scholarly journals Hox genes are essential for the development of eyespots in Bicyclus anynana butterflies

Genetics ◽  
2020 ◽  
Vol 217 (1) ◽  
Author(s):  
Yuji Matsuoka ◽  
Antónia Monteiro
Keyword(s):  
Hox Genes ◽  
Bicyclus Anynana ◽  
Hox Gene ◽  
Novel Traits ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

Abstract The eyespot patterns found on the wings of nymphalid butterflies are novel traits that originated first in hindwings and subsequently in forewings, suggesting that eyespot development might be dependent on Hox genes. Hindwings differ from forewings in the expression of Ultrabithorax (Ubx), but the function of this Hox gene in eyespot development as well as that of another Hox gene Antennapedia (Antp), expressed specifically in eyespots centers on both wings, are still unclear. We used CRISPR-Cas9 to target both genes in Bicyclus anynana butterflies. We show that Antp is essential for eyespot development on the forewings and for the differentiation of white centers and larger eyespots on hindwings, whereas Ubx is essential not only for the development of at least some hindwing eyespots but also for repressing the size of other eyespots. Additionally, Antp is essential for the development of silver scales in male wings. In summary, Antp and Ubx, in addition to their conserved roles in modifying serially homologous segments along the anterior–posterior axis of insects, have acquired a novel role in promoting the development of a new set of serial homologs, the eyespot patterns, in both forewings (Antp) and hindwings (Antp and Ubx) of B. anynana butterflies. We propose that the peculiar pattern of eyespot origins on hindwings first, followed by forewings, could be due to an initial co-option of Ubx into eyespot development followed by a later, partially redundant, co-option of Antp into the same network.

scholarly journals Hox genes are essential for the development of novel serial homologous eyespots on the wings of Bicyclus anynana butterflies

2019 ◽  
Author(s):  
Yuji Matsuoka ◽  
Antónia Monteiro
Keyword(s):  
Hox Genes ◽  
Bicyclus Anynana ◽  
Hox Gene ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

AbstractThe eyespot patterns found on the wings of nymphalid butterflies are novel serial homologous traits that originated first in hindwings and subsequently in forewings, suggesting that eyespot development might be dependent on Hox genes. Hindwings differ from forewings in the expression of Ultrabithorax (Ubx), but the function of this Hox gene in eyespot development as well as that of another Hox gene Antennapedia (Antp), expressed specifically in eyespots centers on both wings, are still unclear. We used CRISPR-Cas9 to target both genes in Bicyclus anynana butterflies. We show that Antp is essential for eyespot development on the forewings and for the differentiation of white centers and larger eyespots on hindwings, whereas Ubx is essential for the development of at least some hindwing eyespots but also for repressing the size of other eyespots. Additionally, Antp is essential for the development of silver scales in male wings. In summary, Antp and Ubx, in addition to their conserved roles in modifying serial homologous traits along the anterior-posterior axis of animals, have acquired a novel role in promoting the development of a new set of serial homologs, the eyespot patterns, in both forewings (Antp) and hindwings (Antp and Ubx) of B. anynana butterflies. We propose that the peculiar pattern of eyespot origins on hindwings first, followed by forewings, could be due to an initial co-option of Ubx into eyespot development, followed by a later, partially redundant co-option of Antp into the same network.

scholarly journals Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
David A. Salamanca-Díaz ◽  
Andrew D. Calcino ◽  
André L. de Oliveira ◽  
Andreas Wanninger
Keyword(s):  
Gene Expression ◽  
Morphological Traits ◽  
Hox Genes ◽  
Current Data ◽  
Phenotypic Traits ◽  
Parahox Gene ◽  
Hox Gene ◽  
Morphological Novelties ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

