The T-Box Transcription Factor SEA-1 Is an Autosomal Element of the X:A Signal that Determines C. elegans Sex

Powell, Jennifer R.; Jow, Margaret M.; Meyer, Barbara J

doi:10.1016/j.devcel.2005.06.009

Cited by 37 publications

(37 citation statements)

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“…Similar nuclear localization and timing of accumulation were observed for the XSE proteins and the ASE SEA-1 (Nicoll et al 1997;Carmi et al 1998;Powell et al 2005;, further implying an early role for SEA-2 in sex determination. The nuclear localization of the zinc finger SEA-2 protein and the presence of PQN protein-protein interaction motifs suggests that SEA-2 acts as a transcription factor that associates with other proteins to achieve transcriptional regulation (Michelitsch and Weissman 2000;Wolfe et al 2000).…”

Section: Sea-2 Accumulates In Nuclei Of Young Embryos During Sex Detesupporting

confidence: 60%

“…1B). Reducing the dose of ASEs in an XSE-deficient XX mutant was expected to restore the X:A balance and thereby reestablish dosage compensation and hermaphrodite viability (Powell et al 2005). The screen was designed to recover both dominant and recessive mutations.…”

Section: A Mos1 Transposon Screen Identified An Asementioning

confidence: 99%

“…1A; Powell et al 2005). This ASE, called SEA-1 (signal element on autosome), was identified as a suppressor of the XX-specific lethality caused by loss of XSEs.…”

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confidence: 99%

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Molecular antagonism between X-chromosome and autosome signals determines nematode sex

et al. 2013

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Sex is determined in Caenorhabditis elegans by the ratio of X chromosomes to the sets of autosomes, the X:A signal. A set of genes called X signal elements (XSEs) communicates X-chromosome dose by repressing the masculinizing sex determination switch gene xol-1 (XO lethal) in a dose-dependent manner. xol-1 is active in 1X:2A embryos (males) but repressed in 2X:2A embryos (hermaphrodites). Here we showed that the autosome dose is communicated by a set of autosomal signal elements (ASEs) that act in a cumulative, dose-dependent manner to counter XSEs by stimulating xol-1 transcription. We identified new ASEs and explored the biochemical basis by which ASEs antagonize XSEs to determine sex. Multiple antagonistic molecular interactions carried out on a single promoter explain how different X:A values elicit different sexual fates. XSEs (nuclear receptors and homeodomain proteins) and ASEs (T-box and zinc finger proteins) bind directly to several sites on xol-1 to counteract each other's activities and thereby regulate xol-1 transcription. Disrupting ASE-and XSE-binding sites in vivo recapitulated the misregulation of xol-1 transcription caused by disrupting cognate signal element genes. XSE-and ASE-binding sites are distinct and nonoverlapping, suggesting that direct competition for xol-1 binding is not how XSEs counter ASEs. Instead, XSEs likely antagonize ASEs by recruiting cofactors with reciprocal activities that induce opposite transcriptional states. Most ASE-and XSE-binding sites overlap xol-1's -1 nucleosome, which carries activating chromatin marks only when xol-1 is turned on. Coactivators and corepressors tethered by proteins similar to ASEs and XSEs are known to deposit and remove such marks. The concept of a sex signal comprising competing XSEs and ASEs arose as a theory for fruit flies a century ago. Ironically, while the recent work of others showed that the fly sex signal does not fit this simple paradigm, our work shows that the worm signal does.

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Section: Sea-2 Accumulates In Nuclei Of Young Embryos During Sex Detesupporting

confidence: 60%

Section: A Mos1 Transposon Screen Identified An Asementioning

confidence: 99%

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Molecular antagonism between X-chromosome and autosome signals determines nematode sex

et al. 2013

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“…The autosomal 1 component of the X:A signal is represented by at least two ASEs. SEA-1 (a T-box transcription factor) and SEA-2 oppose XSEs by activating xol-1 transcription (Powell et al 2005;P. Nix and B. Meyer, unpublished results).…”

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confidence: 97%

“…Only recently have molecular genetic approaches revealed the components of this X:A sex-determining signal. A set of X-linked genes called X signal elements (XSEs) relays X chromosome dose, and a set of autosomally linked genes called autosomal signal elements (ASEs) relays the ploidy (Akerib and Meyer 1994;Hodgkin et al 1994;Nicoll et al 1997;Carmi et al 1998;Carmi and Meyer 1999;Powell et al 2005;reviewed in Meyer 2005;Gladden and Meyer 2007, accompanying article in this issue). Both sets of elements communicate chromosome dose by controlling the sexdetermining gene xol-1 (XO lethal), the direct molecular target of the X:A signal.…”

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confidence: 99%

Revisiting the X:A Signal That Specifies Caenorhabditis elegans Sexual Fate

2007

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In Caenorhabditis elegans, sex is determined by the opposing actions of X-signal elements (XSEs) and autosomal signal elements (ASEs), which communicate the ratio of X chromosomes to sets of autosomes (X:A signal). This study delves more deeply into the mechanism by which XSEs transmit X chromosome dose. We determined the relative contributions of individual XSEs to the X:A signal and showed the order of XSE strength to be sex-1 . sex-2 . fox-1 . ceh-39 $ region 1 XSE. sex-1 exerts a more potent influence on sex determination and dosage compensation than any other XSE by functioning in two separate capacities in the pathway: sex-1 acts upstream as an XSE to repress xol-1 and downstream as an activator of hermaphrodite development and dosage compensation. Furthermore, the process of dosage compensation affects expression of the very XSEs that control it; XSEs become fully dosage compensated once sex is determined. The X:A signal is then equivalent between XO and XX animals, causing sexual differentiation to be controlled by genes downstream of xol-1 in the sex-determination pathway. Prior to the onset of dosage compensation, the difference in XSE expression between XX and XO embryos appears to be greater than twofold, making X chromosome counting a robust process.

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Sex Determination in the Caenorhabditis elegans Germline

Zanetti

Puoti

2012

Advances in Experimental Medicine and Biology

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How is sex determined? In the animal kingdom, there are diverse sets of mechanisms for determining organismal sex, with the predominant ones being chromosomally based, either a dominant-acting sex chromosome or the ratio of the number of X chromosome to autosomes, which lead to oocyte-producing females and sperm-producing males. The resulting germline sexual phenotype is often the logical consequence of somatic sex determination. In this respect however, the Caenorhabditis elegans hermaphrodite is different from mammals and Drosophila. In fact in the C. elegans hermaphrodite germline, male gametes are transiently produced in a female body during larval development. To override chromosomal signals, sex determination of germ cells strongly depends on post-transcriptional regulation. A pivotal role for male gamete production (spermatogenesis) is played by the fem-3 mRNA, which is controlled through FBF and other RNA-binding proteins or splicing factors. Thanks to its powerful genetics, transparent body, small size, and the ability to make sperm and oocytes within one individual, C. elegans represents an excellent system to investigate cellular differentiation and post-transcriptional control.

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The T-Box Transcription Factor SEA-1 Is an Autosomal Element of the X:A Signal that Determines C. elegans Sex

Cited by 37 publications

References 29 publications

Molecular antagonism between X-chromosome and autosome signals determines nematode sex

Molecular antagonism between X-chromosome and autosome signals determines nematode sex

Revisiting the X:A Signal That Specifies Caenorhabditis elegans Sexual Fate

Sex Determination in the Caenorhabditis elegans Germline

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