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PubMed2001

Genomic organization of plant terpene synthases and molecular evolutionary implications.

Terpenoids are the largest, most diverse class of plant natural products and they play numerous functional roles in primary metabolism and in ecological interactions. The first committed step in the formation of the various terpenoid classes is the transformation of the prenyl diphosphate precursors, geranyl diphosphate, farnesyl diphosphate, and geranylgeranyl diphosphate, to the parent structures of each type catalyzed by the respective monoterpene (C(10)), sesquiterpene (C(15)), and diterpene synthases (C(20)). Over 30 cDNAs encoding plant terpenoid synthases involved in primary and secondary metabolism have been cloned and characterized. Here we describe the isolation and analysis of six genomic clones encoding terpene synthases of conifers, [(-)-pinene (C(10)), (-)-limonene (C(10)), (E)-alpha-bisabolene (C(15)), delta-selinene (C(15)), and abietadiene synthase (C(20)) from Abies grandis and taxadiene synthase (C(20)) from Taxus brevifolia], all of which are involved in natural products biosynthesis. Genome organization (intron number, size, placement and phase, and exon size) of these gymnosperm terpene synthases was compared to eight previously characterized angiosperm terpene synthase genes and to six putative terpene synthase genomic sequences from Arabidopsis thaliana. Three distinct classes of terpene synthase genes were discerned, from which assumed patterns of sequential intron loss and the loss of an unusual internal sequence element suggest that the ancestral terpenoid synthase gene resembled a contemporary conifer diterpene synthase gene in containing at least 12 introns and 13 exons of conserved size. A model presented for the evolutionary history of plant terpene synthases suggests that this superfamily of genes responsible for natural products biosynthesis derived from terpene synthase genes involved in primary metabolism by duplication and divergence in structural and functional specialization. This novel molecular evolutionary approach focused on genes of secondary metabolism may have broad implications for the origins of natural products and for plant phylogenetics in general.

Alkyl and Aryl Transferases↗
PubMed1999

Potentials and limitations of histone repeat sequences for phylogenetic reconstruction of Sophophora.

Simplified DNA sequence acquisition has provided many new data sets that are useful for phylogenetic reconstruction, including single- and multiple-copy nuclear and organellar genes. Although transcribed regions receive much attention, nontranscribed regions have recently been added to the repertoire of sequences suitable for phylogenetic studies, especially for closely related taxa. We evaluated the efficacy of a small portion of the histone repeat for phylogenetic reconstruction among Drosophila species. Histone repeats in invertebrates offer distinct advantages similar to those of widely used ribosomal repeats. First, the units are tandemly repeated and undergo concerted evolution. Second, histone repeats include both highly conserved coding and variable intergenic regions. This composition facilitates application of "universal" primers spanning potentially informative sites. We examined a small region of the histone repeat, including the intergenic spacer segments of coding regions from the divergently transcribed H2A and H2B histone genes. The spacer (about 230 bp) exists as a mosaic with highly conserved functional motifs interspersed with rapidly diverging regions; the former aid in alignment of the spacer. There are no ambiguities in alignment of coding regions. Coding and noncoding regions were analyzed together and separately for phylogenetic information. Parsimony, distance, and maximum-likelihood methods successfully retrieve the corroborated phylogeny for the taxa examined. This study demonstrates the resolving power of a small histone region which may now be added to the growing collection of phylogenetically useful DNA sequences.

Animals↗
PubMedDate not supplied

Alcohol dehydrogenases, aldehyde dehydrogenases, and related enzymes.

Several new structures have recently been determined for dehydrogenases which are involved in alcohol metabolism. These structures give new insight into catalytic properties, structure-function relationships, and evolutionary connections. They also explain the structural basis for known metabolic deviations. Among alcohol dehydrogenases, the first primary structures for human enzyme forms have been reported (the beta 1, gamma 1, and "atypical" beta-chains). These structures explained functional properties and enzymatic differences, showed separate and parallel events of isozyme divergence, and suggested differential gene activations. Similarly, for aldehyde dehydrogenases, the first cytoplasmic isozyme structures have been reported in man and horse. The data showed positions of functionally important residues, and established clear differences between the mitochondrial and cytoplasmic isozymes of aldehyde dehydrogenase. For sorbitol dehydrogenase, the first complete structure which establishes a relationship with other "long" alcohol dehydrogenases in a scheme exhibiting both structural divergence and functional convergence has also been reported. Finally, glucose dehydrogenase has been structurally linked with sorbitol dehydrogenase, extending the scheme and adding further enzymes to the group of "short" alcohol dehydrogenases.

