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Article ; Online: The Mechanisms of Molybdate Distribution and Homeostasis with Special Focus on the Model Plant

Weber, Jan-Niklas / Minner-Meinen, Rieke / Kaufholdt, David

2023 Volume 29, Issue 1

Abstract: This review article deals with the pathways of cellular and global molybdate distribution in plants, especially with a full overview for the model ... ...

Abstract	This review article deals with the pathways of cellular and global molybdate distribution in plants, especially with a full overview for the model plant
MeSH term(s)	Humans ; Molybdenum ; Arabidopsis ; Homeostasis ; Biological Transport
Chemical Substances	molybdate (14259-85-9) ; Molybdenum (81AH48963U)
Language	English
Publishing date	2023-12-20
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	1413402-0
ISSN	1420-3049 ; 1431-5165 ; 1420-3049
ISSN (online)	1420-3049
ISSN	1431-5165 ; 1420-3049
DOI	10.3390/molecules29010040
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Article ; Online: The Mechanisms of Molybdate Distribution and Homeostasis with Special Focus on the Model Plant Arabidopsis thaliana

Jan-Niklas Weber / Rieke Minner-Meinen / David Kaufholdt

Molecules, Vol 29, Iss 1, p

2023 Volume 40

Abstract: This review article deals with the pathways of cellular and global molybdate distribution in plants, especially with a full overview for the model plant Arabidopsis thaliana . In its oxidized state as bioavailable molybdate, molybdenum can be absorbed ... ...

Abstract	This review article deals with the pathways of cellular and global molybdate distribution in plants, especially with a full overview for the model plant Arabidopsis thaliana . In its oxidized state as bioavailable molybdate, molybdenum can be absorbed from the environment. Especially in higher plants, molybdenum is indispensable as part of the molybdenum cofactor (Moco), which is responsible for functionality as a prosthetic group in a variety of essential enzymes like nitrate reductase and sulfite oxidase. Therefore, plants need mechanisms for molybdate import and transport within the organism, which are accomplished via high-affinity molybdate transporter (MOT) localized in different cells and membranes. Two different MOT families were identified. Legumes like Glycine max or Medicago truncatula have an especially increased number of MOT1 family members for supplying their symbionts with molybdate for nitrogenase activity. In Arabidopsis thaliana especially, the complete pathway followed by molybdate through the plant is traceable. Not only the uptake from soil by MOT1.1 and its distribution to leaves, flowers, and seeds by MOT2-family members was identified, but also that inside the cell. the transport trough the cytoplasm and the vacuolar storage mechanisms depending on glutathione were described. Finally, supplying the Moco biosynthesis complex by MOT1.2 and MOT2.1 was demonstrated.
Keywords	molybdate transporter ; molybdate distribution ; homeostasis ; Arabidopsis thaliana ; Organic chemistry ; QD241-441
Subject code	580
Language	English
Publishing date	2023-12-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
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Article ; Online: Biosynthesis of polyprenylated xanthones in Hypericum perforatum roots involves 4-prenyltransferase.

Sayed, Hesham M B / Nassar, Sara / Kaufholdt, David / Beerhues, Ludger / Liu, Benye / El-Awaad, Islam

Plant physiology

2023 Volume 192, Issue 4, Page(s) 2971–2988

Abstract: Polyprenylated xanthones are natural products with a multitude of biological and pharmacological activities. However, their biosynthetic pathway is not completely understood. In this study, metabolic profiling revealed the presence of 4-prenylated 1,3,5, ... ...

