The shape and polarity of the C. elegans gonad is defined during early gonadogenesis by two somatic gonadal precursor cells, Z1 and Z4, and their descendants. Z1 and Z4 divide asymmetrically to establish the proximal-distal axes of the gonad and to generate regulatory leader cells that control organ shape. In this paper, we report that
pop-1, the C. elegans TCF/LEF-1 transcription factor, controls the first Z1/Z4 asymmetric division and hence controls proximal-distal axis formation. We have identified two
pop-1(Sys) alleles (for symmetrical sisters) that render the Z1/Z4 divisions symmetrical. The
pop-1(
q645) allele is fully penetrant for the Sys gonadogenesis defect in hermaphrodites, but affects male gonads weakly;
pop-1(
q645) alters a conserved amino acid in the beta-catenin binding domain. The
pop-1(
q624) allele is weakly penetrant for multiple defects and appears to be a partial loss-of-function mutation;
pop-1(
q624) alters a conserved amino acid in the HMG-box DNA binding domain. Zygotic
pop-1(RNAi) confirms the role of
pop-1 in Z1/Z4 asymmetry and reveals additional roles of
pop-1, including one in leader cell migration. Two other Wnt pathway regulators,
wrm-1 and
lit-1, have the same effect as
pop-1 on Z1/Z4 asymmetry. Therefore,
wrm-1 and
lit-1 are required for
pop-1 function, rather than opposing it as observed in the early embryo. We conclude that POP-1 controls the Z1/Z4 asymmetric division and thereby establishes the proximal-distal axes of the gonad. This control over proximal-distal polarity extends our view of Wnt signaling in C. elegans, which had previously been known to control anterior-posterior polarities.