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mab-31 and the TGF-beta pathway act in the ray lineage to pattern C. elegans male sensory rays.

Wong YF, Sheng Q, Chung JW, Chan JK, Chow KL - BMC Dev. Biol. (2010)

Bottom Line: Both mab-31 and sma-6 are required in ray lineage at the late larval stages.They act upstream of C. elegans Pax-6 homolog and repress its function.These findings suggested mab-31 is a key factor that can integrate TFG-beta signals in male sensory ray lineage to define organ identity.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong.

ABSTRACT

Background: C. elegans TGF-beta-like Sma/Mab signaling pathway regulates both body size and sensory ray patterning. Most of the components in this pathway were initially identified by genetic screens based on the small body phenotype, and many of these mutants display sensory ray patterning defect. At the cellular level, little is known about how and where these components work although ray structural cell has been implicated as one of the targets. Based on the specific ray patterning abnormality, we aim to identify by RNAi approach additional components that function specifically in the ray lineage to elucidate the regulatory role of TGF-beta signaling in ray differentiation.

Result: We report here the characterization of a new member of the Sma/Mab pathway, mab-31, recovered from a genome-wide RNAi screen. mab-31 mutants showed ray cell cluster patterning defect and mis-specification of the ray identity. mab-31 encodes a nuclear protein expressed in descendants of ray precursor cells impacting on the ray cell's clustering properties, orientation of cell division plane, and fusion of structural cells. Genetic experiments also establish its relationship with other Sma/Mab pathway components and transcription factors acting upstream and downstream of the signaling event.

Conclusion: mab-31 function is indispensable in Sma/Mab signal recipient cells during sensory rays specification. Both mab-31 and sma-6 are required in ray lineage at the late larval stages. They act upstream of C. elegans Pax-6 homolog and repress its function. These findings suggested mab-31 is a key factor that can integrate TFG-beta signals in male sensory ray lineage to define organ identity.

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Abnormal ray clustering patterns of mutants in Sma/Mab pathway. The formation of daughter cells from ray precursor cells (Rn, n = 1-9) in different developmental stages was examined with apical junction markers ajm-1::gfp. Between mid-L3 and mid-L4 stage, Rn cells were divided by a stereotyped lineage pattern giving rise to ray cell groups (RCG) and were subsequently assembled (A-D) in wild-type animals. No abnormality is noted in the division of Rn.a and Rn.p cells in sma-6 (E) and mab-31 (I) mutants. In wild-type male, R7.aa and R7.ap are born at the dorsal side of R7.p (B). However, in sma-6 (F) and mab-31 (J) mutants, both R7.aa cells and R7.ap cells are skewed towards the ventral side of R7.p cell. The abnormal R7.aa and R7.ap reside next to the R6.aa and R6.ap cells. RCGs were well-separated in wild-type male tail (C) but not in both in sma-6 (G) and mab-31 (K) mutants. At a later stage, cellular components of ray 6 and ray 7 are clustered in close proximity and their structural cells are fused together (arrows in H and L). Lateral view, left side upwards. Hour (hrs) post-hatching at 20°C. Scale bar = 10 μm.
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Figure 2: Abnormal ray clustering patterns of mutants in Sma/Mab pathway. The formation of daughter cells from ray precursor cells (Rn, n = 1-9) in different developmental stages was examined with apical junction markers ajm-1::gfp. Between mid-L3 and mid-L4 stage, Rn cells were divided by a stereotyped lineage pattern giving rise to ray cell groups (RCG) and were subsequently assembled (A-D) in wild-type animals. No abnormality is noted in the division of Rn.a and Rn.p cells in sma-6 (E) and mab-31 (I) mutants. In wild-type male, R7.aa and R7.ap are born at the dorsal side of R7.p (B). However, in sma-6 (F) and mab-31 (J) mutants, both R7.aa cells and R7.ap cells are skewed towards the ventral side of R7.p cell. The abnormal R7.aa and R7.ap reside next to the R6.aa and R6.ap cells. RCGs were well-separated in wild-type male tail (C) but not in both in sma-6 (G) and mab-31 (K) mutants. At a later stage, cellular components of ray 6 and ray 7 are clustered in close proximity and their structural cells are fused together (arrows in H and L). Lateral view, left side upwards. Hour (hrs) post-hatching at 20°C. Scale bar = 10 μm.

