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Journal of Experimental Botany, Vol. 54, No. 386, pp. 1343-1350,
May 1, 2003
© 2003 Oxford University Press
The molecular characterization of PaHB2, a homeobox gene of the HD-GL2 family expressed during embryo development in Norway spruce
Received 2 October 2002; Accepted 23 January 2003
1 Swedish University of Agricultural Sciences, Department of Forest Genetics, Box 7027, S-750 07 Uppsala Sweden
2 Swedish University of Agricultural Sciences, Department of Plant Biology, Box 7080, S-750 07 Uppsala, Sweden
5 To whom correspondence should be addressed. Fax: +46 18 67 3279. E-mail: sara.von.arnold{at}sgen.slu.se
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Abstract |
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PaHB1 (for Picea abies Homeobox1), an evolutionarily conserved HD-GL2 homeobox gene, specifically expressed in the protoderm during somatic embryogenesis in the gymnosperm Norway spruce has been reported previously. An additional HD-GL2 gene designated PaHB2 is reported here. During somatic embryogenesis, the PaHB2 gene is uniformly ex pressed in proembryogenic masses and in early somatic embryos, but it is not detectably transcribed at the beginning of maturation. In mature embryos, PaHB2 expression was essentially detected in the outermost layer of the cortex and the root cap. A similar PaHB2 expression is detected post-embryonically in both the primary root and the hypocotyl. Phylogenetic reconstructions and intron pattern analyses revealed that the PAHB proteins fall within two distinct subclasses comprising highly similar angiosperm homologues. The PAHB1 subclass consists of protoderm/epiderm-specific members. By contrast, the PAHB2 subclass gathers homologues with a subepidermal and protodermal/epidermal activity. This study suggests that at least two distinct HD-GL2 genes with a layer-specific expression already existed in the last common ancestor of angiosperms and gymnosperms. The conserved protodermal/epidermal and subepidermal expression of HD-GL2 genes could be used to study embryo radial pattern formation across seed plants.
Key words: Embryogenesis, gymnosperm, HD-GL2, homeobox, Picea abies, radial pattern.
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Introduction |
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During embryo development in seed plants, the blueprint of the future adult plant is laid down. This basic body plan in angiosperms formally consists of a root/shoot axis of polarity from which embryonic organ systems generate and a radial organization of primary tissue layers: epidermis (derived from the protoderm), cortex and endodermis (derived from the ground tissue), pericycle and vascular tissues (derived from the procambium). Although gymnosperm embryo development generally starts with a free-nuclear stage, the mature embryo also features a similar general body plan: a radial pattern of primary tissues and two meristematic poles (Romberger et al., 1993; Singh, 1978).
Despite striking histological similarities between embryos of these two groups that diverged approximately 300 million years ago (Stewart and Rothwell, 1993), comparative molecular studies of embryo development between gymnosperms and angiosperms are rare. Consequently, the similarities in the developmental processes controlling embryo development in these two groups are unknown. Using the gymnosperm Norway spruce somatic embryogenesis as a model (Filonova et al., 2000), the aim was to characterize the developmental genes conserved across gymnosperms and angiosperms. This approach might unravel common developmental processes between the embryo of the gymnosperms and the angiosperms.
