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The resurrection plant Sporobolus stapfianus: An unlikely model for engineering enhanced plant biomass?

  • SI Plant Desiccation Stress
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The resurrection grass Sporobolus stapfianus Gandoger can rapidly recover from extended periods of time in the desiccated state (water potential equilibrated to 2% relative humidity) (Gaff and Ellis, Bothalia 11:305–308 1974; Gaff and Loveys, Transactions of the Malaysian Society of Plant Physiology 3:286–287 1993). Physiological studies have been conducted in S. stapfianus to investigate the responses utilised by these desiccation-tolerant plants to cope with severe water-deficit. In a number of instances, more recent gene expression analyses in S. stapfianus have shed light on the molecular and cellular mechanisms mediating these responses. S. stapfianus is a versatile research tool for investigating desiccation-tolerance in vegetative grass tissue, with several useful characteristics for differentiating desiccation-tolerance adaptive genes from the many dehydration-responsive genes present in plants. A number of genes orthologous to those isolated from dehydrating S. stapfianus have been successfully used to enhance drought and salt tolerance in model plants as well as important crop species. In addition to the ability to desiccate and rehydrate successfully, the survival of resurrection plants in regions experiencing short sporadic rainfall events may depend substantially on the ability to tightly down-regulate cell division and cell wall loosening activities with decreasing water availability and then grow rapidly after rainfall while water is plentiful. Hence, an analysis of gene transcripts present in the desiccated tissue of resurrection plants may reveal important growth-related genes. Recent findings support the proposition that, as well as being a versatile model for devising strategies for protecting plants from water-loss, resurrection plants may be a very useful tool for pinpointing genes to target for enhancing growth rate and biomass production.

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References

  • Alexandrov NN, Brover VV, Freidin S, Troukhan ME, Tatarinova TV, Zhang H, Swaller TJ, Lu Y-P, Bouck J, Flavell RB, Feldmann KA (2009) Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol Biol 69:179–194

    PubMed  CAS  Google Scholar 

  • Anderson CM, Wagner TA, Perret M, He Z-H, He D, Kohorn BD (2001) WAKs: Cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol Biol 47:197–206

    PubMed  CAS  Google Scholar 

  • Arvidson I (1951) Austrocknungs- und Dürreresistenzverhältnisse einiger Repräsentanten inländischer Planzenvereine nebst Bemerkungen über Wasserabsorption durch oberirdische Organe, Oikos. Acta Oecologica Scandinavica Suppl.1:1

    Google Scholar 

  • Bartels D, Schneider K, Terstappen G, Piatowski D, Salamini F (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181:27–34

    CAS  Google Scholar 

  • Benhamou N, Asselin A (1989) Attempted localization of a substrate for chitinases in plant cell reveals abundant N-acetyl-D-glucosamine residues in secondary wall. Biol Cell 67:341–350

    CAS  Google Scholar 

  • Bewley JD (1979) Physiological aspects of desiccation tolerance. Annu Rev Plant Physiol 30:195–238

    CAS  Google Scholar 

  • Bewley JD, Halmer P, Krochko JE, Winner WE (1978) Metabolism of a drought-tolerant and drought-sensitive moss: respiration, ATP synthesis and carbohydrate status. In: Crowe JH, Clegg JS (eds) Dry biological systems. Academic Press, New York, pp 185–203

    Google Scholar 

  • Blomstedt CK, Gianello RD, Gaff DF, Hamill JD, Neale AD (1998a) Differential gene expression in desiccation-tolerant and desiccation-sensitive tissue of the resurrection grass, Sporobolus stapfianus. Aust J Plant Physiol 25:937–946

    CAS  Google Scholar 

  • Blomstedt CK, Gianello RD, Hamill JD, Neale AD, Gaff DF (1998b) Drought-stimulated genes correlated with desiccation tolerance of the resurrection grass Sporobolus stapfianus. Plant Growth Reg. 24:153–161

    CAS  Google Scholar 

  • Bocca SN, Magioli C, Mangeon A, Junqueira RM, Cardeal V, Margis R, Sachetto-martins G (2005) Survey of glycine-rich proteins (GRPs) in the Eucalyptus expressed sequence tag database (ForEST). Gen Mol Biol 28:608–624

    CAS  Google Scholar 

  • Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341

    PubMed  CAS  Google Scholar 

  • Brini F, Hanin M, Lumbreras V, Amara I, Khoudi H, Hassairi A, Pagès M, Masmoudi K (2007) Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Rep 26:2017–2026

    PubMed  CAS  Google Scholar 

  • Browning R (2004) Plant translation initiation factors: it is not easy to be green. Biochem Soc Trans 32:589–591