AbstractHox genes are key developmental regulators that are involved in establishing morphological features during animal ontogeny. They are commonly expressed along the anterior–posterior axis in a staggered, or collinear, fashion. In mollusks, the repertoire of body plans is widely diverse and current data suggest their involvement during development of landmark morphological traits in Conchifera, one of the two major lineages that comprises those taxa that originated from a uni-shelled ancestor (Monoplacophora, Gastropoda, Cephalopoda, Scaphopoda, Bivalvia). For most clades, and bivalves in particular, data on Hox gene expression throughout ontogeny are scarce. We thus investigated Hox expression during development of the quagga mussel, Dreissena rostriformis, to elucidate to which degree they might contribute to specific phenotypic traits as in other conchiferans. The Hox/ParaHox complement of Mollusca typically comprises 14 genes, 13 of which are present in bivalve genomes including Dreissena. We describe here expression of 9 Hox genes and the ParaHox gene Xlox during Dreissena development. Hox expression in Dreissena is first detected in the gastrula stage with widely overlapping expression domains of most genes. In the trochophore stage, Hox gene expression shifts towards more compact, largely mesodermal domains. Only few of these domains can be assigned to specific developing morphological structures such as Hox1 in the shell field and Xlox in the hindgut. We did not find traces of spatial or temporal staggered expression of Hox genes in Dreissena. Our data support the notion that Hox gene expression has been coopted independently, and to varying degrees, into lineage-specific structures in the respective conchiferan clades. The non-collinear mode of Hox expression in Dreissena might be a result of the low degree of body plan regionalization along the bivalve anterior–posterior axis as exemplified by the lack of key morphological traits such as a distinct head, cephalic tentacles, radula apparatus, and a simplified central nervous system.

Hox genes and the evolution of vertebrate axial morphology

Development ◽  
1995 ◽  
Vol 121 (2) ◽  
pp. 333-346 ◽  
Author(s):  
A.C. Burke ◽  
C.E. Nelson ◽  
B.A. Morgan ◽  
C. Tabin
Keyword(s):  
Hox Genes ◽  
Cervical Vertebrae ◽  
Homeobox Gene ◽  
Paraxial Mesoderm ◽  
Thoracic Vertebrae ◽  
Homeotic Genes ◽  
Evolutionary Variation ◽  
Axial Morphology ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

A common form of evolutionary variation between vertebrate taxa is the different numbers of segments that contribute to various regions of the anterior-posterior axis; cervical vertebrae, thoracic vertebrae, etc. The term ‘transposition’ is used to describe this phenomenon. Genetic experiments with homeotic genes in mice have demonstrated that Hox genes are in part responsible for the specification of segmental identity along the anterior-posterior axis, and it has been proposed that an axial Hox code determines the morphology of individual vertebrae (Kessel, M. and Gruss, P. (1990) Science 249, 347–379). This paper presents a comparative study of the developmental patterns of homeobox gene expression and developmental morphology between animals that have homologous regulatory genes but different morphologies. The axial expression boundaries of 23 Hox genes were examined in the paraxial mesoderm of chick, and 16 in mouse embryos by in situ hybridization and immunolocalization techniques. Hox gene anterior expression boundaries were found to be transposed in concert with morphological boundaries. This data contributes a mechanistic level to the assumed homology of these regions in vertebrates. The recognition of mechanistic homology supports the historical homology of basic patterning mechanisms between all organisms that share these genes.

scholarly journals A re-inducible gap gene cascade patterns the anterior-posterior axis of insects in a threshold-free fashion

2018 ◽  
Author(s):  
Alena Boos ◽  
Jutta Distler ◽  
Heike Rudolf ◽  
Martin Klingler ◽  
Ezzat El-Sherif
Keyword(s):  
Gene Network ◽  
Hox Genes ◽  
Expression Patterns ◽  
Fruit Fly ◽  
Regulation Mechanism ◽  
Gap Gene ◽  
Speed Regulation ◽  
Gap Genes ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

AbstractGap genes mediate the division of the anterior-posterior axis of insects into different fates through regulating downstream hox genes. Decades of tinkering the segmentation gene network of the long-germ fruit fly Drosophila melanogaster led to the conclusion that gap genes are regulated (at least initially) through a threshold-based French Flag model, guided by both anteriorly- and posteriorly-localized morphogen gradients. In this paper, we show that the expression patterns of gap genes in the intermediate-germ beetle Tribolium castaneum are mediated by a threshold-free ‘Speed Regulation’ mechanism, in which the speed of a genetic cascade of gap genes is regulated by a posterior gradient of the transcription factor Caudal. We show this by re-inducing the leading gap gene (namely, hunchback) resulting in the re-induction of the gap gene cascade at arbitrary points in time. This demonstrates that the gap gene network is self-regulatory and is primarily under the control of a posterior speed regulator in Tribolium and possibly all insects.

