macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis

Abstract

Maternal information stored in particular regions of the egg cytoplasm has an important function in the determination of developmental fate during early animal development. Ascidians show mosaic development; such autonomous development has been taken as evidence that prelocalized ooplasmic factors specify tissue precursor cells during embryogenesis. Interest has been concentrated on the mechanisms underlying the formation of muscle cells in the tail, as yellow-coloured myoplasm in eggs is preferentially segregated into muscle-lineage blastomeres. Here we show that maternal messenger RNA of the macho-1 gene is a determinant of muscle fate in the ascidian Halocynthia roretzi. The macho-1 mRNA encodes a zinc-finger protein, and the mRNA is localized to the myoplasm of eggs. Depletion of the mRNA specifically resulted in the loss of primary muscle cells in the tail, as shown by the expression of muscle-specific molecular markers. The myoplasm of macho-1-deficient eggs lost its ability to promote muscle formation. Injection of synthesized macho-1 mRNA caused ectopic muscle formation in non-muscle-lineage cells. Our results indicate that macho-1 maybe both required and sufficient for specification of muscle fate, and that the mRNA is a genuine, localized muscle determinant.

An initial blueprint for myogenic differentiation

“…As noted above, MEF2 and SRF were identified as likely coregulators, in agreement with previous reports (Groisman et al 1996;Molkentin and Olson 1996). Remarkably, our analyses also identified TEAD4, Six1, and Zic1 (a GLIrelated transcription factor that appears to determine muscle lineage in ascidians) (Nishida and Sawada 2001;Imai et al 2002) as additional, novel candidate coregulators (Table 3), reinforcing our factor binding studies and published observations (Fig. 4B).…”

A zinc finger transcription factor, ZicL, is a direct activator ofBrachyuryin the notochord specification ofCiona intestinalis

“…Although the details of ZicL function in the specification and subsequent differentiation of nerve cord cells are obscure, ZicL function in B-line muscle cells appears to be coordinated with the function of another zinc finger transcription factor gene, Ci-macho1 (Satou et al, 2002). Halocynthia macho-1 appears to have the potential to promote the entire genetic cascade for muscle cell differentiation (Nishida and Sawada, 2001). On the other hand, the potential of Ci-macho1 to promote the genetic cascade for muscle cell differentiation appears partial, and requires the collaborative functioning of ZicL (Imai et al, 2002c).…”

“…The notochord-specific expression of Hr-Bra depends on a module between -289 and -250 of the upstream sequence of the gene. The Halocynthia genome also contains two types of Zic-related genes, macho-1 (Nishida and Sawada, 2001) and zicN (Wada and Saiga, 2002). HrzicN is expressed in blastomeres of muscle, notochord, anterior mesenchyme and nerve cord, and the gene seems to be responsible for the differentiation of these types of cell, and a model in which HrzicN may activate Hr-Bra together with FGF/BMP signaling pathway is proposed (Wada and Saiga, 2002).…”

Fertilisation calcium signals in the ascidian egg

“…The determinants as well as numerous other maternal mRNAs (called PEM or postplasmic RNAs, Sasakura et al, 2000) are contained in the contraction pole and they will experience the largest variations in [Ca 2+ ] c setting up a periodic Ca 2+ gradient highest in the vegetal hemisphere. It is remarkable that the recently identified muscle determinant (macho1 mRNA, Nishida and Sawada, 2001) is in fact located on the ER which accumulates in the contraction pole . The close proximity of these determinants with the origin of the meiosis II Ca 2+ waves suggests that some Ca 2+ dependant processes may play a role in the maturation or priming of these determinants.…”