    PubMed  CAS  Google Scholar 

  • Campillo E, Lewis L (1992) Occurrence of 9.5 cellulase and other hydrolases in the flower reproductive organ undergoing major cell wall disruption. Plant Physiol 99:1015–1020

    PubMed  Google Scholar 

  • Carneiro NP, Hughes PA, Larkins BA (1999) The eEFlA gene family is differentially expressed in maize endosperm. Plant Mol Biol 41:801–813

    PubMed  CAS  Google Scholar 

  • Cassab GI (1998) Plant Cell Wall Proteins. Annu Rev Plant Physiol Plant Mol Biol 49:281–309

    PubMed  CAS  Google Scholar 

  • Catala R, Ouyang J, Abreu IA, Hu Y, Deo H, Zhang X, Chua N-H (2007) The Arabidopsis E3 SUMO ligase regulates plant growth and drought responses. Plant Cell 19:2952–2966

    PubMed  CAS  Google Scholar 

  • Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel B (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 104:20131–20136

    PubMed  CAS  Google Scholar 

  • Collett H, Shen A, Gardner M, Farrant JM, Denby KJ, Illing N (2004) Towards transcript profiling of desiccation tolerance in Xerophyta humilis: Construction of a normalized 11 k X. humilis cDNA set and microarray expression analysis of 424 cDNAs in response to dehydration. Physiol. Plant 122:39–53

    CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nature Reviews Molecular and Cellular Biology 6:850–861

    CAS  Google Scholar 

  • Cui X-H, Hao F-S, Chen H, Chen J, Wang X-C (2008) Expression of the Vicia faba VfPIP1 gene in Arabidopsis thaliana plants improves their drought resistance. J of Plant Res: 121:207–214

    CAS  Google Scholar 

  • Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soils. Annu Rev Plant Physiol Plant Mol Biol 42:55–76

    CAS  Google Scholar 

  • Davies WJ, Wilkinson S, Loveys BR (2002) Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytol 153:449–460

    CAS  Google Scholar 

  • de Oliveira D, Seurinck J, Inzé D, Montagu MV, Bottermana J (1990) Differential Expression of Five Arabidopsis Genes Encoding Glycine-Rich Proteins. The Plant J 2:427–436

    Google Scholar 

  • Decreux A, Thomas A, Spies B, Brasseur R, Cutsem Pv, Messiaen J (2006) In vitro characterization of the homogalacturonan-binding domain of the wall-associated kinase WAK1 using site-directed mutagenesis. Phytochemistry 67:1068–1079

    PubMed  CAS  Google Scholar 

  • Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolai M, Bedu M, Robaglia C, Meyer C (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Reports 8:864–870

    PubMed  CAS  Google Scholar 

  • Di Blasi S, Puliga S, Losi L, Vazzana C (1998) S. stapfianus and E. curvula cv. Consol in vivo photosynthesis, PSII activity and ABA content during dehydration. Plant Growth Regul 25:97–104

    CAS  Google Scholar 

  • Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Luyyanov K, Gurskaya N, Sverdlov ED, Siebert P (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030

    PubMed  CAS  Google Scholar 

  • Diaz-trivino S, Castellano MM, Sanchez MP, Ramirez-parra E, Desvoyes B, Gutierrez C (2005) The genes encoding Arabidopsis ORC subunits are E2F targets and the two ORC1 genes are differentially expressed in proliferating and endoreplicating cells. Nucl Acids Res 33:5404–5414

    PubMed  CAS  Google Scholar 

  • Diédhiou CJ, Popova OV, Dietz K-J, Golldack D (2008) The SUI-homologous translation initiation factor eIF-1 is involved in regulation of ion homeostasis in rice. Plant Biol 10:298–309

    PubMed  Google Scholar 

  • Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S (2008) Activation of the Indole-3-Acetic Acid-Amido Synthetase GH3–8 Suppresses Expansin Expression and Promotes Salicylate- and Jasmonate-Independent Basal Immunity in Rice. Plant Cell 20:228–240

    PubMed  CAS  Google Scholar 

  • Domingo C, Sauri A, Mansilla E, Conejero V, Vera P (1999) Identification of novel peptide motif that mediates cross-linking of proteins to cell walls. The Plant J 20:563–570

    CAS  Google Scholar 

  • Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99:787–822

    PubMed  CAS  Google Scholar 

  • Duncker B, Chesnokov IN, McConkey B (2009) The origin recognition complex protein family. Genome Biol 10:214–218

    PubMed  Google Scholar 

  • Dunn M, Morris A, Jack PL, Hughes M (1993) A low-temperature-responsive translation elongation factor from barley (Hordeum vulgare L.). Plant Mol. Biol 23:221–225