Abstract	Polyprenylated xanthones are natural products with a multitude of biological and pharmacological activities. However, their biosynthetic pathway is not completely understood. In this study, metabolic profiling revealed the presence of 4-prenylated 1,3,5,6-tetrahydroxyxanthone derivatives in St. John's wort (Hypericum perforatum) root extracts. Transcriptomic data mining led to the detection of 5 variants of xanthone 4-prenyltransferase (HpPT4px) comprising 4 long variants (HpPT4px-v1 to HpPT4px-v4) and 1 short variant (HpPT4px-sh). The full-length sequences of all 5 variants were cloned and heterologously expressed in yeast (Saccharomyces cerevisiae). Microsomes containing HpPT4px-v2, HpPT4px-v4, and HpPT4px-sh catalyzed the addition of a prenyl group at the C-4 position of 1,3,5,6-tetrahydroxyxanthone; 1,3,5-trihydroxyxanthone; and 1,3,7-trihydroxyxanthone, whereas microsomes harboring HpPT4px-v1 and HpPT4px-v3 additionally accepted 1,3,6,7-tetrahydroxyxanthone. HpPT4px-v1 produced in Nicotiana benthamiana displayed the same activity as in yeast, while HpPT4px-sh was inactive. The kinetic parameters of HpPT4px-v1 and HpPT4px-sh chosen as representative variants indicated 1,3,5,6-tetrahydroxyxanthone as the preferred acceptor substrate, rationalizing that HpPT4px catalyzes the first prenylation step in the biosynthesis of polyprenylated xanthones in H. perforatum. Dimethylallyl pyrophosphate was the exclusive prenyl donor. Expression of the HpPT4px transcripts was highest in roots and leaves, raising the question of product translocation. C-terminal yellow fluorescent protein fusion of HpPT4px-v1 localized to the envelope of chloroplasts in N. benthamiana leaves, whereas short, truncated, and masked signal peptides led to the disruption of plastidial localization. These findings pave the way for a better understanding of the prenylation of xanthones in plants and the identification of additional xanthone-specific prenyltransferases.
MeSH term(s)	Hypericum/genetics ; Hypericum/metabolism ; Dimethylallyltranstransferase/genetics ; Dimethylallyltranstransferase/metabolism ; Saccharomyces cerevisiae/genetics ; Saccharomyces cerevisiae/metabolism ; Xanthones/metabolism ; Xanthones/pharmacology ; Plant Extracts/pharmacology
Chemical Substances	prenyl ; Dimethylallyltranstransferase (EC 2.5.1.1) ; Xanthones ; Plant Extracts
Language	English
Publishing date	2023-04-16
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
DOI	10.1093/plphys/kiad219
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Article ; Online: Cytosolic aromatic aldehyde dehydrogenase provides benzoic acid for xanthone biosynthesis in Hypericum.

Singh, Poonam / Kaufholdt, David / Awadalah, Mina / Hänsch, Robert / Beerhues, Ludger / Gaid, Mariam

Plant physiology and biochemistry : PPB

2021 Volume 160, Page(s) 82–93

Abstract: Benzoic acid is a building block of a multitude of well-known plant natural products, such as paclitaxel and cocaine. Its simple chemical structure contrasts with its complex biosynthesis. Hypericum species are rich in polyprenylated benzoic acid-derived ...

Abstract	Benzoic acid is a building block of a multitude of well-known plant natural products, such as paclitaxel and cocaine. Its simple chemical structure contrasts with its complex biosynthesis. Hypericum species are rich in polyprenylated benzoic acid-derived xanthones, which have received attention due to their biological impact on human health. The upstream biosynthetic sequence leading to xanthones is still incomplete. To supply benzoic acid for xanthone biosynthesis, Hypericum calycinum cell cultures use the CoA-dependent non-β-oxidative pathway, which starts with peroxisomal cinnamate CoA-ligase (HcCNL). Here, we use the xanthone-producing cell cultures to identify the transcript for benzaldehyde dehydrogenase (HcBD), a pivotal player in the non-β-oxidative pathways. In addition to benzaldehyde, the enzyme efficiently catalyzes the oxidation of trans-cinnamaldehyde in vitro. The enzymatic activity is strictly dependent on the presence of NAD
MeSH term(s)	Aldehyde Oxidoreductases/metabolism ; Benzoic Acid/metabolism ; Hypericum/enzymology ; Plant Proteins/metabolism ; Xanthones/metabolism
Chemical Substances	Plant Proteins ; Xanthones ; Benzoic Acid (8SKN0B0MIM) ; Aldehyde Oxidoreductases (EC 1.2.-) ; benzaldehyde dehydrogenase (NAD+) (EC 1.2.1.28)
Language	English
Publishing date	2021-01-12
Publishing country	France
Document type	Journal Article
ZDB-ID	742978-2
ISSN	1873-2690 ; 0981-9428
ISSN (online)	1873-2690
ISSN	0981-9428
DOI	10.1016/j.plaphy.2021.01.011
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Article ; Online: A promiscuous coenzyme A ligase provides benzoyl-coenzyme A for xanthone biosynthesis in Hypericum.

