Evolution of developmental genes
From Purdue Genomics Database Facility
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Contents |
Evolution of developmental genes in land plants
M. Hasebe, T. Nishiyama et al.
(mhasebe@nibb.ac.jp)
A comparison of eumetazoan genomes revealed that their common ancestor had complex sets of genes similar to those used in extant bilateral metazoan development (Carroll et al., 2005; Putnam et al., 2007). In contrast, the evolution of developmental genes in another major lineage of multicellular land organisms, the land plants, has remained a mystery due to a lack of genomic data for non-flowering plants. By incorporating the accumulated genomic sequence data for the lycopod Selaginella moellendorffii and the moss Physcomitrella patens, we analysed the phylogenetic relationships of homologues of 826 Arabidopsis thaliana genes that function in development and identified putative orthologues to each gene. Here we show that S. moellendorffii and P. patens retain 88% and 86% of putative orthologues, respectively, including those involved in flowering plant specific development. Eighty-one percent of putative orthologues was shared in all the land plants. However, we also found flowering plant and vascular plant specific putative orthologues. Furthermore, lineage-specific expansions and contractions especially in cytoskeleton-, epigenetic gene regulation-, light signalling-, and phytohormone-related gene families were conspicuous. These data suggest that divergence in the number of putative orthologues amongst various land plant lineages contributed to the divergence of development in land plants.
The common ancestor of metazoans and land plants is inferred to be unicellular, and the developmental networks that produce a multicellular body are thought to have originated and been elaborated in parallel (Douzery et al., 2004). The result is that different gene families regulate the various developmental processes in each group, although similar mechanisms act to establish complex multicellular states(Arabidopsis-genome-initiative, 2000), including cell cycle regulation, organization of the cytoskeleton, receptor-signal transduction pathways, cell-cell interactions, transcription factor networks, and the epigenetic regulation of histones, genomic DNA, and several small RNA molecules.
Land plants are monophyletic and phylogenetically related to freshwater green algae (Turmel et al., 2007). Bryophytes are basal lineages in land plants (Judd et al., 2002). Next to bryophytes, clubmosses (lycopods) branched from the other extant land plant lineage leading to flowering plants (angiosperms). A comparison of the developmental genes that exist in each of the land plant lineages will be helpful in understanding the diversity of development and morphology in land plants. A previous comparison of ESTs from the moss Physcomitrella patens and genomic data from the flowering plant Arabidopsis thaliana suggested a similarity between the two genomes in terms of their genetic content (Nishiyama et al., 2003). A genome-wide comparison of transcription-associated proteins in A. thaliana, Oryza sativa, P. patens, and Chlamydomonas reinhardtii showed that the number of gene families was similar amongst land plants but that the size of each tended to be bigger in angiosperms than in P. patens and Ch. reinhardtii(Richardt et al., 2007). Detailed phylogenetic analyses of 13 families of transcription factor genes involved in development showed a similar tendency (Floyd and Bowman, 2007). However, it is unknown whether it is the case in many other genes involved in development. Thus, making global comparisons of the phylogenetic relationships between genes involved in development and deducing the factors and events that led to the diverse developmental pathways of land plants pose major challenges.
A TAIR database (http://www.arabidopsis.org) search using "development" as the keyword uncovered 1,534 A. thaliana genes. From this initial pool, those genes whose functions were relatively well-known were selected. Together with other well-characterized genes, in total, 402 genes were used as queries for phylogenetic analyses. Homologous sequences were collected for each query from public DNA databases, and phylogenetic analyses by the neighbor joining (NJ) and maximum likelihood (ML) methods were performed. Based on the resulting phylogenetic trees (available at http://moss.nibb.ac.jp/treedb/), we identified a monophyletic group containing all genes putatively descended from a common ancestral gene in land plants for each A. thaliana gene. The genes included in the group were defined as land plant orthologues, and the number of genes from A. thaliana, O. sativa, S. moellendorffii, and P. patens was determined. Since each phylogenetic tree contains several A. thaliana genes and we could examine 826 A. thaliana developmental genes. Land plant orthologues of the 731 and 708 developmental genes in the 826 A. thaliana were identified in S. moellendorffii and P. patens, corresponding to 88% and 86%, respectively. This indicates that the common ancestor of land plants had most of the gene families used in angiosperm development. Land plant orthologues involved in the basic molecular machinery of development, such as the cell cycle, cytoskeleton, DNA methylation, histone modification, chromatin remodeling, endogenous small RNA regulation, and circadian clock, were largely conserved in the land plant lineages (103 of 110 land plant orthologous groups).
