Membrane transporters and carbon metabolism implicated in chloride homeostasis differentiate salt stress responses in tolerant and sensitive Citrus rootstocks

Functional and Integrative Genomics

Volumn 9, Issue 3, 2009, Pages 293-309

  Brumós, Javier ^a   Colmenero Flores, José M ^a,d   Conesa, Ana ^c   Izquierdo, Pedro ^a   Sánchez, Guadalupe ^a   Iglesias, Domingo J ^a   López Climent, María F ^b   Gómez Cadenas, Aurelio ^b   Talón, Manuel ^a  

^a INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

^b UNIVERSITAT JAUME I   (Spain)

^c CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^d INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SEVILLA   (Spain)

Author keywords

Carbon metabolism; Chloride transport; Citrus rootstock; Genomics; Salt stress

Indexed keywords

ABC TRANSPORTER; CARRIER PROTEIN; CHLORIDE; NICOTINAMIDE RIBOSIDE TRANSPORTER 1; NICOTINAMIDE RIBOSIDE TRANSPORTER 2; PORIN; POTASSIUM CHLORIDE; SODIUM; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ARTICLE; CARBON METABOLISM; CARBON UTILIZATION; CITRUS FRUIT; CITRUS RESHNI; CONTROLLED STUDY; ELECTROLYTE BALANCE; ENERGY METABOLISM; EVAPOTRANSPIRATION; EVOLUTIONARY ADAPTATION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENOTYPE; HOMEOSTASIS; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; NONHUMAN; OSMOTIC STRESS; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAF; PLANT METABOLISM; PLANT ROOT; PRIORITY JOURNAL; SALINITY; SALT STRESS; SALT TOLERANCE; STOMATAL CONDUCTANCE; SWEET ORANGE;

CITRUS; CITRUS SINENSIS X PONCIRUS TRIFOLIATA; CLEOPATRA MANDARIN;

EID: 67649976987     PISSN: 1438793X     EISSN: 14387948     Source Type: Journal    
DOI: 10.1007/s10142-008-0107-6     Document Type: Article

References (72)