Mentions: Ray identity determination is a dynamic process of ray precursor (Rn) cells differentiation in late larval stages of C. elegans male development. The underlying process of cellular specification of Rn cells is not well understood. Therefore, we examined and compared ray cell cluster profiles of wild-type, sma-6(wk7), and mab-31(tm2718) animals. To achieve this, we traced the Rn cells lineage with an apical junction marker ajm-1::GFP. We were particularly interested in differentiation of R6 and R7, since rays 6-7 fusion was the most obvious phenotype in both mab-31 and other sma mutants. When R(6/7).a and R(6/7).p cells were born, there was no detectable difference in wild-type (Figure 2A), sma-6 (Figure 2E) and mab-31 mutants (Figure 2I). In the wild-type animal, R7.aa and R7.ap (descendents of R7.a) were produced along the A-P axis and stayed on the dorsal side of R7.p (Figure 2B). However, in sma-6 and mab-31 mutants, these two cells were present on the ventral side of R7.p after their birth (Figure 2F and 2J). In these mutants, the abnormal ray cell group derived from R7 sat next to that of R6 (Figure 2G and 2K) and subsequently, their structural cells were juxtaposed to each other and were fused together (Figure 2H and 2L). However, no cellular abnormality was observed in differentiation of R6a.a, R6a.p. or R6.p cells, in both mutants, as compared with those in wild-type animals. The defect in rays 6-7 fusion involved mis-localization of ray 7 precursors to ray 6 precursors during ray identity determination window at the L4 larval stage. Our observation suggested that both sma-6 and mab-31 mutants have a wild-type ray lineage with ray precursor cells born at the right time. The defects in these mutants were simply due to transformation of the ray cell identity, which dictates the cell cluster's positioning with respect to other ray cell groups. Indeed, similar defects were subsequently observed in other sma mutants (sma-4 and dbl-1, data not shown) also, inferring that the mab-31 gene probably acts in the same canonical dbl/sma pathway.


mab-31 and the TGF-beta pathway act in the ray lineage to pattern C. elegans male sensory rays.

Wong YF, Sheng Q, Chung JW, Chan JK, Chow KL - BMC Dev. Biol. (2010)

