Plastidic phosphoglucose isomerase is an important determinant of starch accumulation in mesophyll cells, growth, photosynthetic capacity, and biosynthesis of plastidic cytokinins in Arabidopsis

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Bahaji, Abdellatif ^a   Sánchez López, Ángela M ^a   De Diego, Nuria ^b   Muñoz, Francisco J ^a   Baroja Fernández, Edurne ^a   Li, Jun ^a   Ricarte Bermejo, Adriana ^a   Baslam, Marouane ^a   Aranjuelo, Iker ^c   Almagro, Goizeder ^a   Humplík, Jan F ^b   Novák, Ondřej ^b   Spíchal, Lukáš ^c   Doležal, Karel ^c   Pozueta Romero, Javier ^a  

^a INSTITUTO DE AGROBIOTECNOLOGÍA   (Spain)

^b PALACKÝ UNIVERSITY   (Czech Republic)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

2 C METHYL D ERYTHRITOL 4 PHOSPHATE; BETA AMYLASE; CYTOKININ; GLUCOSE 6 PHOSPHATE ISOMERASE; PHOSPHATE; STARCH; UNCLASSIFIED DRUG; 2-C-METHYLERYTHRITOL 4-PHOSPHATE; ARABIDOPSIS PROTEIN; ERYTHRITOL; SUGAR PHOSPHATE;

ARABIDOPSIS; ARTICLE; BIOACCUMULATION; BIOSYNTHESIS; CELL GRANULE; CELL GROWTH; CHLOROPLAST; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; GENE; GENE FREQUENCY; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GROWTH RATE; GUARD CELL; INTRON; MESOPHYLL CELL; MICROSCOPY; MOLECULAR DYNAMICS; NULL ALLELE; PHENOTYPE; PHOSPHOGLUCOSE ISOMERASE 1 GENE; PHOSPHOGLUCOSE ISOMERASE 2 GENE; PHOSPHOGLUCOSE ISOMERASE 3 GENE; PHOSPHOGLUCOSE ISOMERASE GENE; PHOTOSYNTHETIC CAPACITY; PLANT GENE; PLANT GROWTH; PLANT LEAF; PLANT PARAMETERS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX1 GENE; SIGNAL TRANSDUCTION; ALLELE; ANALOGS AND DERIVATIVES; CHEMISTRY; GENE LOCUS; GENETICS; METABOLISM; MUTATION; PHOTOSYNTHESIS;

ARABIDOPSIS;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOKININS; ERYTHRITOL; GENETIC LOCI; GLUCOSE-6-PHOSPHATE ISOMERASE; MESOPHYLL CELLS; METABOLIC NETWORKS AND PATHWAYS; MUTATION; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAVES; STARCH; SUGAR PHOSPHATES;

EID: 84926060100     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119641     Document Type: Article

References (121)

1. Bahaji A, Li J, Sánchez-López AM, Baroja-Fernández E, Muñoz FJ, Ovecka M, et al. (2014b) Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields. Biotechnol Adv 32: 87-106. doi: 10.1016/j.biotechadv.2013.06.006 PMID: 23827783
2. Stitt M and Quick WP (1989) Photosynthetic carbon partitioning: its regulation and possibilities for manipulation. Physiol Plantarum 77: 633-641.
3. Rao M, Terry N (1995) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet. Plant Physiol 107: 195-202.
4. Dreier W, Schnarrenberger C, Börner T (1995) Light- and stress-dependent enhancement of amylolytic activities in white and green barley leaves: beta-amylases are stress-induced proteins. J Plant Physiol 145: 342-348.
5. Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44: 730-743. PMID: 16297066
6. Ezquer I, Li J, Ovecka M, Baroja-Fernández E, Muñoz FJ, Montero M, et al. (2010) Microbial volatile emissions promote accumulation of exceptionally high levels of starch in leaves in mono- and dicotyledonous plants. Plant Cell Physiol 51: 1674-1693. doi: 10.1093/pcp/pcq126 PMID: 20739303
7. Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P, Trost P, et al. (2010) Thioredoxin-regulated β-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. J Exp Bot 62: 545-555. doi: 10.1093/jxb/erq288 PMID: 20876336
8. Li J, Ezquer I, Bahaji A, Montero M, Ovecka M, Baroja-Fernández E, et al. (2011) Microbial volatiles induced accumulation of exceptionally high levels of starch in Arabidopsis leaves is a process involving NTRC and starch synthases class III and IV. Mol Plant Microbe Interact 24: 1165-1178. doi: 10.1094/MPMI-05-11-0112 PMID: 21649509
9. Sulpice R, Pyl E-T, Ishihara H, Trenkamp S, Steinfath M, Witucka-Wall H, et al. (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci USA 106: 10348-10353. doi: 10.1073/pnas.0903478106 PMID: 19506259
10. Werner T, Holst K, Pörs Y, Guivarc'h A, Mustroph A, Chiriqui D, et al. (2008) Cytokinin deficiency causes distinct changes of sink and source parameters in tobacco shoots and roots. J Exp Bot 59: 2659-2672. doi: 10.1093/jxb/ern134 PMID: 18515826
11. Erickson JL, Ziegler J, Guevara D, Abel S, Klösgen RB, Mathur J, et al. (2014) Agrobacterium-derived cytokinin influences plastid morphology and starch accumulation in Nicotiana benthamiana during transient assay. BMC Plant Biol 14: 127. doi: 10.1186/1471-2229-14-127 PMID: 24886417
12. Ramon M, Rolland F, Thevelein JM, Van Dijck P, Leyman B (2007) ABI4 mediates the effects of exogenous trehalose on Arabidopsis growth and starch breakdown. Plant Mol Biol 63: 195-206. PMID: 17031512
13. Muñoz-Bertomeu J, Bermúdez MA, Segura J, Ros R. (2011) Arabidopsis plants deficient in plastidial glyceraldehyde-3-phosphate dehydrogenase show alterations in abscisic acid (ABA) signal transduction: interaction between ABA and primary metabolism. J Exp Bot 62: 1229-1239. doi: 10.1093/jxb/erq353 PMID: 21068209
14. Schlüter U, Köpke D, Altmann T, Müssig C (2002) Analysis of carbohydrate metabolism of CPD antisense plants and the brassinosteroid-deficient cbb1 mutant. Plant Cell Environ 25: 783-791.
15. Oh M-H, Sun J, Oh DH, Zielinski RE, Clouse SD, Huber SC (2011) Enhancing Arabidopsis leaf growth by engineering the BRASSINOSTEROID INSENSITIVE1 receptor kinase. Plant Physiol 157: 120-131. doi: 10.1104/pp.111.182741 PMID: 21795582
16. Arnon DI (1955) The chloroplast as a complete photosynthetic unit. Science 122: 9-16. PMID: 14385811
17. Streb S, Egli B, Eicke S, Zeeman SC (2009) The debate on the pathway of starch synthesis: a closer look at low-starch mutants lacking plastidial phosphoglucomutase supports the chloroplast-localised pathway. Plant Physiol 151: 1769-1772. doi: 10.1104/pp.109.144931 PMID: 19776162
18. Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opinion Plant Biol 15: 1-11.
19. Kleczkowski LA (1999) A phosphoglycerate to inorganic phosphate ratio is the major factor in controlling starch levels in chloroplasts via ADP-glucose pyrophosphorylase regulation. FEBS Lett 448: 153-156. PMID: 10217430
20. Kleczkowski LA (2000) Is leaf ADP-glucose pyrophosphorylase an allosteric enzyme? Biochim Biophys Acta 1476: 103-108. PMID: 10606772
21. Heuer B, Hansen MJ, Anderson LE (1982) Light modulation of phosphofructokinase in pea leaf chloroplasts. Plant Physiol 69: 1404-1406. PMID: 16662412
22. Dietz K-J (1985) A possible rate-limiting function of chloroplast hexosemonophosphate isomerase in starch synthesis of leaves. Biochem Biophys Acta 839: 240-248.
