Cargando…

Comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of Arabidopsis

Temperature affects seed germination and seedling growth, which is a critical and complex stage in plant life cycle. However, comprehensive metabolic basis on temperature implicating seed germination and seedling growth remains less known. Here, we applied the high-throughput untargeted metabolomic...

Descripción completa

Detalles Bibliográficos
Autores principales: Qian, Wenjuan, Zhu, Yuxuan, Chen, Qinsheng, Wang, Shuaiyao, Chen, Longlong, Liu, Ting, Tang, Huiru, Yao, Hongyan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10090499/
https://www.ncbi.nlm.nih.gov/pubmed/37063208
http://dx.doi.org/10.3389/fpls.2023.1132881
_version_ 1785022971867299840
author Qian, Wenjuan
Zhu, Yuxuan
Chen, Qinsheng
Wang, Shuaiyao
Chen, Longlong
Liu, Ting
Tang, Huiru
Yao, Hongyan
author_facet Qian, Wenjuan
Zhu, Yuxuan
Chen, Qinsheng
Wang, Shuaiyao
Chen, Longlong
Liu, Ting
Tang, Huiru
Yao, Hongyan
author_sort Qian, Wenjuan
collection PubMed
description Temperature affects seed germination and seedling growth, which is a critical and complex stage in plant life cycle. However, comprehensive metabolic basis on temperature implicating seed germination and seedling growth remains less known. Here, we applied the high-throughput untargeted metabolomic and advanced shotgun lipidomic approaches to profile the Arabidopsis 182 metabolites and 149 lipids under moderate (22°C, 28°C) and extreme high (34°C, 40°C) temperatures. Our results showed that a typical feature of the metabolism related to organic acids/derivates and amines was obviously enriched at the moderate temperature, which was implicated in many cellular responses towards tricarboxylic acid cycle (TCA), carbohydrates and amino acids metabolism, peptide biosynthesis, phenylpropanoid biosynthesis and indole 3-acetate (IAA) biosynthetic pathway. Whereas, under extreme high temperatures, there was no seed germination, but 148 out of total 182 metabolites were highly enriched, involving in the galactose metabolism, fatty acid degradation, tryptophan/phenylalanine metabolism, and shikimic acid-mediated pathways especially including alkaloids metabolism and glucosinolate/flavone/flavonol biosynthesis. Phosphatidylcholine (PC) and phosphatidylethanolamine (PE) also exhibited the gradually increased tendency from moderate temperatures to extreme high temperatures; whereas phosphatidylserine (PS), phosphatidic acid (PA), phosphatidylglycerol (PG), monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG) and sulfoquinovosyldiacylglycerol (SQDG) were contrary to decrease. Another typical feature of the distinguished metabolites between 22°C and 28°C, the TCA, disaccharides, nucleotides, polypeptides, SQDG and the biosynthesis of fatty acids and glucobrassicin-mediated IAA were obviously decreased at 28°C, while amino acids, trisaccharides, PE, PC, PA, PS, MGDG, DGDG and diacylglycerol (DAG) preferred to enrich at 28°C, which characterized the alteration of metabolites and lipids during fast seedling growth. Taking together, our results provided the comprehensive metabolites phenotyping, revealed the characteristics of metabolites necessary for seed germination and/or seedling growth under different temperatures, and provided insights into the different metabolic regulation of metabolites and lipid homeostasis for seed germination and seedling growth.
format Online
Article
Text
id pubmed-10090499
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-100904992023-04-13 Comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of Arabidopsis Qian, Wenjuan Zhu, Yuxuan Chen, Qinsheng Wang, Shuaiyao Chen, Longlong Liu, Ting Tang, Huiru Yao, Hongyan Front Plant Sci Plant Science Temperature affects seed germination and seedling growth, which is a critical and complex stage in plant life cycle. However, comprehensive metabolic basis on temperature implicating seed germination and seedling growth remains less known. Here, we applied the high-throughput untargeted metabolomic and advanced shotgun lipidomic approaches to profile the Arabidopsis 182 metabolites and 149 lipids under moderate (22°C, 28°C) and extreme