Alcohol Oxidoreductases↗
PubMed2002

Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome.

The recent sequencing of several eukaryotic genomes has generated considerable interest in the study of gene duplication events. The classical model of duplicate gene evolution is that recurrent mutation ultimately results in one copy becoming a pseudogene, and only rarely will a beneficial new function evolve. Here, we study divergence between coding sequence duplications in Drosophila melanogaster as a function of the linkage relationship between paralogs. The mean K(a)/K(s) between all duplicates in the D. melanogaster genome is 0.2803, indicating that purifying selection is maintaining the structure of duplicate coding sequences. However, the mean K(a)/K(s) between duplicates that are both on the X chromosome is 0.4701, significantly higher than the genome average. Further, the distribution of K(a)/K(s) for these X-linked duplicates is significantly shifted toward higher values when compared with the distributions for paralogs in other linkage relationships. Two models of molecular evolution provide qualitative explanations of these observations-relaxation of selective pressure on the duplicate copies and, more likely, positive selection on recessive adaptations. We also show that there is an excess of X-linked duplicates with low K(s), suggesting a larger proportion of relatively young duplicates on the D. melanogaster X chromosome relative to autosomes.

Animals↗
PubMed2000

Divergent effects of extracellular oxygen on the growth, morphology, and function of human skin microvascular endothelial cells.

Partial pressure of extracellular oxygen influences a number of major cellular functions. The purpose of this study was to determine if the proliferation, morphology, and synthesis of proteins important in the function of skin microvascular endothelial cells were significantly altered by an extracellular oxygen tension used to culture endothelial cells. Microvascular endothelial cells were isolated from the dermis of neonatal foreskins and were studied at a venous capillary oxygen level (5% O(2), 38 mm Hg) and at an atmospheric oxygen level (20.8% O(2,) 158 mm Hg). At all time points studied and at all passage numbers, a significant inhibition of proliferation was observed at 20.8% O(2) compared to identical cultures grown and subcultured at 5% O(2). Two morphologically distinct endothelial cell populations were observed at 5% O(2). When mediators of angiogenesis and inflammation-such as basic fibroblast growth factor (bFGF), phorbol myristate acetate (PMA), and interleukin-1beta (IL-1beta)-were studied, additional differences in proliferation were observed. Atmospheric O(2) inhibited the synthesis of a major basement membrane protein (Type IV collagen), a major surface protein (PECAM-1), and increased the synthesis of von Willebrand factor (vWf). The rate of vascular channel formation induced by collagen gels was decreased at 5% O(2). These results demonstrate that an increase in extracellular oxygen tension from 5 to 20.8% can significantly alter the cellular physiology of human skin microvascular endothelial cells.

Atmospheric Pressure↗
PubMed2005

The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins.

Several DNA-damage detection and repair mechanisms have evolved to repair double-strand breaks induced by mutagens. Later in evolutionary history, DNA single- and double-strand cuts made possible immune diversity by V(D)J recombination and recombination at meiosis. Such cuts are induced endogenously and are highly regulated and controlled. In meiosis, DNA cuts are essential for the initiation of homologous recombination, and for the formation of joint molecule and crossovers. Many proteins that function during somatic DNA-damage detection and repair are also active during homologous recombination. However, their meiotic functions may be altered from their somatic roles through localization, posttranslational modifications and/or interactions with meiosis-specific proteins. Presumably, somatic repair functions and meiotic recombination diverged during evolution, resulting in adaptations specific to sexual reproduction. (c) 2005 Wiley Periodicals, Inc.

Animals↗
PubMed2004

Higher plant cortical microtubule array analyzed in vitro in the presence of the cell wall.

