The importance of thiamine (vitamin B1) in plant health: From crop yield to biofortification

Abstract

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.

Keywords: Biofortification; coenzyme; defense; food security; genetic engineering; metabolism; micronutrient; physiology; plant; plant biochemistry; plant defense; thiamine; vitamin; yield.

Figure 1.

Broad classification of vitamins. Vitamins are divided into two general groups, those that are fat-soluble (A, D, E, and K) and those that are water-soluble (B₁, B₂, B₃, B₅, B₆, B₇, B₉, B₁₂, and C).

Figure 2.

Chemical structures of the vitamin B₁ family. The basic unit thiamine (blue) is shown at the top, comprising pyrimidine (purple) and thiazolium (pink) heterocycles linked by a methylene bridge (green). Thiamine derivatives vary in their phosphorylation states (black) and adenosylation states (red) and include TMP, TDP, TTP, ATDP, and ATTP. Those marked with an asterisk have been implicated as signaling molecules.

Figure 3.

Biosynthesis, transport, and roles of the coenzyme thiamine diphosphate in the model plant Arabidopsis. TDP biosynthesis (black) and its roles in the plant cell (blue dashed arrows, coenzyme activity) are displayed, with currently uncharacterized aspects of the pathways shown in gray. TMP is generated from the condensation of HMP-PP and HET-P, catalyzed via TH1 in the chloroplast. HET-P is synthesized by THI1 and a NUDIX hydrolase using NAD⁺, glycine, and a sulfur atom from the THI1 backbone, which renders this protein inactive as a catalyst for this reaction after one cycle (*). HMP-PP is formed from aminoimidazole ribonucleotide (AIR) by THIC and the phosphorylation activity of TH1. To generate the coenzyme form, TDP, TMP is first dephosphorylated to thiamine catalyzed by TH2/PALE1 in the cytosol (or mitochondrion) or uncharacterized phosphatases (in the chloroplast or cytosol) before phosphorylation to TDP by TPK in the cytosol. TDP has many roles in the cell, including in a negative feedback loop whereby TDP regulates thiamine biosynthesis through THIC gene expression in the nucleus via a riboswitch. TDP may be transported from the cytosol into the plastid via the nucleotide cation symporter 1 (NCS1), and into the mitochondrion by thiamine phosphate carriers (TPC1 and TPC2), whereas other thiamine vitamer transporters have not yet been characterized, particularly at the chloroplast envelope (gray). Enzymes requiring TDP as a coenzyme (dashed arrows) take key positions in central metabolism; in the chloroplast, TDP is involved in carbon assimilation, acting as a coenzyme for the Calvin cycle enzyme transketolase (TK) and for the TDP-dependent enzymes 2-deoxyxylulose 5-phosphate synthase (DXPS) and acetohydroxyacid synthase (AHAS) for isoprenoid and branched-chain amino acid biosynthesis, respectively. Another TDP-dependent enzyme, pyruvate dehydrogenase (PDH), is involved in lipid biosynthesis in the chloroplast. In the cytosol, TDP-dependent enzymes include TK in the pentose phosphate pathway, important for generating NADPH and pentoses, and also pyruvate decarboxylase (PDC) involved in anaerobic respiration/fermentation. In the mitochondrion, the TDP-dependent enzyme PDH is involved in feeding carbon into the TCA cycle, and α-ketoglutarate dehydrogenase (α-KGDH) is a key enzyme that modulates flux through the TCA cycle, affecting the redox, energy, and nitrogen balance of the cell. Branched-chain oxy-acid dehydrogenase (BCOADH) is a mitochondrial TDP-dependent enzyme complex that is involved in branched-chain amino acid catabolism.

Figure 4.

Importance of maintaining thiamine diphosphate balance in plants. TDP levels are regulated by the circadian clock, light/dark cycles, and a riboswitch. Balancing of TDP levels is important and may in turn be integrated into the balance of carbon (C) and nitrogen (N) that yields healthy thriving plants possibly mediated through α-ketoglutarate (α-KG) abundance. α-KG lies at the intersection between carbon and nitrogen metabolism and is metabolized by α-ketoglutarate dehydrogenase (not shown) during carbon metabolism by the TCA cycle or GDH during nitrogen metabolism. ATTP and TTP act as allosteric activators of GDH in mammalian systems, but a similar function in plants has not yet been explored. Application of thiamine primes plants against biotic stress via up-regulation of PR genes and salicyclic acid (SA). Thiamine also positively influences against abiotic stress via abscisic acid (ABA). Inhibition of riboswitch function (red line) leads to TDP imbalance. Inappropriate perturbation of TDP levels impacts carbon/nitrogen balance, plant health, and yield. This figure was made with BioRender.