Homeobox genes encode homeodomain (HD) transcription regulators found in all kinds of eukaryotic organisms including yeast, animals and plants. The homeodomain proteins are typically involved in cell differentiation and patterning (Gehring et al., 1994; Chan et al., 1998; Kappen, 2000). The AtML1 (for Arabidopsis thaliana meristem L1 layer) gene (Lu et al., 1996; Sessions et al., 1999), related counterparts in maize ZmOCL (for Zea mays outer cell layer) (Ingram et al., 1999, 2000) and rice (ROC1) (Ito et al., 2002) are essentially protodermal/epidermal-specific in angiosperm embryos. They belong to the Homeodomain-Glabra2 (HD-GL2) plant-specific family (Lu et al., 1996) and their members are characterized by an amino-terminal homeodomain linked to a putative leucine zipper (HD-ZIP) followed by a sterol/lipid-binding START domain (Ponting and Aravind, 1999; Tsujishita and Hurley, 2000). The recently cloned Norway spruce homeobox gene PaHB1 (Picea abies Homeobox1) belongs to the HD-GL2 family (Ingouff et al., 2001). Similarly to its angiosperm homologues, PaHB1 expression switches from a ubiquitous expression to a protoderm-specific localization during somatic embryo development (Ingouff et al., 2001). The conserved protoderm-specific pattern of HD-GL2 genes among highly divergent plants raises the possibility of conserved function and similar developmental pathways during embryo development in seed plants. Recently another HD-GL2 gene, ANTHOCYANINLESS2 (ANL2) was isolated in Arabidopsis (Kubo et al., 1999). The anl2 mutant has an aberrant radial root patterning (Kubo et al., 1999). The anl2 roots produce extra cells called intervening cells, located between the cortical and epidermal layers. ANL2 might be involved in maintaining subepidermal-layer identity during plant development.
A new member of the HD-GL2 family from Norway spruce called PaHB2 is reported here. The PaHB2 gene structure and the corresponding predicted PAHB2 protein, are highly similar to those of the ANL2 gene. PaHB2 transcripts are uniformly expressed in early somatic embryos to become preferentially localized in the outer cortical layer and the root cap in mature embryos. A similar expression pattern is perpetuated post-embryonically in the primary root and the hypocotyl. Phylogenetic reconstructions and intron pattern analyses revealed that the PAHB proteins belong to two distinct subclasses with highly similar angiosperm homologues. The PAHB1 subclass gathers protoderm/epiderm-specific angiosperm members whereas the PAHB2 subclass is more heterogeneous and consists of homologues with a subepidermal or epidermal activity. This study suggests that at least two distinct HD-GL2 genes with a layer-specific expression already existed in the last common ancestor of angiosperms and gymnosperms.
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Materials and methods |
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Plant material
Embryogenic cell lines of Norway spruce (Picea abies (L.) Karst) were initiated from mature zygotic embryos and established as described by Egertsdotter and von Arnold (1993). The cell line 95:88:22 was stored in liquid nitrogen and then thawed 2 months before being used in these experiments. Embryogenic cultures were maintained under proliferation conditions and induced to mature according to Filonova et al. (2000).
Surface-sterilized seeds of Norway spruce were germinated in Magenta jars containing sterile vermiculite and water. The seedlings were grown at 22 °C under continuous light (200–300 µmol cm–2 s–1). After 6 weeks, each part of the seedlings (needles, hypocotyl, epicotyl, and root) was collected and frozen at –80 °C until use. Immature female and male strobili cones were harvested from a 40-year-old Norway spruce tree, 2 weeks prior to pollen release.
RNA extraction, cDNA synthesis
Total RNA was extracted according to Chang et al. (1993). Five micrograms of DNase I-treated total RNA were subjected to a reverse-transcription using SuperScript II (Gibco-BRL) and an adapter-dT17 primer (5'-GACTCGAGTCGACATCGAT17(G/A/C)-3') according to the manufacturer’s instructions. The absence of genomic DNA contamination in single-strand cDNA (ss-cDNA) samples was monitored by PCR (35 cycles: 94 °C/20 s, 55 °C/20 s, 72 °C/1 min) using P9 and P11 oligonucleotides. These two primers are specific for a p34cdc2 protein kinase from Norway spruce (cdc2Pa) and span two introns (Kvarnheden et al., 1995).
Cloning of PaHB2 cDNA
The PaHB2 cDNA was isolated using two previously described degenerate oligonucleotides d-HOX2 and d-HOX3 (Ingouff et al., 2001). The corresponding amino acids in the HD-GL2 homeodomain are HPDDEKQR and QVKFWFQ, respectively.
A 3'-RACE PCR reaction was carried out for 35 cycles (94 °C/20 s, 47 °C/20 s, 72 °C/1 min) using ss-cDNA from proliferating cultures and the oligonucleotides d-HOX2 and adapter (5'-GAC TCGAGTCGACATCGA-3'). One tenth of the first PCR reaction was then amplified with the nested d-HOX3 and the adapter oligonucleotides.
