Variation and constraint in<i>Hox</i>gene evolution

Heffer, Alison; Xiang, Jie; Pick, Leslie

doi:10.1073/pnas.1210847110

Cited by 24 publications

(16 citation statements)

References 52 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The hierarchy of segmentation genes first discovered in Drosophila has been found in many insects, though the roles of some of these transcription factors have changed throughout evolution. Interestingly, many of these early developmental genes have a later function in embryogenesis or development (Heffer et al 2013), such as a shared role of ftz-f1 in molting across divergent taxa. These highly conserved roles may explain the long-term retention of these regulatory genes in insect genomes, despite variation in other functions.…”

Section: The Pair-rule Function Of Ftz-f1 Is Conserved Despite Variatmentioning

confidence: 99%

The evolving role of the orphan nuclear receptor ftz‐f1, a pair‐rule segmentation gene

Heffer

Grubbs

Mahaffey

et al. 2013

Evolution and Development

Self Cite

View full text Add to dashboard Cite

Segmentation is a critical developmental process that occurs by different mechanisms in diverse taxa. In insects, there are three common modes of embryogenesis-short-, intermediate-, and long-germ development-which differ in the number of segments specified at the blastoderm stage. While genes involved in segmentation have been extensively studied in the long-germ insect Drosophila melanogaster (Dm), it has been found that their expression and function in segmentation in short- and intermediate-germ insects often differ. Drosophila ftz-f1 encodes an orphan nuclear receptor that functions as a maternally expressed pair-rule segmentation gene, responsible for the formation of alternate body segments during Drosophila embryogenesis. Here we investigated the expression and function of ftz-f1 in the short-germ beetle, Tribolium castaneum (Tc). We found that Tc-ftz-f1 is expressed in stripes in Tribolium embryos. These stripes overlap alternate Tc-Engrailed (Tc-En) stripes, indicative of a pair-rule expression pattern. To test whether Tc-ftz-f1 has pair-rule function, we utilized embryonic RNAi, injecting double-stranded RNA corresponding to Tc-ftz-f1 coding or non-coding regions into early Tribolium embryos. Knockdown of Tc-ftz-f1 produced pair-rule segmentation defects, evidenced by loss of expression of alternate En stripes. In addition, a later role for Tc-ftz-f1 in cuticle formation was revealed. These results identify a new pair-rule gene in Tribolium and suggest that its role in segmentation may be shared among holometabolous insects. Interestingly, while Tc-ftz-f1 is expressed in pair-rule stripes, the gene is ubiquitously expressed in Drosophila embryos. Thus, the pair-rule function of ftz-f1 is conserved despite differences in expression patterns of ftz-f1 genes in different lineages. This suggests that ftz-f1 expression changed after the divergence of lineages leading to extant beetles and flies, likely due to differences in cis-regulatory sequences. We propose that the dependence of Dm-Ftz-F1 on interaction with the homeodomain protein Ftz which is expressed in stripes in Drosophila, loosened constraints on Dm-ftz-f1 expression, allowing for ubiquitous expression of this pair-rule gene in Drosophila.

show abstract

Section: The Pair-rule Function Of Ftz-f1 Is Conserved Despite Variatmentioning

confidence: 99%

The evolving role of the orphan nuclear receptor ftz‐f1, a pair‐rule segmentation gene

Heffer

Grubbs

Mahaffey

et al. 2013

Evolution and Development

Self Cite

View full text Add to dashboard Cite

show abstract

“…For example, fushi tarazu and oskar may have initially functioned in the central nervous system but later became involved in the patterning of the early embryo, as seen today in Drosophila (Ewen-Campen et al 2012 ;Heffer et al 2013 ). The evolution of new functional roles has been documented to occur even if the phenotypic traits previously controlled by a gene are subjected to strong stabilizing selection; this is why the evolution of new functions in a lineage of orthologous genes (i.e., independent from gene duplications) has been called developmental system drift (DSD) (True and Haag 2001 ;Haag 2014 ).…”

Section: Evolving Gene Functionsmentioning

confidence: 97%

EvoDevo and Its Significance for Animal Evolution and Phylogeny

Minelli

2015

Evolutionary Developmental Biology of Invertebrates 1

View full text Add to dashboard Cite

“…Thus, expression in the CNS appeared to be the only stable feature of ftz , which may be the feature that provides selective pressure against its total loss. We reasoned that if ftz CNS function is the broadly conserved essential function of this gene, then neither motif that varies in different Ftz proteins would be required for its CNS role (Heffer et al 2013b). …”

Section: Why Is Ftz Present In All Arthropod Genomes?mentioning

confidence: 99%

“…Rescue of Eve expression in RP2 neurons is shown (percent rescue) for different transgenes, as indicated. From Heffer et al (2013b).…”

Section: Figmentioning

confidence: 99%

Hox genes, evo-devo, and the case of the ftz gene

Pick

2015

Chromosoma

Self Cite

View full text Add to dashboard Cite

The discovery of the broad conservation of embryonic regulatory genes across animal phyla, launched by the cloning of homeotic genes in the 1980s, was a founding event in the field of evolutionary developmental biology (evo-devo). While it had long been known that fundamental cellular processes, commonly referred to as housekeeping functions, are shared by animals and plants across the planet—processes such as the storage of information in genomic DNA, transcription, translation and the machinery for these processes, universal codon usage, and metabolic enzymes—Hox genes were different: mutations in these genes caused “bizarre” homeotic transformations of insect body parts that were certainly interesting but were expected to be idiosyncratic. The isolation of the genes responsible for these bizarre phenotypes turned out to be highly conserved Hox genes that play roles in embryonic patterning throughout Metazoa. How Hox genes have changed to promote the development of diverse body plans remains a central issue of the field of evo-devo today. For this Memorial article series, I review events around the discovery of the broad evolutionary conservation of Hox genes and the impact of this discovery on the field of developmental biology. I highlight studies carried out in Walter Gehring's lab and by former lab members that have continued to push the field forward, raising new questions and forging new approaches to understand the evolution of developmental mechanisms.

show abstract

Variation and constraint inHoxgene evolution

Cited by 24 publications

References 52 publications

The evolving role of the orphan nuclear receptor ftz‐f1, a pair‐rule segmentation gene

The evolving role of the orphan nuclear receptor ftz‐f1, a pair‐rule segmentation gene

EvoDevo and Its Significance for Animal Evolution and Phylogeny

Hox genes, evo-devo, and the case of the ftz gene

Contact Info

Product

Resources

About