Divisions of labor in the thiamin biosynthetic pathway among organs of maize

Guan, Jiahn‐Chou; Hasnain, Ghulam; Garrett, Timothy J.; Chase, Carlene A.; Gregory, Jesse F.; Hanson, Andrew D.; McCarty, Donald R.

doi:10.3389/fpls.2014.00370

Cited by 26 publications

(29 citation statements)

References 37 publications

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“…Both types of genes are expressed in developing grains, including endosperm tissue, at levels broadly comparable to those in leaves ( Supplementary Figures 5 and 6). As leaves are a major site of thiamin synthesis [38,39], this transcriptomic evidence supports the inference that thiamin is synthesized in cereal grains using a non-Cys THI4 as the thiazole synthase.…”

Section: Transcriptome Data Indicate That Cereal Grains Have a Complesupporting

confidence: 76%

“…To validate the assumption that wheat, barley, and oat grains express all the genes (besides THI4) needed to synthesize thiamin de novo, as is the case for maize endosperm [38], we searched wheat and barley RNA-seq datasets for expression data on THIC (which makes the pyrimidine moiety of thiamin) and TH1 (the bifunctional enzyme that phosphorylates the pyrimidine moiety and couples it to the thiazole moiety). Both types of genes are expressed in developing grains, including endosperm tissue, at levels broadly comparable to those in leaves ( Supplementary Figures 5 and 6).…”

Section: Transcriptome Data Indicate That Cereal Grains Have a Complementioning

confidence: 99%

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Bioinformatic and experimental evidence for suicidal and catalytic plant THI4s

Joshi

Beaudoin

Patterson

et al. 2020

Preprint

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Like fungi and some prokaryotes, plants use a thiazole synthase (THI4) to make the thiazole precursor of thiamin. Fungal THI4s are suicide enzymes that destroy an essential active-site Cys residue to obtain the sulfur atom needed for thiazole formation. In contrast, certain prokaryotic THI4s have no active-site Cys, use sulfide as sulfur donor, and are truly catalytic. The presence of a conserved activesite Cys in plant THI4s and other indirect evidence implies that they are suicidal. To confirm this, we complemented the Arabidopsis tz-1 mutant, which lacks THI4 activity, with a His-tagged Arabidopsis THI4 construct. LC-MS analysis of tryptic peptides of the THI4 extracted from leaves showed that the active-site Cys was predominantly in desulfurated form, consistent with THI4 having a suicide mechanism in planta. Unexpectedly, transcriptome datamining and deep proteome profiling showed that barley, wheat, and oat have both a widely expressed canonical THI4 with an active-site Cys, and a THI4-like paralog (non-Cys THI4) that has no active-site Cys and is the major type of THI4 in developing grains. Transcriptomic evidence also indicated that barley, wheat, and oat grains synthesize thiamin de novo, implying that their non-Cys THI4s synthesize thiazole. Structure modeling supported this inference, as did demonstration that non-Cys THI4s have significant capacity to complement thiazole auxotrophy in Escherichia coli. There is thus a prima facie case that non-Cys cereal THI4s, like their prokaryotic counterparts, are catalytic thiazole synthases. Bioenergetic calculations show that, relative to suicide THI4s, such enzymes could save substantial energy during the grain filling period. Short title: Suicidal and catalytic plant THI4 enzymes

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Section: Transcriptome Data Indicate That Cereal Grains Have a Complesupporting

confidence: 76%

Section: Transcriptome Data Indicate That Cereal Grains Have a Complementioning

confidence: 99%

Bioinformatic and experimental evidence for suicidal and catalytic plant THI4s

Joshi

Beaudoin

Patterson

et al. 2020

Preprint

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“…The biosynthesis of thiamine is uncommon from other vitamins. This is because previous study by Guan et al revealed that the energy cost of thiamine synthesis is higher as compared to other vitamin cofactors [42]. Therefore, the location of riboswitch at the initial pathway strongly suggests that a novel riboswitch regulates the regulation of thiamine.…”