The amplification products were visualized by agarose gel blotting, probed with the full-length PaHB1 cDNA and washed at low stringency.
Two major signals were obtained in the d-HOX3-adapter PCR reaction: one at 2.1 kb and another at 2.5 kb. The two bands were purified from an agarose gel and cloned in pGEM-T-Easy vector (Promega) to be sequenced. The partial 2.1 kb-insert sequence was identical to PaHB1 whereas the partial 2.5 kb-insert sequence was similar but not identical to PaHB1. Specific primers derived from the sequenced 2.5 kb-fragment were used to carry out 5'-RACE-PCR according to Zhang and Frohman (1998).
The integrity of the PaHB2 sequence was checked by sequencing three independent PaHB2 PCR products with the dye-terminator PRISM ready reaction kit (Amersham-Pharmacia) and an ABI PRISM 377 automated sequencer (Applied Biosciences).
Analysis of exon/intron organization
Total genomic DNA was extracted according to Bernatzky and Tanksley (1986). Seventy nanograms of DNA were used as a substrate for the PCR reaction (94 °C/15 s, 59 °C/15 s, 68 °C/5 min, 35 cycles) with the oligonucleotides 5HS0 (5'-GAGGTATTAGGCTACAAGGGTTTG-3') and 3HR6 (5'-GAAGCTTCAGTTTCTGTCTGTC-3'). Alignments of sequences from the PCR-amplified genomic fragment with the full-length PaHB2 cDNA were carried out to determine the exon–intron boundaries.
Phylogenetic analysis
Amino acid sequences deduced from 20 HD-GL2 genes were aligned using CLUSTAL W (Thompson et al., 1994) and further refined manually (complete alignment available from the authors on request). The phylogenetic analyses were based on the amino acid region between the homeodomain and the carboxy-terminal end of the protein. Regions with gaps in the alignment were excluded from the analyses. Phylogenetic trees were constructed with Neighbor–Joining (NJ) and maximum parsimony (MP) methods. NJ analyses were carried out in MEGA2 (Kumar et al., 2000) by using the Poisson correction distance. The MP searches were conducted in PAUP version 4.0b (Swofford, 1999). Heuristic search strategies, consisting of ASIS addition sequences followed by TBR branch swapping, were performed. Nodal support was estimated using bootstrap analyses based on 1000 and 500 replicates in NJ and MP analyses respectively.
Expression pattern analysis by RT-PCR
One-tenth of each ss-cDNA sample was amplified by PCR (94 °C/15 s, 55 °C/15 s, 72 °C/1 min, 35 cycles) with the oligonucleotides 3HS7 (5'-CTGGCTTTGCCATTCTT-3') and 3HR6 (5'-GAAGC TTCAGTTTCTGTCTGTC-3') located in the 3'-untranslated region (UTR) of PaHB2. The PCR products were visualized by agarose gel blotting and probed with the full-length PaHB2 cDNA under stringent conditions.
In situ hybridization
The proembryogenic masses of proliferating cultures, maturing and mature somatic embryos placed, respectively, 1 week and 3 weeks on ABA, and germinated seeds were fixed for 5 h under vacuum in 4% paraformaldehyde, 5% acetic acid and 50% ethanol. The tissues were dehydrated through a graded series of ethanol (50–100% [v/v]) and embedded in Paraplast Plus (Sigma).
A 253 bp PCR fragment located in the 5'-UTR of PaHB2 was ligated into pGEM-T Easy (Promega). The sense and antisense riboprobes were labelled with digoxigenin using T7 and SP6 polymerases (DIG RNA Labeling Kit, Roche Biochemicals). The pre-hybridization, hybridization and washes were performed according to Langdale (1992) with the modifications described by Cantón et al. (1999).
