Homeosis

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Antennapedia mutation Antennapedia2.jpg
Antennapedia mutation

In evolutionary developmental biology, homeosis is the transformation of one organ into another, arising from mutation in or misexpression of certain developmentally critical genes, specifically homeotic genes. In animals, these developmental genes specifically control the development of organs on their anteroposterior axis. [1] In plants, however, the developmental genes affected by homeosis may control anything from the development of a stamen or petals to the development of chlorophyll. [2] Homeosis may be caused by mutations in Hox genes, found in animals, or others such as the MADS-box family in plants. Homeosis is a characteristic that has helped insects become as successful and diverse as they are. [3]

Contents

Homeotic mutations work by changing segment identity during development. For example, the Ultrabithorax genotype gives a phenotype wherein metathoracic and first abdominal segments become mesothoracic segments. [4] Another well-known example is Antennapedia : a gain-of-function allele causes legs to develop in the place of antennae. [5]

In botany, Rolf Sattler has revised the concept of homeosis (replacement) by his emphasis on partial homeosis in addition to complete homeosis; [6] this revision is now widely accepted.

Homeotic mutants in angiosperms are thought to be rare in the wild: in the annual plant Clarkia (Onagraceae), homeotic mutants are known where the petals are replaced by a second whorl of sepal-like organs, originating via a mutation governed by a single recessive gene. [7] The absence of lethal or deleterious consequences in floral mutants resulting in distinct morphological expressions has been a factor in the evolution of Clarkia, and perhaps also in many other plant groups. [8]

Homeotic mechanisms in animals

Following the work on homeotic mutants by Ed Lewis, [9] the phenomenology of homeosis in animals was further elaborated by discovery of a conserved DNA binding sequence present in many homeotic proteins. [10] Thus, the 60 amino acid DNA binding protein domain was named the homeodomain, while the 180 bp nucleotide sequence encoding it was named the homeobox. The homeobox gene clusters studied by Ed Lewis were named the Hox genes, although many more homeobox genes are encoded by animal genomes than those in the Hox gene clusters.

The homeotic-function of certain proteins was first postulated to be that of a "selector" as proposed by Antonio Garcia-Bellido. [11] By definition selectors were imagined to be (transcription factor) proteins that stably determined one of two possible cell fates for a cell and its cellular descendants in a tissue. While most animal homeotic functions are associated with homeobox-containing factors, not all homeotic proteins in animals are encoded by homeobox genes, and further not all homeobox genes are necessarily associated with homeotic functions or (mutant) phenotypes. The concept of homeotic selectors was further elaborated or at least qualified by Michael Akam in a so-called "post-selector gene" model that incorporated additional findings and "walked back" the "orthodoxy" of selector-dependent stable binary switches. [12]

The concept of tissue compartments is deeply intertwined with the selector model of homeosis because the selector-mediated maintenance of cell fate can be restricted into different organizational units of an animal's body plan. [13] In this context, newer insights into homeotic mechanisms were found by Albert Erives and colleagues by focusing on enhancer DNAs that are co-targeted by homeotic selectors and different combinations of developmental signals. [14] This work identifies a protein biochemical difference between the transcription factors that function as homeotic selectors versus the transcription factors that function as effectors of developmental signaling pathways, such as the Notch signaling pathway and the BMP signaling pathway. [14] This work proposes that homeotic selectors function to "license" enhancer DNAs in a restricted tissue compartment so that the enhancers are enabled to read-out developmental signals, which are then integrated via polyglutamine-mediated aggregation. [14]

Homeotic mechanisms in plants

Like the complex multicellularity seen in animals, the multicellularity of land plants is developmentally organized into tissue and organ units via transcription factor genes with homeotic effects. [15] Although plants have homeobox-containing genes, plant homeotic factors tend to possess MADS-box DNA binding domains. Animal genomes also possess a small number MADS-box factors. Thus, in the independent evolution of multicellularity in plants and animals, different eukaryotic transcription factor families were co-opted to serve homeotic functions. MADS-domain factors have been proposed to function as co-factors to more specialized factors and thereby help to determine organ identity. [15] This has been proposed to correspond more closely to the interpretation of animal homeotics outlined by Michael Akam. [16]

See also

Related Research Articles

Homeobox DNA pattern affecting anatomy development

A homeobox is a DNA sequence, around 180 base pairs long, found within genes that are involved in the regulation of patterns of anatomical development (morphogenesis) in animals, fungi, plants, and numerous single cell eukaryotes. Homeobox genes encode homeodomain protein products that are transcription factors sharing a characteristic protein fold structure that binds DNA to regulate expression of target genes. Homeodomain proteins regulate gene expression and cell differentiation during early embryonic development, thus mutations in homeobox genes can cause developmental disorders.

<i>Drosophila</i> embryogenesis Embryogenesis of the fruit fly Drosophila, a popular model system

Drosophila embryogenesis, the process by which Drosophila embryos form, is a favorite model system for genetics and developmental biology. The study of its embryogenesis unlocked the century-long puzzle of how development was controlled, creating the field of evolutionary developmental biology. The small size, short generation time, and large brood size make it ideal for genetic studies. Transparent embryos facilitate developmental studies. Drosophila melanogaster was introduced into the field of genetic experiments by Thomas Hunt Morgan in 1909.

