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

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.

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Abbreviations

ABA:

Abscisic acid

LCA:

Last common ancestor

MYA:

Million years ago

NCED:

9-cis-epoxycarotenoid dioxygenase

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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.).

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Correspondence to Wolfgang Frank.

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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)

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)

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)

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)

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)

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)

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)

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)

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)

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)

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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 (2010). https://doi.org/10.1007/s11103-009-9550-6

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Keywords

  • Salt tolerance
  • Transcription factors
  • NCED
  • Physcomitrella patens
  • Abscisic acid
  • Gene expression profiling