    CAS  Google Scholar 

  • Ejiri S-I (2002) Moonlighting functions of polypeptide elongation factor 1: From actin bundling to zinc finger protein R1-associated nuclear localization. Biosci Biotechnol Biochem 66:1–21

    PubMed  CAS  Google Scholar 

  • Farrant JM (2000) A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecol 151:29–39

    Google Scholar 

  • Ferry N, Raemaekers RJM, Majerus MEN, Jouanin L, Port GP, Gatehouse JA, Gatehouse AMR (2003) Impact of oilseed rape expressing the insecticidal cysteine protease inhibitor oryzacystatin on the beneficial predator Harmonia axyridis (multicoloured Asian ladybeetle). Mol Ecol 12:493–504

    PubMed  CAS  Google Scholar 

  • Forsberg J, Ström J, Kieselbach T, Larsson H, Alexciev K, Engström A, Akerlund H-E (2005) Protease activities in the chloroplast capable of cleaving an LHCII N-terminal peptide. Physiol Plant 123:21–29

    CAS  Google Scholar 

  • Fusaro A, Mangeon A, Junqueira RM, Rocha CAB, Coutinho TC, Margis R, Sachetto-martins G (2001) Classification, expression pattern and comparative analysis of sugarcane expressed sequences tags (ESTs) encoding glycine-rich proteins (GRPs). Genet Mol Biol 24:263–273

    CAS  Google Scholar 

  • Gaddour K, Vicente-carbajosa J, Lara P, Isabel-lamoneda I, Díaz I, Carbonero P (2001) A constitutive cystatin-encoding gene from barley (Icy) responds differentially to abiotic stimuli. Plant Mol Biol 45:599–608

    PubMed  CAS  Google Scholar 

  • Gaff DF (1971) The desiccation tolerant higher plants of Southern Africa. Science 174:1033–1034

    PubMed  CAS  Google Scholar 

  • Gaff DF (1980) Protoplasmic tolerance of extreme water stress. In: Turner NC KP (ed) Adaption of plants to water and high temperature stress. John Wiley and Sons, New York

    Google Scholar 

  • Gaff DF, Churchill DM (1976) Borya nitida Labill—an Australian species in the Liliaceae with desiccation-tolerant leaves. Aust J Bot 24:209–224

    Google Scholar 

  • Gaff DF, Ellis RP (1974) Southern African grasses with foliage that revives after dehydration. Bothalia 11:305–308

    Google Scholar 

  • Gaff DF, Loveys BR (1993) Abscisic acid levels in drying plants of a resurrection grass. Trans Malays Soc Plant Physiol 3:286–287

    Google Scholar 

  • Gaff DF, McGregor GR (1979) The effect of dehydration and re-hydration on the nitrogen content of various fractions from resurrection plants. Biologia Plantarum (Praha) 21:92–99

    CAS  Google Scholar 

  • Gaff D, Bartels D, Gaff JL (1997) Changes in gene expression during drying in a desiccation tolerant grass Sporobolus stapfianus and a desiccation sensitive grass Sporobolus pyramidalis. Aust J Plant Physiol 24:617–622

    Google Scholar 

  • Gaff DF, Blomstedt CK, Neale AD, Le TN, Hamill JD, Ghasempour HR (2009) Sporobolus stapfianus Gandoger, a model desiccation-tolerant grass. Funct Plant Biol 36:1–11

    Google Scholar 

  • Ghasempour H, Gaff DF, Williams RP, Gianello RD (1998) Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Reg. 24:185–191

    CAS  Google Scholar 

  • Ghasempour H, Anderson E, Gaff D (2001) Effects of growth substances on the protoplasmic drought tolerance of leaf cells of the resurrection grass Sporobolus stapfianus. Aust J Plant Physiol 28:1115–1120

    CAS  Google Scholar 

  • Giannakouros T, Nikolakaki H, Georgatsos J (1990) Concentration-dependent effects of polyamines on peptide chain initiation and elongation in a cell-free system of protein synthesis. Mol Cell Biochem 99:9–19

    PubMed  CAS  Google Scholar 

  • Grudkowska M, Zagdańska B (2004) Multifunctional role of plant cysteine proteinases. Acta Biochem Polonica 51:609–624

    CAS  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    PubMed  CAS  Google Scholar 

  • He Z-H, Cheeseman I, He D, Kohorn BD (1999) A cluster of five cell wall-associated receptor kinase genes, Wak1–5, are expressed in specific organs of Arabidopsis. Plant Mol Biol 39:1189–1196

    PubMed  CAS  Google Scholar 

  • He L, Ban Y, Miyata S-I, Kitashiba H, Moriguchi T (2008) Apple aminopropyl transferase, MdACL5 interacts with putative elongation factor 1-a and S-adenosylmethionine synthase revealed. Biochem Biophys Res Commun 366:162–167