Plant morphogenesis depends on an array of microtubules in the cell cortex, the cortical array. Although the cortical array is known to be essential for morphogenesis, it is not known how the array becomes organized or how it functions mechanistically. Here, we report the development of an in vitro model that provides good access to the cortical array while preserving the array's organization and, importantly, its association with the cell wall. Primary roots of maize (Zea mays) are sectioned, without fixation, in a drop of buffer and then incubated as desired before eventual fixation. Sectioning removes cytoplasm except for a residuum comprising cortical microtubules, vesicles, and fragments of plasma membrane underlying the microtubules. The majority of the cortical microtubules remain in the cut-open cells for more than 1 h, fully accessible to the incubation solution. The growth zone or more mature tissue can be sectioned, providing access to cortical arrays that are oriented either transversely or obliquely to the long axis of the root. Using this assay, we report, first, that cortical microtubule stability is regulated by protein phosphorylation; second, that cortical microtubule stability is a function of orientation, with divergent microtubules within the array depolymerizing within minutes of sectioning; and third, that the polarity of microtubules in the cortical array is not uniform. These results suggest that the organization of the cortical array involves random nucleation followed by selective stabilization of microtubules formed at the appropriate orientation, and that the signal specifying alignment must treat orientations of +/- 180 degrees as equivalent.

Adenosine Triphosphate↗
PubMed1994

Regulation and evolution of the single alpha-tubulin gene of the ciliate Tetrahymena thermophila.

The single alpha-tubulin gene of Tetrahymena thermophila was isolated from a genomic library and shown to encode a single protein. Comparisons of the rates of evolution of this gene with other alpha-tubulin sequences revealed that it belongs to a group of more evolutionarily constrained alpha-tubulin proteins in animals, plants, and protozoans versus the group of more rapidly evolving fungal and variant animal alpha-tubulins. The single alpha-tubulin of Tetrahymena must be used in a variety of microtubule structures, and we suggest that equivalently conserved alpha-tubulins in other organisms are evolutionarily constrained because they, too, are multifunctional. Reduced constraints on fungal tubulins are consistent with their simpler microtubule systems. The animal variant alpha-tubulins may also have diverged because of fewer functional requirements or they could be examples of specialized tubulins. To analyze the role of tubulin gene expression in regulation of the complex microtubule system of Tetrahymena, alpha-tubulin mRNA amounts were examined in a number of cell states. Message levels increased in growing versus starved cells and also during early stages of conjugation. These changes were correlated with increases in transcription rates. Additionally, alpha-tubulin mRNA levels oscillate in a cell cycle dependent fashion caused by changes in both transcription and decay rates. Therefore, as in other organisms, Tetrahymena adjusts alpha-tubulin message amounts via message decay. However the complex control of alpha-tubulin mRNA during the Tetrahymena life cycle involves regulation of both decay and transcription rates.

Amino Acid Sequence↗
PubMed1994

Determination of the structure of the DNA binding domain of gamma delta resolvase in solution.

The DNA binding domain (DBD) of gamma delta resolvase (residues 141-183) is responsible for the interaction of this site-specific DNA recombinase with consensus site DNA within the gamma delta transposable element in Escherichia coli. Based on chemical-shift comparisons, the proteolytically isolated DBD displays side-chain interactions within a hydrophobic core that are highly similar to those of this domain when part of the intact enzyme (Liu T, Liu DJ, DeRose EF, Mullen GP, 1993, J Biol Chem 268:16309-16315). The structure of the DBD in solution has been determined using restraints obtained from 2-dimensional proton NMR data and is represented by 17 conformers. Experimental restraints included 458 distances based on analysis of nuclear Overhauser effect connectivities, 17 phi and chi 1 torsion angles based on analysis of couplings, and 17 backbone hydrogen bonds determined from NH exchange data. With respect to the computed average structure, these conformers display an RMS deviation of 0.67 A for the heavy backbone atoms and 1.49 A for all heavy atoms within residues 149-180. The DBD consists of 3 alpha-helices comprising residues D149-Q157, S162-T167, and R172-N183. Helix-2 and helix-3 form a backbone fold, which is similar to the canonical helix-turn-helix motif. The conformation of the NH2-terminal residues, G141-R148, appears flexible in solution. A hydrophobic core is formed by side chains donated by essentially all hydrophobic residues within the helices and turns. Helix-1 and helix-3 cross with a right-handed folding topology. The structure is consistent with a mechanism of DNA binding in which contacts are made by the hydrophilic face of helix-3 in the major groove and the amino-terminal arm in the minor groove. This structure represents an important step toward analysis of the mechanism of DNA interaction by gamma delta resolvase and provides initial structure-function comparisons among the divergent DBDs of related resolvases and invertases.

