Exogenous Nitro-Oleic Acid inhibits primary root growth by reducing the mitosis in the meristem in Arabidopsis thaliana

Nitric oxide (NO) is a second messenger that regulates a broad range of physiological processes in plants. NO-derived molecules called reactive nitrogen species (RNS) can react with unsaturated fatty acids generating nitrated fatty acids (NO2-FA). NO2-FA work as signaling molecules in mammals where production and targets have been described under different stress conditions. Recently, NO2-FAs were detected in plants, however their role(s) on plant physiological processes is still poorly known. Here we show that exogenous application of nitro-oleic acid (NO2-OA) inhibits Arabidopsis primary root growth; this inhibition is not likely due to nitric oxide (NO) production or impaired auxin or cytokinin root responses. Deep analyses showed that roots incubated with NO2-OA had a lower cell number in the division area. Although this NO2-FA did not affect the signaling mechanisms maintaining the stem cell niche, plants incubated with NO2-OA showed a reduction of cell division in the meristematic area. Therefore, this work shows that NO2-OA inhibits mitotic processes subsequently reducing primary root growth.

[1]  N. Kúsz,et al.  Nitro-Oleic Acid in Seeds and Differently Developed Seedlings of Brassica napus L. , 2020, Plants.

[2]  C. García-Mata,et al.  Nitro-oleic acid triggers ROS production via NADPH oxidase activation in plants: A pharmacological approach. , 2020, Journal of plant physiology.

[3]  J. B. Barroso,et al.  Post-Translational Modification of Proteins Mediated by Nitro-Fatty Acids in Plants: Nitroalkylation , 2019, Plants.

[4]  Xiaofeng Wang,et al.  Hydrogen Sulfide Disturbs Actin Polymerization via S-Sulfhydration Resulting in Stunted Root Hair Growth1 , 2018, Plant Physiology.

[5]  Elke Barbez,et al.  PILS6 is a temperature-sensitive regulator of nuclear auxin input and organ growth in Arabidopsis thaliana , 2018, Proceedings of the National Academy of Sciences.

[6]  B. Müller,et al.  Plant development regulated by cytokinin sinks , 2016, Science.

[7]  F. J. Corpas,et al.  Nitro-linolenic acid is a nitric oxide donor. , 2016, Nitric oxide : biology and chemistry.

[8]  F. J. Corpas,et al.  Nitric oxide release from nitro-fatty acids in Arabidopsis roots , 2016, Plant signaling & behavior.

[9]  F. J. Corpas,et al.  Nitro-fatty acids in plant signaling: nitro-linolenic acid induces the molecular 1 chaperone network in Arabidopsis 2 , 2015 .

[10]  Daniel R. Lewis,et al.  Nitric Oxide Plays a Role in Stem Cell Niche Homeostasis through Its Interaction with Auxin1[W][OPEN] , 2014, Plant Physiology.

[11]  Jarkko Salojärvi,et al.  PLETHORA gradient formation mechanism separates auxin responses , 2014, Nature.

[12]  L. De Veylder,et al.  A quiescent path to plant longevity. , 2014, Trends in cell biology.

[13]  B. Freeman,et al.  Olives and Olive Oil Are Sources of Electrophilic Fatty Acid Nitroalkenes , 2014, PloS one.

[14]  Stacy L. Gelhaus,et al.  Nitrated fatty acids: synthesis and measurement. , 2013, Free radical biology & medicine.

[15]  Philip N Benfey,et al.  Control of Arabidopsis root development. , 2012, Annual review of plant biology.

[16]  O. Lorenzo,et al.  Nitric-oxide , 2012, Reactions Weekly.

[17]  Tom Beeckman,et al.  A novel sensor to map auxin response and distribution at high spatio-temporal resolution , 2012, Nature.

[18]  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.

[19]  B. Freeman,et al.  Formation and signaling actions of electrophilic lipids. , 2011, Chemical reviews.

[20]  B. Freeman,et al.  Gas-Phase Fragmentation Analysis of Nitro-Fatty Acids , 2011, Journal of the American Society for Mass Spectrometry.

[21]  C. Carlberg,et al.  Electrophilic Nitro-fatty Acids Activate NRF2 by a KEAP1 Cysteine 151-independent Mechanism* , 2011, Journal of Biological Chemistry.

[22]  M. P. Cole,et al.  Nitro–Fatty Acids Reduce Atherosclerosis in Apolipoprotein E–Deficient Mice , 2010, Arteriosclerosis, thrombosis, and vascular biology.

[23]  G. Jürgens,et al.  Survival of the flexible: hormonal growth control and adaptation in plant development , 2009, Nature Reviews Genetics.

