Transcriptomic and proteomic analyses of a pale-green durum wheat mutant shows variations in photosystem components and metabolic deficiencies under drought stress

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Peremarti, Ariadna ^a,b   Marè, Caterina ^c   Aprile, Alessio ^d   Roncaglia, Enrica ^e   Cattivelli, Luigi ^c   Villegas, Dolors ^b   Royo, Conxita ^b  

^a Forest Sciences and Technology Centre of Catalonia   (Spain)

^b IRTA   (Spain)

^c ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^d UNIVERSITY OF SALENTO   (Italy)

^e UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Chlorophyll content; Oxidative stress; Pale green mutant; Proteomics; Transcriptomics; Triticum turgidum L var. durum; Water stress

Indexed keywords

CAROTENOID; CHITINASE; CHLOROPHYLL; PEROXIDASE; XANTHOPHYLL;

ARTICLE; BIOMASS; CARBOHYDRATE METABOLISM; CHLOROPHYLL CONTENT; CHLOROPLAST; CITRIC ACID CYCLE; CONTROLLED STUDY; DROUGHT RESISTANCE; DROUGHT STRESS; GENE EXPRESSION; GENE IDENTIFICATION; GENOTYPE; GRAIN YIELD; MICROARRAY ANALYSIS; MUTATION; NONHUMAN; OXIDATIVE STRESS; PHOTOSYNTHESIS; PLANT METABOLISM; PROTEIN EXPRESSION; PROTEOMICS; TRANSCRIPTOMICS; TRITICUM DURUM; UPREGULATION; WATER AVAILABILITY; WATER STRESS; DROUGHT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PRINCIPAL COMPONENT ANALYSIS; ULTRASTRUCTURE; WHEAT;

TRITICUM AESTIVUM; TRITICUM TURGIDUM; TRITICUM TURGIDUM SUBSP. DURUM;

CHLOROPHYLL; CHLOROPLASTS; DROUGHTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; OXIDATIVE STRESS; PHOTOSYNTHESIS; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS; TRITICUM;

EID: 84896716495     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-125     Document Type: Article

References (128)

1. Kumar S, Sehgal SK, Kumar U, Prasad PVV, Joshi AK, Gill BS. Genomic characterization of drought tolerance-related traits in spring wheat. Euphytica 2012, 186(1):265-276.
2. Pradhan GP, Prasad PVV, Fritz AK, Kirkham MB, Gill BS. High temperature tolerance in Aegilops species and its potential transfer to wheat. Crop Sci 2012, 52(1):292-304.
3. Blum A, Shpiler L, Golan G, Mayer J. Yield stability and canopy temperature of wheat genotypes under drought-stress. Field Crops Res 1989, 22(4):289-296.
4. Araus JL, Slafer GA, Reynolds MP, Royo C. Plant breeding and drought in C-3 cereals: what should we breed for?. Annals of Botany 2002, 89(7):925-940. 10.1093/aob/mcf049, 12102518.
5. Gregersen PL, Culetic A, Boschian L, Krupinska K. Plant senescence and crop productivity. Plant Mol Biol 2013, 82(6):603-622. 10.1007/s11103-013-0013-8, 23354836.
6. Tardy F, Creach A, Havaux M. Photosynthetic pigment concentration, organization and interconversions in a pale green Syrian landrace of barley (Hordeum vulgare L., Tadmor) adapted to harsh climatic conditions. Plant Cell Environ 1998, 21(5):479-489.
7. Carvalho RF, Takaki M, Azevedo RA. Plant pigments: the many faces of light perception. Acta Physiologiae Plantarum 2011, 33(2):241-248.
8. Pogson BJ, Albrecht V. Genetic Dissection of chloroplast biogenesis and development: an overview. Plant Physiol 2011, 155(4):1545-1551. 10.1104/pp.110.170365, 3091115, 21330494.
