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      Is Open Access

      A neutral invertase controls cell division besides hydrolysis of sucrose for nutrition during germination and seed setting in rice

      research-article
      Author(s): 1 , 3 , ∗ , 2 , 2
      Publication date (Electronic):
      Journal: iScience
      Publisher: Elsevier
      Keywords: Cell biology, Plant biology, Plant development

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          Summary

          Sucrose is the transport form of carbohydrate in plants serving as signal molecule besides nutrition, but the signaling is elusive. Here, neutral invertase 8 (OsNIN8) mutated at G461R into OsNIN8m, which increased its charge and hydrophobicity, decreased hydrolysis of sucrose to 13% and firmer binding to sucrose than the wildtype. This caused downstream metabolites and energy accumulation forming overnutrition. Paradoxically, division of subinitials in longitudinal cell lineages was only about 15 times but more than 100 times in wildtype, resulting in short radicle. Further, mutation of OsNIN8 into deficiency of hydrolysis but maintenance of sucrose binding allowed cell division until ran out of energy showing the association but not hydrolysis gave the signal. Chemically, sucrose binding to OsNIN8 was exothermic but to OsNIN8m was endothermic. Therefore, OsNIN8m lost the signal function owing to change of thermodynamic state. So, OsNIN8 sensed sucrose for cell division besides hydrolyzed sucrose.

          Graphical abstract

          Highlights

          • •

            OsNIN8 binds to and hydrolyzes sucrose for cell division in root tip during germination

          • •

            OsNIN8 Wildtype exothermic association with sucrose initiates signal for cell division

          • •

            The signal controls cell division of subinitials in longitudinal cell lineages

          • •

            Sucrose roles of nutrition and signal can be separated in different mutants

          Abstract

          Cell biology; Plant biology; Plant development

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          Most cited references63

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          Sucrose metabolism: gateway to diverse carbon use and sugar signaling.

          Yong-Ling Ruan (2014)
          Sucrose metabolism plays pivotal roles in development, stress response, and yield formation, mainly by generating a range of sugars as metabolites to fuel growth and synthesize essential compounds (including protein, cellulose, and starch) and as signals to regulate expression of microRNAs, transcription factors, and other genes and for crosstalk with hormonal, oxidative, and defense signaling. This review aims to capture the most exciting developments in this area by evaluating (a) the roles of key sucrose metabolic enzymes in development, abiotic stress responses, and plant-microbe interactions; (b) the coupling between sucrose metabolism and sugar signaling from extra- to intracellular spaces; (c) the different mechanisms by which sucrose metabolic enzymes could perform their signaling roles; and (d) progress on engineering sugar metabolism and transport for high yield and disease resistance. Finally, the review outlines future directions for research on sugar metabolism and signaling to better understand and improve plant performance.
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            Genetic compensation triggered by mutant mRNA degradation

            Mohamed El-Brolosy, Zacharias Kontarakis, Andrea Rossi … (2019)
            Genetic robustness, or the ability of an organism to maintain fitness in the presence of mutations, can be achieved via protein feedback loops. Recent evidence suggests that organisms may also respond to mutations by upregulating related gene(s) independently of protein feedback loops, a phenomenon called transcriptional adaptation. However, the prevalence of transcriptional adaptation and its underlying molecular mechanisms are unknown. Here, by analyzing several models of transcriptional adaptation in zebrafish and mouse, we show a requirement for mRNA degradation. Alleles that fail to transcribe the mutated gene do not display transcriptional adaptation and exhibit more severe phenotypes than alleles displaying mutant mRNA decay. Transcriptome analysis reveals the upregulation of a substantial proportion of the genes that exhibit sequence similarity with the mutated gene’s mRNA, suggesting a sequence dependent mechanism. Besides implications for our understanding of disease-causing mutations, these findings will help design mutant alleles with minimal transcriptional adaptation-derived compensation.
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              Thermodynamics of protein association reactions: forces contributing to stability

              Philip Ross, S. Subramanian (2002)
              Article 0 comments Cited 358 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Zizhang Wang
                Journal
                Journal ID (nlm-ta): iScience
                Journal ID (iso-abbrev): iScience
                Title: iScience
                Publisher: Elsevier
                ISSN (Electronic): 2589-0042
                Publication date PMC-release: 08 June 2024
                Publication date Collection: 19 July 2024
                Publication date (Electronic): 08 June 2024
                Volume: 27
                Issue: 7
                Electronic Location Identifier: 110217
                Affiliations
                [1 ]Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
                [2 ]Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of Sciences, Beijing 100190, China
                Author notes
                [∗ ]Corresponding author zizhangw@ 123456ibcas.ac.cn
                [3]

                Lead contact

                Article
                Publisher Item ID: S2589-0042(24)01442-1 Publisher ID: 110217
                DOI: 10.1016/j.isci.2024.110217
                PMC ID: 11237924
                PubMed ID: 38993663
                SO-VID: bf94502d-886e-429b-b45b-73328222b3b8
                Copyright © © 2024 The Authors
                License:

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 10 February 2023
                Date revision received : 25 May 2023
                Date accepted : 5 June 2024
                Categories
                Subject: Article

                Keywords: cell biology,plant biology,plant development
                Data availability:
                Keywords: cell biology, plant biology, plant development

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