Growth inhibition by selenium is associated with changes in primary metabolism and nutrient levels in Arabidopsis thaliana

Plant Cell and Environment

Volumn 39, Issue 10, 2016, Pages 2235-2246

  Ribeiro, Dimas M ^a   Silva Júnior, Dalton D ^a   Cardoso, Flávio Barcellos ^a   Martins, Auxiliadora O ^a   Silva, Welder A ^a   Nascimento, Vitor L ^a   Araújo, Wagner L ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

Author keywords

carbon metabolism; cell wall; photosynthesis; plant growth; starch turnover; TCA cycle

Indexed keywords

CARBON; CELLS AND CELL COMPONENTS; GENE EXPRESSION; GROWTH RATE; HERB; INHIBITION; METABOLISM; NUTRIENT DYNAMICS; ORGANIC ACID; PHOTOSYNTHESIS; ROOT SYSTEM; SELENIUM; STARCH;

ARABIDOPSIS THALIANA;

CARBON; SELENIUM;

ARABIDOPSIS; CELL WALL; CITRIC ACID CYCLE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PLANT ROOT; SHOOT;

ARABIDOPSIS; CARBON; CELL WALL; CITRIC ACID CYCLE; GENE EXPRESSION REGULATION, PLANT; PHOTOSYNTHESIS; PLANT ROOTS; PLANT SHOOTS; SELENIUM; STRESS, PHYSIOLOGICAL;

EID: 84981335360     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12783     Document Type: Article

References (59)

