Cotton Ascorbate Oxidase Promotes Cell Growth in Cultured Tobacco Bright Yellow-2 Cells through Generation of Apoplast Oxidation

Ascorbate oxidase (AO) plays an important role in cell growth through the modulation of reduction/oxidation (redox) control of the apoplast. Here, a cotton (Gossypium hirsutum) apoplastic ascorbate oxidase gene (GhAO1) was obtained from fast elongating fiber tissues. GhAO1 belongs to the multicopper oxidase (MCO) family and includes a signal peptide and several transmembrane regions. Analyses of quantitative real-time polymerase chain reaction (QRT-PCR) and enzyme activity showed that GhAO1 was expressed abundantly in 15-day post-anthesis (dpa) wild-type (WT) fibers in comparison with fuzzless-lintless (fl) mutant ovules. Subcellular distribution analysis in onion cells demonstrated that GhAO1 is localized in the cell wall. In transgenic tobacco bright yellow-2 (BY-2) cells with ectopic overexpression of GhAO1, the enhancement of cell growth with 1.52-fold increase in length versus controls was indicated, as well as the enrichment of both total ascorbate in whole-cells and dehydroascorbate acid (DHA) in apoplasts. In addition, promoted activities of AO and monodehydroascorbate reductase (MDAR) in apoplasts and dehydroascorbate reductase (DHAR) in whole-cells were displayed in transgenic tobacco BY-2 cells. Accumulation of H2O2, and influenced expressions of Ca2+ channel genes with the activation of NtMPK9 and NtCPK5 and the suppression of NtTPC1B were also demonstrated in transgenic tobacco BY-2 cells. Finally, significant induced expression of the tobacco NtAO gene in WT BY-2 cells under indole-3-acetic acid (IAA) treatment appeared; however, the sensitivity of the NtAO gene expression to IAA disappeared in transgenic BY-2 cells, revealing that the regulated expression of the AO gene is under the control of IAA. Taken together, these results provide evidence that GhAO1 plays an important role in fiber cell elongation and may promote cell growth by generating the oxidation of apoplasts, via the auxin-mediated signaling pathway.

• Publication year

  2017

• Venue

  International Journal of Molecular Sciences

• Publication date

  2017-06-23

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.3390/ijms18071346PMID 28644407PMCID 5535839
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Metabolites of 2,3-diketogulonate delay peroxidase action and induce non-enzymic H2O2 generation: Potential roles in the plant cell wall

  2017cited by this paper
• AIK1, A Mitogen-Activated Protein Kinase, Modulates Abscisic Acid Responses through the MKK5-MPK6 Kinase Cascade1[OPEN]

  2016cited by this paper
• A Cotton Annexin Affects Fiber Elongation and Secondary Cell Wall Biosynthesis Associated with Ca2+ Influx, ROS Homeostasis, and Actin Filament Reorganization1

  2016cited by this paper
• Cloning and Functional Analysis of the Promoter of an Ascorbate Oxidase Gene from Gossypium hirsutum

  2016cited by this paper
• Reactive Oxygen Species (ROS): Beneficial Companions of Plants’ Developmental Processes

  2016cited by this paper
• An NADPH-Oxidase/Polyamine Oxidase Feedback Loop Controls Oxidative Burst Under Salinity1

  2016cited by this paper
• Interactions between Auxin, Microtubules and XTHs Mediate Green Shade- Induced Petiole Elongation in Arabidopsis

  2014cited by this paper
• Altered apoplastic ascorbate redox state in tobacco plants via ascorbate oxidase overexpression results in delayed dark-induced senescence in detached leaves.

  2013cited by this paper
• The Gossypium raimondii genome, a huge leap forward in cotton genomics.

  2013cited by this paper
• A diminution in ascorbate oxidase activity affects carbon allocation and improves yield in tomato under water deficit.

  2013cited by this paper
• Ascorbate oxidase is the potential conductor of a symphony of signaling pathways

  2013cited by this paper
• A burst of plant NADPH oxidases.

  2012cited by this paper
• Spatiotemporal manipulation of auxin biosynthesis in cotton ovule epidermal cells enhances fiber yield and quality

  2011cited by this paper
• How cotton fibers elongate: a tale of linear cell-growth mode.

  2011cited by this paper
• Spermidine oxidase-derived H₂O₂ regulates pollen plasma membrane hyperpolarization-activated Ca(2+) -permeable channels and pollen tube growth.