9. Greiner S. Plastome mutants of higher plants. Genomics of Chloroplasts and Mitochondria 2012, 237-266. Netherlands: Springer, Bock R, Knoop V, [Govindjee and Sharkey TD (Series Editors): Advances in Photosynthesis and Respiration, vol 35.].
10. Leister D. Chloroplast research in the genomic age. Trends Genet 2003, 19(1):47-56. 10.1016/S0168-9525(02)00003-3, 12493248.
11. Bollivar DW. Recent advances in chlorophyll biosynthesis. Photosynthesis Res 2006, 90(2):173-194.
12. Zhang H, Li J, Yoo J, Yoo S, Cho S, Koh H, Seo HS, Paek N. Rice chlorina-1 and chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. Plant Mol Biol 2006, 62(3):325-337. 10.1007/s11103-006-9024-z, 16915519.
13. Chen Q, Wang LF, Su N, Qin HD, Niu HB, Wang JL, Zhai HQ, Wan JM. Photosystem 2 photochemistry and pigment composition of a yellow mutant of rice (Oryza sativa L.) under different irradiances. Photosynthetica 2008, 46(1):35-39.
14. Prina AR, Arias MC, Lainez V, Landau A, Maldonado S. A cytoplasmically inherited mutant controlling early chloroplast development in barley seedlings. Theor Appl Genet 2003, 107(8):1410-1418. 10.1007/s00122-003-1391-0, 12920517.
15. Morosinotto T, Bassi R, Frigerio S, Finazzi G, Morris E, Barber J. Biochemical and structural analyses of a higher plant Photosystem II supercomplex of a Photosystem I-less mutant of barley - Consequences of a chronic over-reduction of the plastoquinone pool. Febs Journal 2006, 273(20):4616-4630.
16. Frigerio S, Campoli C, Zorzan S, Fantoni L, Crosatti C, Drepper F, Haehnel W, Cattivelli L, Morosinotto T, Bassi R. Photosynthetic antenna size in higher plants is controlled by plastoquinone redox state at post-transcriptional rather than transcriptional level. J Biol Chem 2007, 282(40):29457-29469. 10.1074/jbc.M705132200, 17675669.
17. Campoli C, Caffarri S, Svensson JT, Bassi R, Stanca AM, Cattivelli L, Crosatti C. Parallel pigment and transcriptomic analysis of four barley Albina and Xantha mutants reveals the complex network of the chloroplast-dependent metabolism. Plant Mol Biol 2009, 71(1-2):173-191.
18. Falbel TG, Staehelin LA. Characterization of a family of chlorophyll-deficient wheat (Triticum) and barley (Hordeum vulgare) mutants with defects in the magnesium-insertion step of chlorophyll biosynthesis. Plant Physiol 1994, 104(2):639-648. 10.1104/pp.104.2.639, 159242, 8159789.
19. Falbel TG, Meehl JB, Staehelin LA. Severity of mutant phenotype in a series of chlorophyll-deficient wheat mutants depends on light intensity and the severity of the block in chlorophyll synthesis. Plant Physiol 1996, 112(2):821-832. 10.1104/pp.112.2.821, 158007, 8883392.
20. Liu X, Xu H, Zhang J, Liang G, Liu Y, Guo A. Effect of low temperature on chlorophyll biosynthesis in albinism line of wheat (Triticum aestivum) FA85. Physiol Plantarum 2012, 145(3):384-394.
21. Bassi R, Caffarri S. Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls. Photosynthesis Res 2000, 64(2-3):243-256.
22. Jahns P, Holzwarth AR. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta-Bioenergetics 2012, 1817(1):182-193.
23. Choudhury NK, Behera RK. Photoinhibition of photosynthesis: role of carotenoids in photoprotection of chloroplast constituents. Photosynthetica 2001, 39(4):481-488.
24. Takahashi S, Badger MR. Photoprotection in plants: a new light on Photosystem II damage. Trends Plant Sci 2011, 16(1):53-60. 10.1016/j.tplants.2010.10.001, 21050798.