Amino Acid Sequence↗
PubMed2026

Doublesex gene influences sex differentiation and embryonic development in predatory mite Phytoseiulus persimilis.

BACKGROUND: Phytoseiulus persimilis is an effective biocontrol agent characterized by paternal genome elimination (PGE), an unusual reproductive system in which males eliminate the paternal genome during embryogenesis. However, the molecular mechanism underlying sex determination and reproductive regulation in this species remain poorly understood. RESULTS: Transcriptome-based analyses identified two doublesex (dsx) homologs, Ppdsx1 and Ppdsx2, as candidate regulators of reproduction. Weighted gene co-expression network analysis (WGCNA) assigned Ppdsx2 to a pre-mating-associated co-expression module enriched for reproductive and signaling pathways. Functional analyses revealed clear divergence between the two genes. RNA interference (RNAi) of Ppdsx1 reduced the proportion of female offspring, whereas RNAi of Ppdsx2 induced sex reversal, developmental abnormalities, and impaired egg viability. Yeast two-hybrid and glutathione S-transferase (GST) pull-down assays further demonstrated interactions between Dsx proteins and vitellogenin (Vg)-derived fragments identified from a complementary DNA (cDNA) library screen, suggesting a previously unrecognized connection between sex determination and reproductive nutrient allocation. CONCLUSIONS: Ppdsx1 contributes to maintenance of the female developmental pathway, whereas Ppdsx2 represents a strong candidate component of the PGE-associated sex-determination cascade. The observed Dsx-Vg fragment interaction suggests a potential link between reproductive developmental programs and nutrient allocation pathways. These findings provide new insights into the molecular basis of sex determination and reproductive regulation in phytoseiid mites and establish a foundation for future studies on the coupling of reproductive development and resource allocation. © 2026 Society of Chemical Industry.

Animals↗
PubMed2000

The isolation of FOS-1, a gene encoding a putative two-component histidine kinase from Aspergillus fumigatus.

In fungi, two-component histidine kinases are involved in response mechanisms to extracellular changes in osmolarity, resistance to dicarboximide fungicides, and cell-wall assembly. In the human opportunistic fungus, Candida albicans, each of the three histidine kinases plays a role in virulence. Here, we identify, for the first time, a gene, FOS-1, from the human pathogenic fungus Aspergillus fumigatus that predicts a protein with homology to two-component histidine kinases. The predicted FOS-1 protein is highly homologous to bacterial and other fungal histidine kinases in several functional domains, but is divergent at the amino- and carboxy-termini. A mutant lacking the FOS-1 locus, DeltaFOS-1, did not exhibit a detectable defect in either hyphal growth or morphology when grown on solid or liquid medium. However, in liquid medium, conidiophore development of the DeltaFOS-1 mutant was delayed. Compared to wild type, the DeltaFOS-1 strain was neither osmotically sensitive nor sensitive or resistant to a number of nondicarboximide antifungal drugs, but was highly resistant to dicarboximide fungicides and resistant to novozym 234, suggesting that FOS-1p may play a role in the regulation of cell-wall assembly.

Amino Acid Sequence↗
PubMed1990

Cloning and sequencing of cDNAs encoding two self-incompatibility associated proteins in Solanum chacoense.

We have isolated and sequenced cDNAs for S2- and S3-alleles of the self-incompatibility locus (S-locus) in Solanum chacoense Bitt., a wild potato species displaying gametophytic self-incompatibility. The S2- and S3-alleles encode pistil-specific proteins of 30 kDa and 31 kDa, respectively, which were previously identified based on cosegregation with their respective alleles in genetic crosses. The amino acid sequence homology between the S2- and S3-proteins is 41.5%. This high degree of sequence variability between alleles is a distinctive feature of the S-gene system. Of the 31 amino acid residues which were previously found to be conserved among three Nicotiana alata S-proteins (S2, S3, and S6) and two fungal ribonucleases (RNase T2 and RNase Rh), 27 are also conserved in the S2- and S3-proteins of S. chacoense. These residues include two histidines implicated in the active site of the RNase T2, six cysteines, four of which form disulfide bonds in RNase T2, and hydrophobic residues which might form the core structure of the protein. The finding that these residues are conserved among S-proteins with very divergent sequences suggests a functional role for the ribonuclease activity of the S-protein in gametophytic self-incompatibility.

