Secretory phospholipases A2 in durum wheat (Triticum durum Desf.): Gene expression, enzymatic activity, and relation to drought stress adaptation

International Journal of Molecular Sciences

Volumn 14, Issue 3, 2013, Pages 5146-5169

  Verlotta, Angelo ^a   Liberatore, Maria T ^a   Cattivelli, Luigi ^a   Trono, Daniela ^a  

^a ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

Author keywords

Drought stress; Durum wheat; Phospholipase A2

Indexed keywords

LINOLEIC ACID; LINOLENIC ACID; PALMITIC ACID; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 GROUP I; PHOSPHOLIPASE A2 GROUP II; PHOSPHOLIPASE A2 GROUP III; PHOSPHOLIPASE A2 GROUP IV;

ARTICLE; DEVELOPMENTAL STAGE; DROUGHT STRESS; ENZYME ACTIVITY; EVOLUTIONARY ADAPTATION; FATTY ACID ANALYSIS; GENE EXPRESSION; GENE SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYTOCHEMISTRY; PLANT LEAF; PLANT RESPONSE; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; THERMOSTABILITY; TRITIEUM DURUM; VEGETATIVE STAGE; WHEAT;

EID: 84875066834     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14035146     Document Type: Article

References (63)

1. Munnik, T.; Testerink, C. Plant phospholipid signaling: "In a nutshell". J. Lipid Res. 2009, 50, S260-S265.
2. Wang, G.; Ryu, S.; Wang, X. Plant phospholipases: An overview. Methods Mol. Biol. 2012, 861, 123-137.
3. Schaloske, R.H.; Dennis, E.A. The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta 2006, 1761, 1246-1259.
4. Scherer, G.F.E.; Ryu, S.B.; Wang, X.; Matos, A.R.; Heitz, T. Patatin-related phospholipase A: Nomenclature, subfamilies and functions in plants. Trends Plant Sci. 2010, 15, 693-700.
5. Ståhl, U.; Ek, B.; Stymne, S. Purification and characterization of a low-molecular-weight phospholipase A2 from developing seeds of elm. Plant Physiol. 1998, 117, 197-205.
6. Ståhl, U.; Lee, M.; Sjodahl, S.; Archer, D.; Cellini, F.; Ek, B.; Iannacone, N.; MacKenzie, D.; Semeraro, L.; Tramontano, E. et al. Plant low-molecular-weight phospholipase A2s (PLA2s) are structurally related to the animal secretory PLA2s and are present as a family of isoforms in rice (Oryza sativa). Plant Mol. Biol. 1999, 41, 481-490.
7. Domingues, S.J.S.; Souza, T.F.; Soares, A.M.S.; Jacinto, T.; Machado, O.L.T. Activation of phospholipase PLA2 activity in Ricinus communis leaves in response to mechanical wounding. Braz. J. Plant Physiol. 2007, 19, 35-42.
8. Kim, J.Y.; Chung, Y.S.; Ok, S.H.; Lee, S.G.; Chung, W.I.; Kim, I.Y.; Shin, J.S. Characterization of the full-length sequences of phospholipase A2 induced during flower development. Biochim. Biophys. Acta 1999, 1489, 389-392.
9. Lee, H.Y.; Bahn, S.C.; Shin, J.S.; Hwang, I.; Back, K.; Doelling, J.H.; Ryu, S.B. Multiple forms of secretory phospholipase A2 in plants. Prog. Lipid Res. 2005, 44, 52-67.
10. Mariani, M.E.; Villarreal, M.A.; Cheung, F.; Leiva, E.P.; Madoery, R.R.; Fidelio, G.D. In silico and in vitro characterization of phospholipase A2 isoforms from soybean (Glycine max). Biochimie 2012, 94, 2608-2619.
11. Matos, A.R.; Pham-Thi, A.-T. Lipid deacylating enzymes in plants: Old activities, new genes. Plant Physiol. Biochem. 2009, 47, 491-503.
