Spatial and temporal regulation of the metabolism of reactive oxygen and nitrogen species during the early development of pepper (Capsicum annuum) seedlings.

BACKGROUND AND AIMS The development of seedlings involves many morphological, physiological and biochemical processes, which are controlled by many factors. Some reactive oxygen and nitrogen species (ROS and RNS, respectively) are implicated as signal molecules in physiological and phytopathological processes. Pepper (Capsicum annuum) is a very important crop and the goal of this work was to provide a framework of the behaviour of the key elements in the metabolism of ROS and RNS in the main organs of pepper during its development. METHODS The main seedling organs (roots, hypocotyls and green cotyledons) of pepper seedlings were analysed 7, 10 and 14 d after germination. Activity and gene expression of the main enzymatic antioxidants (catalase, ascorbate-glutathione cycle enzymes), NADP-generating dehydrogenases and S-nitrosoglutathione reductase were determined. Cellular distribution of nitric oxide ((·)NO), superoxide radical (O2 (·-)) and peroxynitrite (ONOO(-)) was investigated using confocal laser scanning microscopy. KEY RESULTS The metabolism of ROS and RNS during pepper seedling development was highly regulated and showed significant plasticity, which was co-ordinated among the main seedling organs, resulting in correct development. Catalase showed higher activity in the aerial parts of the seedling (hypocotyls and green cotyledons) whereas roots of 7-d-old seedlings contained higher activity of the enzymatic components of the ascorbate glutathione cycle, NADP-isocitrate dehydrogenase and NADP-malic enzyme. CONCLUSIONS There is differential regulation of the metabolism of ROS, nitric oxide and NADP dehydrogenases in the different plant organs during seedling development in pepper in the absence of stress. The metabolism of ROS and RNS seems to contribute significantly to plant development since their components are involved directly or indirectly in many metabolic pathways. Thus, specific molecules such as H2O2 and NO have implications for signalling, and their temporal and spatial regulation contributes to the success of seedling establishment.

[1]  A. D. Shapiro Nitric oxide signaling in plants. , 2021, Vitamins and hormones.

[2]  F. J. Corpas,et al.  Part of a Special Issue on Reactive Oxygen and Nitrogen Species , 2022 .

[3]  Xiaoning Li,et al.  Interaction of nitric oxide and reactive oxygen species and associated regulation of root growth in wheat seedlings under zinc stress. , 2015, Ecotoxicology and environmental safety.

[4]  J. Axelrod,et al.  Coordinating cell polarity: heading in the right direction? , 2014, Development.

[5]  M. Arasimowicz-Jelonek,et al.  New insights into pioneer root xylem development: evidence obtained from Populus trichocarpa plants grown under field conditions. , 2014, Annals of botany.

[6]  F. Pomar,et al.  Nitric oxide is required for determining root architecture and lignin composition in sunflower. Supporting evidence from microarray analyses. , 2014, Nitric oxide : biology and chemistry.

[7]  Gerrit T. S. Beemster,et al.  Leaf development: a cellular perspective , 2014, Front. Plant Sci..

[8]  L. Lanfranco,et al.  NO homeostasis is a key regulator of early nitrate perception and root elongation in maize* , 2013, Journal of experimental botany.

[9]  E. Vierling,et al.  S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis , 2013, Front. Plant Sci..

[10]  R. Vaňková,et al.  Redox control of plant growth and development. , 2013, Plant science : an international journal of experimental plant biology.

[11]  F. J. Corpas,et al.  Current overview of S-nitrosoglutathione (GSNO) in higher plants , 2013, Front. Plant Sci..

[12]  F. J. Corpas,et al.  Antioxidant Systems from Pepper (Capsicum annuum L.): Involvement in the Response to Temperature Changes in Ripe Fruits , 2013, International journal of molecular sciences.

[13]  Marek Šebela,et al.  Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. , 2013, Biochimie.

[14]  F. J. Corpas,et al.  Protein tyrosine nitration in higher plants grown under natural and stress conditions , 2013, Front. Plant Sci..

