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A Novel Stress-Inducible Antioxidant Enzyme Identified from The

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A Novel Stress-Inducible Antioxidant Enzyme Identified from The Planta (2002) 215: 716–726 DOI 10.1007/s00425-002-0819-0 ORIGINAL ARTICLE Shaheen B. Mowla Æ Jennifer A. Thomson Jill M. Farrant Æ Sagadevan G. Mundree A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker Received: 25 March 2002 / Accepted: 30 May 2002 / Published online: 10 July 2002 Ó Springer-Verlag 2002 Abstract A cDNA corresponding to 1-Cys peroxire- which may function to protect nucleic acids within the doxin, an evolutionarily conserved thiol-specific an- nucleus against oxidative injury. tioxidant enzyme, was isolated from Xerophyta viscosa Baker, a resurrection plant indigenous to Southern Af- Keywords Desiccation stress Æ Peroxiredoxin Æ rica and belonging to the family Velloziaceae. The Resurrection plant Æ Xerophyta cDNA, designated XvPer1, contains an open reading frame that encodes a polypeptide of 219 residues with a Abbreviations ABA: abscisic acid Æ Cys: cysteine Æ NLS: predicted molecular weight of 24.2 kDa. The XvPer1 nuclear localisation signal Æ PFD: photon flux densi- polypeptide shows significant sequence identity (approx. ty Æ Prx: peroxiredoxin Æ ROS: reactive oxygen spe- 70%) to other recently identified plant 1-Cys peroxire- cies Æ RWC: relative water content Æ ww: water potential doxins and relatively high levels of sequence similarity (approx. 40%) to non-plant 1-Cys peroxiredoxins. The XvPer1 cDNA contains a putative polyadenylation site. Introduction As for all 1-Cys peroxiredoxins identified to date, the amino acid sequence proposed to constitute the active Xerophyta viscosa Baker (family Velloziaceae) is a site of the enzyme, PVCTTE, is highly conserved in monocotyledonous desiccation-tolerant plant belonging XvPer1. It also contains a putative bipartite nuclear to a small group of angiosperms commonly referred to localization signal. Southern blot analysis revealed that as resurrection plants (Gaff 1971; Bewley and Oliver there is a single copy of XvPer1 in the X. viscosa genome. 1992; Vertucci and Farrant 1995; Ingram and Bartels All angiosperm 1-Cys peroxiredoxins described to date 1996). Desiccation tolerance is defined as the ability to are seed-specific and absent in vegetative tissues even revive from the air-dried state, which is the most severe under stress conditions; therefore, XvPer1 is unique in form of water stress, since under these conditions the that it is expressed in the vegetative tissues of X. viscosa. majority of protoplasmic water is lost from the cell. The XvPer1 transcript was absent in fully hydrated X. X. viscosa can be dehydrated to 5% relative water con- viscosa tissue but levels increased in tissues subjected to tent (RWC) and upon rewatering the plant rehydrates ° abiotic stresses such as dehydration, heat (42 C), high completely within 80 h, resuming full physiological ac- l –2 –1 light intensity (1,500 mol photons m s ) and when tivities (Sherwin and Farrant 1996). l treated with abscisic acid (100 M ABA) and sodium Many resurrection plants are being studied in an at- chloride (100 mM NaCl). Western blot analyses corre- tempt to understand the mechanisms that enable vege- lated with the patterns of expression of XvPer1 tative tissues to withstand desiccation. The ultimate aim transcripts under different stress conditions. Immuno- is to identify characteristics that may be used to produce fluorescence analyses revealed that XvPer1 is localized in crops with improved tolerance to osmotic stress. X. vis- the nucleus of dehydrated X. viscosa leaf cells. These cosa, being monocotyledonous, can serve as a model for results suggest that XvPer1 is a stress-inducible gene, the identification of characteristics that could be used to improve stress tolerance of cereal crops (Mundree and Farrant 2000). S.B. Mowla Æ J.A. Thomson Æ J.M. Farrant Æ S.G. Mundree (&) In addition to water limitation, the presence of high Department of Molecular and Cell Biology, light intensities during dehydration can be extremely University of Cape Town, Private Bag, Rondebosch, 7701, South Africa damaging to photosynthetically active tissues (Sherwin E-mail: [email protected] and Farrant 1998). Even under mild water-stress con- Fax: +27-21-6897573 ditions, closure of the stomata can result in excitation 717 energy being transferred from chlorophyll to oxygen, functions: as an antioxidant, an endogenous regulator of leading to the formation of oxygen free radicals. If un- apoptosis (Ichimiya et al. 1997), and as an intracellular quenched, these molecules can cause considerable dam- signalling molecule (Kang et al. 1998; Kowaltowski et al. age to the subcellular milieu. Reactive oxygen species 1998). Plant 2-Cys Prx proteins also function as radical (ROS) play a significant