scholarly journals Hox genes regulate asexual reproductive behavior and tissue segmentation in adult animals

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Christopher P. Arnold ◽  
Analí Migueles Lozano ◽  
Frederick G. Mann ◽  
Stephanie H. Nowotarski ◽  
Julianna O. Haug ◽  
...  
Keyword(s):  
Asexual Reproduction ◽  
Hox Genes ◽  
Adult Stage ◽  
Tissue Segmentation ◽  
Hox Gene ◽  
Downstream Effector ◽  
Effector Genes ◽  
And Behavior ◽  
Insight Into ◽  
Anterior Posterior

AbstractHox genes are highly conserved transcription factors renowned for their roles in the segmental patterning of the embryonic anterior-posterior (A/P) axis. We report functions for Hox genes in A/P tissue segmentation and transverse fission behavior underlying asexual reproduction in adult planarian flatworms, Schmidtea mediterranea. Silencing of each of the Hox family members identifies 5 Hox genes required for asexual reproduction. Among these, silencing of hox3 genes results in supernumerary fission segments, while silencing of post2b eliminates segmentation altogether. The opposing roles of hox3 and post2b in segmentation are paralleled in their respective regulation of fission behavior. Silencing of hox3 increases the frequency of fission behavior initiation while silencing of post2b eliminates fission behavior entirely. Furthermore, we identify a network of downstream effector genes mediating Hox gene functions, providing insight into their respective mechanisms of action. In particular, we resolve roles for post2b and effector genes in the functions of the marginal adhesive organ in fission behavior regulation. Collectively, our study establishes adult stage roles for Hox genes in the regulation of tissue segmentation and behavior associated with asexual reproduction.

scholarly journals A re-inducible gap gene cascade patterns the anterior–posterior axis of insects in a threshold-free fashion

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Alena Boos ◽  
Jutta Distler ◽  
Heike Rudolf ◽  
Martin Klingler ◽  
Ezzat El-Sherif
Keyword(s):  
Gene Network ◽  
Hox Genes ◽  
Morphogen Gradient ◽  
Regulation Mechanism ◽  
Morphogen Gradients ◽  
Gap Gene ◽  
Speed Regulation ◽  
Gap Genes ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

Gap genes mediate the division of the anterior-posterior axis of insects into different fates through regulating downstream hox genes. Decades of tinkering the segmentation gene network of Drosophila melanogaster led to the conclusion that gap genes are regulated (at least initially) through a threshold-based mechanism, guided by both anteriorly- and posteriorly-localized morphogen gradients. In this paper, we show that the response of the gap gene network in the beetle Tribolium castaneum upon perturbation is consistent with a threshold-free ‘Speed Regulation’ mechanism, in which the speed of a genetic cascade of gap genes is regulated by a posterior morphogen gradient. We show this by re-inducing the leading gap gene (namely, hunchback) resulting in the re-induction of the gap gene cascade at arbitrary points in time. This demonstrates that the gap gene network is self-regulatory and is primarily under the control of a posterior regulator in Tribolium and possibly other short/intermediate-germ insects.

scholarly journals Disappearance of Temporal Collinearity in Vertebrates and its Eventual Reappearance

2021 ◽  
Author(s):  
Spyros Papageorgiou
Keyword(s):  
Hox Genes ◽  
Hox Cluster ◽  
Spatial Dimensions ◽  
Anterior Posterior ◽  
As If ◽  
Anterior Posterior Axis

It was observed that a cluster of ordered genes (Hox1, Hox2, Hox3,…) in the genome are activated in the ontogenetic units (1, 2, 3,…) of an embryo along the Anterior/Posterior axis following the same order of the Hox genes. This Spatial Collinearity (SC) is very strange since it correlates events of very different spatial dimensions. It was later observed in vertebrates, that, in the above ordering, first is Hox1expressed in ontogenetic unit 1, followed later by Hox2 in unit 2, and even later Hox3 in unit 3….This temporal collinearity (TC) is an enigma and even to-day is explored in depth. In 1999 T. Kondo and D. Duboule, after posterior upstream extended DNA excisions , concluded that the Hox cluster behaves ‘as if’ TC disappears. Here the consideration of TC really disappearing is taken face value and its repercussions are analyzed. Furthermore, an experiment is proposed to test TC disappearance. An outcome of this experiment could be the reappearance (partial or total) of TC.