  2010cited by this paper
• Cotton GhPOX1 encoding plant class III peroxidase may be responsible for the high level of reactive oxygen species production that is related to cotton fiber elongation.

  2009cited by this paper
• The ascorbate peroxidase regulated by H2O2 and ethylene is involved in cotton fiber cell elongation by modulating ROS homeostasis

  2008cited by this paper
• Altered stomatal dynamics in ascorbate oxidase over-expressing tobacco plants suggest a role for dehydroascorbate signalling.

  2008cited by this paper
• Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs

  2007cited by this paper
• A cotton ascorbate peroxidase is involved in hydrogen peroxide homeostasis during fibre cell development.

  2007cited by this paper
• Control of Plant Development by Reactive Oxygen Species1

  2006cited by this paper
• The role of reactive oxygen species in cell growth: lessons from root hairs.

  2006cited by this paper
• Journal of Experimental Botany Advance Access published September 22, 2006 Journal of Experimental Botany, Page 1 of 11

  2006cited by this paper
• Ascorbate Oxidase-Dependent Changes in the Redox State of the Apoplast Modulate Gene Transcript Accumulation Leading to Modified Hormone Signaling and Orchestration of Defense Processes in Tobacco1[W]

  2006cited by this paper
• Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context

  2005cited by this paper
• Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-l-threonate

  2005cited by this paper
• Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants.

  2005cited by this paper
• Redox Homeostasis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses

  2005cited by this paper
• Production of Reactive Oxygen Intermediates (O2˙−, H2O2, and ˙OH) by Maize Roots and Their Role in Wall Loosening and Elongation Growth

  2004cited by this paper
• Zonal Changes in Ascorbate and Hydrogen Peroxide Contents, Peroxidase, and Ascorbate-Related Enzyme Activities in Onion Roots1

  2003cited by this paper
• Apoplastic ascorbate metabolism and its role in the regulation of cell signalling.

  2003influential reference
• The Function of Ascorbate Oxidase in Tobacco1

  2003cited by this paper
• Reactive oxygen species produced by NADPH oxidase regulate plant cell growth

  2003cited by this paper
• Evidence that hydroxyl radicals mediate auxin-induced extension growth

  2002cited by this paper
• Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth.

  2002cited by this paper
• ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis.

  2001cited by this paper
• Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis.

  2001cited by this paper
• Role of auxin-induced reactive oxygen species in root gravitropism.

  2001cited by this paper
• Simulating ozone detoxification in the leaf apoplast through the direct reaction with ascorbate

  2000cited by this paper
• Expansion of transgenic tobacco protoplasts expressing pumpkin ascorbate oxidase is more rapid than that of wild-type protoplasts

  2000cited by this paper
• Auxin metabolism in the root apical meristem.

  2000cited by this paper
• Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells

  1999cited by this paper
• Characterization and expression of a new class of zinc finger protein that binds to silencer region of ascorbate oxidase gene.

  1998cited by this paper
• Melon ascorbate oxidase: cloning of a multigene family, induction during fruit development and repression by wounding

  1997cited by this paper
• cDNA cloning and gene expression of ascorbate oxidase in tobacco

  1996cited by this paper
• Structure of the genomic DNA encoding cucumber ascorbate oxidase and its expression in transgenic plants

  1994cited by this paper
• Ascorbate oxidase of Cucumis melo L. var. reticulatus: purification, characterization and antibody production

  1994cited by this paper
• Tobacco BY-2 Cell Line as the “HeLa” Cell in the Cell Biology of Higher Plants

  1992cited by this paper
• Regulation of ascorbate oxidase expression in pumpkin by auxin and copper.

  1992cited by this paper
• Expression of Ascorbic Acid Oxidase in Zucchini Squash (Cucurbita pepo L.).

  1991cited by this paper
• Molecular cloning and nucleotide sequence of full-length cDNA for ascorbate oxidase from cultured pumpkin cells.

  1990cited by this paper
• Functional evidence for an auxin receptor at the plasmalemma of tobacco mesophyll protoplasts.

  1989cited by this paper
• Ascorbate free radical enhances vacuolization in onion root meristems

  1989cited by this paper
• Hormonal Control of Elongation of Tobacco Cells Derived from Protoplasts

  1983cited by this paper
• A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.

