University of Oulu

Jaana Vuosku, Katja Karppinen, Riina Muilu-Mäkelä, Tomonobu Kusano, G H M Sagor, Komlan Avia, Emmi Alakärppä, Johanna Kestilä, Marko Suokas, Kaloian Nickolov, Leena Hamberg, Outi Savolainen, Hely Häggman, Tytti Sarjala, Scots pine aminopropyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants, Annals of Botany, Volume 121, Issue 6, 11 May 2018, Pages 1243–1256, https://doi.org/10.1093/aob/mcy012

Scots pine aminopropyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants

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Author: Vuosku, Jaana1; Karppinen, Katja1; Muilu-Mäkelä, Riina2;
Organizations: 1University of Oulu, Department of Ecology and Genetics, Oulu, Finland
2Natural Resources Institute Finland, Bio-based Business and Industry, Parkano, Finland
3Tohoku University, Graduate School of Life Sciences, Sendai, Miyagi, Japan
4University of Oulu, Department of Ecology and Genetics, Oulu, Finland
5Natural Resources Institute Finland, Management and Production of Renewable Resources, Vantaa, Finland
Format: article
Version: accepted version
Access: open
Online Access: PDF Full Text (PDF, 0.3 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe2019040911577
Language: English
Published: Oxford University Press, 2018
Publish Date: 2019-04-09
Description:

Abstract

Background and Aims: Polyamines are small metabolites present in all living cells and play fundamental roles in numerous physiological events in plants. The aminopropyltransferases (APTs), spermidine synthase (SPDS), spermine synthase (SPMS) and thermospermine synthase (ACL5), are essential enzymes in the polyamine biosynthesis pathway. In angiosperms, SPMS has evolved from SPDS via gene duplication, whereas in gymnosperms APTs are mostly unexplored and no SPMS gene has been reported. The present study aimed to investigate the functional properties of the SPDS and ACL5 proteins of Scots pine (Pinus sylvestris L.) in order to elucidate the role and evolution of APTs in higher plants.

Methods: Germinating Scots pine seeds and seedlings were analysed for polyamines by high-performance liquid chromatography (HPLC) and the expression of PsSPDS and PsACL5 genes by in situ hybridization. Recombinant proteins of PsSPDS and PsACL5 were produced and investigated for functional properties. Also gene structures, promoter regions and phylogenetic relationships of PsSPDS and PsACL5 genes were analysed.

Key Results: Scots pine tissues were found to contain spermidine, spermine and thermospermine. PsSPDS enzyme catalysed synthesis of both spermidine and spermine. PsACL5 was found to produce thermospermine, and PsACL5 gene expression was localized in the developing procambium in embryos and tracheary elements in seedlings.

Conclusions: Contrary to previous views, our results demonstrate that SPMS activity is not a novel feature developed solely in the angiosperm lineage of seed plants but also exists as a secondary property in the Scots pine SPDS enzyme. The discovery of bifunctional SPDS from an evolutionarily old conifer reveals the missing link in the evolution of the polyamine biosynthesis pathway. The finding emphasizes the importance of pre-existing secondary functions in the evolution of new enzyme activities via gene duplication. Our results also associate PsACL5 with the development of vascular structures in Scots pine.

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Series: Annals of botany
ISSN: 0305-7364
ISSN-E: 1095-8290
ISSN-L: 0305-7364
Volume: 121
Issue: 6
Pages: 1243 - 1256
DOI: 10.1093/aob/mcy012
OADOI: https://oadoi.org/10.1093/aob/mcy012
Type of Publication: A1 Journal article – refereed
Field of Science: 1181 Ecology, evolutionary biology
1183 Plant biology, microbiology, virology
Subjects:
Funding: The Research was funded by the Academy of Finland (Project 121994 to TS), by Thule Institute (to HH) and by grants from the Finnish Cultural Foundation and the Niemi Foundation (to JV).
Copyright information: © The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This is a pre-copyedited, author-produced version of an article accepted for publication in Annals of Botany following peer review. The version of record Jaana Vuosku, Katja Karppinen, Riina Muilu-Mäkelä, Tomonobu Kusano, G H M Sagor, Komlan Avia, Emmi Alakärppä, Johanna Kestilä, Marko Suokas, Kaloian Nickolov, Leena Hamberg, Outi Savolainen, Hely Häggman, Tytti Sarjala, Scots pine aminopropyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants, Annals of Botany, Volume 121, Issue 6, 11 May 2018, Pages 1243–1256, is available online at: https://doi.org/10.1093/aob/mcy012