Abstract
The moss Physcomitrella patens possesses a single copy of a Group 1 LEA gene, designated PpLEA-1. Sequence analysis of the PpLEA-1 gene reveals the gene to contain a single intron in a position conserved in all members of the Group 1 LEA gene family, but also to contain a premature termination codon within the first exon. Nevertheless, a PpLEA-1 transcript accumulates in moss tissues in response both to the imposition of osmotic stress, and to the plant growth regulator abscisic acid (ABA). This response appears to be mediated at the transcriptional level, and observation of the pattern of gene expression, reported by histochemical staining of plants expressing a PpLea-1::GUS transgene suggests that the promoter responds preferentially to ABA in protonemal filaments, whereas osmotic stress induces gene expression primarily in the gametophores. Quantitative analysis of promoter activity by transient expression in Physcomitrella protoplasts shows the PpLEA-1 promoter to be highly active in response to ABA and osmotic stress. ABA-mediated transgene expression from the PpLea-1 promoter occurs at a level similar to that driven by the highly active promoter of the wheat Group 1 LEA gene, Em. Site-directed mutagenesis of the PpLEA-1 promoter indicates that ABA-inducibility is mediated via an ACGT-core motif similar to that seen in the ABA response elements of higher plant LEA genes. However, whereas the wheat Em promoter is active in moss tissues, the moss promoter is not reciprocally active in cereal cells: no activity, ABA-inducible or otherwise was detected in barley aleurone protoplasts transfected with the PpLEA-1::GUS construct. We propose that ABA activation of gene expression in moss cells represents an ancestral state, with only minimal requirements for promoter recognition, whereas cereal cells require the interaction of additional factors with ABA-responsive promoters.
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Abbreviations
- ABA:
-
Abscisic acid
- CTAB:
-
Hexadecyltrimethyl-ammonium-bromide
- GUS:
-
β-glucuronidase
- LEA:
-
Late Embryogenesis Abundant
- MOPS:
-
3-[N-Morpholino]propanesulphonic acid
- PEG:
-
Polyethylene glycol
- X-gluc:
-
5-bromo−4-chloro−3-indolyl-β-D-glucuronic acid
References
N.W. Ashton D.J. Cove (1977) ArticleTitleThe isolation and preliminary characterisation of auxotrophic and analogue resistant mutants of the moss Physcomitrella patens Mol. Gen. Genet. 154 87–95 Occurrence Handle10.1007/BF00265581
D. Bartels F. Salamini (2001) ArticleTitleDesiccation tolerance in the resurrection plant Craterostigma plantagienum. A contribution to the study of drought tolerance at the molecular level Plant Physiol 127 1346–1353 Occurrence Handle10.1104/pp.127.4.1346 Occurrence Handle11743072
J.D. Bewley (1995) ArticleTitlePhysiological aspects of desiccation tolerance – a retrospect Int. J. Plant Sci 156 393–403 Occurrence Handle10.1086/297261
J.D. Bewley P. Halmer J.E. Krochko W.E. Winner (1978) Metabolism of a drought tolerant and drought-sensitive moss: respiration, ATP synthesis and carbohydrate status J.H. Crowe J.S. Clegg (Eds) Dry Biological Systems Academic Press New York 185–203
M.M. Bradford (1976) ArticleTitleA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding Anal. Biochem 72 248–254 Occurrence Handle942051
S.M. Brady S.F. Sarkar D. Bonetta P. McCourt (2003) ArticleTitleThe ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis Plant J. 34 67–75 Occurrence Handle10.1046/j.1365-313X.2003.01707.x Occurrence Handle12662310