23. Sharkey TD, Vassey TL (1989) Low oxygen inhibition of photosynthesis is caused by inhibition of starch synthesis. Plant Physiol 90: 385-387. PMID: 16666779
24. Jones TWA, Gottlieb LD, Pichersky E (1986) Reduced enzyme activity and starch level in an induced mutant of chloroplast phosphoglucose isomerase. Plant Physiol 81: 367-371. PMID: 16664822
25. Kruckeberg AL, Neuhaus HE, Feil R, Gottlieb LD, Sitt M (1989) Decreased-acitivity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. Biochem J 261: 457-467. PMID: 2775228
26. Yu T-S, Lue W-L, Wang S-M, Chen J (2000) Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiol 123: 319-325. PMID: 10806248
27. Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US, et al. (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17: 760-775. PMID: 15722468
28. Kunz HH, Häusler RE, Fettke J, Herbst K, Niewiadomski P, Gierth M, et al. (2010) The role of plastidial glucose-6-phosphate/phosphate translocators in vegetative tissues of Arabidopsis thaliana mutants impaired in starch biosynthesis. Plant Biol (Stuttg) 12 Suppl 1: 115-128. doi: 10.1111/j.1438-8677.2010.00349.x PMID: 20712627
29. Caspar T, Huber SC, Somerville C (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol 79: 11-17. PMID: 16664354
30. Kofler H, Häusler RE, Schulz B, Gröner F, Flügge U-I, Weber A (2000) Molecular characterization of a new mutant allele of the plastid phosphoglucomutase in Arabidopsis, and complementation of the mutant with the wild-type cDNA. Mol Gen Genet. 262: 978-986.
31. Ventriglia T, Kuhn ML, Ruiz MT, Ribeiro-Pedro M, Valverde F, Ballicora MA, et al. (2008) Two Arabidopsis ADP-glucose pyrophosphorylase large subunits (APL1 and APL2) are catalytic. Plant Physiol 148: 65-76. doi: 10.1104/pp.108.122846 PMID: 18614708
32. Bahaji A, Li J, Ovecka M, Ezquer I, Muñoz FJ, Baroja-Fernández E, et al. (2011) Arabidopsis thaliana mutants lacking ADP-glucose pyrophosphorylase accumulate starch and wild-type ADP-glucose content: further evidence for the occurrence of important sources, other than ADP-glucose pyrophosphorylase, of ADP-glucose linked to leaf starch biosynthesis. Plant Cell Physiol 52: 1162-1176. doi: 10.1093/pcp/pcr067 PMID: 21624897
33. Tsai HL, Lue WL, Lu KJ, Hsieh MH, Wang SM, Chen J (2009) Starch synthesis in Arabidopsis is achieved by spatial cotranscription of core starch metabolism genes. Plant Physiol 151: 1582-1595. doi: 10.1104/pp.109.144196 PMID: 19759345
34. Yu T-S, Kofler H, Häusler RE, Hille D, Flügge U-I, Zeeman SC, et al. (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13: 1907-1918. PMID: 11487701
35. Edner C, Li J, Albrecht T, Mahlow S, Hejazi M, Hussain H, et al. (2007) Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial β-amylases. Plant Physiol 145: 17-28. PMID: 17631522
36. Kang F, Rawsthorne S (1996) Metabolism of glucose-6-phosphate and utilization of multiple metabolites for fatty acid synthesis by plastids from developing oilseed rape embryos. Planta 199: 321-327.
37. Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber A, et al. (1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 10: 105-117. PMID: 9477574
38. Fox SR, Hill LM, Rawsthorne S, Hills MJ (2000) Inhibition of the glucose-6-phosphate transporter in oilseed rape (Brassica naupul L.) plastids by acyl-CoA thioesters reduces fatty acid synthesis. Biochem. J 352: 525-532. PMID: 11085947
39. Weber A, Flügge U-I (2002) Interaction of cytosolic and plastidic nitrogen metabolism in plants. J Exp Bot 53: 865-874. PMID: 11912229
40. Bowsher CG, Lacey AE, Hanke GT, Clarkson DT, Saker LR, Stulen I, et al. (2007) The effect of Glc6P uptake and its subsequent oxidation within pea root plastids on nitrite reduction and glutamate synthesis. J Exp Bot 58: 1109-1118. PMID: 17220512
41. Zhang L, Häusler RE, Greiten C, Hajirezaei M-R, Haferkamp I, Neuhaus HE, et al. (2008) Overriding the co-limiting import of carbon and energy into tuber amyloplasts increases the starch content and yield of transgenic potato plants. Plant Biotechnol J 6: 453-464. doi: 10.1111/j.1467-7652.2008.00332.x PMID: 18363632
42. Caspar T, Lin TP, Monroe J, Bernhard W, Spilatro S, Preiss J, et al. (1989) Altered regulation of b-amylase activity in mutants of Arabidopsis with lesions in starch metabolism. Proc Natl Acad Sci USA 86: 5830-5833. PMID: 16594057
43. Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kavanagh TA (1999) An Arabidopsis gene encoding a chloroplast-targeted β-amylase. Plant J 20: 519-527. PMID: 10652124
44. Sparla F, Costa A, Schiavo FL, Pupillo P, Trost P (2006) Redox regulation of a novel plastid-targeted β-amylase of Arabidopsis. Plant Physiol 141: 840-850. PMID: 16698902
45. Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, et al. (2008) β-amylase4, a noncatalytic protein required for starch breakdown, acts usptream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell 20: 1040-1058. doi: 10.1105/tpc.107.056507 PMID: 18390594
46. Kaplan F, Guy CL (2004) β-amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135:1674-1684. PMID: 15247404
47. Hendriks JHM, Kolbe A, Gibon Y, Stitt M, Geigenberger P (2003) ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133: 838-849. PMID: 12972664
48. Li J, Almagro G, Muñoz FJ, Baroja-Fernández E, Bahaji A, Montero M, et al. (2012) Posttranslational redox modification of ADP-glucose pyrophosphorylase in response to light is not a major determinant of fine regulation of leaf starch accumulation in Arabidopsis. Plant Cell Physiol 53: 433-444. doi: 10.1093/pcp/pcr193 PMID: 22210900
49. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30: 1126-1149. PMID: 17661751
50. Hanson KR, McHale NA (1988) A starchless mutant of Nicotiana sylvestris containing a modified plastid phosphoglucomutase. Plant Physiol 88: 838-844. PMID: 16666394
51. Lin T-P, Caspar T, Somerville C, Preiss J (1988) Isolation and characterization of a starchless mutant of Arabidopsis thaliana (L.) Heynh lacking ADPglucose pyrophosphorylase activity. Plant Physiol 86: 1131-1135. PMID: 16666044
52. Schneider A, Häusler RE, Kolukisaoglu Ü, Kunze R, van der Graaff E, Schwacke R, et al. (2002) An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J 32: 685-699. PMID: 12472685
53. Ragel P, Streb S, Feil R, Sahrawy M, Annunziata MG, Lunn JE, et al. (2013) Loss of starch granule initiation has a deleterious effect on the growth of Arabidopsis thaliana plants due to accumulation of ADP-glucose. Plant Physiol 163: 75-85. doi: 10.1104/pp.113.223420 PMID: 23872660
54. Kunz HH, Zamani-Nour S, Häusler RE, Ludewig K, Schroeder JI, Malinova I, et al. (2014) Loss of cytosolic phosphoglucose isomerase affects carbohydrate metabolism in leaves and is essential for fertility of Arabidopsis thaliana. Plant Physiol 166: 753-765. doi: 10.1104/pp.114.241091 PMID: 25104722
55. Bahaji A, Baroja-Fernández E, Sánchez-López AM, Muñoz FJ, Li J, Almagro G, et al. (2014a) HPLC-MS/MS analyses show that the near-starchless aps1 and pgm leaves accumulate wild type levels of ADPglucose: further evidence for the occurrence of important ADPglucose biosynthetic pathway(s) alternative to the pPGI-pPGM-AGP pathway. PLoS ONE 9(8): e104997. doi: 10.1371/journal.pone.0104997 PMID: 25133777
56. Lichtenthaler HK, Schwender J, Disch A, RohmerM (1997) Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett 400: 271-274. PMID: 9009212
57. Phillips MA, León P, Boronat A, Rodríguez-Concepción M (2008) The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci 13: 619-623. doi: 10.1016/j.tplants.2008.09.003 PMID: 18948055
58. Pulido P, Perello C, Rodríguez-Concepción M. (2012) New insights into plant isoprenoid metabolism. Mol Plant 5: 964-967. doi: 10.1093/mp/sss088 PMID: 22972017
59. Synková H, Van Loven K, Pospísilová J, Valcke R (1999) Photosynthesis of transgenic Pssu-ipt tobacco. J Plant Physiol 155: 173-182.