Abnormal ray clustering patterns of mutants in Sma/Mab pathway. The formation of daughter cells from ray precursor cells (Rn, n = 1-9) in different developmental stages was examined with apical junction markers ajm-1::gfp. Between mid-L3 and mid-L4 stage, Rn cells were divided by a stereotyped lineage pattern giving rise to ray cell groups (RCG) and were subsequently assembled (A-D) in wild-type animals. No abnormality is noted in the division of Rn.a and Rn.p cells in sma-6 (E) and mab-31 (I) mutants. In wild-type male, R7.aa and R7.ap are born at the dorsal side of R7.p (B). However, in sma-6 (F) and mab-31 (J) mutants, both R7.aa cells and R7.ap cells are skewed towards the ventral side of R7.p cell. The abnormal R7.aa and R7.ap reside next to the R6.aa and R6.ap cells. RCGs were well-separated in wild-type male tail (C) but not in both in sma-6 (G) and mab-31 (K) mutants. At a later stage, cellular components of ray 6 and ray 7 are clustered in close proximity and their structural cells are fused together (arrows in H and L). Lateral view, left side upwards. Hour (hrs) post-hatching at 20°C. Scale bar = 10 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 2: Abnormal ray clustering patterns of mutants in Sma/Mab pathway. The formation of daughter cells from ray precursor cells (Rn, n = 1-9) in different developmental stages was examined with apical junction markers ajm-1::gfp. Between mid-L3 and mid-L4 stage, Rn cells were divided by a stereotyped lineage pattern giving rise to ray cell groups (RCG) and were subsequently assembled (A-D) in wild-type animals. No abnormality is noted in the division of Rn.a and Rn.p cells in sma-6 (E) and mab-31 (I) mutants. In wild-type male, R7.aa and R7.ap are born at the dorsal side of R7.p (B). However, in sma-6 (F) and mab-31 (J) mutants, both R7.aa cells and R7.ap cells are skewed towards the ventral side of R7.p cell. The abnormal R7.aa and R7.ap reside next to the R6.aa and R6.ap cells. RCGs were well-separated in wild-type male tail (C) but not in both in sma-6 (G) and mab-31 (K) mutants. At a later stage, cellular components of ray 6 and ray 7 are clustered in close proximity and their structural cells are fused together (arrows in H and L). Lateral view, left side upwards. Hour (hrs) post-hatching at 20°C. Scale bar = 10 μm.
Mentions: Ray identity determination is a dynamic process of ray precursor (Rn) cells differentiation in late larval stages of C. elegans male development. The underlying process of cellular specification of Rn cells is not well understood. Therefore, we examined and compared ray cell cluster profiles of wild-type, sma-6(wk7), and mab-31(tm2718) animals. To achieve this, we traced the Rn cells lineage with an apical junction marker ajm-1::GFP. We were particularly interested in differentiation of R6 and R7, since rays 6-7 fusion was the most obvious phenotype in both mab-31 and other sma mutants. When R(6/7).a and R(6/7).p cells were born, there was no detectable difference in wild-type (Figure 2A), sma-6 (Figure 2E) and mab-31 mutants (Figure 2I). In the wild-type animal, R7.aa and R7.ap (descendents of R7.a) were produced along the A-P axis and stayed on the dorsal side of R7.p (Figure 2B). However, in sma-6 and mab-31 mutants, these two cells were present on the ventral side of R7.p after their birth (Figure 2F and 2J). In these mutants, the abnormal ray cell group derived from R7 sat next to that of R6 (Figure 2G and 2K) and subsequently, their structural cells were juxtaposed to each other and were fused together (Figure 2H and 2L). However, no cellular abnormality was observed in differentiation of R6a.a, R6a.p. or R6.p cells, in both mutants, as compared with those in wild-type animals. The defect in rays 6-7 fusion involved mis-localization of ray 7 precursors to ray 6 precursors during ray identity determination window at the L4 larval stage. Our observation suggested that both sma-6 and mab-31 mutants have a wild-type ray lineage with ray precursor cells born at the right time. The defects in these mutants were simply due to transformation of the ray cell identity, which dictates the cell cluster's positioning with respect to other ray cell groups. Indeed, similar defects were subsequently observed in other sma mutants (sma-4 and dbl-1, data not shown) also, inferring that the mab-31 gene probably acts in the same canonical dbl/sma pathway.

Bottom Line: Both mab-31 and sma-6 are required in ray lineage at the late larval stages.They act upstream of C. elegans Pax-6 homolog and repress its function.These findings suggested mab-31 is a key factor that can integrate TFG-beta signals in male sensory ray lineage to define organ identity.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong.

ABSTRACT

Background: C. elegans TGF-beta-like Sma/Mab signaling pathway regulates both body size and sensory ray patterning. Most of the components in this pathway were initially identified by genetic screens based on the small body phenotype, and many of these mutants display sensory ray patterning defect. At the cellular level, little is known about how and where these components work although ray structural cell has been implicated as one of the targets. Based on the specific ray patterning abnormality, we aim to identify by RNAi approach additional components that function specifically in the ray lineage to elucidate the regulatory role of TGF-beta signaling in ray differentiation.

Result: We report here the characterization of a new member of the Sma/Mab pathway, mab-31, recovered from a genome-wide RNAi screen. mab-31 mutants showed ray cell cluster patterning defect and mis-specification of the ray identity. mab-31 encodes a nuclear protein expressed in descendants of ray precursor cells impacting on the ray cell's clustering properties, orientation of cell division plane, and fusion of structural cells. Genetic experiments also establish its relationship with other Sma/Mab pathway components and transcription factors acting upstream and downstream of the signaling event.

Conclusion: mab-31 function is indispensable in Sma/Mab signal recipient cells during sensory rays specification. Both mab-31 and sma-6 are required in ray lineage at the late larval stages. They act upstream of C. elegans Pax-6 homolog and repress its function. These findings suggested mab-31 is a key factor that can integrate TFG-beta signals in male sensory ray lineage to define organ identity.

Show MeSH
Related in: MedlinePlus