Physiological and proteomic analyses of drought stress response in Holm oak provenances

Journal of Proteome Research

Volumn 12, Issue 11, 2013, Pages 5110-5123

  Valero Galván, José ^a,b   González Fernández, Raquel ^b   Navarro Cerrillo, Rafael Ma ^b   Gil Pelegrín, Eustaquio ^c   Jorrín Novo, Jesús V ^b  

^a UNIVERSIDAD AUTÓNOMA DE CIUDAD JUÁREZ   (Mexico)

^b UNIVERSITY OF CÓRDOBA   (Spain)

^c Agrifood Institute of Aragón IA2   (Spain)

Author keywords

biomass; chlorophyll fluorescence; drought stress in Holm oak; Holm oak proteomics; Quercus ilex; water potential

Indexed keywords

PROTEOME;

ARTICLE; CHLOROPLAST; CONTROLLED STUDY; DROUGHT STRESS; DROUGHT TOLERANCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; OAK; PHOTOSYNTHESIS; PHOTOSYSTEM II; PLANT DEFENSE; PLANT LEAF; PLANT ROOT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEOMICS; QUANTUM CHEMISTRY; SEEDLING; SOIL; SPAIN; TWO DIMENSIONAL ELECTROPHORESIS; WATER CONTENT; XYLEM;

ANALYSIS OF VARIANCE; DROUGHTS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, PLANT; PLANT LEAVES; PLANT PROTEINS; PROTEOMICS; QUERCUS; SEEDLING; SPAIN; STRESS, PHYSIOLOGICAL; TANDEM MASS SPECTROMETRY;

EID: 84887232060     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400591n     Document Type: Article

References (69)