[15]  F. J. Corpas,et al.  Protein tyrosine nitration in pea roots during development and senescence , 2013, Journal of experimental botany.

[16]  Huan Wang,et al.  Responses of root architecture development to low phosphorus availability: a review , 2012, Annals of botany.

[17]  B. Mueller‐Roeber,et al.  ROS homeostasis during development: an evolutionary conserved strategy , 2012, Cellular and Molecular Life Sciences.

[18]  G. Loake,et al.  AtGSNOR1 function is required for multiple developmental programs in Arabidopsis , 2012, Planta.

[19]  Joaquín Herrero,et al.  The promoter region of the Zinnia elegans basic peroxidase isoenzyme gene contains cis-elements responsive to nitric oxide and hydrogen peroxide , 2012, Planta.

[20]  F. J. Corpas,et al.  Cytosolic NADP-isocitrate dehydrogenase in Arabidopsis leaves and roots , 2012, Biologia plantarum.

[21]  J. M. Palma,et al.  Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. , 2012, Plant, cell & environment.

[22]  Ulrich Schurr,et al.  Analyzing Lateral Root Development: How to Move Forward , 2012, Plant Cell.

[23]  K. T. ten Tusscher,et al.  Joining forces: feedback and integration in plant development. , 2011, Current opinion in genetics & development.

[24]  F. J. Corpas,et al.  Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. , 2011, Plant science : an international journal of experimental plant biology.

[25]  M. Petřivalský,et al.  The role of nitric oxide in the germination of plant seeds and pollen. , 2011, Plant science : an international journal of experimental plant biology.

[26]  F. J. Corpas,et al.  Detection and quantification of S-nitrosoglutathione (GSNO) in pepper (Capsicum annuum L.) plant organs by LC-ES/MS. , 2011, Plant & cell physiology.

[27]  Daniel R. Lewis,et al.  Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport , 2011, Proceedings of the National Academy of Sciences.

[28]  F. J. Corpas,et al.  Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress , 2011, Plant signaling & behavior.

[29]  E. Ishii‐Iwamoto,et al.  Changes in Energy Metabolism and Antioxidant Defense Systems During Seed Germination of the Weed Species Ipomoea triloba L. and the Responses to Allelochemicals , 2011, Journal of Chemical Ecology.

[30]  M. Hashimoto,et al.  Nitric oxide production induced in roots of Lotus japonicus by lipopolysaccharide from Mesorhizobium loti. , 2011, Plant & cell physiology.

[31]  J. León,et al.  In vivo protein tyrosine nitration in Arabidopsis thaliana , 2011, Journal of experimental botany.

[32]  P. Benfey,et al.  Intercellular Communication during Plant Development , 2011, Plant Cell.

[33]  Alexandre Boscari,et al.  Both Plant and Bacterial Nitrate Reductases Contribute to Nitric Oxide Production in Medicago truncatula Nitrogen-Fixing Nodules1[W][OA] , 2010, Plant Physiology.

[34]  F. Pallardó,et al.  A nuclear glutathione cycle within the cell cycle. , 2010, The Biochemical journal.

[35]  S. Gilroy,et al.  ROS in plant development. , 2010, Physiologia plantarum.

[36]  A. Zafra,et al.  Cellular localization of ROS and NO in olive reproductive tissues during flower development , 2010, BMC Plant Biology.

[37]  P. Nick,et al.  Plant cell division is specifically affected by nitrotyrosine , 2009, Journal of experimental botany.

[38]  C. Job,et al.  Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. , 2009, The Plant journal : for cell and molecular biology.

[39]  C. Tang,et al.  Atmospheric nitric oxide stimulates plant growth and improves the quality of spinach (Spinacia oleracea) , 2009 .

[40]  A. Krieger-Liszkay,et al.  In Vivo Cell Wall Loosening by Hydroxyl Radicals during Cress Seed Germination and Elongation Growth1[W][OA] , 2009, Plant Physiology.