1. Araújo W.L., Nunes-Nesi A., Nikoloski Z., Sweetlove L.J. & Fernie A.R. (2012) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant, Cell and Environment 35(1), 1–21.
2. Arvidsson S., Kwasniewski M., Riano-Pachon D.M. & Mueller-Roeber B. (2008) QuantPrime – a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics 9, 465.
3. Baerenfaller K., Massonnet C., Walsh S., Baginsky S., Bühlmann P., Hennig L. & Gruissem W. (2012) Systems-based analysis of Arabidopsis leaf growth reveals adaptation to water deficit. Molecular Systems Biology 8, 606.
4. Caldana C., Scheible W.R., Mueller-Roeber B. & Ruzicic S. (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3, 7.
5. Cross J.M., Von Korff M., Altmann T., Bartzetko L., Sulpice R., Gibon Y., …, Stitt M. (2006) Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiology 142, 1574–1588.
6. Davis T.Z., Stegelmeier B.L., Panter K.E., Cook D., Gardner D.R. & Hall J.O. (2012) Toxicokinetics and pathology of plant-associated acute selenium toxicosis in steers. Journal of Veterinary Diagnostic Investigation 24, 319–327.
7. Dimkovikj A., Fisher B., Hutchison K. & Van Hoewyk D. (2015) Stuck between a ROS and a hard place: Analysis of the ubiquitin proteasome pathway in selenocysteine treated Brassica napus reveals different toxicities during selenium assimilation. Journal of Plant Physiology 181, 50–54.
8. Dimkovikj A. & Van Hoewyk D. (2014) Selenite activates the alternative oxidase pathway and alters primary metabolism in Brassica napus roots: evidence of a mitochondrial stress response. BMC Plant Biology 14, 259.
9. Feng R., Wei C. & Tu S. (2013) The roles of selenium in protecting plants against abiotic stresses. Environmental and Experimental Botany 87, 58–68.
10. Fernie A.R. & Stitt M. (2012) On the discordance of metabolomics with proteomics and transcriptomics: Coping with increasing complexity in logic, chemistry, and network interactions scientific correspondence. Plant Physiology 158, 1139–1145.
11. Fernie A.R., Trethewey R.N., Krotzky A.J. & Willmitzer L. (2004) Metabolite profiling: from diagnostics to systems biology. Nature Reviews. Molecular Cell Biology 5, 763–769.
12. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Hohne M, Hendriks JHM, …, Stitt M (2004) A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. The Plant Cell 16, 3304–3325.
13. Gibon Y., Pyl E.T., Sulpice R., Lunn J.E., Höhne M., Günther M. & Stitt M. (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant, Cell and Environment 32(7), 859–874.
14. Goh H.H., Sloan J., Dorca-Fornell C. & Fleming A.J. (2012) Inducible repression of multiple expansin genes leads to growth suppression during leaf development. Plant Physiology 159, 1759–1770.
15. Guerrero B., Llugany M., Palacios O. & Valiente M. (2014) Dual effects of different selenium species on wheat. Plant Physiology and Biochemistry 83, 300–307.
16. Hamilton S.J. (2004) Review of selenium toxicity in the aquatic food chain. Science of the Total Environment 326, 1–31.
17. Hummel I., Pantin F., Sulpice R., Piques M., Rolland G., Dauzat M. & Muller B. (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: An integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiology 154, 357–372.
18. 2 labeling and analysis of enrichment in individual amino acids in their free pools and in protein. Plant Physiology 168(1), 74–93.
19. Kopka J., Schauer N., Krueger S., Birkemeyer C., Usadel B., Bergmuller E., …, Stitt M. (2005) GMD@CSB.DB: the golm metabolome database. Bioinformatics 21, 1635–1638.
20. Lehotai N., Lyubenova L., Schröder P., Feigl G., Ördög A., Szilágyi K., …, Kolbert Z. (2016) Nitro-oxidative stress contributes to selenite toxicity in pea (Pisum sativum L). Plant and Soil 400, 107–122.
21. Lemire J., Mailloux R., Auger C., Whalen D. & Appanna V.D. (2010) Pseudomonas fluorescens orchestrates a fine metabolic-balancing act to counter aluminium toxicity. Environmental Microbiology 12(6), 1384–90.
22. Li H.F., McGrath S.P. & Zhao F.J. (2008) Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytologist 178, 92–102.
23. Lisec J., Schauer N., Kopka J., Willmitzer L. & Fernie A.R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1, 387–396.
24. Michaeli S., Fait A., Lagor K., Nunes-Nesi A., Grillich N., Yellin A., …, Fromm H. (2011) A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism. The Plant Journal 67, 485–98.
25. Misra S., Boylan M., Selvam A., Spallholz J.E. & Björnstedt M. (2015) Redox-active selenium compounds – from toxicity and cell death to cancer treatment. Nutrients 7, 3536–3556.
26. Nancharaiah Y.V. & Lens P.N. (2015) Ecology and biotechnology of selenium-respiring bacteria. Microbiology Molecular Biology Reviews 79, 61–80.
27. Nawaz F., Ashraf M.Y., Ahmad R., Waraich E.A., Shabbir R.N. & Bukhari M.A. (2015) Supplemental selenium improves wheat grain yield and quality through alterations in biochemical processes under normal and water deficit conditions. Food Chemistry 175, 350–357.
28. Nunes-Nesi A., Fernie A.R. & Stitt M. (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Molecular Plant 3, 973–996.
29. Pal S.K., Liput M., Piques M., Ishihara H., Obata T., Martins M.C., …, Stitt M. (2013) Diurnal changes of polysome loading track sucrose content in the rosette of wild-type Arabidopsis and the starchless pgm mutant. Plant Physiology 162(3), 1246–65.
30. Pantin F., Simonneau T., Rolland G., Dauzat M. & Muller B. (2011) Control of leaf expansion: a developmental switch from metabolics to hydraulics. Plant Physiology 156, 803–815.