scholarly journals Staggered Hox expression is more widespread among molluscs than previously appreciated

2018 ◽  
Vol 285 (1888) ◽  
pp. 20181513 ◽  
Author(s):  
Tim Wollesen ◽  
Sonia Victoria Rodríguez Monje ◽  
André Luiz de Oliveira ◽  
Andreas Wanninger
Keyword(s):  
Gene Expression ◽  
Morphological Traits ◽  
Hox Genes ◽  
Developmental Stages ◽  
Early Stage ◽  
Genomic Data ◽  
Published Data ◽  
Hox Gene ◽  
The Central Nervous System ◽  
Anterior Posterior

Hox genes are expressed along the anterior–posterior body axis in a colinear fashion in the majority of bilaterians. Contrary to polyplacophorans, a group of aculiferan molluscs with conserved ancestral molluscan features, gastropods and cephalopods deviate from this pattern by expressing Hox genes in distinct morphological structures and not in a staggered fashion. Among conchiferans, scaphopods exhibit many similarities with gastropods, cephalopods and bivalves, however, the molecular developmental underpinnings of these similar traits remain unknown. We investigated Hox gene expression in developmental stages of the scaphopod Antalis entalis to elucidate whether these genes are involved in patterning morphological traits shared by their kin conchiferans. Scaphopod Hox genes are predominantly expressed in the foot and mantle but also in the central nervous system. Surprisingly, the scaphopod mid-stage trochophore exhibits a near-to staggered expression of all nine Hox genes identified. Temporal colinearity was not found and early-stage and late-stage trochophores, as well as postmetamorphic individuals, do not show any apparent traces of staggered expression. In these stages, Hox genes are expressed in distinct morphological structures such as the cerebral and pedal ganglia and in the shell field of early-stage trochophores. Interestingly, a re-evaluation of previously published data on early-stage cephalopod embryos and of the gastropod pre-torsional veliger shows that these developmental stages exhibit traces of staggered Hox expression. Considering our results and all gene expression and genomic data available for molluscs as well as other bilaterians, we suggest a last common molluscan ancestor with colinear Hox expression in predominantly ectodermal tissues along the anterior–posterior axis. Subsequently, certain Hox genes have been co-opted into the patterning process of distinct structures (apical organ or prototroch) in conchiferans.

scholarly journals Dorsoventral dissociation of Hox gene expression underpins the diversification of molluscs

2019 ◽  
Author(s):  
Pin Huan ◽  
Qian Wang ◽  
Sujian Tan ◽  
Baozhong Liu
Keyword(s):  
Gene Expression ◽  
Hox Genes ◽  
Expression Patterns ◽  
Ventral Side ◽  
Shell Formation ◽  
Dynamic Changes ◽  
Hox Gene ◽  
Expression Model ◽  
Almost All ◽  
Anterior Posterior

AbstractUnlike the Hox genes in arthropods and vertebrates, those in molluscs show diverse expression patterns and, with some exceptions, have generally been described as lacking the canonical staggered pattern along the anterior-posterior (AP) axis. This difference is unexpected given that almost all molluscs share highly conserved early development. Here, we show that molluscan Hox expression can undergo dynamic changes, which may explain why previous research observed different expression patterns. Moreover, we reveal that a key character of molluscan Hox expression is that the dorsal and ventral expression is dissociated. We then deduce a generalized molluscan Hox expression model, including conserved staggered Hox expression in the neuroectoderm on the ventral side and lineage-specific dorsal expression that strongly correlates with shell formation. This generalized model clarifies a long-standing debate over whether molluscs possess staggered Hox expression and it can be used to explain the diversification of molluscs. In this scenario, the dorsoventral dissociation of Hox expression allows lineage-specific dorsal and ventral patterning in different clades, which may have permitted the evolution of diverse body plans in different molluscan clades.

Sign in / Sign up

Export Citation Format

Share Document