Alleles↗
PubMed1994

Two distinct P element subfamilies in the genome of Drosophila bifasciata.

The genome of Drosophila bifasciata harbours two distinct subfamilies of P-homologous sequences, designated M-type and O-type elements based on similarities to P element sequences from other species. Both subfamilies have some general features in common: they are of similar length (M-type: 2935 bp, O-type: 2986 bp), are flanked by direct repeats of 8 bp (the presumptive target sequence), contain terminal inverted repeats, and have a coding region consisting of four exons. The splice sites are at homologous positions and the exons have the coding capacity for proteins of 753 amino acids (M-type) and 757 amino acids (O-type). It seems likely that both types of element represent functional transposons. The nucleotide divergence of the two P element subfamilies is high (31%). The main structural difference is observed in the terminal inverted repeats. Whereas the termini of M-type elements consists of 31 bp inverted repeats, the inverted repeats of the O-type elements are interrupted by non-complementary stretches of DNA, 12 bp at the 5' end and 14 bp at the 3' end. This peculiarity is shared by all members of the O-type subfamily. Comparison with other P element sequences indicates incongruities between the phylogenies of the species and the P transposons. M-type and O-type elements apparently have no common origin in the D. bifasciata lineage. The M-type sequence seems to be most closely related to the P element from Scaptomyza pallida and thus could be considered as a more recent invader of the D. bifasciata gene pool. The origin of the O-type elements cannot be unequivocally deduced from the present data.(ABSTRACT TRUNCATED AT 250 WORDS)

Amino Acid Sequence↗
PubMed1995

Expression of a cytochrome P450 gene family in maize.

Maize seedlings, like seedlings of many other plants, are rich in cytochrome P450 (P450) enzyme activity. Four P450 genes (CYPzm1-4), isolated from a seedling-specific cDNA library, are characterized by a transient and seedling-specific expression pattern. The maximum steady state mRNA levels are reached at 3 days in root and at 7 days in shoot tissue, respectively. All four genes belong to one gene family and are closely related to the CYP71 family of plant P450 genes, which includes the enzymes of the ripening avocado fruit (CYP71A1) and eggplant hypocotyls (CYP71A2, A3, A4). The expression of these related P450 genes in monocot and dicot plants indicates that these enzymes play a significant role in plants; however, the in vivo enzyme functions are unknown. The divergence of the four members of the maize gene family is sufficiently high to account for different substrate and/or reaction specificity. Although the general expression pattern of the four genes is identical, the maximum steady-state mRNA levels vary in different maize lines. In situ hybridisation reveals the highest mRNA levels in the coleoptile, the first developed leaflets, the ground tissue of the nodular complex, and in the cortex and pith of the region of cell division in the root. The mapping of the maize CYPzm genes shows that, as in animals, P450 genes of the same family can be clustered. The presence of the CYPzm gene cluster in maize argues for generation of distinct plant P450 gene families by gene duplication.

Amino Acid Sequence↗
PubMed1978

Conservation and chromosomal localization of DNA satellites in balenopterid whales.

DNA satellites were isolated from three balenopterid species, viz. the minke, sei, and fine whales. In each of them at least two DNA satellites were recognizable with buoyant densities in neutral CsCl of rho = 1.702/1.703 and rho = 1.710/1;711, respectively. cRNAs from each satellite group were used for filter and in situ hybridisations. Homo-and heterologous DNA-cRNA hybrids within each satellite group yielded virtually identical melting curve profiles showing conservation of at least a considerable part of the DNA satellite sequences. There was no evident sequence homology between the rho = 1.702/1.703 and the rho = 1.710/1;711 satellites by filter hybridisation.--The in situ hybridisation showed that in each species the rho = 1.702/1.703 satellite was located in centromeric-paracentromeric C-bands in a few pairs, whereas the rho = 1.710/1.711 satellite was located in terminal C-bands throughout the karyotypes.--The data on the whale DNA satellites indicate that the quantitative evolution of the sateliite DNA sequences preceded species divergence of the balenopterids and that the satellite sequences have remained relatively unaltered since the divergence took place. The function of satellite DNA is considered to imply the introduction of both chromosomal and genic polymorphisms and thus being of great importance in speciation, Based upon these concepts a model is postulated for the function of satellite DNA. According to this model at meiotic pairing euchromatinheterochromatin overlapping between homologous chromosomes is considered to be of a general occurrence. This overlapping is presumed to be accentuated by the size heteromorphism frequently observed between homologous heterochromatic segments (C-bands). In the region of such euchromatinheterochromatin overlapping, cross-over would be excluded. The overlapping is suggested to be rectified progresssively in the chromosome arms, leaving unaffected crossing-over distant to the euchromatin-heterochromatin junctions. The consequence of this will be that genes in the proximity of the junctions are collectively inherited and selected, whereas genes distant to the the heterochromatin will be independently assorted and selected.