However, we discovered conspicuous expansions of certain gene families, which resulted in different numbers of land plant orthologues in each genome (Table 1). Furthermore, 81 land plant orthologues were contracted and lost in some lineages (Tables 1-3). We could not find members for 12%, 16%, and 10% of the 424 land plant orthologous groups in S. moellendorffii, P patens, and both species, respectively. Together, these land plant orthologous groups with their variations in size are likely related to the divergence of developmental processes in different land plant lineages.
Those genes involved in phytohormone synthesis and signalling are one of the most plausible candidates. Phytohormones are small molecules that function as growth regulators in various aspects of plant development (Davies et al., 1991). Several genes encoding biosynthesis and metabolic enzymes of auxin, including CYP79B2, CYP79B3, NITs, CYP83B1/SUR2, and CYP79F1/SPS1, the efflux carrier MDR1/PGP1, the efflux regulator PID, and the auxin signalling regulator ARF17, were found only in angiosperms (Table 2). In contrast, several auxin-related gene families involved in metabolism (e.g. GH3.6/DFL1) and in signalling (e. g. AUX/IAAs and ARFs) were expanded in the angiosperm lineage (Table 1). This implies that the evolution of auxin regulation using newly evolved putative orthologues is correlated with the evolution of angiosperm-specific development. Thus, the change in size of the putative orthologue groups was likely an important factor in the rise of developmental diversity.
We also found differences in the number of putative orthologues for other phytohormone genes (Tables 1-3). For example, as expected based on biochemical data (Osborne et al., 1996), the key ethylene biosynthetic enzymes ACC synthase and ACC oxidase genes, ACSs and ACOs, were absent from S. moellendorffii and P. patens. In addition, putative orthologues of brassinosteroid receptor BRI1 were not identified in either species, although further characterisation is necessary to determine whether closely related homologues perform the function. In contrast, several gene families, including the CKXs cytokinin level regulators (Schmülling et al., 2003), ARRs cytokinin signalling, and BIN2 brassinosteroid signalling, were expanded in each lineage (Table 1).
In addition to phytohormones, light signalling pathways are also important in plant development (Chen et al., 2004). Land plant orthologues were identified in all lineages for 43 of the 54 land plant orthologous group examined, which include 90 A. thaliana light signalling genes. Not found were 14 FAR1-related genes and 10 other genes (Tables 2 and 3). As observed for phytohormones, the genes for both light perception and signal transduction were expanded in each lineage (Table 1), suggesting that a range of modifications were made to the basic light signalling network in each lineage.
Similar expansions were observed between each genome for other land plant orthologues governing various developmental processes and stages (Table 1). Regulation of the cell cycle is indispensable for proper development (Inzé and De Veylder, 2006). Land plant orthologues of all A. thaliana cell cycle regulators except CDKB2;1 and CDKB2;2 were found in all lineages (Table 2), whilst the land plant orthologues of CYCB, CYCD, and KRP were expanded mainly in the angiosperm lineages, and the CYCA genes were expanded in both the angiosperm and P. patens lineages (Table 1). Several genes involved in epigenetic regulation, including METs, CMTs, DRMs, and AGOs, were expanded in a lineage-specific manner. Several transcription factors involved in development were expanded in an angiosperm lineage, including the class IV homeodomain leucine zipper genes (ANL2, GL2, and PDF2), in addition to the previously reported transcription factors (Floyd and Bowman, 2007; Richardt et al., 2007) PLTs, WUS, and BEL1, whilst a substantial number of transcription factors were expanded in each lineage, including ABI4, MIKCC- and MIKC*-type MADS-box genes, VNDs, NSTs, and ATHBs (Table 1).
Several land plant orthologues were conspicuously expanded in S. moellendorffii and P. patens lineages and not in the angiosperm lineages, including MBD11 methyl CpG binding protein gene, PHOTs and NPH3 involved in blue light signalling of phototropism, COP1 a negative regulator of photomorphogenesis (Richardt et al., 2007), and EMS1/EXS for microspore formation (Table 1). Functional changes following the expansion and contraction of a putatively orthologous group should be a major source of developmental diversity in land plants. The land plant orthologues expanded in each lineage in parallel, suggesting that the common ancestor of land plants had fewer genes than the extant land plants. Parsimony dictates the inference that many of the land plant orthologues expanded after the divergence of each lineage, rather than the parallel loss of multiple genes in each lineage. The smaller number of the putatively orthologous genes in Ch. reinhardtii and Cy. merolae (phylogenetic trees in http://moss.nibb.ac.jp/treedb/) also supports this inference, although it may simply reflect their unicellular life cycles. The expansion of the land plant orthologues in each land plant lineage is correlated with the divergence of development amongst land plants. Polyploidy and aneuploidy are frequently observed in land plant lineages(Wendel, 2000), and these events are a likely driving force behind the parallel expansion of land plant orthologues, although the mechanism that allows the retention of amplified genes remains unknown (Shiu et al., 2005).