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Results |
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Molecular cloning of PaHB2 cDNA
To identify additional HD-GL2 genes expressed during somatic embryogenesis in Norway spruce, two previously described degenerate oligonucleotides binding in the homeobox and RT-PCR were used (Ingouff et al., 2001). Two main PCR products of approximately 2100 bp and 2500 bp were amplified from Norway spruce proliferating embryogenic cell cDNA. The sequences obtained from the 2100 bp PCR product were identical to PaHB1. The sequenced 2500 bp PCR fragment was different from PaHB1 and designated PaHB2. Specific primers were designed and used to isolate the full-length PaHB2 cDNA by RACE experiments (Zhang and Frohman, 1998).
The longest PaHB2 cDNA was 3110 bp long (Genbank accession number AF328842 [GenBank] ), with a putative ORF of 2126 bp. The PaHB2 gene encodes a predicted protein of 708 amino acids, which is highly similar to HD-GL2 proteins. PAHB2 is 60% and 56% identical to the Arabidopsis proteins ANL2 and GL2-1, respectively, and 60% identical to OCL1 from maize. The N-terminal part of PAHB2 (amino acids 1–25) is shorter than in its close relatives. When this region is omitted in the sequence comparisons, PAHB2 shares 68% identity with ANL2 and 63% identity with GL2-1 and OCL1. PAHB2 shows 56% identity with PAHB1 (62% with the N-terminal region excluded).
The PAHB2 protein presents a typical HD-GL2 protein domain organization: an N-terminal homeodomain linked to a non-canonical leucine zipper domain, and a putative StAR-related lipid transfer (START) domain. The N-terminal end of PAHB2 comprises a short stretch rich in aspartate and glycine, which is reminiscent of the N-terminal regions of HD-GL2 proteins.
The longest 5'- and 3'-untranslated regions (UTR) of PaHB2 examined are 397 bp and 587 bp, respectively. A BLAST search in the UTR database (Pesole et al., 2000) with the 5'-UTR of PaHB2 showed no significant sequence similarity. A similar sequence analysis of 3'-UTR revealed a highly conserved 17-nt long motif in the PaHB2 gene and close homologues (ANL2, OCL1, OCL2, OCL3). This motif was also present in PaHB1 and most of the angiosperm HD-GL2 genes used in this study (Table 1). It is noteworthy that this motif was not detected in FWA, GL2 and PDF2 from Arabidopsis, HAHR1 from sunflower and GhGL2 from cotton.
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PaHB2 encodes a HD-GL2 protein homologous to ANL2
To visualize the evolutionary relationships between members of the HD-GL2 family, an unrooted phylogenetic tree was generated by the Neighbor–Joining distance method, presented in Fig. 1A, using an amino acid alignment comprising the HD-ZIP motif, the START domain and the downstream region of the protein until the carboxy-terminal end. The phylogenetic analysis revealed that the HD-GL2 family consists of at least three distinct subgroups comprising proteins from monocot and dicot plants. In the maximum parsimony analysis, the general tree topology was unchanged but the defined subgroups were supported with lower bootstrap values (data not shown).
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The gymnosperm protein PAHB1 belongs to the highly supported subclass including ATML1, PDF2, GL2-2, GL2-3, ZMOCL5, and O39. However, the spruce protein PAHB2 together with these angiosperm proteins, ANL2 and GL2-1 from Arabidopsis and OCL1, OCL2 and OCL3 from maize represent a second subclass. The third subclass only consists of angiosperm proteins: GL2, GL2-4 and GL2-5 from Arabidopsis, OCL4 from maize, HAHR1 from sunflower, and GHGL2 from cotton.
The HD-GL2 genes present a very similar overall exon–intron organization with nine possible conserved intron positions numbered from 1 to 9 (Tavares et al., 2000; Ingouff et al., 2001). The intron positions 1, 2, 4, 5, 7, and 9 are found in all the members whereas intron positions 3, 6 and 8 can be present/absent in different combinations. Figure 1B shows the position of these introns (when available) in relation to the deduced amino acid sequence of the gene. It has previously been shown that the phylogenetic classification of HD-GL2 proteins is supported by the exon–intron structures of the corresponding genes (Ingouff et al., 2001). For example, in the PaHB1 subclass the corresponding genes all feature the intron positions from 1 to 9, except for AtML1, which lacks position 3.
