Skip to main content
Log in

Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Regulatory networks of salt stress and abscisic acid (ABA) responses have previously been analyzed in seed plants. Here, we report microarray expression profiles of 439 genes encoding transcription-associated proteins (TAPs) in response to salt stress and ABA in the salt-tolerant moss Physcomitrella patens. Fourteen and 56 TAP genes were differentially expressed within 60 min of NaCl and ABA treatment, respectively, indicating that these responses are regulated at the transcriptional level. Overlapping expression profiles, as well as the up-regulation of ABA biosynthesis genes, suggest that ABA mediates the salt stress responses in P. patens. Comparison to public gene expression data of Arabidopsis thaliana and phylogenetic analyses suggest that the role of DREB-like, Dof, and bHLH TAPs in salt stress responses have been conserved during embryophyte evolution, and that the function of ABI3-like, bZIP, HAP3, and CO-like TAPs in seed development and flowering emerged from pre-existing ABA and light signalling pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

LCA:

Last common ancestor

MYA:

Million years ago

NCED:

9-cis-epoxycarotenoid dioxygenase

References

  • Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868

    Article  CAS  PubMed  Google Scholar 

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    Article  CAS  PubMed  Google Scholar 

  • Abraham E, Rigo G, Szekely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Baldi P, Long AD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes. Bioinformatics 17:509–519

    Article  CAS  PubMed  Google Scholar 

  • Benito B, Rodriguez-Navarro A (2003) Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens. Plant J 36:382–389

    Article  CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate–a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodol 57:289–300

    Google Scholar 

  • Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1232–1238

    Article  CAS  PubMed  Google Scholar 

  • Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The 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

    Article  CAS  PubMed  Google Scholar 

  • Buck MJ, Atchley WR (2003) Phylogenetic analysis of plant basic helix-loop-helix proteins. J Mol Evol 56:742–750

    Article  CAS  PubMed  Google Scholar 

  • Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17:427–431

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Costa LM, Biderre-Petit C, Kbhaya B, Dey N, Perez P, McCarty DR, Gutierrez-Marcos JF, Becraft PW (2007) Abscisic acid and stress signals induce Viviparous1 expression in seed and vegetative tissues of maize. Plant Physiol 143:720–731

    Article  CAS  PubMed  Google Scholar 

  • Chao DY, Luo YH, Shi M, Luo D, Lin HX (2005) Salt-responsive genes in rice revealed by cDNA microarray analysis. Cell Res 15:796–810

    Article  CAS  PubMed  Google Scholar 

  • Chen WJ, Zhu T (2004) Networks of transcription factors with roles in environmental stress response. Trends Plant Sci 9:591–596

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574

    Article  CAS  PubMed  Google Scholar 

  • Chen NZ, Zhang XQ, Wei PC, Chen QJ, Ren F, Chen J, Wang XC (2007) AtHAP3b plays a crucial role in the regulation of flowering time in Arabidopsis during osmotic stress. J Biochem Mol Biol 40:1083–1089

    CAS  PubMed  Google Scholar 

  • Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198

    Article  PubMed  CAS  Google Scholar 

  • Chernys JT, Zeevaart JA (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124:343–353

    Article  CAS  PubMed  Google Scholar 

  • Chico JM, Chini A, Fonseca S, Solano R (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 11:486–494

    Article  CAS  PubMed  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  CAS  PubMed  Google Scholar 

  • Cho SH, Hoang Q, Phee JW, Kim YY, Shin HY, Shin JS (2007) Modified suppression subtractive hybridization identifies an AP2-containing protein involved in metal responses in Physcomitrella patens. Mol Cells 23:100–107

    CAS  PubMed  Google Scholar 

  • Choe SE, Boutros M, Michelson AM, Church GM, Halfon MS (2005) Preferred analysis methods for Affymetrix GeneChips revealed by a wholly defined control dataset. Genome Biol 6:R16

    Article  PubMed  Google Scholar 

  • Clamp M, Cuff J, Searle SM, Barton GJ (2004) The Jalview Java alignment editor. Bioinformatics 20:426–427

    Article  CAS  PubMed  Google Scholar 

  • Cleveland WS (1979) Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74:829–836

