soils. Much research has focused on the physiological basis of halophyte salt tolerance, whereas the elucidation of molecular mechanisms has traditionally lagged behind due to the absence of a model halophyte system. However, over the last decade and a half, two Arabidopsis (Arabidopsis thaliana) relatives, Eutrema salsugineum and Schrenkiella parvula, have been established as transformation-competent models with various genetic resources including high-quality genome assemblies. These models have facilitated powerful comparative analyses with salt-sensitive Arabidopsis to unravel the genetic adaptations that enable a halophytic lifestyle. The aim of this review is to explore what has been learned about halophytism using E. salsugineum and S. parvula. We consider evidence from physiological and molecular studies suggesting that differences in salt tolerance between related halophytes and salt-sensitive plants are associated with alterations in the regulation of basic physiological, biochemical, and molecular processes. Furthermore, we discuss how salt tolerance mechanisms of the halophytic models are reflected at the level of their genomes, where evolutionary processes such as subfunctionalization and/or neofunctionalization have altered the expression and/or functions of genes to facilitate adaptation to saline conditions. Lastly, we summarize the many areas of research still to be addressed with E. salsugineum and S. parvula as well as obstacles hindering further progress in understanding halophytism.

Plants are unsurpassed biochemists that synthesize a plethora of molecules in response to an ever-changing environment. The majority of these molecules, considered as specialized metabolites, effectively protect the plant against pathogens and herbivores. However, this defense most probably comes at a great expense, leading to reduction of growth (known as the ‘growth–defense trade-off’). Plants employ several strategies to reduce the high metabolic costs associated with chemical defense. Production of specialized metabolites is tightly regulated by a network of transcription factors facilitating its fine-tuning in time and space. Multifunctionality of specialized metabolites—their effective recycling system by re-using carbon, nitrogen, and sulfur, thus re-introducing them back to the primary metabolite pool—allows further cost reduction. Spatial separation of biosynthetic enzymes and their substrates, and sequestration of potentially toxic substances and conversion to less toxic metabolite forms are the plant’s solutions to avoid the detrimental effects of metabolites they produce as well as to reduce production costs. Constant fitness pressure from herbivores, pathogens, and abiotic stressors leads to honing of specialized metabolite biosynthesis reactions to be timely, efficient, and metabolically cost-effective. In this review, we assess the costs of production of specialized metabolites for chemical defense and the different plant mechanisms to reduce the cost of such metabolic activity in terms of self-toxicity and growth.

Summary: Solanum steroidal glycoalkaloids (SGAs) are renowned defence metabolites exhibiting spectacular structural diversity. Genes and enzymes generating the SGA precursor pathway, SGA scaffold and glycosylated forms have been largely identified. Yet, the majority of downstream metabolic steps creating the vast repertoire of SGAs remain untapped. Here, we discovered that members of the 2‐OXOGLUTARATE‐DEPENDENT DIOXYGENASE (2‐ODD) family play a prominent role in SGA metabolism, carrying out three distinct backbone‐modifying oxidative steps in addition to the three formerly reported pathway reactions. The GLYCOALKALOID METABOLISM34 (GAME34) enzyme catalyses the conversion of core SGAs to habrochaitosides in wild tomato S. habrochaites. Cultivated tomato plants overexpressing GAME34 ectopically accumulate habrochaitosides. These habrochaitoside enriched plants extracts potently inhibit Puccinia spp. spore germination, a significant Solanaceae crops fungal pathogen. Another 2‐ODD enzyme, GAME33, acts as a desaturase (via hydroxylation and E/F ring rearrangement) forming unique, yet unreported SGAs. Conversion of bitter α‐tomatine to ripe fruit, nonbitter SGAs (e.g. esculeoside A) requires two hydroxylations; while the known GAME31 2‐ODD enzyme catalyses hydroxytomatine formation, we find that GAME40 catalyses the penultimate step in the pathway and generates acetoxy‐hydroxytomatine towards esculeosides accumulation. Our results highlight the significant contribution of 2‐ODD enzymes to the remarkable structural diversity found in plant steroidal specialized metabolism.