[24]  B. Scheres,et al.  Members of the GCN5 Histone Acetyltransferase Complex Regulate PLETHORA-Mediated Root Stem Cell Niche Maintenance and Transit Amplifying Cell Proliferation in Arabidopsis[W] , 2009, The Plant Cell Online.

[25]  Eva Benková,et al.  Hormone interactions at the root apical meristem , 2009, Plant Molecular Biology.

[26]  Takashi Aoyama,et al.  A Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem , 2008, Science.

[27]  R. Radi,et al.  Protein and lipid nitration: role in redox signaling and injury. , 2008, Biochimica et biophysica acta.

[28]  Y. E. Chen,et al.  Molecular recognition of nitrated fatty acids by PPARγ , 2008, Nature Structural &Molecular Biology.

[29]  B. Freeman,et al.  Nitro-fatty Acid Formation and Signaling* , 2008, Journal of Biological Chemistry.

[30]  H. Rubbo,et al.  Nitrated fatty acids: mechanisms of formation, chemical characterization, and biological properties. , 2008, Free radical biology & medicine.

[31]  Renze Heidstra,et al.  PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development , 2007, Nature.

[32]  P. Hogeweg,et al.  Auxin transport is sufficient to generate a maximum and gradient guiding root growth , 2007, Nature.

[33]  B. Freeman,et al.  Nitro-fatty Acid Reaction with Glutathione and Cysteine , 2007, Journal of Biological Chemistry.

[34]  Ben Scheres,et al.  Stem-cell niches: nursery rhymes across kingdoms , 2007, Nature Reviews Molecular Cell Biology.

[35]  Renze Heidstra,et al.  Cytokinins Determine Arabidopsis Root-Meristem Size by Controlling Cell Differentiation , 2007, Current Biology.

[36]  M. Lenhard,et al.  Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers , 2007, Nature.

[37]  Jifeng Zhang,et al.  Nitrated Fatty Acids: Endogenous Anti-inflammatory Signaling Mediators* , 2006, Journal of Biological Chemistry.

[38]  B. Freeman,et al.  Reversible Post-translational Modification of Proteins by Nitrated Fatty Acids in Vivo* , 2006, Journal of Biological Chemistry.

[39]  Michael Sauer,et al.  A Molecular Framework for Plant Regeneration , 2006, Science.

[40]  J. Polacco,et al.  Nitric Oxide Functions as a Positive Regulator of Root Hair Development , 2006, Plant signaling & behavior.

[41]  Ding Chen,et al.  Cloning and Functional Characterization of a Formin-Like Protein (AtFH8) from Arabidopsis1 , 2005, Plant Physiology.

[42]  R. Amasino,et al.  The PLETHORA Genes Mediate Patterning of the Arabidopsis Root Stem Cell Niche , 2004, Cell.

[43]  B. Freeman,et al.  Red cell membrane and plasma linoleic acid nitration products: synthesis, clinical identification, and quantitation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  G. Pagnussat,et al.  Nitric Oxide Mediates the Indole Acetic Acid Induction Activation of a Mitogen-Activated Protein Kinase Cascade Involved in Adventitious Root Development1 , 2004, Plant Physiology.

[45]  S. Sabatini,et al.  SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. , 2003, Genes & development.

[46]  R. Meagher,et al.  Both Vegetative and Reproductive Actin Isovariants Complement the Stunted Root Hair Phenotype of the Arabidopsisact2-1 Mutation1 , 2002, Plant Physiology.

[47]  D. Inzé,et al.  Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana , 2000, Planta.

[48]  P. Doerner,et al.  Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. , 1999, The Plant journal : for cell and molecular biology.

[49]  Claudia van den Berg,et al.  Short-range control of cell differentiation in the Arabidopsis root meristem , 1997, Nature.

[50]  G. Hagen,et al.  Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. , 1997, The Plant cell.

[51]  D. Inzé,et al.  Developmental expression of the arabidopsis cyclin gene cyc1At. , 1994, The Plant cell.

[52]  S. Barnes,et al.  Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. , 1994, The Journal of biological chemistry.

[53]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

[54]  H. Spencer Origin of Classes among the “Parasol” Ants , 1894, Nature.

[55]  J. Palatnik,et al.  Analysis of Expression Gradients of Developmental Regulators in Arabidopsis thaliana Roots. , 2018, Methods in molecular biology.

[56]  E. Feraru,et al.  Histochemical Staining of β-Glucuronidase and Its Spatial Quantification. , 2017, Methods in molecular biology.

[57]  S. Sabatini,et al.  Analysis of root meristem size development. , 2010, Methods in molecular biology.

[58]  Tatsuo Kakimoto,et al.  Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. , 2004, The Plant journal : for cell and molecular biology.

[59]  B. Scheres,et al.  Analysis of Root Development in Arabidopsis Thaliana , 1994 .

[60]  F. Warner Analysis of expression. , 1885 .