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Plant Molecular Biology

, 67:429 | Cite as

Analysis of Arabidopsis arginase gene transcription patterns indicates specific biological functions for recently diverged paralogs

  • Disa L. Brownfield
  • Christopher D. Todd
  • Michael K. Deyholos
Article

Abstract

The detailed expression patterns of transcripts of two Arabidopsis arginase genes, ARGAH1 and ARGAH2, have not been previously described, and phylogenetic analysis suggests that they diverged independently of duplication events in other lineages. Therefore, we used β-glucuronidase reporter fusions and quantitative reverse-transcriptase PCR to analyze tissue-specific expression of ARGAH1 and ARGAH2 during Arabidopsis development, and in response to the availability of nutrients and exposure to methyl jasmonate (MeJA). We demonstrated tissue-specific transcript expression and enzyme activity in pollen for ARGAH1, but not ARGAH2. Conversely, we demonstrated MeJA-inducibility of ARGAH2, but not ARGAH1. In addition, we used microarrays to identify genes for which transcript abundance following MeJA treatment differed in wild type and ARGAH2 mutants. These ARGAH2 and MeJA responsive genes included a putative pathogenesis-related protein pathogenesis response-1 (At2g14610), and a gene of unknown function (At5g03090). Interestingly, these genes had opposite responses to the loss of ARGAH2, suggesting multiple downstream effects of arginase activity, following MeJA treatment. These results, and the variety and complexity of expression patterns of ARGAH1 and ARGAH2 transcript expression and their related reporter gene fusions that we observed point to multiple functions of arginase genes in Arabidopsis, some of which have resulted through a sub-functionalization not shared by all angiosperms.

Keywords

Arginase Defense Jasmonate Jasmonic acid Nitrogen Pollen 

Abbreviations

ARGAH

Arginase (Arabidopsis)

FDR

False discovery rate

GUS

Beta-glucuronidase

LeARG

Arginase (tomato)

MeJA

Methyl jasmonate

MS

Murashige and Skoog

NO

Nitric oxide

PR

Pathogenesis related

qRT-PCR

Quantitative reverse-transcriptase PCR

SA

Salicyclic acid

SAM

Statistical analysis of microarrays

Notes

Acknowledgments

Microarrays were printed at the University of Alberta Department of Biological Sciences by Dr. Anthony Cornish. We thank Mohsen Mohammadi for assistance with phylogenetic software. This research was funded by separate NSERC Discovery Grants to MKD and the late David Gifford.