    Article  Google Scholar 

  • Corrêa LG, Riano-Pachon DM, Schrago CG, dos Santos RV, Mueller-Roeber B, Vincentz M (2008) The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes. PLoS ONE 3:e2944

    Article  PubMed  CAS  Google Scholar 

  • Cuming AC, Cho SH, Kamisugi Y, Graham H, Quatrano RS (2007) Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss, Physcomitrella patens. New Phytol 176:275–287

    Article  CAS  PubMed  Google Scholar 

  • De Bodt S, Raes J, Van de Peer Y, Theissen G (2003) And then there were many: MADS goes genomic. Trends Plant Sci 8:475–483

    Article  PubMed  CAS  Google Scholar 

  • Decker EL, Frank W, Sarnighausen E, Reski R (2006) Moss systems biology en route: phytohormones in Physcomitrella development. Plant Biol (Stuttg) 8:397–405

    Article  CAS  Google Scholar 

  • Denby K, Gehring C (2005) Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. Trends Biotechnol 23:547–552

    Article  CAS  PubMed  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):S15–S45

    CAS  PubMed  Google Scholar 

  • Frank W, Decker EL, Reski R (2005a) Molecular tools to study Physcomitrella patens. Plant Biol (Stuttg) 7:220–227

    Article  CAS  Google Scholar 

  • Frank W, Ratnadewi D, Reski R (2005b) Physcomitrella patens is highly tolerant against drought, salt and osmotic stress. Planta 220:384–394

    Article  CAS  PubMed  Google Scholar 

  • Frank W, Baar KM, Qudeimat E, Woriedh M, Alawady A, Ratnadewi D, Gremillon L, Grimm B, Reski R (2007) A mitochondrial protein homologous to the mammalian peripheral-type benzodiazepine receptor is essential for stress adaptation in plants. Plant J 51:1004–1018

    Article  CAS  PubMed  Google Scholar 

  • Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839

    Article  CAS  PubMed  Google Scholar 

  • Goode JA, Stead AD, Duckett JG (1993) Redifferentiation of moss protonemata–an experimental and immunofluorescence study of brood cell-formation. Can J Bot 71:1510–1519

    Google Scholar 

  • Gremme G, Brendel V, Sparks ME, Kurtz S (2005) Engineering a software tool for gene structure prediction in higher organisms. Inf Softw Technol 47:965–978

    Article  Google Scholar 

  • Guo AY, Chen X, Gao G, Zhang H, Zhu QH, Liu XC, Zhong YF, Gu X, He K, Luo J (2008) PlantTFDB: a comprehensive plant transcription factor database. Nucleic Acids Res 36:D966–D969

    Article  CAS  PubMed  Google Scholar 

  • Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Katoh E, Xiang H, Tanahashi T, Hasebe M, Banks JA, Ashikari M, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2007) The GID1-mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the Bryophyte Physcomitrella patens. Plant Cell 19:3058–3079

    Article  CAS  PubMed  Google Scholar 

  • Hohe A, Reski R (2002) Optimisation of a bioreactor culture of the moss Physcomitrella patens for mass production of protoplasts. Plant Sci 163:69–74

    Article  CAS  Google Scholar 

  • Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737

    Article  CAS  PubMed  Google Scholar 

  • Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264

    Article  PubMed  Google Scholar 

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333

    Article  CAS  PubMed  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  CAS  PubMed  Google Scholar 

  • Jia W, Wang Y, Zhang S, Zhang J (2002) Salt-stress-induced ABA accumulation is more sensitively triggered in roots than in shoots. J Exp Bot 53:2201–2206

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25

    Article  PubMed  CAS  Google Scholar 

  • Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8:217–230

    Article  CAS  PubMed  Google Scholar 

  • Kamisugi Y, Cuming AC (2005) 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

    Article  CAS  PubMed  Google Scholar 

  • Kant S, Kant P, Raveh E, Barak S (2006) Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila. Plant Cell Environ 29:1220–1234

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Liu 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

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905

    Article  CAS  PubMed  Google Scholar 

  • Kim JB, Kang JY, Kim SY (2004) Over-expression of a transcription factor regulating ABA-responsive gene expression confers multiple stress tolerance. Plant Biotechnol J 2:459–466