Animals↗
PubMed1992

Distribution of hyaluronan and its CD44 receptor in the epithelia of human skin appendages.

Biotinylated hyaluronan (HA) binding complex (HABC) from bovine articular cartilage proteoglycan was used as a histological probe to study the localization of HA in human skin. The distribution of HA was compared with its presumptive cell surface receptor, CD44, using monoclonal antibodies. In epidermis both HA and CD44 were found in the basal and spinous cell layers, but neither was present in the stratum granulosum and stratum corneum. In the keratinizing parts of hair follicles, i.e. in the outer and inner epidermal root sheath, pilosebaceous duct and the actual hair, HA and CD44 were found between the vital but not the terminally differentiated cells. In the sebaceous glands a small amount of HA was found around all cells, whereas CD44 was restricted to the basal cell layer. The secretory acini of the sweat glands stained intensively with anti-CD44 antibodies but only weakly with HABC. In the sweat gland, CD44 was localized on the basal and lateral surfaces of the clear cells, whereas the dark cells and the myoepithelial cells were negative. Both the lower and upper layers of the sweat gland ducts showed a faint but constant staining for CD44 and only minor amounts of HA. While in the keratinizing skin epithelia both HA and its CD44 receptor showed an intense staining with a close co-distribution, in the sweat and sebaceous glands their distribution patterns were not similar. It is suggested that in epithelia with divergent differentiation programs the functions of CD44 and HA may be different.

Biotin↗
PubMed1987

Nucleotide sequence of the delta-beta-globin intergenic segment in the macaque: structure and evolutionary rates in higher primates.

A 5600-base-pair (bp) fragment including the beta-globin gene and about 4000 bp of its 5' flanking sequence was cloned from the DNA of Macaca cynomolgus (an Old World monkey), and the 5' flanking region was sequenced. Comparison with human, chimpanzee, mouse, rabbit, and Xenopus orthologous sequences reveals a tandemly repeated sequence called RS4 at the same position (about 500 bp 5' from the transcription start of the adult beta-globin gene) in all six species. We suggest that a tandemly repeated sequence has been maintained by functional constraints since the divergence between amphibians and reptiles. Excluding tandemly repeated sequences as well as about 400 nucleotides upstream from the cap site, the average base substitution frequencies among human, chimpanzee, and macaque intergenic sequences were calculated. They appear to be strongly correlated with the delta T50 values measured between the corresponding nuclear DNAs. They are also similar to base substitution frequencies calculated by Chang and Slightom (1984) at the pseudo-eta-globin locus. Thus, exclusion of sequences involved in specific modes of variation might allow the use of intergenic sequences for the accurate calculation of genetic distances. Using a time scale based on the dating of the Atlantic split, we estimate the base substitution rate of primate noncoding DNA to be 1.0 X 10(-9) substitution/site/year.

Animals↗
PubMed1989

Classical plant taxonomic ambiguities extend to the molecular level.

The molecular evolution of cytochrome c from angiosperms is compared to that from vertebrates. On the basis of a cladistic analysis from 26 plant species, compared to that from 27 vertebrate species, we find that although the vertebrate sequences yield reasonably well-defined minimal trees that are congruent with the biological tree, the plant sequences yield multiple minimal trees that are not only highly incongruent with each other, but none of which is congruent with any reasonably biological tree. That is, the plant sequence set is much more homoplastic than that of the animal. However, as judged by the relative rate test, the extent of divergence, and degree of functional constraint, cytochrome c evolution in plants does not appear to differ from that of vertebrates.

Animals↗