[41]  H. El-Maarouf-Bouteau,et al.  The Mechanisms Involved in Seed Dormancy Alleviation by Hydrogen Cyanide Unravel the Role of Reactive Oxygen Species as Key Factors of Cellular Signaling during Germination[C][W] , 2009, Plant Physiology.

[42]  F. J. Corpas,et al.  Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. , 2009, Plant & cell physiology.

[43]  F. J. Corpas,et al.  NADP-dehydrogenases from pepper fruits: effect of maturation. , 2009, Physiologia plantarum.

[44]  F. J. Corpas,et al.  Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. , 2008, Plant & cell physiology.

[45]  H. El-Maarouf-Bouteau,et al.  From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. , 2008, Comptes rendus biologies.

[46]  F. Cánovas,et al.  Spatial distribution of cytosolic NADP(+)-isocitrate dehydrogenase in pine embryos and seedlings. , 2008, Tree physiology.

[47]  V. Shulaev,et al.  Reactive oxygen signaling and abiotic stress. , 2008, Physiologia plantarum.

[48]  J. Hancock,et al.  Nitric oxide synthesis and signalling in plants. , 2008, Plant, cell & environment.

[49]  E. Vierling,et al.  Modulation of Nitrosative Stress by S-Nitrosoglutathione Reductase Is Critical for Thermotolerance and Plant Growth in Arabidopsis [W] , 2008, The Plant Cell Online.

[50]  F. J. Corpas,et al.  Need of biomarkers of nitrosative stress in plants. , 2007, Trends in plant science.

[51]  C. Bailly,et al.  ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. , 2007, The Plant journal : for cell and molecular biology.

[52]  F. J. Corpas,et al.  Nitrosative stress in plants , 2007, FEBS letters.

[53]  S. Jurga,et al.  A comparative study of water distribution, free radical production and activation of antioxidative metabolism in germinating pea seeds. , 2006, Journal of plant physiology.

[54]  F. Van Breusegem,et al.  Reactive oxygen species as signals that modulate plant stress responses and programmed cell death , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[55]  H. Hirt,et al.  Reactive oxygen species signaling in plants. , 2006, Antioxidants & redox signaling.

[56]  F. J. Corpas,et al.  The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. , 2006, Plant, cell & environment.

[57]  Jordi Moreno-Romero,et al.  Modification of intracellular levels of glutathione-dependent formaldehyde dehydrogenase alters glutathione homeostasis and root development. , 2006, Plant, cell & environment.

[58]  L. Dolan,et al.  The role of reactive oxygen species in cell growth: lessons from root hairs. , 2006, Journal of experimental botany.

[59]  F. J. Corpas,et al.  Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. , 2006, Journal of experimental botany.

[60]  G. Noctor Metabolic signalling in defence and stress: the central roles of soluble redox couples. , 2006, Plant, cell & environment.

[61]  R. Hayes,et al.  Supplemental and dietary vitamin E, beta-carotene, and vitamin C intakes and prostate cancer risk. , 2006, Journal of the National Cancer Institute.

[62]  Russell L. Jones,et al.  Nitric oxide reduces seed dormancy in Arabidopsis. , 2006, Journal of experimental botany.

[63]  F. J. Corpas,et al.  Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development , 2006, Planta.

[64]  C. Foyer,et al.  Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context , 2005 .

[65]  F. J. Corpas,et al.  Peroxisomal Monodehydroascorbate Reductase. Genomic Clone Characterization and Functional Analysis under Environmental Stress Conditions1 , 2005, Plant Physiology.

[66]  C. Foyer,et al.  Redox Homeostasis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses , 2005, The Plant Cell Online.

[67]  G. Loake,et al.  A central role for S-nitrosothiols in plant disease resistance , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[68]  M. Pedreño,et al.  Nitric oxide production by the differentiating xylem of Zinnia elegans. , 2004, The New phytologist.

[69]  A. Gow,et al.  Biological significance of nitric oxide-mediated protein modifications. , 2004, American journal of physiology. Lung cellular and molecular physiology.