    PubMed  CAS  Google Scholar 

  • His I, Driouich A, Nicol F, Jauneau A, Hofte H (2001) Korrigan (kor) is a dwarf mutant of Arabidopsis thaliana (L.) Heynh. that is deficient in a membrane-bound endo-1, 4-beta-glucanase. Planta 212:348–358

    PubMed  CAS  Google Scholar 

  • Höfler K, Migsch H, Rottenburg W (1941) Über die Austrocknungsresistenz landwirtschaftlicher Kulturpflanzen. Forschungsdienst 12:50–61

    Google Scholar 

  • Holmström K-O, Welin B, Mandal A, Kristiansdottir I, Teeri TH, Lamark T, Strøm AR, Tapio PE (1994) Production of the Escherichia coli betaine-aldehyde dehydrogenase, an enzyme required for the synthesis of the osmoprotectant glycine betaine, in transgenic plants. The Plant J. 6:749–758

    Google Scholar 

  • Ingram G, Waites R (2006) Keeping it together; co-ordinating plant growth. Curr Opin Plant Biol 9:12–20

    PubMed  CAS  Google Scholar 

  • Itturriaga G, Cushman M, Cushman J (2006) An EST catalogue from the resurrection plant Selaginella lepidophylla reveals abiotic stress adaptive genes. Plant Sci 170:1173–1184

    Google Scholar 

  • Jain M, Kaur N, Tyagi AK, Khurana JP (2006) The auxin-responsive GH3 gene family in rice (Oryza sativa). Funct Integr Genomics 6:36–46

    PubMed  CAS  Google Scholar 

  • Jones L, McQueen-mason S (2004) A role for expansins in dehydration and rehydration of the resurrection plant Craterostigma plantagineum. FEBS letters 559:61–65

    PubMed  CAS  Google Scholar 

  • Kakehi J-I, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is Required for Stem Elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349

    PubMed  CAS  Google Scholar 

  • Kanneganti V, Gupta AK (2008) Wall associated kinases from plants–an overview. Physiol. Mol. Biol. Plants 14:1009–1118

    Google Scholar 

  • Kariola T, Brader G, Helenius E, Li J, Heino P, Palva E (2006) EARLY RESPONSE TO DEHYDRATION 15, A negative regulator of ABA-responses in Arabidopsis. Plant Physiol 142:1559–1573

    PubMed  CAS  Google Scholar 

  • Kasprzewska A (2003) Plant chitinases-regulation and function. Cell Mol Biol Lett 8:809–824

    PubMed  CAS  Google Scholar 

  • Kasuga M, Lui Q, Miura S, Yamaguchi-shinozaki K, Shinozaki K (1999) Improving plant drought, salt and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    PubMed  CAS  Google Scholar 

  • Khacho M, Mekhail K, Pilon-larose K, Pause A, Côté J, Lee S (2008) eEF1A is a novel component of the mammalian nuclear protein export machinery. Mol Biol Cell 19:5296–5308

    PubMed  CAS  Google Scholar 

  • Khan S, Stone J (2007) Arabidopsis thaliana GH3.9 influences primary root growth. Planta 226:21–34

    PubMed  CAS  Google Scholar 

  • Kim E, Kim YS, Park S-H, Koo YJ, Choi YD, Chung Y-Y, Lee I-J, Kim J-K (2009) Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol 149:1751–1760

    PubMed  CAS  Google Scholar 

  • Kishor KPB, Hong Z, Miao G-H, Hu CAA, Verma DPS (1995) Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants. Plant Physiol 108:1387–1394

    PubMed  CAS  Google Scholar 

  • Krishnamurthy R, Bhagwat KA (1989) Polyamines as Modulators of Salt Tolerance in Rice Cultivars. Plant Physiol 91:500–504

    PubMed  CAS  Google Scholar 

  • Kuang J, Gaff D, Gianello R, Blomstedt C, Neale A, Hamill J (1995) Changes in in vivo protein complements in drying leaves of the desiccation-tolerant grass Sporobolus stapfianus and the desiccation-sensitive grass Sporobolus pyramidalis. Aust J Plant Physiol 22:1027–1034

    Google Scholar 

  • Lally D, Ingmire P, Tong H-Y, He Z-H (2001) Antisense Expression of a Cell Wall-Associated Protein Kinase, WAK4, Inhibits Cell Elongation and Alters Morphology. Plant Cell 13:1317–1332

    PubMed  CAS  Google Scholar 

  • Le T-N, Blomstedt CK, Kuang J, Tenlen J, Gaff DF, Hamill JD, Neale AD (2007) Genes differentially expressed in desiccation tolerant leaf tissue of the resurrection grass Sporobolus stapfianus. Funct Plant Biol 34:589–600

