Arabidopsis lipocalins AtCHL and AtTIL have distinct but overlapping functions essential for lipid protection and seed longevity

Plant, Cell and Environment

Volumn 37, Issue 2, 2014, Pages 368-381

  Boca, Simona ^a,b,c   Koestler, Fleur ^d   Ksas, Brigitte ^a,b,c   Chevalier, Anne ^a,b,c   Leymarie, Juliette ^e   Fekete, Agnes ^d   Mueller, Martin J ^d   Havaux, Michel ^a,b,c  

^a IRFM   (France)

^b CNRS   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

Lipid peroxidation; Lipidomics; Oxidative stress.

Indexed keywords

DICOTYLEDON; ENVIRONMENTAL STRESS; FUNCTIONAL ROLE; LIGAND; LIPID; LONGEVITY; PHYTOCHEMISTRY; PROTEIN; SEED PRODUCTION; SURVIVAL; TOLERANCE;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS);

ARABIDOPSIS PROTEIN; AT5G58070 PROTEIN, ARABIDOPSIS; CHL PROTEIN, ARABIDOPSIS; LIPOCALIN;

ARABIDOPSIS; ARTICLE; DROUGHT; GENETICS; HEAT; LIGHT; LIPID PEROXIDATION; LIPIDOMICS; OXIDATIVE STRESS; OXIDATIVE STRESS.; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT SEED; RADIATION EXPOSURE;

LIPID PEROXIDATION; LIPIDOMICS; OXIDATIVE STRESS.;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DROUGHTS; HOT TEMPERATURE; LIGHT; LIPID PEROXIDATION; LIPOCALINS; OXIDATIVE STRESS; SEEDS; STRESS, PHYSIOLOGICAL;

EID: 84891625408     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12159     Document Type: Article

References (62)