    Article  CAS  PubMed  Google Scholar 

  • Knight CD, Sehgal A, Atwal K, Wallace JC, Cove DJ, Coates D, Quatrano RS, Bahadur S, Stockley PG, Cuming AC (1995) Molecular responses to abscisic acid and stress are conserved between moss and cereals. Plant Cell 7:499–506

    Article  CAS  PubMed  Google Scholar 

  • Knight H, Zarka DG, Okamoto H, Thomashow MF, Knight MR (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol 135:1710–1717

    Article  CAS  PubMed  Google Scholar 

  • Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    Article  CAS  PubMed  Google Scholar 

  • Kroemer K, Reski R, Frank W (2004) Abiotic stress response in the moss Physcomitrella patens: evidence for an evolutionary alteration in signaling pathways in land plants. Plant Cell Rep 22:864–870

    Article  CAS  PubMed  Google Scholar 

  • Kurup S, Jones HD, Holdsworth MJ (2000) Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. Plant J 21:143–155

    Article  CAS  PubMed  Google Scholar 

  • Lang D, Eisinger J, Reski R, Rensing SA (2005) Representation and high-quality annotation of the Physcomitrella patens transcriptome demonstrates a high proportion of proteins involved in metabolism in mosses. Plant Biol (Stuttg) 7:238–250

    Article  CAS  Google Scholar 

  • Lang D, Zimmer AD, Rensing SA, Reski R (2008) Exploring plant biodiversity: the Physcomitrella genome and beyond. Trends Plant Sci 13:542–549

    Article  CAS  PubMed  Google Scholar 

  • Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine. Genome Res 16:414–427

    Article  CAS  PubMed  Google Scholar 

  • Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240

    Article  CAS  PubMed  Google Scholar 

  • Liu N, Zhong NQ, Wang GL, Li LJ, Liu XL, He YK, Xia GX (2007) Cloning and functional characterization of PpDBF1 gene encoding a DRE-binding transcription factor from Physcomitrella patens. Planta 226:827–838

    Article  CAS  PubMed  Google Scholar 

  • Lu G, Paul AL, McCarty DR, Ferl RJ (1996) Transcription factor veracity: is GBF3 responsible for ABA-regulated expression of Arabidopsis Adh? Plant Cell 8:847–857

    Article  CAS  PubMed  Google Scholar 

  • Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305

    Article  CAS  PubMed  Google Scholar 

  • Lunde C, Drew DP, Jacobs AK, Tester M (2007) Exclusion of Na+ via sodium ATPase (PpENA1) ensures normal growth of Physcomitrella patens under moderate salt stress. Plant Physiol 144:1786–1796

    Article  CAS  PubMed  Google Scholar 

  • Ma S, Bohnert HJ (2007) Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biol 8:R49

    Article  PubMed  CAS  Google Scholar 

  • Ma S, Gong Q, Bohnert HJ (2006) Dissecting salt stress pathways. J Exp Bot 57:1097–1107

    Article  CAS  PubMed  Google Scholar 

  • Maizel A, Busch MA, Tanahashi T, Perkovic J, Kato M, Hasebe M, Weigel D (2005) The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science 308:260–263

    Article  CAS  PubMed  Google Scholar 

  • Mallappa C, Yadav V, Negi P, Chattopadhyay S (2006) A basic leucine zipper transcription factor, G-box-binding factor 1, regulates blue light-mediated photomorphogenic growth in Arabidopsis. J Biol Chem 281:22190–22199

    Article  CAS  PubMed  Google Scholar 

  • Marella HH, Sakata Y, Quatrano RS (2006) Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3-like genes from Physcomitrella patens. Plant J 46:1032–1044

    Article  CAS  PubMed  Google Scholar 

  • Martin A, Lang D, Heckmann J, Zimmer AD, Vervliet-Scheebaum M, Reski R (2009) A uniquely high number of ftsZ genes in the moss Physcomitrella patens. Plant Biol (Stuttg) 11:744–750

    Article  CAS  Google Scholar 

  • Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer DG, Dolan L (2007) An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316:1477–1480

    Article  CAS  PubMed  Google Scholar 

  • Millar AA, Jacobsen JV, Ross JJ, Helliwell CA, Poole AT, Scofield G, Reid JB, Gubler F (2006) Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8’-hydroxylase. Plant J 45:942–954