31. Pfeifer J., Kirchgessner N., Colombi T. & Walter A. (2015) Rapid phenotyping of crop root systems in undisturbed field soils using X-ray computed tomography. Plant Methods 11, 41.
32. Pilkington S.M., Encke B., Krohn N., Höhne M., Stitt M. & Pyl E.T. (2015) Relationship between starch degradation and carbon demand for maintenance and growth in Arabidopsis thaliana in different irradiance and temperature regimes. Plant, Cell and Environment 38, 157–171.
33. Pilon-Smits E.A., Quinn C.F., Tapken W., Malagoli M. & Schiavon M. (2009) Physiological functions of beneficial elements. Current Opinion in Plant Biology 12, 267–274.
34. Piques M., Schulze W.X., Hohne M., Usadel B., Gibon Y., Rohwer J. & Stitt M. (2009) Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Molecular Systems Biology 5, 314.
35. Pyl E.T., Piques M., Ivakov A., Schulze W., Ishihara H., Stitt M. & Sulpice R. (2012) Metabolism and growth in Arabidopsis depend on the daytime temperature but are temperature-compensated against cool nights. The Plant Cell 24, 2443–2469.
36. 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. Analytical Biochemistry 363, 58–69.
37. Renault H., El Amrani A., Berger A., Mouille G., Soubigou-Taconnat L., Bouchereau A. & Deleu C. (2013) γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis. Plant Cell and Environment 36, 1009–1018.
38. Saidi I., Chtourou Y. & Djebali W. (2014) Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. Journal Plant Physiology 171(5), 85–91.
39. Schiavon M., Pilon M., Malagoli M. & Pilon-Smits E.A. (2015) Exploring the importance of sulfate transporters and ATP sulphurylases for selenium hyperaccumulation a comparison of Stanleya pinnata and Brassica juncea (Brassicaceae). Frontiers Plant Science 6, 2.
40. Shibagaki N., Rose A., McDermott J.P., Fujiwara T., Hayashi H., Yoneyama T. & Davies J.P. (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. The Plant Journal 29, 475–48.
41. Singh R., Lemire J., Mailloux R.J., Chénier D., Hamel R. & Appanna V.D. (2009) An ATP and oxalate generating variant tricarboxylic acid cycle counters aluminum toxicity in Pseudomonas fluorescens. PloS One 4, e7344.
42. Smith A.M. & Stitt M. (2007) Coordination of carbon supply and plant growth. Plant, Cell & Environment 30, 1126–1149.
43. Stitt M. & Zeeman S.C. (2012) Starch turnover: pathways, regulation and role in growth. Current Opinion in Plant Biology 15, 282–292.
44. Studart-Guimarães C., Fait A., Nunes-Nesi A., Carrari F., Usadel B. & Fernie A.R. (2007) Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the gamma-aminobutyrate shunt in illuminated tomato leaves. Plant Physiology 145, 626–639.
45. Sulpice R., Flis A., Ivakov A.A., Apelt F., Krohn N., Encke B. & Stitt M. (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Molecular Plant 7, 137–155.
46. Sulpice R, Trenkamp S, Steinfath M, Usadel B, Gibon Y, Witucka-Wall H, …, Stitt M. (2010) Network analysis of enzyme activities and metabolite levels and their relationship to biomass in a large panel of Arabidopsis accessions. The Plant Cell 22, 2872–2893.
47. Sun X., Zhong Y., Huang Z. & Yang Y. (2014) Selenium accumulation in unicellular green alga Chlorella vulgaris and its effects on antioxidant enzymes and content of photosynthetic pigments. PloS One 9, 11.
48. Sweetlove L.J., Beard K.F.M., Nunes-Nesi A., Fernie A.R. & Ratcliffe R.G. (2010) Not just a circle: flux modes in the plant TCA cycle. Trends in Plant Science 15(8), 462–470.
49. Tamaoki M., Freeman J.L. & Pilon-Smits E.A. (2008) Cooperative ethylene and jasmonic acid signaling regulates selenite resistance in Arabidopsis. Plant Physiology 146, 1219–1230.
50. Terry N., Zayed A.M., de Souza M.P. & Tarun A.S. (2000) Selenium in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 51, 401–432.
51. Vallentine P., Hung C.Y., Xie J. & Van Hoewyk D. (2014) The ubiquitin–proteasome pathway protects Chlamydomonas reinhardtii against selenite toxicity, but is impaired as reactive oxygen species accumulate. AoB Plants 6, plu062.
52. Van Hoewyk D. (2013) A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to selenium stress in plants. Annals of Botany 112, 965–972.
53. Van Hoewyk D., Takahashi H., Inoue E., Hess A., Tamaoki M. & Pilon-Smits E.A. (2008) Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiologia Plantarum 132, 236–53.
54. Van Sandt V.S.T., Suslov D., Verbelen J.P. & Vissenberg K. (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Annals of Botany 100, 1467–1473.
55. Wallenberg M., Misra S., Wasik A.M., Marzano C., Björnstedt M., Gandin V. & Fernandes A.P. (2014) Selenium induces a multi-targeted cell death process in addition to ROS formation. Journal of Cellular and Molecular Medicine 18(4), 671–684.
56. Wang P., Menzies N.W., Lombi E., McKenna B.A., James S., Tang C. & Kopittke P.M. (2015) Synchrotron-based X-ray absorption near-edge spectroscopy imaging for laterally resolved speciation of selenium in fresh roots and leaves of wheat and rice. Journal of Experimental Botany 66(15), 4795–4806.
57. Yang P., Fu H., Walker J., Papa C.M., Smalle J., Ju Y.M. & Vierstra R.D. (2004) Purification of the Arabidopsis 26 S Proteasome: Biochemical and molecular analyses revealed the presence of multiple isoforms. Journal of Biological Chemistry 279(8), 6401–6413.
58. Yazdanbakhsh N., Sulpice R., Graf A., Stitt M. & Fisahn J. (2011) Circadian control of root elongation and C partitioning in Arabidopsis thaliana. Plant, Cell & Environment 34, 877–894.
59. Zhong L. & Holmgren A. (2000) Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. The Journal of Biological Chemistry 275, 18121–18128.