high (34°C, 40°C) temperatures. Our results showed that a typical feature of the metabolism related to organic acids/derivates and amines was obviously enriched at the moderate temperature, which was implicated in many cellular responses towards tricarboxylic acid cycle (TCA), carbohydrates and amino acids metabolism, peptide biosynthesis, phenylpropanoid biosynthesis and indole 3-acetate (IAA) biosynthetic pathway. Whereas, under extreme high temperatures, there was no seed germination, but 148 out of total 182 metabolites were highly enriched, involving in the galactose metabolism, fatty acid degradation, tryptophan/phenylalanine metabolism, and shikimic acid-mediated pathways especially including alkaloids metabolism and glucosinolate/flavone/flavonol biosynthesis. Phosphatidylcholine (PC) and phosphatidylethanolamine (PE) also exhibited the gradually increased tendency from moderate temperatures to extreme high temperatures; whereas phosphatidylserine (PS), phosphatidic acid (PA), phosphatidylglycerol (PG), monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG) and sulfoquinovosyldiacylglycerol (SQDG) were contrary to decrease. Another typical feature of the distinguished metabolites between 22°C and 28°C, the TCA, disaccharides, nucleotides, polypeptides, SQDG and the biosynthesis of fatty acids and glucobrassicin-mediated IAA were obviously decreased at 28°C, while amino acids, trisaccharides, PE, PC, PA, PS, MGDG, DGDG and diacylglycerol (DAG) preferred to enrich at 28°C, which characterized the alteration of metabolites and lipids during fast seedling growth. Taking together, our results provided the comprehensive metabolites phenotyping, revealed the characteristics of metabolites necessary for seed germination and/or seedling growth under different temperatures, and provided insights into the different metabolic regulation of metabolites and lipid homeostasis for seed germination and seedling growth. Frontiers Media S.A. 2023-03-29 /pmc/articles/PMC10090499/ /pubmed/37063208 http://dx.doi.org/10.3389/fpls.2023.1132881 Text en Copyright © 2023 Qian, Zhu, Chen, Wang, Chen, Liu, Tang and Yao 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
Qian, Wenjuan
Zhu, Yuxuan
Chen, Qinsheng
Wang, Shuaiyao
Chen, Longlong
Liu, Ting
Tang, Huiru
Yao, Hongyan
Comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of Arabidopsis
title Comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of Arabidopsis
title_full Comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of Arabidopsis
title_fullStr Comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of Arabidopsis
title_full_unstemmed Comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of Arabidopsis
title_short Comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of Arabidopsis
title_sort comprehensive metabolomic and lipidomic alterations in response to heat stress during seed germination and seedling growth of arabidopsis
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10090499/
https://www.ncbi.nlm.nih.gov/pubmed/37063208
http://dx.doi.org/10.3389/fpls.2023.1132881
work_keys_str_mv AT qianwenjuan comprehensivemetabolomicandlipidomicalterationsinresponsetoheatstressduringseedgerminationandseedlinggrowthofarabidopsis
AT zhuyuxuan comprehensivemetabolomicandlipidomicalterationsinresponsetoheatstressduringseedgerminationandseedlinggrowthofarabidopsis
AT chenqinsheng comprehensivemetabolomicandlipidomicalterationsinresponsetoheatstressduringseedgerminationandseedlinggrowthofarabidopsis
AT wangshuaiyao comprehensivemetabolomicandlipidomicalterationsinresponsetoheatstressduringseedgerminationandseedlinggrowthofarabidopsis
AT chenlonglong comprehensivemetabolomicandlipidomicalterationsinresponsetoheatstressduringseedgerminationandseedlinggrowthofarabidopsis
AT liuting comprehensivemetabolomicandlipidomicalterationsinresponsetoheatstressduringseedgerminationandseedlinggrowthofarabidopsis
AT tanghuiru comprehensivemetabolomicandlipidomicalterationsinresponsetoheatstressduringseedgerminationandseedlinggrowthofarabidopsis
AT yaohongyan comprehensivemetabolomicandlipidomicalterationsinresponsetoheatstressduringseedgerminationandseedlinggrowthofarabidopsis