Functional characterization of an Arabidopsis prolyl aminopeptidase AtPAP1 in response to salt and drought stresses

Plant Cell, Tissue and Organ Culture

Volumn 114, Issue 3, 2013, Pages 325-338

  Sun, Xiaoli ^a   Wang, Feifei ^a,b   Cai, Hua ^a   Zhao, Chaoyue ^a   Ji, Wei ^a   Zhu, Yanming ^a  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^b NORTHEAST INSTITUTE OF GEOGRAPHY AND AGRICULTURAL ECOLOGY   (China)

Author keywords

AtPAP1; Drought; High salinity; Prolyl aminopeptidase; Promoter activity

Indexed keywords

AMINO PEPTIDASE; ATPAP1; FUNCTIONAL CHARACTERIZATION; HIGH SALINITY; ONION EPIDERMAL CELLS; PROMOTER ACTIVITIES; PROTEIN SEQUENCE ALIGNMENTS; QUANTITATIVE REAL TIME PCR;

CYTOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; POLYMERASE CHAIN REACTION;

DROUGHT;

ALLIUM CEPA; ARABIDOPSIS; ESCHERICHIA COLI;

EID: 84882840786     PISSN: 01676857     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11240-013-0328-9     Document Type: Article

References (51)

1. Albertson NH, Koomey M (1997) Molecular cloning and characterization of a proline iminopeptidase from Serratia marcescens: cloning of the enzyme gene and crystallization of the expressed enzyme. J Biochem 122: 601-605.
2. Allaker RP, Young KA, Hardie JM (1994) Rapid detection of proline iminopeptidase as an indicator of Eikenella corrodens periodontal infection. Lett Appl Microbiol 19: 325-327.
3. Barnett NM, Naylor AW (1966) Amino acid and protein metabolism in Bermuda grass during water stress. Plant Physiol 41: 1222-1230.
4. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline in water-stress studies. Plant Soil 39: 205-207.
5. Bolumar T, Sanz Y, Aristory MC, Toldra F (2003) Purification and characterization of a prolyl aminopeptidase from Debaryomyces hansenii. Appl Environ Microbiol 69: 227-232.
6. Chliep MS, Ebert B, Simon-Rosin U, Zoeller D, Fisahn J (2010) Quantitative expression analysis of selected transcription factors in pavement, basal and trichome cells of mature leaves from Arabidopsis thaliana. Protoplasma 241: 29-36.
7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
8. Cunningham DF, O'Connor B (1997) Proline specific peptidases. Biochim Biophys Acta 1343: 160-186.
9. Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein and protein S-Glutathionylation in Arabidopsis. Plant Physiol 138: 2233-2244.
10. Dolferus R, Ji XM, Richards RA (2011) Abiotic stress and control of grain number in cereals. Plant Sci 181: 331-341.
11. FitzGerald RJ, O'Cuinn G (2006) Enzymatic debittering of food protein hydrolysates. Biotechnol Adv 24: 234-237.
12. Gao S, Yuan L, Zhai H, Liu CL, He SZ, Liu QC (2011) Transgenic sweetpotato plants expressing an LOS5 gene are tolerant to salt stress. Plant Cell Tiss Organ Cult 107: 205-213.
13. Gilbert C, Atlan D, Banc B, Portalier R (1994) Proline iminopeptidase from Lacto-bacillus delbrueckii subsp. bulgaricus CNRZ 397: purification and characterization. Microbiology 140: 537-542.
14. Islam SM, Tuteja N (2012) Enhancement of androgenesis by abiotic stress and other pretreatments in major crop species. Plant Sci 182: 134-144.
15. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
16. Jin TC, Chang Q, Li WF, Yin DX, Li ZJ, Wang DL, Liu B, Liu LX (2010) Stress-inducible expression of GmDREB1 conferred salt tolerance in transgenic alfalfa. Plant Cell Tiss Organ Cult 100: 219-227.
17. 1-pyrroline-5-carboxylate synthetase (P5CS) gene from Vigna aconitifolia demonstrates salt tolerance. Plant Cell Tiss Organ Cult 107: 383-395.
18. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D'Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50: 347-363.
19. Kishor P, Hong Z, Miao GH, Hu C, Verma D (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108: 1387-1394.
20. Kitazono A, Kitano A, Tsuru D, Yoshimoto T (1994) Isolation and characterization of the prolyl aminopeptidase gene (pap) from Aeromonas sobria: comparison with the Bacillus coagulans enzyme. J Biochem 116: 818-825.
21. Kitazono A, Kitano A, Kabashima T, Ito K, Yoshimoto T (1996) Prolyl aminopeptidase is also present in Enterobacteriaceae: cloning and sequencing of the Hafnia alvei enzyme-gene and characterization of the expressed enzyme. J Biochem 119: 468-474.
22. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63: 1593-1608.
23. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299-306.
24. Li N, Wu JM, Zhang LF, Zhang YZ, Feng H (2010) Characterization of a unique proline iminopeptidase from white-rot basidiomycetes Phanerochaete chrysosporium. Biochimie 92: 779-788.
25. Mahon S, O'Donoghue AJ, Goetz DH, Murray PG, Craik CS, Tuohy MG (2009) Characterization of a multimeric, eukaryotic prolyl aminopeptidase: an inducible and highly specific intracellular peptidase from the non-pathogenic fungus Talaromyces emersonii. Microbiology 155: 3673-3682.