The PaHB2 exon–intron boundaries are located at positions 1, 2, 3, 4, 5, 6, 7, and 9 (Fig. 1B). It is noteworthy that the genes belonging to the PaHB2 subclass (ANL2, FWA, GL2-1, and OCL1) closely resemble PaHB2 gene structure except for intron position 3 that seems to have been lost in genes of all subclasses (for example AtML1, ANL2 and GL2) (Fig. 1A, B). Even if PaHB2 features a unique intron position (position 3) among this subclass, a specific intron pattern can be defined for the PaHB2 subclass, presence of position 1, 2, 4, 5, 6, 7, and 9 and absence of position 8. In the third subclass, the exon–intron boundaries (see GL2, GL2-4 and GL2-5) correspond to a unique combination in the HD-GL2 family. They are characterized by the presence of the positions 1, 2, 4, 5, 7, 8, and 9 and the absence of the intron position 6.
The phylogenetic relationships between HD-GL2 proteins are supported by the intron-exon structures of the corresponding genes.
Expression pattern of PaHB2
Expression of PaHB2 in different organs and in embryogenic cultures was analysed by RT-PCR (Fig. 2) using PaHB2 specific oligonucleotides. An amplification product was obtained in all analysed parts of the seedling (needles, epicotyl, hypocotyl, and root), in reproductive organs (immature male and female strobili) and during somatic embryogenesis in proliferating cells and in mature embryos (Fig. 2).
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The spatial expression pattern of PaHB2 was further investigated by RNA in situ hybridization during somatic embryogenesis (Fig. 3) and in the primary root (Fig. 4). Control experiments with the DIG-labelled PaHB2 sense riboprobe were performed on sections of tissues from proliferating embryogenic cultures consisting of proembryogenic masses and early somatic embryos (data not shown) and maturing somatic embryos (Figs 3D, F, I, K, 4B) and confirmed that hybridization of the antisense probe was specific (Figs 3A, C, E, H, J, 4A). In proembryogenic masses of proliferating embryogenic cultures, PaHB2 transcripts were detected in all embryonic cells (data not shown). In early somatic embryos which still do not feature any sign of tissue differentiation, PaHB2 was mainly expressed in the embryonal mass and in the embryonal tube cells that are derived from periclinal cell divisions of the embryonal mass (Fig. 3A). These results suggest that PaHB2 is expressed in the apical region of the somatic embryo during early somatic embryo development. However, since the vacuolated cells are damaged during the sample preparation, it cannot be excluded that PaHB2 is expressed in suspensor cells.
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At the beginning of late embryogeny, a distinct protoderm is defined and a root meristem is visible at the proximal part of the embryo (Fig. 3B). At this stage, in situ hybridization experiments showed no hybridization signal specific to PaHB2 transcripts in any tissue of the maturing embryo after 1 week on ABA (compare Fig. 3C, D, E, F) suggesting that PaHB2 was not expressed. Figure 3G shows a mature somatic embryo after 3 weeks on ABA where all the primary tissues are defined (protoderm, cortex, vascular tissues) and the cotyledons have expanded. In sections hybridized with the antisense riboprobe a specific signal was detected in the outermost layer of the embryonal cortex (Fig. 3H). The PaHB2 transcripts were also detected in the root cap (Fig. 3J). Expression was neither detected in the cotyledons and in the shoot apical meristem (data not shown).
After germination, the PaHB2 gene is expressed in the cortex of the root and the hypocotyl, and in the root cap (Fig. 4A). No PaHB2 mRNA was detected in the vascular tissue. PaHB2 transcripts were also clearly excluded from the root meristem (Fig. 4A). Control experiments on comparable sections with the sense probe did not show any signals (Fig. 4B).
