Polyamines: Molecules with Regulatory Functions in Plant Abiotic Stress Tolerance
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Planta (2010) 231:1237–1249 DOI 10.1007/s00425-010-1130-0 REVIEW Polyamines: molecules with regulatory functions in plant abiotic stress tolerance Rubén Alcázar · Teresa Altabella · Francisco Marco · Cristina Bortolotti · Matthieu Reymond · Csaba Koncz · Pedro Carrasco · Antonio F. Tiburcio Received: 2 December 2009 / Accepted: 18 February 2010 / Published online: 11 March 2010 © Springer-Verlag 2010 Abstract Early studies on plant polyamine research mechanisms of their action in abiotic stress tolerance. pointed to their involvement in responses to diVerent envi- Recent advances in the cross talk between polyamines and ronmental stresses. During the last few years, genetic, tran- abscisic acid are discussed and integrated with processes of scriptomic and metabolomic approaches have unravelled reactive oxygen species (ROS) signalling, generation of key functions of diVerent polyamines in the regulation of nitric oxide, modulation of ion channel activities and Ca2+ abiotic stress tolerance. Nevertheless, the precise molecular homeostasis, amongst others. mechanism(s) by which polyamines control plant responses to stress stimuli are largely unknown. Recent studies indi- Keywords Polyamine metabolism · Abiotic stress · Plant cate that polyamine signalling is involved in direct interac- tolerance · Abscisic acid · Signalling tions with diVerent metabolic routes and intricate hormonal cross-talks. Here we discuss the integration of polyamines Abbreviations with other metabolic pathways by focusing on molecular ABA Abscisic acid ACC Amino cyclopropane carboxylic acid ACL5 Acaulis5 ADC Arginine decarboxylase This review is dedicated to the memory of Prof. Arthur W. Galston AIH Agmatine iminohydrolase (Yale University, New Haven, CT, USA) for his pioneering work and CPA N-Carbamoyl putrescine amidohydrolase important contribution to the plant polyamine Weld. DAO Diamine oxidase R. Alcázar and T. Altabella contributed equally to this work. Dap 1,3-Diaminopropane dcSAM Decarboxylated SAM T. Altabella · C. Bortolotti · A. F. Tiburcio (&) FAD Flavin adenine dinucleotide Departament de Productes Naturals, Biologia Vegetal i Edafologia, Facultat de Farmàcia, GABA -Aminobutyric acid Universitat de Barcelona, Av. Joan XIII s/n, LSD Lysine-speciWc demethylase 08028 Barcelona, Spain NO Nitric oxide e-mail: [email protected] ODC Ornithine decarboxylase R. Alcázar · M. Reymond · C. Koncz PAO Polyamine oxidase Max-Planck Institut für Züchtungsforschung, Pro Proline Carl-von-Linné-Weg 10, 50829 Cologne, Germany Put Putrescine SAM S-Adenosyl methionine F. Marco Fundacion CEAM, Parque Tecnologic c/Charles Darwin 14, SAMDC S-Adenosyl methionine decaboxylase Paterna, 46980 Valencia, Spain ROS Reactive oxygen species SMO Spermine oxidase P. Carrasco Spd Spermidine Departament de Bioquímica i Biologia Molecular, Facultat de Ciències Biològiques, Universitat de València, SDPS Spermidine synthase Dr. Moliner 50, Burjassot, 46100 Valencia, Spain Spm Spermine 123 1238 Planta (2010) 231:1237–1249 SPMS Spermine synthase ripening, and abiotic and biotic plant stress responses (Gal- TCA Tricarboxylic acid ston and Kaur-Sawhney 1990; Kumar et al. 1997; Walden tSpm Thermospermine et al. 1997; Malmberg et al. 1998; Bouchereau et al. 1999; Bagni and Tassoni 2001; Alcázar et al. 2006b; Kusano et al. 2008). Introduction Changes in plant polyamine metabolism occur in response to a variety of abiotic stresses (Bouchereau et al. Polyamines can be considered as one of the oldest group of 1999; Alcázar et al. 2006b; Groppa and Benavides 2008). substances known in biochemistry (Galston 1991). Indeed, The importance of this process is illustrated by the fact that the tetramine spermine (Spm) was discovered more than in stressed plants, the levels of Put may account for 1.2% of 300 years ago in ageing human spermatozoa (van the dry matter, representing at least 20% of the nitrogen Leeuwenhoek 1678), whilst the diamine putrescine (Put) and (Galston 1991). However, the physiological signiWcance of cadaverine (Cad) were identiWed in putrefying cadavers increased polyamine levels in abiotic stress responses is more than 100 years ago (Brieger 1885). The structure and still unclear (Alcázar et al. 2006b; Kusano et al. 2008; Gill chemistry of the most abundant polyamines Put, Spm and and Tuteja 2010). Complete sequencing of the Arabidopsis the triamine spermidine (Spd) were further elucidated in the genome has facilitated the use of global ‘omic’ approaches 1920s, and it was revealed that they are nitrogen-containing in the identiWcation of target genes in polyamine biosynthe- compounds of low molecular weight (Dudley et al. 1926, sis and signalling pathways. Loss and gain of function 1927). Nowadays, Put