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Title:Transcriptional deregulation of stress-growth balance in Nicotiana benthamiana biofactories producing insect sex pheromones
Authors:ID Juteršek, Mojca (Author)
ID Petek, Marko (Author)
ID Ramšak, Živa (Author)
ID Gimenéz, Elena Moreno (Author)
ID Gianoglio, Silvia (Author)
ID Fernández, Rubèn Mateos (Author)
ID Orzaez, Diego (Author)
ID Gruden, Kristina (Author)
ID Baebler, Špela (Author)
Files:URL URL - Source URL, visit https://doi.org/10.3389/fpls.2022.941338
 
.pdf PDF - Presentation file, download (7,68 MB)
MD5: 4E3F3E2B261AB7CD2B84923707A0E746
 
Language:English
Typology:1.01 - Original Scientific Article
Organization:Logo NIB - National Institute of Biology
Abstract:Plant biofactories are a promising platform for sustainable production of high-value compounds, among which are insect sex pheromones, a green alternative to conventional insecticides in agriculture. Recently, we have constructed transgenic Nicotiana benthamiana plants (“Sexy Plants”, SxP) that successfully produce a blend of moth (Lepidoptera) sex pheromone compounds (Z)-11-hexadecen-1-ol and (Z)-11-hexadecenyl acetate. However, efficient biosynthesis of sex pheromones resulted in growth and developmental penalty, diminishing the potential for commercial use of SxP in biomanufacturing. To gain insight into the underlying molecular responses, we analysed the whole-genome transcriptome and evaluated it in relation to growth and pheromone production in low- and high-producing transgenic plants of v1.0 and v1.2 SxP lines. In our study, high-producing SxPv1.2 plants accumulated the highest amounts of pheromones but still maintained better growth compared to v1.0 high producers. For an in-depth biological interpretation of the transcriptomic data, we have prepared a comprehensive functional N. benthamiana genome annotation as well as gene translations to Arabidopsis thaliana, enabling functional information transfer by using Arabidopsis knowledge networks. Differential gene expression analysis, contrasting pheromone producers to wild-type plants, revealed that while only a few genes were differentially regulated in low-producing plants, high-producing plants exhibited vast transcriptional reprogramming. They showed signs of stress-like response, manifested as downregulation of photosynthesis-related genes and significant differences in expression of hormonal signalling and secondary metabolism-related genes, the latter presumably leading to previously reported volatilome changes. Further network analyses confirmed stress-like response with activation of jasmonic acid and downregulation of gibberellic acid signalling, illuminating the possibility that the observed growth penalty was not solely a consequence of a higher metabolic burden imposed upon constitutive expression of a heterologous biosynthetic pathway, but rather the result of signalling pathway perturbation. Our work presents an example of comprehensive transcriptomic analyses of disadvantageous stress signalling in N. benthamiana biofactory that could be applied to other bioproduction systems.
Keywords:transcriptomics, plant biotechnology, jasmonic acid, growthstress tradeoffs, network analysis, growth penalty, insect sex pheromone
Publication status:Published
Publication version:Version of Record
Publication date:26.10.2022
Year of publishing:2022
Number of pages:str. 1-14
Numbering:Vol. 13, [article no.] 941338
PID:20.500.12556/DiRROS-19391 New window
UDC:577
ISSN on article:1664-462X
DOI:10.3389/fpls.2022.941338 New window
COBISS.SI-ID:127685123 New window
Note:Soavtorji: Marko Petek, Živa Ramšak, Elena Moreno-Giménez, Silvia Gianoglio, Rubén Mateos-Fernández, Diego Orzáez, Kristina Gruden and Špela Baebler; Nasl. z nasl. zaslona; Opis vira z dne 2. 11. 2022;
Publication date in DiRROS:17.07.2024
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Downloads:221
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Record is a part of a journal

Title:Frontiers in plant science
Shortened title:Front. plant sci.
Publisher:Frontiers Research Foundation
ISSN:1664-462X
COBISS.SI-ID:3011663 New window

Document is financed by a project

Funder:EC - European Commission
Project number:722361
Name:Cofund on Biotechnologies
Acronym:ERA CoBioTech

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:P4-0165-2022
Name:Biotehnologija in sistemska biologija rastlin

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:P4-0431-2022
Name:Kmetijstvo naslednje generacije

Funder:Other - Other funder or multiple funders
Project number:FPU grant
Name:Spain, Ministry of Science, Innovation and Universities, predoctoral FPU grant

Funder:UKRI - UK Research and Innovation
Funding programme:BBSRC
Project number:BB/R021554/1
Name:17-ERACoBioTech - SUSPHIRE - Sustainable Bioproduction of Pheromones for Insect Pest Control in Agriculture

Funder:Other - Other funder or multiple funders
Funding programme:Spanish Ministry of Science, Innovation and Universities
Project number:FPU18/02019
Name:PhD grant

Funder:Other - Other funder or multiple funders
Funding programme:Generalitat Valenciana
Project number:ACIF/2019/226
Name:PhD grant

Licences

License:CC BY 4.0, Creative Commons Attribution 4.0 International
Link:http://creativecommons.org/licenses/by/4.0/
Description:This is the standard Creative Commons license that gives others maximum freedom to do what they want with the work as long as they credit the author.

Secondary language

Language:Slovenian
Keywords:biotehnologija, feromoni žuželk, zaščita rastlin, jasmonska kislina, giberelini, Nicotiana benthamiana


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