    CAS  Google Scholar 

  • Lee J, Takei K, Sakakibara H, Cho HS, Kim DM, Kim YS, Min SR, Kim WT, Sohn DY, Lim YP, Pai H-S (2003) CHRK1, a chitinase-related receptor-like kinase, plays a role in plant development and cytokinin homeostasis in tobacco. Plant Mol Biol 53:877–890

    PubMed  CAS  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses Volume 2 Water, radiation, salt, and other stresses, vol 2nd. Academic Press Inc, New York

    Google Scholar 

  • Li Z-Y, Chen S-Y (1999) Inducible expression of translation elongation factor 1A gene in rice seedlings in response to environmental stresses. Acta Botanica Sinica 41:800–806

    CAS  Google Scholar 

  • Li WL, Faris JD, Muthukrishna S, Liu DJ, Chen PD, Gill BS (2001) Isolation and characterisation of novel cDNA clones of acidic chitinases and β-1,3-glucanases from wheat spikes infected by Fusarium graminearum. Theor Appl Genet 102:353–362

    CAS  Google Scholar 

  • Libertini E, Li Y, McQueen-Mason SJ (2004) Phylogenetic analysis of the plant endo-β-1,4-glucanase gene family. J Mol Evol 58:505–516

    Google Scholar 

  • Liu K, Kang B-C, Jiang H, Moore SL, Li H, Watkins CB, Setter TL, Jahn MM (2005) A GH3-like gene, CcGH3, isolated from Capsicum chinense L. fruit is regulated by auxin and ethylene. Plant Mol Biol 58:447–464

    PubMed  CAS  Google Scholar 

  • Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 49:249–272

    PubMed  CAS  Google Scholar 

  • Lopez-Casado G, Urbanowicz BR, Damasceno CMB, Rose J (2008) Plant glycosyl hydrolases and biofuels: a natural marriage. Curr Opin Plant Biol 11:329–337

    PubMed  CAS  Google Scholar 

  • Lukash TO, Turkivska HV, Negrutskii BS, El’skaya AV (2004) Chaperone-like activity of mammalian elongation factor eEF1A: renaturation of aminoacyl-tRNA synthetases. Int J Biochem Cell Biol 36:1341–1347

    PubMed  CAS  Google Scholar 

  • Mahouachi J, Arbona V, Gomez-cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Reg. 53:43–51

    CAS  Google Scholar 

  • Martinez M, Abraham Z, Carbonero P, Diaz I (2005) Comparative phylogenetic analysis of cystatin gene families from Arabidopsis, rice and barley. Mol Gen Genomics 273:423–432

    CAS  Google Scholar 

  • Marty I, Monfort A, Stiefel V, Ludevid D, Delseny M, Puigdomènech P (1996) Molecular characterization of the gene coding for GPRP, a class of proteins rich in glycine and proline interacting with membranes in Arabidopsis thaliana. Plant Mol Biol 30:625–636

    PubMed  CAS  Google Scholar 

  • Meins F Jr, Bernard Fritig, Linthorst Huub JM, Mikkelsen Jorn D, Neuhaus J-m, Ryals J (1994) Plant Chitinase Genes. Plant Mol. Biol. Reporter 12:S22–S28

    CAS  Google Scholar 

  • Mohamed EA, Iwaki T, Munir I, Tamoi M, Shigeoka S, Wadano A (2003) Overexpression of bacterial catalase in tomato leaf chloroplasts enhances photo-oxidative stress tolerance. Plant Cell Environ 26:2037–2046

    CAS  Google Scholar 

  • Mølhøj M, Pagent S, Höfte H (2002) Towards understanding the role of membrane-bound endo-ß-1, 4-glucanases in cellulose biosynthesis. Plant Cell Physiol 43:1399–1406

    PubMed  Google Scholar 

  • Moons A, Prinsen E, Bauw G, Montagu MV (1997) Antagonistic effects if abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243–2259

    PubMed  CAS  Google Scholar 

  • Moore R, Cyr R (2000) Association between elongation factor -1α and microtubules in vivo is domain dependent and conditional. Cell Motil Cytoskeleton 45:279–292

    PubMed  CAS  Google Scholar 

  • Moore JP, Nguema-ona E, Chevalier L, Lindsey GG, Brandt WF, Lerouge P, Farrant JM, Driouich A (2006) Response of the Leaf Cell Wall to Desiccation in the Resurrection Plant Myrothamnus flabellifolius. Plant Physiol 141:651–662

    PubMed  CAS  Google Scholar 

  • Moore JP, Vicré-gibouin M, Farrant JM, Driouich A (2008a) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plant 134:237–245