Singh, Poonam / Preu, Lutz / Beuerle, Till / Kaufholdt, David / Hänsch, Robert / Beerhues, Ludger / Gaid, Mariam

The Plant journal : for cell and molecular biology

2020 Volume 104, Issue 6, Page(s) 1472–1490

Abstract: Benzoic acid-derived compounds, such as polyprenylated benzophenones and xanthones, attract the interest of scientists due to challenging chemical structures and diverse biological activities. The genus Hypericum is of high medicinal value, as ... ...

Abstract	Benzoic acid-derived compounds, such as polyprenylated benzophenones and xanthones, attract the interest of scientists due to challenging chemical structures and diverse biological activities. The genus Hypericum is of high medicinal value, as exemplified by H. perforatum. It is rich in benzophenone and xanthone derivatives, the biosynthesis of which requires the catalytic activity of benzoate-coenzyme A (benzoate-CoA) ligase (BZL), which activates benzoic acid to benzoyl-CoA. Despite remarkable research so far done on benzoic acid biosynthesis in planta, all previous structural studies of BZL genes and proteins are exclusively related to benzoate-degrading microorganisms. Here, a transcript for a plant acyl-activating enzyme (AAE) was cloned from xanthone-producing Hypericum calycinum cell cultures using transcriptomic resources. An increase in the HcAAE1 transcript level preceded xanthone accumulation after elicitor treatment, as previously observed with other pathway-related genes. Subcellular localization of reporter fusions revealed the dual localization of HcAAE1 to cytosol and peroxisomes owing to a type 2 peroxisomal targeting signal. This result suggests the generation of benzoyl-CoA in Hypericum by the CoA-dependent non-β-oxidative route. A luciferase-based substrate specificity assay and the kinetic characterization indicated that HcAAE1 exhibits promiscuous substrate preference, with benzoic acid being the sole aromatic substrate accepted. Unlike 4-coumarate-CoA ligase and cinnamate-CoA ligase enzymes, HcAAE1 did not accept 4-coumaric and cinnamic acids, respectively. The substrate preference was corroborated by in silico modeling, which indicated valid docking of both benzoic acid and its adenosine monophosphate intermediate in the HcAAE1/BZL active site cavity.
MeSH term(s)	Acyl Coenzyme A/metabolism ; Cloning, Molecular ; Coenzyme A Ligases/genetics ; Coenzyme A Ligases/metabolism ; Cytosol/enzymology ; Hypericum/enzymology ; Hypericum/metabolism ; Metabolic Networks and Pathways ; Molecular Docking Simulation ; Peroxisomes/enzymology ; Phylogeny ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Xanthones/metabolism
Chemical Substances	Acyl Coenzyme A ; Plant Proteins ; Xanthones ; benzoyl-coenzyme A (6756-74-7) ; xanthone (9749WEV0CA) ; Coenzyme A Ligases (EC 6.2.1.-)
Language	English
Publishing date	2020-11-03
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.15012
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Article ; Online: Moonlighting Arabidopsis molybdate transporter 2 family and GSH-complex formation facilitate molybdenum homeostasis.

Weber, Jan-Niklas / Minner-Meinen, Rieke / Behnecke, Maria / Biedendieck, Rebekka / Hänsch, Veit G / Hercher, Thomas W / Hertweck, Christian / van den Hout, Lena / Knüppel, Lars / Sivov, Simon / Schulze, Jutta / Mendel, Ralf-R / Hänsch, Robert / Kaufholdt, David

Communications biology

2023 Volume 6, Issue 1, Page(s) 801

Abstract: Molybdenum (Mo) as essential micronutrient for plants, acts as active component of molybdenum cofactor (Moco). Core metabolic processes like nitrate assimilation or abscisic-acid biosynthesis rely on Moco-dependent enzymes. Although a family of molybdate ...