1. Ancillo G, Gadea J, Forment J, Guerri J, Navarro L (2007) Class prediction of closely related plant varieties using gene expression profiling. J Exp Bot 58:1927-1933
2. Arbona V, Marco AJ, Iglesias DJ, López-Climent MF, Talón M, Gómez-Cadenas A (2005) Carbohydrate depletion in roots and leaves of salt-stressed potted Citrus clementina L. Plant Growth Reg 46:153-160
3. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: Tool for the unification of biology. Nat Genet 25:25-29
4. Bañuls J, Primo-Millo E (1992) Effects of chloride and sodium on gas exchange parameters and water relations of Citrus plants. Physiol Plantarum 86:115-123
5. Bañuls J, Primo-Millo E (1995) Effects of salinity on some Citrus scion-rootstock combinations. Ann Bot 76:97-102
6. Bañuls J, Serna MD, Legaz F, Talon M, Primo-Millo E (1997) Growth and gas exchange parameters of Citrus plants stressed with different salts. J Plant Physiol 150:194-199
7. Barrett HC, Rhodes AM (1976) Numerical taxonomic study of affinity relationships in cultivated Citrus and its close relatives. Syst Bot 1:105-136
8. Blüthgen N, Kielbasa SM, Herzel H (2005) Inferring combinatorial regulation of transcription in silico. Nucl Acids Res 33:272-279
9. Cercos M, Soler G, Iglesias D, Gadea J, Forment J, Talon M (2006) Global analysis of gene expression during development and ripening of Citrus fruit flesh. A proposed mechanism for citric acid utilization. Plant Mol Biol 62:513-527
10. Colmenero-Flores JM, Moreno LP, Smith C, Covarrubias AA (1999) Pvlea-18, a member of a new late embryogenesis abundant protein family that accumulates during water stress and in the growing regions of well-irrigated bean seedlings. Plant Physiol 120:93-103
11. Colmenero-Flores JM, Martinez G, Gamba G, Vazquez N, Iglesias DJ, Brumos J, Talon M (2007) Identification and functional characterization of cation-chloride cotransporters in plants. Plant J 50:278-292
12. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676
13. Conesa A, Nueda MJ, Ferrer A, Talon M (2006) maSigPro: A method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics 22:1096-1102
14. Cramer G, Ergül A, Grimplet J, Tillett R, Tattersall E, Bohlman M, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch K, Schooley D, Cushman J (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111-134
15. De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The Nitrate/Proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939-942
16. de Vries SC, Springer J, Wessels JGH (1982) Diversity of abundant mRNA sequences and patterns of protein synthesis in etiolated and greened pea seedlings. Planta 156:129-135
17. Fecht-Bartenbach JVD, Bogner M, Krebs M, Stierhof Y-D, Schumacher K, Ludewig U (2007) Function of the anion transporter AtCLC-d in the trans-Golgi network. Plant J 50:466-474
18. Forment J, Gadea J, Huerta L, Abizanda L, Agusti J, Alamar S, Alos E, Andres F, Arribas R, Beltran JP, Berbel A, Blazquez MA, Brumos J, Canas LA, Cercos M, Colmenero-Flores JM, Conesa A, Estables B, Gandia M, Garcia-Martinez JL, Gimeno J, Gisbert A, Gomez G, Gonzalez-Candelas L, Granell A, Guerri J, Lafuente MT, Madueño F, Marcos JF, Marques MC, Martinez F, Martinez-Godoy MA, Miralles S, Moreno P, Navarro L, Pallas V, Perez-Amador MA, Perez-Valle J, Pons C, Rodrigo I, Rodriguez PL, Royo C, Serrano R, Soler G, Tadeo F, Talon M, Terol J, Trenor M, Vaello L, Vicente O, Vidal C, Zacarias L, Conejero V (2005) Development of a Citrus genome-wide EST collection and cDNA microarray as resources for genomic studies. Plant Mol Biol 57:375-391
19. Gaedeke N, Klein M, Kolukisaoglu U, Forestier C, Müller A, Ansorge M, Becker D, Mamnun Y, Kuchler K, Schulz B, Mueller-Roeber B, Martinoia E (2001) The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J 20:1875-1887
20. Gandía M, Conesa A, Ancillo G, Gadea J, Forment J, Pallás V, Flores R, Duran-Vila N, Moreno P, Guerri J (2007) Transcriptional response of Citrus aurantifolia to infection by Citrus tristeza virus. Virology 367:298-306
21. Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA (2000) Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J Biol Chem 275:5668-5674
22. Geelen D, Lurin C, Bouchez D, Frachisse JM, Lelievre F, Courtial B, Barbier-brygoo H, Maurel C (2000) Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content. Plant J 21:259-267
23. Gómez-Cadenas A, Tadeo FR, Primo-Millo E, Talon M (1998) Involvement of abscisic acid and ethylene in the responses of Citrus seedlings to salt shock. Physiol Plant 103:475-484
24. Gómez-Cadenas A, Iglesias DJ, Arbona V, Colmenero-Flores JM, Primo-Millo E, Talón M (2003) in Recent Res Devel Plant Mol Biol, vol. 1, pp 281-298, Research Signpost, Keral
25. Hechenberger M, Schwappach B, Fischer WN, Frommer WB, Jentsch TJ, Steinmeyer K (1996) A family of putative chloride channels from Arabidopsis and functional complementation of a yeast strain with a CLC gene disruption. J Biol Chem 271:33632-33638
26. Herde O, Peña-Cortés HL, Willmitzer L, Fisahn J (1997) Stomatal responses to jasmonic acid, linolenic acid and abscisic acid in wild-type and ABA-deficient tomato plants. Plant Cell Environ 20:136-141
27. Huang N-C, Liu K-H, Lo H-J, Tsay Y-F (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11:1381-1392
28. Iglesias DJ, Cercós M, Colmenero-Flores JM, Naranjo MA, Ríos G, Carrera E, Ruiz-Rivero O, Lliso I, Morillon R, Tadeo FR, Talon M (2007) Physiology of Citrus fruiting. Braz J Plant Physiol 19(4):333-362
29. Jentsch TJ, Stein V, Weinreich F, Zdebik AA (2002) Molecular structure and physiological function of chloride channels. Physiol Rev 82:503-568
30. Jeong J, Suh S, Guan C, Tsay Y-F, Moran N, Oh CJ, An CS, Demchenko KN, Pawlowski K, Lee Y (2004) A nodule-specific dicarboxylate transporter from alder is a member of the peptide transporter family. Plant Physiol 134:969-978
31. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889-906
32. Khelil A, Menu T, Ricard B (2007) Adaptive response to salt involving carbohydrate metabolism in leaves of a salt-sensitive tomato cultivar. Plant Physiol Biochem 45:551-559