12. Reina-Pinto, J.J.; Voisin, D.; Kurdyukov, S.; Faust, A.; Haslam, R.P.; Michaelson, L.V.; Efremova, N.; Franke, B.; Schreiber, L.; Napier, J.A. et al. Misexpression of FATTY ACID ELONGATION1 in the Arabidopsis epidermis induces cell death and suggests a critical role for phospholipase A2 in this process. Plant Cell 2009, 21, 1252-1272.
13. Gustavsson, M.H.; Sommarin, M. Characterization of a plasma membrane-associated phospholipase A2 activity increased in response to cold acclimation. J. Plant Physiol. 2002, 159, 1219-1227.
14. Holk, A.; Rietz, S.; Zahn, M.; Quader, H.; Scherer, G.F.E. Molecular identification of cytosolic, patatin-related phospholipases A from Arabidopsis with potential functions in plant signal transduction. Plant Physiol. 2002, 130, 90-101.
15. Rietz, S.; Dermendjiev, G.; Oppermann, E.; Tafesse, F.G.; Effendi, Y.; Holk, A.; Parkera, J.E.; Teige, M.; Scherer, G.F.E. Roles of Arabidopsis patatin-related phospholipases A in root development are related to auxin responses and phosphate deficiency. Mol. Plant 2010, 3, 525-538.
16. Li, M.; Bahn, S.C.; Guo, L.; Musgrave, W.; Berg, H.; Welti, R.; Wang, X. Patatin-related phospholipase pPLAIIIβ-induced changes in lipid metabolism alter cellulose content and cell elongation in Arabidopsis. Plant Cell 2011, 23, 1107-1123.
17. Lee, H.Y.; Bahn, S.C.; Kang, Y.-M.; Lee, K.H.; Kim, H.J.; Noh, E.K.; Palta, J.P.; Shin, J.S.; Ryu, S.B. Secretory low molecular weight phospholipase A2 plays important roles in cell elongation and shoot gravitropism in Arabidopsis. Plant Cell 2003, 15, 1990-2002.
18. Seo, J.; Lee, H.Y.; Choi, H.; Choi, Y.; Lee, Y.; Kim, Y.-W.; Ryu, S.B.; Lee, Y. Phospholipase A2β mediates light-induced stomatal opening in Arabidopsis. J. Exp. Bot. 2008, 59, 3587-3594.
19. Lee, O.R.; Kim, S.J.; Kim, H.J.; Hong, J.K.; Ryu, S.B.; Lee, S.H.; Ganguli, A.; Cho, H.-T. Phospholipase A2 is required for PIN-FORMED protein trafficking to the plasma membrane in the Arabidopsis root. Plant Cell 2010, 22, 1812-1825.
20. Kim, H.J.; Ok, S.H.; Bahn, S.C.; Jang, J.; Oh, S.A.; Park, S.K.; Twell, D.; Ryu, S.B.; Shin, J.S. Endoplasmic reticulum- and Golgi-localized phospholipase A2 plays critical roles in Arabidopsis pollen development and germination. Plant Cell 2011, 23, 94-110.
21. Jung, J.; Kumar, K.; Lee, H.Y.; Park, Y., II; Cho, H.-T.; Ryu, S.B. Translocation of phospholipase A2α to apoplasts is modulated by developmental stages and bacterial infection in Arabidopsis. Front. Plant Sci. 2012, doi:10.3389/fpls.2012.00126.
22. Heinze, M.; Herre, M.; Massalski, C.; Hermann, I.; Conrad, U.; Roos, W. Signal transfer in the plant plasma membrane: Phospholipase A2 is regulated via an inhibitory Gα protein and a cyclophilin. Biochem. J. 2012, doi:10.1042/BJ20120793.
23. Ryu, S.B.; Lee, H.Y.; Hwang, I.W.; Jiwan, P.P. Transgenic plants with increased resistance to biotic and abiotic stresses and accelerated flowering time due to overexpression of a secretory phospholipase A2 (sPLA2). PCT Int. Appl. Patent US2010/0100984A1, 22 April 2010.
24. Singh, A.; Baranwal, V.; Shankar, A.; Kanwar, P.; Ranjan, R.; Yadav, S.; Pandey, A.; Kapoor, S.; Pandey, G.K. Rice phospholipase A superfamily: Organization, phylogenetic and expression analysis during abiotic stresses and development. PLoS One 2012, 7, e30947.
25. Elias, E.M.; Manthey, F.A. End products: present and future uses. In Durum Wheat Breeding: Current Approaches and Future Strategies; Royo, C., Nachit, M.M., di Fonzo, N., Araus, J.L., Pfeiffer, W.H., Slafer, G.A., Eds.; Food Products Press: New York, NY, USA, 2005; Volume 1, pp. 63-86.