    Article  CAS  PubMed  Google Scholar 

  • Minami A, Nagao M, Arakawa K, Fujikawa S, Takezawa D (2003) Abscisic acid-induced freezing tolerance in the moss Physcomitrella patens is accompanied by increased expression of stress-related genes. J Plant Physiol 160:475–483

    Article  CAS  PubMed  Google Scholar 

  • Minami A, Nagao M, Ikegami K, Koshiba T, Arakawa K, Fujikawa S, Takezawa D (2005) Cold acclimation in bryophytes: low-temperature-induced freezing tolerance in Physcomitrella patens is associated with increases in expression levels of stress-related genes but not with increase in level of endogenous abscisic acid. Planta 220:414–423

    Article  CAS  PubMed  Google Scholar 

  • Montiel G, Gantet P, Jay-Allemand C, Breton C (2004) Transcription factor networks. Pathways to the knowledge of root development. Plant Physiol 136:3478–3485

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Risueno MA, Martinez M, Vicente-Carbajosa J, Carbonero P (2007) The family of DOF transcription factors: from green unicellular algae to vascular plants. Mol Genet Genomics 277:379–390

    Article  CAS  PubMed  Google Scholar 

  • Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475

    Article  CAS  PubMed  Google Scholar 

  • Oldenhof H, Wolkers WF, Bowman JL, Tablin F, Crowe JH (2006) Freezing and desiccation tolerance in the moss Physcomitrella patens: an in situ Fourier transform infrared spectroscopic study. Biochim Biophys Acta 1760:1226–1234

    CAS  PubMed  Google Scholar 

  • Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151:85–100

    Article  Google Scholar 

  • Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6:1567–1582

    Article  CAS  PubMed  Google Scholar 

  • Parcy F, Valon C, Kohara A, Misera S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277

    Article  CAS  PubMed  Google Scholar 

  • Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046

    Article  CAS  PubMed  Google Scholar 

  • Park DH, Lim PO, Kim JS, Cho DS, Hong SH, Nam HG (2003) The Arabidopsis COG1 gene encodes a Dof domain transcription factor and negatively regulates phytochrome signaling. Plant J 34:161–171

    Article  CAS  PubMed  Google Scholar 

  • Pavlidis P, Li Q, Noble WS (2003) The effect of replication on gene expression microarray experiments. Bioinformatics 19:1620–1627

    Article  CAS  PubMed  Google Scholar 

  • Pearson RD (2008) A comprehensive re-analysis of the Golden Spike data: towards a benchmark for differential expression methods. BMC Bioinformatics 9:164

    Article  PubMed  Google Scholar 

  • Qian Z, Cai YD, Li Y (2006) Automatic transcription factor classifier based on functional domain composition. Biochem Biophys Res Commun 347:141–144

    Article  CAS  PubMed  Google Scholar 

  • Qin X, Zeevaart JA (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96:15354–15361

    Article  CAS  PubMed  Google Scholar 

  • Qudeimat E, Faltusz AM, Wheeler G, Lang D, Brownlee C, Reski R, Frank W (2008) A PIIB-type Ca2+ -ATPase is essential for stress adaptation in Physcomitrella patens. Proc Natl Acad Sci USA 105:19555–19560

    Article  CAS  PubMed  Google Scholar 

  • Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767

    Article  CAS  PubMed  Google Scholar 

  • Rensing SA, Fritzowsky D, Lang D, Reski R (2005) Protein encoding genes in an ancient plant: analysis of codon usage, retained genes and splice sites in a moss, Physcomitrella patens. BMC Genomics 6:43

    Article  PubMed  CAS  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69

    Article  CAS  PubMed  Google Scholar 

  • Reski R, Abel WO (1985) Induction of budding on chloronemata and caulonemata of the moss, Physcomitrella patens, using isopentenyladenine. Planta 165:354–358

    Article  CAS  Google Scholar 

  • Riano-Pachon DM, Ruzicic S, Dreyer I, Mueller-Roeber B (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinformatics 8:42

