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. 2002 Jan 22;99(2):769-74.
doi: 10.1073/pnas.012511099.

Evolution of Germ-Line Signals That Regulate Growth and Aging in Nematodes

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Free PMC article

Evolution of Germ-Line Signals That Regulate Growth and Aging in Nematodes

Mavji N Patel et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

We show that a signal from the germ line represses growth in the nematode Caenorhabditis elegans. Laser-microbeam ablation of cells that give rise to the germ line causes adults to become giant. Ablation of these cells in self-sterile mutant worms also causes gigantism, suggesting that the germ line represses growth because it is the source of a growth-antagonizing signal rather than because of a sink of resources required for reproduction. The C. elegans germ line also emits a signal that represses longevity. This longevity-repressing signal requires the activity of DAF-16, a forkhead/winged-helix transcription factor, but we find that that the growth-repressing signal does not. The growth-repressing signal also does not require the activity of DBL-1, a transforming growth factor beta-related protein that promotes growth in worms. By ablating the germ-line precursors of other species of free-living nematodes, we also found that both the growth-repressing and longevity-repressing signals are evolutionarily variable. Some species have both signals; others have just one or the other. We suggest that variation in germ-line signaling contributes to body size and life-history diversity in the nematodes.

Figures

Figure 1
Figure 1
Growth and survival of wild-type N2 grown at 20°C after ablation of germ-line and somatic precursor cells in hatchling nematodes. (a) The four precursor cells seen in a hatchling. Z1 and Z4 give rise to the somatic gonad and Z2 and Z3 give rise to the germ line. Growth (b, volume, mm3) and survival (c, days) of N2 hermaphrodites in which the germ-line precusors, Z2 and Z3 (solid line) were ablated or else left intact (♦). ■, Z2/3(−); ▴, Z1–4(−). n, total number of nematodes observed, followed by the number of independent experiments performed in parentheses; v, mean maximum body size (±SE); l = mean longevity (±SE). P values are based on a comparison of ablated and intact animals. (b) Intact control, n = 194(3), v = 0.0058 mm3 (± 0.00008); Z2/3(−), n = 65(2), v = 0.0084 mm3 (± 0.0002), P < 0.0001. (c) Intact control, n = 366(3), l = 9.9 (± 0.2); Z2/3(−), n = 67(2), l = 12.9 (± 0.5), P < 0.0001. (d) A wild-type hermaphrodite with intact gonads (Upper) and a germ-line-ablated hermaphrodite (Lower), both grown at 20°C for 11 days from hatching.
Figure 2
Figure 2
Responses of fer-6, daf-16, and dbl-1 mutants to ablation of germ-line precursors, Z2/3. Intact control (⧫) and Z2/3(−) (solid line). (a and b) fer-6 (hc6), control, and Z2/3(−) nematodes were reared at 25°C. Intact control, n = 29(1), v = 0.0031 mm3 (± 0.0002); Z2/3(−), n = 26(1), v = 0.0044 mm3 (± 0.0003), P < 0.0001; intact control, n = 29(1), l = 8.7 (± 0.4); Z2/3(−), n = 29(1), l = 11.0 (± 0.6), P = 0.0003. A wild-type N2 experiment was run alongside at 25°C; intact control, n = 35(1), v = 0.0074 mm3 (± 0.0002); Z2/3(−), n = 55(1), v = 0.0084 mm3 ± (0.0002), P < 0.0001; intact control, n = 29(1), l = 9.9 ± 0.4; Z2/3(−), n = 55(1), l = 15.3 (± 0.8), P < 0.0001. (c and d) daf-16 (mu86), intact control, n = 51(2), v = 0.0086 mm3 (± 0.0004); Z2/Z3(−), n = 59(2), v = 0.0114 mm3 (± 0.0002), P < 0.0001; intact control, n = 51(2), l = 10.8 (± 0.4); Z2/3(−), n = 59(2), l = 11.7 (± 0.4), P = 0.3. In one experiment, all of the gonadal precursor cells Z1-Z4(−) were ablated as well: n = 28(1), v = 0.0108 mm3 (± 0.0003), l = 11.6 (± 0.6). Z2/3(−) versus Z1-Z4(−), P = 0.8 for body size and P = 0.8 for survival. (e and f) dbl-1 (nk3), intact control, n = 44(2), v = 0.0035 mm3 (± 0.0001); Z2/3(−), n = 50(2), v = 0.0055 mm3 (± 0.0001), P < 0.0001; intact control, n = 48(2), l = 14.3 (± 1.1); Z2/3(−), n = 55(2), l = 20.2 (± 1.4), P < 0.001.
Figure 3
Figure 3
Response of selected free-living nematode species to ablation of germ-line precursor cells, Z2/3. Intact control worms (♦); Z2/3(−) worms (▪). (a and b) Caenorhabditis briggsae (AF16), intact control n = 35(2); v = 0.0044 mm3 (± 0.0001); Z2/3(−), n = 44(2), v = 0.0056 mm3 (± 0.0001), P < 0.0001; intact control, n = 45(2), l = 18.6 ± (0.8); Z2/3(−), n = 44(2), l = 26.2 (± 1.2), P < 0.0001. (c and d) Rhabditis sp. (PS1191), intact control, n = 25(1), v = 0.0138 mm3 (± 0.0005); Z2/3(−), n = 27(1), v = 0.0158 mm3 (± 0.0005), P = 0.007; intact control, n = 34 (1), l = 12.9 (± 0.8); Z2/3(−), n = 31(1), l = 14.2 (± 0.7), P = 0.2. (e and f) O. sp. (CEW1), intact control, n = 15(1), v = 0.0017 mm3 (± 0.0003); Z2/3(−), n = 20(1), v = 0.0033 mm3 (± 0.0008), P < 0.0001; intact control, n = 15(1), l = 9.2 (± 0.4); Z2/3(−), n = 20(1), l = 9.9 (± 0.4), P = 0.2. (g and h) O. myriophila (BW290), intact control, n = 54(1), v = 0.0200 mm3 (± 0.0008); Z2/3(−), n = 30(1), v = 0.0260 mm3 (± 0.00009), P < 0.0001; intact control, n = 54 (1); l = 12.9 (± 0.4); Z2/3(−), n = 30(1); l = 13.4 (± 0.5), P = 0.6. (i and j) P. pacificus (PS1843), intact control, n = 42(2), v = 0.0095 mm3 (± 0.0002); Z2/3(−), n = 21(2), v = 0.0083 mm3 (± 0.0004), P < 0.0001; intact control, n = 42(2), l = 17.1 (± 0.9); Z2/3(−), n = 21(2), l = 27.1 (± 2.5), P < 0.0001. (k and l) P. maupasi (PS321), intact control, n = 30(2), v = 0.0119 mm3 (± 0.0003); Z2/3(−), n = 36(2), v = 0.0097 mm3 (± 0.0002), P < 0.0001; intact control, n = 30(2), l = 25.6 (± 1.4); Z2/3(−), n = 36(2), l = 36.3 (± 1.5), P < 0.0001.
Figure 4
Figure 4
Intact (Upper) and Z2/3(−) ablated (Lower) 11-day-old nematodes of O. sp. (CEW1; a and b) and P. pacificus (c and d).

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