Cargando…
Transcriptomic and Metabolomic Response to High Light in the Charophyte Alga Klebsormidium nitens
The characterization of the molecular mechanisms, such as high light irradiance resistance, that allowed plant terrestralization is a cornerstone in evolutionary studies since the conquest of land by plants played a pivotal role in life evolution on Earth. Viridiplantae or the green lineage is divid...
Autores principales: | , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9121098/ https://www.ncbi.nlm.nih.gov/pubmed/35599877 http://dx.doi.org/10.3389/fpls.2022.855243 |
_version_ | 1784711083260379136 |
---|---|
author | Serrano-Pérez, Emma Romero-Losada, Ana B. Morales-Pineda, María García-Gómez, M. Elena Couso, Inmaculada García-González, Mercedes Romero-Campero, Francisco J. |
author_facet | Serrano-Pérez, Emma Romero-Losada, Ana B. Morales-Pineda, María García-Gómez, M. Elena Couso, Inmaculada García-González, Mercedes Romero-Campero, Francisco J. |
author_sort | Serrano-Pérez, Emma |
collection | PubMed |
description | The characterization of the molecular mechanisms, such as high light irradiance resistance, that allowed plant terrestralization is a cornerstone in evolutionary studies since the conquest of land by plants played a pivotal role in life evolution on Earth. Viridiplantae or the green lineage is divided into two clades, Chlorophyta and Streptophyta, that in turn splits into Embryophyta or land plants and Charophyta. Charophyta are used in evolutionary studies on plant terrestralization since they are generally accepted as the extant algal species most closely related to current land plants. In this study, we have chosen the facultative terrestrial early charophyte alga Klebsormidium nitens to perform an integrative transcriptomic and metabolomic analysis under high light in order to unveil key mechanisms involved in the early steps of plants terrestralization. We found a fast chloroplast retrograde signaling possibly mediated by reactive oxygen species and the inositol polyphosphate 1-phosphatase (SAL1) and 3′-phosphoadenosine-5′-phosphate (PAP) pathways inducing gene expression and accumulation of specific metabolites. Systems used by both Chlorophyta and Embryophyta were activated such as the xanthophyll cycle with an accumulation of zeaxanthin and protein folding and repair mechanisms constituted by NADPH-dependent thioredoxin reductases, thioredoxin-disulfide reductases, and peroxiredoxins. Similarly, cyclic electron flow, specifically the pathway dependent on proton gradient regulation 5, was strongly activated under high light. We detected a simultaneous co-activation of the non-photochemical quenching mechanisms based on LHC-like stress related (LHCSR) protein and the photosystem II subunit S that are specific to Chlorophyta and Embryophyta, respectively. Exclusive Embryophyta systems for the synthesis, sensing, and response to the phytohormone auxin were also activated under high light in K. nitens leading to an increase in auxin content with the concomitant accumulation of amino acids such as tryptophan, histidine, and phenylalanine. |
format | Online Article Text |
id | pubmed-9121098 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-91210982022-05-21 Transcriptomic and Metabolomic Response to High Light in the Charophyte Alga Klebsormidium nitens Serrano-Pérez, Emma Romero-Losada, Ana B. Morales-Pineda, María García-Gómez, M. Elena Couso, Inmaculada García-González, Mercedes Romero-Campero, Francisco J. Front Plant Sci Plant Science The characterization of the molecular mechanisms, such as high light irradiance resistance, that allowed plant terrestralization is a cornerstone in evolutionary studies since the conquest of land by plants played a pivotal role in life evolution on Earth. Viridiplantae or the green lineage is divided into two clades, Chlorophyta and Streptophyta, that in turn splits into Embryophyta or land plants and Charophyta. Charophyta are used in evolutionary studies on plant terrestralization since they are generally accepted as the extant algal species most closely related to current land plants. In this study, we have chosen the facultative terrestrial early charophyte alga Klebsormidium nitens to perform an integrative transcriptomic and metabolomic analysis under high light in order to unveil key mechanisms involved in the early steps of plants terrestralization. We found a fast chloroplast retrograde signaling possibly mediated by reactive oxygen species and the inositol polyphosphate 1-phosphatase (SAL1) and 3′-phosphoadenosine-5′-phosphate (PAP) pathways inducing gene expression and accumulation of specific metabolites. Systems used by both Chlorophyta and Embryophyta were activated such as the xanthophyll cycle with an accumulation of zeaxanthin and protein folding and repair mechanisms constituted by NADPH-dependent thioredoxin reductases, thioredoxin-disulfide reductases, and peroxiredoxins. Similarly, cyclic electron flow, specifically the pathway dependent on proton gradient regulation 5, was strongly activated under high light. We detected a simultaneous co-activation of the non-photochemical quenching mechanisms based on LHC-like stress related (LHCSR) protein and the photosystem II subunit S that are specific to Chlorophyta and Embryophyta, respectively. Exclusive Embryophyta systems for the synthesis, sensing, and response to the phytohormone auxin were also activated under high light in K. nitens leading to an increase in auxin content with the concomitant accumulation of amino acids such as tryptophan, histidine, and phenylalanine. Frontiers Media S.A. 2022-05-06 /pmc/articles/PMC9121098/ /pubmed/35599877 http://dx.doi.org/10.3389/fpls.2022.855243 Text en Copyright © 2022 Serrano-Pérez, Romero-Losada, Morales-Pineda, García-Gómez, Couso, García-González and Romero-Campero. 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 Serrano-Pérez, Emma Romero-Losada, Ana B. Morales-Pineda, María García-Gómez, M. Elena Couso, Inmaculada García-González, Mercedes Romero-Campero, Francisco J. Transcriptomic and Metabolomic Response to High Light in the Charophyte Alga Klebsormidium nitens |
title | Transcriptomic and Metabolomic Response to High Light in the Charophyte Alga Klebsormidium nitens |
title_full | Transcriptomic and Metabolomic Response to High Light in the Charophyte Alga Klebsormidium nitens |
title_fullStr | Transcriptomic and Metabolomic Response to High Light in the Charophyte Alga Klebsormidium nitens |
title_full_unstemmed | Transcriptomic and Metabolomic Response to High Light in the Charophyte Alga Klebsormidium nitens |
title_short | Transcriptomic and Metabolomic Response to High Light in the Charophyte Alga Klebsormidium nitens |
title_sort | transcriptomic and metabolomic response to high light in the charophyte alga klebsormidium nitens |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9121098/ https://www.ncbi.nlm.nih.gov/pubmed/35599877 http://dx.doi.org/10.3389/fpls.2022.855243 |
work_keys_str_mv | AT serranoperezemma transcriptomicandmetabolomicresponsetohighlightinthecharophytealgaklebsormidiumnitens AT romerolosadaanab transcriptomicandmetabolomicresponsetohighlightinthecharophytealgaklebsormidiumnitens AT moralespinedamaria transcriptomicandmetabolomicresponsetohighlightinthecharophytealgaklebsormidiumnitens AT garciagomezmelena transcriptomicandmetabolomicresponsetohighlightinthecharophytealgaklebsormidiumnitens AT cousoinmaculada transcriptomicandmetabolomicresponsetohighlightinthecharophytealgaklebsormidiumnitens AT garciagonzalezmercedes transcriptomicandmetabolomicresponsetohighlightinthecharophytealgaklebsormidiumnitens AT romerocamperofranciscoj transcriptomicandmetabolomicresponsetohighlightinthecharophytealgaklebsormidiumnitens |