B vitamins are a source of coenzymes for a vast array of enzyme reactions, particularly those of metabolism. As metabolism is the basis of decisions that drive maintenance, growth, and development, B ...vitamin-derived coenzymes are key components that facilitate these processes. For over a century, we have known about these essential compounds and have elucidated their pathways of biosynthesis, repair, salvage, and degradation in numerous organisms. Only now are we beginning to understand their importance for regulatory processes, which are becoming an important topic in plants. Here, I highlight and discuss emerging evidence on how B vitamins are integrated into vital processes, from energy generation and nutrition to gene expression, and thereby contribute to the coordination of growth and developmental programs, particularly those that concern maintenance of a stable state, which is the foundational tenet of plant homeostasis. Expected final online publication date for the
, Volume 75 is May 2024. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Ensuring that people have access to sufficient and nutritious food is necessary for a healthy life and the core tenet of food security. With the global population set to reach 9.8 billion by 2050, ...and the compounding effects of climate change, the planet is facing challenges that necessitate significant and rapid changes in agricultural practices. In the effort to provide food in terms of calories, the essential contribution of micronutrients (vitamins and minerals) to nutrition is often overlooked. Here, we focus on the importance of thiamine (vitamin B1) in plant health and discuss its impact on human health. Vitamin B1 is an essential dietary component, and deficiencies in this micronutrient underlie several diseases, notably nervous system disorders. The predominant source of dietary vitamin B1 is plant-based foods. Moreover, vitamin B1 is also vital for plants themselves, and its benefits in plant health have received less attention than in the human health sphere. In general, vitamin B1 is well-characterized for its role as a coenzyme in metabolic pathways, particularly those involved in energy production and central metabolism, including carbon assimilation and respiration. Vitamin B1 is also emerging as an important component of plant stress responses, and several noncoenzyme roles of this vitamin are being characterized. We summarize the importance of vitamin B1 in plants from the perspective of food security, including its roles in plant disease resistance, stress tolerance, and crop yield, and review the potential benefits of biofortification of crops with increased vitamin B1 content to improve human health.
In plants, primary and specialized metabolism have classically been distinguished as either essential for growth or required for survival in a particular environment. Coenzymes (organic cofactors) ...are essential for growth but their importance to specialized metabolism is often not considered. In line with the recent proposal of viewing primary and specialized metabolism as an integrated whole rather than segregated lots with a defined interface, we highlight here the importance of collating information on the regulation of coenzyme supply with metabolic demands using examples of vitamin B derived coenzymes. We emphasize that coenzymes can have enormous influence on the outcome of metabolic as well as engineered pathways and should be taken into account in the era of synthetic biology.
•B vitamin derived coenzymes are essential for primary and specialized metabolism.•The role of coenzymes in specialized metabolism deserves more attention.•Coenzyme supply must be coordinated between primary and specialized metabolism.•Sufficient coenzyme supply is crucial in metabolic engineering.•Coenzymes should be considered in measurements of enzyme turnover rates.
Summary
Plant fitness is a measure of the capacity of a plant to survive and reproduce in its particular environment. It is inherently dependent on plant health. Molecular timekeepers like the ...circadian clock enhance fitness due to their ability to coordinate biochemical and physiological processes with the environment on a daily basis. Central metabolism underlies these events and it is well established that diel metabolite adjustments are intimately and reciprocally associated with the genetically encoded clock. Thus, metabolic pathway activities are time‐of‐day regulated. Metabolite rhythms are driven by enzymes, a major proportion of which rely on organic coenzymes to facilitate catalysis. The B vitamin complex is the key provider of coenzymes in all organisms. Emerging evidence suggests that B vitamin levels themselves undergo daily oscillations in animals but has not been studied in any depth in plants. Moreover, it is rarely considered that daily rhythmicity in coenzyme levels may dictate enzyme activity levels and therefore metabolite levels. Here we put forward the proposal that B‐vitamin‐derived coenzyme rhythmicity is intertwined with metabolic and clock derived rhythmicity to achieve a tripartite homeostasis integrated into plant fitness.