26. Marinovaa M, Dolashkia A, Altenberend F, Stevanovic S, Voelter W, Tchorbanova B (2008) Characterization of an aminopeptidase and a proline iminopeptidase from cabbage leaves. Z Naturforsch C 63: 105-112.
27. Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A (2009) Unraveling delta1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. J Biol Chem 284: 26482-26492.
28. Mohamed MA, Ibrahim TA (2012) Enhanced in vitro production of Ruta graveolens L. coumarins and rutin by mannitol and ventilation. Plant Cell Tiss Organ Cult 111: 335-343.
29. Mueller LA, Hinz U, Uzé M, Sautter C, Zryd JP (1997) Biochemical complementation of the betalain biosynthetic pathway in Portulaca grandiflora by a fungal 3, 4-dihydroxyphenylalanine dioxygenase. Planta 203: 260-263.
30. Nishiuchi T, Hamada T, Kodama H, Iba K (1997) Wounding changes the spatial expression pattern of the Arabidopsis plastid omega-3 fatty acid desaturase gene (FAD7) through different signal transduction pathways. Plant Cell 9: 1701-1712.
31. Oviedo Ovando ME, Isola MC, Maldonado AM, Franzoni L (2004) Purification and properties of iminopeptidase from peanut seeds. Plant Sci 166: 1143-1148.
32. Patade VY, Bhargava S, Suprasanna P (2012) Effects of NaCl and iso-osmotic PEG stress on growth, osmolytes accumulation and antioxidant defense in cultured sugarcane cells. Plant Cell Tiss Organ Cult 108: 279-286.
33. Peng ZH, Peng KQ, Hu JJ, Xiao LT (2002) Reseach progress on accumulation of proline under osmotic stress in plants. Chin Agric Sci Bull 18: 80-83.
34. Qu LJ, Wu LQ, Fan ZM, Guo L, Li YQ, Chen ZL (2005) Over-expression of the bacterial nhaA gene in rice enhances salt and drought tolerance. Plant Sci 168: 297-302.
35. Quan XQ, Zhang YJ, Shan L, Bi YP (2007) The roles of prolines in plant growth and the tolerance to abiotic stresses. Lett Biotechnol 18: 159-162.
36. Sarid S, Berger A, Katchalski E (1959) Proline iminopeptide. J Biol Chem 234: 1740-1746.
37. Selby T, Allaker RP, Dymock D (2003) Characterization and expression of adjacent proline iminopeptidase and aspartase genes from Eikenella corrodens. Oral Microbiol Immunol 18: 256-259.
38. Shangguan XX, Xu B, Yu ZX, Wang LJ, Chen XY (2008) Promoter of a cotton fibre MYB gene functional in trichomes of Arabidopsis and glandular trichomes of tobacco. J Exp Bot 59: 3533-3542.
39. Somboonwatthanaku I, Dorling S, Leung S, McManus MT (2010) Proline biosynthetic gene expression in tissue cultures of rice (Oryza sativa L.) in response to saline treatment. Plant Cell Tiss Organ Cult 103: 369-376.
40. Stein H, Honig A (2011) Elevation of free proline and proline-rich protein levels by simultaneous manipulations of proline biosynthesis and degradation in plants. Plant Sci 181: 140-150.
41. Stewart GR, Lee JA (1974) Role of proline accumulation in halophytes. Planta 120: 279-289.
42. Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15: 89-97.
43. Szawłowska U, Zdunek-Zastocka E, Bielawski W (2011) Biochemical characterisation of prolyl aminopeptidase from shoots of triticale seedlings and its activity changes in response to suboptimal growth conditions. Plant Physiol Biochem 49: 1342-1349.
44. Szawłowska U, Grabowska A, Zdunek-Zastocka E, Bielawski W (2012) TsPAP1 encodes a novel plant prolyl aminopeptidase whose expression is induced in response to suboptimal growth conditions. Biochem Biophys Res Commun 419: 104-109.
45. Tocquin P, Corbesier L, Havelange A, Pieltain A, Kurtem E, Bernier G, Périlleux C (2003) A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biol 3: 2.
46. Weterings K, Schrauwen J, Wullems G, Twell D (1995) Functional dissection of the promoter of the pollen-specific gene NPT303 reveals a novel pollen-specific, and conserved cis-regulatory element. Plant J 8: 55-63.
47. Willems E, Leyns L, Vandesompele J (2008) Standardization of real-time PCR gene expression data from independent biological replicates. Anal Biochem 379: 127-129.
48. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An 'electronic fluorescent pictograph' browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718.
49. Yang YL, Yang F, Li XN, Shi RX, Lu J (2013) Signal regulation of proline metabolism in callus of the halophyte Nitraria tangutorum Bobr. grown under salinity stress. Plant Cell Tiss Organ Cult 112: 33-42.
50. Yoshimoto T, Tsuru D (1985) Proline iminopeptidase from Bacillus coagulans: purification and enzymatic properties. J Biochem 97: 1477-1485.
51. Zhang L, Jia Y, Wang L, Wang R (2007) A proline iminopeptidase gene upregulated in planta by a LuxR homologue is essential for pathogenicity of Xanthomonas campestris pv, campestris. Mol Microbiol 65: 121-136.