Nitric Oxide (NO) Scaffolds the Peroxisomal Protein–Protein Interaction Network in Higher Plants
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International Journal of Molecular Sciences Review Nitric Oxide (NO) Scaffolds the Peroxisomal Protein–Protein Interaction Network in Higher Plants Francisco J. Corpas * , Salvador González-Gordo and José M. Palma Antioxidant, Free Radical and Nitric Oxide in Biotechnology, Food and Agriculture Group, Department of Biochemistry, Cell and Molecular Biology of Plants, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), C/ Profesor Albareda, 1, E-18008 Granada, Spain; [email protected] (S.G.-G.); [email protected] (J.M.P.) * Correspondence: [email protected] Abstract: The peroxisome is a single-membrane subcellular compartment present in almost all eukaryotic cells from simple protists and fungi to complex organisms such as higher plants and animals. Historically, the name of the peroxisome came from a subcellular structure that contained high levels of hydrogen peroxide (H2O2) and the antioxidant enzyme catalase, which indicated that this organelle had basically an oxidative metabolism. During the last 20 years, it has been shown that plant peroxisomes also contain nitric oxide (NO), a radical molecule than leads to a family of derived molecules designated as reactive nitrogen species (RNS). These reactive species can mediate post-translational modifications (PTMs) of proteins, such as S-nitrosation and tyrosine nitration, thus affecting their function. This review aims to provide a comprehensive overview of how NO could affect peroxisomal metabolism and its internal protein-protein interactions (PPIs). Remarkably, many of the identified NO-target proteins in plant peroxisomes are involved in the metabolism of reactive oxygen species (ROS), either in its generation or its scavenging. Therefore, Citation: Corpas, F.J.; González- it is proposed that NO is a molecule with signaling properties with the capacity to modulate the Gordo, S.; Palma, J.M. Nitric Oxide peroxisomal protein-protein network and consequently the peroxisomal functions, especially under (NO) Scaffolds the Peroxisomal adverse environmental conditions. Protein–Protein Interaction Network in Higher Plants. Int. J. Mol. Sci. 2021, Keywords: antioxidant; catalase; nitric oxide; peroxisome; reactive nitrogen species; S-nitrosation; 22, 2444. https://doi.org/10.3390/ tyrosine nitration ijms22052444 Academic Editor: Sławomir Borek 1. Overview of the Diversity of Peroxisomes in Eukaryotic Cells Received: 3 February 2021 Accepted: 25 February 2021 Peroxisomes are single-membrane subcellular organelles that appear in almost all Published: 28 February 2021 eukaryotic cells of the four kingdoms including protists, fungi, plants and animals [1–6]. The first structural identification of these organelles was done by electron microscope Publisher’s Note: MDPI stays neutral analyses in mouse kidney cells [7]. Years later, those new structures were isolated and with regard to jurisdictional claims in biochemically characterized in rat liver being recognized as a new cellular compartment published maps and institutional affil- having a prominent hydrogen peroxide (H2O2) metabolism [8,9]. From that time, studies iations. on peroxisomes were gradually extended to other organisms [1,10–18]. Figure1 shows some representative species, belonging to each kingdom, where peroxisomes have been studied, and Table1 displays various examples of the diversity of functions exerted by peroxisomes depending on the organism. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Int. J. Mol. Sci. 2021, 22, 2444. https://doi.org/10.3390/ijms22052444 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 2444 2 of 14 Int. J. Mol. Sci. 2021, 22, 2444 2 of 14 Figure 1. Peroxisomes are single-membrane subcellular organelles that appear in almost all eukary- otic cells from the four kingdoms: protists, fungi, plants and animals. Figure 1. Peroxisomes are single-membrane subcellular organelles that appear in almost all eu- karyoticTable 1. Diversitycells from ofthe functions four kingdoms: exerted protists, by peroxisomes fungi, plants depending and animals. on the organism. Organism/Organ (Species) Peroxisomal Function Ref. Free-living marine diplonemidTable 1. DiversityPeroxisome of functions undergoes exerted by remodeling peroxisomes metabolism depending involving on the organism. the housing [19] (Diplonema papillatum) gluconeogenesis Organism/Organ (Species) Peroxisomal Function Ref. Ascomycete (Sclerotinia sclerotiorum) Peroxisome is involved in the fungi sexual development [20] Free-living marine diplone- Peroxisome undergoes remodeling metabolism involving the [19] Fungusmid (Diplonema (Alternaria papillatum alternate)) housing Peroxisome gluconeogenesis of the fungus is necessary for its pathogenesis in citrus [21] Ascomycete (Sclerotinia sclero- Peroxisomal malate dehydrogenase 2 connects lipid catabolism to Chlamydomonas Peroxisome is involved in the fungi sexual development [20] [22,23] tiorum) photosynthesis FungusPea leaves (Alternaria (Pisum sativum alternate)) Peroxisome Peroxisomes of the involvefungus is in nece leaf senescencessary for its pathogenesis in cit- [21] [24,25] ChlamydomonasLeaf tomato (Solanum lycopersicum)Peroxisomal Peroxisomes malate involve dehydrogenase in pathogen 2 connects defence lipid catabolism to [22,23] [26,27] photosynthesis Peroxisomal NADP-isocitrate dehydrogenase is required for stomatal PeaLeaves leaves (Arabidopsis (Pisum thalianasativum)) PeroxisomesmovementPeroxisomal involve in leaf senescence trehalose-6-phosphate phosphatase I is essential[24,25] for [28,29] flowering and development Leaf tomato (Solanum lycoper- Peroxisomes involve in pathogen defence [26,27] sicum) Peroxisomal and chloroplastic chorismate synthase, involved in shikimate Petunia (Petunia hybrida) [30] Leaves (Arabidopsis thaliana) Peroxisomalpathway, NADP-isocitrate are need for flower dehy developmentdrogenase is required for sto- [28,29] Mussels (Mytilus edulis)matal Peroxisomemovement proliferation in response to environmental pollutants [31] Peroxisomal trehalose-6-phosphate phosphatase I is essential for Impaired of peroxisomal fat oxidation induces hepatic lipid accumulation and Nile tilapia (Oreochromis niloticus) flowering and development [32] oxidative damage Petunia (Petunia hybrida) Peroxisomal and chloroplastic chorismate synthase, involved in [30] Rat liver (Rattus norvegicus)shikimate Peroxisomes pathway, participate are need for in theflower metabolism development of xenobiotic acyl compounds [33] Mussels (Mytilus edulis) PeroxisomeDefects proliferation in genes encoding in respon peroxisomalse to environmental proteins lead pollutants to a variety [31] of human Human (Homo sapiens) diseases. For example, X-linked adrenoleukodystrophy, acatalasemia, [34–38] Nile tilapia Impairedcerebro-hepato-renal of peroxisomal fat syndrome, oxidation etc.Host induces defense hepatic lipid ac- [32] (Oreochromis niloticus) cumulation and oxidative damage Rat liver PeroxisomesAt the morphological participate level,in the such metabolism as it has of been xenobiotic mentioned, acyl peroxisomes[33] seem to have (Rattus norvegicus) a verycompounds basic structure because they have a single lipid bilayer membrane that engulfs an amorphous matrix which sometimes has protein crystals. Figure2 shows the visualization Int. J. Mol. Sci. 2021, 22, 2444 3 of 14 Human Defects in genes encoding peroxisomal proteins lead to a variety [34–38] of human diseases. For example, X-linked adrenoleukodystrophy, (Homo sapiens) acatalasemia, cerebro-hepato-renal syndrome, etc. Host defense At the morphological level, such as it has been mentioned, peroxisomes seem to Int. J. Mol. Sci. 2021, 22, 2444 have a very basic structure because they have a single lipid bilayer membrane that3 en- of 14 gulfs an amorphous matrix which sometimes has protein crystals. Figure 2 shows the visualization of leaf peroxisomes from different plant species including transgenic Ara- bidopsis thaliana expressing cyan fluorescent protein (CFP) through the addition of pe- of leaf peroxisomes from different plant species including transgenic Arabidopsis thaliana roxisomal targeting signal 1 (PTS1), thus using a confocal scanning laser microscope expressing cyan fluorescent protein (CFP) through the addition of peroxisomal targeting (CLSM) peroxisomes appear as fluorescence punctuates (Figure 2a); in Cakile maritima signal 1 (PTS1), thus using a confocal scanning laser microscope (CLSM) peroxisomes using a transmission electron microscope (TEM) where the peroxisome is close to chlo- appear as fluorescence punctuates (Figure2a); in Cakile maritima using a transmission roplast and mitochondrion (Figure 2b); and in pea (Pisum sativum L.) leaf peroxisome electron microscope (TEM) where the peroxisome is close to chloroplast and mitochondrion housing the NADP-isocitrate dehydrogenase (NADP-ICDH) detected by its immuno- (Figure2b); and in pea ( Pisum sativum L.) leaf peroxisome housing the NADP-isocitrate localization by TEM (Figure 2c). Nevertheless, research on peroxisome morphology and dehydrogenase (NADP-ICDH) detected by its immunolocalization by TEM (Figure2c). biogenesisNevertheless, is a very research active on research peroxisome area morphology [39–42]. Thus, and a biogenesisrecent report, is a using very active Arabidopsis research seedlings,area [39– 42suggests]. Thus, the