The conservation of common land plant orthologues in diverse lineages allows for comparisons of molecular function amongst orthologous genes in different lineages, which will provide valuable insights into the evolution of developmental genes at the molecular level (Maizel et al., 2005). Such studies will help elucidate the land plant body plan, which involves a core developmental network common to all land plants.
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Methods
Data sets.
We obtained P. patens and S. moellendorffii WGS sequences and the quality and ancillary data from ftp://ftp.ncbi.nih.gov/pub/TraceDB/. Sequences judged to be ESTs were excluded from the analysis. The NCBI nr data set was obtained from ftp://ftp.ncbi.nih.gov/blast/db/. Amino acid sequences of S. moellendorffii filtered model data were obtained from Selmo1_GeneModels_FilteredModels2_aa.fasta.gz. The Ch. reinhardtii and Cy. merolae protein data sets were obtained from ftp://ftp.jgi-psf.org/pub/JGI_data/Chlamy/v3.0/proteins.Chlre3.fasta.gz and http://merolae.biol.s.u-tokyo.ac.jp/download/cds.fasta, respectively. The taxonomy database(Wheeler et al., 2000) was obtained from ftp://ftp.ncbi.nih.gov/pub/taxonomy. Phylogenetic analyses. We performed each phylogenetic analysis in three steps: automatic collection of homologous sequences and alignment, manual selection of well-aligned regions and exclusion of sequences with insufficient similarity or mutant alleles, and automatic reconstruction of genetic phylogeny using the NJ and ML methods. Statistical support was examined with bootstrapping.
Alignment of the collected sequences
To prepare the alignments, Web-based interfaces were established. The blast-assemble-both interface allows a similarity search against the data sets for each query. BLASTP (Altschul et al., 1997) with word size 2 and TBLASTN (Altschul et al., 1997) were used for the protein and WGS nucleotide data sets, respectively. An assembly and a putative amino acid sequences of the collected WGS data were obtained using CAP3 (Huang and Madan, 1999) and GenomeScan (http://genes.mit.edu/genomescan.html), respectively. All amino acid sequences were aligned with MAFFT version 5.743 (Katoh et al., 2005) using the EINSI option (--ep 0 --genafpair --maxiterate 1,000). When a single gene from P. patens or S. moellendorffii was scattered into multiple contigs, a blast-assemble-bothext interface was used, in which a MEGABLAST search of the original WGS data with the contigs as queries and reassembly with CAP3 using a more moderate parameter set (-b 30 -c 20 -d 21 -s 401 -u 1) were performed.
The resulting alignment was manually edited with MacClade version 4.08 on Mac OS X(Maddison and Maddison, 2000) to remove unnecessary sequences and to mark which amino acid sites to include or exclude from the analysis. Those sequences that lacked a region conserved in the other sequences were removed from the main analysis, and a separate analysis using the sites that the partial sequences had in common with the other sequences was performed to identify their phylogenetic positions.
Reconstruction and manual curation of the gene trees
Phylogenetic analyses were performed using makenjtree interface. The NJ tree (Saitou and Nei) was reconstructed using PHYLIP ver. 3.65(Felsenstein, 2005) and the ML tree was searched with local re-arrangement using MOLPHY-2.3b3 (Adachi and Hasegawa) under the JTT model (Jones et al., 1992). Each tree was investigated to identify orthologous land plant genes putatively derived from a single gene in the last common ancestor of land plants. Each minimum land plant clade consisted of genes from all of P. patens, S. moellendorffii, O. sativa, and A. thaliana. Because we cannot exclude the possibility of parallel gene losses, the genes included in the minimum land plant clade were designated as putative orthologues. Then, a maximum land plant clade was defined as a clade that contains neither the minimum land plant clades nor non-land plant genes. The maximum land plant clade lacks genes from some of the four species. We also regarded genes included in the maximum land plant clade as putative orthologues. Both minimum and maximum land plant clades were designated as putatively orthologueous land plant clades.
