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Misregulation of tetrapyrrole biosynthesis in transgenic tobacco seedlings expressing mammalian biliverdin reductase

Misregulation of tetrapyrrole biosynthesis in transgenic tobacco seedlings expressing mammalian biliverdin reductase
Misregulation of tetrapyrrole biosynthesis in transgenic tobacco seedlings expressing mammalian biliverdin reductase
Previous studies have established that the expression of mammalian biliverdin IXalpha reductase (BVR) in transgenic tobacco (Nicotiana tabacum cv. Maryland Mammoth) resulted in the loss of photoregulatory activity of all phytochromes together with a pronounced chlorophyll deficiency. This study was undertaken to assess the contribution of BVR-mediated alteration of tetrapyrrole metabolism to the observed phenotypes of BVR transgenic plants. BVR expression in dark-grown plants led to the reduced accumulation of protochlorophyllide and transcripts for the two committed enzymes for 5-aminolevulinic acid (ALA) synthesis despite the marked increased capacity for synthesis of ALA. Together with the observation that Mg-porphyrin accumulation in dark-grown seedlings treated with an iron chelator was unaffected by BVR expression, these results indicate that BVR diverts tetrapyrrole metabolism toward heme synthesis while also reducing heme levels to de-repress ALA synthesis. By contrast with dark-grown seedlings, light-grown BVR plants showed a marked inhibition of ALA synthesis compared with wild-type plants - a result that was correlated with the disappearance of the CHL I subunit of Mg-chelatase and an increase in heme oxygenase protein levels. As transcript levels of all tetrapyrrole biosynthetic genes tested were not strongly affected by BVR expression, these results implicate misregulated tetrapyrrole metabolism to be a major mechanism for BVR-dependent inhibition of chlorophyll biosynthesis in light-grown plants.
chlorophyll synthesis, chloroplast, phytochrome, phytochromobilin, aminolevulinic acid, protochlorophyllide
0960-7412
717-728
Franklin, K.A.
7a209e67-01a0-4d87-8990-ffe751389d3f
Linley, P.J.
31574fdd-77ae-4ed1-af05-0f4bc271424a
Montgomery, B.L.
3c567b55-e34a-4349-8ec0-b40902605bc0
Lagarias, J.C.
adfeba99-ddf0-46f1-bde8-2baad0d11489
Thomas, B.
017efe01-f15e-4819-bc02-a2f8ca15be13
Jackson, S.D.
df63bb6a-dc92-4ce7-920e-6a669f40e0b5
Terry, M.J.
a8c2cd6b-8d35-4053-8d77-3841c2427c3b
Franklin, K.A.
7a209e67-01a0-4d87-8990-ffe751389d3f
Linley, P.J.
31574fdd-77ae-4ed1-af05-0f4bc271424a
Montgomery, B.L.
3c567b55-e34a-4349-8ec0-b40902605bc0
Lagarias, J.C.
adfeba99-ddf0-46f1-bde8-2baad0d11489
Thomas, B.
017efe01-f15e-4819-bc02-a2f8ca15be13
Jackson, S.D.
df63bb6a-dc92-4ce7-920e-6a669f40e0b5
Terry, M.J.
a8c2cd6b-8d35-4053-8d77-3841c2427c3b

Franklin, K.A., Linley, P.J., Montgomery, B.L., Lagarias, J.C., Thomas, B., Jackson, S.D. and Terry, M.J. (2003) Misregulation of tetrapyrrole biosynthesis in transgenic tobacco seedlings expressing mammalian biliverdin reductase. The Plant Journal, 35 (6), 717-728. (doi:10.1046/j.1365-313X.2003.01840.x).

Record type: Article

Abstract

Previous studies have established that the expression of mammalian biliverdin IXalpha reductase (BVR) in transgenic tobacco (Nicotiana tabacum cv. Maryland Mammoth) resulted in the loss of photoregulatory activity of all phytochromes together with a pronounced chlorophyll deficiency. This study was undertaken to assess the contribution of BVR-mediated alteration of tetrapyrrole metabolism to the observed phenotypes of BVR transgenic plants. BVR expression in dark-grown plants led to the reduced accumulation of protochlorophyllide and transcripts for the two committed enzymes for 5-aminolevulinic acid (ALA) synthesis despite the marked increased capacity for synthesis of ALA. Together with the observation that Mg-porphyrin accumulation in dark-grown seedlings treated with an iron chelator was unaffected by BVR expression, these results indicate that BVR diverts tetrapyrrole metabolism toward heme synthesis while also reducing heme levels to de-repress ALA synthesis. By contrast with dark-grown seedlings, light-grown BVR plants showed a marked inhibition of ALA synthesis compared with wild-type plants - a result that was correlated with the disappearance of the CHL I subunit of Mg-chelatase and an increase in heme oxygenase protein levels. As transcript levels of all tetrapyrrole biosynthetic genes tested were not strongly affected by BVR expression, these results implicate misregulated tetrapyrrole metabolism to be a major mechanism for BVR-dependent inhibition of chlorophyll biosynthesis in light-grown plants.

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Published date: 2003
Keywords: chlorophyll synthesis, chloroplast, phytochrome, phytochromobilin, aminolevulinic acid, protochlorophyllide

Identifiers

Local EPrints ID: 37625
URI: http://eprints.soton.ac.uk/id/eprint/37625
ISSN: 0960-7412
PURE UUID: 39e1a88f-3701-417d-ba8f-f5d47f32b6e5
ORCID for M.J. Terry: ORCID iD orcid.org/0000-0001-5002-2708

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Date deposited: 25 May 2006
Last modified: 16 Mar 2024 02:52

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Contributors

Author: K.A. Franklin
Author: P.J. Linley
Author: B.L. Montgomery
Author: J.C. Lagarias
Author: B. Thomas
Author: S.D. Jackson
Author: M.J. Terry ORCID iD

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