Abstract
In plant cells, severe oxygen deprivation (hypoxia/anoxia) dramatically curtails the efficient production of adenosine triphosphate (ATP) via mitochondrial oxidative phosphorylation. Survival is mediated in part by limiting energy consumption and maximizing the substrate level production of ATP. This strategy entails regulation of gene expression at transcriptional, posttranscriptional, and translational levels. Based on studies on Arabidopsis thaliana, low oxygen stress promotes an energy conservation program that tailors cytosolic protein synthesis to the proteins required for anaerobic metabolism to maintain cell viability. For example, mRNAs that encode enzymes associated with energy-efficient sucrose catabolism and anaerobic metabolism are efficiently translated. Despite maintained abundance during low oxygen stress, mRNAs encoding proteins associated with growth, such as components of the ribosome, translational machinery, and cell walls, are poorly translated. This chapter summarizes the robust evidence of selective translation during hypoxia and proposes that an important component of this process is the sequestration of mRNAs from the translational machinery until reoxygenation. Cytosolic domains known as stress granules and processing bodies, which in animals contain translationally repressed RNA and RNA-binding proteins, are found in plants. Their possible role in mRNA sequestration and regulation of translational activity is discussed.
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Abbreviations
- ADH:
-
Alcohol dehydrogenase
- AlaAT:
-
Alanine aminotransferase
- ANP:
-
Anaerobic polypeptide
- ANT:
-
Adenine nucleotide translocator
- ATP:
-
Adenosine triphosphate
- CDS:
-
Coding sequence
- DCP:
-
Decapping protein
- DHH1p:
-
DExD/H-box helicase 1
- DNP:
-
Dinitrophenol
- eEF:
-
Eukaryotic elongation factor
- eIF:
-
Eukaryotic initiation factor
- GUS:
-
β-Glucuronidase
- HUP:
-
Hypoxia-responsive unknown protein
- LDH:
-
Lactate dehydrogenase
- LUC:
-
Luciferase
- mRNP:
-
Messenger RNA ribonucleoprotein complex
- P:
-
Peptidyl
- PB:
-
Processing body
- PDC:
-
Pyruvate decarboxylase
- PRD:
-
Prion-related domain
- RBP:
-
RNA-binding protein
- RH12:
-
RNA helicase 12
- RPS6:
-
Ribosomal protein S6
- SG:
-
Stress granule
- SUS:
-
Sucrose synthase
- TIA-1:
-
T-cell intracellular antigen 1
- TIAR:
-
T-cell intracellular antigen 1-related
- UBP1:
-
Oligouridylate-binding protein 1
- UTR:
-
Untranslated region
- VCS:
-
Varicose
References
Agarwal S, Grover A (2005) Isolation and transcription profiling of low-O2 stress-associated cDNA clones from the flooding-stress-tolerant FR13A rice genotype. Ann Bot 96:831–844
Alexandrov N, Troukhan M, Brover V, Tatarinova T, Flavell R, Feldmann K (2006) Features of Arabidopsis genes and genome discovered using full-length cDNAs. Plant Mol Biol 60:69–85
Anderson P, Kedersha N (2008) Stress granules: the Tao of RNA triage. Trends Biochem Sci 33:141–150
Andrews DL, MacAlpine DM, Johnson JR, Kelley PM, Cobb BG, Drew MC (1994) Differential induction of mRNAs for the glycolytic and ethanolic fermentative pathways by hypoxia and anoxia in maize seedlings. Plant Physiol 106:1575–1582
Armstrong W, Beckett PM (2011) The respiratory down-regulation debate. New Phytol 190:276–278
Arpagaus S, Braendle R (2000) The significance of {alpha}-amylase under anoxia stress in tolerant rhizomes (Acorus calamus L.) and non-tolerant tubers (Solanum tuberosum L., var. Desiree). J Exp Bot 51:1475–1477
Bailey-Serres J, Dawe RK (1996) Both 5′ and 3′ sequences of maize adh1 mRNA are required for enhanced translation under low-oxygen conditions. Plant Physiol 112:685–695
Bailey-Serres J, Freeling M (1990) Hypoxic stress-induced changes in ribosomes of maize seedling roots. Plant Physiol 94:1237–1243
Bailey-Serres J, Voesenek LAC (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339
Bailey-Serres J, Voesenek LA (2010) Life in the balance: a signaling network controlling survival of flooding. Curr Opin Plant Biol 13:489–494
Bailey-Serres J, Kloeckener-Gruissem B, Freeling M (1988) Genetic and molecular approaches to the study of the anaerobic response and tissue specific gene expression in maize. Plant Cell Environ 11:351–357
Bailey-Serres J, Vangala S, Szick K, Lee C (1997) Acidic phosphoprotein complex of the 60S ribosomal subunit of maize seedling roots (components and changes in response to flooding). Plant Physiol 114:1293–1305
Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17:129–138
Bologa KL, Fernie AR, Leisse A, Ehlers Loureiro M, Geigenberger P (2003) A bypass of sucrose synthase leads to low internal oxygen and impaired metabolic performance in growing potato tubers. Plant Physiol 132:2058–2072
Branco-Price C, Kawaguchi R, Ferreira R, Bailey-Serres J (2005) Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot (Lond) 96:647–660
Branco-Price C, Kaiser KA, Jang CJH, Larive CK, Bailey-Serres J (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J 56:743–755
Chen M-Q, Zhang A-H, Zhang Q, Zhang B-C, Nan J, Li X, Liu N, Qu H, Lu C-M, Sudmorgen et al (2012) Arabidopsis NMD3 is required for nuclear export of 60S ribosomal subunits and affects secondary cell wall thickening. PLoS One 7:e35904
Davies DD, Grego S, Kenworthy P (1974) The control of the production of lactate and ethanol by higher plants. Planta 118:297–310
Decker CJ, Teixeira D, Parker R (2007) Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J Cell Biol 179:437–449
Del Gatto-Konczak F, Bourgeois CF, Le Guiner C, Kister L, Gesnel M-C, Stévenin J, Breathnach R (2000) The RNA-binding protein TIA-1 is a novel mammalian splicing regulator acting through intron sequences adjacent to a 5′ splice site. Mol Cell Biol 20:6287–6299
Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250
Edwards JM, Roberts TH, Atwell BJ (2012) Quantifying ATP turnover in anoxic coleoptiles of rice (Oryza sativa) demonstrates preferential allocation of energy to protein synthesis. J Exp Bot 63:4389–4402
Eisinger-Mathason TSK, Andrade J, Groehler AL, Clark DE, Muratore-Schroeder TL, Pasic L, Smith JA, Shabanowitz J, Hunt DF, Macara IG et al (2008) Codependent functions of RSK2 and the apoptosis-promoting factor TIA-1 in stress granule assembly and cell survival. Mol Cell 31:722–736
Fennoy SL, Bailey-Serres J (1995) Post-transcriptional regulation of gene expression in oxygen-deprived roots of maize. Plant J 7:287–295
Fennoy SL, Nong T, Bailey-Serres J (1998) Transcriptional and post-transcriptional processes regulate gene expression in oxygen-deprived roots of maize. Plant J 15:727–735
Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P (2004) Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15:5383–5398
Goeres DC, Van Norman JM, Zhang W, Fauver NA, Spencer ML, Sieburth LE (2007) Components of the Arabidopsis mRNA decapping complex are required for early seedling development. Plant Cell 19:1549–1564
Gottschald OR, Malec V, Krasteva G, Hasan D, Kamlah F, Herold S, Rose F, Seeger W, Hänze J (2010) TIAR and TIA-1 mRNA-binding proteins co-aggregate under conditions of rapid oxygen decline and extreme hypoxia and suppress the HIF-1α pathway. J Mol Cell Biol 2:345–356
Hole DJ, Cobb BG, Hole PS, Drew MC (1992) Enhancement of anaerobic respiration in root tips of Zea mays following low-oxygen (hypoxic) acclimation. Plant Physiol 99:213–218
Huang S, Colmer TD, Millar AH (2008) Does anoxia tolerance involve altering the energy currency towards PPi? Trends Plant Sci 13:221–227
Hummel M, Cordewener JHG, de Groot JCM, Smeekens S, America AHP, Hanson J (2012) Dynamic protein composition of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MSE proteomics. Proteomics 12:1024–1038
Iwasaki S, Takeda A, Motose H, Watanabe Y (2007) Characterization of Arabidopsis decapping proteins AtDCP1 and AtDCP2, which are essential for post-embryonic development. FEBS Lett 581:2455–2459
Johnson J, Cobb BG, Drew MC (1989) Hypoxic induction of anoxia tolerance in root tips of Zea mays. Plant Physiol 91:837–841
Johnson JR, Cobb BG, Drew MC (1994) Hypoxic induction of anoxia tolerance in roots of Adh1 null Zea mays L. Plant Physiol 105:61–67
Kawaguchi R, Bailey-Serres J (2002) Regulation of translational initiation in plants. Curr Opin Plant Biol 5:460–465
Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, Scheuner D, Kaufman RJ, Golan DE, Anderson P (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169:871–884
Kelley P, Freeling M (1984) Anaerobic expression of maize glucose phosphate isomerase I. J Biol Chem 259:673–677
Kelley PM, Tolan DR (1986) The complete amino acid sequence for the anaerobically induced aldolase from maize derived from cDNA clones. Plant Physiol 82:1076–1080