26. Mansfeld, J. Plant phospholipases A2: Perspectives on biotechnological applications. Biotechnol. Lett. 2009, 31, 1373-1380.
27. NCBI Conserved Domain Database. Available online: http://www.ncbi.nlm.nih.gov/Structure/cdd/cdd.shtml (accessed on 12 March 2012).
28. Yang, H.-C.; Mosior, M.; Johnson, C.A.; Chen, Y.; Dennis, E.A. Group-specific assays that distinguish between the four major types of mammalian phospholipase A2. Anal. Biochem. 1999, 269, 278-288.
29. Winget, J.M.; Pan, Y.H.; Bahnson, B.J. The interfacial binding surface of phospholipase A2s. Biochim. Biophys. Acta 2006, 1761, 1260-1269.
30. URGI Wheat Sequence Repository. Available online: http://urgi.versailles.inra.fr/Species/Wheat/Sequence-Repository (accessed on 10 September 2012).
31. Ježek, J.; Jabůrek, M.; Zelenka, J.; Ježek, P. Mitochondrial phospholipase A2 activated by reactive oxygen species in heart mitochondria induces mild uncoupling. Physiol. Res. 2010, 59, 737-747.
32. Trono, D.; Soccio, M.; Laus, M.N.; Pastore D. The existence of phospholipase A2 activity in plan mitochondria and its activation by hyperosmotic stress in durum wheat (Triticum durum Desf.). Plant Sci. 2013, 199-200, 91-102.
33. Fujikawa, Y.; Fujikawa, R.; Iijima, N.; Esaka, M. Characterization of secretory phospholipase A2 with phospholipase A1 activity in tobacco, Nicotiana tabacum (L.) Lipids 2012, 47, 303-312.
34. Mansfeld, J.; Ulbrich-Hofmann, R. Secretory phospholipase A2α from Arabidopsis thaliana: Functional parameters and substrate preference. Chem. Phys. Lipids 2007, 150, 156-166.
35. Fujikawa, R.; Fujikawa, Y.; Iijima, N.; Esaka, M. Molecular cloning, expression, and characterization of secretory phospholipase A2 in tobacco. Lipids 2005, 40, 901-908.
36. AOCS Lipid Library. Available online: http://lipidlibrary.aocs.org (accessed on 25 October 2012).
37. Bahn, S.C.; Lee, H.Y.; Kim, H.J.; Ryu, S.B.; Shin, J.S. Characterization of Arabidopsis secretory phospholipase A2-γ cDNA and its enzymatic properties. FEBS Lett. 2003, 553, 113-118.
38. Jung, K.M.; Kim, D.K. Purification and characterization of a membrane-associated 48-kilodalton phospholipase A2 in leaves of broad bean. Plant Physiol. 2000, 123, 1057-1068.
39. Rietz, S.; Holk, A.; Scherer, G.F.E. Expression of the patatin related phospholipase A gene AtPLA IIA in Arabidopsis thaliana is up-regulated by salicylic acid, wounding, ethylene, and iron and phosphate deficiency. Planta 2004, 219, 743-753.
40. Boyer, J.S. Plant productivity and environment. Science 1982, 218, 443-448.
41. Passioura, J.B.; Condon, A.G.; Richards, R.A. Water deficits, the development of leaf area and crop productivity. In Water Deficits Plant Responses from Cell to Community; Smith, J.A.C., Griffiths, H., Eds.; BIOS Scientific Publishers limited: Oxford, UK, 1993; pp. 253-264.
42. Kader, M.A.; Lindberg, S. Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav. 2010, 5, 233-238.
43. Reddy, A.S.N. Calcium: Silver bullet in signaling. Plant Sci. 2001, 160, 381-404.
44. Schachtman, D.P.; Goodger, J.Q.D. Chemical root to shoot signalling under drought. Trends Plant Sci. 2008, 13, 281-287.
