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Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin
The monoterpene camphor is produced in glandular secretory trichomes of the medicinal plant Artemisia annua, which also produces the antimalarial drug artemisinin. We have found that, depending on growth conditions, camphor can accumulate at levels ranging from 1- 10% leaf dry weight (LDW) in the Ar...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9597464/ https://www.ncbi.nlm.nih.gov/pubmed/36311056 http://dx.doi.org/10.3389/fpls.2022.1000819 |
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author | Czechowski, Tomasz Branigan, Caroline Rae, Anne Rathbone, Deborah Larson, Tony R. Harvey, David Catania, Theresa M. Zhang, Dong Li, Yi Salmon, Melissa Bowles, Dianna J. O´Maille, Paul Graham, Ian A. |
author_facet | Czechowski, Tomasz Branigan, Caroline Rae, Anne Rathbone, Deborah Larson, Tony R. Harvey, David Catania, Theresa M. Zhang, Dong Li, Yi Salmon, Melissa Bowles, Dianna J. O´Maille, Paul Graham, Ian A. |
author_sort | Czechowski, Tomasz |
collection | PubMed |
description | The monoterpene camphor is produced in glandular secretory trichomes of the medicinal plant Artemisia annua, which also produces the antimalarial drug artemisinin. We have found that, depending on growth conditions, camphor can accumulate at levels ranging from 1- 10% leaf dry weight (LDW) in the Artemis F1 hybrid, which has been developed for commercial production of artemisinin at up to 1% LDW. We discovered that a camphor null (camphor-0) phenotype segregates in the progeny of self-pollinated Artemis material. Camphor-0 plants also show reduced levels of other less abundant monoterpenes and increased levels of the sesquiterpene precursor farnesyl pyrophosphate plus sesquiterpenes, including enzymatically derived artemisinin pathway intermediates but not artemisinin. One possible explanation for this is that high camphor concentrations in the glandular secretory trichomes play an important role in generating the hydrophobic conditions required for the non-enzymatic conversion of dihydroartemisinic acid tertiary hydroperoxide to artemisinin. We established that the camphor-0 phenotype associates with a genomic deletion that results in loss of a Bornyl diPhosphate Synthase (AaBPS) gene candidate. Functional characterization of the corresponding enzyme in vitro confirmed it can catalyze the first committed step in not only camphor biosynthesis but also in a number of other monoterpenes, accounting for over 60% of total volatiles in A. annua leaves. This in vitro analysis is consistent with loss of monoterpenes in camphor-0 plants. The AaBPS promoter drives high reporter gene expression in A. annua glandular secretory trichomes of juvenile leaves with expression shifting to non-glandular trichomes in mature leaves, which is consistent with AaBPS transcript abundance. |
format | Online Article Text |
id | pubmed-9597464 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-95974642022-10-27 Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin Czechowski, Tomasz Branigan, Caroline Rae, Anne Rathbone, Deborah Larson, Tony R. Harvey, David Catania, Theresa M. Zhang, Dong Li, Yi Salmon, Melissa Bowles, Dianna J. O´Maille, Paul Graham, Ian A. Front Plant Sci Plant Science The monoterpene camphor is produced in glandular secretory trichomes of the medicinal plant Artemisia annua, which also produces the antimalarial drug artemisinin. We have found that, depending on growth conditions, camphor can accumulate at levels ranging from 1- 10% leaf dry weight (LDW) in the Artemis F1 hybrid, which has been developed for commercial production of artemisinin at up to 1% LDW. We discovered that a camphor null (camphor-0) phenotype segregates in the progeny of self-pollinated Artemis material. Camphor-0 plants also show reduced levels of other less abundant monoterpenes and increased levels of the sesquiterpene precursor farnesyl pyrophosphate plus sesquiterpenes, including enzymatically derived artemisinin pathway intermediates but not artemisinin. One possible explanation for this is that high camphor concentrations in the glandular secretory trichomes play an important role in generating the hydrophobic conditions required for the non-enzymatic conversion of dihydroartemisinic acid tertiary hydroperoxide to artemisinin. We established that the camphor-0 phenotype associates with a genomic deletion that results in loss of a Bornyl diPhosphate Synthase (AaBPS) gene candidate. Functional characterization of the corresponding enzyme in vitro confirmed it can catalyze the first committed step in not only camphor biosynthesis but also in a number of other monoterpenes, accounting for over 60% of total volatiles in A. annua leaves. This in vitro analysis is consistent with loss of monoterpenes in camphor-0 plants. The AaBPS promoter drives high reporter gene expression in A. annua glandular secretory trichomes of juvenile leaves with expression shifting to non-glandular trichomes in mature leaves, which is consistent with AaBPS transcript abundance. Frontiers Media S.A. 2022-10-12 /pmc/articles/PMC9597464/ /pubmed/36311056 http://dx.doi.org/10.3389/fpls.2022.1000819 Text en Copyright © 2022 Czechowski, Branigan, Rae, Rathbone, Larson, Harvey, Catania, Zhang, Li, Salmon, Bowles, O´Maille and Graham https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Plant Science Czechowski, Tomasz Branigan, Caroline Rae, Anne Rathbone, Deborah Larson, Tony R. Harvey, David Catania, Theresa M. Zhang, Dong Li, Yi Salmon, Melissa Bowles, Dianna J. O´Maille, Paul Graham, Ian A. Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin |
title |
Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin |
title_full |
Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin |
title_fullStr |
Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin |
title_full_unstemmed |
Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin |
title_short |
Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin |
title_sort | artemisia annua l. plants lacking bornyl diphosphate synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9597464/ https://www.ncbi.nlm.nih.gov/pubmed/36311056 http://dx.doi.org/10.3389/fpls.2022.1000819 |
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