Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Phylogenetic relationship of potato CAT1 and CAT2 genes, their differential expression in non-photosynthetic organs and during leaf development, and their association with different cellular processes

Isabel Santos A B C , Helena Pires B , José M. Almeida A B , Fernanda Fidalgo A B , Ana Confraria B , Márcia Duarte B , Júlio Borlido B and Roberto Salema B
+ Author Affiliations
- Author Affiliations

A Botany Department, School of Sciences, University of Porto, Rua do Campo Alegre, 1191, 4150-180 Porto, Portugal.

B Institute for Molecular and Cellular Biology, University of Porto, Rua do Campo Alegre, 823, 4150-180 Porto, Portugal.

C Corresponding author. Email: isantos@ibmc.up.pt

Functional Plant Biology 33(7) 639-651 https://doi.org/10.1071/FP06024
Submitted: 23 January 2006  Accepted: 30 March 2006   Published: 3 July 2006

Abstract

Plants contain multiple forms of catalase (CAT) and their specific functions remain uncertain. We cloned two potato cDNAs corresponding to CAT1 and CAT2 genes, analysed their phylogenetic relationship, and studied their expression and activity in different organs to gain clues to their functions. Phylogenetic trees and the alignment of CAT cDNA sequences provided evidence that CAT1 and CAT2 genes have high identity to catalases of other solanaceous species, but are not phylogenetically closely related to one another, which contradicts the phylogenetic closeness ascribed to these genes. Northern blot analyses revealed that expression of CAT genes is controlled by leaf developmental phase. CAT2 expression was higher in both very young and senescent leaves, whereas CAT1 mRNA accumulated mainly in mature leaf, where the lowest CAT2 expression occurred. CAT1 and CAT2 are also differentially expressed in root, sprout and petal. Expression and activity patterns are consistent with different physiological roles for CAT1 and CAT2 isoforms. CAT1 is considered to be associated with photorespiration whereas CAT2 would fulfill physiological roles unrelated to this process. CAT2 appears to be a multifunctional isoform, associated with glyoxysomal activity in leaf senescence, other processes in non-photosynthetic organs and defence, functions that in other solanaceous species are fulfilled by two different isoforms.

Keywords: catalase gene expression; catalase genes relationship; potato catalase genes.


Acknowledgments

We thank Drs Jorge Vieira, Cristina Vieira and Ramiro Morales-Hojas for making possible the parsimony analysis of the nucleotide sequences and for helpful comments. We thank Dr Robert Graveland from HZPC Holland B.V. Research & Development, The Netherlands, for the gift of potato seeds. This work was supported by the Fundação para a Ciência e Tecnologia (FCT, Lisboa, Portugal: project POCTI / BME / 33044 / 2000).


References


Almeida JM, Fidalgo F, Confraria A, Santos A, Pires H, Santos I (2005) Effect of hydrogen peroxide on catalase gene expression, isoform activities and levels in leaves of potato sprayed with homobrassinolide and ultrastructural changes in mesophyll cells. Functional Plant Biology 32, 707–720.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bagnoli F, Danti S, Magherini V, Cozza R, Innocenti AM, Racchi ML (2004) Molecular cloning, characterization and expression of two catalase genes from peach. Functional Plant Biology 31, 349–357.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dangl JL , Dietrich RA , Thomas H (2000) Senescence and programmed cell death. In ‘Biochemistry and molecular biology of plants’. (Eds B Buchanan, W Gruissem, R Jones) pp. 1044–1100. (American Society of Plant Physiologists: Rockville)

Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57, 779–795.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dat JF, Pellinen R, Beeckman T, Van de Cotte B, Langebartels C, Kangasjarvi J, Inzé D, Van Breusegem F (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process tobacco. The Plant Journal 33, 621–632.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Desikan R, Cheung M-K, Clarke A, Golding S, Sagi M, Fluhr R, Rock C, Hancock J, Neill S (2004) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Functional Plant Biology 31, 913–920.
Crossref | GoogleScholarGoogle Scholar | open url image1

Durner J, Klessig DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. Journal of Biological Chemistry 271, 28492–28501.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Feierabend J (2005) Catalases in plants: molecular and functional properties role in stress defence. In ‘Antioxidants and reactive oxygen species in plants’. (Ed. N Smirnoff) pp. 101–140. (Blackwell Publishing: Oxford)

Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences USA 85, 8998–9002.
Crossref |
open url image1

Frugoli JA, Zong HH, Nuccio ML, McCourt P, McPeek MA, Thomas TL, McLung CR (1996) Catalase is encoded by a multigene family in Arabidopsis thaliana (L.) Heynh. Plant Physiology 112, 327–336.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Frugoli JA, McPeek MA, Thomas TL, McClung CR (1998) Intron loss and gain during evolution of the catalase gene family in Angiosperms. Genetics 149, 355–365.
PubMed |
open url image1

