Skip to main content
Log in

Overexpression of the 3′(2′),5′-bisphosphate nucleotidase gene AtAHL confers enhanced resistance to Pectobacterium carotovorum in Arabidopsis

  • Original Article
  • Biochemistry/Molecular Biology
  • Published:
Journal of the Korean Society for Applied Biological Chemistry Submit manuscript

Abstract

The Arabidopsis AtAHL gene encodes a 3′(2′),5′-bisphosphate nucleotidase that catalyzes the conversion of adenosine 3′,5′-bisphosphate (PAP) into adenosine monophosphate and inorganic phosphate. We have generated transgenic Arabidopsis overexpressing this gene under control of the cauliflower mosaic virus 35S (CaMV 35S) promoter. Transgenic lines integrating a single copy of the insert DNA and constitutively expressing the AtAHL gene were selected. The transgenic lines of Arabidopsis plants exhibited enhanced resistance to Pectobacterium carotovorum subsp. carotovorum. In general, plant defense responses and sulfur metabolism are linked through jasmonic acid signaling. The expression of sulfur-related defense genes is known to be induced via a jasmonate-mediated signaling pathway. In this work, we observed that the expression of AtAHL was also induced by jasmonate treatment in Arabidopsis. Our data suggest that PAP catabolic activity enhanced by the jasmonate signaling pathway contributes to the rapid flux of the sulfur activation pathway, accelerates the incorporation of activated sulfur into sulfur-containing defense molecules such as defensins, thionins, and glucosinolates, and thereby increases defense resistance in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aguilar I, Alamillo JM, García-Olmedo F, and Rodríguez-Palenzuela P (2002) Natural variability in the Arabidopsis response to infection with Erwinia carotovora subsp. carotovora. Planta 215, 205–209.

    Article  CAS  Google Scholar 

  • Brader G, Mikkelsen MD, Halkier BA, and Palva ET (2006) Altering glucosinolate profiles modulates disease resistance in plants. Plant J 46, 758–767.

    Article  CAS  Google Scholar 

  • Brader G, Tas E, and Palva ET (2001) Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiol 126, 849–860.

    Article  CAS  Google Scholar 

  • Broekaert WF, Terras FRG, Cammue BPA, and Osborn RW (1995) Plant defensins: Novel antimicrobial peptides as components of the host defense system. Plant Physiol 108, 1353–1358.

    Article  CAS  Google Scholar 

  • Carpenter CD and Simon AE (1998) Preparation of RNA. Methods Mol Biol 82, 85–89.

    CAS  Google Scholar 

  • Cheong J-J and Kwon H-B (1999) Arabidopsis AtAHL gene encodes a 3′(2′),5-bisphosphate nucleotidase sensitive to toxic heavy metal ions. Agric Chem Biotechnol 42, 169–174.

    CAS  Google Scholar 

  • Clough SJ and Bent AF (1998) Floral dip; a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16, 735–743.

    Article  CAS  Google Scholar 

  • Cooper RM and Williams JS (2004) Elemental sulfur as an induced antifungal substance in plant defence. J Exp Bot 55, 1947–1953.

    Article  CAS  Google Scholar 

  • Dichtl B, Stevens A, and Tollervey D (1997) Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes. EMBO J 16, 7184–7195.

    Article  CAS  Google Scholar 

  • Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79, 331–348.

    Article  CAS  Google Scholar 

  • Epple P, Apel K, and Bohlmann H (1997) Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell 9, 509–520.

    CAS  Google Scholar 

  • Falk KL, Tokuhisa JG, and Gershenzon (2007) The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biol 9, 573–581.

    Article  CAS  Google Scholar 

  • Gil-Mascarell R, López-Coronado JM, Bellés JM, Serrano R, and Rodríguez PL (1999) The Arabidopsis HAL2-like gene family includes a novel sodium-sensitive phosphatase. Plant J 17, 373–383.

    Article  CAS  Google Scholar 

  • Halkier BA and Gerschenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57, 303–333.

    Article  CAS  Google Scholar 

  • Hell R (1997) Molecular physiology of plant sulfur metabolism. Planta 202, 138–148.

    Article  CAS  Google Scholar 

  • Jost R, Altschmied L, Bloem E, Bogs J, Gershenzon J, Hähnel U et al. (2005) Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynth Res 86, 491–508.

    Article  CAS  Google Scholar 

  • Jung C, Lyou SH, Yeu SY, Kim MA, Rhee S, Kim M et al. (2007) Microarray-based screening of jasmonate-responsive genes in Arabidopsis thaliana. Plant Cell Report 26, 1053–1063.