25. Petrov VD, Van Breusegem F. Hydrogen peroxide-a central hub for information flow in plant cells. AoB plants 2012, pls014.
26. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 2010, 48(12):909-930. 10.1016/j.plaphy.2010.08.016, 20870416.
27. Fleury D, Jefferies S, Kuchel H, Langridge P. Genetic and genomic tools to improve drought tolerance in wheat. J Exp Bot 2010, 61(12):3211-3222. 10.1093/jxb/erq152, 20525798.
28. Leader DJ. Transcriptional analysis and functional genomics in wheat. J Cereal Sci 2005, 41(2):149-163.
29. Qin D, Wu H, Peng H, Yao Y, Ni Z, Li Z, Zhou C, Sun Q. Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 2008, 9:432. 10.1186/1471-2164-9-432, 2614437, 18808683.
30. Sutton F, Chen D, Ge X, Kenefick D. Cbf genes of the Fr-A2 allele are differentially regulated between long-term cold acclimated crown tissue of freeze-resistant and -susceptible, winter wheat mutant lines. BMC Plant Biol 2009, 9:34. 10.1186/1471-2229-9-34, 2663559, 19309505.
31. Desmond OJ, Manners JM, Schenk PM, Maclean DJ, Kazan K. Gene expression analysis of the wheat response to infection by Fusarium pseudograminearum. Physiol Mol Plant Pathol 2008, 73(1-3):40-47.
32. Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ. Cold- and light-induced changes in the transcriptome of wheat leading to phase transition from vegetative to reproductive growth. BMC Plant Biology 2009, 9:55. 10.1186/1471-2229-9-55, 2685395, 19432994.
33. Wan Y, Underwood C, Toole G, Skeggs P, Zhu T, Leverington M, Griffiths S, Wheeler T, Gooding M, Poole R, Edwards KJ, Gezan S, Welham S, Snape J, Mills ENC, Mitchell RAC, Shewry PR. A novel transcriptomic approach to identify candidate genes for grain quality traits in wheat. Plant Biotech J 2009, 7(5):401-410.
34. Krugman T, Chague V, Peleg Z, Balzergue S, Just J, Korol AB, Nevo E, Saranga Y, Chalhoub B, Fahima T. Multilevel regulation and signalling processes associated with adaptation to terminal drought in wild emmer wheat. Funct Integr Genomics 2010, 10(2):167-186. 10.1007/s10142-010-0166-3, 20333536.
35. Bahrman N, Le Gouis J, Negroni L, Amilhat L, Leroy P, Laine AL, Jaminon O. Differential protein expression assessed by two-dimensional gel electrophoresis for two wheat varieties grown at four nitrogen levels. Proteomics 2004, 4(3):709-719. 10.1002/pmic.200300571, 14997493.
36. Ouerghi Z, Remy R, Ouelhazi L, Ayadi A, Brulfert J. Two-dimensional electrophoresis of soluble leaf proteins, isolated from two wheat species (Triticum durum and Triticum aestivum) differing in sensitivity towards NaCl. Electrophoresis 2000, 21(12):2487-2491. 10.1002/1522-2683(20000701)21:12<2487::AID-ELPS2487>3.0.CO;2-B, 10939462.
37. Gao L, Yan X, Li X, Guo G, Hu Y, Ma W, Yan Y. Proteome analysis of wheat leaf under salt stress by two-dimensional difference gel electrophoresis (2D-DIGE). Phytochemistry 2011, 72(10):1180-1191. 10.1016/j.phytochem.2010.12.008, 21257186.
38. Xu J, Li Y, Sun J, Du L, Zhang Y, Yu Q, Liu X. Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance. Plant Biology 2013, 15(2):292-303. 10.1111/j.1438-8677.2012.00639.x, 22963252.
39. Caruso G, Cavaliere C, Foglia P, Gubbiotti R, Samperi R, Lagana A. Analysis of drought responsive proteins in wheat (Triticum durum) by 2D-PAGE and MALDI-TOF mass spectrometry. Plant Sci 2009, 177(6):570-576.