role in causing damage to living scavengers coupled to the photosynthetic machinery in cells under severe stress conditions. Some examples of chloroplast (Baier and Dietz 1997, 1999). – ROS are O2 radicals, OH¢ and H2O2 (Foyer et al. 1994). The cellular function of 1-Cys Prx is not completely By themselves, those compounds are relatively unreac- understood. Its protein structure has been elucidated tive and can even be used by the plant in a beneficial and several cDNAs encoding the protein have been manner. For example, H2O2, produced from the oxida- isolated and characterised from yeast, animal, and plant tive burst generated during hypersensitive plant–patho- cells (Goldmark et al. 1992; Aalen et al. 1994; Stacy et al. gen interaction, functions as a local trigger of 1996, 1999). In angiosperms, it is specifically expressed programmed cell death and causes rapid cross-linking of in the nucleus of immature embryos and the aleurone cell wall proteins (Levine et al. 1994). H2O2 also appears layers of the seed (Haslekas et al. 1998). The expression to act as a signal molecule that induces the transcription level increases late in seed development and is main- – of defence-related genes. However, O2 radicals and tained in mature seeds during storage. However, when H2O2 can react to produce ROS that are damaging to non-dormant seeds are imbibed the transcript level de- essential cellular components. Transition metals catalyse creases dramatically and transcripts disappear com- the formation of OH¢ radicals through the Haber-Weiss pletely after seed germination. This suggests that the reaction and this accounts for much of the toxicity of functional role of 1-Cys Prx in angiosperms might be the – O2 radicals and H2O2. They are capable of causing in- maintenance of seed dormancy. However, this sugges- discriminate lipid peroxidation, protein denaturation, tion had to be questioned when it was reported that the and damage to DNA (Inze´and Van Montagu 1995). transcript levels did not correlate with abscisic acid To combat oxidative stress, complex protective (ABA) levels. ABA is required for the induction of seed mechanisms have been evolved by plants to mitigate and dormancy in ABA-deficient or insensitive mutants of repair the damage initiated by free radicals (Price et al. Arabidopsis (Stacy et al. 1996). 1994). The primary constituents of these protective Recently, transgenic tobacco plants constitutively mechanisms include enzymes such as superoxide expressing rice 1-Cys peroxiredoxin (R1C-Prx) were dismutase (SOD), catalases and peroxidases, and free- generated (Lee et al. 2000). These transgenics showed radical scavengers such as carotenoids, ascorbate, toc- enhanced resistance against oxidative stress imposed by opherols, and oxidized and reduced glutathione (GSSG H2O2 as compared to wild-type control plants. There- and GSH, respectively). fore, the in vivo function of 1-Cys Prx in angiosperms Like most resurrection plants, X. viscosa grows in may not be related to the maintenance of seed dormancy, shallow soils on rocky outcrops at high altitudes where but rather to protective activity against oxidative stress. there is little shade. Upon drying, it loses its chlorophyll Using differential screening of an X. viscosa cDNA (poikilochlorophyllous), and the leaf blades fold in half library (Ndima et al. 2001), a peroxiredoxin homologue along the midrib, with only the abaxial surface being was identified. In this paper we describe the isolation exposed to light. The leaves initially turn yellow, and and characterisation of the XvPer1 cDNA. We investi- then dark purple when in a more advanced dry state. The gate its expression pattern under different stress condi- abaxial surfaces have a reflective sticky coating, which tions in X. viscosa. We also localised the protein to the may serve to reduce light absorbed by the leaf. The ac- nucleus of leaf cells under desiccation stress, which tivities of the three common antioxidant enzymes, makes it unique among angiosperms as other peroxire- ascorbate peroxidase, glutathione reductase and SOD, doxins have been found to be almost entirely confined to increase during dehydration (Sherwin and Farrant 1998). seeds and are absent in vegetative tissues, even upon Peroxiredoxins are one of the most recently discov- dehydration. ered types of enzymatic antioxidant (Chae et al. 1994). They have been shown to be active on substrates such as hydroperoxides and alkyl hydroperoxides. Based on Material and methods their amino acid sequences and immunological proper- ties, the peroxiredoxin (Prx) proteins can be divided into Plant material six distinct groups (Prx I–VI), all of which contain one or two conserved cysteine (Cys) residues, called 1-Cys Xerophyta viscosa Baker plants were collected from Cathedral Peak Nature Reserve, (Kwazulu Natal Province,
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