    PubMed  CAS  Google Scholar 

  • Moore JP, Le NT, Brandt WF, Driouich A, Farrant JM (2008b) Towards a systems- based understanding of plant desiccation tolerance. Trends Plant Sci 14:110–117

    Google Scholar 

  • Neale A, Waleithner JA, Lund M, Bonnett HT, Kelly A, Meeks-wagner DR, Dennis ES, Peacock W (1990) Chitinase, ß-1, 3-glucanase, osmotin, and extensin are expressed in tobacco explants during flower formation. Plant Cell 2:673–684

    PubMed  CAS  Google Scholar 

  • Neale AD, Blomstedt CK, Bronson P, Le TN, Guthridge K, Evans J, Gaff DF, Hamill JD (2000) The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe drought stress. Plant Cell and Environ 23:265–277

    CAS  Google Scholar 

  • O’Mahony P, Oliver M (1999) Characterization of a desiccation-responsive small GTP-binding protein (Rab2) from the desiccation-tolerant grass Sporobolus stapfianus. Plant Mol Biol 39:809–821

    PubMed  Google Scholar 

  • Oliver MJ (2007) Lessons on dehydration tolerance from desiccation-tolerant plants. In: Jenks MA, Wood AJ (eds) Plant Desiccation Tolerance. Blackwell, Ames, Iowa, USA

    Google Scholar 

  • Oliver MJ, Hudgeons J, Dowd SE, Payton PR (2009) A combined subtractive suppression hybridization and expression profiling strategy to identify novel desiccation response transcripts from Tortula ruralis gametophytes. Physiol Plant 136:437–460

    PubMed  CAS  Google Scholar 

  • Panasyuk G, Nemazanyy I, Filonenko V, Negrutskii B, El’skaya AV (2008) A2 isoform of mammalian translation factor eEF1A displays increased tyrosine phosphorylation and ability to interact with different signalling molecules. Int J Biochem Cell Biol 40:63–71

    PubMed  CAS  Google Scholar 

  • Park AR, Cho SK, Yun UJ, Jin MY, Lee SH, Sachetto-martins G, Park OK (2001) Interaction of the Arabidopsis Receptor Protein Kinase Wak1 with a Glycine-rich Protein, AtGRP-3. J Biol Chem 276:26688–26693

    PubMed  CAS  Google Scholar 

  • Park Y, Tominaga R, Sugiyama J, Furuta Y, Tanimoto E, Samejima M, Sakai F, Hayashi T (2003) Enhancement of growth by expression of poplar cellulase in Arabidopsis thaliana. The Plant J. 33:1099–1106

    CAS  Google Scholar 

  • Park J-E, Park J-Y, Kim Y-S, Staswick PE, Jeon J, Yun J, Kim S-Y, Kim J, Lee Y-H, Park C-M (2007) GH3-mediated Auxin Homeostasis Links Growth Regulation with Stress Adaptation Response in Arabidopsis. J Biol Chem 282:10036–10046

    PubMed  CAS  Google Scholar 

  • Patil V, Widholm J (1997) Possible correlation between increased vigour and chitinase activity expression in tobacco. J Experimental Bot 48:1943–1950

    CAS  Google Scholar 

  • Rangan L, Rout A, Sudarshan M, Gregorio G (2009) Molecular cloning, expression and mapping of the translation initiation factor eIF1 gene in Oryza sativa. Funct Plant Biol 36:442–452

    CAS  Google Scholar 

  • Rausell A, Kanhonou R, Yenush L, Serrano R, Ros R (2003) The translation initiation factor eIF1A is an important determinant in the tolerance to NaCl stress in yeast and plants. The Plant J. 34:257–267

    CAS  Google Scholar 

  • Rivard D, Girard C, Anguenot R, Vézina L-P, Trépanier S, Michaud D (2007) MsCYS1, a developmentally-regulated cystatin from alfalfa. Plant Physiol Biochem 45:508–514

    PubMed  CAS  Google Scholar 

  • Robaglia C, Menand B, Lei Y, Sormani R, Nicolai M, Gery C, Teoule E, Deprost D, Meyer C (2004) Plant growth: the translational connection. Biochem Soc Trans 32:581–584

    PubMed  CAS  Google Scholar 

  • Rohde W, Rosch K, Kroeger K, Salamini F (1990) Nucleotide sequence of a Hordeum vulgare gene encoding a glycine-rich protein with homology to vertebrate cytokeratins. Plant Mol Biol 14:1057–1059

    PubMed  CAS  Google Scholar 

  • Roy SD, Saxena M, Bhomkar PS, Pooggin M, Hohn T, Bhalla-sarin N (2008) Generation of marker free salt tolerant transgenic plants of Arabidopsis thaliana using the gly I gene and cre gene under inducible promoters. Plant Cell Tiss Organ Cult 95:1–11

