{"title":"Integrated physiological, transcriptomic, and metabolomic analyses of <i>Chrysanthemum</i> 'Boju' under excessive indole-3-acetic acid stress.","authors":"Yuqing Wang, Yingying Duan, Na Chen, Wanyue Ding, Yaowu Liu, Shihai Xing","doi":"10.3389/fpls.2025.1531585","DOIUrl":null,"url":null,"abstract":"<p><strong>Introduction: </strong>Indole-3-acetic acid (IAA) is a key plant hormone involved in regulating development and responses to abiotic stress. However, excessive IAA treatment can induce oxidative stress, impair growth, and potentially lead to plant death. This study investigates the effects of excessive IAA exposure on the growth of <i>Chrysanthemum morifolium</i> (Boju), focusing on the underlying molecular mechanisms.</p><p><strong>Methods: </strong>We treated <i>C. morifolium</i> with 10 mg/L IAA for nine consecutive days. The impact of this treatment was assessed from various perspectives, including physiological (chlorophyll, carotenoids, and MDA content), biochemical (antioxidant enzyme activities), and molecular (transcriptomic and metabolomic analyses).</p><p><strong>Results: </strong>IAA treatment significantly increased chlorophyll a, chlorophyll b, and carotenoid levels by 37%, 46%, and 25%, respectively, compared to pre-treatment levels, suggesting that <i>C. morifolium</i> was experiencing stress. Additionally, the malondialdehyde (MDA) content was 1.79 times higher than pre-treatment levels, confirming oxidative stress. To combat this, the plant enhanced its antioxidant defense mechanisms, as shown by a 93.8% increase in peroxidase (POD) activity and a 45% increase in superoxide dismutase (SOD) activity. Exogenous IAA treatment also led to a significant reduction in endogenous hormone levels, including gibberellins (GA<sub>3</sub> and GA<sub>4</sub>), abscisic acid (ABA), and IAA, with decreases of 93%, 45%, 99%, and 99%, respectively.Transcriptomic and metabolomic analyses identified 263 differentially expressed metabolites and 144 differentially expressed genes.</p><p><strong>Discussion: </strong>These results suggest that <i>C. morifolium</i> is experiencing stress under prolonged IAA treatment and likely limits its growth by reducing endogenous hormone levels to mitigate oxidative stress. The transcriptomic and metabolomic results showed the upregulation of stress-related genes, including proB (Glutamate 5-kinase), proA (Glutamate-5-semialdehyde dehydrogenase), GAD (Glutamate decarboxylase), and peroxidases, alongside the downregulation of PK (Pyruvate kinase), indicateing a complex response involving the regulation of amino acid biosynthesis, coumaric acid metabolism, starch and sucrose metabolism, and pyruvate metabolism. This study highlights the nonlinear effects of IAA on plant growth and stress responses, emphasizing the intricate molecular mechanisms involved in coping with excessive IAA-induced stress.</p>","PeriodicalId":12632,"journal":{"name":"Frontiers in Plant Science","volume":"16 ","pages":"1531585"},"PeriodicalIF":4.1000,"publicationDate":"2025-04-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12061948/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Plant Science","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.3389/fpls.2025.1531585","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Introduction: Indole-3-acetic acid (IAA) is a key plant hormone involved in regulating development and responses to abiotic stress. However, excessive IAA treatment can induce oxidative stress, impair growth, and potentially lead to plant death. This study investigates the effects of excessive IAA exposure on the growth of Chrysanthemum morifolium (Boju), focusing on the underlying molecular mechanisms.
Methods: We treated C. morifolium with 10 mg/L IAA for nine consecutive days. The impact of this treatment was assessed from various perspectives, including physiological (chlorophyll, carotenoids, and MDA content), biochemical (antioxidant enzyme activities), and molecular (transcriptomic and metabolomic analyses).
Results: IAA treatment significantly increased chlorophyll a, chlorophyll b, and carotenoid levels by 37%, 46%, and 25%, respectively, compared to pre-treatment levels, suggesting that C. morifolium was experiencing stress. Additionally, the malondialdehyde (MDA) content was 1.79 times higher than pre-treatment levels, confirming oxidative stress. To combat this, the plant enhanced its antioxidant defense mechanisms, as shown by a 93.8% increase in peroxidase (POD) activity and a 45% increase in superoxide dismutase (SOD) activity. Exogenous IAA treatment also led to a significant reduction in endogenous hormone levels, including gibberellins (GA3 and GA4), abscisic acid (ABA), and IAA, with decreases of 93%, 45%, 99%, and 99%, respectively.Transcriptomic and metabolomic analyses identified 263 differentially expressed metabolites and 144 differentially expressed genes.
Discussion: These results suggest that C. morifolium is experiencing stress under prolonged IAA treatment and likely limits its growth by reducing endogenous hormone levels to mitigate oxidative stress. The transcriptomic and metabolomic results showed the upregulation of stress-related genes, including proB (Glutamate 5-kinase), proA (Glutamate-5-semialdehyde dehydrogenase), GAD (Glutamate decarboxylase), and peroxidases, alongside the downregulation of PK (Pyruvate kinase), indicateing a complex response involving the regulation of amino acid biosynthesis, coumaric acid metabolism, starch and sucrose metabolism, and pyruvate metabolism. This study highlights the nonlinear effects of IAA on plant growth and stress responses, emphasizing the intricate molecular mechanisms involved in coping with excessive IAA-induced stress.
期刊介绍：
In an ever changing world, plant science is of the utmost importance for securing the future well-being of humankind. Plants provide oxygen, food, feed, fibers, and building materials. In addition, they are a diverse source of industrial and pharmaceutical chemicals. Plants are centrally important to the health of ecosystems, and their understanding is critical for learning how to manage and maintain a sustainable biosphere. Plant science is extremely interdisciplinary, reaching from agricultural science to paleobotany, and molecular physiology to ecology. It uses the latest developments in computer science, optics, molecular biology and genomics to address challenges in model systems, agricultural crops, and ecosystems. Plant science research inquires into the form, function, development, diversity, reproduction, evolution and uses of both higher and lower plants and their interactions with other organisms throughout the biosphere. Frontiers in Plant Science welcomes outstanding contributions in any field of plant science from basic to applied research, from organismal to molecular studies, from single plant analysis to studies of populations and whole ecosystems, and from molecular to biophysical to computational approaches.
Frontiers in Plant Science publishes articles on the most outstanding discoveries across a wide research spectrum of Plant Science. The mission of Frontiers in Plant Science is to bring all relevant Plant Science areas together on a single platform.
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