and Spd are believed to be ubiqui- mutations aVecting polyamine metabolism provide useful tous in all living cells. Earlier contentions that Spm does tools to gain new insights into molecular mechanisms not occur in prokaryotes are incorrect, since this tetramine underlying polyamine functions. Recent studies indicate is also present in various bacterial cells (Pegg and Michael that polyamines may act as cellular signals in intricate cross 2009). It has been suggested that plants had acquired a part talk with hormonal pathways, including abscisic acid of the polyamine biosynthetic pathway from an ancestral (ABA) regulation of abiotic stress responses. A progress in cyanobacterial precursor of the chloroplast (Illingworth unravelling the molecular functions of polyamines has also et al. 2003). Therefore, it can be assumed that this is an facilitated the generation of Arabidopsis transgenic plants ancient metabolic route in plants, which is also present in resistant to various stresses. However, the transfer of the all organisms (Minguet et al. 2008). Many results support latter technology to valuable crops have some current con- the contention that polyamines are essential for life. Thus, strains in the agricultural industry despite the fact that chemically or genetically induced depletion of Put and/or breeding stress-resistant varieties by making use of natu- Spd levels is lethal in yeast, protists and plants (Hamasaki- rally occurring compounds is a basic prerequisite of sus- Katagiri et al. 1998; Roberts et al. 2001; Imai et al. 2004b; tainable agriculture. We envisage that further exploitation Urano et al. 2005). Organisms deWcient in Spm are viable, of natural variability can open new alternatives for both but show diVerent degrees of dysfunction. This indicates fundamental and applied plant polyamine research. that Spm, albeit not essential, must also play very important roles in growth and development (Imai et al. 2004a; Wang et al. 2004; Yamaguchi et al. 2007; Minguet et al. 2008). Polyamine biosynthesis Since polyamines are protonated at normal cellular pH, their biological function was initially associated with the Metabolic studies indicate that the intracellular levels of capability of binding diVerent anionic macromolecules polyamines in plants are mostly regulated by anabolic and (DNA, RNA, chromatin and proteins), thus conWning them catabolic processes, as well as by their conjugation to as substances with a structural role. However, it was later hydroxycinnamic acids. Schematic representation of these conWrmed that in addition to stabilizing macromolecular processes and their interactions with other metabolic path- structures, polyamines act as regulatory molecules in many ways are depicted in Fig. 1. The biosynthesis of polyamines fundamental cellular processes (Igarashi and Kashiwagi is initiated with the formation of diamine Put. In mammals 2000; Seiler and Raul 2005; Alcázar et al. 2006b; Kusano and fungi, Put is formed from ornithine in a reaction cata- et al. 2008). These include cell division, diVerentiation and lysed by ornithine decarboxylase (ODC, EC 4.1.1.17). In proliferation, cell death, DNA and protein synthesis and plants and bacteria, however, there is an alternative path- gene expression (Igarashi and Kashiwagi 2000; Childs way for the formation of Put, which is synthesized from et al. 2003; Seiler and Raul 2005). In plants, polyamines arginine in a reaction catalysed by arginine decarboxylase have been implicated in many physiological processes, (ADC, EC 4.1.1.19) followed by two successive steps cata- such as organogenesis, embryogenesis, Xoral initiation lysed by agmatine iminohydrolase (AIH, EC 3.5.3.12) and development, leaf senescence, fruit development and and N-carbamoylputrescine amidohydrolase (CPA, EC 123 Planta (2010) 231:1237–1249 1239 Fig. 1 Polyamine metabolism and interaction with other metabolic SAM decarboxylase, 20 spermidine synthase, 21 spermine synthase, routes. Biosynthetic pathways for polyamines and related metabolites 22 thermospermine synthase, 23 glutamate decarboxylase, 24 diamine are indicated by continuous lines. Dashed lines show the formation of oxidase, 25 putrescine hydroxycinnamoyl transferase, 26 polyamine putrescine-derived alkaloids, polyamine conjugation and catabolic oxidase, 27 -aminobutyrate aminotransferase, 28 succinic semialde- processes. Numbers refer to the following enzymes: 1 nitrate reductase, hyde dehydrogenase, 29 arginase, 30 ornithine aminotransferase, 31 2 nitrite reductase, 3 nitrogenase, 4 glutamine synthetase, 5 glutamate nitric oxide synthase, 32 ACC synthase, 33 ACC oxidase, 34 nitrate synthase, 6 glutamate N-acetyltransferase, 7 acetylglutamate kinase, 8 reductase, 35 lysine decarboxylase. It has been shown recently that N-acetyl--phosphate reductase, 9 acetylornithine transaminase,