*National Institute for Basic Biology, Okazaki, Japan;
Department of Molecular Biomechanics, Graduate University for Advanced Studies, Okazaki, Japan; and
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo, Japan
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Abstract |
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Introduction |
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Many homeobox genes have been isolated from vascular plants. They are classified into seven groups based on their amino acid sequence similarities: KNOX, BELL, ZM-HOX, HAT1, HAT2, ATHB8, and GL2 (Bharathan et al. 1997
). The KNOX and BELL genes belong to the TALE homeobox genes, while the other genes belong to the typical homeobox genes (Bharathan et al. 1997
; Chan et al. 1998
). The HAT1, HAT2, ATHB8, and GL2 genes are characterized by the leucine zipper motif (Landschulz, Johnson, and McKnight 1988
) adjacent to the C-terminus of the homeodomain and have been renamed the HD-Zip I, HD-Zip II, HD-Zip III, and HD-Zip IV subfamilies, respectively (Meijer et al. 1997
; Aso et al. 1999
).
The functions of the HD-Zip genes are diverse among the different subfamilies, and even within the same subfamily (Chan et al. 1998
). HD-Zip I and II genes are likely involved in signal transduction networks of light (Carabelli et al. 1993, 1996
; Schena, Lloyd, and Davis 1993
; Aoyama et al. 1995
; Steindler et al. 1997, 1999
), dehydration-induced ABA (Söderman, Mattsson, and Engström 1996
; Frank et al. 1998
; Lee and Chun 1998
; Söderman et al. 1999
), or auxin (Kawahara, Komamine, and Fukuda 1995
). These signal transduction networks are related to the general growth regulation of plants. The overexpression of sense or antisense HD-Zip I or II mRNA usually alters growth rate and development (Schena, Lloyd, and Davis 1993
; Aoyama et al. 1995
; Meijer et al. 1997
). Most members of the HD-Zip III subfamily play roles in cell differentiation in the stele (Baima et al. 1995
; Zhong and Ye 1999
), although the functions of some genes remain unknown (Sessa et al. 1998
; Aso et al. 1999
). HD-Zip IV genes are related to the differentiation of the outermost cell layer (Rerie, Feldmann, and Marks 1994
; Cristina et al. 1996
; Lu et al. 1996
; Masucci and Schiefelbein 1996
; Ingram et al. 1999
; Kubo et al. 1999
).
HD-Zip genes have been reported only from vascular plants (Bharathan et al. 1997
; Aso et al. 1999
) and are not found in the entire genome of either the metazoan Caenorhabditis elegans or the fungus Saccharomyces cerevisiae. Since genes with either a leucine zipper motif or a homeodomain have been reported in metazoa, fungi, and green plants, Schena and Davis (1992)
speculated that the HD-Zip genes originated in the green plant lineage by exon shuffling between a gene encoding a homeodomain and another gene encoding a leucine zipper motif. Although there have been a large number of studies of angiosperm HD-Zip genes, little is known about these genes in other green plants, and the origin of the HD-Zip genes is not yet well understood. Aso et al. (1999)
reported HD-Zip I, II, and III genes from the fern Ceratopteris richardii and indicated that the four HD-Zip subfamilies had already diverged before the divergence between the angiosperm and fern lineages, approximately 400 MYA (Stewart and Rothwell 1993
, p. 510). In addition to these studies, analyses of HD-Zip genes in other land plants and green algae are necessary to further understand the evolution of the HD-Zip gene family.
Physcomitrella patens is a moss. Mosses diverged from the vascular plant lineage approximately 430 MYA (Stewart and Rothwell 1993
, p. 510). Unlike vascular plants, the haploid gametophyte generation is dominant in mosses. Dominance of the haploid generation is also conspicuous in the charophyceaen algae, the green algae most closely related to the land plants (Graham and Wilcox 2000
, p. 499). The body plans and life histories of mosses and vascular plants differ extensively. For example, unlike vascular plants, mosses form simple leaf- and stem-like organs in their gametophyte generation (Hébant 1977
; Bold, Alexopoulos, and Delevoryas 1987
, pp. 270276, 314334; Reski 1998
). We chose to study P. patens because it is well developed as a model organism (Cove, Knight, and Lamparter 1997
; Reski 1998
), and this will enable further studies on gene function.