40. Ford KL, Cassin A, Bacic A. Quantitative proteomic analysis of wheat cultivars with differing drought stress tolerance. Front Plant Sci 2011, 2:44. 3355674, 22639595.
41. Jiang Y, Yang B, Harris NS, Deyholos MK. Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 2007, 58(13):3591-3607. 10.1093/jxb/erm207, 17916636.
42. Peng Z, Wang M, Li F, Lv H, Li C, Xia G. A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol Cell Proteomics 2009, 8(12):2676-2686. 10.1074/mcp.M900052-MCP200, 2816014, 19734139.
43. Aprile A, Mastrangelo AM, De Leonardis AM, Galiba G, Roncaglia E, Ferrari F, De Bellis L, Turchi L, Giuliano G, Cattivelli L. Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genomics 2009, 10:279. 10.1186/1471-2164-10-279, 2713995, 19552804.
44. Landau AM, Lokstein H, Scheller HV, Lainez V, Maldonado S, Raul Prina A. A cytoplasmically inherited barley mutant is defective in Photosystem I assembly due to a temperature-sensitive defect in ycf3 splicing. Plant Physiol 2009, 151(4):1802-1811. 10.1104/pp.109.147843, 2785965, 19812182.
45. Fristedt R, Willig A, Granath P, Crevecoeur M, Rochaix J, Vener AV. Phosphorylation of Photosystem II controls functional macroscopic folding of photosynthetic membranes in Arabidopsis. Plant Cell 2009, 21(12):3950-3964. 10.1105/tpc.109.069435, 2814517, 20028840.
46. Simpson DJ, Vonwettstein D. Macromolecular Physiology of Plastids. 14. Viridis mutants in barley - Genetic, fluoroscopic and ultrastructural characterization. Carlsberg Res Commun 1980, 45(4):283-314.
47. Cui Y, Jia Q, Yin Q, Lin G, Kong M, Yang Z. The GDC1 gene encodes a novel ankyrin domain-containing protein that is essential for grana formation in Arabidopsis. Plant Physiol 2011, 155(1):130-141. 10.1104/pp.110.165589, 3075748, 21098677.
48. Austin JR, Frost E, Vidi P, Kessler F, Staehelin LA. Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 2006, 18(7):1693-1703. 10.1105/tpc.105.039859, 1488921, 16731586.
49. Bréhélin C, Kessler F, van Wijk KJ. Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 2007, 12(6):260-266. 10.1016/j.tplants.2007.04.003, 17499005.
50. Bréhélin C, Kessler F. The plastoglobule: a bag full of lipid biochemistry tricks. Photochem Photobiol 2008, 84(6):1388-1394. 10.1111/j.1751-1097.2008.00459.x, 19067960.
51. Pogson BJ, Niyogi KK, Bjorkman O, DellaPenna D. Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc Natl Acad Sci USA 1998, 95(22):13324-13329. 10.1073/pnas.95.22.13324, 23800, 9789087.
52. Dall'Osto L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R. Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 2006, 6:32. 10.1186/1471-2229-6-32, 1769499, 17192177.
53. Wehner A, Grasses T, Jahns P. De-epoxidation of violaxanthin in the minor antenna proteins of photosystem II, LHCB4, LHCB5, and LHCB6. J Biol Chem 2006, 281(31):21924-21933. 10.1074/jbc.M602915200, 16754673.
54. Kar RK. Plant responses to water stress: role of reactive oxygen species. Plant Signal Behav 2011, 6(11):1741-1745. 10.4161/psb.6.11.17729, 3329347, 22057331.
55. Baier M, Dietz KJ. Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot 2005, 56(416):1449-1462. 10.1093/jxb/eri161, 15863449.
56. Colville L, Smirnoff N. Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. J Exp Bot 2008, 59(14):3857-3868. 10.1093/jxb/ern229, 18849295.
