Plant Peroxisomes and Glyoxysomes

Peroxisomes and glyoxysomes are membrane enclosures containing enzymes that participate in photorespiration in leaves, nitrogen metabolism in root nodules and fat conversions in seeds. Oxidases in these organelles circumvent energy conservation by producing hydrogen peroxide, which is detoxified by catalase in the matrix and ascorbate peroxidase in the membrane. Some hydrogen peroxide may oxidize proteins within the organelles or function as a signalling molecule. Processes in these organelles also produce hormones (jasmonic acid, indole acetic acid). Peroxisomal proteins are brought in from the cytosol by peroxisomal targeting sequences (PTS). The recognition of the PTS and translocation into the organelles are processes conducted by Peroxins. Genomic and proteomic analyses have recently revealed that plant peroxisomes and glyoxysomes can contain over a 100 different protein molecules, many having unknown functions.

Keywords: microbodies; hydrogen peroxide; photorespiration; glyoxylate cycle; fatty acid oxidation; peroxisomal-targeting sequence

Figure 1. A leaf-type peroxisome in an oat coleoptile. The crystal, probably catalase, within the peroxisome is typical of leaf peroxisomes. Reproduced and modified, with permission, from Vigil (1973).
Figure 2. -Oxidation and glyoxylate cycle enzymes in glyoxysomes. The -oxidation enzymes are acyl–CoA oxidase (AO), enoyl–CoA hydratase combined with 3-hydroxy acyl–CoA dehydrogenase in the bifunctional protein (BP) and 3-ketoacyl–CoA thiolase (TH). Glyoxylate-cycle enzymes are isocitrate lyase (IL) and malate synthase (MS), citrate synthase (CS), aconitase (AC) and malate dehydrogenase (MD). Membrane enzymes include ascorbate peroxidase (AP) and ascorbate free radical reductase (AR). Both catalase (CAT) and AP consume hydrogen peroxide. Asc, ascorbate; Asc; ascorbate free radical.
Figure 3. Metal-catalysed oxidation of ICL and CAT detected using both dinitrophyenyl hydrazine (DNP) derivatization and biotinylation. (A1) Samples (17 g of castor bean glyoxysomal protein) were treated with DNP and detected with anti-DNP antibody. (A2) The same nitrocellulose membrane was stripped with 3 M guanidine thiocyanate, reprobed with ICL and CAT antibodies one at a time. (B1) Biotinylated samples (1 g of protein) were detected with avidin-HRP. (B2) The same membrane was reprobed with ICL and CAT antibodies after stripping with 3 M guanidine thiocyanate. Lane 1, control sample not incubated with 100 M CuCl2/4 mM ascorbate; lane 2, sample incubated with 100 M CuCl2/4 mM ascorbate for 30 min and lane 3, sample incubated with 100 M CuCl2/4 mM ascorbate for 1 h. Kwak and Donaldson (unpublished).
close
 References
    Bunkelmann JR and Trelease RN (1996) Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes. Plant Physiology 110: 589–598.
    Cooper TJ and Beevers H (1969a) Mitochondria and glyoxysomes from castor bean endosperm. Enzyme constitutents and catalytic capacity. Journal of Biological Chemistry 244: 3507–3513.
    Cooper TJ and Beevers H (1969b) Beta-oxidation in glyoxysomes from castor bean endosperm. Journal of Biological Chemistry 244: 3514–3520.
    Corpas FJ, Barroso JB, Carreras A et al. (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiology 136(1): 2722–2733.
    book Donaldson RP (1987) "Transfer of reducing equivalents (electrons) through the glyoxysomal membrane during -oxidation, glyoxylate cycle, and the conversion of triglyceride to hexose". In: Newman DW and Wilson KG (eds) Models in Plant Biochemistry and Physiology. Boca Raton: CRC Press.
