Polyamine Oxidases Play Various Roles in Plant Development and Abiotic Stress Tolerance

Abstract

Polyamines not only play roles in plant growth and development, but also adapt to environmental stresses. Polyamines can be oxidized by copper-containing diamine oxidases (CuAOs) and flavin-containing polyamine oxidases (PAOs). Two types of PAOs exist in the plant kingdom; one type catalyzes the back conversion (BC-type) pathway and the other catalyzes the terminal catabolism (TC-type) pathway. The catabolic features and biological functions of plant PAOs have been investigated in various plants in the past years. In this review, we focus on the advance of PAO studies in rice, Arabidopsis, and tomato, and other plant species.

Keywords: back conversion pathway; polyamine catabolism; polyamine oxidase; polyamines; stress response; terminal catabolism pathway.

Figure 1

Polyamine biosynthesis pathway in Arabidopsis thaliana. ADC, arginine decarboxylase; AIH, agmatine iminohydrolase; CPA, N-carbamoylputrescine amidohydrolase; SPDS, Spd synthase; SPMS, Spm synthase; ACL5, ACAULIS5, T-Spm synthase; SAM, S-adenosylmethionine; SAMDC, S-adenosylmethionine decarboxylase; dcSAM, decarboxylated S-adenosylmethionine; ACC, 1-amino-cyclopropane-1-carboxylic-acid.

Figure 2

Phylogenetic relationship of polyamine oxidases (PAOs) among rice, Arabidopsis, tomato, and other plants. The neighbor-joining tree was constructed by amino acid sequence alignment using Clustal X 1.83 and MEGA 5.0. The bootstrap values, displayed at the branch nodes, were obtained with 1000 repetitions. Roman numerals (I~V) indicate clade numbers. The analyzed genes and their accession numbers are listed in Table 1. Os, Oryza sativa; At, Arabidopsis thaliana; Sl, Solanum lycopersicum; Bd, Brachypodium distachyon; Br, Solanum lycopersicum; Cs, Citrus sinensis; Sm, Selaginella moellendorffii; Vv, Vitis vinifera; Md, Malus domestica; Sel, Selaginella lepidophylla; Zm, Zea mays; Hv, Hordeum vulgare; Pp, Physcomitrella patens; Rc, Ricinus communis; Nt, Nicotiana tabacum; Bj, Brassica juncea; Pt, Populus trichocarpa; Sb, Sorghum bicolor; Gm, Glycine max PAO1-like; Mt, Medicago truncatula; Ah, Amaranthus hypochondriacus; Gh, Gossypium hirsutum; Syn, Synechocystis.

Figure 3

Alignment of amino acid sequences of twenty reported peroxisomal PAOs from Oryza sativa, Arabidopsis thaliana, Solanum lycopersicum, Brachypodium distachyon, Brassica rapa, Citrus sinensis, and Malus domestica. The alignment was performed by the Clustal X 1.83 software and exhibited by the Boxshade program (http://www.ch.embnet.org/software/BOX_form.html.). Black and gray indicate the complete and partial homology of the amino acid sequences, respectively. The percentages at the end of the alignment showed the identity between OsPAO3 and other PAOs.

Figure 4

Predicted tertiary structures of the reported peroxisomal PAOs. Twenty have been reported; peroxisomal plant PAOs were analyzed. (A–J), The protein 3-D structures of OsPAO3 (A); OsPAO4 (B); OsPAO5 (C); AtPAO2 (D); AtPAO3 (E); AtPAO5 (F); SlPAO2 (G); SlPAO3 (H); SlPAO4 (I); SlPAO5 (J); BdPAO2 (K); BdPAO4 (L); BrPAO2 (M); BrPAO3 (N); BrPAO4 (O); CsPAO2 (P); CsPAO3 (Q); MdPAO2 (R); MdPAO3 (S); and MdPAO4 (T) were obtained using the Protein Structure Prediction Server program (http://ps2v3.life.nctu.edu.tw/) and Chimera 1.13 software. (U) Merged image of all PAOs, except OsPAO4 and CsPAO2, was performed by Chimera 1.13 software. (V) Merged image of OsPAO4 and CsPAO2 was similarly performed. The light blue and light yellow colors indicate the protein structures of OsPAO4 and CsPAO2, respectively. (W) Evolution relationship among the peroxisomal PAOs.

Figure 5

Diagrammatic representation of the roles of PAO involved in developmental growth and environmental stress response in plants. The thick upright arrows indicate increase in the activity or concentrations. The cartoon pictures of smiling and bitter faces indicate the plant growth under normal or stress conditions, respectively. ROS: reactive oxygen species.