45. Felle, H.H.; Herrmann, A.; Hückelhoven, R.; Kogel, K.-H. Root-to-shoot signalling: apoplastic alkalinization, a general stress response and defence factor in barley (Hordeum vulgare). Protoplasma 2005, 227, 17-24.
46. Sahsah, Y.; Campos, P.; Gareil, M.; Zuily-Fodil, Y.; Pham-Thi, A.T. Enzymatic degradation of polar lipids in Vigna unguiculata leaves and influence of drought stress. Physiol. Plant. 1998, 104, 577-586.
47. Matos, A.R.; d'Arcy-Lameta, A.; França, M.; Pêtres, S.; Edelman, L.; Kader, J.; Zuily-Fodil, Y.; Pham-Thi, A.T. A novel patatin-like gene stimulated by drought stress encodes a galactolipid acyl hydrolase. FEBS Lett. 2001, 491, 188-192.
48. Matos, A.R.; Gigon, A.; Laffray, D.; Petrês, S.; Zuily-Fodil, Y.; Pham-Thi, A.T. Effects of progressive drought stress on the expression of patatin-like lipid acyl hydrolase genes in Arabidopsis leaves. Physiol. Plant. 2008, 134, 110-120.
49. Alferez, F.; Lluch, Y.; Burns, J.K. Phospholipase A2 and postharvest peel pitting in citrus fruit. Postharv. Biol. Technol. 2008, 49, 69-76.
50. Liao, H.-L.; Burns, J.K. Light controls phospholipase A2α and β gene expression in Citrus sinensis. J. Exp. Bot. 2010, 61, 2469-2478.
51. Navari-Izzo, F.; Milone, M.T.; Quartacci, M.F.; Pinzini, C. Metabolic changes in wheat plants subjected to a water-deficit stress programme. Plant Sci. 1993, 92, 151-157.
52. Quartacci, M.F.; Pinzino, C.; Sgherri, C.L.M.; Navari-Izzo, F. Lipid composition and protein dynamics in thylakoids of two wheat cultivars differently sensitive to drought. Plant Physiol. 1995, 108, 191-197.
53. Weber, H. Fatty acid-derived signals in plants. Trends Plant Sci. 2002, 7, 217-224.
54. Lehmann, J.; Atzorn, R.; Brückner, C.; Reinbothe, S.; Leopold, J.; Wasternack, C. Accumulation of jasmonate, abscisic acid, specific transcripts and proteins in osmotically stressed barley leaf segments. Planta 1995, 1, 156-162.
55. Walia, H.; Wilson, C.; Condamine, P.; Liu, X.; Ismail, A.M.; Closem, T.J. Large-scale expression profiling and physiological characterization of jasmonic acid mediated adaptation of barley to salinity stress. Plant Cell Environ. 2007, 30, 410-421.
56. Rice Annotation Project Database. Available online: http://rapdb.dna.affrc.go.jp (accessed on 10 May 2011).
57. ExPASy ProtParam tool. Available online: http://web.expasy.org/protparam/ (accessed on 21 February 2012).
58. iPSORT. Available online: http://ipsort.hgc.jp (accessed on 20 March 2012).
59. TargetP. Available online: http://www.cbs.dtu.dk/services/TargetP (accessed on 20 March 2012).
60. Predotar. Available online: http://urgi.versailles.inra.fr/predotar/predotar.html (accessed on 20 March 2012).
61. Harris, D.A. Spectrophotometric assays. In Spectrophotometry and Spectrofluorimetry: A Practical Approach; Bashford, C.L., Harris, D.A., Eds.; IRL Press: Oxford, UK, 1987; pp. 59-61.
62. Pastore, D.; Trono, D.; Padalino, L.; Simone, S.; Valenti, D.; Di Fonzo, N.; Passarella, S. Inhibition by α-tocopherol and L-ascorbate of linoleate hydroperoxidation and β-carotene bleaching activities in durum wheat semolina. J. Cereal Sci. 2000, 31, 41-54.
63. Gambacorta, G.; Sinigaglia, M.; Schena, A.; Baiano, A.; Lamacchia, C.; Pati, S.; La Notte, E. Changes in free fatty acid and diacylglycerol compounds in short-ripening dry-cured sausage. J. Food Lipids 2009, 16, 1-18.