PROTEIN L-ISOASPARTYL METHYLTRANSFERASE2 Is Differentially expressed in chickpea and enhances seed vigor and longevity by reducing abnormal isoaspartyl accumulation predominantly in seed nuclear proteins

Plant Physiology

Volumn 161, Issue 3, 2013, Pages 1141-1157

  Verma, Pooja ^a   Kaur, Harmeet ^a   Petla, Bhanu Prakash ^a   Rao, Venkateswara ^a   Saxena, Saurabh C ^a   Majee, Manoj ^a  

^a NATIONAL INSTITUTE OF PLANT GENOME RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874624120     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.206243     Document Type: Article

References (51)

1. Ahmad F, Gaur PM, Croser J (2005) Chickpea (Cicer arietinum L.). In R Singh, P Jauhar, eds, Genetic Resources, Chromosome Engineering and Crop Improvement: Grain Legumes, Vol 1. CRC Press, Boca Raton, FL, pp 187-217
2. Aswad DW, Paranandi MV, Schurter BT (2000) Isoaspartate in peptides and proteins: formation, significance, and analysis. J Pharm Biomed Anal 21: 1129-1136
3. Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14: 93-107
4. Berridge MV, Tan AS, McCoy KD, Wang R (1996) The biochemical and cellular basis of cell proliferation assays that use tetrazolium salts. Biochemica 4: 725-732
5. Blackman SA, Obendorf RL, Leopold AC (1995) Desiccation tolerance in developing soybean seeds: the role of stress proteins. Physiol Plant 93: 630-638
6. Chen T, Nayak N, Majee SM, Lowenson J, Schäfermeyer KR, Eliopoulos AC, Lloyd TD, Dinkins R, Perry SE, Forsthoefel NR, et al (2010) Substrates of the Arabidopsis thaliana protein isoaspartyl methyltransferase 1 identified using phage display and biopanning. J Biol Chem 285: 37281-37292
7. Clarke S (2003) Aging as war between chemical and biochemical processes: protein methylation and the recognition of age-damaged proteins for repair. Ageing Res Rev 2: 263-285
8. Clerkx EJM, Blankestijn-DeVries H, Ruys GJ, Groot SPC, Koornneef M (2004) Genetic differences in seed longevity of various Arabidopsis mutants. Physiol Plant 121: 448-461
9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
10. Debeaujon I, Léon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122: 403-414
11. Delouche YC, Baskin C (1973) Accelerated ageing techniques for predicting the relative storability of seeds lots. Seeds Sci Technol 1: 427-452
12. Dinkins RD, Majee SM, Nayak NR, Martin D, Xu Q, Belcastro MP, Houtz RL, Beach CM, Downie AB (2008) Changing transcriptional initiation sites and alternative 59-and 39-splice site selection of the first intron deploys Arabidopsis protein isoaspartyl methyltransferase2 variants to different subcellular compartments. Plant J 55: 1-13
13. Finney DJ (1952) Probit Analysis. Cambridge University Press, Cambridge, UK
14. Finney DJ, Stevens WL (1948) A table for the calculation of working probits and weights in probit analysis. Biometrika 35: 191-201
15. Ingrosso D, D'Angelo S, di Carlo E, Perna AF, Zappia V, Galletti P (2000) Increased methyl esterification of altered aspartyl residues in erythrocyte membrane proteins in response to oxidative stress. Eur J Biochem 267: 4397-4405
16. Johnson BA, Langmack EL, Aswad DW (1987) Partial repair of deamidationdamaged calmodulin by protein carboxyl methyltransferase. J Biol Chem262: 12283-12287
17. Kagan RM, McFadden HJ, McFadden PN, O'Connor C, Clarke S (1997) Molecular phylogenetics of a protein repair methyltransferase. Comp Biochem Physiol B Biochem Mol Biol 117: 379-385
18. Kapoor N, Arya A, Siddiqui MA, Amir A, Kumar H (2010) Seed deterioration in chickpea (Cicer arietinum L.) under accelerated aging. Asian J Plant Sci 9: 158-162
19. Kaur H, Shukla RK, Yadav G, Chattopadhyay D, Majee M (2008) Two divergent genes encoding L-myo-inositol 1-phosphate synthase1 (CaMIPS1) and 2 (CaMIPS2) are differentially expressed in chickpea. Plant Cell Environ 31: 1701-1716
20. Kim E, Lowenson JD, MacLaren DC, Clarke S, Young SG (1997) Deficiency of a protein-repair enzyme results in the accumulation of altered proteins, retardation of growth, and fatal seizures in mice. Proc Natl Acad Sci USA 94: 6132-6137
21. Kindrachuk J, Parent J, Davies GF, Dinsmore M, Attah-Poku S, Napper S (2003) Overexpression of L-isoaspartate O-methyltransferase in Escherichia coli increases heat shock survival by a mechanism independent of methyltransferase activity. J Biol Chem 278: 50880-50886
22. Lanteri S, Nada E, Balleti P, Quagliotti L, Bino RJ (1996) Effects of controlled deterioration and osmoconditioning on germination and nuclear replication in seeds of pepper (Capsicum annuum L.). Ann Bot (Lond) 77: 591-597
23. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948
24. Léon-Kloosterziel KM, van de Bunt GA, Zeevaart JA, Koornneef M (1996) Arabidopsis mutants with a reduced seed dormancy. Plant Physiol 110: 233-240
25. Lowenson JD, Clarke S (1992) Recognition of D aspartyl residues in polypeptides by the erythrocyte L-isoaspartyl/D aspartyl protein methyl transferase: implication for the repair hypothesis. J Biol Chem 276: 5985-5995