    Article  PubMed  CAS  Google Scholar 

  • Riano-Pachon DM, Corrêa LG, Trejos-Espinosa R, Mueller-Roeber B (2008) Green transcription factors: a chlamydomonas overview. Genetics 179:31–39

    Article  CAS  PubMed  Google Scholar 

  • Richardt S, Lang D, Reski R, Frank W, Rensing SA (2007) PlanTAPDB, a phylogeny-based resource of plant transcription-associated proteins. Plant Physiol 143:1452–1466

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1101

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646

    Article  CAS  PubMed  Google Scholar 

  • Riese M, Faigl W, Quodt V, Verelst W, Matthes A, Saedler H, Munster T (2005) Isolation and characterization of new MIKC*-Type MADS-box genes from the moss Physcomitrella patens. Plant Biol (Stuttg) 7:307–314

    Article  CAS  Google Scholar 

  • Rohde A, Van Montagu M, Boerjan W (1999) The ABSCISIC ACID-INSENSITIVE 3 (ABI3) gene is expressed during vegetative quiescence processes in Arabidopsis. Plant Cell Environ 22:261–270

    Article  CAS  Google Scholar 

  • Rohde A, Prinsen E, De Rycke R, Engler G, Van Montagu M, Boerjan W (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell 14:1885–1901

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rossini L, Cribb L, Martin DJ, Langdale JA (2001) The maize golden2 gene defines a novel class of transcriptional regulators in plants. Plant Cell 13:1231–1244

    Article  CAS  PubMed  Google Scholar 

  • Saavedra L, Svensson J, Carballo V, Izmendi D, Welin B, Vidal S (2006) A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant J 45:237–249

    Article  CAS  PubMed  Google Scholar 

  • Sakakibara K, Nishiyama T, Kato M, Hasebe M (2001) Isolation of homeodomain-leucine zipper genes from the moss Physcomitrella patens and the evolution of homeodomain-leucine zipper genes in land plants. Mol Biol Evol 18:491–502

    CAS  PubMed  Google Scholar 

  • Sakakibara K, Nishiyama T, Sumikawa N, Kofuji R, Murata T, Hasebe M (2003) Involvement of auxin and a homeodomain-leucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development 130:4835–4846

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  CAS  PubMed  Google Scholar 

  • Satoh R, Fujita Y, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K (2004) A novel subgroup of bZIP proteins functions as transcriptional activators in hypoosmolarity-responsive expression of the ProDH gene in Arabidopsis. Plant Cell Physiol 45:309–317

    Article  CAS  PubMed  Google Scholar 

  • Schmitz G, Theres K (2005) Shoot and inflorescence branching. Curr Opin Plant Biol 8:506–511

    Article  CAS  PubMed  Google Scholar 

  • Schnepf E, Reinhard C (1997) Brachycytes in Funaria protonemate: Induction by abscisic acid and fine structure. J Plant Physiol 151:166–175

    CAS  Google Scholar 

  • Schwartz SH, Qin X, Zeevaart JA (2001) Characterization of a novel carotenoid cleavage dioxygenase from plants. J Biol Chem 276:25208–25211

    Article  CAS  PubMed  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  CAS  PubMed  Google Scholar 

  • Shen H, Cao K, Wang X (2007) A conserved proline residue in the leucine zipper region of AtbZIP34 and AtbZIP61 in Arabidopsis thaliana interferes with the formation of homodimer. Biochem Biophys Res Commun 362:425–430

    Article  CAS  PubMed  Google Scholar 

  • Shigyo M, Hasebe M, Ito M (2006) Molecular evolution of the AP2 subfamily. Gene 366:256–265

    Article  CAS  PubMed  Google Scholar 

  • Shigyo M, Tabei N, Yoneyama T, Yanagisawa S (2007) Evolutionary processes during the formation of the plant-specific Dof transcription factor family. Plant Cell Physiol 48:179–185

    Article  CAS  PubMed  Google Scholar 

  • Singer SD, Krogan NT, Ashton NW (2007) Clues about the ancestral roles of plant MADS-box genes from a functional analysis of moss homologues. Plant Cell Rep 26:1155–1169

    Article  CAS  PubMed  Google Scholar 

  • Song C-P, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu J-K (2005) Role of an arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396