    Article  CAS  Google Scholar 

  • Klaassen CD and Boles JW (1997) The importance of 3′-phosphoadenosine 5′-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J 11, 404–418.

    CAS  Google Scholar 

  • Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97, 479–495.

    Article  CAS  Google Scholar 

  • Kopriva S and Koprivova A (2004) Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55, 1775–1783.

    Article  CAS  Google Scholar 

  • Kopriva S, Fritzemeier K, Wiedemann G, and Reski R (2007) The Putative moss 3-phosphoadenosine-5-phosphosulfate reductase is a novel form of adenosine-5-phosphosulfate reductase without an iron-sulfur cluster. J Biol Chem 282, 22930–22938.

    Article  CAS  Google Scholar 

  • Koprivova A, Meyers AJ, Schween G, Herschbach C, Reski R, and Kopriva S (2002) Functional knockout of the adenosine 5′-phosphosulfate reductase gene in Physcomitrella patens revives an old rout of sulfate assimilation. J Biol Chem 277, 32195–32201.

    Article  CAS  Google Scholar 

  • Kruse C, Jost R, Lipschis M, Kopp B, Hartmann, and Hell R (2007) Sulfurenhanced defence: effects of sulfur metabolism, nitrogen supply, and pathogen lifestyle. Plant Biol 9, 608–619.

    Article  CAS  Google Scholar 

  • Leyh TS (1993) The physical biochemistry and molecular genetics of sulfate activation. Crit Rev Biochem Mol Biol 28, 515–542.

    Article  CAS  Google Scholar 

  • Murguía JR, Bellés JM, and Serrano R (1996) The yeast HAL2 nucleotidase is an in vivo target of salt toxicity. J Biol Chem 271, 29029–29033.

    Article  Google Scholar 

  • Peng Z and Verma DP (1995) A rice HAL2-like gene encodes a Ca2+-sensitive 3′(2′)-phosphohydrolase and complements yeast met22 and Escherichia coli cysQ mutations. J Biol Chem 270, 29105–29110.

    Article  CAS  Google Scholar 

  • Perombelon MCM and Kelman A (1980) Ecology of the soft rot Erwinias. Annu Rev Phytopathol 18, 361–387.

    Article  Google Scholar 

  • Quintero FJ, Garciadeblas B, and Rodriguez-Navarro A (1996) The SAL1 gene of Arabidopsis, encoding an enzyme with 3′(2′),5′-bisphosphate nucleotidase and inositol polyphosphate 1-phosphatase activities, increases salt tolerance in yeast. Plant Cell 8, 529–537.

    CAS  Google Scholar 

  • Rausch T and Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10, 503–509.

    Article  CAS  Google Scholar 

  • Rodríguez VM, Chetelat A, Majcherczyk P, and Farmer EE (2010) Chloroplastic phosphoadenosine phosphosulfate metabolism regulates basal levels of the prohormone jasmonic acid in Arabidopsis leaves. Plant Physiol 152, 1335–1345.

    Article  Google Scholar 

  • Rojo E, León J, and Sánchez-Serrano JJ (1999) Cross-talk between wound signaling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20, 135–142.

    Article  CAS  Google Scholar 

  • Sasaki-sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N et al. (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44, 653–668.

    Article  CAS  Google Scholar 

  • Sønderby IE, Geu-Flores F, and Halkier BA (2010) Biosynthesis of glucosinolates — gene discovery and beyond. Trends Plant Sci 15, 283–290.

    Article  Google Scholar 

  • Takahashi H, Kopriva S, Giordano M, Saito K, and Hell R (2011) Sulfur Assimilation in Photosynthetic Organisms: Molecular Functions and Regulations of Transporters and Assimilatory Enzymes. Annul Rev Plant Biol 62, 157–184.

    Article  CAS  Google Scholar 

  • Thomma BPHJ, Cammue BPA, and Thevissen K (2002) Plant defensins. Planta 216, 193–202.

    Article  CAS  Google Scholar 

  • Yang L-M, Fernandez MD, and Lamppa GK (1994) Acyl carrier protein (ACP) import into chloroplasts: Covalent modification by a stromal holo ACP synthase is stimulated by exogenously added CoA and inhibited by adenosine 3′,5′-bisphosphate. Eur J Biochem 224, 743–750.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jong-Joo Cheong.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, H.J., Choi, Y.D., Song, S.I. et al. Overexpression of the 3′(2′),5′-bisphosphate nucleotidase gene AtAHL confers enhanced resistance to Pectobacterium carotovorum in Arabidopsis . J Korean Soc Appl Biol Chem 56, 21–26 (2013). https://doi.org/10.1007/s13765-012-2178-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13765-012-2178-2

Keywords

Navigation