    CAS  Google Scholar 

  • Sachetto-Martins G, Franco LO, de Oliveira DE (2000) Plant glycine-rich proteins: a family or just proteins with a common motif? Biochim Biophys Acta 1492:1–14

    PubMed  CAS  Google Scholar 

  • Safra-dassa L, Shani Z, Danin A, Roiz L, Shoseyov O, Wolf S (2006) Growth modulation of transgenic potato plants by heterologous expression of bacterial carbohydrate-binding module. Mol Breeding 17:355–364

    CAS  Google Scholar 

  • Schachtman DP, Goodger JQD (2008) Chemical root to shoot signalling under drought. Trends Plant Sci 13:281–287

    PubMed  CAS  Google Scholar 

  • Schnepf E (1961) Über Veränderungen der plasmatischen Feinstrukturen während des Welkens. Planta (Berlin) 57:156–175

    Google Scholar 

  • Schultz R, Lee T-J, Allen GC, Thompson WF, Hanley-bowdion L (2009) Dynamic localization of the DNA replication proteins MCM5 and MCM7 in plants. Plant Physiol 150:658–669

    Google Scholar 

  • Sgherri CLM, Loggini B, Puliga S, Navari-Izzo F (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochemistry 35:561–565

    CAS  Google Scholar 

  • Shani Z, Dekel M, Tsabary G, Goren R, Shoseyov O (2004) Growth enhancement of transgenic plants by overexpression of Arabidopsis thaliana endo1, 4-b-glucanase cel1. Plant Mol Biol 14:321–330

    Google Scholar 

  • Sheokand S, Dahiya P, Vincent JL, Brewin NJ (2005) Modified expression of cysteine protease affects seed germination, vegetative growth and nodule development in transgenic lines of Medicago truncatula. Plant Sci 169:966–975

    CAS  Google Scholar 

  • Shimizu M, Suzuki K, Miyazawa Y, Fujii N, Takahashi H (2006) Differential accumulation of the mRNA of the auxin-repressed gene CsGRP1 and the auxin-induced peg formation during gravimorphogenesis of cucumber seedlings. Planta 225:13–22

    PubMed  CAS  Google Scholar 

  • Shin D, Moon S-J, Park SR, Kim B-G, Byun M-O (2009) Elongation factor 1α from A. thaliana functions as molecular chaperone and confers resistance to salt stress in yeast and plants. Plant Sci 177:156–160

    CAS  Google Scholar 

  • Showalter AM (1993) Structure and Function of Plant Cell Wall Proteins. Plant Cell 5:9–23

    PubMed  CAS  Google Scholar 

  • Smart LB, Cameron K, Bennett AB (2000) Isolation of genes predominantly expressed in guard cells and epidermal cells of Nicotiana glauca. Plant Mol Biol 42:857–869

    PubMed  CAS  Google Scholar 

  • Smirnoff N (1992) The carbohydrates of bryophytes in relation to desiccation-tolerance. J Bryol 17:185–191

    Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acid. Plant Cell 17:616–627

    PubMed  CAS  Google Scholar 

  • Stone S, Williams LA, Farmer LM, Vierstra RD, Callis J (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signalling. Plant Cell 18:3415–3428

    PubMed  CAS  Google Scholar 

  • Takase T, Nakazawa M, Ishikawa A, Manabe K, Matsui M (2003) DFL2, a new member of the Arabidopsis GH3 gene family, is involved in red light-specific hypocotyl elongation. Plant Cell Physiol 44:1071–1080

    PubMed  CAS  Google Scholar 

  • Taleisnik E, Rodríguez AA, Bustos D, Erdei L, Ortega L, Senn ME (2009) Leaf expansion in grasses under salt stress. J Plant Physiol 166:1123–1140

    PubMed  CAS  Google Scholar 

  • Tani T, Sobajima H, Okada K, Chujo T, Arimura S, Tsutsumi N, Nishimura M, Seto H, Nojiri H, Yamane H (2008) Identification of the OsOPR7 gene encoding 12-oxophytodienoate reductase involved in the biosynthesis of jasmonic acid in rice. Planta 227:517–526

    PubMed  CAS  Google Scholar 

  • Tardif G, Kane NA, Adam H, Labrie L, Major G, Gulick P, Sarhan F, Laliberté J-F (2007) Interaction network of proteins associated with abiotic stress response and development in wheat. Plant Mol Biol 63:703–718

    PubMed  CAS  Google Scholar 

  • Termaat A, Passioura J, Munns R (1985) Shoot turgor does not limit shoot growth of NaCl-affected wheat and barley. Plant Physiol 77:869–872