W.M. Butler A.C. Cuming (1993) ArticleTitleDifferential molecular responses to abscisic acid and osmotic stress in viviparous maize embryos Planta 189 47–54 Occurrence Handle10.1007/BF00201342
J. Casaretto T-H.D. Ho (2003) ArticleTitleThe transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells Plant Cell 15 271–284 Occurrence Handle10.1105/tpc.007096 Occurrence Handle12509536
P.M. Chandler M. Robertson (1994) ArticleTitleGene expression regulated by abscisic acid and its relation to stress tolerance Annu. Rev. Plant Physiol. Plant Mol. Biol. 45 113–141 Occurrence Handle10.1146/annurev.pp.45.060194.000553
A.C. Cuming (1984) ArticleTitleDevelopmental regulation of gene expression in wheat embryos – molecular cloning of a cDNA sequence encoding the early methionine labelled (Em) polypeptide Eur. J. Biochem. 145 351–357 Occurrence Handle10.1111/j.1432-1033.1984.tb08561.x Occurrence Handle6548709
A.C. Cuming (1999) LEA proteins P.R. Shewry R. Casey (Eds) Seed Proteins Kluwer Academic Publishers Dordrecht 753–780
B. Chen A.E. Przybyla (1994) ArticleTitleAn efficient site-directed mutagenesis method based on PCR BioTechniques 17 657–659 Occurrence Handle7833020
T.J.K. Dilks M.C.F. Proctor (1974) ArticleTitleThe pattern of recovery of bryophytes after desiccation J. Bryol. 82 115–125
L.S. Dure SuffixIII M. Crouch J. Harada T-H.D. Ho J. Mundy R.S. Quatrano T. Thomas Z.R. Sung (1989) ArticleTitleCommon amino acid sequence domains among the LEA proteins of higher plants Plant Mol. Biol. 12 475–486 Occurrence Handle10.1007/BF00036962
A.P. Feinberg B. Vogelstein (1984) ArticleTitleA technique for radiolabelling DNA restriction endonuclease fragments to high specific activity Anal. Biochem. 137 266–267 Occurrence Handle10.1016/0003-2697(84)90381-6 Occurrence Handle6329026
Frank, W., Ratnadewi, D. and Reski, R. 2004. Physcomitrella patens is highly tolerant against drought, salt and osmotic stress. Planta Onlinefirst : 1432--2048.
G.A. Galau D.W. Hughes L.S. Dure SuffixIII (1986) ArticleTitleAbscisic acid induction of cloned cotton late-embryogenesis-abundant (lea) mRNAs Plant Mol. Biol. 7 155–170 Occurrence Handle10.1007/BF00021327
S.S.L. Gampala R.R. Finkelstein S.S.M. Sun C.D. Rock (2002) ArticleTitleABI5 interacts with abscisic acid signalling effectors in rice protoplasts J. Biol. Chem. 277 1689–1694 Occurrence Handle10.1074/jbc.M109980200 Occurrence Handle11704678
J. Giraudat B.M. Hauge C. Valon J. Smalle F. Parcy H.M. Goodman (1992) ArticleTitleIsolation of the Arabidopsis ABI3 gene by positional cloning Plant Cell 4 1251–1261 Occurrence Handle10.1105/tpc.4.10.1251 Occurrence Handle1359917
M.J. Guiltinan W.R. Marcotte R.S. Quatrano (1990) ArticleTitleA plant leucine zipper protein that recognises an abscisic acid response element Science 250 267–271 Occurrence Handle2145628
T. Hattori T. Terada S. Hamasuna (1995) ArticleTitleRegulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1 Plant J. 7 913–925 Occurrence Handle10.1046/j.1365-313X.1995.07060913.x Occurrence Handle7599651
D.L. Herrin G.W. Schmidt (1988) ArticleTitleRapid, reversible staining of Northern blots prior to hybridization Biotechniques 6 196–200 Occurrence Handle2483319
T. Hobo Y. Kowyama T. Hattori (1999) ArticleTitleA bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription Proc Natl. Acad. Sci. USA 96 15348–15353 Occurrence Handle10.1073/pnas.96.26.15348