1. Newman, B. D.; Wilcox, B. P.; Archer, S. R.; Breshears, D. D.; Dahm, C. N.; Duffy, C. J.; McDowell, N. G.; Phillips, F. M.; Scanlon, B. R.; Vivoni, E. R. Ecohydrology of water-limited environments: A scientific vision Water Resour. Res. 2006, 42 (6) W06302
2. Hogg, E. H.; Brandt, J. P.; Kochtubajda, B. Factors affecting interannual variation in growth of western Canadian aspen forests during 1951-2000 Can. J. For. Res. 2005, 35 (3) 610-622
3. van Mantgem, P. J.; Stephenson, N. L.; Byrne, J. C.; Daniels, L. D.; Franklin, J. F.; Fulé, P. Z.; Harmon, M. E.; Larson, A. J.; Smith, J. M.; Taylor, A. H.; Veblen, T. T. Widespread Increase of Tree Mortality Rates in the Western United States Science 2009, 323 (5913) 521-524
4. Giorgi, F.; Lionello, P. Climate change projections for the Mediterranean region Global Planet. Change 2008, 63 (2-3) 90-104
5. Lionello, P.; Malanotte-Rizzoli, P.; Boscolo, R.; Alpert, P.; Artale, V.; Li, L.; Luterbacher, J.; May, W.; Trigo, R.; Tsimplis, M.; Ulbrich, U.; Xoplaki, E., The Mediterranean climate: An Overview of the Main Characteristics and Issues. In Developments in Earth and Environmental Sciences; Lionello, P. M.-R.; Boscolo, R., Eds.; Elsevier: Amsterdam, 2006; Vol. 4, pp 1-26.
6. Giorgi, F. Climate change hot-spots Geophys. Res. Lett. 2006, 33 (8) L08707
7. Pulido, F. J.; Díaz, M.; Hidalgo de Trucios, S. J. Size structure and regeneration of Spanish holm oak Quercus ilex forests and dehesas: effects of agroforestry use on their long-term sustainability For. Ecol. Manage. 2001, 146 (1-3) 1-13
8. Gea-Izquierdo, G.; Cañellas, I.; Montero, G. Acorn production in Spanish holm oak woodlands Invest. Agrar: Sist. Recur. For. 2006, 15, 339-354
9. Sánchez, M. E.; Caetano, P.; Ferraz, J.; Trapero, A. Phytophthora disease of Quercus ilex in south-western Spain For. Pathol. 2002, 32 (1) 5-18
10. de Sampaio e Paiva Camilo-Alves, C.; Clara, M.; Almeida Ribeiro, N. Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review Eur. J. For. Res. 2013, 132 (3) 411-432
11. Gallego, F. J.; de Algaba, A. P.; Fernandez-Escobar, R. Etiology of oak decline in Spain Eur. J. For. Res. 1999, 29 (1) 17-27
12. Acherar, M.; Rambal, S. Comparative water relations of four Mediterranean oak species Vegetation 1992, 99-100 (1) 177-184
13. David, T.; Henriques, M.; Kurz-Besson, C.; Nunes, J.; Valente, F.; Vaz, M.; Pereira, J.; Siegwolf, R.; Chaves, M.; Gazarini, L.; David, J. Water-use strategies in two co-occurring Mediterranean evergreen oaks: surviving the summer drought Tree Physiol. 2007, 27, 793-803
14. Mediavilla, S.; Escudero, A. Stomatal responses to drought at a Mediterranean site: a comparative study of co-occurring woody species differing in leaf longevity Tree Physiol. 2003, 23 (14) 987-996
15. Ramírez-Valiente, J. A.; Valladares, F.; Gil, L.; Aranda, I. Population differences in juvenile survival under increasing drought are mediated by seed size in cork oak (Quercus suber L.) For. Ecol. Manage. 2009, 257 (8) 1676-1683
16. Baeza, M.; Pastor, A.; Martín, J.; Ibáñez, M. Mortalidad post-implantación en repoblaciones de Pinus halepenesis, Quercus ilex, Ceratonia siliqua y Tetraclinis articulata en la provincia de Alicante Studia Oecol. 1991, 139-146
17. Villar-Salvador, P.; Planelles, R.; Enríquez, E.; Rubira, J. P. Nursery cultivation regimes, plant functional attributes, and field performance relationships in the Mediterranean oak Quercus ilex L For. Ecol. Manage. 2004, 196 (2-3) 257-266
18. Corcuera, L.; Camarero, J. J.; Gil-Pelegrín, E. Effects of a severe drought on Quercus ilex radial growth and xylem anatomy Trees 2004, 18 (1) 83-92
19. Peguero-Pina, J.; Morales, F.; Flexas, J.; Gil-Pelegrín, E.; Moya, I. Photochemistry, remotely sensed physiological reflectance index and de-epoxidation state of the xanthophyll cycle in Quercus coccifera under intense drought Oecologia 2008, 156 (1) 1-11