•Gene clusters in plants encode secondary metabolites implicated in defense.•Clustering of entire pathways facilitates co-inheritance and co-regulation.•Cluster prediction and regulation studies ...require a multidisciplinary approach.•Cluster knowledge can serve crop biofortification and industrial production.
Gene clusters are common features of prokaryotic genomes also present in eukaryotes. Most clustered genes known are involved in the biosynthesis of secondary metabolites. Although horizontal gene transfer is a primary source of prokaryotic gene cluster (operon) formation and has been reported to occur in eukaryotes, the predominant source of cluster formation in eukaryotes appears to arise de novo or through gene duplication followed by neo- and sub-functionalization or translocation. Here we aim to provide an overview of the current knowledge and open questions related to plant gene cluster functioning, assembly, and regulation. We also present potential research approaches and point out the benefits of a better understanding of gene clusters in plants for both fundamental and applied plant science.
•B vitamins are provisioned in plants by de novo, salvage and damage processing pathways.•They are linked to developmental, epigenetic, stress and metabolic cofactor roles.•Non-cofactor structural ...derivatives may be part of the B vitamin economy.•Division of labor may handle the costs of the functional load.
Plants use B vitamin compounds as cofactors for metabolism. Biosynthesis de novo of these metabolites in plants is almost fully elucidated. However, salvaging of precursors as well as cofactor derivatives is only being unraveled. Furthermore, processing of these compounds when damaged by cellular activities to prevent deleterious effects on metabolism is emerging. Recent investigations indicate that the role of B vitamins goes beyond metabolism and are being linked with epigenetic traits, specific developmental cues, the circadian clock, as well as abiotic and biotic stress responses. More in depth investigations on the regulation of the provision of these compounds through biosynthesis de novo, salvage and transport is suggesting that plants may share the cost of this load by division of labor.
Nitric oxide (NO) has emerged as an important signal molecule in plants, having myriad roles in plant development. In addition, NO also orchestrates both biotic and abiotic stress responses, during ...which intensive cellular metabolic reprogramming occurs. Integral to these responses is the location of NO biosynthetic and scavenging pathways in diverse cellular compartments, enabling plants to effectively organize signal transduction pathways. NO regulates plant metabolism and, in turn, metabolic pathways reciprocally regulate NO accumulation and function. Thus, these diverse cellular processes are inextricably linked. This review addresses the numerous redox pathways, located in the various subcellular compartments that produce NO, in addition to the mechanisms underpinning NO scavenging. We focus on how this molecular dance is integrated into the metabolic state of the cell. Within this context, a reciprocal relationship between NO accumulation and metabolite production is often apparent. We also showcase cellular pathways, including those associated with nitrate reduction, that provide evidence for this integration of NO function and metabolism. Finally, we discuss the potential importance of the biochemical reactions governing NO levels in determining plant responses to a changing environment.
Nitric oxide (NO) has emerged as an important signal molecule in plants, having myriad roles in plant biotic and abiotic stress responses, during which intensive cellular metabolic reprogramming occurs. Numerous redox pathways, located in the various subcellular compartments produce NO, in addition to the mechanisms that underpin NO scavenging. Here, we focus on how this molecular dance is integrated into the metabolic state of the cell.In addition, we discuss the potential importance of the biochemical reactions governing NO levels in determining plant responses to a changing environment.