57. Bahrini I, Sugisawa M, Kikuchi R, Ogawa T, Kawahigashi H, Ban T, Handa H. Characterization of a wheat transcription factor, TaWRKY45, and its effect on Fusarium head blight resistance in transgenic wheat plants. Breed Sci 2011, 61(2):121-129.
58. Qiu Y, Yu D. Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 2009, 65(1):35-47.
59. Nomura T, Ishizuka A, Kishida K, Islam AKMR, Endo TR, Iwamura H, Ishihara A. Chromosome arm location of the genes for the biosynthesis of hordatines in barley. Genes Genet Syst 2007, 82(6):455-464. 10.1266/ggs.82.455, 18270436.
60. Meng Y, Moscou MJ, Wise RP. Blufensin1 negatively impacts basal defense in response to barley powdery mildew. Plant Physiol 2009, 149(1):271-285. 10.1104/pp.108.129031, 2613711, 19005086.
61. Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA. The enigmatic LEA proteins and other hydrophilins. Plant Physiol 2008, 148(1):6-24. 10.1104/pp.108.120725, 2528095, 18772351.
62. Saez A, Rodrigues A, Santiago J, Rubio S, Rodriguez PL. HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. Plant Cell 2008, 20(11):2972-2988. 10.1105/tpc.107.056705, 2613670, 19033529.
63. Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM. Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci USA 2009, 106(13):5418-5423. 10.1073/pnas.0811088106, 2664011, 19276109.
64. Kam J, Gresshoff PM, Shorter R, Xue G. The Q-type C(2)H(2) zinc finger subfamily of transcription factors in Triticum aestivum is predominantly expressed in roots and enriched with members containing an EAR repressor motif and responsive to drought stress. Plant Mol Biol 2008, 67(3):305-322. 10.1007/s11103-008-9319-3, 18347915.
65. Soderman E, Hjellstrom M, Fahleson J, Engstrom P. The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions. Plant Mol Biol 1999, 40(6):1073-1083. 10.1023/A:1006267013170, 10527431.
66. Himmelbach A, Hoffmann T, Leube M, Hohener B, Grill E. Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 2002, 21(12):3029-3038. 10.1093/emboj/cdf316, 126069, 12065416.
67. Zaina G, Morassutti C, De Amicis F, Fogher C, Marchetti S. Endonuclease genes up-regulated in tissues undergoing programmed cell death are expressed during male gametogenesis in barley. Gene 2003, 315:43-50.
68. Aoyagi S, Sugiyama M, Fukuda H. BEN1 and ZEN1 cDNAs encoding S1-type DNases that are associated with programmed cell death in plants. FEBS Lett 1998, 429(2):134-138. 10.1016/S0014-5793(98)00563-8, 9650576.
69. Muramoto Y, Watanabe A, Nakamura T, Takabe T. Enhanced expression of a nuclease gene in leaves of barley plants under salt stress. Gene 1999, 234(2):315-321. 10.1016/S0378-1119(99)00193-6, 10395904.
70. Helm M, Schmid M, Hierl G, Terneus K, Tan L, Lottspeich F, Kieliszewski MJ, Gietl C. KDEL-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds. Am J Bot 2008, 95(9):1049-1062. 10.3732/ajb.2007404, 21632425.
71. Martinez M, Cambra I, Carrillo L, Diaz-Mendoza M, Diaz I. Characterization of the entire cystatin gene family in barley and their target Cathepsin L-Like Cysteine-Proteases, partners in the hordein mobilization during seed germination. Plant Physiol 2009, 151(3):1531-1545. 10.1104/pp.109.146019, 2773090, 19759340.
72. Martinez DE, Bartoli CG, Grbic V, Guiamet JJ. Vacuolar cysteine proteases of wheat (Triticum aestivum L.) are common to leaf senescence induced by different factors. J Exp Bot 2007, 58(5):1099-1107. 10.1093/jxb/erl270, 17218544.