F.A. Hoekstra E.A. Golovina J. Buitink (2001) ArticleTitleMechanisms of plant desiccation tolerance Trends Plant Sci. 6 431–440 Occurrence Handle10.1016/S1360-1385(01)02052-0 Occurrence Handle11544133
J. Ingram D. Bartels (1996) ArticleTitleThe molecular basis of dehydration tolerance in plants Ann. Rev. Plant Physiol. Mol. Biol. 47 377–403 Occurrence Handle10.1146/annurev.arplant.47.1.377
J.V. Jacobsen T.J Close (1991) ArticleTitleControl of transient expression of chimaeric genes by gibberellic acid and abscisic acid in protoplasts prepared from mature barley aleurone layers Plant. Mol. Biol. 16 713–724 Occurrence Handle10.1007/BF00023435 Occurrence Handle1831055
R.A. Jefferson (1988) ArticleTitleAssaying chimeric genes in plants: the GUS gene fusion system Plant Mol. Biol. Rep. 5 387–405
T.A. Kavanagh R.A. Jefferson M.W. Bevan (1988) ArticleTitleTargeting a foreign protein to chloroplasts using fusions to the transit peptide of the chlorophyll a/b protein Molec. Gen. Genet. 215 38–45 Occurrence Handle10.1007/BF00331300 Occurrence Handle3071742
R. Kenrick P.R. Crane (1997) ArticleTitleThe origin and early evolution of plants on land Nature 389 33–39 Occurrence Handle10.1038/37918
C.D. Knight A. Seghal K. Atwal J.C. Wallace D.J. Cove D. Coates R.S. Quatrano S. Bahadur P.G. Stockley A.C. Cuming (1995) ArticleTitleMolecular responses to abscisic acid and stress are conserved between moss and cereals Plant Cell 7 499–506 Occurrence Handle10.1105/tpc.7.5.499 Occurrence Handle12242376
Knight, C.D., Cove, D.J., Cuming, A.C. and Quatrano, R.S., 2002. Moss gene technology. In: P.M. Gilmartin and Bowler, C. (Eds.), Molecular Plant Biology Vol. 2 A Practical Approach, Oxford University Press, pp. 285--301
J.C. Litts G.W. Colwell R.L. Chakerian R.S. Quatrano (1991) ArticleTitleSequence analysis of a functional member of the Em gene family from wheat DNA Seq. 1 263–274 Occurrence Handle1806042
W.R. Marcotte S.H. Russell R.S. Quatrano (1989) ArticleTitleAbscisic acid responsive sequences from the Em gene of wheat Plant Cell 1 969–979 Occurrence Handle10.1105/tpc.1.10.969 Occurrence Handle2562556
D.R. McCarty T. Hattori C.B. Carson V. Vasil M. Lazar I.K. Vasil (1991) ArticleTitleThe viviparous-1 developmental gene of maize encodes a novel transcriptional activator Cell 66 895–905 Occurrence Handle10.1016/0092-8674(91)90436-3 Occurrence Handle1889090
W.D. McCubbin C.M. Kay B.G. Lane (1985) ArticleTitleHydrodynamic and optical properties of the wheat-germ Em protein Can. J. Biochem. Cell Biol. 63 3607–3618
S. Nakamura T.J. Lynch R.R. Finkelstein (2001) ArticleTitlePhysical interaction between ABA-response loci of Arabidopsis Plant J. 26 627–635 Occurrence Handle10.1046/j.1365-313x.2001.01069.x Occurrence Handle11489176
M.J. Oliver Z. Tuba B.D. Mishler (2000) ArticleTitleThe evolution of vegetative desiccation tolerance in land plants Plant Ecol. 151 85–100 Occurrence Handle10.1023/A:1026550808557
M.J. Oliver A.J. Wood P. O’Mahony (1998) ArticleTitle“To dryness and beyond” – preparation for the dried state and rehydration in vegetative desiccation-tolerant plants Plant Growth Regul. 24 193–201 Occurrence Handle10.1023/A:1005863015130
S. Onde T.S. Futers A.C. Cuming (1994) ArticleTitleRapid analysis of an osmotic stress responsive promoter by transient expression in intact wheat embryos J. Exp. Bot. 45 561–566
R.S. Quatrano D. Bartels T-H.D. Ho M. Pages (1997) ArticleTitleNew insights into ABA-mediated processes Plant Cell 9 470–475 Occurrence Handle10.1105/tpc.9.4.470