SUMMARY
B vitamins are a group of water‐soluble micronutrients that are required in all life forms. With the lack of biosynthetic pathways, humans depend on dietary uptake of these compounds, either ...directly or indirectly, from plant sources. B vitamins are frequently given little consideration beyond their role as enzyme accessory factors and are assumed not to limit metabolism. However, it should be recognized that each individual B vitamin is a family of compounds (vitamers), the regulation of which has dedicated pathways. Moreover, it is becoming increasingly evident that individual family members have physiological relevance and should not be sidelined. Here, we elaborate on the known forms of vitamins B1, B6 and B9, their distinct functions and importance to metabolism, in both human and plant health, and highlight the relevance of vitamer homeostasis. Research on B vitamin metabolism over the past several years indicates that not only the total level of vitamins but also the oft‐neglected homeostasis of the various vitamers of each B vitamin is essential to human and plant health. We briefly discuss the potential of plant biology studies in supporting human health regarding these B vitamins as essential micronutrients. Based on the findings of the past few years we conclude that research should focus on the significance of vitamer homeostasis – at the organ, tissue and subcellular levels – which could improve the health of not only humans but also plants, benefiting from cross‐disciplinary approaches and novel technologies.
Significance Statement
We provide an up‐to‐date review on the metabolism of selected B vitamins in humans and plants in the context of the health of both. We emphasize the significance of vitamer homeostasis, which could improve the health of not only humans but also plants, benefiting from cross‐disciplinary approaches and novel technologies.
Plants sense temperature changes and respond by altering growth and metabolic activity to acclimate to the altered environmental conditions. The B vitamins give rise to vital coenzymes that are ...indispensable for growth and development but their inherent reactive nature renders them prone to destruction especially under stress conditions. Therefore, plant survival strategies would be expected to include mechanisms to sustain B vitamin supply under demanding circumstances. Here, using the example of vitamin B₆, we investigate the regulation of biosynthesis across eudicot and monocot species under heat stress. Most eudicots carry a pseudoenzyme PDX1.2 that is a noncatalytic homolog of the PDX1 subunit of the vitamin B₆ biosynthesis protein machinery, PYRIDOXINE BIOSYNTHESIS PROTEIN1. Using Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum) as models, we show that PDX1.2 is transcriptionally regulated by the HSFA1 transcription factor family. Monocots only carry catalytic PDX1 homologs that do not respond to heat stress as demonstrated for rice (Oryza sativa) and maize (Zea mays), suggesting fundamental differences in the regulation of vitamin B₆ biosynthesis across the two lineages. Investigation of the molecular mechanism of PDX1.2 transcription reveals two alternative transcriptional start sites, one of which is exclusive to heat stress. Further data suggest that PDX1.2 leads to stabilization of the catalytic PDX1s under heat stress conditions, which would serve to maintain vitamin B₆ homeostasis in times of need in eudicots that carry this gene. Our analyses indicate an important abiotic stress tolerance strategy in several eudicots, which has not been evolutionarily adapted (or is not required) by monocots such as grasses.
Vitamin B6 is well known in its biochemically active form as pyridoxal 5'-phosphate, an essential cofactor of numerous metabolic enzymes. The vitamin is also implicated in numerous human body ...functions ranging from modulation of hormone function to its recent discovery as a potent antioxidant. Its de novo biosynthesis occurs only in bacteria, fungi and plants, making it an essential nutrient in the human diet. Despite its paramount importance, its biosynthesis was predominantly investigated in Escherichia coli, where it is synthesized from the condensation of deoxyxylulose 5-phosphate and 4-phosphohydroxy-L-threonine catalysed by the concerted action of PdxA and PdxJ. However, it has now become clear that the majority of organisms capable of producing this vitamin do so via a different route, involving precursors from glycolysis and the pentose phosphate pathway. This alternative pathway is characterized by the presence of two genes, Pdx1 and Pdx2. Their discovery has sparked renewed interest in vitamin B6, and numerous studies have been conducted over the last few years to characterize the new biosynthesis pathway. Indeed, enormous progress has been made in defining the nature of the enzymes involved in both pathways, and important insights have been provided into their mechanisms of action. In the present review, we summarize the recent advances in our knowledge of the biosynthesis of this versatile molecule and compare the two independent routes to the biosynthesis of vitamin B6. Surprisingly, this comparison reveals that the key biosynthetic enzymes of both pathways are, in fact, very similar both structurally and mechanistically.
PDF