Determination of gene number
The genes in the putatively orthologous land plant clade were counted to determine the number of putative orthologues. Sequences derived from a single locus in A. thaliana or O. sativa were counted as one gene. Since the WGS sequences of S. moellendorffii were derived from a diploid plant, pairs of highly similar sequences, presumably allelic, were frequently detected. These pairs were counted as two alleles of one locus. If multiple non-overlapping sequences could be considered as fragments of a single gene, they were counted as one gene. Those sequences with in-frame stop codons in a conserved region and those sequences lacking a significant portion of the conserved region were judged to be pseudogenes and excluded from the count.
Table 1
A list of putatively orthologueous genes with conspicuous expansion during land plant evolution. The number of land plant orthologues for each genome is indicated. Categories
| Categories | Genes | Arabidopsis thaliana | Oryza sativa | Selaginella moellendorffii | Physcomitrella patens |
| Cell cycle regulation | CYCA1;1 to 2, A2;1 to 4, A3;1 to 4 | 10 | 7 | 3 (6) | 8 |
| Cell cycle regulation | CYCB1;1 to 5, B2;1 to 5, B3;1 | 11 | 5 | 1 (2) | 2 |
| Cell cycle regulation | CYCD4;1 to 2, D5;1, D6;1, D7;1 | 10 | 12 | 3 (5) | 2 |
| Cell cycle regulation | KRP1 to 7 | 7 | 6 | 3 (6) | 1 |
| Cytoskeleton | WAVE1 to 5/ATSCAR1 to 5 | 5 | 3 | 2 (3) | 7 |
| Epigenetic gene regulation | HDT1 to 4 | 4 | 3 | 1 (2) | 3 |
| Epigenetic gene regulation | MBD11 | 2 | 1 | 2 (4) | 7 |
| Epigenetic gene regulation | MET1 to 4 | 4 | 2 | 1 (2) | 1 |
| Epigenetic gene regulation | CMT1 to 3 | 3 | 3 | 1 (2) | 1 |
| Epigenetic gene regulation | DRM1 to 3 | 3 | 4 | 3 (6) | 2 |
| RISC complex | AGO2, 3, 7 | 3 | 3 | 1 (2) | 1 |
| RISC complex | AGO4, 6, 8, 9 | 4 | 3 | 1 (2) | 3 |
| Light signalling | FAR1, FRS1 to 12, FHY3 | 14 | 56 | 0 (0) | 0 |
| Light signalling | PHOT1, 2 | 2 | 2 | 2 (4) | 6 |
| Light signalling | NPH3 | 2 | 1 | 3 (6) | 15 |
| Light signalling | COP1 | 1 | 1 | 1 (2) | 9 |
| Light signalling | OBP3 | 13 | 4 | 0 | 0 |
| Light signalling | PIF1/PIL5, PIF3-4, PIL1-4, HFR/PIL6 | 14 | 10 | 3 (6) | 3 |
| Light signalling | ZFP1 | 27 | 27 | 6 (11) | 10 |
| Auxin biosynthesis and metabolism | GH3.6/DFL1 | 19 | 11 | 17 (29) | 2 |
| Auxin signalling | SKP1/ASK1 | 17 | 12 | 1 (2) | 3 |
| Auxin signalling | IAA1-20, IAA26-34 | 29 | 30 | 4 (7) | 2 |
| Auxin signalling | ETT/ARF3,ARF1,2,4,9,11 to 15,18, 20, and 21 | 15 | 9 | 2 (4) | 4 |
| Cytokinin biosynthesis | CKX1 to 7 | 7 | 11 | 2 (4) | 6 |
| Cytokinin signalling | ARR3 to 9, 15 to 17 | 11 | 15 | 2 (4) | 7 |
| Gibberellic acid biosynthesis | GA1/KSA/CPS, GA2/KSB | 11 | 13 | 9 (13) | 2 |
| Abscisic acid biosynthesis | ABA2, ATA1 | 11 | 20 | 5 (10) | 2 |
| Brassinosteroid biosynthesis | CPD, DWF4, ROT3, BR6OX1 and 2 | 19 | 16 | 4 (8) | 3 |
| Brassinosteroid signalling | BIN2, AT1G06390, AT2G30980 | 10 | 9 | 2 (4) | 6 |
| Seed | ABI4 | 9 | 5 | 4 (6) | 7 |