73. Gilroy EM, Hein I, van der Hoorn R, Boevink PC, Venter E, McLellan H, Kaffarnik F, Hrubikova K, Shaw J, Holeva M, Lopez EC, Borras-Hidalgo O, Pritchard L, Loake GJ, Lacomme C, Birch PRJ. Involvement of cathepsin B in the plant disease resistance hypersensitive response. Plant J 2007, 52(1):1-13. 10.1111/j.1365-313X.2007.03226.x, 17697096.
74. Rampino P, Pataleo S, Falco V, Mita G, Perrotta C. Identification of candidate genes associated with senescence in durum wheat (Triticum turgidum subsp durum) using cDNA-AFLP. Mol Biol Rep 2011, 38(8):5219-5229. 10.1007/s11033-010-0673-2, 21197602.
75. Krupinska K, Haussuhl K, Schafer A, van der Kooij TAW, Leckband G, Lorz H, Falk J. A novel nucleus-targeted protein is expressed in barley leaves during senescence and pathogen infection. Plant Physiol 2002, 130(3):1172-1180. 10.1104/pp.008565, 166638, 12427984.
76. Rousseau F, Setif P, Lagoutte B. Evidence for the involvement of PSI-E subunit in the reduction of ferredoxin by Photosystem-I. EMBO J 1993, 12(5):1755-1765. 413394, 8387913.
77. Sonoike K. Photoinhibition of Photosystem I. physiol Plantarum 2011, 142(1):56-64.
78. Yi X, Hargett SR, Frankel LK, Bricker TM. The PsbP protein, but not the PsbQ protein, is required for normal thylakoid architecture in Arabidopsis thaliana. FEBS Lett 2009, 583(12):2142-2147. 10.1016/j.febslet.2009.05.048, 19500580.
79. de Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall'Osto L. Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted Photosystem II macrostructure and are defective in photoprotection. Plant Cell 2011, 23(7):2659-2679. 10.1105/tpc.111.087320, 3226214, 21803939.
80. Pfannschmidt T, Schütze K, Brost M, Oelmüller R. A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 2001, 276(39):36125-36130. 10.1074/jbc.M105701200, 11468291.
81. Fey V, Wagner R, Bräutigam K, Pfannschmidt T. Photosynthetic redox control of nuclear gene expression. J Exp Bot 2005, 56(416):1491-1498. 10.1093/jxb/eri180, 15863445.
82. Pfannschmidt T, Bräutigam K, Wagner R, Dietzel L, Schröter Y, Steiner S, Nykytenko A. Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot 2009, 103(4):599-607. 2707342, 18492734.
83. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 2012, 63(4):1637-1661. 10.1093/jxb/ers013, 22371324.
84. Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 2005, 17(7):1866-1875. 10.1105/tpc.105.033589, 1167537, 15987996.
85. Bienert GP, Moller ALB, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 2007, 282(2):1183-1192. 10.1074/jbc.M603761200, 17105724.
86. Hoque TS, Uraji M, Ye W, Hossain MA, Nakamura Y, Murata Y. Methylglyoxal-induced stomatal closure accompanied by peroxidase-mediated ROS production in Arabidopsis. J Plant Physiol 2012, 169(10):979-986. 10.1016/j.jplph.2012.02.007, 22437147.
87. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 2003, 22(11):2623-2633. 10.1093/emboj/cdg277, 156772, 12773379.
88. Luan S. The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 2009, 14(1):37-42. 10.1016/j.tplants.2008.10.005, 19054707.
89. Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim B, Lee S, Kudla J, Luan S. Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 2007, 52(2):223-239. 10.1111/j.1365-313X.2007.03236.x, 17922773.
90. Coello P, Hey SJ, Halford NG. The sucrose non-fermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield. J Exp Bot 2011, 62(3):883-893. 10.1093/jxb/erq331, 20974737.
91. Chen L, Ren F, Zhou L, Wang Q, Zhong H, Li X. The Brassica napus Calcineurin B-Like 1/CBL-interacting protein kinase 6 (CBL1/CIPK6) component is involved in the plant response to abiotic stress and ABA signalling. J Exp Bot 2012, 63(17):6211-6222. 10.1093/jxb/ers273, 3481211, 23105131.
92. Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. Plos Genetics 2012, 8(6):e1002767. 10.1371/journal.pgen.1002767, 3386168, 22761583.
93. Miller G, Shulaev V, Mittler R. Reactive oxygen signaling and abiotic stress. Physiol Plantarum 2008, 133(3):481-489.
94. Krasensky J, Jonak C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 2012, 63(4):1593-1608. 10.1093/jxb/err460, 22291134.
95. Vijn I, Smeekens S. Fructan: more than a reserve carbohydrate?. Plant Physiol 1999, 120(2):351-359. 10.1104/pp.120.2.351, 1539216, 10364386.
96. Xue G, McIntyre CL, Jenkins CLD, Glassop D, van Herwaarden AF, Shorter R. Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiol 2008, 146(2):441-454. 2245852, 18083795.
97. Park YB, Cosgrove DJ. Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis. Plant Physiol 2012, 158(1):465-475. 10.1104/pp.111.189779, 3252101, 22108526.
98. Wormit A, Butt SM, Chairam I, McKenna JF, Nunes-Nesi A, Kjaer L, O'Donnelly K, Fernie AR, Woscholski R, Barter MCL, Hamann T. Osmosensitive changes of carbohydrate metabolism in response to cellulose biosynthesis inhibition. Plant Physiol 2012, 159(1):105-117. 10.1104/pp.112.195198, 3375954, 22422940.
99. Keunen E, Peshev D, Vangronsveld J, Van Den Ende W, Cuypers A. Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 2013, doi:10.1111/pce.12061.
100. Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR. Protein degradation - an alternative respiratory substrate for stressed plants. Trends Plant Sci 2011, 16(9):489-498.
101. Mohammadi M, Kav NNV, Deyholos MK. Transcriptional profiling of hexaploid wheat (Triticum aestivum L.) roots identifies novel, dehydration-responsive genes. Plant Cell Environ 2007, 30(5):630-645. 10.1111/j.1365-3040.2007.01645.x, 17407540.
102. Fujiki Y, Ito M, Itoh T, Nishida I, Watanabe A. Activation of the promoters of Arabidopsis genes for the branched-chain alpha-keto acid dehydrogenase complex in transgenic tobacco BY-2 cells under sugar starvation. Plant Cell Physiol 2002, 43(3):275-280. 10.1093/pcp/pcf032, 11917081.
103. Taylor NL, Heazlewood JL, Day DA, Millar AH. Lipoic acid-dependent oxidative catabolism of alpha-keto acids in mitochondria provides evidence for branched-chain amino acid catabolism in Arabidopsis. Plant Physiol 2004, 134(2):838-848. 10.1104/pp.103.035675, 344558, 14764908.
104. Galili G. The aspartate-family pathway of plants: linking production of essential amino acids with energy and stress regulation. Plant Signal Behav 2011, 6(2):192-5. 10.4161/psb.6.2.14425, 3121977, 21512320.
105. Xu H, Zhang J, Zeng J, Jiang L, Liu E, Peng C, He Z, Peng X. Inducible antisense suppression of glycolate oxidase reveals its strong regulation over photosynthesis in rice. J Exp Bot 2009, 60(6):1799-1809. 10.1093/jxb/erp056, 19264754.
106. Miyashita Y, Good AG. NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark-induced carbon starvation. J Exp Bot 2008, 59(3):667-680. 10.1093/jxb/erm340, 18296429.
107. Renault H, El Amrani A, Berger A, Mouille G, Soubigou-Taconnat L, Bouchereau A, Deleu C. γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant Cell Environ 2013, 36(5):1009-1018. 10.1111/pce.12033, 23148892.
108. Melo-Oliveira R, Oliveira IC, Coruzzi GM. Arabidopsis mutant analysis and gene regulation define a nonredundant role for glutamate dehydrogenase in nitrogen assimilation. Proc Natl Acad Sci USA 1996, 93(10):4718-4723. 10.1073/pnas.93.10.4718, 39345, 8643469.