Morphogen Biological substance that guides development by non-uniform distribution

A morphogen is a substance whose non-uniform distribution governs the pattern of tissue development in the process of morphogenesis or pattern formation, one of the core processes of developmental biology, establishing positions of the various specialized cell types within a tissue. More specifically, a morphogen is a signaling molecule that acts directly on cells to produce specific cellular responses depending on its local concentration.

Hox genes, a subset of homeobox genes, are a group of related genes that specify regions of the body plan of an embryo along the head-tail axis of animals. Hox proteins encode and specify the characteristics of 'position', ensuring that the correct structures form in the correct places of the body. For example, Hox genes in insects specify which appendages form on a segment, and Hox genes in vertebrates specify the types and shape of vertebrae that will form. In segmented animals, Hox proteins thus confer segmental or positional identity, but do not form the actual segments themselves.

<i>Antennapedia</i> Hox gene

Antennapedia is a Hox gene first discovered in Drosophila which controls the formation of legs during development. Loss-of-function mutations in the regulatory region of this gene result in the development of the second leg pair into ectopic antennae. By contrast gain-of-function alleles convert antennae into ectopic legs.

ABC model of flower development Model for genetics of flower development

The ABC model of flower development is a scientific model of the process by which flowering plants produce a pattern of gene expression in meristems that leads to the appearance of an organ oriented towards sexual reproduction, a flower. There are three physiological developments that must occur in order for this to take place: firstly, the plant must pass from sexual immaturity into a sexually mature state ; secondly, the transformation of the apical meristem's function from a vegetative meristem into a floral meristem or inflorescence; and finally the growth of the flower's individual organs. The latter phase has been modelled using the ABC model, which aims to describe the biological basis of the process from the perspective of molecular and developmental genetics.

Ultrabithorax

Ultrabithorax (Ubx) is a homeobox gene found in insects, and is used in the regulation of patterning in morphogenesis. There are many possible products of this gene, which function as transcription factors. Ubx is used in the specification of serially homologous structures, and is used at many levels of developmental hierarchies. In Drosophila melanogaster it is expressed in the third thoracic (T3) and first abdominal (A1) segments and represses wing formation. The Ubx gene regulates the decisions regarding the number of wings and legs the adult flies will have. The developmental role of the Ubx gene is determined by the splicing of its product, which takes place after translation of the gene. The specific splice factors of a particular cell allow the specific regulation of the developmental fate of that cell, by making different splice variants of transcription factors. In D. melanogaster, at least six different isoforms of Ubx exist.

HOXB6

Homeobox protein Hox-B6 is a protein that in humans is encoded by the HOXB6 gene.

HOXB5 Protein-coding gene in humans

Homeobox protein Hox-B5 is a protein that in humans is encoded by the HOXB5 gene.

HOXA7 Protein-coding gene in the species Homo sapiens

Homeobox protein Hox-A7 is a protein that in humans is encoded by the HOXA7 gene.

HOXA3 Protein-coding gene in the species Homo sapiens

Homeobox protein Hox-A3 is a protein that in humans is encoded by the HOXA3 gene.

In evolutionary developmental biology, homeotic genes are genes which regulate the development of anatomical structures in various organisms such as echinoderms, insects, mammals, and plants. Homeotic genes often encode transcription factor proteins, and these proteins affect development by regulating downstream gene networks involved in body patterning.

<i>Bithorax</i> complex

The Bithorax complex (BX-C) is one of two Drosophila melanogaster  homeotic gene complexes, located on the right arm of chromosome 3. It is responsible for the differentiation of the posterior two-thirds of the fly by the regulation of three genes within the complex: Ultrabithorax (Ubx), abdominal A (abd-A), and Abdominal B (Abd-B).

Homeotic selector genes confer segment identity in Drosophila. They encode homeodomain proteins which interact with Hox and other homeotic genes to initiate segment-specific gene regulation. Homeodomain proteins are transcription factors that share a DNA-binding domain called the homeodomain. Changes in the expression and function of homeotic genes are responsible for the changes in the morphology of the limbs of arthropods as well as in the axial skeletons of vertebrates. Mutations in homeotic selector genes do not lead to elimination of a segment or pattern, but instead cause the segment to develop incorrectly.

Zerknüllt is a gene in the Antennapedia complex of Drosophila and other insects, where it operates very differently from the canonical Hox genes in the same gene cluster. Comparison of Hox genes between species showed that the Zerknüllt gene evolved from one of the standard Hox genes in insects through accumulating many amino acid changes, changing expression pattern, losing ancestral function and gaining a new function.

Michael Levine is an American developmental and cell biologist at Princeton University, where he is the Director of the Lewis-Sigler Institute for Integrative Genomics and a Professor of Molecular Biology.