References

  1. Alabadi D, Aguero MS, Perez-Amador MA et al (1996) Arginase, arginine decarboxylase, ornithine decarboxylase and polyamines in tomato ovaries—changes in unpollinated ovaries and parthenocarpic fruits induced by auxin or gibberellin. Plant Physiol 112:1237–1244PubMedGoogle Scholar
  2. Bate N, Twell D (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol Biol 37:859–869PubMedCrossRefGoogle Scholar
  3. Boter M, Ruiz-Rivero O, Abdeen A et al (2004) Conserved myc transcription factors play a key role in jasmonate signaling both in tomato and arabidopsis. Gene Dev 18:1577–1591PubMedCrossRefGoogle Scholar
  4. Buchanan BB, Gruissem W, Jones RS (eds) (2000) Biochemistry and molecular biology of plants. American Society of Plant Biology, Rockville, MDGoogle Scholar
  5. Chen H, McCaig BC, Melotto M et al (2004) Regulation of plant arginase by wounding, jasmonate, and the phytotoxin coronatine. J Biol Chem 279:45998–46007PubMedCrossRefGoogle Scholar
  6. Cooke JEK, Brown KA, Wu R et al (2003) Gene expression associated with n-induced shifts in resource allocation in poplar. Plant Cell Environ 26:757–770CrossRefGoogle Scholar
  7. Corpas FJ, Barroso JB, Carreras A et al (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254PubMedCrossRefGoogle Scholar
  8. Devoto A, Turner JG (2005) Jasmonate-regulated arabidopsis stress signalling network. Physiol Plant 123:161–172CrossRefGoogle Scholar
  9. Devoto A, Ellis C, Magusin A et al (2005) Expression profiling reveals coi1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol Biol 58:497–513PubMedCrossRefGoogle Scholar
  10. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochem Bull 19:11–15Google Scholar
  11. Filichkin SA, Leonard JM, Monteros A et al (2004) A novel endo-beta-mannanase associated with anther and gene in tomato leman5 is pollen development. Plant Physiol 134:1080–1087PubMedCrossRefGoogle Scholar
  12. Goldraij A, Polacco JC (1999) Arginase is inoperative in developing soybean embryos. Plant Physiol 119:297–303PubMedCrossRefGoogle Scholar
  13. Higo K, Ugawa Y, Iwamoto M et al (1999) Plant cis-acting regulatory DNA elements (place) database: 1999. Nucleic Acids Res 27:297–300PubMedCrossRefGoogle Scholar
  14. Hong-Qi Z, Croes AF, Linskens HF (1982) Protein synthesis in germinating pollen of petunia: role of proline. Planta 154:199–203CrossRefGoogle Scholar
  15. Honys D, Twell D (2003) Comparative analysis of the arabidopsis pollen transcriptome. Plant Physiol 132:640–652PubMedCrossRefGoogle Scholar
  16. Jenkinson CP, Grody WW, Cederbaum SD (1996) Comparative properties of arginases. Comp Biochem Physiol 114B:107–132Google Scholar
  17. Jiang YQ, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25PubMedCrossRefGoogle Scholar
  18. King JE, Gifford DJ (1997) Amino acid utilization in seeds of loblolly pine during germination and early seedling growth. Plant Physiol 113:1125–1135PubMedGoogle Scholar
  19. Klessig DF, Malamy J (1994) The salicylic-acid signal in plants. Plant Mol Biol 26:1439–1458PubMedCrossRefGoogle Scholar
  20. Krumpelman PM, Freyermuth SK, Cannon JF et al (1995) Nucleotide-sequence of arabidopsis-thaliana arginase expressed in yeast. Plant Physiol 107:1479–1480PubMedCrossRefGoogle Scholar
  21. Lebel E, Heifetz P, Thorne L et al (1998) Functional analysis of regulatory sequences controlling PR-1 gene expression in arabidopsis. Plant J16:223–233Google Scholar
  22. Lescot M, DehaisP, Thijs G et al (2002) Plantcare, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327PubMedCrossRefGoogle Scholar
  23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative pcr and the 2(t)(-delta delta c) method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  24. Micallef BJ, Shelp BJ (1989a) Arginine metabolism in developing soybean cotyledons. 3. Utilization. Plant Physiol 91:170–174PubMedGoogle Scholar
  25. Micallef BJ, Shelp BJ (1989b) Arginine metabolism in developing soybean cotyledons. 1. Relationship to nitrogen nutrition. Plant Physiol 90:624–630PubMedCrossRefGoogle Scholar
  26. Palmieri L, Todd CD, Arrigoni R et al (2006) Arabidopsis mitochondria have two basic amino acid transporters with partially overlapping specificities and differential expression in seedling development. Bioenergetics 1757:1277–1283Google Scholar
  27. Perez-Amador MA, Lidder P, Johnson MA et al (2001) New molecular phenotypes in the dst mutants of arabidopsis revealed by DNA microarray analysis. Plant Cell 13:2703–2717PubMedCrossRefGoogle Scholar
  28. Prestridge DS (1991) Signal scan—a computer-program that scans DNA-sequences for eukaryotic transcriptional elements. Comput Appl Biosci 7:203–206PubMedGoogle Scholar
  29. Rogers HJ, Bate N, Combe J et al (2001) Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol Biol 45:577–585PubMedCrossRefGoogle Scholar
  30. Rouster J, van Mechelen J, Cameron-Mills V (1998) The untranslated leader sequence of the barley lipoxygenase 1 (lox1) gene confers embryo-specific expression. Plant J 15:435–440PubMedCrossRefGoogle Scholar
  31. Saeed AI, Sharov V, White J et al (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–384PubMedGoogle Scholar
  32. Schwacke R, Grallath S, Breitkreuz KE et al (1999) Leprot1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. Plant Cell 11:377–391PubMedCrossRefGoogle Scholar
  33. Todd CD, Cooke JEK, Mullen RT et al (2001) Regulation of loblolly pine (Pinus taeda L.) arginase in developing seedling tissue during germination and post-germinative growth. Plant Mol Biol 45:555–565PubMedCrossRefGoogle Scholar
  34. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121PubMedCrossRefGoogle Scholar
  35. Twell D, Yamaguchi J, Wing RA et al (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Gene Dev 5:496–507PubMedCrossRefGoogle Scholar
  36. Ward ER, Uknes SJ, Williams SC et al (1991) Coordinate gene activity in response to agents that induce systemic acquired-resistance. Plant Cell 3:1085–1094PubMedCrossRefGoogle Scholar
  37. Weigel D, Glazebrook J (2002) How to transform Arabidopsis. In: Arabidopsis: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  38. Zonia LE, Stebbins NE, Polacco JC (1995) Essential role of urease in germination of nitrogen-limited Arabidopsis thaliana seeds. Plant Physiol 107:1097–1103PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Disa L. Brownfield
    • 1
  • Christopher D. Todd
    • 2
  • Michael K. Deyholos
    • 1
  1. 1.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  2. 2.Department of BiologyUniversity of SaskatchewanSaskatoonCanada

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