26. Majee M, Maitra S, Dastidar KG, Pattnaik S, Chatterjee A, Hait NC, Das KP, Majumder AL (2004) A novel salt-tolerant L-myo-inositol-1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice: molecular cloning, bacterial overexpression, characterization, and functional introgression into tobacco-conferring salt tolerance phenotype. J Biol Chem 279: 28539-28552
27. McFadden PN, Clarke S (1987) Conversion of isoaspartyl peptides to normal peptides: implications for the cellular repair of damaged proteins. Proc Natl Acad Sci USA 84: 2595-2599
28. Mudgett MB, Clarke S (1993) Characterization of plant L-isoaspartyl methyltransferases that may be involved in seed survival: purification, cloning, and sequence analysis of the wheat germ enzyme. Biochemistry 32: 11100-11111
29. Mudgett MB, Clarke S (1994) Hormonal and environmental responsiveness of a developmentally regulated protein repair L-isoaspartyl methyltransferase in wheat. J Biol Chem 269: 25605-25612
30. Mudgett MB, Lowenson JD, Clarke S (1997) Protein repair L-isoaspartyl methyltransferase in plants: phylogenetic distribution and the accumulation of substrate proteins in aged barley seeds. Plant Physiol 115: 1481-1489
31. O'Connor CM (1987) Regulation and subcellular distribution of a protein methyltransferase and its damaged aspartyl substrate sites in developing Xenopus oocytes. J Biol Chem 262: 10398-10403
32. O'Connor CM (2006) Protein L-isoaspartyl, D-aspartyl O-methyl transferase: catalysts of protein repair. In SG Clarke, F Tamanoi, eds, The Enzymes, Vol XXIV. Elsevier, Amsterdam, pp 385-433
33. O'Connor CM, Germain BJ (1987) Kinetic and electrophoretic analysis of transmethylation reactions in intact Xenopus laevis oocytes. J Biol Chem 262: 10404-10411
34. Ogé L, BourdaisG, Bove J, Collet B, Godin B, Granier F, Boutin JP, JobD, Jullien M, Grappin P (2008) Protein repair L-isoaspartyl methyltransferase 1 is involved in both seed longevity and germination vigor in Arabidopsis. Plant Cell 20: 3022-3037
35. Patel K, Borchardt RT (1990) Chemical pathways of peptide degradation. II. Kinetics of deamidation of an asparaginyl residue in a model hexapeptide. Pharm Res 7: 703-711
36. Pourcel L, Routaboul JM, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17: 2966-2980
37. Prieto-Dapena P, Castaño R, Almoguera C, Jordano J (2006) Improved resistance to controlled deterioration in transgenic seeds. Plant Physiol 142: 1102-1112
38. Rajjou L, Debeaujon I (2008) Seed longevity: survival and maintenance of high germination ability of dry seeds. C R Biol 331: 796-805
39. Rajjou L, Lovigny Y, Groot SPC, Belghazi M, Job C, Job D (2008) Proteomewide characterization of seed aging in Arabidopsis: a comparison between artificial and natural aging protocols. Plant Physiol 148: 620-641
40. Shen-Miller J, Mudgett MB, Schopf JW, Clarke S, Berger R (1995) Exceptional seed longevity and robust growth: ancient sacred lotus from China. Am J Bot 82: 1367-1380
41. Smith CD, Carson M, Friedman AM, Skinner MM, Delucas L, Chantalat L, Weise L, Shirasawa T, Chattopadhyay D (2002) Crystal structure of human L-isoaspartyl-O-methyl-transferase with S-adenosyl homocysteine at 1.6-A resolution and modeling of an isoaspartyl-containing peptide at the active site. Protein Sci 11: 625-635
42. Syam Prakash SR, Jayabaskaran C (2006) Expression and localization of calcium-dependent protein kinase isoforms in chickpea. J Plant Physiol 163: 1135-1149
43. TeKrony DM (1995) Accelerated aging. In HA van de Venter, ed, Seed Vigour Testing Seminar. International Seed Testing Association, Zurich, pp 53-73
44. Thapar N, Kim AK, Clarke S (2001) Distinct patterns of expression but similar biochemical properties of protein L-isoaspartyl methyltransferase in higher plants. Plant Physiol 125: 1023-1035
45. Verma P, Singh A, Kaur H, Majee M (2010) Protein L-isoaspartyl methyltransferase1 (CaPIMT1) from chickpea mitigates oxidative stressinduced growth inhibition of Escherichia coli. Planta 231: 329-336
46. Villa ST, Xu Q, Downie AB, Clarke SG (2006) Arabidopsis protein repair L-isoaspartyl methyltransferase: predominant activities at lethal temperatures. Physiol Plant 128: 581-592
47. Visick JE, Cai H, Clarke S (1998) The L-isoaspartyl protein repair methyltransferase enhances survival of aging Escherichia coli subjected to secondary environmental stresses. J Bacteriol 180: 2623-2629
48. Wehmeyer N, Vierling E (2000) The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiol 122: 1099-1108
49. Wharton MJ (1955) The use of tetrazolium test for determining the viability of seeds of the genus Brassica. Proc Int Seed Test Assoc USA 20: 81-88
50. Xu Q, Belcastro MP, Villa ST, Dinkins RD, Clarke SG, Downie AB (2004) A second protein L-isoaspartyl methyltransferase gene in Arabidopsis produces two transcripts whose products are sequestered in the nucleus. Plant Physiol 136: 2652-2664
51. Young AL, Carter WG, Doyle HA, Mamula MJ, Aswad DW (2001) Structural integrity of histone H2B in vivo requires the activity of protein L-isoaspartate O-methyltransferase, a putative protein repair enzyme. J Biol Chem 276: 37161-37165