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Discussion |
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PaHB2 is a member of the HD-GL2 family
A highly conserved gymnosperm HD-GL2 gene PaHB1 has recently been characterized using degenerate oligonucleotides (Ingouff et al., 2001). In this work, an additional gene PaHB2 coding for a typical predicted HD-GL2 protein is described. PAHB2 has an N-terminal homeodomain linked to a truncated leucine zipper (a dimerization domain) followed by the START domain (a predicted lipid/sterol binding domain). PAHB2 shares consistent sequence identity with the HD-GL2 proteins downstream of the START domain. However, this C-terminal end of the HD-GL2 protein does not match any known functional domain.
A highly conserved 17 nt-long motif is present in the 3'-UTR of the two gymnosperm and most of the angiosperm HD-GL2 genes used in this study (Table 1). This motif was not detected in genes outside the plant-specific HD-GL2 family. Homeobox genes expressed during embryogenesis in metazoans sometimes feature regulatory elements located in their 3'-UTR that influence mRNA subcellular localization (Bashirullah et al., 1998), mRNA translation (Dubnau and Struhl, 1996; Rivera-Pomar et al., 1996) and mRNA stability (Fontes et al., 1999). Further molecular analyses are required to test if this motif has any regulatory function.
Cell-specific expression of PaHB2 during embryo development and post-embryonic growth
Unlike the case for model angiosperm plants (Arabidopsis and maize), the relationships between the initial cells and the primary tissues are not clearly established in gymnosperm embryos. However, the PaHB2 transcripts are detected before any signs of tissue differentiation in the young embryo, but it is not detectably transcribed at the beginning of the maturation when cortex specification is thought to take place (Romberger et al., 1993; Filonova et al., 2000). Later PaHB2 expression becomes restricted to the outer cortex cell layer and the root cap in the mature embryo. Therefore, it is at present unclear if PAHB2 is involved in the specification and/or maintenance of the cortex identity.
After germination PaHB2 specific expression pattern is maintained in the cortex of both roots and hypocotyls and in the root cap, demonstrating that the mechanism responsible for the post-embryonic expression of PaHB2 is already in place during embryo maturation.
Correlation between structure and function of PaHB genes and angiosperm homologues
Despite a high degree of similarity, the two-gymnosperm PAHB proteins, PAHB1 (Ingouff et al., 2001) and PAHB2 (this report), fall within two distinct monophyletic subclasses. These observed phylogenetic relationships were further supported by comparative analyses of HD-GL2 gene structure. The fact that each PAHB protein is phylogenetically more closely related to angiosperm counterparts than to the other spruce protein suggests that at least two ancestor proteins belonging to two distinct subgroups were already present before angiosperms and gymnosperms separated, about 300 million years ago (Stewart and Rothwell, 1993).
By contrast to PAHB1, which groups with members from dicot and monocot plants having an outer cell layer-specific activity, PAHB2 clearly belongs to the well-supported subgroup comprising two Arabidopsis proteins (ANL2, GL2-1) and three maize proteins (OCL1, OCL2 and OCL3). The anl2 mutant is affected in the radial pattern of the primary root; roots produce intervening cells, located between the cortical and epidermal layers (Kubo et al., 1999). Thus ANL2 activity is probably taking place in the subepidermal layers of the roots. The spruce PaHB2 gene exhibits a spatial expression localized in the cortical layers of both the primary root and the hypocotyl and in the root cap. Similarly to ANL2 and PaHB2, a subepidermal expression was described for OCL2 in the meristem (Ingram et al., 2000). The other two maize genes have an expression restricted to the protoderm layer (OCL1) and to the suspensor of the embryo (OCL3) (Ingram et al., 1999, 2000). Although the PAHB2 subclass includes genes with distinct tissue-specific expression, these data show that the PAHB2 subclass comprises members which have a subepidermal activity in both angiosperms and gymnosperms.