The Cdx gene family, also called caudal genes, are a group of genes found in many animal genomes. Cdx genes contain a homeobox DNA sequence and code for proteins that act as transcription factors. The gene after which the gene family is named is the caudal or cad gene of the fruitfly Drosophila melanogaster. The human genome has three Cdx genes, called CDX1, CDX2 and CDX4. The zebrafish has no cdx2 gene, but two copies of cdx1 and one copy of cdx4. The Cdx gene in the nematode Caenorhabditis elegans is called pal-1.

Hox genes in amphibians and reptiles

Hox genes play a massive role in some amphibians and reptiles in their ability to regenerate lost limbs, especially HoxA and HoxD genes.

Evo-devo gene toolkit

The evo-devo gene toolkit is the small subset of genes in an organism's genome whose products control the organism's embryonic development. Toolkit genes are central to the synthesis of molecular genetics, palaeontology, evolution and developmental biology in the science of evolutionary developmental biology (evo-devo). Many of them are ancient and highly conserved among animal phyla.

Thomas Charles Kaufman is an American geneticist. He is known for his work on the zeste-white region of the Drosophila X chromosome. He is currently a Distinguished Professor of biology at Indiana University, where he conducts his current research on Homeotic Genes in evolution and development.

References

  1. ↑ Hombría, James Castelli-Gair; Lovegrove, Bridget (2003-10-01). "Beyond homeosis—HOX function in morphogenesis and organogenesis". Differentiation. 71 (8): 461–476. doi:10.1046/j.1432-0436.2003.7108004.x. ISSN   1432-0436. PMID   14641327.
  2. ↑ Sattler, Rolf (October 1998). "Homeosis in Plants". American Journal of Botany. 75 (10): 1606–1617. doi:10.2307/2444710. JSTOR   2444710.
  3. ↑ Lodish et al., 2003. Molecular Cell Biology, 5th Edition. W.H. Freeman and Company, New York.[ page needed ]
  4. ↑ Nüsslein-Volhard, Christiane; Wieschaus, Eric (1980). "Mutations affecting segment number and polarity in Drosophila". Nature. 287 (5785): 795–801. Bibcode:1980Natur.287..795N. doi:10.1038/287795a0. PMID   6776413. S2CID   4337658.
  5. ↑ Schneuwly, Stephan; Klemenz, Roman; Gehring, Walter J. (1987). "Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia". Nature. 325 (6107): 816–818. Bibcode:1987Natur.325..816S. doi:10.1038/325816a0. PMID   3821869. S2CID   4320668.
  6. ↑ Sattler, R. (1988). "Homeosis in Plants". American Journal of Botany. 75 (10): 1606–1617. doi:10.2307/2444710. JSTOR   2444710.
  7. ↑ Ford, V. S.; Gottlieb, L. D. (1992). "Bicalyx is a natural homeotic floral variant". Nature. 358 (6388): 671–673. Bibcode:1992Natur.358..671F. doi:10.1038/358671a0. S2CID   4333498.
  8. ↑ Gottlieb, L. D. (1984). "Genetics and Morphological Evolution in Plants". The American Naturalist. 123 (5): 681–709. doi:10.1086/284231. JSTOR   2461245. S2CID   55441586.
  9. ↑ Lewis, EB (1978). "A gene complex controlling segmentation in Drosophila". Nature. 276 (5688): 565–570. Bibcode:1978Natur.276..565L. doi:10.1038/276565a0. PMID   103000. S2CID   2619820.
  10. ↑ McGinnis, W; Levine, MS; Hafen, E; Kuroiwa, A; Gehring, WJ (1984). "A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes". Nature. 308 (5958): 428–433. Bibcode:1984Natur.308..428M. doi:10.1038/308428a0. PMID   6323992. S2CID   4235713.
  11. ↑ Garcia-Bellido, A (1975). "Genetic control of wing disc development in Drosophila.". Ciba Foundation Symposium 29 ‐ Cell Patterning. Novartis Foundation Symposia. pp. 161––182. doi:10.1002/9780470720110.ch8. hdl: 10261/47429 . ISBN   9780470720110. PMID   1039909.
  12. ↑ Akam, M (1998). "Hox genes, homeosis and the evolution of segment identity: no need for hopeless monsters". International Journal of Developmental Biology. 42 (3): 445–451. PMID   9654030.
  13. ↑ Umetsu, D; Dahmann, C (2015). "Signals and mechanics shaping compartment boundaries in Drosophila". Wiley Interdiscip Rev Dev Biol. 4 (4): 407–417. doi:10.1002/wdev.178. PMID   25755098. S2CID   20256811.
  14. 1 2 3 Stroebele, E; Erives, A (2016). "Integration of Orthogonal Signaling by the Notch and Dpp Pathways in Drosophila". Genetics. 203 (1): 219–240. doi:10.1534/genetics.116.186791. PMC   4858776 . PMID   26975664.
  15. 1 2 Sablowski, R (2015). "Control of patterning, growth, and differentiation by floral organ identity genes". Journal of Experimental Botany. 66 (4): 1065–1073. doi: 10.1093/jxb/eru514 . PMID   25609826.
  16. ↑ Akam, M (1998). "Hox genes: From master genes to micromanagers". Current Biology. 8 (19): R676–8. doi: 10.1016/s0960-9822(98)70433-6 . PMID   9768351.
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