Section: Thiamine Pyrophosphate: the Dominant Class Of Riboswitchmentioning

confidence: 94%

The Role of Thiamine in Plants and Current Perspectives in Crop Improvement

Subki¹,

Abidin²,

Yusof³

2018

B Group Vitamins - Current Uses and Perspectives

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Current research is focusing on selecting potential genes that can alleviate stress and produce disease-tolerant crop variety. The novel paradigm is to investigate the potential of thiamine as a crop protection molecule in plants. Thiamine or vitamin B 1 is important for primary metabolism for all living organisms. The active form, thiamine pyrophosphate (TPP), is a cofactor for the enzymes involved in the synthesis of amino acids, tricarboxylic acid cycle and pentose phosphate pathway. Recently, thiamine is shown to have a role in the processes underlying protection of plants against biotic and abiotic stresses. The aim of this chapter is to review the role of thiamine in plant growth and disease protection and also to highlight that TPP and its intermediates are involved in management of stress. The perspectives on its potential for manipulating the biosynthesis pathway in crop improvement will also be discussed.

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“…Plants can synthesize all B vitamins except B 12 (cyanocobalamin), making them an important source of vitamin nutrition. Moreover, recent studies highlight emerging roles of B vitamins in plant development (Guan et al, 2014;Colinas et al, 2016) and responses to stress (reviewed in Hanson et al, 2016). Biotin, pyridoxine, riboflavin, and thiamin mutants have been studied extensively in Arabidopsis (Li and R edei, 1969;Schneider et al, 1989;Patton et al, 1998;Wagner et al, 2006;Meinke et al, 2009;Hedtke et al, 2012;Hiltunen et al, 2012;Pommerrenig et al, 2013;Hasnain et al, 2013;Mimura et al, 2016;Hsieh et al, 2017) as well as maize (Woodward et al, 2010;Hasnain et al, 2013;Li et al, 2014;Yang et al, 2017b;Dong et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Construction and applications of a B vitamin genetic resource for investigation of vitamin‐dependent metabolism in maize

Suzuki

Mimura

et al. 2019

The Plant Journal

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Summary The B vitamins provide essential co‐factors for central metabolism in all organisms. In plants, B vitamins have surprising emerging roles in development, stress tolerance and pathogen resistance. Hence, there is a paramount interest in understanding the regulation of vitamin biosynthesis as well as the consequences of vitamin deficiency in crop species. To facilitate genetic analysis of B vitamin biosynthesis and functions in maize, we have mined the UniformMu transposon resource to identify insertional mutations in vitamin pathway genes. A screen of 190 insertion lines for seed and seedling phenotypes identified mutations in biotin, pyridoxine and niacin biosynthetic pathways. Importantly, isolation of independent insertion alleles enabled genetic confirmation of genotype‐to‐phenotype associations. Because B vitamins are essential for survival, null mutations often have embryo lethal phenotypes that prevent elucidation of subtle, but physiologically important, metabolic consequences of sub‐optimal (functional) vitamin status. To circumvent this barrier, we demonstrate a strategy for refined genetic manipulation of vitamin status based on construction of heterozygotes that combine strong and hypomorphic mutant alleles. Dosage analysis of pdx2 alleles in endosperm revealed that endosperm supplies pyridoxine to the developing embryo. Similarly, a hypomorphic bio1 allele enabled analysis of transcriptome and metabolome responses to incipient biotin deficiency in seedling leaves. We show that systemic pipecolic acid accumulation is an early metabolic response to sub‐optimal biotin status highlighting an intriguing connection between biotin, lysine metabolism and systemic disease resistance signaling. Seed‐stocks carrying insertions for vitamin pathway genes are available for free, public distribution via the Maize Genetics Cooperation Stock Center.

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Divisions of labor in the thiamin biosynthetic pathway among organs of maize

Cited by 26 publications

References 37 publications

Bioinformatic and experimental evidence for suicidal and catalytic plant THI4s

Bioinformatic and experimental evidence for suicidal and catalytic plant THI4s

The Role of Thiamine in Plants and Current Perspectives in Crop Improvement

Construction and applications of a B vitamin genetic resource for investigation of vitamin‐dependent metabolism in maize

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