60. Yang S, Yu H, Xu Y, Goh CJ (2003) Investigation of cytokinin-deficient phenotypes in Arabidopsis by ectopic expression of orchid DSCKX1. FEBS Lett 555: 291-296. PMID: 14644430
61. Yaronskaya E, Vershilovskaya I, Poers Y, Alawady AE, Averina N, Grimm B (2006) Cytokinin effects on tetrapyrrole biosynthesis and photosynthetic activity in barley seedlings. Planta 224: 700-709. PMID: 16506064
62. Cortleven A, Noben JP, Valcke R (2011) Analysis of the photosynthetic apparatus in transgenic tobacco plants with altered endogenous cytokinin content: a proteomic study. Proteome Sci 9: 33. doi: 10.1186/1477-5956-9-33 PMID: 21703031
63. Cortleven A, Valcke R (2012) Evaluation of the photosynthetic activity in transgenic tobacco plants with altered endogenous cytokinin content: lessons from cytokinin. Physiol Plantarum 144: 394-408. doi: 10.1111/j.1399-3054.2011.01558.x PMID: 22182256
64. Quick WP, Scheibe R, Neuhaus HE (1995) Induction of hexose-phosphate translocator activity in spinach chloroplasts. Plant Physiol 109: 113-121. PMID: 12228584
65. Eicks M, Maurino V, Knappe S, Flügge UI, Fischer K (2002) The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol 128: 512-522. PMID: 11842155
66. Fettke J, Malinova I, Albrecht T, Hejazi M, Steup M (2011) Glucose-1-phosphate transport into protoplasts and chloroplasts from leaves of Arabidopsis. Plant Physiol 155: 1723-1734. doi: 10.1104/pp.110.168716 PMID: 21115809
67. Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Gröner F, et al. (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12: 787-801. PMID: 10810150
68. Giese JO, Herbers K, Hoffmann M, Klösgen RB, Sonnewald U (2005) Isolation and functional characterization of a novel plastidic hexokinase from Nicotiana tabacum. FEBS Lett 579: 827-831. PMID: 15670855
69. Cho MH, Lim H, Shin DH, Jeon JS, Bhoo SH, Park YI, et al. (2011) Role of the plastidic glucose translocator in the export of starch degradation products from the chloroplasts in Arabidopsis thaliana. New Phytol 109: 101-112.
70. Pozueta-Romero J, Ardila F, Akazawa T (1991) ADPglucose transport by adenylate translocator in chloroplasts is linked to starch biosynthesis. Plant Physiol 97: 1565-1572. PMID: 16668585
71. Baroja-Fernández E, Muñoz FJ, Zandueta-Criado A, Morán-Zorzano MT, Viale AM, Alonso-Casajús N, et al. (2004) Most of ADP-glucose linked to starch biosynthesis occurs outside the chloroplast in source leaves. Proc Nat Acad Sci USA 101: 13080-13085. PMID: 15326306
72. 14 in the glucose phosphates formed during photosynthesis. Plant Physiol. 31: 411-412. PMID: 16654912
73. 14 in sugars formed during photosynthesis. Proc. Natl. Acad. Sci. USA 43: 446-451. PMID: 16590038
74. 2. Z. Pflanzenphysiol. 76: 176-181.
75. Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J, et al. (2013) Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell 25: 694-714. doi: 10.1105/tpc.112.106989 PMID: 23444331
76. Schulze W, Stitt M, Schulze ED, Neuhaus HE, Fichtner K (1991) A quantification of the significance of assimilatory starch for growth of Arabidopsis thaliana L. Heynh. Plant Physiol 95: 890-895. PMID: 16668068
77. Huber SC, Hanson KR (1992) Carbon partitioning and growth of a starchless mutant of Nicotiana sylvestris. Plant Physiol 99: 1449-1454. PMID: 16669057
78. Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, et al. (2004) Adjustment of diurnal starch turnover to short days: inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39: 847-862. PMID: 15341628
79. 2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14: 741-762.
80. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Biol 47: 509-540.