Abstract	Molybdenum (Mo) as essential micronutrient for plants, acts as active component of molybdenum cofactor (Moco). Core metabolic processes like nitrate assimilation or abscisic-acid biosynthesis rely on Moco-dependent enzymes. Although a family of molybdate transport proteins (MOT1) is known to date in Arabidopsis, molybdate homeostasis remained unclear. Here we report a second family of molybdate transporters (MOT2) playing key roles in molybdate distribution and usage. KO phenotype-analyses, cellular and organ-specific localization, and connection to Moco-biosynthesis enzymes via protein-protein interaction suggest involvement in cellular import of molybdate in leaves and reproductive organs. Furthermore, we detected a glutathione-molybdate complex, which reveals how vacuolar storage is maintained. A putative Golgi S-adenosyl-methionine transport function was reported recently for the MOT2-family. Here, we propose a moonlighting function, since clear evidence of molybdate transport was found in a yeast-system. Our characterization of the MOT2-family and the detection of a glutathione-molybdate complex unveil the plant-wide way of molybdate.
MeSH term(s)	Arabidopsis/genetics ; Arabidopsis/metabolism ; Molybdenum/metabolism ; Membrane Transport Proteins/genetics ; Membrane Transport Proteins/metabolism ; Pteridines ; Homeostasis
Chemical Substances	molybdate (14259-85-9) ; Molybdenum (81AH48963U) ; Membrane Transport Proteins ; Pteridines
Language	English
Publishing date	2023-08-02
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2399-3642
ISSN (online)	2399-3642
DOI	10.1038/s42003-023-05161-x
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Article ; Online: Physiological Importance of Molybdate Transporter Family 1 in Feeding the Molybdenum Cofactor Biosynthesis Pathway in

Minner-Meinen, Rieke / Weber, Jan-Niklas / Kistner, Sarah / Meyfarth, Paul / Saudhof, Merve / van den Hout, Lena / Schulze, Jutta / Mendel, Ralf-Rainer / Hänsch, Robert / Kaufholdt, David

Molecules (Basel, Switzerland)

2022 Volume 27, Issue 10

Abstract: Molybdate uptake and molybdenum cofactor (Moco) biosynthesis were investigated in detail in the last few decades. The present study critically reviews our present knowledge about eukaryotic molybdate transporters (MOT) and focuses on the model ... ...

Abstract	Molybdate uptake and molybdenum cofactor (Moco) biosynthesis were investigated in detail in the last few decades. The present study critically reviews our present knowledge about eukaryotic molybdate transporters (MOT) and focuses on the model plant
MeSH term(s)	Anion Transport Proteins/metabolism ; Arabidopsis/genetics ; Arabidopsis/metabolism ; Molybdenum/metabolism ; Molybdenum Cofactors
Chemical Substances	Anion Transport Proteins ; Molybdenum Cofactors ; molybdate (14259-85-9) ; Molybdenum (81AH48963U)
Language	English
Publishing date	2022-05-15
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	1413402-0
ISSN	1420-3049 ; 1431-5165 ; 1420-3049
ISSN (online)	1420-3049
ISSN	1431-5165 ; 1420-3049
DOI	10.3390/molecules27103158
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Article: Cytosolic aromatic aldehyde dehydrogenase provides benzoic acid for xanthone biosynthesis in Hypericum

Singh, Poonam / Kaufholdt, David / Awadalah, Mina / Hänsch, Robert / Beerhues, Ludger / Gaid, Mariam

