Iron assimilation and transcription factor controlled synthesis of riboflavin in plants

Vorwieger, Astrid; Gryczka, C.; Czihal, Andreas; Douchkov, Dimitar; Tiedemann, Jens; Mock, Hans‐Peter; Jakoby, Marc; Weißhaar, Bernd; Saalbach, Isolde; Bäumlein, Helmut

doi:10.1007/s00425-006-0476-9

Cited by 81 publications

(72 citation statements)

References 54 publications

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“…Specifically, Helicobacter pylori does not produce siderophores under Fe-limited conditions, but produces riboflavin that can reduce Fe(III) in ferritins (12). Sugar beet and sunflower roots excrete micromolar amounts of riboflavin-5Ј and riboflavin-3Ј sulfate when grown in Fe-poor soils, leading to reduction and uptake of Fe (42). In Pichia gulliermondii, growth in low-Fe(III) medium leads to riboflavin excretion, whereas mutations preventing ribof lavin overproduction significantly slow Fe-limited growth (43).…”

Section: Resultsmentioning

confidence: 99%

Shewanella secretes flavins that mediate extracellular electron transfer

Marsili¹,

Baron²,

Shikhare³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

1,737

1,507

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Bacteria able to transfer electrons to metals are key agents in biogeochemical metal cycling, subsurface bioremediation, and corrosion processes. More recently, these bacteria have gained attention as the transfer of electrons from the cell surface to conductive materials can be used in multiple applications. In this work, we adapted electrochemical techniques to probe intact biofilms of Shewanella oneidensis MR-1 and Shewanella sp. MR-4 grown by using a poised electrode as an electron acceptor. This approach detected redox-active molecules within biofilms, which were involved in electron transfer to the electrode. A combination of methods identified a mixture of riboflavin and riboflavin-5 -phosphate in supernatants from biofilm reactors, with riboflavin representing the dominant component during sustained incubations (>72 h). Removal of riboflavin from biofilms reduced the rate of electron transfer to electrodes by >70%, consistent with a role as a soluble redox shuttle carrying electrons from the cell surface to external acceptors. Differential pulse voltammetry and cyclic voltammetry revealed a layer of flavins adsorbed to electrodes, even after soluble components were removed, especially in older biofilms. Riboflavin adsorbed quickly to other surfaces of geochemical interest, such as Fe(III) and Mn(IV) oxy(hydr)oxides. This in situ demonstration of flavin production, and sequestration at surfaces, requires the paradigm of soluble redox shuttles in geochemistry to be adjusted to include binding and modification of surfaces. Moreover, the known ability of isoalloxazine rings to act as metal chelators, along with their electron shuttling capacity, suggests that extracellular respiration of minerals by Shewanella is more complex than originally conceived.bioelectrochemistry ͉ biogeochemistry ͉ redox mediator ͉ riboflavin

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Section: Resultsmentioning

confidence: 99%

Shewanella secretes flavins that mediate extracellular electron transfer

Marsili¹,

Baron²,

Shikhare³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

1,737

1,507

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“…Interestingly, however, free flavins, especially riboflavin, have been detected in the roots and/or root exudates of some taxonomically unrelated dicotyledonous plants, including tobacco and sunflower, growing under conditions of Fe deficiency [3,4]. Recently, Vorwieger et al [5] confirmed that the ectopic expression of Arabidopsis basic helix-loop-helix transcription factors, which are induced under Fe deficiency, induced riboflavin excretion in transgenic hairy roots of tobacco and sunflower, although not in those of tomato, which do not excrete riboflavin under Fe-deficient conditions. Hence, riboflavin secretion under Fe deficiency is genetically regulated.…”

Section: Introductionmentioning

confidence: 99%

Increased de novo riboflavin synthesis and hydrolysis of FMN are involved in riboflavin secretion from Hyoscyamus albus hairy roots under iron deficiency