109. Matiolli CC, Tomaz JP, Duarte GT, Prado FM, Vieira Del Bem LE, Silveira AB, Gauer L, Guedes Correa LG, Drumond RD, Carvalho Viana AJ, Di Mascio P, Meyer C, Vincentz M. The Arabidopsis bZIP gene AtbZIP63 is a sensitive integrator of transient abscisic acid and glucose signals. Plant Physiol 2011, 157(2):692-705. 10.1104/pp.111.181743, 3192551, 21844310.
110. Dietz K, Vogel MO, Viehhauser A. AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 2010, 245(1-4):3-14.
111. Price J, Laxmi A, St Martin SK, Jang JC. Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 2004, 16(8):2128-2150. 10.1105/tpc.104.022616, 519203, 15273295.
112. Ndamukong I, Jones DR, Lapko H, Divecha N, Avramova Z. Phosphatidylinositol 5-Phosphate links dehydration stress to the activity of ARABIDOPSIS TRITHORAX-LIKE Factor ATX1. Plos One 2010, 5(10):e13396. 10.1371/journal.pone.0013396, 2954176, 20967218.
113. Wilson PB, Estavillo GM, Field KJ, Pornsiriwong W, Carroll AJ, Howell KA, Woo NS, Lake JA, Smith SM, Harvey Millar A, Von Caemmerer S, Pogson BJ. The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J 2009, 58(2):299-317. 10.1111/j.1365-313X.2008.03780.x, 19170934.
114. Zadoks JC, Chang TT, Konzak CF. Decimal code for growth stages of cereals. Weed Res 1974, 14(6):415-421.
115. Villegas D, Aparicio N, Blanco R, Royo C. Biomass accumulation and main stem elongation of durum wheat grown under Mediterranean conditions. Ann Bot 2001, 88(4):617-627.
116. Taylor KL, Brackenridge AE, Vivier MA, Oberholster A. High-performance liquid chromatography profiling of the major carotenoids in Arabidopsis thaliana leaf tissue. J Chromatogr A 2006, 1121(1):83-91. 10.1016/j.chroma.2006.04.033, 16701678.
117. Britton G, Liaaen-Jensen S, Pfander H. Carotenoids: Handbook 2004, Birkhäuser: Basel.
118. Aprile A, Federici C, Close TJ, De Bellis L, Cattivelli L, Roose ML. Expression of the H plus -ATPase AHA10 proton pump is associated with citric acid accumulation in lemon juice sac cells. Funct Integr Genomics 2011, 11(4):551-563. 10.1007/s10142-011-0226-3, 21556928.
119. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4(2):249-264. 10.1093/biostatistics/4.2.249, 12925520.
120. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20(3):307-315. 10.1093/bioinformatics/btg405, 14960456.
121. Benjamini Y, Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 1995, 57(1):289-300.
122. Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Guldener U, Mannhaupt G, Munsterkotter M, Mewes HW. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 2004, 32(18):5539-5545. http://mips.helmholtz-muenchen.de/proj/funcatDB, 10.1093/nar/gkh894, 524302, 15486203.
123. Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA. PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res 2012, 40(D1):D1194-D1201. http://www.plexdb.org, 10.1093/nar/gkr938, 3245067, 22084198.
124. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45. 10.1093/nar/29.9.e45, 55695, 11328886.
125. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3(7):0034.1.
126. Jiang Q, Chen H, Pan X, Pan Q, Shi Y, Li X, Zhang G, Wang Y, Xie S, Shen S. Proteomic analysis of wheat (Triticum aestivum L.) hybrid necrosis. Plant Sci 2008, 175(3):394-401.
127. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 1976, 72(1-2):248-254.
128. Perez-Hedó M, Sanchez-Lopez I, Eizaguirre M. Comparative analysis of hemolymph proteome maps in diapausing and non-diapausing larvae of Sesamia nonagrioides. Proteome Sci 2012, 10(1):58. 10.1186/1477-5956-10-58, 3542258, 23021110.