    Gietl C, Faber KN, van der Klei IJ and Veenhuis M (1994) Mutational analysis of the N-terminal topogenic signal of watermelon glyoxysomal malate dehydrogenase using the heterologous host Hansenula polymorpha. Proceedings of the National Academy of Sciences of the USA 91: 3151–3155.
    Hanks JF, Tolbert NE and Schubert KR (1981) Localization of enzymes of ureide bisynthesis in peroxisomes and microsomes of nodules. Plant Physiology 68: 65–69.
    Hänsch R, Lang C, Riebeseel E et al. (2006) Plant sulfite oxidase as novel producer of H2O2: combination of enzyme catalysis with a subsequent non-enzymatic reaction step. Journal of Biological Chemistry 281(10): 6884–6888.
    Hayashi M, Yagi M, Nito K, Kamada T and Nishimura M (2005) Differential contribution of two peroxisomal protein receptors to the maintenance of peroxisomal functions in Arabidopsis. Journal of Biological Chemistry 280(15): 14829–14835
    book Heinze M and Gerhardt B (2002) "Plant catalases". In: Baker A and Graham IA (eds) Plant Peroxisomes: Biochemistry, Cell Biology and Biotechnological Applications. London: Kluwer Academic Publishers.
    Ishikawa T, Yoshimura K, Sakai K et al. (1998) Molecular characterization and physiological role of a glyoxysome-bound ascorbate peroxidase from spinach. Plant Cell Physiology 39(1): 23–34.
    Jedd G and Chua N-H (2002) Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant and Cell Physiology 43(4): 384–392.
    Karyotou K and Donaldson RP (2005) Ascorbate peroxidase, a scavenger of hydrogen peroxide in glyoxysomal membranes. Archives of Biochemistry and Biophysics 434: 248–257.
    Koo AJK, Chung HS, Kobayashi Y et al. (2006) Identification of a peroxisomal acyl-activating enzyme involved in the biosynthesis of jasmonic acid in Arabidopsis. Journal of Biological Chemistry 281(44): 33511–33520.
    Muench DG and Mullen RT (2003) Peroxisome dynamics in plant cells: a role for the cytoskeleton. Plant Science 164(3): 307–315.
    Mullen RT, Lee MS, Flynn CR and Trelease RN (1997a) Diverse amino acid residues function within the type 1 peroxisomal targeting signal. Implications for the role of accessory residues upstream of the type 1 peroxisomal targeting signal. Plant Physiology 115(3): 881–889.
    Mullen RT, Lee MS and Trelease RN (1997b) Identification of the peroxisomal targeting signal for cottonseed catalase. Plant Journal 12(2): 313–322.
    Mullen RT and Trelease RN (2006) The ER-peroxisome connection in plants: development of the “ER semi-autonomous peroxisome maturation and replication” model for plant peroxisome biogenesis. Biochimica et Biophysica Acta 1763(12): 1655–1668.
    Nguyen AT and Donaldson RP (2005) Metal-catalyzed oxidation induces carbonylation of peroxisomal proteins and loss of enzymatic activities. Archives of Biochemistry and Biophysics 439(1): 25–31.
    Nito K, Kamigaki A, Kondo M, Hayashi M and Nishimura M (2007) Functional classification of Arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants. Plant and Cell Physiology 48(6): 763–774.
    Orr CWM (1967) Studies on ascorbic acid. I. Factors influencing the ascorbate-mediated inhibition of catalase. Biochemistry 6(10): 2995–2999.
    Orth T, Reumann S, Zhang X et al. (2007) The PEROXIN11 protein family controls peroxisome proliferation in Arabidopsis. Plant Cell 19: 333–350.
    Peremyslov VV, Prokhnevsky AI, Avisar D and Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis thaliana. Plant Physiolology 146(3): 1109–1116.
    Reumann S, Babujee L, Ma CL et al. (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19(10): 3170–3193.