20. Vilagrosa, A.; Morales, F.; Abadía, A.; Bellot, J.; Cochard, H.; Gil-Pelegrin, E. Are symplast tolerance to intense drought conditions and xylem vulnerability to cavitation coordinated? An integrated analysis of photosynthetic, hydraulic and leaf level processes in two Mediterranean drought-resistant species Environ. Exp. Bot. 2010, 69 (3) 233-242
21. Corcuera, L.; Morales, F.; Abadia, A.; Gil-Pelegrin, E. Seasonal changes in photosynthesis and photoprotection in a Quercus ilex subsp. ballota woodland located in its upper altitudinal extreme in the Iberian Peninsula Tree Physiol. 2005, 25 (5) 599-608
22. Echevarría-Zomeño, S.; Ariza, D.; Jorge, I.; Lenz, C.; Del Campo, A.; Jorrin, J. V.; Navarro, R. M. Changes in the protein profile of Quercus ilex leaves in response to drought stress and recovery J. Plant Physiol. 2009, 166 (3) 233-45
23. Peguero-Pina, J. J.; Sancho-Knapik, D.; Morales, F.; Flexas, J.; Gil-Pelegrín, E. Differential photosynthetic performance and photoprotection mechanisms of three Mediterranean evergreen oaks under severe drought stress Funct. Plant Biol. 2009, 36, 453-462
24. Bahrman, N.; Petit, R. J. Genetic polymorphism in maritime pine (Pinus pinaster Ait.) assessed by two-dimensional gel electrophoresis of needle, bud, and pollen proteins J. Mol. Evol. 1995, 41 (2) 231-237
25. Basha, S. M. Identification of Cultivar Differences in Seed Polypeptide Composition of Peanuts (Arachis hypogaea L.) by Two-Dimensional Polyacrylamide Gel Electrophoresis Plant Physiol. 1979, 63 (2) 301-6
26. Chevalier, F.; Martin, O.; Rofidal, V.; Devauchelle, A. D.; Barteau, S.; Sommerer, N.; Rossignol, M. Proteomic investigation of natural variation between Arabidopsis ecotypes Proteomics 2004, 4 (5) 1372-81
27. Emre, IÌ. Electrophoretic analysis of some Lathyrus L. species based on seed storage proteins Genet. Resour. Crop Evol. 2009, 56 (1) 31-38
28. Abril, N.; Gion, J. M.; Kerner, R.; Müller-Starck, G.; Cerrillo, R.; Plomion, C.; Renaut, J.; Valledor, L.; Jorrin-Novo, J. Proteomics research on forest trees, the most recalcitrant and orphan plant species Phytochemistry 2011, 72 (10) 1219-1242
29. Jorrín-Novo, J. V.; Maldonado, A. M.; Echevarría- Zomeño, S.; Valledor, L.; Castillejo, M. A.; Curto, M.; Valero, J.; Sghaier, B.; Donoso, G.; Redondo, I. Plant proteomics update (2007-2008): Second-generation proteomic techniques, an appropriate experimental design, and data analysis to fulfill MIAPE standards, increase plant proteome coverage and expand biological knowledge J. Proteomics 2009, 72 (3) 285-314
30. Valero-Galván, J.; Valledor, L.; González-Fernández, R.; Navarro-Cerrillo, R.; Jorrín-Novo, J. V. Proteomic analysis of Holm oak (Quercus ilex subsp. ballota [Desf.] Samp.) pollen J. Proteomics 2012, 75 (9) 2736-2744
31. Valero-Galván, J.; Valledor, L.; Navarro-Cerrillo, R.; Gil-Pelegrín, E.; Jorrín-Novo, J. V. Studies of variability in Holm oak (Quercus ilex subsp. ballota [Desf.] Samp.) through acorn protein profile analysis J. Proteomics 2011, 74, 1244-1255
32. Hamanishi, E.; Campbell, M. Genome-wide responses to drought in forest trees Forestry 2011, 84 (3) 273-283
33. Kosová, K.; Vítámvás, P.; Prášil, I.; Renaut, J. Plant proteome changes under abiotic stress-Contribution of proteomics studies to understanding plant stress response J. Proteomics 2011, 74 (8) 1301-1322
34. Martín, M.; Navarro-Cerrillo, R.; Ortega, P.; Alvarez, J. The use of cotyledon proteins to assess the genetic diversity in sweet holm oak J. For. Sci. 2009, 55 (11) 526-531
35. Sergeant, K.; Spieß, N.; Renaut, J.; Wilhelm, E.; Hausman, J. F. One dry summer: A leaf proteome study on the response of oak to drought exposure J. Proteomics 2011, 74 (8) 1385-1395