1. Asada K. (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391-396.
2. Bhatia S., Knoch B., Wong J., Kim W.S., Else P.L., Oakley A.J. & Garner B. (2012) Selective reduction of hydroperoxyeicosatetranoic acids to their hydroxy derivatives by apolipoprotein D: implications for lipid antioxidant activity and Alzheimer's disease. Biochemical Journal 442, 713-721.
3. Birtic S., Ksas B., Genty B., Mueller M.J., Triantaphylidès C. & Havaux M. (2011) Using spontaneous photon emission to image lipid oxidation patterns in plant tissues. Plant Journal 67, 1103-1115.
4. Bonomini F., Filippini F., Hayek T., Aviram M., Keidar S., Rodella L.F., Coleman R. & Rezzani R. (2010) Apolipoprotein E and its role in aging and survival. Experimental Gerontology 45, 149-157.
5. Bratt T. (2000) Lipocalins and cancer. Biochimica et Biophysica Acta 1482, 318-326.
6. Bugos R.C., Hieber A.D. & Yamamoto H.Y. (1998) Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. Journal of Biological Chemistry 273, 15321-15324.
7. Charron J.B., Ouellet F., Pelletier H., Danyluk J., Chauve C. & Sarhan F. (2005) Identification, expression, and evolutionary analyses of plant lipocalins. Plant Physiology 139, 2017-2028.
8. Charron J.B., Ouellet F., Houde M. & Sarhan F. (2008) The plant apolipoprotein D ortholog protects Arabidopsis against oxidative stress. BMC Plant Biology 8, 86.
9. Châtelain E., Satour P., Laugier E., Ly Vu B., Payet N., Rey P. & Montrichard F. (2013) Evidence for the participation of the methionine sulfoxide reductase repair system in plant seed longevity. Proceedings of the National Academy of Sciences United States of America 110, 3633-3638.
10. Chi W.T., Fung R.W., Liu H.C., Hsu C.C. & Chamg Y.Y. (2009) Temperature-induced lipocalin is required for basal and acquired thermotolerance in Arabidopsis. Plant Cell and Environment 32, 917-927.
11. Cordray P., Doyle K., Edes K., Moos P.J. & Fitzpatrick F.A. (2007) Oxidation of 2-Cys-peroxiredoxins by arachidonic acid peroxide metabolites of lipoxygenases and cyclooxygenase-2. Journal of Biological Chemistry 282, 32623-32629.
12. Delouche J.C. & Baskin C.C. (1973) Accelerated aging techniques for predicting the relative storability of seed lots. Seed Science and Technology 1, 427-452.
13. Farmer E.E. & Davoine C. (2007) Reactive electrophile species. Current Opinion in Plant Biology 10, 380-386.
14. Farmer E.E. & Mueller M.J. (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annual Review of Plant Biology 64, 429-450. doi:10.1146/annurev-arplant-050312-120132.
15. Fernandez-Robredo P., Recalde S., Arnaiz G., Moreno-Orduna M., Salinas-Alaman A., Sadaba L.M. & Garcia-Layana A. (2009) Effect of zeaxanthin and antioxidant supplementation on vascular endothelial growth factor (VEGF) expression in apolipoprotein-E deficient mice. Current Eye Research 34, 543-552.
16. Flower D.R. (1996) The lipocalin protein family: structure and function. Biochemical Journal 318, 1-14.
17. Flower D.R., North A.C.T. & Sansom C.E. (2000) The lipocalin protein family: structural and sequence overview. Biochimica et Biophysica Acta 1482, 9-24.
18. Ganfornina M.D., Do Carmo S., Lora J.M., Torres-schumann S., Vogel M., Allhorn M., Gonzalez C., Bastiani M.J., Rassart E. & Sanchez D. (2008) Apolipoprotein D is involved in the mechanisms regulating protection from oxidative stress. Aging Cell 7, 506-515.
19. Garner B., Waldeck A.R., Witting P.K., Rye K.-A. & Stocker R. (1998) Oxidation of high density OK, Abduragimov lipoproteins. II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. Journal of Biological Chemistry 273, 6088-6095.
20. Gasymov A.R., Prasher P., Yisifov T.N. & Glasgow B.J. (2005) Tear lipocalin: evidence for a scavenging function to remove lipids from the human corneal surface. Investigative Ophthalmology & Visual Science 46, 3589-3596.
21. Gillet B., Beyly A., Peltier G. & Rey P. (1998) Molecular characterization of CDSP 34, a chloroplastic protein induced by water deficit in Solanum tuberosum L. plants, and regulation of CDSP 34 expression by ABA and high illumination. Plant Journal 16, 257-262.
22. Grzyb J., Latowski D. & Strzalka K. (2006) Lipocalins - a family portrait. Journal of Plant Physiology 163, 895-915.
23. Hager A. & Holocher K. (1994) Localization of the xanthophyll-cycle enzyme violaxanthin de-epoxidase within the thylakoid lumen and abolition of its mobility by a (light-dependent) pH decrease. Planta 192, 581-589.
24. Harman G.E. & Mattick L.R. (1976) Association of lipid oxidation with seed aging and death. Nature 260, 323-324.
25. Havaux M. (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science 3, 147-151.
26. Havaux M. (2003) Spontaneous and thermoinduced photon emission: new methods to detect and quantify oxidative stress in plants. Trends in Plant Science 8, 409-413.
27. Havaux M. & Niyogi K.K. (1999) The violaxanthin cycle protects plants from photo-oxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences United States of America 96, 8762-8767.
28. Havaux M., Eymery F., Porfirova S., Rey P. & Doermann P. (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. The Plant Cell 17, 3451-3469.
29. Kar R.K. (2011) Plant responses to water stress. Role of reactive oxygen species. Plant Signaling and Behavior 6, 1741-1745.
30. Kjellsen T.D., Shiryaeva L., Schröder W.P. & Strimbeck G.R. (2010) Proteomics of extreme freezing tolerance in Siberian spruce (Picea obovata). Journal of Proteomics 73, 965-975.
31. Kosmala A., Perlikowski D., Pawlowicz I. & Rapacz M. (2012) Changes in the chloroplast proteome following water deficit and subsequent watering in a high- and a low-drought-tolerant genotype of Festuca arundinacea. Journal of Experimental Botany 63, 6161-6172.
