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      Low light intensity elongates period and defers peak time of photosynthesis: a computational approach to circadian-clock-controlled photosynthesis in tomato

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          Abstract

          Photosynthesis is involved in the essential process of transforming light energy into chemical energy. Although the interaction between photosynthesis and the circadian clock has been confirmed, the mechanism of how light intensity affects photosynthesis through the circadian clock remains unclear. Here, we propose a first computational model for circadian-clock-controlled photosynthesis, which consists of the light-sensitive protein P, the core oscillator, photosynthetic genes, and parameters involved in the process of photosynthesis. The model parameters were determined by minimizing the cost function ( \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{upgreek} \usepackage{mathrsfs} \setlength{\oddsidemargin}{-69pt} \begin{document} }{}$\boldsymbol{\delta} =\mathbf{8.56}$\end{document} ), which is defined by the errors of expression levels, periods, and phases of the clock genes ( CCA1, PRR9, TOC1, ELF4, GI, and RVE8). The model recapitulates the expression pattern of the core oscillator under moderate light intensity (100 μmol m −2 s −1). Further simulation validated the dynamic behaviors of the circadian clock and photosynthetic outputs under low (62.5 μmol m −2 s −1) and normal (187.5 μmol m −2 s −1) intensities. When exposed to low light intensity, the peak times of clock and photosynthetic genes were shifted backward by 1–2 hours, the period was elongated by approximately the same length, and the photosynthetic parameters attained low values and showed delayed peak times, which confirmed our model predictions. Our study reveals a potential mechanism underlying the circadian regulation of photosynthesis by the clock under different light intensities in tomato.

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          Most cited references90

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          Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression.

          The CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene encodes a MYB-related transcription factor involved in the phytochrome induction of a light-harvesting chlorophyll a/b-protein (Lhcb) gene. Expression of the CCA1 gene is transiently induced by phytochrome and oscillates with a circadian rhythm. Constitutive expression of CCA1 protein in transgenic plants abolished the circadian rhythm of several genes with dramatically different phases. These plants also had longer hypocotyls and delayed flowering, developmental processes regulated by light and the circadian clock. Furthermore, the expression of both endogenous CCA1 and the related LHY gene was suppressed. Our results suggest that CCA1 is a part of a feedback loop that is closely associated with the circadian clock in Arabidopsis.
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            PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock.

            An interlocking transcriptional-translational feedback loop of clock-associated genes is thought to be the central oscillator of the circadian clock in plants. TIMING OF CAB EXPRESSION1 (also called PSEUDO-RESPONSE REGULATOR1 [PRR1]) and two MYB transcription factors, CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), play pivotal roles in the loop. Genetic studies have suggested that PRR9, PRR7, and PRR5 also act within or close to the loop; however, their molecular functions remain unknown. Here, we demonstrate that PRR9, PRR7, and PRR5 act as transcriptional repressors of CCA1 and LHY. PRR9, PRR7, and PRR5 each suppress CCA1 and LHY promoter activities and confer transcriptional repressor activity to a heterologous DNA binding protein in a transient reporter assay. Using a glucocorticoid-induced PRR5-GR (glucorticoid receptor) construct, we found that PRR5 directly downregulates CCA1 and LHY expression. Furthermore, PRR9, PRR7, and PRR5 associate with the CCA1 and LHY promoters in vivo, coincident with the timing of decreased CCA1 and LHY expression. These results suggest that the repressor activities of PRR9, PRR7, and PRR5 on the CCA1 and LHY promoter regions constitute the molecular mechanism that accounts for the role of these proteins in the feedback loop of the circadian clock.
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              The Multifaceted Roles of HY5 in Plant Growth and Development.