36. Jorge, I.; Navarro, R. M.; Lenz, C.; Ariza, D.; Jorrin, J. Variation in the holm oak leaf proteome at different plant developmental stages, between provenances and in response to drought stress Proteomics 2006, 6 (Suppl 1) S207-14
37. Wang, W.; Vignani, R.; Scali, M.; Cresti, M. A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis Electrophoresis 2006, 27 (13) 2782-2786
38. Ramagli, L. S.; Rodriguez, L. V. Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer Electrophoresis 1985, 6 (11) 559-563
39. Gorg, A.; Postel, W.; Baumer, M.; Weiss, W. Two-dimensional polyacrylamide gel electrophoresis, with immobilized pH gradients in the first dimension, of barley seed proteins: discrimination of cultivars with different malting grades Electrophoresis 1992, 13 (4) 192-203
40. Mathesius, U.; Keijzers, G.; Natera, S. H.; Weinman, J. J.; Djordjevic, M. A.; Rolfe, B. G. Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting Proteomics 2001, 1 (11) 1424-40
41. Sharov, A.; Dudekula, D.; Ko, M. A web-based tool for principal component and significance analysis of microarray data Bioinformatics 2005, 21 (10) 2548-2549
42. Valledor, L.; Jorrín, J. Back to the basics: Maximizing the information obtained by quantitative two dimensional gel electrophoresis analyses by an appropriate experimental design and statistical analyses J. Proteomics 2011, 74 (1) 1-18
43. Brumbarova, T.; Matros, A.; Mock, H.; Bauer, P. A proteomic study showing differential regulation of stress, redox regulation and peroxidase proteins by iron supply and the transcription factor FER Plant J. 2008, 54, 321-334
44. Sechi, S.; Chait, B. T. Modification of Cysteine Residues by Alkylation. A Tool in Peptide Mapping and Protein Identification Anal. Chem. 1998, 70 (24) 5150-5158
45. Baker, N. R.; Rosenqvist, E. Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities J. Exp. Bot. 2004, 55 (403) 1607-1621
46. Baquedano, F.; Castillo, F. Comparative ecophysiological effects of drought on seedlings of the Mediterranean water-saver Pinus halepensis and water-spenders Quercus coccifera, and Quercus ilex Trees 2006, 20 (6) 689-700
47. Corcuera, L.; Camarero, J.; Gil-Pelegrín, E. Effects of a severe drought on Quercus ilex radial growth and xylem anatomy Trees 2004, 18 (1) 83-92
48. Corcuera, L.; Camarero, J. J.; Sisó, S.; Gil-Pelegrín, E. Radial-growth and wood-anatomical changes in overaged Quercus pyrenaica coppice stands: functional responses in a new Mediterranean landscape Trees 2006, 20 (1) 91-98
49. Limousinmgrt, J.-M.; Longepierre, D.; Huc, R.; Rambal, S. Change in hydraulic traits of Mediterranean Quercus ilex subjected to long-term throughfall exclusion Tree Physiol. 2010, 30 (8) 1026-1036
50. Limousinmgrt, J.-M.; Rambal, S.; Ourcival, J.-M.; Rodríguez- Calcerrada, J.; Pérez-Ramos, I.; Rodríguez-Cortina, R.; Misson, L.; Joffre, R. Morphological and phenological shoot plasticity in a Mediterranean evergreen oak facing long-term increased drought Oecologia 2012, 169 (2) 565-577
51. Jorge, I.; Navarro, R. M.; Lenz, C.; Ariza, D.; Porras, C.; Jorrin, J. The holm oak leaf proteome: analytical and biological variability in the protein expression level assessed by 2-DE and protein identification tandem mass spectrometry de novo sequencing and sequence similarity searching Proteomics 2005, 5 (1) 222-34
52. Sghaier-Hammami, B.; Valero-Galván, J.; Romero-Rodríguez, M. C.; Navarro-Cerrillo, R. M.; Abdelly, C.; Jorrín-Novo, J. Physiological and proteomics analyses of Holm oak (Quercus ilex subsp. ballota [Desf.] Samp.) responses to Phytophthora cinnamomi Plant Physiol. Biochem. 2013, 71, 191-202