Heinze M , Gerhardt B (2002) Plant catalases In ‘Plant peroxisomes: biochemistry, cell biology and biotechnological application’. (Eds A Baker, IA Graham) pp. 103–140. (Kluwer Academic Publishers: Dordrecht)

Jiang CZ, Rodermel SR, Shibles RM (1993) Photosynthesis, rubisco activity and amount, and their regulation by transcription in senescing soybean leaves. Plant Physiology 101, 105–112.
PubMed |
open url image1

Klotz MG, Klassen RG, Loewen PC (1997) Phylogenetic relationships among prokaryotic and eukaryotic catalases. Molecular Biology and Evolution 14, 951–958.
PubMed |
open url image1

Lino-Neto T, Piques MC, Barbeta C, Sousa MF, Tavares RM, Pais MS (2004) Identification of Zantedeschia aethiopica Cat1 and Cat2 catalases genes and their expression analysis during spathe senescence and regreening. Plant Science 167, 889–898.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lohman KN, Gan S, Manorama CJ, Amasino RM (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiologia Plantarum 92, 322–328.
Crossref | GoogleScholarGoogle Scholar | open url image1

McClung CR (1997) Regulation of catalases in Arabidopsis. Free Radical Biology & Medicine 23, 489–496.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Physiologia Plantarum 15, 473–497.
Crossref |
open url image1

Navarre DA, Mayo D (2004) Differential characteristics of salicylic acid-mediated signaling in potato. Physiological and Molecular Plant Pathology 64, 179–188.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ni W, Trelease RN (1991) Post-transcriptional regulation of catalase isozyme expression in cotton seeds. The Plant Cell 3, 737–744.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niebel A, Heungens K, Bartels N, Inzé D, Van Montagu M, Gheysen G (1995) Characterization of a pathogen-induced catalase and its systemic expression upon nematode bacterial infection. Molecular Plant-Microbe Interactions 8, 371–379.
PubMed |
open url image1

Redinbaugh MG, Sabre M, Scandalios JG (1990) Expression of the maize Cat3 catalase gene is under the influence of a circadian rhythm. Proceedings of the National Academy of Sciences USA 87, 6853–6857.
Crossref |
open url image1

Rojas-Beltran JA, Dejaeghere F, Koth MAA, Jardin PD (2000) Expression and activity of antioxidant enzymes during potato tuber dormancy. Potato Research 43, 383–393.
Crossref |
open url image1

Santos I, Fidalgo F, Almeida JM, Salema R (2004) Biochemical and ultrastructural changes in leaves of potato plants grown under supplementary UV-B radiation. Plant Science 167, 925–935.
Crossref | GoogleScholarGoogle Scholar | open url image1

Scandalios JG , Guan L , Polidoros AN (1997) Catalases in plants: gene structure, properties, regulation and expression. In ‘Oxidative stress and the molecular biology of antioxidant defenses’. (Ed. JG Scandalios) pp. 343–406. (Cold Spring Harbor Laboratory Press: New York)

Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. (Sinauer Associates: Sunderland, MA)

Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T , et al. (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proceedings of the National Academy of Sciences USA 100, 16113–16118.
Crossref | GoogleScholarGoogle Scholar | open url image1

Willekens H, Langebartels C, Tire C, Van Montagu M, Inzé D, Van Camp W (1994a) Differential expression of catalase genes in Nicotiana plumbaginifolia (L.). Proceedings of the National Academy of Sciences USA 91, 10 450–10 454.
Crossref |
open url image1

Willekens H, Villarroel R, Van Montagu M, Inzé D, Van Camp W (1994b) Molecular identification of catalases from Nicotiana plumbaginifolia (L.). FEBS Letters 352, 79–83.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Willekens H, Van Camp W, Van Montagu M, Inzé D, Sandermann H, Langebartels C (1994c) Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia (L.). Plant Physiology 106, 1007–1014.
PubMed |
open url image1

Willekens H, Inzé D, Van Montagu M, Van Camp W (1995) Catalases in plants. Molecular Breeding 1, 207–228.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wu G, Shah DM (1995) Isolation and characterization of a potato catalase cDNA (GenBank U27082). Plant Physiology 108, 1748–1749. open url image1

Yi S-Y, Yu S-H, Choi D (1999) Molecular cloning of a catalase cDNA from Nicotiana glutinosa L. and its repression by tobacco mosaic virus infection. Molecules and Cells 9, 320–325.
PubMed |
open url image1

Yu D, Liu Y, Fan B, Klessig DF, Chen Z (1997) Is the high basal level of salicylic acid important for disease resistance in potato? Plant Physiology 115, 343–349.
PubMed |
open url image1

Zhong HH, Young JC, Pease EA, Hangarter RP, McClung CR (1994) Interactions between light and the circadian clock in the regulation of CAT2 expression in Arabidopsis. Plant Physiology 104, 889–898.
PubMed |
open url image1