    Reumann S, Ma C, Lemke S and Babujee L (2004) AraPerox: a database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiology 136: 2587–2608.
    Reumann S, Maier E, Heldt HW and Benz R (1998) Permeability properties of the porin of spinach leaf peroxisomes. European Journal of Biochemistry 251(1–2): 359–366.
    del Río LA, Sandalio LM, Corpas FJ, Palma JM and Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiology 141: 330–335.
    del Río LA, Sandalio LM, Palma JM, Bueno P and Corpas FJ (1992) Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Radical Biology and Medicine 13: 557–580.
    Schilmiller AL, Koo AJ and Howe GA (2007) Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiology 143(2): 812–824.
    Schumann U, Prestele J, O'Geen H et al. (2007) Requirement of the C3HC4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts. Proceedings of the National Academy of Sciences of the USA 104: 1069–1074.
    Sparkes IA, Hawes C and Baker A (2005) AtPEX2 and AtPEX10 are targeted to peroxisomes independently of known endoplasmic reticulum trafficking routes. Plant Physiology 139: 690–700.
    Tolbert NE (1981) Metabolic pathways in peroxisomes and glyoxysomes. Annual Review of Biochemistry 50: 133–157.
    Vigil EL (1973) Plant microbodies. Journal of Histochemistry and Cytochemistry 21(11): 958–962.
    Wang GE, Conover RC, Benoit S et al. (2004) Role of a bacterial organic hydroperoxide detoxification system in preventing catalase inactivation. Journal of Biological Chemistry 279(50): 51908–51914.
    Wolins NE and Donaldson RP (1994) Specific binding of the peroxisomal protein targeting sequence to glyoxysomal membranes. Journal of Biological Chemistry 269(2): 1149–1153.
    Wolins NE and Donaldson RP (1997) Binding of the peroxisomal targeting sequence SKL is specified by a low-affinity site in castor bean glyoxysomal membranes. A domain next to the SKL binds to a high-affinity site. Plant Physiology 113(3): 943–949.
    Woodward AW and Bartel B (2005) The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Molecular Biology of the Cell 16(2): 573–583.
    Yamazaki RK and Tolbert NE (1970) Enzymic characterization of leaf peroxisomes. Journal of Biological Chemistry 245: 5137–5144.
    Yanik T and Donaldson RP (2005) A protective association between catalase and isocitrate lyase in peroxisomes. Archives of Biochemistry and Biophysics 435(2): 243–252.
    Zolman BK and Bartel B (2004) An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. Proceedings of the National Academy of Science of the USA 101(6): 1786–1791.
    Zolman BK, Monroe-Augustus M, Silva ID and Bartel B (2005) Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22. Plant Cell 7(12): 3422–3435.
    Zolman BK, Nyberg M and Bartel B (2007) IBR3, a novel peroxisomal acyl-CoA dehydrogenase-like protein required for indole-3-butyric acid response. Plant Molecular Biology 64(1–2): 59–72.
 Further Reading
    book Baker A and Graham IA (2002) Plant Peroxisomes: Biochemistry, Cell Biology and Biotechnological Applications. London: Kluwer Academic Publishers.
    Nishimura M, Hayashi M, Kato A, Yamaguchi K and Mano S (1996) Functional transformation of microbodies in higher plant cells. Cell Structure and Function 21(5): 387–393.
    Nyathi Y and Baker A (2006) Plant peroxisomes as a source of signalling molecules. Biochimica et Biophysica Acta 1763(12): 1478–1495.
    Olsen LJ and Harada JJ (1995) Peroxisomes and their assembly in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 46: 123–146.
    Tolbert NE and Essner E (1981) Peroxisomes and glyoxysomes. Journal of Cell Biology 91: 271s–283s.
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Donaldson, Robert Paul, Kwak, Yoon, Yanik, Tulin, and Sharma, Vishakha(Dec 2008) Plant Peroxisomes and Glyoxysomes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001677.pub2]