53. Kottapalli, K. R.; Rakwal, R.; Shibato, J.; Burow, G.; Tissue, D.; Burke, J.; Puppala, N.; Burow, M.; Payton, P. Physiology and proteomics of the water-deficit stress response in three contrasting peanut genotypes Plant, Cell Environ. 2009, 32 (4) 380-407
54. Blodner, C.; Majcherczyk, A.; Kues, U.; Polle, A. Early drought-induced changes to the needle proteome of Norway spruce Tree Physiol. 2007, 27 (10) 1423-1431
55. Bogeat-Triboulot, M.-B.; Brosche, M.; Renaut, J.; Jouve, L.; Le Thiec, D.; Fayyaz, P.; Vinocur, B.; Witters, E.; Laukens, K.; Teichmann, T.; Altman, A.; Hausman, J.-F.; Polle, A.; Kangasjarvi, J.; Dreyer, E. Gradual Soil Water Depletion Results in Reversible Changes of Gene Expression, Protein Profiles, Ecophysiology, and Growth Performance in Populus euphratica, a Poplar Growing in Arid Regions Plant Physiol. 2007, 143 (2) 876-892
56. Ingle, R. A.; Schmidt, U. G.; Farrant, J. M.; Thomson, J. A.; Mundree, S. G. Proteomic analysis of leaf proteins during dehydration of the resurrection plant Xerophyta viscosa Plant, Cell Environ. 2007, 30 (4) 435-446
57. Plomion, C.; Lalanne, C.; Claverol, S.; Meddour, H.; Kohler, A.; Bogeat-Triboulot, M.-B.; Barre, A.; Le Provost, G.; Dumazet, H.; Jacob, D.; Bastien, C.; Dreyer, E.; de Daruvar, A.; Guehl, J.-M.; Schmitter, J.-M.; Martin, F.; Bonneu, M. Mapping the proteome of poplar and application to the discovery of drought-stress responsive proteins Proteomics 2006, 6 (24) 6509-6527
58. Bonhomme, L.; Monclus, R.; Vincent, D.; Carpin, S.; Claverol, S.; Lomenech, A.; Labas, V.; Plomion, C.; Brignolas, F.; Morabito, D. Genetic variation and drought response in two Populus x euramericana genotypes through 2-DE proteomic analysis of leaves from field and glasshouse cultivated plants Phytochemistry 2009, 70 (8) 988-1002
59. Bonhomme, L.; Monclus, R.; Vincent, D.; Carpin, S.; Lomenech, A.; Plomion, C.; Brignolas, F.; Morabito, D. Leaf proteome analysis of eight Populus xeuramericana genotypes: genetic variation in drought response and in water-use efficiency involves photosynthesis-related proteins Proteomics 2009, 9 (17) 4121-42
60. Martin-StPaul, N. K.; Limousin, J.-M.; Rodríguez-Calcerrada, J.; Ruffault, J.; Rambal, S.; Letts, M. G.; Misson, L. Photosynthetic sensitivity to drought varies among populations of Quercus ilex along a rainfall gradient Funct. Plant Biol. 2012, 39 (1) 25-37
61. Chaves, M. M.; Flexas, J.; Pinheiro, C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell Annals of Botany 2009, 103 (4) 551-560
62. Niyogi, K. K. Safety valves for photosynthesis Curr. Opin. Plant Biol. 2000, 3 (6) 455-460
63. Scharte, J.; Schön, H.; Weis, E. Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae Plant, Cell Environ. 2005, 28 (11) 1421-1435
64. Reddy, A. R.; Chaitanya, K. V.; Vivekanandan, M. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants J. Plant Physiol. 2004, 161 (11) 1189-1202
65. Baier, M.; Dietz, K. J. Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis Plant Physiol. 1999, 119 (4) 1407-14
66. Molina-Rueda, J. J.; Tsai, C. J.; Kirby, E. G. The Populus superoxide dismutase gene family and its responses to drought stress in transgenic poplar overexpressing a pine cytosolic glutamine synthetase (GS1a) PLoS One 2013, 8 (2) e56421
67. Hura, T.; Hura, K.; Ostrowska, A.; Grzesiak, M.; Dziurka, K. The cell wall-bound phenolics as a biochemical indicator of soil drought resistance in winter triticale Plant Soil Environ. 2013, 59 (5) 189-195
68. Yang, J.; Zhang, J.; Liu, K.; Wang, Z.; Liu, L. Involvement of polyamines in the drought resistance of rice J. Exp. Bot. 2007, 58 (6) 1545-1555
69. Chiera, J. M.; Streeter, J. G.; Finer, J. J. Ononitol and pinitol production in transgenic soybean containing the inositol methyl transferase gene from Mesembryanthemum crystallinum Plant Sci. 2006, 171 (6) 647-654