81. Herrmann KM (1995) The shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol 107: 7-12. PMID: 7870841
82. Bowsher CG, Boulton EL, Rose J, Nayagam S, Emes MJ (2002) Reductant for glutamate synthase is generated by the oxidative pentose phosphate pathway in non-photosynthetic root plastids. Plant J 2: 893-898. PMID: 12399398
83. Jong F, Thodey K, Lejay LV, BevanMW(2014) Glucose elevates NITRATE TRANSPORTER2.1 protein levels and nitrate activity independently of its HEXOKINASE1-mediated stimulation of NITRATE TRANSPORTER2.1 expression. Plant Physiol 164: 308-320. doi: 10.1104/pp.113.230599 PMID: 24272701
84. Pérez-Ruiz JM, Spínola MC, Kirchsteiger K, Moreno J, Sahrawy M, Cejudo FJ (2006) Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18: 2356-2368. PMID: 16891402
85. Lepistö A, Kangasjärvi S, Luomala E-M, Brader G, Sipari N, Keränen M, et al. (2009) Chloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis. Plant Physiol 149: 1261-1276. doi: 10.1104/pp.108.133777 PMID: 19151130
86. Kirchsteiger K, Ferrández J, Pascual MB, González M, Cejudo FJ (2012) NADPH thioredoxin reductase C is localized in plastids of photosynthetic and nonphotosynthetic tissues and is involved in lateral root formation in Arabidopsis. Plant Cell 24: 1534-1548. doi: 10.1105/tpc.111.092304 PMID: 22505729
87. Lejay L, Wirth J, Pervent M, Cross JM-F, Tillard P, Gojon A (2008) Oxidative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root iron transporters by photosynthesis. Plant Physiol 146: 2036-2053. doi: 10.1104/pp.107.114710 PMID: 18305209
88. Xiong Y, DeFraia C, Williams D, Zhang X, Mou Z (2009) Characterization of Arabidopsis 6-phosphogluconolactonase T-DNA insertion mutants reveals an essential role for the oxidative section of the plastidic pentose phosphate pathway in plant growth and development. Plant Cell Physiol 50: 1277-1291. doi: 10.1093/pcp/pcp070 PMID: 19457984
89. Bussell JD, Keech O, Fenske R, Smith SM (2013) Requirement for the plastidial oxidative pentose phosphate pathway for nitrate assimilation in Arabidopsis. Plant J 75: 578-591. doi: 10.1111/tpj.12222 PMID: 23621281
90. Brauner K, Hörmiller I, Nägele T, Heyer AG (2014) Exaggerated root respiration accounts for growth retardation in a starchless mutant of Arabidopsis thaliana. Plant J 79: 82-91. doi: 10.1111/tpj.12555 PMID: 24836712
91. Frehner M, Pozueta-Romero J, Akazawa T. (1990) Enzyme sets of glycolysis, gluconeogenesis, and oxidative pentose phosphate pathway are not complete in nongreen highly purified amyloplasts of sycamore (Acer pseudoplatanus L.) cell suspension cultures. Plant Physiol 94: 538-544. PMID: 16667746
92. apRees T, Thomas SM, Fuller WA, Chapman B (1975) Location of gluconeogenesis from phosphoenolpyruvate in cotyledons of Cucurbita pepo.Biochem Biophys Acta. 385: 145-156. PMID: 164923
93. Journet EP, Douce R (1985) Enzymic capacities of purified cauliflower bud plastids for lipid synthesis and carbohydrate metabolism. Plant Physiol 79: 458-467. PMID: 16664432
94. Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, et al. (2014) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc Natl Acad Sci USA 111: 7150-7155. doi: 10.1073/pnas.1321519111 PMID: 24778257
95. Rivero RM, Shulaev V, Blumwald E (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol 150: 1530-1540. doi: 10.1104/pp.109.139378 PMID: 19411371
96. Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006) Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis. J Exp Bot 57: 2259-2266. PMID: 16798847
97. Havlová M, Dobrev PI, Motyka V, Storchová H, Libus J, Dobrá J, et al. (2008) The role of cytokinins in responses to water deficit in tobacco plants over-expressing trans-zeating O-glucosyltransferase gene under 35S or SAG12 promoters. Plant Cell Environ 31: 341-353. PMID: 18088334
98. Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol J 9: 747-758. doi: 10.1111/j.1467-7652.2010.00584.x PMID: 21284800
99. Miyazawa Y, Sakai A, Miyagishima S, Takano H, Kawano S, Kuroiwa T (1999) Auxin and cytokinin have opposite effects on amyloplast development and the expression of starch synthesis genes in cultured bright yellow-2 tobacco cells. Plant Physiol 121: 461-469. PMID: 10517837
100. Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98: 10487-10492. PMID: 11504909
101. Kasahara H, Takei K, Ueda N, Hishiyama S, Yamaya T, Kamiya Y, et al. (2004) Distinct isoprenoid origins of cis- and trans-zeatin biosyntheses in Arabidopsis. J Biol Chem 279: 14049-14054. PMID: 14726522
102. Helliwell CA, Sullivan JA, Mould RM, Gray JC, Peacock WJ, Dennis ES (2001) A plastid envelope location of Arabidopsis ent-kaurene oxidase links the plastid and endoplasmic reticulum steps of the gibberellin biosynthesis pathway. Plant J. 28: 201-208.