33. Liu KH, Huang CY, Tsay Y-F (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involving multiple phases of nitrate uptake. Plant Cell 11:865-874
34. López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2008) Relationship between salt tolerance and photosynthetic machinery performance in Citrus. Env Exp Bot 62:176-184
35. Lurin C, Geelen D, Barbier-Brygoo H, Guern J, Maurel C (1996) Cloning and functional expression of a plant voltage-dependent chloride channel. Plant Cell 8(4):701-711, 8:701-711
36. Maas EV (1993) Salinity and citriculture. Tree Physiol 12:195-216
37. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence. A practical guide. J Exp Bot 51:659-668
38. Moya JL, Primo-Millo E, Talon M (1999) Morphological factors determining salt tolerance in Citrus seedlings: The shoot to root ratio modulates passive root uptake of chloride ions and their accumulation in leaves. Plant Cell Environ 22:1425-1433
39. Moya JL, Tadeo FR, Gomez-Cadenas A, Primo-Millo E, Talon M (2002) Transmissible salt tolerance traits identified through reciprocal grafts between sensitive Carrizo and tolerant Cleopatra Citrus genotypes. J Plant Physiol 159:991-998
40. Moya JL, Gomez-Cadenas A, Primo-Millo E, Talon M (2003) Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin Citrus rootstocks is linked to water use. J Exp Bot 54:825-833
41. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239-250
42. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651-681
43. Myhre S, Tveit H, Mollestad T, Laegreid A (2006) Additional gene ontology structure for improved biological reasoning. Bioinformatics 22:2020-2027
44. Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483-486
45. Nueda MJ, Conesa A, Westerhuis JA, Hoefsloot HCJ, Smilde AK, Talon M, Ferrer A (2007) Discovering gene expression patterns in time course microarray experiments by ANOVA-SCA. Bioinformatics 23:1792-1800
46. Ozturk ZN, Talamè V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley. Plant Mol Biol 48:551-573
47. Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: Roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181-1199
48. Pierik R, Tholen D, Poorter H, Visser E, Voesenek L (2006) The Janus face of ethylene: Growth inhibition and stimulation. TRENDS Plant Sci 11:176-183
49. Poorter H (2002) Plant growth and carbon economy. In: Encyclopedia of life sciences. Macmillan Publisher, Nature Publishing Group, London
50. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: Protein domains identifier. Nucl Acids Res 33:W116-W120
51. Reiner A, Yekutieli D, Benjamini Y (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19:368-375
52. Roberts SK (2006) Plasma membrane anion channels in higher plants and their putative functions in roots. New Phytol 169:647-666
53. Romero-Aranda R, Moya JL, Tadeo FR, Legaz F, Primo-Millo E, Talon M (1998) Physiological and anatomical disturbances induced by chloride salts in sensitive and tolerant Citrus: Beneficial and detrimental effects of cations. Plant Cell Environ 21:1243-1253
54. Sahi C, Singh A, Blumwald E, Grover A (2006) Beyond osmolytes and transporters: Novel plant salt-stress tolerance-related genes from transcriptional profiling data. Physiol Plantarum 127:1-9
55. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
56. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279-292
57. Smyth GK (2005) Limma: Linear models for microarray data. In: Gentleman R, Carey V, Huber W, Irizarry R, Duboit S (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, Berlin, pp 397-420
58. Storey R, Walker RR (1999) Citrus and salinity. Sci Hort 78:39-81
59. Sugiura M, Georgescu MN, Takahashi M (2007) A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant Cell Physiol 48:1022-1035
60. Suh SJ, Wang Y-F, Frelet A, Leonhardt N, Klein M, Forestier C, Mueller-Roeber B, Cho MH, Martinoia E, Schroeder JI (2007) The ATP Binding Cassette Transporter AtMRP5 Modulates Anion and Calcium Channel Activities in Arabidopsis Guard Cells. J Biol Chem 282:1916-1924
61. Syvertsen JP, Boman B, Tucker DPH (1989) Salinity in Florida Citrus production. Proc Fla State Hort Soc 102:61-64
62. Tadeo F, Cercos M, Colmenero-Flores JM, Iglesias DJ, Naranjo MA, Ríos G, Carrera E, Ruiz-Rivero O, Lliso I, Morillon R, Talon M (2008) Molecular physiology of development and quality of Citrus. Adv Bot Res 47:147-223
63. Talon M, Gmitter FGJ (2008) Citrus genomics. Int J Plant Genomics ID 528361
64. Terol J, Conesa A, Colmenero J, Cercos M, Tadeo F, Agusti J, Alos E, Andres F, Soler G, Brumos J, Iglesias D, Gotz S, Legaz F, Argout X, Courtois B, Ollitrault P, Dossat C, Wincker P, Morillon R, Talon M (2007) Analysis of 13000 unique Citrus clusters associated with fruit quality, production and salinity tolerance. BMC Genomics 8:31
65. Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401:914-917
66. White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: A review. Ann Bot 88:967-988
67. Wing-Yen FL, Fuk-Ling W, Sau-Na T, Tsui-Hung P, Guihua S, Hon-Ming L (2006) Tonoplast-located GmCLC1 and GmNHX1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY)-2 cells. Plant Cell Environ 29:1122
68. Xu G, Magen H, Tarchitzky J, Kafkafi U (2000) Advances in chloride nutrition. In Advances in Agronomy. Elsevier vol 68, pp 96-150
69. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: A robust composite method addressing single and multiple slide systematic variation. Nucl Acids Res 30:e15
70. Yeo AR, Lee L-S, Izard P, Boursier PJ, Flowers TJ (1991) Short-and long-term effects of salinity on leaf growth in rice (Oryza sativa L.). J Exp Bot 42:881-889
71. Yokoyama T, Kodama N, Aoshima H, Izu H, Matsushita K, Yamada M (2001) Cloning of a cDNA for a constitutive NRT1 transporter from soybean and comparison of gene expression of soybean NRT1 transporters. Biochim Biophys Acta 1518:79-86
72. Zhou J-J, Theodoulou FL, Muldin I, Ingemarsson B, Miller AJ (1998) Cloning and functional characterization of a Brassica napus transporter that is able to transport nitrate and histidine. J Biol Chem 273:12017-12023