    Article  CAS  PubMed  Google Scholar 

  • Sorefan K, Booker J, Haurogne K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, Leyser O (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17:1469–1474

    Article  CAS  PubMed  Google Scholar 

  • Sun Z, Hans J, Walter MH, Matusova R, Beekwilder J, Verstappen FW, Ming Z, van Echtelt E, Strack D, Bisseling T, Bouwmeester HJ (2008) Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions. Planta 228:789–801

    Article  CAS  PubMed  Google Scholar 

  • Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Seki M, Ishida J, Satou M, Sakurai T, Narusaka M, Kamiya A, Nakajima M, Enju A, Akiyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Mol Biol 56:29–55

    Article  CAS  PubMed  Google Scholar 

  • Takezawa D, Minami A (2004) Calmodulin-binding proteins in bryophytes: identification of abscisic acid-, cold-, and osmotic stress-induced genes encoding novel membrane-bound transporter-like proteins. Biochem Biophys Res Commun 317:428–436

    Article  CAS  PubMed  Google Scholar 

  • Tamminen I, Makela P, Heino P, Palva ET (2001) Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana. Plant J 25:1–8

    Article  CAS  PubMed  Google Scholar 

  • Tan BC, Schwartz SH, Zeevaart JA, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240

    Article  CAS  PubMed  Google Scholar 

  • Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56

    Article  CAS  PubMed  Google Scholar 

  • Tanahashi T, Sumikawa N, Kato M, Hasebe M (2005) Diversification of gene function: homologs of the floral regulator FLO/LFY control the first zygotic cell division in the moss Physcomitrella patens. Development 132:1727–1736

    Article  CAS  PubMed  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • Tintelnot S (2006) Influence of abscic acid on the plant cell wall: Analysis of extracellular proteins of the moss Physcomitrella patens. Unversity of Freiburg, http://www.freidok.uni-freiburg.de/volltexte/2492/

  • Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G (2007) The tify family previously known as ZIM. Trends Plant Sci 12:239–244

    Article  CAS  PubMed  Google Scholar 

  • Veron AS, Kaufmann K, Bornberg-Bauer E (2007) Evidence of interaction network evolution by whole-genome duplications: a case study in MADS-box proteins. Mol Biol Evol 24:670–678

    Article  CAS  PubMed  Google Scholar 

  • Volkov V, Wang B, Dominy PJ, Fricke W, Amtmann A (2004) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Environ 27:1–14

    Article  CAS  Google Scholar 

  • Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ 30:410–421

    Article  CAS  PubMed  Google Scholar 

  • Wang PC, Du YY, An GY, Zhou Y, Miao C, Song CP (2006) Analysis of global expression profiles of Arabidopsis genes under abscisic acid and H2O2 applications. J Integr Plant Biol 48:62–74

    Article  CAS  Google Scholar 

  • Wang X, Yang P, Gao Q, Liu X, Kuang T, Shen S, He Y (2008) Proteomic analysis of the response to high-salinity stress in Physcomitrella patens. Planta 228:167–177

    Article  CAS  PubMed  Google Scholar 

  • Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18:2971–2984

    Article  CAS  PubMed  Google Scholar 

  • Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123:1337–1349

    Article  CAS  PubMed  Google Scholar 

  • Wong CE, Li Y, Labbe A, Guevara D, Nuin P, Whitty B, Diaz C, Golding GB, Gray GR, Weretilnyk EA, Griffith M, Moffatt BA (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140:1437–1450

    Article  CAS  PubMed  Google Scholar 

  • Wu Z, Irizarry RA, Gentleman F, Martinez-Murillo F, Spencer F (2004) A model based background adjustment for oligonucleotide expression arrays. J Am Stat 99:909–917

    Article  Google Scholar 

  • Xie Z, Li X, Glover BJ, Bai S, Rao GY, Luo J, Yang J (2008) Duplication and functional diversification of HAP3 genes leading to the origin of the seed-developmental regulatory gene, LEAFY COTYLEDON1 (LEC1), in nonseed plant genomes. Mol Biol Evol 25:1581–1592

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391

    Article  CAS  PubMed  Google Scholar 

  • Yasumura Y, Moylan EC, Langdale JA (2005) A conserved transcription factor mediates nuclear control of organelle biogenesis in anciently diverged land plants. Plant Cell 17:1894–1907