S. Ramanjulu D. Bartels (2002) ArticleTitleDrought and desiccation induced modulation of gene expression in plants Plant Cell Environ. 25 141–151 Occurrence Handle10.1046/j.0016-8025.2001.00764.x Occurrence Handle11841659
M. Robertson A.C. Cuming P.M. Chandler (1995) ArticleTitleSequence analysis and hormonal regulation of a dehydrin promoter from barley, Hordeum vulgare Physiol. Plant. 94 470–478 Occurrence Handle10.1034/j.1399-3054.1995.940315.x
A. Rohde E. Prinsen R. Rycke ParticleDe G. Engler M. Montagu ParticleVan W. Boerjan (2002) ArticleTitlePtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar Plant Cell 14 1885–1901 Occurrence Handle10.1105/tpc.003186 Occurrence Handle12172029
T.F. Schulz J. Medina A. Hill R.S. Quatrano (1998) ArticleTitle14-3-3 proteins are part of an abscisic acid VIVIPAROUS1 (VP1) response complex in the Em promoter and interact with VP1 and EmBP1 Plant Cell 10 837–847 Occurrence Handle10.1105/tpc.10.5.837 Occurrence Handle9596641
Q.J. Shen J.A. Casaretto P. Zhang T-H.D. Ho (2004) ArticleTitleFunctional definition of ABA-response complexes: the promoter units necessary and sufficient for ABA induction of gene expression in barley (Hordeum vulgare L.) Plant Mol. Biol. 54 111–124 Occurrence Handle10.1023/B:PLAN.0000028773.94595.e8 Occurrence Handle15159638
Q. Shen P. Zhang T-H.D. Ho (1996) ArticleTitleModular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley Plant Cell 8 1107–1119 Occurrence Handle10.1105/tpc.8.7.1107 Occurrence Handle8768371
R.M. Taylor A.C. Cuming (1993) ArticleTitleSelective proteolysis of the wheat Em polypeptide. Identification of an endopeptidase activity in germinating wheat embryos FEBS Lett. 331 71–75 Occurrence Handle10.1016/0014-5793(93)80299-A Occurrence Handle8405414
Thuring, R.W.J., Sanders, J.P.M. and Borst, P. 1975. Freezesqueeze method for recovering long DNA from agarose gels. Anal. Biochem. : 213--220.
V. Vasil W.R Marcotte SuffixJr. L. Rosenkrans S.M. Cocciolone I.K. Vasil R.S. Quatrano D.R. McCarty (1995) ArticleTitleOverlap of Viviparous1 (VP1) and abscisic acid response elements in the Em promoter: G-box elements are sufficient but not necessary for VP1 transactivation Plant Cell 7 1511–1518 Occurrence Handle10.1105/tpc.7.9.1511 Occurrence Handle8589631
J.D. Williamson R.S. Quatrano A.C. Cuming (1985) ArticleTitleEm polypeptide and its messenger RNA levels are modulated by abscisic acid during embryogenesis in wheat Eur. J. Biochem. 152 501–507 Occurrence Handle10.1111/j.1432-1033.1985.tb09224.x Occurrence Handle2932332
M.J. Wise A. Tunnacliffe (2004) ArticleTitlePOPP the question: what do LEA proteins do? Trends in Plant Sci. 9 13–17 Occurrence Handle10.1016/j.tplants.2003.10.012
D. Yang L. Wu Y-S. Hwang L. Chen N. Huang (2001) ArticleTitleExpression of the REB transcriptional activator in rice grains improves the yield of recombinant proteins whose genes are controlled by a Reb-responsive promoter Proc Natl. Acad. Sci. USA 98 11438–11443 Occurrence Handle10.1073/pnas.201411298
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Kamisugi, Y., Cuming, A.C. The Evolution of the Abscisic Acid-response in Land Plants: Comparative Analysis of Group 1 LEA Gene Expression in Moss and Cereals. Plant Mol Biol 59, 723–737 (2005). https://doi.org/10.1007/s11103-005-0909-z
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DOI: https://doi.org/10.1007/s11103-005-0909-z