Plant physiology and biochemistry. 2021 Mar., v. 160

2021

Abstract	Benzoic acid is a building block of a multitude of well-known plant natural products, such as paclitaxel and cocaine. Its simple chemical structure contrasts with its complex biosynthesis. Hypericum species are rich in polyprenylated benzoic acid-derived xanthones, which have received attention due to their biological impact on human health. The upstream biosynthetic sequence leading to xanthones is still incomplete. To supply benzoic acid for xanthone biosynthesis, Hypericum calycinum cell cultures use the CoA-dependent non-β-oxidative pathway, which starts with peroxisomal cinnamate CoA-ligase (HcCNL). Here, we use the xanthone-producing cell cultures to identify the transcript for benzaldehyde dehydrogenase (HcBD), a pivotal player in the non-β-oxidative pathways. In addition to benzaldehyde, the enzyme efficiently catalyzes the oxidation of trans-cinnamaldehyde in vitro. The enzymatic activity is strictly dependent on the presence of NAD⁺ as co-factor. HcBD is localized to the cytosol upon ectopic expression of reporter fusion constructs. HcBD oxidizes benzaldehyde, which moves across the peroxisome membrane, to form benzoic acid. Increases in the HcCNL and HcBD transcript levels precede the elicitor-induced xanthone accumulation. The current work addresses a crucial step in the yet incompletely understood CoA-dependent non-β-oxidative route of benzoic acid biosynthesis. Addressing this step may offer a new biotechnological tool to enhance product formation in biofactories.
Keywords	Hypericum calycinum ; aldehyde dehydrogenase ; benzaldehyde ; benzoic acid ; biosynthesis ; chemical structure ; cocaine ; cytosol ; enzyme activity ; human health ; oxidation ; paclitaxel ; plant physiology ; xanthone
Language	English
Dates of publication	2021-03
Size	p. 82-93.
Publishing place	Elsevier Masson SAS
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	742978-2
ISSN	1873-2690 ; 0981-9428
ISSN (online)	1873-2690
ISSN	0981-9428
DOI	10.1016/j.plaphy.2021.01.011
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Article ; Online: Impact of wildfires on SO

Weber, Jan-Niklas / Kaufholdt, David / Minner-Meinen, Rieke / Bloem, Elke / Shahid, Afsheen / Rennenberg, Heinz / Hänsch, Robert

Environmental pollution (Barking, Essex : 1987)

2020 Volume 272, Page(s) 116389

Abstract: Frequency and intensity of wildfire occurrences are dramatically increasing worldwide due to global climate change, having a devastating effect on the entire ecosystem including plants. Moreover, distribution of fire-smoke can influence the natural ... ...

Abstract	Frequency and intensity of wildfire occurrences are dramatically increasing worldwide due to global climate change, having a devastating effect on the entire ecosystem including plants. Moreover, distribution of fire-smoke can influence the natural environment over very long distances, i.e. hundreds of kilometres. Dry plant matter contains 0.1-0.9% (w/w) sulphur, which is mainly released during combustion into the atmosphere as sulphur dioxide (SO
MeSH term(s)	Ecosystem ; Fagus ; Germany ; Plant Leaves ; Quercus ; Trees ; Wildfires
Language	English
Publishing date	2020-12-30
Publishing country	England
Document type	Journal Article
ZDB-ID	280652-6
ISSN	1873-6424 ; 0013-9327 ; 0269-7491
ISSN (online)	1873-6424
ISSN	0013-9327 ; 0269-7491
DOI	10.1016/j.envpol.2020.116389
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Article ; Online: Split-HaloTag imaging assay for sophisticated microscopy of protein-protein interactions

Minner-Meinen, Rieke / Weber, Jan-Niklas / Albrecht, Andreas / Matis, Rainer / Behnecke, Maria / Tietge, Cindy / Frank, Stefan / Schulze, Jutta / Buschmann, Henrik / Walla, Peter Jomo / Mendel, Ralf-R / Hänsch, Robert / Kaufholdt, David

Plant communications

2021 Volume 2, Issue 5, Page(s) 100212

Abstract: An ever-increasing number of intracellular multi-protein networks have been identified in plant cells. Split-GFP-based protein-protein interaction assays combine the advantages ... ...

Abstract	An ever-increasing number of intracellular multi-protein networks have been identified in plant cells. Split-GFP-based protein-protein interaction assays combine the advantages of
MeSH term(s)	Botany/instrumentation ; Plants/metabolism ; Protein Interaction Domains and Motifs
Language	English
Publishing date	2021-06-12
Publishing country	China
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2590-3462
ISSN (online)	2590-3462
DOI	10.1016/j.xplc.2021.100212
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