              ELONGATED HYPOCOTYL5 (HY5), a member of the bZIP transcription factor family, inhibits hypocotyl growth and lateral root development, and promotes pigment accumulation in a light-dependent manner in Arabidopsis. Recent research on its role in different processes such as hormone, nutrient, abiotic stress (abscisic acid, salt, cold), and reactive oxygen species signaling pathways clearly places HY5 at the center of a transcriptional network hub. HY5 regulates the transcription of a large number of genes by directly binding to cis-regulatory elements. Recently, HY5 has also been shown to activate its own expression under both visible and UV-B light. Moreover, HY5 acts as a signal that moves from shoot to root to promote nitrate uptake and root growth. Here, we review recent advances on HY5 research in diverse aspects of plant development and highlight still open questions that need to be addressed in the near future for a complete understanding of its function in plant signaling and beyond.
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                Author and article information

                Contributors
                Journal
                Hortic Res
                Hortic Res
                hr
                Horticulture Research
                Oxford University Press
                2662-6810
                2052-7276
                June 2023
                25 April 2023
                25 April 2023
                : 10
                : 6
                : uhad077
                Affiliations
                College of Horticulture, Nanjing Agricultural University/State Key Laboratory of Crop Genetics and Germplasm Enhancement/Key Laboratory of Horticultural Crop Biology and Germplasm Creation in East China of Ministry of Agriculture and Rural Affairs Nanjing 210095, Jiangsu, China
                College of Horticulture, Nanjing Agricultural University/State Key Laboratory of Crop Genetics and Germplasm Enhancement/Key Laboratory of Horticultural Crop Biology and Germplasm Creation in East China of Ministry of Agriculture and Rural Affairs Nanjing 210095, Jiangsu, China
                College of Horticulture, Nanjing Agricultural University/State Key Laboratory of Crop Genetics and Germplasm Enhancement/Key Laboratory of Horticultural Crop Biology and Germplasm Creation in East China of Ministry of Agriculture and Rural Affairs Nanjing 210095, Jiangsu, China
                The Institute of Agricultural Information, Jiangsu Province Academy of Agricultural Sciences , Nanjing 210014, Jiangsu, China
                College of Horticulture, Nanjing Agricultural University/State Key Laboratory of Crop Genetics and Germplasm Enhancement/Key Laboratory of Horticultural Crop Biology and Germplasm Creation in East China of Ministry of Agriculture and Rural Affairs Nanjing 210095, Jiangsu, China
                Laboratory for Genetic Improvement of High Efficiency Horticultural Crops in Jiangsu Province, Institute of Vegetable Crop, Jiangsu Province Academy of Agricultural Sciences , Nanjing 210014, Jiangsu, China
                College of Horticulture, Nanjing Agricultural University/State Key Laboratory of Crop Genetics and Germplasm Enhancement/Key Laboratory of Horticultural Crop Biology and Germplasm Creation in East China of Ministry of Agriculture and Rural Affairs Nanjing 210095, Jiangsu, China
                College of Horticulture, Nanjing Agricultural University/State Key Laboratory of Crop Genetics and Germplasm Enhancement/Key Laboratory of Horticultural Crop Biology and Germplasm Creation in East China of Ministry of Agriculture and Rural Affairs Nanjing 210095, Jiangsu, China
                College of Sciences, Nanjing Agricultural University , Nanjing 210095, Jiangsu China
                Author notes

                Ting Huang, HuiLiu and Jian-Ping Tao, Equal contribution.

                Article
                uhad077
                10.1093/hr/uhad077
                10261901
                37323229
                426077b1-a04d-4926-8629-d1821dfb5dd9
                © The Author(s) 2023. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 3 August 2022
                : 9 April 2023
                : 1 June 2023
                Page count
                Pages: 14
                Funding
                Funded by: National Natural Science Foundation of China, DOI 10.13039/501100001809;
                Award ID: 11171155
                Award ID: 11871268
                Funded by: National Natural Science Foundation of Jiangsu Province, China;
                Award ID: BK20171370
                Award ID: BK20221009
                Funded by: Jiangsu Agricultural Science and Technology Innovation Fund, DOI 10.13039/100007540;
                Award ID: CX (21) 3025
                Funded by: China Postdoctoral Science Foundation, DOI 10.13039/501100002858;
                Award ID: 2021 M701742
                Funded by: Priority Academic Program Development of Jiangsu Higher Education Institution Project (PAPD);
                Categories
                Article
                AcademicSubjects/SCI01140

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