Cargando…
Integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis
Plant specialized 1,4-naphthoquinones present a remarkable case of convergent evolution. Species across multiple discrete orders of vascular plants produce diverse 1,4-naphthoquinones via one of several pathways using different metabolic precursors. Evolution of these pathways was preceded by events...
Autores principales: | , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8969065/ https://www.ncbi.nlm.nih.gov/pubmed/35048120 http://dx.doi.org/10.1093/hr/uhab087 |
_version_ | 1784679182360379392 |
---|---|
author | Suttiyut, Thiti Auber, Robert P Ghaste, Manoj Kane, Cade N McAdam, Scott A M Wisecaver, Jennifer H Widhalm, Joshua R |
author_facet | Suttiyut, Thiti Auber, Robert P Ghaste, Manoj Kane, Cade N McAdam, Scott A M Wisecaver, Jennifer H Widhalm, Joshua R |
author_sort | Suttiyut, Thiti |
collection | PubMed |
description | Plant specialized 1,4-naphthoquinones present a remarkable case of convergent evolution. Species across multiple discrete orders of vascular plants produce diverse 1,4-naphthoquinones via one of several pathways using different metabolic precursors. Evolution of these pathways was preceded by events of metabolic innovation and many appear to share connections with biosynthesis of photosynthetic or respiratory quinones. Here, we sought to shed light on the metabolic connections linking shikonin biosynthesis with its precursor pathways and on the origins of shikonin metabolic genes. Downregulation of Lithospermum erythrorhizon geranyl diphosphate synthase (LeGPPS), recently shown to have been recruited from a cytoplasmic farnesyl diphosphate synthase (FPPS), resulted in reduced shikonin production and a decrease in expression of mevalonic acid and phenylpropanoid pathway genes. Next, we used LeGPPS and other known shikonin pathway genes to build a coexpression network model for identifying new gene connections to shikonin metabolism. Integrative in silico analyses of network genes revealed candidates for biochemical steps in the shikonin pathway arising from Boraginales-specific gene family expansion. Multiple genes in the shikonin coexpression network were also discovered to have originated from duplication of ubiquinone pathway genes. Taken together, our study provides evidence for transcriptional crosstalk between shikonin biosynthesis and its precursor pathways, identifies several shikonin pathway gene candidates and their evolutionary histories, and establishes additional evolutionary links between shikonin and ubiquinone metabolism. Moreover, we demonstrate that global coexpression analysis using limited transcriptomic data obtained from targeted experiments is effective for identifying gene connections within a defined metabolic network. |
format | Online Article Text |
id | pubmed-8969065 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-89690652022-04-01 Integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis Suttiyut, Thiti Auber, Robert P Ghaste, Manoj Kane, Cade N McAdam, Scott A M Wisecaver, Jennifer H Widhalm, Joshua R Hortic Res Article Plant specialized 1,4-naphthoquinones present a remarkable case of convergent evolution. Species across multiple discrete orders of vascular plants produce diverse 1,4-naphthoquinones via one of several pathways using different metabolic precursors. Evolution of these pathways was preceded by events of metabolic innovation and many appear to share connections with biosynthesis of photosynthetic or respiratory quinones. Here, we sought to shed light on the metabolic connections linking shikonin biosynthesis with its precursor pathways and on the origins of shikonin metabolic genes. Downregulation of Lithospermum erythrorhizon geranyl diphosphate synthase (LeGPPS), recently shown to have been recruited from a cytoplasmic farnesyl diphosphate synthase (FPPS), resulted in reduced shikonin production and a decrease in expression of mevalonic acid and phenylpropanoid pathway genes. Next, we used LeGPPS and other known shikonin pathway genes to build a coexpression network model for identifying new gene connections to shikonin metabolism. Integrative in silico analyses of network genes revealed candidates for biochemical steps in the shikonin pathway arising from Boraginales-specific gene family expansion. Multiple genes in the shikonin coexpression network were also discovered to have originated from duplication of ubiquinone pathway genes. Taken together, our study provides evidence for transcriptional crosstalk between shikonin biosynthesis and its precursor pathways, identifies several shikonin pathway gene candidates and their evolutionary histories, and establishes additional evolutionary links between shikonin and ubiquinone metabolism. Moreover, we demonstrate that global coexpression analysis using limited transcriptomic data obtained from targeted experiments is effective for identifying gene connections within a defined metabolic network. Oxford University Press 2022-01-20 /pmc/articles/PMC8969065/ /pubmed/35048120 http://dx.doi.org/10.1093/hr/uhab087 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Nanjing Agricultural University https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Article Suttiyut, Thiti Auber, Robert P Ghaste, Manoj Kane, Cade N McAdam, Scott A M Wisecaver, Jennifer H Widhalm, Joshua R Integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis |
title | Integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis |
title_full | Integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis |
title_fullStr | Integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis |
title_full_unstemmed | Integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis |
title_short | Integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis |
title_sort | integrative analysis of the shikonin metabolic network identifies new gene connections and reveals evolutionary insight into shikonin biosynthesis |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8969065/ https://www.ncbi.nlm.nih.gov/pubmed/35048120 http://dx.doi.org/10.1093/hr/uhab087 |
work_keys_str_mv | AT suttiyutthiti integrativeanalysisoftheshikoninmetabolicnetworkidentifiesnewgeneconnectionsandrevealsevolutionaryinsightintoshikoninbiosynthesis AT auberrobertp integrativeanalysisoftheshikoninmetabolicnetworkidentifiesnewgeneconnectionsandrevealsevolutionaryinsightintoshikoninbiosynthesis AT ghastemanoj integrativeanalysisoftheshikoninmetabolicnetworkidentifiesnewgeneconnectionsandrevealsevolutionaryinsightintoshikoninbiosynthesis AT kanecaden integrativeanalysisoftheshikoninmetabolicnetworkidentifiesnewgeneconnectionsandrevealsevolutionaryinsightintoshikoninbiosynthesis AT mcadamscottam integrativeanalysisoftheshikoninmetabolicnetworkidentifiesnewgeneconnectionsandrevealsevolutionaryinsightintoshikoninbiosynthesis AT wisecaverjenniferh integrativeanalysisoftheshikoninmetabolicnetworkidentifiesnewgeneconnectionsandrevealsevolutionaryinsightintoshikoninbiosynthesis AT widhalmjoshuar integrativeanalysisoftheshikoninmetabolicnetworkidentifiesnewgeneconnectionsandrevealsevolutionaryinsightintoshikoninbiosynthesis |