In this study, we isolated 10 HD-Zip genes from P. patens and included these in a phylogenetic analysis with previously reported HD-Zip genes isolated from vascular plants. We used the gene tree to determine the phylogenetic relationships of the HD-Zip genes and whether four HD-Zip subfamilies were present in the last common ancestor of the mosses and vascular plants. The difference in evolutionary rates between the HD- Zip I and II subfamilies is reported, and the reason is discussed.
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Materials and Methods |
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Cloning the HD-Zip Genes
Using ISOGEN (Nippon Gene, Tokyo, Japan), total RNA was extracted from the wild-type protonemata 1 week after inoculation and from gametophores grown for 1 month after inoculation of protonemata onto G medium. Complementary DNA was synthesized from the total RNA using the 3' RACE system (Life Technologies, Inc., Rockville, Md.). PCR amplifications were performed according to Aso et al. (1999)
using a homeodomain-specific primer, HB1 (Bürglin et al. 1989
) or HD1 (Aso et al. 1999
). The PCR products were separated on 1% (w/v) agarose gels (SeaKem GTG, FMC BioProducts, Rockland, Maine). The DNA fragments between 0.5 and 2 kb were purified with the GeneClean III kit (BIO 101 Inc., La Jolla, Calif.), and cloned using the CLONEAMP pAMP1 system (Life Technologies, Inc.). In all, 326 clones were obtained using HB1 (96 from the protonema cDNA and 230 from the gametophore cDNA), and 84 clones were obtained using HD1 (30 from the protonema cDNA and 54 from the gametophore cDNA). These candidate clones were sorted into 58 groups according to their digestion patterns using AluI, and then two or three clones from each group were sequenced with the Dye Terminator Cycle Sequencing FS Ready Reaction Kit (Perkin-Elmer Applied Biosystems, Foster City, Calif.) or the Big Dye Terminator Cycle Sequencing FS Ready Reaction Kit (Perkin-Elmer Applied Biosystems) using an ABI PRISM 377 DNA sequencer (Perkin-Elmer Applied Biosystems). The 5' region of each gene encoding a homeodomain was cloned using the 5' RACE system (Life Technologies, Inc.) and sequenced. The nucleotide sequences of the gene-specific primers are deposited in the DNA database, with the sequence of each gene as additional information. Total genomic DNA was extracted from the wild-type protonemata 1 week after inoculation using PHYTOPURE (Amersham Pharmacia Biotech, Uppsala, Sweden) and further purified using the CTAB method (Murray and Thompson 1980
).
Two gene-specific primers located close to each end of the putative mRNA were synthesized. Nested PCR amplifications were performed with the cDNA or genomic DNA using these primers to obtain cDNA and genomic DNA clones. The PCR product was cloned into pBluescriptII SK+ (Stratagene, La Jolla, Calif.) or pGEM3z (Promega, Madison, Wis.). To exclude PCR errors, at least two clones obtained from independent PCR were sequenced for each gene. When discrepancies were found, the majority from at least three independently amplified PCR products was selected.
Phylogenetic Analysis
Plant HD-Zip genes similar to P. patens HD-Zip genes were obtained from the nr and dbest data sets at NCBI using the programs blastx or tblastn (version 2.0.10) (Altschul et al. 1997
). Genes containing undetermined amino acid residues within the HD-Zip domain were not used for further analysis. Nucleotide sequences were translated to amino acid sequences based on the universal code. Genes with identical amino acid sequences in the region used for the analysis were treated as a single operational taxonomic unit. The deduced amino acid sequences of 96 HD-Zip genes used in this study were aligned using CLUSTAL W, version 1.8 (Thompson, Higgins, and Gibson 1994
), and then revised manually. Eighty-four amino acid sites without indels were used for the phylogenetic analysis.
To search for the maximum-likelihood (ML) tree, we used neighbor-joining (NJ) and most-parsimonious (MP) trees as start trees for a local rearrangement search (Adachi and Hasegawa 1996
). NJdist and ProtML programs were in the MOLPHY, version 2.3b3, package (Adachi and Hasegawa 1996
). An NJ tree (Saitou and Nei 1987
) was obtained with NJdist based on the ML distance under the JTT model (Jones, Taylor, and Thornton 1992
) calculated with ProtML. MP trees were obtained by heuristic searches with tree bisection-reconnection (TBR) using PAUP*, version 4.0 b4a (Swofford 2000). Three kinds of heuristic search were performed: (1) a heuristic search from a simple addition sequence without the steepest-descent option, (2) 84 searches from a random tree without the steepest-descent option, and (3) 10 searches from a random tree with the steepest-descent option. These analyses found 205,787 trees with 1,330 steps. The likelihoods of all these trees were calculated using ProtML under the JTT model, and the trees were sorted according to their Akaike information criterion (AIC) values (Adachi and Hasegawa 1996
). The best 1,000 trees were subjected to further local rearrangement searches (Adachi and Hasegawa 1996
). Further phylogenetic analyses constraining a monophyletic relationship of HD-Zip I genes were performed. The approximate likelihood (Adachi and Hasegawa 1996
) of all of the 6,081,075 trees obtained under this constraint was calculated. For the best 10,000 trees, log likelihood was calculated. An ML tree found in this search was further subjected to a local rearrangement search.