    Article  CAS  PubMed  Google Scholar 

  • Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP (2007) Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr Biol 17:1225–1230

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K (2005) Evolutionary process of stress response systems controlled by abscisic acid in photosynthetic organisms. Yakugaku Zasshi 125:927–936

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Igarashi E, Mukai M, Hirata K, Miyamoto K (2003) Induction of tolerance to oxidative stress in the green alga, Chlamydomonas reinhardtii, by abscisic acid. Plant Cell Environ 26:451–457

    Article  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  Google Scholar 

  • Zimmer A, Lang D, Richardt S, Frank W, Reski R, Rensing SA (2007) Dating the early evolution of plants: detection and molecular clock analyses of orthologs. Mol Genet Genomics 278:393–402

    Article  CAS  PubMed  Google Scholar 

  • Zobell O, Coupland G, Reiss B (2005) The family of CONSTANS-like genes in Physcomitrella patens. Plant Biol (Stuttg) 7:266–275

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Richard Haas for technical support. This work was supported by the German Research Foundation (grants Re 837/6-3 to R.R. and W.F. and Re 837/10-2 to R.R. and S.A.R.), the Federal Ministry of Education and Research (grant FRISYS 0313921), the Excellence Initiative of the German Federal and State Governments (grant EXC 294), and the German Academic Exchange Service (Ph.D. fellowships to E.Q. and L.G.G.C.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wolfgang Frank.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11103_2009_9550_MOESM1_ESM.pdf

Images of P. patens protonemata before and after treatment with ABA and NaCl. Size bars were inserted using the Axiovert v4.7 software. a: untreated; b: 30 min 10 µM ABA; c: 60 min 10 µM ABA; d: 30 min 250 mM NaCl; e: 60 min 250 mM NaCl (PDF 225 kb)

11103_2009_9550_MOESM2_ESM.xls

Annotation and normalized expression data of P. patens microarray TAP features and internal control genes. Differential expression upon 10 µM ABA and 250 mM NaCl was determined using the regularized t-test CyberT. q-values indicate FDR-corrected P-values and fold change factors were calculated from the average expression under treated and control conditions. TAP family classification is based on the presence of protein domain patterns and the cited literature describes the phylogenetic and/or functional characterization of individual genes (XLS 136 kb)

11103_2009_9550_MOESM3_ESM.xls

Annotation and normalized expression data of A. thaliana TAP features of the ATH1 microarray. Differential expression upon 10 µM ABA and 150 mM NaCl was determined using the regularized t-test CyberT. q-values indicate FDR-corrected P-values and fold change factors were calculated from the average expression under treated and control conditions. TAP family classification is based on the presence of protein domain patterns (XLS 609 kb)

11103_2009_9550_MOESM4_ESM.pdf

Multiple sequence alignments of plant NCED and TAP proteins. MAFFT linsi alignments of conserved regions covering the NCED or DNA-binding domains of a: NCED, b: AP2/EREBP, c: bHLH, d: B3, e: tify proteins. The blue color code of residues represents the relative identity of this residue within a column. The consensus sequence is shown below the alignments (PDF 2026 kb)

11103_2009_9550_MOESM5_ESM.xls

Classification, microarray representation and differential expression of P. patens and A. thaliana TAP genes per family. The number of P. patens and A. thaliana TAP genes per family is listed, that were predicted, are represented by probe sets on the P. patens 12K TAP and A. thaliana ATH1 microarray platforms, and show differential expression upon salt stress or ABA treatment in P. patens protonema and A. thaliana seedlings. The separate results for the salt stress datasets of roots and shoots were combined according to Ma et al. (2006). TAP families are divided into the groups of transcription factors (TFs), other transcriptional regulators (TRs), and putative TAPs according to Richardt et al. (2007) (XLS 31 kb)

11103_2009_9550_MOESM6_ESM.xls

A. thaliana TAP genes differentially expressed upon salt stress and/or ABA. Genes with significant changes in transcript abundance (FDR q-value < 0.05, estimated fold change > 2) are shown. According to Ma et al. (2006) only genes with significant expression changes in the same direction in the separate root and shoot expression data are considered as differentially expressed upon salt stress. For separate expression data of roots and shoots see Supplementary Table S2. TAP family classification is based on the presence of protein domain patterns (XLS 38 kb)