Higa

Khandakar

Mori

et al. 2012

Plant Physiology and Biochemistry

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Riboflavin secretion by Hyoscyamus albus hairy roots under Fe deficiency was examined to determine where riboflavin is produced and whether production occurs via an enhancement of riboflavin biosynthesis or a stimulation of flavin mononucleotide (FMN) hydrolysis. Confocal fluorescent microscopy showed that riboflavin was mainly localized in the epidermis and cortex of the root tip and, at the cellular level, in the apoplast. The expressions of three genes involved in the de novo biosynthesis of riboflavin (GTP cyclohydrolase II/3,6, riboflavin synthase) were compared between Fe-starved and Fe-replete roots over a time course of 7 days, using RT-PCR. All three genes were found to be highly expressed over the period 1-7 days in the roots cultured under Fe deficiency. Since riboflavin secretion began to be detected only from 3 days, there was a lag phase observed between the increased transcript accumulations and riboflavin secretion. To determine whether FMN hydrolysis might contribute to the riboflavin secretion in Fe-deficient root cultures, FMN hydrolase activity was determined and was found to be substantially increased after 3 days, when riboflavin secretion became detectable. These results suggested that not only de novo riboflavin synthesis but also the hydrolysis of FMN contributes to riboflavin secretion under conditions of Fe deficiency. Respiration activity was assayed during the time-course, and was also found to be enhanced after 3 days under Fe deficiency, suggesting a possible link with riboflavin secretion. On the other hand, several respiratory inhibitors were found not to affect riboflavin synthase transcript accumulation.Key words: Hyoscyamus albus; hairy roots; iron deficiency; riboflavin secretion; riboflavin biosynthesis; FMN hydrolase; respiration. RibA: GTP cyclohydrolase II · RibB: 3,4-dihydroxy-2-butanone 4-phosphate synthase · RibC: 6,7-dimethyl-8-ribityllumazine synthase · RibD: riboflavin synthase

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“…The identiWcation of transcription factors in Arabidopsis is eased by the availability of the complete genome sequence and functional genome projects. In a recent study Vorwieger et al (2007) identiWed two iron-regulated BHLH genes whose function in Arabidopsis was however, not investigated any further by these authors. Here, we studied regulation of these two BHLH genes (BHLH038, BHLH039) and of their closest homologs (BHLH100, BHLH101) that we termed subgroup Ib BHLH genes in leaves and roots in various nutritional situations as well as in mutant backgrounds and split-root situations related to iron deWciency.…”

Section: Introductionmentioning

confidence: 99%

Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana

Hong-yu

Klatte

Jakoby

et al. 2007

Planta

225

202

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Networks of transcription factors control physiological, developmental and environmental responses. Root iron acquisition responses are controlled by the essential bHLH protein FIT. Recently, two group Ib BHLH genes were reported to be iron deWciency-regulated. Here, we studied expression patterns of these two group Ib BHLH genes and of their two closest homologs to analyze whether their regulation would support a function in iron deWciency responses. We found that BHLH038, BHLH039, BHLH100 and BHLH101 (comprising a subgroup of BHLH Ib genes) were up regulated by iron deWciency in roots and leaves. Single insertion mutants had no visible phenotype and were capable of inducing root iron acquisition responses, presumably due to functional redundancy. SpeciWc metal treatments like nickel, high zinc or high copper resulted in induction of the four BHLH Ib genes whereas high iron, low copper and low zinc repressed gene expression. Induction of the four BHLH Ib genes was also found in multiple iron acquisition mutants including Wt. Ectopic activation of FIT did not suppress the four BHLH Ib genes. Split-root analyses using promoter-GUS lines showed that FIT and BHLH100 promoters were controlled by diVerent local and systemic signals involved in their regulation by iron. These results indicated that the four BHLH Ib genes were induced independently from FIT by conditions causing iron deWciency. Taken together, BHLH038, BHLH039, BHLH100 and BHLH101 function diVerently from FIT and may be involved in mediating a signal related to iron deWciencyinduced stress and/or internal iron homeostasis.

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Iron assimilation and transcription factor controlled synthesis of riboflavin in plants

Cited by 81 publications

References 54 publications

Shewanella secretes flavins that mediate extracellular electron transfer

Shewanella secretes flavins that mediate extracellular electron transfer

Increased de novo riboflavin synthesis and hydrolysis of FMN are involved in riboflavin secretion from Hyoscyamus albus hairy roots under iron deficiency

Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana

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