[70]  Julian I Schroeder,et al.  Reactive Oxygen Species Activation of Plant Ca2+ Channels. A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechanotransduction1 , 2004, Plant Physiology.

[71]  C. Bailly Active oxygen species and antioxidants in seed biology , 2004, Seed Science Research.

[72]  Rafael Radi,et al.  Nitric oxide, oxidants, and protein tyrosine nitration , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[73]  C. Bailly,et al.  Catalase activity and expression in developing sunflower seeds as related to drying. , 2004, Journal of experimental botany.

[74]  L. Lamattina,et al.  Nitric oxide plays a central role in determining lateral root development in tomato , 2004, Planta.

[75]  C. García-Mata,et al.  Nitric oxide: the versatility of an extensive signal molecule. , 2003, Annual review of plant biology.

[76]  E. Gwóźdź,et al.  Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus , 2003 .

[77]  E. Titarenko,et al.  The gene encoding glutathione‐dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid , 2003, FEBS letters.

[78]  Jonathan D. G. Jones,et al.  Reactive oxygen species produced by NADPH oxidase regulate plant cell growth , 2003, Nature.

[79]  W. Ullrich,et al.  Generation and possible roles of NO in plant roots and their apoplastic space. , 2002, Journal of experimental botany.

[80]  E. Taleisnik,et al.  Reactive Oxygen Species in the Elongation Zone of Maize Leaves Are Necessary for Leaf Extension1 , 2002, Plant Physiology.

[81]  G. Pagnussat,et al.  Nitric Oxide Is Required for Root Organogenesis1 , 2002, Plant Physiology.

[82]  A. Sakamoto,et al.  Arabidopsis glutathione‐dependent formaldehyde dehydrogenase is an S‐nitrosoglutathione reductase , 2002, FEBS letters.

[83]  M. Marone,et al.  Semiquantitative RT-PCR analysis to assess the expression levels of multiple transcripts from the same sample , 2001, Biological Procedures Online.

[84]  L. Lamattina,et al.  Nitric oxide in plants: the history is just beginning , 2001 .

[85]  Y. Leshem,et al.  Non-invasive photoacoustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria anannasa (Duch.) and avocados Persea americana (Mill.). , 2000, Journal of experimental botany.

[86]  Barroso,et al.  Peroxisomal NADP-Dependent Isocitrate Dehydrogenase. Characterization and Activity Regulation during Natural Senescence. , 1999, Plant physiology.

[87]  F. Cánovas,et al.  Purification and characterization of NADP+-linked isocitrate dehydrogenase from scots pine . Evidence for different physiological roles of the enzyme in primary development , 1998, Plant physiology.

[88]  José,et al.  A dehydrogenase-mediated recycling system of NADPH in plant peroxisomes. , 1998, The Biochemical journal.

[89]  C. Gouvêa,et al.  NO·–releasing substances that induce growth elongation in maize root segments , 1997, Plant Growth Regulation.

[90]  A. Wellburn,et al.  Effects of NO (+ NO2) pollution on growth, nitrate reductase activities and associated protein contents in glasshouse lettuce grown hydroponically in winter with CO2 enrichment , 1996 .

[91]  K. Asada,et al.  Inactivation Mechanism of Ascorbate Peroxidase at Low Concentrations of Ascorbate; Hydrogen Peroxide Decomposes Compound I of Ascorbate Peroxidase , 1996 .

[92]  M. Nishimura,et al.  A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. , 1995, Plant & cell physiology.

[93]  M. Walter,et al.  Primary Metabolism in Plant Defense (Regulation of a Bean Malic Enzyme Gene Promoter in Transgenic Tobacco by Developmental and Environmental Cues) , 1995, Plant physiology.

[94]  K. Asada,et al.  Thylakoid Membrane-Bound, NADPH-Specific Pyridine Nucleotide Dehydrogenase Complex Mediates Cyclic Electron Transport in the Cyanobacterium Synechocystis sp. PCC 6803 , 1995 .