During plant embryogenesis, the first histologically detectable tissue is the protoderm. Subsequent steps of radial patterning are confined to the inner cells where the ground and conductive tissues will be defined. Both PaHB genes switch from a uniform expression in early somatic embryos to a distinct tissue-specific expression in nearby cells at different stages of embryo maturation. The protoderm-specific expression of PaHB1 clearly precedes the outer cortex-specific expression of PaHB2. At present it is not known if this differential layer-specific expression of HD-GL2 genes in gymnosperms is mimicked by the corresponding PaHB homologues in angiosperm embryos.
The protoderm/epiderm-specific and the subepiderm-specific pattern of HD-GL2 genes are present among HD-GL2 genes of highly divergent seed plants. The HD-GL2 genes could therefore be used as molecular markers to study radial pattern formation across seed plants.
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Acknowledgements |
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We thank Ulf Lagercrantz for helping with the phylogenetic analyses and critical reading of the manuscript and Lada Filonova and Peter Bozhkov for providing the histological sections. This work was supported by the Swedish Council for Agricultural and Forestry Research (MI), the Swedish International Development Cooperation Agency (MW) and a Marie Curie post-doctoral fellowship (IF).
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bashirullah A, Cooperstock RL, Lipshitz HD. 1998. RNA localization in development. Annual Review of Biochemistry 67, 335–394.[CrossRef][Web of Science][Medline]
Bernatzky R, Tanksley SD. 1986. Genetics of actin-related sequences in tomato. Theoretical and Applied Genetics 73, 314–321.[CrossRef]
Cantón FR, Suàrez MF, Josè-Estanyol M, Cánovas FM. 1999. Expression analysis of a cytosolic glutamine synthetase gene in cotyledons of Scots pine seedlings: developmental, light regulation and spatial distribution of specific transcripts. Plant Molecular Biology 40, 623–634.[CrossRef][Web of Science][Medline]
Chan RL, Gago GM, Palena CM, Gonzalez DH. 1998. Homeoboxes in plant development. Biochimica et Biophysica Acta 1442, 1–19.[Medline]
Chang S, Puryear J, Cairney J. 1993. A simple and efficient method for isolating RNA from pine tree. Plant Molecular Biology Reporter 11, 114–117.
Dubnau J, Struhl G. 1996. RNA recognition and translational regulation by a homeodomain protein. Nature 379, 694–699.[CrossRef][Medline]
Egertsdotter U, von Arnold S. 1993. Classification of embryogenic cell lines of Picea abies as regards protoplast isolation and culture. Journal of Plant Physiology 141, 222–229.
Filonova LH, Bozhkov PV, von Arnold S. 2000. Developmental pathway of somatic embryogenesis in Picea abies as revealed by time-lapse tracking. Journal of Experimental Botany 51, 249–264.
Fontes AM, Ito J, Jacob-Lorena M. 1999. Control of messenger RNA stability during development. Current Topics in Developmental Biology 44, 171–202.[Web of Science][Medline]
Gehring WJ, Affolter M, Bürglin T. 1994. Homeodomain proteins. Annual Review of Biochemistry 63, 487–526.[CrossRef][Web of Science][Medline]
Ingouff M, Farbos I, Lagercrantz U, von Arnold S. 2001. PaHB1 is an evolutionary conserved HD-GL2 homeobox gene expressed in the protoderm during Norway spruce embryo development. Genesis 30, 220–230.[CrossRef][Web of Science][Medline]
Ingram GC, Magnard JL, Vergne P, Dumas C, Rogowsky PM. 1999. ZmOCL1, an HDGL2 family homeobox gene, is expressed in the outer cell layer throughout maize development. Plant Molecular Biology 40, 343–354.[CrossRef][Web of Science][Medline]
Ingram GC, Boisnard-Lorig C, Dumas C, Rogowsky PM. 2000. Expression patterns of genes encoding HD-ZipIV homeodomain proteins define specific domains in maize embryos and meristems. The Plant Journal 22, 401–414.[CrossRef][Web of Science][Medline]
Ito M, Sentoku N, Nishimura A, Hong SK, Sato Y, Matsuoka M. 2002. Position dependent expression of GL2-type homeobox gene, Roc1: significance for protoderm differentiation and radial pattern formation in early rice embryogenesis. The Plant Journal 29, 497–507.[CrossRef][Web of Science][Medline]
Kappen C. 2000. Analysis of a complete homeobox repertoire: implications for the evolution of diversity. Proceedings of the National Academy of Sciences, USA 97, 4481–4486.
Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M. 1999. ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. The Plant Cell 11, 1217–1226.
Kumar S, Tamura K, Jakobsen I, Nei M. 2000. MEGA: Molecular evolutionary genetics analysis, version 2. softwares for microcomputers.
Kvarnheden A, Tandre K, Engström P. 1995. A cdc2 homologue and closely related processed retropseudogenes from Norway spruce. Plant Molecular Biology 27, 391–403.[CrossRef][Web of Science][Medline]
Langdale JA. 1992. In situ hybridization. In: Freeling M, Walbot V, ed. The maize handbook. Berlin: Springer-Verlag, 165–180.
Lu P, Porat R, Nadeau JA, O’Neill SD. 1996. Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. The Plant Cell 8, 2155–2168.[Abstract]
Pesole G, Liuni S, Grillo G, Licciulli F, Larizza A, Makalowski W, Saccone C. 2000. UTRdb and UTRsite: specialized database of sequences and functional elements of 5' and 3' untranslated regions of eukaryotic mRNAs. Nucleic Acids Research 28, 193–196.
Ponting CP, Aravind L. 1999. START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends in Biochemical Sciences 24, 130–132.[CrossRef][Web of Science][Medline]
Rivera-Pomar R, Niessing D, Schmidt-Ott U, Gehring WJ, Jäckle H. 1996. RNA binding and translational suppression by bicoid. Nature 379, 746–749.[CrossRef][Medline]
Romberger JA, Hejnowicz Z, Hill JF. 1993. Plant structure: function and development. Berlin: Springer-Verlag.
Sessions A, Weigel D, Yanovsky MF. 1999. The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. The Plant Journal 20, 259–263[CrossRef][Web of Science][Medline]
Singh H. 1978. Embryology of gymnosperms. In: Zimmerman W, Carlquist Z, Ozenda P, Wulff HD, eds. Handbuch der Pflanzenanatomie. Berlin, Stuttgart: Gebrüder Borntraeger, 187–241.
Stewart WN, Rothwell GW. 1993. Paleobotany and the evolution of plants. Cambridge: Cambridge University Press.
Swofford DL. 1999. PAUP: phylogenetic analysis using parsimony, version 4.0b2. Sunderland: Sinauer Associates, Inc Publishers.
Tavares R, Aubourg S, Lecharny A, Kreis M. 2000. Organization and structural evolution of four multigene families in Arabidopsis thaliana: AtLCAD, AtLGT, AtMYST, and AtHD-GL2. Plant Molecular Biology 42, 703–717.[CrossRef][Web of Science][Medline]
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
Tsujishita Y, Hurley JH. 2000. Structure and lipid transport mechanism of a StAR-related domain. Nature Structural Biology 7, 408–414.[CrossRef][Web of Science][Medline]
Zhang Y, Frohman MA. 1998. Using Rapid Amplification of cDNAs Ends (RACE) to obtain full-length cDNAs. In: Cowell IG, Austin CA, eds. cDNA library protocols, Vol. 69. Totowa: Humana Press Inc., 61–88.
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  M. Nakamura, H. Katsumata, M. Abe, N. Yabe, Y. Komeda, K. T. Yamamoto, and T. Takahashi Characterization of the Class IV Homeodomain-Leucine Zipper Gene Family in Arabidopsis Plant Physiology, August 1, 2006; 141(4): 1363 - 1375. [Abstract] [Full Text] [PDF]
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 C. Guillet-Claude, N. Isabel, B. Pelgas, and J. Bousquet The Evolutionary Implications of knox-I Gene Duplications in Conifers: Correlated Evidence from Phylogeny, Gene Mapping, and Analysis of Functional Divergence Mol. Biol. Evol., December 1, 2004; 21(12): 2232 - 2245. [Abstract] [Full Text] [PDF]
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