| Lateral root | RPD1 | 15 | 17 | 10 (20) | 4 |
| Root | PLT1 and 2 | 8 | 11 | 1 (2) | 3 |
| Root / Shoot meristem | WUS, WOX1 to 14 | 16 | 10 | 9 (16) | 3 |
| Shoot meristem / Gynoecium | BEL1, BLR, PNF, PNY | 13 | 13 | 2 (2) | 4 |
| Epidermal cell differentiation | ANL2, ATML1, GL2, PDF2 | 17 | 10 | 5 (9) | 4 |
| Stomata development | SDD1 | 3 | 13 | 0 | 0 |
| Vascular system | VND1-7, NST1 and 2 | 13 | 10 | 4 (7) | 8 |
| Lignin synthesis | CCR1, 2 | 2 | 13 | 3 (5) | 1 |
| Lignin synthesis | COMT | 13 | 12 | 16 (28) | 3 |
| Flowering | CO | 18 | 17 | 3 (5) | 6 |
| Floral organ | AG, PI, AP3, AP1, SHP1 and 2, SEP1 to 3 | 38 | 34 | 3 (5) | 6 |
| Pollen | AGL30, AGL65, AGL66, AGL94, and AGL104 | 6 | 3 | 3 (6) | 11 |
| Pollen | EMS1/EXS | 1 | 2 | 2 (2) | 6 |
| Pollen | TPD1 | 4 | 14 | 5 (9) | 9 |
| Pollen | GPAT1 | 8 | 15 | 10 (20) | 7 |
| Other transcription factors | ATHB1, 3, 5-7, 12, 13, and 16 | 17 | 12 | 4 (8) | 17 |
Table 2
A. thaliana genes without putative orthologues in S. moellendorffii or P. patens
| Categories | Gene |
| Cell cycle regulation | CDKB2;1, 2;2 |
| Epigenetic gene regulation | HDA6 and 7, MSI2, 3, and 5 |
| RISC complex | AGO10/ZLL/PNH |
| Light signalling | FAR1, FRS1 to 12, FHY3, PKS1, LAF1, OBP3, MIF1, CIP1*, CIP4* |
| Auxin biosynthesis and metabolism | CYP79B2, 3, NIT1 to 3, CYP83B1/SUR2, CYP79F1/SPS1 |
| Auxin signalling | ARF17 |
| Auxin carriers | MDR/PGP1, PID |
| Cytokinin biosynthesis | CYP735A1 and 2 |
| Ethylene biosynthesis | ACS1-9 and 11, ACO1 and 2 |
| Brassinosteroid signalling | BRI1, BRL1, BSU1* |
| Embryo Defective | EMB1875 * |
| Lateral root | NAC1 |
| Shoot meristem | AS2, ULT1 |
| Leaf | CRC, FIL, INO, ARGOS, ARL |
| Epidermal cell differentiation | TTG1, MYB23, GL1, WER, CPC, ETC1 and 2, TRY, SUB |
| Stomata opening | AGG1 |
| Stomata development | SDD1 |
| Vascular system | DRP1A |
| Lignin synthesis | FAH1 |
| Phase transition | SWN, MEA* |
| Flowering | FT, TFL1, FD, EMF1 |
| Floral organ | HUA1 |
| Pollen | BCP1* |
| Phosphoinosities | SOS5 |
| * Genes found in A. thaliana but not in O. sativa |
Table 3
A. thaliana genes with putative orthologues in S. moellendorffii, but not in P. patens
| Categories | Gene |
| Epigenetic gene regulation | CHR15/MOM |
| Epigenetic gene regulation | CHR37 and 41 |
| Light signalling | LKP2, FKF1, ZTL/LKP1, CIP8 |
| Circadian clock | TOC1 |
| Gibberellic acid signalling | GID1L1 to 3 |
| Ethylen signalling | CTR1 |
| Seed | LEC1 |
| Embryo | EMB3001 |
| Embryo | EMB3007* |
| Shoot meristem | CLV1 |
| Shoot meristem | CLV2 |
| Shoot meristem | AS1 |
| Axillary meristem | MAX1 |
| Axillary meristem | RAX1 |
| Epidermal cell differentiation | RIC2 |
| Stomata opening | GPA1 |
| Stomata opening | GORK |
| Flowering | TFL2/LHP1 |
| Flowering | VIN3 |
| Flowering | GI |
| Floral organ | AP2 |
| Floral organ | UFO |
| Pollen | MYB4 and 32 |
| Phosphoinosities | DGK1 and 2 |
| Phosphoinosities | PTEN* |
| * Genes found in A. thaliana but not in O. sativa |