Kim T-H, Kim B-H, Yahalom A, Chamovitz DA, von Arnim AG (2004) Translational regulation via 5′ mRNA leader sequences revealed by mutational analysis of the Arabidopsis translation initiation factor subunit eIF3h. Plant Cell 16:3341–3356
Kim B-H, Cai X, Vaughn JN, von Arnim AG (2007) On the functions of the h subunit of eukaryotic initiation factor 3 in late stages of translation initiation. Genome Biol 8:R60
Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494
Lal SK, Lee C, Sachs MM (1998) Differential regulation of enolase during anaerobiosis in maize. Plant Physiol 118:1285–1293
Lambermon MHL, Simpson GG, Kirk DAW, Hemmings-Mieszczak M, Klahre U, Filipowicz W (2000) UBP1, a novel hnRNP-like protein that functions at multiple steps of higher plant nuclear pre-mRNA maturation. EMBO J 19:1638–1649
Lambermon MHL, Fu Y, Wieczorek Kirk DA, Dupasquier M, Filipowicz W, Lorković ZJ (2002) UBA1 and UBA2, two proteins that interact with UBP1, a multifunctional effector of pre-mRNA maturation in plants. Mol Cell Biol 22:4346–4357
Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231
Laszlo A, St. Lawrence P (1983) Parallel induction and synthesis of PDC and ADH in anoxic maize roots. Mol Gen Genet 192:110–117
Lee SC, Mustroph A, Sasidharan R, Vashisht D, Pedersen O, Oosumi T, Voesenek LAC, Bailey-Serres J (2011) Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. New Phytol 190:457–471
Licausi F, Weits DA, Pant BD, Scheible W-R, Geigenberger P, van Dongen JT (2011) Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. New Phytol 190:442–456
Limami AM, Glévarec G, Ricoult C, Cliquet J-B, Planchet E (2008) Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedlings under hypoxic stress. J Exp Bot 59:2325–2335
Lin CY, Key JL (1967) Dissociation and reassembly of polyribosomes in relation to protein synthesis in the soybean root. J Mol Biol 26:237–247
Lin CY, Key JL, Bracker CE (1966) Association of D-RNA with polyribosomes in the soybean root. Plant Physiol 41:976–982
Liu F, VanToai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129
Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138
Lorković ZJ, Wieczorek Kirk DA, Klahre U, Hemmings-Mieszczak M, Filipowicz W (2000) RBP45 and RBP47, two oligouridylate-specific hnRNP-like proteins interacting with poly(A)+ RNA in nuclei of plant cells. RNA 6:1610–1624
Manjunath S, Lee C-HK, Winkle PV, Bailey-Serres J (1998) Molecular and biochemical characterization of cytosolic phosphoglucomutase in maize expression during development and in response to oxygen deprivation. Plant Physiol 117:997–1006
Manjunath S, Williams AJ, Bailey-Serres J (1999) Oxygen deprivation stimulates Ca2+-mediated phosphorylation of mRNA cap-binding protein eIF4E in maize roots. Plant J 19:21–30
Miyashita Y, Dolferus R, Ismond KP, Good AG (2007) Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana. Plant J 49:1108–1121
Mohanty B, Krishnan SPT, Swarup S, Bajic VB (2005) Detection and preliminary analysis of motifs in promoters of anaerobically induced genes of different plant species. Ann Bot 96:669–681
Mustroph A, Zanetti ME, Jang CJH, Holtan HE, Repetti PP, Galbraith DW, Girke T, Bailey-Serres J (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc Natl Acad Sci U S A 106:18843–18848
Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang H, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J (2010) Cross-kingdom comparison of transcriptomic adjustments to low oxygen stress highlights conserved and plant-specific responses. Plant Physiol 152:1484–1500
Mustroph A, Hess N, Sasidharan R (2013) Hypoxic energy metabolism and PPi as an alternative energy currency. In: Dongen JT, Licausi F (eds) Low oxygen stress in plants. Springer, New York
Parker R, Sheth U (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25:635–646
Paul A-L, Ferl RJ (1991) Adh1 and Adh2 regulation. Maydica 36:129–134
Ricoult C, Echeverria LO, Cliquet J-B, Limami AM (2006) Characterization of alanine aminotransferase (AlaAT) multigene family and hypoxic response in young seedlings of the model legume Medicago truncatula. J Exp Bot 57:3079–3089
Roberts JKM, Callis J, Jardetzky O, Walbot V, Freeling M (1984) Cytoplasmic acidosis as a determinant of flooding intolerance in plants. Proc Natl Acad Sci U S A 81:6029–6033
Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152:1501–1513
Rosado A, Sohn EJ, Drakakaki G, Pan S, Swidergal A, Xiong Y, Kang B-H, Bressan RA, Raikhel NV (2010) Auxin-mediated ribosomal biogenesis regulates vacuolar trafficking in Arabidopsis. Plant Cell 22:143–158
Russell DA, Sachs MM (1991) The maize cytosolic glyceraldehyde-3-phosphate dehydrogenase gene family: organ-specific expression and genetic analysis. Mol Gen Genet 229:219–228
Russell DA, Wong DM-L, Sachs MM (1990) The anaerobic response of soybean. Plant Physiol 92:401–407
Sachs MM, Ho THD (1986) Alteration of gene expression during environmental stress in plants. Annu Rev Plant Physiol 37:363–376
Sachs MM, Freeling M, Okimoto R (1980) The anaerobic proteins of maize. Cell 20:761–767
Saglio PH, Drew MC, Pradet A (1988) Metabolic acclimation to anoxia induced by low (2–4 kPa partial pressure) oxygen pretreatment (hypoxia) in root tips of Zea mays. Plant Physiol 86:61–66
Springer B, Werr W, Starlinger P, Bennett DC, Zokolica M, Freeling M (1986) The Shrunken gene on chromosome 9 of Zea mays L is expressed in various plant tissues and encodes an anaerobic protein. Mol Gen Genet 205:461–468
Szakonyi D, Byrne ME (2011) Ribosomal protein L27a is required for growth and patterning in Arabidopsis thaliana. Plant J 65:269–281
Szick K, Springer M, Bailey-Serres J (1998) Evolutionary analyses of the 12-kDa acidic ribosomal P-proteins reveal a distinct protein of higher plant ribosomes. Proc Natl Acad Sci U S A 95:2378–2383
Szick-Miranda K, Bailey-Serres J (2001) Regulated heterogeneity in 12-kDa P-protein phosphorylation and composition of ribosomes in maize (Zea mays L.). J Biol Chem 276:10921–10928
Szick-Miranda K, Jayachandran S, Tam A, Werner-Fraczek J, Williams AJ, Bailey-Serres J (2003) Evaluation of translational control mechanisms in response to oxygen deprivation in maize. Russ J Plant Physiol 50:774–786
van Dongen JT, Fröhlich A, Ramírez-Aguilar SJ, Schauer N, Fernie AR, Erban A, Kopka J, Clark J, Langer A, Geigenberger P (2009) Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Ann Bot 103:269–280
Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytol 170:213–226
Warner JR, Rich A, Hall CE (1962) Electron microscope studies of ribosomal clusters synthesizing hemoglobin. Science 138:1399–1403
Warner JR, Knopf PM, Rich A (1963) A multiple ribosomal structure in protein synthesis. Proc Natl Acad Sci U S A 49:122–129
Weber C, Nover L, Fauth M (2008) Plant stress granules and mRNA processing bodies are distinct from heat stress granules. Plant J 56:517–530
Webster C, Gaut RL, Browning KS, Ravel JM, Roberts JK (1991) Hypoxia enhances phosphorylation of eukaryotic initiation factor 4A in maize root tips. J Biol Chem 266:23341–23346
Williams AJ, Werner-Fraczek J, Chang I-F, Bailey-Serres J (2003) Regulated phosphorylation of 40S ribosomal protein S6 in root tips of maize. Plant Physiol 132:2086–2097
Xu J, Chua NH (2011) Processing bodies and plant development. Curr Opin Plant Biol 14:88–93
Xu J, Yang J-Y, Niu Q-W, Chua N-H (2006) Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell 18:3386–3398
Yamasaki S, Stoecklin G, Kedersha N, Simarro M, Anderson P (2007) T-cell intracellular antigen-1 (TIA-1)-induced translational silencing promotes the decay of selected mRNAs. J Biol Chem 282:30070–30077
Zanetti ME, Chang I-F, Gong F, Galbraith DW, Bailey-Serres J (2005) Immunopurification of polyribosomal complexes of Arabidopsis for global analysis of gene expression. Plant Physiol 138:624–635
Zeng Y, Wu Y, Avigne WT, Koch KE (1999) Rapid repression of maize invertases by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiol 121:599–608
Zhang T, Delestienne N, Huez G, Kruys V, Gueydan C (2005) Identification of the sequence determinants mediating the nucleo-cytoplasmic shuttling of TIAR and TIA-1 RNA-binding proteins. J Cell Sci 118:5453–5463
Zhang W, Murphy C, Sieburth LE (2010) Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc Natl Acad Sci U S A 107:15981–15985
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Sorenson, R., Bailey-Serres, J. (2014). Selective mRNA Translation Tailors Low Oxygen Energetics. In: van Dongen, J., Licausi, F. (eds) Low-Oxygen Stress in Plants. Plant Cell Monographs, vol 21. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1254-0_6
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