[95]  L. Willmitzer,et al.  Cloning and Expression Analysis of the Cytosolic NADP+-Dependent Isocitrate Dehydrogenase from Potato (Implications for Nitrogen Metabolism) , 1995, Plant physiology.

[96]  E. E. Burns,et al.  Provitamin A and Ascorbic Acid Content of Fresh Pepper Cultivars (Capsicum annuum) and Processed Jalapeños , 1994 .

[97]  D. Higgs,et al.  Vitamin C content of foods: sample variability. , 1991, The American journal of clinical nutrition.

[98]  R. Mittler,et al.  Purification and characterization of pea cytosolic ascorbate peroxidase. , 1991, Plant physiology.

[99]  M. Galleano,et al.  Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. , 1991, Biochimica et biophysica acta.

[100]  R. N. Trelease,et al.  Post-Transcriptional Regulation of Catalase Isozyme Expression in Cotton Seeds. , 1991, The Plant cell.

[101]  R. N. Trelease,et al.  Two temporally synthesized charge subunits interact to form the five isoforms of cottonseed (Gossypium hirsutum) catalase. , 1990, The Biochemical journal.

[102]  M. Redinbaugh,et al.  The distribution of catalase activity, isozyme protein, and transcript in the tissues of the developing maize seedling. , 1990, Plant physiology.

[103]  J. Jacquot,et al.  Purification and comparative properties of the cytosolic isocitrate dehydrogenases (NADP) from pea (Pisum sativum) roots and green leaves. , 1988, European journal of biochemistry.

[104]  K. Asada,et al.  Inactivation of Ascorbate Peroxidase in Spinach Chloroplasts on Dark Addition of Hydrogen Peroxide : Its Protection by Ascorbate , 1984 .

[105]  T. Mansfield,et al.  The effects of nitric oxide pollution on the growth of tomato , 1979 .

[106]  L. Schrader,et al.  Low Temperature Effects on Soybean (Glycine max [L.] Merr. cv. Wells) Mitochondrial Respiration and Several Dehydrogenases during Imbibition and Germination. , 1977, Plant physiology.

[107]  F. J. Corpas,et al.  Nitration and S-Nitrosylation: Two Post-translational Modifications (PTMs) Mediated by Reactive Nitrogen Species (RNS) and Their Role in Signalling Processes of Plant Cells , 2015 .

[108]  F. J. Corpas,et al.  Peroxynitrite (ONOO-) is endogenously produced in arabidopsis peroxisomes and is overproduced under cadmium stress. , 2014, Annals of botany.

[109]  D. Gallie The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. , 2013, Journal of experimental botany.

[110]  M. Iwaya-Inoue,et al.  Regulation of soybean seed germination through ethylene production in response to reactive oxygen species. , 2013, Annals of botany.

[111]  Área de Bioquímica,et al.  Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation , 2013 .

[112]  P. Mullineaux,et al.  Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.) , 2004, Planta.

[113]  J. Schroeder,et al.  Update on Reactive Oxygen Species Activation of Ca 2 1 Channels Reactive Oxygen Species Activation of Plant Ca 2 1 Channels . A Signaling Mechanism in Polar Growth , Hormone Transduction , Stress Signaling , and Hypothetically Mechanotransduction 1 , 2004 .

[114]  K. Asada,et al.  Generation of superoxide anion and localization of CuZn-superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignification. , 1997, Plant & cell physiology.

[115]  Y. Leshem,et al.  The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage , 1996 .

[116]  F. J. Corpas,et al.  Kinetic properties of hexose-monophosphate dehydrogenases. I. Isolation and partial purification of glucose-6-phosphate dehydrogenase from rat liver and kidney cortex. , 1995, Life sciences.

[117]  S. Gálvez,et al.  On the function of the NADP-dependent isocitrate dehydrogenase isoenzymes in living organisms , 1995 .

[118]  H. Aebi,et al.  Catalase in vitro. , 1984, Methods in enzymology.

[119]  S. Hendricks,et al.  Breaking of seed dormancy by catalase inhibition. , 1975, Proceedings of the National Academy of Sciences of the United States of America.