103. Takei K, Yamaya T, Sakakibara H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J Biol Chem 279: 41866-41872. PMID: 15280363
104. Åstot C, Doležal K, Nordström A, Wang Q, Kunkel T, Moritz T, et al. (2000) An alternative cytokinin biosynthesis pathway. Proc Natl Acad Sci USA 97: 14778-14783. PMID: 11114204
105. Szydlowski N, Ragel P, Raynaud S, Lucas MM, Roldán I, Montero M, et al. (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthase. Plant Cell 21: 2443-2457. doi: 10.1105/tpc.109.066522 PMID: 19666739
106. Clough SJ, Bent A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743. PMID: 10069079
107. Baroja-Fernández E, Muñoz FJ, Li J, Bahaji A, Almagro G, Montero M, et al. (2012) Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production. Proc Natl Acad Sci USA 109: 321-326. doi: 10.1073/pnas.1117099109 PMID: 22184213
108. Kleczkowski LA, Randall DD (1986) Maize leaf adenylate kinase. Purification and partial characterization. Plant Physiol 81: 1110-1114. PMID: 16664952
109. Baroja-Fernández E, Muñoz FJ, Montero M, Etxeberria E, Sesma MT, Ovecka M, et al. (2009) Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield. Plant Cell Physiol 50: 1651-1662. doi: 10.1093/pcp/pcp108 PMID: 19608713
110. Pérez P, Morcuende R, Martín del Molino I, Mártínez-Carrasco R (2005) Diurnal changes of Rubisco in response to elevated CO2, temperature and nitrogen in wheat grown under temperature gradient tunnels. Environ Exp Bot 53: 13-27.
111. Liu X, Zhang S, Shan X, Zhu YG (2005) Toxicity of arsenate and arsenite on germination, seedling growth and amylolitic activity of wheat. Chemosphere 61: 293-301. PMID: 16168752
112. Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: Application to redox profiling during Arabidopsis rosette development. Anal Biochem 363: 58-69. PMID: 17288982
113. Sweetlove LJ, Burrell MM, ap Rees T (1996) Starch metabolism in tubers of transgenic potato (Solanum tuberosum) with increased ADPglucose pyrophosphorylase. Biochem J 320: 493-498. PMID: 8973558
114. Novák O, Hauserová E, Amakorová P, Doležal K, Strnad M (2008) Cytokinin profilig in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69: 2214-2224. doi: 10.1016/j.phytochem.2008.04.022 PMID: 18561963
115. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry and photosynthesis and the gas exchange of leaves. Planta 153: 376-387. doi: 10.1007/BF00384257 PMID: 24276943
116. 2. Plant Physiol 98: 1429-1436. PMID: 16668811
117. Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54: 2393-2401. PMID: 14512377
118. 2 fixation in leaves. Physiol Plantarum 86: 180-187.
119. 2 partia1 pressure and leaf inversion. Planta 189: 182-190.
120. Morales F, Abadía A, Abadía J (1991) Chlorophyll fiuorescence and photon yield of oxygen evolution in iron-deficient sugar beet (Beta vulgaris L.) leaves. Plant Physiol 97: 886-893. PMID: 16668527
121. Spíchal L (2012) Cytokinins - recent news and views of evolutionally old molecules. Funct Plant Biol 39: 267-284.