  1976cited by this paper

• Contrary to convention: Apoplastic ascorbate oxidation surfaces as a crucial conductor in salt stress

  2026cites this paper
• QTL Mapping and Candidate Gene Analysis for Cotton Fiber Quality and Early Maturity Using F2 and F3 Generations

  2025cites this paper
• Sustainable medicinal plant production - responses of Lamiaceae plants to organic acid elicitors spraying during environmental stress: A review

  2025cites this paper
• Revisiting the role of ascorbate oxidase in plant systems

  2024cites this paper
• Ascorbic acid as a master redox regulator of fruit ripening

  2024cites this paper
• Gene Profiling of the Ascorbate Oxidase Family Genes under Osmotic and Cold Stress Reveals the Role of AnAO5 in Cold Adaptation in Ammopiptanthus nanus

  2023cites this paper
• Ascorbate oxidation stimulates rice root growth via effects on auxin and abscisic acid levels

  2023cites this paper
• Multicopper oxidases GbAO and GbSKS are involved in the Verticillium dahliae resistance in Gossypium barbadense.

  2022cites this paper
• Alkaline Salt Tolerance of the Biomass Plant Arundo donax

  2022cites this paper
• The Multiple Roles of Ascorbate in the Abiotic Stress Response of Plants: Antioxidant, Cofactor, and Regulator

  2021cites this paper
• Plant Copper Metalloenzymes As Prospects for New Metabolism Involving Aromatic Compounds

  2021cites this paper
• Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes

  2021cites this paper
• Genome-Wide Analysis of MDHAR Gene Family in Four Cotton Species Provides Insights into Fiber Development via Regulating AsA Redox Homeostasis

  2021influential citation
• Ascorbate oxidation activates systemic defence against root-knot nematode Meloidogyne graminicola in rice.

  2020cites this paper
• The semi-dwarfing gene Rht-dp from dwarf polish wheat (Triticum polonicum L.) is the "Green Revolution” gene Rht-B1b

  2020cites this paper
• Characterisation of the non-oxidative degradation pathway of dehydroascorbic acid in slightly acidic aqueous solution.

  2019cites this paper
• Vitamin C in Plants: Novel Concepts, New Perspectives, and Outstanding Issues

  2019cites this paper
• Vitamin C in Plants: From Functions to Biofortification

  2019cites this paper
• Regulation of Ascorbate-Glutathione Pathway in Mitigating Oxidative Damage in Plants under Abiotic Stress

  2019cites this paper
• GhVTC1, the Key Gene for Ascorbate Biosynthesis in Gossypium hirsutum, Involves in Cell Elongation under Control of Ethylene

  2019influential citation
• Deep Transcriptome Analysis Reveals Reactive Oxygen Species (ROS) Network Evolution, Response to Abiotic Stress, and Regulation of Fiber Development in Cotton

  2019influential citation
• A Cotton (Gossypium hirsutum) Myo-Inositol-1-Phosphate Synthase (GhMIPS1D) Gene Promotes Root Cell Elongation in Arabidopsis

  2019cites this paper
• Genome-Wide Identification and Expression Analysis of the Ascorbate Oxidase Gene Family in Gossypium hirsutum Reveals the Critical Role of GhAO1A in Delaying Dark-Induced Leaf Senescence

  2019cites this paper
• Triacontanol Alleviated Nickel Toxicity in Maize Seedling by Controlling Its Uptake and Enhancing Antioxidant System

  2019cites this paper
• Genome-wide investigation and expression profiling of APX gene family in Gossypium hirsutum provide new insights in redox homeostasis maintenance during different fiber development stages

  2018cites this paper
• A dual-model strategy for fluorometric determination of ascorbic acid and of ascorbic acid oxidase activity by using DNA-templated gold-silver nanoclusters

  2018cites this paper
• Oxalyltransferase, a plant cell‐wall acyltransferase activity, transfers oxalate groups from ascorbate metabolites to carbohydrates

  2018cites this paper
• A Gossypium hirsutum GDSL lipase/hydrolase gene (GhGLIP) appears to be involved in promoting seed growth in Arabidopsis

  2018cites this paper
• The Role of Ascorbate in Plant Growth and Development

  2017cites this paper
• Ascorbate Oxidase in Plant Growth, Development, and Stress Tolerance

  2017cites this paper