{"title":"Gaseous exchange-dependent in vitro culture extensively alters plant growth and metabolic landscape revealed by comprehensive metabolomics","authors":"Anoop Kumar Verma , Poonam Rakwal , Rama Pandey , Nichole Birse , CH Ratnasekhar","doi":"10.1016/j.plaphy.2025.109765","DOIUrl":null,"url":null,"abstract":"<div><div>A complex interplay of environmental factors profoundly influences plant cellular metabolism, with gaseous exchange serving as a fundamental physiological process critical to growth and survival. While well-characterized in natural environments, the role of gaseous exchange in plant <em>in-vitro</em> culture remains underexplored. Plant <em>in-vitro</em> culture offers a versatile platform for studying metabolism, where metabolic networks are highly flexible and sensitive to environmental factors. Despite advancements in understanding these dynamics, there has been relatively little investigation into how gaseous exchange within tissue culture systems affects cellular metabolism. In the present study, we investigated the effects of gaseous exchange on plant growth and metabolism by comparing traditional Parafilm- and micropore-tape-based cultures designed to facilitate different levels of gaseous exchange. A comprehensive metabolomics approach using liquid chromatography-high-resolution mass spectrometry and gas chromatography-mass spectrometry was employed to delineate the metabolic changes in <em>Arabidopsis</em> under Parafilm- and micropore-tape-sealed culture conditions at two and three weeks of growth. Metabolic profiling identified increased levels of oxidized glutathione, arginine, ornithine, and aspartic acid, and decreased levels of TCA cycle intermediates and phenylpropanoid metabolites, indicating that restricted gas exchange alters the redox status and reprograms primary and secondary metabolism. This reprogramming affected amino acid metabolism, arginine metabolism, energy metabolism, as well as phenylpropanoid and flavonoid biosynthetic pathways. Restricted gaseous exchange in Parafilm-wrapped cultures also led to altered accumulation of several essential macro- and microelements in <em>Arabidopsis seedlings</em>. The present study demonstrated that restricted gaseous exchange inhibits plant growth and disrupts metabolism.</div></div>","PeriodicalId":20234,"journal":{"name":"Plant Physiology and Biochemistry","volume":"222 ","pages":"Article 109765"},"PeriodicalIF":6.1000,"publicationDate":"2025-03-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Physiology and Biochemistry","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0981942825002931","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
A complex interplay of environmental factors profoundly influences plant cellular metabolism, with gaseous exchange serving as a fundamental physiological process critical to growth and survival. While well-characterized in natural environments, the role of gaseous exchange in plant in-vitro culture remains underexplored. Plant in-vitro culture offers a versatile platform for studying metabolism, where metabolic networks are highly flexible and sensitive to environmental factors. Despite advancements in understanding these dynamics, there has been relatively little investigation into how gaseous exchange within tissue culture systems affects cellular metabolism. In the present study, we investigated the effects of gaseous exchange on plant growth and metabolism by comparing traditional Parafilm- and micropore-tape-based cultures designed to facilitate different levels of gaseous exchange. A comprehensive metabolomics approach using liquid chromatography-high-resolution mass spectrometry and gas chromatography-mass spectrometry was employed to delineate the metabolic changes in Arabidopsis under Parafilm- and micropore-tape-sealed culture conditions at two and three weeks of growth. Metabolic profiling identified increased levels of oxidized glutathione, arginine, ornithine, and aspartic acid, and decreased levels of TCA cycle intermediates and phenylpropanoid metabolites, indicating that restricted gas exchange alters the redox status and reprograms primary and secondary metabolism. This reprogramming affected amino acid metabolism, arginine metabolism, energy metabolism, as well as phenylpropanoid and flavonoid biosynthetic pathways. Restricted gaseous exchange in Parafilm-wrapped cultures also led to altered accumulation of several essential macro- and microelements in Arabidopsis seedlings. The present study demonstrated that restricted gaseous exchange inhibits plant growth and disrupts metabolism.
期刊介绍:
Plant Physiology and Biochemistry publishes original theoretical, experimental and technical contributions in the various fields of plant physiology (biochemistry, physiology, structure, genetics, plant-microbe interactions, etc.) at diverse levels of integration (molecular, subcellular, cellular, organ, whole plant, environmental). Opinions expressed in the journal are the sole responsibility of the authors and publication does not imply the editors'' agreement.
Manuscripts describing molecular-genetic and/or gene expression data that are not integrated with biochemical analysis and/or actual measurements of plant physiological processes are not suitable for PPB. Also "Omics" studies (transcriptomics, proteomics, metabolomics, etc.) reporting descriptive analysis without an element of functional validation assays, will not be considered. Similarly, applied agronomic or phytochemical studies that generate no new, fundamental insights in plant physiological and/or biochemical processes are not suitable for publication in PPB.
Plant Physiology and Biochemistry publishes several types of articles: Reviews, Papers and Short Papers. Articles for Reviews are either invited by the editor or proposed by the authors for the editor''s prior agreement. Reviews should not exceed 40 typewritten pages and Short Papers no more than approximately 8 typewritten pages. The fundamental character of Plant Physiology and Biochemistry remains that of a journal for original results.