32. Lechner M., Wojnar P. & Redl B. (2001) Human tear lipocalin acts as an oxidative-stress-induced scavenger of potentially harmful lipid peroxidation products in a cell culture system. Biochemical Journal 356, 129-135.
33. Levesque-Tremblay G., Havaux M. & Ouellet F. (2009) The chloroplastic lipocalin AtCHL prevents lipid peroxidation and protects Arabidopsis against oxidative stress. Plant Journal 60, 691-702.
34. Magistretti P.S. & Pellerin L. (1996) Cellular mechanisms of brain energy metabolism. Relevance to functional brain imaging and to neurodegenerative disorders. Annals of the New York Academy of Sciences 777, 380-387.
35. Mano J., Belles-Boix E., Babiychuk E., Inze D., Torii Y., Hiraoka E., Takimoto K., Slooten L., Asada K. & Kushnir S. (2005) Protection against photooxidative injury of tobacco leaves by 2-alkenal reductase. Detoxication of lipid peroxide-derived reactive carbonyls. Plant Physiology 139, 1773-1783.
36. Miller G., Suzuki N., Ciftci-Yilmaz S. & Mittler R. (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell and Environment 33, 453-476.
37. Montillet J.L., Cacas J.L., Garnier L., etal. (2004) The upstream oxylipin profile of Arabidopsis thaliana: a tool to scan for oxidative stresses. Plant Journal 40, 439-451.
38. Mueller M.J. & Berger S. (2009) Reactive electrophile species: pattern recognition and signalling. Phytochemistry 70, 1511-1521.
39. Muffat J., Walker D.W. & Benzer S. (2008) Human ApoD, an apolipoprotein up-regulated in neurodegenerative diseases, extends lifespan and increases stress resistance in Drosophila. Proceedings of the National Academy of Sciences United States of America 105, 7088-7093.
40. Munné-Bosch S. (2007) Alpha-tocopherol: a multifaceted molecule in plants. Vitamins & Hormones 76, 375-392.
41. Navarro A., del Valle E., Juarez A., Martinez E., Ordonez C., Astudillo A. & Tolivia J. (2010) Apolipoprotein D synthesis progressively increases in frontal cortex during human lifespan. Age 32, 85-96.
42. Nebel A., Kleindorp R., Caliebe A., etal. (2011) A genome-wide association study confirms APOE as the major gene influencing survival in long-lived individuals. Mechanisms of Ageing and Development 132, 324-330.
43. Niyogi K.K., Grossman A.R. & Björkman O. (1998) Arabidopsis mutants define a central role for the xanthophylls cycle in the regulation of photosynthetic energy conversion. The Plant Cell 10, 1121-1134.
44. Pamplona R. (2008) Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity. Biochimica et Biophysica Acta 1777, 1249-1262.
45. Penuelas J. & Munné-Bosch S. (2005) Isoprenoids: an evolutionary pool for photoprotection. Trends in Plant Science 10, 166-169.
46. Porfirova S., Bergmüller E., Tropf S., Lemke R. & Dörmann P. (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proceedings of the National Academy of Sciences United States of America 99, 12495-12500.
47. Rajjou L. & Debeaujon I. (2008) Seed longevity: survival and maintenance of high germination ability of dry seeds. Comptes Rendus Biologies 331, 796-805.
48. Ramel F., Birtic S., Cuiné S., Triantaphylidès C., Ravanat J.L. & Havaux M. (2012) Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiology 158, 1267-1278.
49. Rassart E., Bedirian A., Do Carmo S., Guinard O., Sirois J., Terrisse L. & Milne R. (2000) Apolipoprotein D. Biochimica et Biophysica Acta 1482, 185-198.
50. Ruiz M., Wicker-Thomas C., Sanchez D. & Ganfornina M.D. (2012) Grasshopper Lazarillo, a GPI-anchored lipocalin, increases Drosophila longevity and stress resistance, and functionally replaces its secreted homolog Nlaz. Insect Biochemistry and Molecular Biology 42, 776-789.
51. Sanchez D., López-Arias B., Torroja L., Canal I., Wang X., Bastiani M.J. & Ganfornina M.D. (2006) Loss of glial Lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Current Biology 16, 680-686.
52. Sattler S.E., Gilliland L.U., Magallanes-Lundback M., Pollard M. & DellaPenna D. (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. The Plant Cell 16, 1419-1432.
53. Stiti N., Missihoun T.D., Kotchoni S.O., Kirch H.-H. & Bartels D. (2011) Aldehyde dehydrogenases in Arabidopsis thaliana: biochemical requirements, metabolic pathways, and functional analysis. Frontiers in Plant Science 2, 65.
54. Terrisse L., Poirier J., Bertrand P., Merched A., Visvikis S., Siest G., Milne R. & Rassart E. (1998) Increased levels of apolipoprotein D in cerebrospinal fluid and hippocampus of Alzheimer's patients. Journal of Neurochemistry 71, 1643-1650.
55. Tesnier K., Strookman-Donkers H.M., Van Pijlen J.G., Van der Geest A., Bino R.J. & Groot S. (2002) A controlled deterioration test for Arabidopsis thaliana reveals genetic variation in seed quality. Seed Science and Technology 30, 149-165.
56. Vieira Dos Santos C., Cuiné S., Rouhier N. & Rey P. (2005) The Arabidopsis plastidic methionine sulfoxide reductase B proteins. Sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A, and induction by photooxidative stress. Plant Physiology 138, 909-922.
57. Virtanen T. (2001) Lipocalin allergens. Allergy 56 (Suppl 67), 48-51.
58. Vogt M. & Skerra A. (2004) Construction of an artificial receptor protein ('anticalin') based on the human apolipoprotein D. Chembiochem 5, 191-199.
59. Walker D.W., Muffat J., Rundel C. & Benzer S. (2006) Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Current Biology 16, 674-679.
60. Xu S. & Venge P. (2000) Lipocalins as biochemical markers of disease. Biochimica et Biophysica Acta 1482, 298-307.
61. Zhang C., Ding Z., Xu X., Wang Q., Qin G. & Tian S. (2010) Crucial roles of membrane stability and its related proteins in the tolerance of peach fruit to chilling injury. Amino Acids 39, 181-194.
62. Zoeller M., Stingl N., Krischke M., Fekete A., Waller F., Berger S. & Mueller M.J. (2012) Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiology 160, 365-378.