The local bootstrap probability of each branch was estimated by using the resampling-of-estimated-log-likelihood (RELL) method (Kishino, Miyata, and Hasegawa 1990
; Hasegawa and Kishino 1994
).
Difference in Evolutionary Rates Between the HD-Zip I and the HD-Zip II Subfamilies
We examined whether the evolutionary rate in the HD-Zip I subfamily was higher than that of the HD-Zip II subfamily. Rate is the distance divided by the divergence time. If we focus on ortholog pairs of two defined species, the divergence time is a constant, and the rate can be compared by comparing the distance. Every pair of species that has ortholog pairs in both the HD-Zip I and the HD-Zip II subfamilies was used. The ortholog pairs were determined according to tree topology and species phylogeny. For each pair (i), the evolutionary distance (di) was calculated with ProtML under a JTT model using the -D option. The distance (di, dj) of two pairs (i, j), one from the HD-Zip I subfamily and the other from the HD-Zip II subfamily, were compared. To test whether the distance was different between pairs i and j, i.e., di > dj, the difference di - dj (Dij) was tested against 0. Dij was calculated for each set of amino acid data resampled in a bootstrap test, and standard deviations were calculated from 10,000 bootstrap samples.
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Results |
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Pphb4 clusters in the HD-Zip II subfamily, whose monophyly is supported with high local bootstrap probability (91%). Pphb3 is sister to the HD-Zip II subfamily with 87% local bootstrap support. Pphb10 clusters in the HD-Zip III subfamily, whose monophyly has 99% local bootstrap support. No gene that clusters with the HD- Zip IV subfamily was found in this study.
Difference in Evolutionary Rates Between the HD-Zip I and the HD-Zip II Subfamilies
Six species pairs had ortholog pairs in both the HD- Zip I and the HD-Zip II subfamilies. The compared ortholog pairs and the result of comparisons are shown in tables 1,
2,
3,
4,
5,
and 6 . In comparisons of distances between ortholog pairs of a eudicot (Arabidopsis, Glycine, or Lycopersicon) and a monocot (Oryza), every HD-Zip I ortholog pair had a longer distance than any HD-Zip II ortholog pair. In most comparisons, >95% of differences in the bootstrap samples were positive, and the minimum bootstrap proportion was 79%. On the other hand, some comparisons of species pairs between eudicots were negative but not significantly different from 0.
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In the angiosperm HD-Zip I genes, the a1 and d1 sites are mainly occupied by threonine and leucine, respectively. In the fern HD-Zip I genes, the a1 site is occupied by asparagine instead of threonine, and the d1 site is variable and occupied by leucine, valine, or isoleucine (Aso et al. 1999
). The a1 sites of the Pphb genes in the HD-Zip I subfamily are all threonine, except for Pphb9, which has isoleucine. Leucine residues occupy the d1 sites as observed in angiosperm HD-Zip I genes.
The a1 and d1 sites of HD-Zip II genes are fixed with leucine and threonine, respectively. As in the angiosperms, the a1 and d1 sites of Pphb4 are leucine and threonine, respectively. The a1 and d1 sites of Pphb3 are alanine and asparagine, respectively, unlike any other HD-Zip genes.
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Discussion |
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The fact that the mosses have HD-Zip I and II genes is not surprising, because their roles in angiosperms (e.g., light, ABA, and auxin signal transduction networks) are likely general to all plants, including mosses. A phytochrome gene which encodes a photosensor pigment of plants has been cloned in P. patens (Kolukisaoglu et al. 1993
), and some phototropic responses that should be caused by the light signal transduction network have also been reported in mosses (Russell et al. 1998
). The desiccation stress response networks mediated by ABA, which involve angiosperm HD-Zip I or II genes, are likely conserved between P. patens and angiosperms (Knight et al. 1995
). Auxin is an important developmental regulator in both angiosperms and mosses (reviewed in Cove 1992
), although its roles in development are different in the two because of their developmental and morphological differences. It is unclear whether these plants use similar cascades for light-, ABA-, and auxin-mediated networks, and further characterization of P. patens HD-Zip I and II gene functions and comparison with angiosperm HD-Zip genes are necessary.