11103_2009_9550_MOESM7_ESM.pdf

Phylogeny of plant AP2/EREBP TFs. The tree was calculated using Bayesian inference (BI) and BI posterior probabilities are shown. All P. patens proteins that carry an AP2 domain and were found to be differentially expressed upon high salinity or ABA treatment are included, as well as annotated AP2/EREBP proteins from A. thaliana. The following plant proteins are included as well: GhDBP1 (AAO43165), and GhDBP2 (AAT39542) from Gossypium hirsutum; GmDERBb (AAQ57226), GmDREB1 (AAP47161), GmDREB3 (ABB36646), GmDREBa (AAT12423), and GmDREBc (AAP83131) from Glycine max; HvCBF1 (AAK01088), HvCBF2 (AAM13419), and HvCBF6 (AAX23701) from Hordeum vulgare; OsDREB1A (AAN02486), OsDREB1B (AAX28958), OsDREB1C (BAA90812), OsDREB1D (AAX23721), OsDREB1E (AAX23722), OsDREB1F (AAX23723), OsDREB2A (AAN02487), and OsPAP (NP_922723) from O. sativa; TaCBF1 (AAL37944), TaCBF6 (AAX28964), and TaDREB1 (AAL01124) from Triticum aestivum: ZmDBF1 (AAM80486), and ZmDBF2 (AAM80485) from Zea mays. The expression of P. patens genes in protonema is indicated using the following color code: red, induced by both ABA and salt; yellow, induced by ABA; blue, induced by salt; green, repressed by ABA (PDF 588 kb)

11103_2009_9550_MOESM8_ESM.pdf

Phylogeny of plant bHLH TFs. The tree was calculated using Bayesian inference (BI) and BI posterior probabilities are shown. All P. patens proteins carrying a HLH domain and being represented by probe sets on the microarray are included, as well as annotated bHLH proteins from A. thaliana; OsMYC (AAS66204), OsRa (AAC49219), OsRb (AAC49220), and OsBP-5 (CAD32238) from O. sativa; and ZmLc (ABD72707) from Zea mays. The expression of P. patens genes in protonema is indicated using the following color code: yellow, induced by ABA; blue, induced by salt; green, repressed by ABA (PDF 759 kb)

11103_2009_9550_MOESM9_ESM.pdf

Phylogeny of plant B3 TFs. The tree was calculated using Bayesian inference (BI) and BI posterior probabilities are shown. All classified P. patens and A. thaliana proteins are included carrying a B3 domain. The following plant ABI3/VP1 proteins are included as well: LeABI3 (AAW84252) from Lycopersicon esculentum; DcC-ABI3 (BAA82596) from Daucus carota; PtABI3 (CAA05921) from Populus trichocarpa; PvAlf (AAA87030) from Phaseolus vulgaris; HvVP1 (AAO06117) from Hordeum vulgare; TaVP1 (BAB40614) from Triticum aestivum; OsVP1 (S43768) from O. sativa; CpVP1 (CAA04184) from Craterostigma plantagineum; AfVP1 (CAA04553) from Avena fatua; ZmVP1 (NP_001105540) from Zea mays. The expression of P. patens genes in protonema is indicated using the following color code: red, induced by both ABA and salt; yellow, induced by ABA; grey, not represented by probe sets on the microarray (PDF 849 kb)

11103_2009_9550_MOESM10_ESM.pdf

Phylogeny of plant tify TFs. The tree was calculated using Bayesian inference (BI) and BI posterior probabilities are shown. All classified P. patens and A. thaliana proteins are included carrying the tify domain and optionally GATA and CCT domains. NtPPS3 (BAD04852) from Nicotiana benthamiana is included as well. The expression of P. patens genes in protonema is indicated using the following color code: blue, induced by salt; grey, not represented by probe sets on the microarray (PDF 355 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Richardt, S., Timmerhaus, G., Lang, D. et al. Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling. Plant Mol Biol 72, 27–45 (2010). https://doi.org/10.1007/s11103-009-9550-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-009-9550-6

Keywords

Navigation