    PubMed  CAS  Google Scholar 

  • Terol J, Domingo C, Talon M (2006) The GH3 family in plants: Genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371:279–290

    PubMed  CAS  Google Scholar 

  • Thomae A, Pich D, Brocher J, Spindler M-P, Berens C, Hock R, Hammerschmidt W, Schepers A (2008) Interaction between HMGA1a and the origin recognition complex creates site-specific replication origins. Proc Natl Acad Sci USA 105:1692–1697

    PubMed  CAS  Google Scholar 

  • Toldi O, Tuba Z, Scott P (2009) Vegetative desiccation tolerance: Is it a goldmine for bioengineering crops? Plant Sci 176:187–199

    CAS  Google Scholar 

  • Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812

    PubMed  CAS  Google Scholar 

  • Turck F, Zilbermann F, Kozma SC, Thomas G, Nagy F (2004) Phytohormones participate in an S6 kinase signal transduction pathway in Arabidopsis. Plant Physiol 134:1527–1535

    PubMed  CAS  Google Scholar 

  • Van der Vyver C, Schneidereit J, Driscoll S, Turner J, Kunert K, Foyer C (2003) Oryzacystatin I expression in transformed tobacco produces a conditional growth phenotype and enhances chilling tolerance. Plant Biotechnol J 1:101–112

    PubMed  Google Scholar 

  • Villalobos M, Bartels D, Iturriaga G (2004) Stress tolerance and glucose insensitive phenotypes in arabidopsis overexpressing the CpMYB10 transcription factor gene. Plant Physiol 135:309–324

    PubMed  CAS  Google Scholar 

  • Wagner TA, Kohorn BD (2001) Wall-Associated Kinases Are Expressed throughout Plant Development and Are Required for Cell Expansion. Plant Cell 13:303–318

    PubMed  CAS  Google Scholar 

  • Wang L, Li X, Chen S, Liu G (2009a) Enhanced drought tolerance in transgenic Leymus chinensis plants with constitutively expressed wheat TaLEA3. Biotechnol Lett 31:313–319

    PubMed  CAS  Google Scholar 

  • Wang L, Shang H, Lui Y, Zheng M, Wu R, Phillips J, Bartels D, Deng X (2009b) A role for a cell wall localized glycine-rich protein in dehydration and rehydration of the resurrection plant Boea hygrometrica. Plant Biol 11:837–848

    PubMed  CAS  Google Scholar 

  • Whittaker A, Martinelli T, Bochicchio A, Vazzana C, Farrant J (2004) Comparison of sucrose metabolism during the rehydration of desiccation-tolerant and desiccation-sensitive leaf material of Sporobolus stapfianus. Physiol Plant 122:11–20

    CAS  Google Scholar 

  • Xu D, Su P, Zhang R, Li H, Zhao L, Wang G (2010) Photosynthetic parameters and carbon reserves of a resurrection plant Reaumuria soongorica during dehydration and rehydration. Plant Growth Regul 60:183–190

    CAS  Google Scholar 

  • Yamaguchi-shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:1360–1385

    Google Scholar 

  • Yanga EJ, Ohb YA, Leea ES, Parka AR, Choa SK, Yoob YJ, Park OK (2003) Oxygen-evolving enhancer protein 2 is phosphorylated by glycine-rich protein 3/wall-associated kinase 1 in Arabidopsis. Biochem Biophys Res Commun 305:862–868

    Google Scholar 

  • Zhang J, Creelman RA, Zhu J-K (2004) From laboratory to field. Using information from Arabidopsis to engineer salt cold and drought tolerance in crops. Plant Physiol 135:615–621

    PubMed  CAS  Google Scholar 

  • Zhang Z, Li Q, Li Z, Staswick PE, Wang M, Zhu Y, He Z (2007) Dual Regulation Role of GH3.5 in Salicylic Acid and Auxin Signalling during Arabidopsis-Pseudomonas syringae Interaction. Plant Physiol 145:450–464

    PubMed  CAS  Google Scholar 

  • Zhong R, Kays SJ, Schroeder BP, Ye Z-H (2002) Mutation of a Chitinase-Like Gene Causes Ectopic Deposition of Lignin, Aberrant Cell Shapes, and Overproduction of Ethylene. Plant Cell 14:165–179

    PubMed  CAS  Google Scholar 

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Correspondence to Alan D. Neale.

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Blomstedt, C.K., Griffiths, C.A., Fredericks, D.P. et al. The resurrection plant Sporobolus stapfianus: An unlikely model for engineering enhanced plant biomass?. Plant Growth Regul 62, 217–232 (2010). https://doi.org/10.1007/s10725-010-9485-6

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