Most angiosperm HD-Zip III genes are involved in the differentiation of vascular tissue (Baima et al. 1995
; Zhong and Ye 1999
). Some mosses, including P. patens, have water-conducting hydroids and nutrient-conducting leptoids in the gametophyte similar to the tracheids and sieve elements of vascular plants, respectively (Bell 1992
, pp.118120). However, the homologies of these cells are ambiguous, because in vascular plants, tracheids and sieve elements are formed in the sporophyte generation. Furthermore, the cell wall thickening common to tracheids does not occur in hydroids, although the leptoids are similar to sieve elements at the ultrastructural level (Schofield and Hébant 1984
). Determining the function of Pphb10, the moss HD-Zip III gene, may give insights into the evolution of vascular tissue in land plants.
Differences in Evolutionary Rates Between the HD- Zip I and the HD-Zip II Subfamilies
The amino acid residues in the homeodomain and the leucine zipper motif of the HD-Zip I subfamily appear less conserved than those of the HD-Zip II subfamily in the alignment (fig. 2
). Chan et al. (1998)
pointed out the possibility that the evolutionary rate was higher in the former subfamily than in the latter. Comparison of the evolutionary distances for the ortholog pairs of eudicots and rice indicated that HD-Zip I genes evolved faster than HD-Zip II genes after the split of eudicots and monocots (tables 13
). Within eudicots, the differences are not clear, perhaps because the difference has not accumulated enough to be significant (table 46
). Some metazoan homeobox genes have been reported to function as a complex with other cofactors that regulate the homeobox gene (Mann and Chan 1996
; Bürglin 1998
; González-Crespo et al. 1998
; Mann and Affolter 1998
). The leucine zipper motif also plays a role in protein-protein interaction (O'Shea, Rutkowski, and Kim 1989
). HD-Zip II genes may evolve slowly because HD- Zip II genes interact with cofactors that regulate the function of HD-Zip II genes strictly, while HD-Zip I genes may evolve faster because these genes do not interact strictly with cofactors and have relaxed specificity. In animals, helix 3 of the homeodomain is essential for DNA recognition (Kissinger et al. 1990
), while helices 1 and 2 are involved in less stringent interactions with other proteins (Chan et al. 1994
; Zappavigna, Sartori, and Mavilio 1994
; Grueneberg et al. 1995
). Figure 2
shows that the amino acid residues of helix 3 of HD- Zip I and II genes are highly conserved throughout HD- Zip I and II genes, while helices 1 and 2 of HD-Zip I genes have more variety than those of HD-Zip II genes. This suggests that a difference in the protein-protein interactions of the HD-Zip I and II subfamilies may be one of the reasons for the difference in their respective evolutionary rates.
Some HD-Zip genes are reported to dimerize via the leucine zipper motif and bind DNA in vitro (Sessa, Morelli, and Ruberti 1993
; Gonzalez et al. 1997
; Sessa et al. 1998
). The a1 and d1 sites of the leucine zipper motif are important for determining the dimerization partner (Gonzalez et al. 1997
). Amino acids in the a1 and d1 sites of HD-Zip I genes vary, while those of HD- Zip II genes are always leucine and threonine, respectively. Given that the amino acids of HD-Zip II genes are highly conserved, these genes likely select their dimerization partner more strictly than do HD-Zip I genes, perhaps to maintain specificity of pairing. Further studies on the protein-protein interactions of HD-Zip genes are required to test this hypothesis. The functions of those genes that have not been well characterized must also be studied, especially in additional nonvascular plants. Physcomitrella patens may be an ideal model with which to analyze gene functions, since it is amenable to transgenic methods (Cove, Knight, and Lamparter 1997
; Schaefer and Zrÿd 1997
). Such studies will help to elucidate the evolution of HD-Zip genes in land plants.
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Acknowledgements |
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Footnotes |
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1 Keywords: Physcomitrella
moss
homeobox
leucine zipper
molecular evolution
gene family
2 Address for correspondence and reprints: Mitsuyasu Hasebe, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji-cho, Okazaki 444-8585, Japan. mhasebe{at}nibb.ac.jp
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