Abstract
InGryllotalpa fossor (Orthoptera) (23, X0 male; 24, XX female) we have established the existence of random X chromosome inactivation for dosage compensation of X-linked genes. Both cytogenetical (DNA replication and transcription) and biochemical (X-linked glucose-6-phosphate dehydrogenase) studies have indicated that one of the two X chromosomes in the female soma (hepatic caeca) is late replicating and transcriptionally silent leaving the other X chromosome to remain active as in males thereby ensuring the production of almost the same amount of X-linked glucose-6-phosphate dehydrogenase in both sexes. Even in oogonia, one of the two X chromosomes continues to retain inactive. Only prior to their entry into meiosis the inactive X chromosome is reactivated. Accordingly, there is two-fold increase m the level of X-linked glucose-6-phosphate dehydrogenase in oocytes, From this it is implied that the restoration of X chromosome inactivation should occur some time during early embryogenesis. Thus, dosage compensation inGryllotalpa seems to be analogous to that in mammals. Our work bears testimony to the ancient origin of this mechanism.
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Abbreviations
- 5-BrdU:
-
5-Bromodeoxyuridine
- AO:
-
acridine orange
- [3H]UdR:
-
tritiated uridine
- G6PD:
-
glucose-6-phosphate dehydrogenase
- 5-mC:
-
methyl cytosine
- ActD:
-
actinomycin D
References
Ali S and Rao SRV 1982 Insect sex chromosomes. VII. Negative heteropycnosis and transcriptional activity of the X chromosome in the spermatogonia ofAcheta domesticus (H);Chromosoma (Berl.) 86 571–576
Alston R. E 1967Cellular continuity and development (Palo Alto: Scott, Foresman)
Arora P 1978Cytogenetical studies on the chromosomes of Gryllotalpa fossor (Scudder) withspecial reference to X chromosome, Ph.D. thesis, University of Delhi, Delhi
Arora P and Rao SRV 1979 Insect sex chromosomes. IV. DNA replication inGryllotalpa fossor;Cytobios 26 45–55
Arora P and Rao SRV 1980 Insect sex chromosomes. V.3H-Uridine induced aberrations in the X chromosomes of tetraploid spermatogonia fromGryllotalpa fossor;Chromosoma (Berl.) 77 373–378
Baker B S and Belote J B 1983 Sex determination and dosage compensation inDrosophila melanogaster;Annu. Rev. Genet. 17 345–393
Barr M L and Bertram E G 1949 A morphological distinction between neurons of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis; Nature(London) 163 676–677
Berlowitz L, Loewus M W and Pallota D 1968 Heterochromatin and genetic activity in mealy bugs. 1. Compensation for inactive chromatin by increase in cell number;Genetics 60 93–99
Bhattacharya M, Sher Ali and Rao SRV 1983 Insect sex chromosomes. VIII. Identification of active/inactive X chromosomes inGryllotalpa fossor by 5-BrdU/AO fluorescence;Exp. Cell Res. 144 228–231
Brown S W and Chandra I-I S 1973 Inactivation system of the mammalian X chromosome;Proc. Natl. Acad. Sri. USA 70 195–199
Chandra H S 1979 Dosage compensation inDrosophila and man; inScientific culture in the contemporary world (eds) V Mathieu and P Rossi Monti (special volume published in collaboration with UNESCO) (Milano: Scientia-International Review of Scientific Synthesis) pp 227–246
Chandra H S 1985 Is human X chromosome inactivation a sex-determining device?;Proc. Natl. Acad. Sci. USA 82 6947–6949
Cook A G 1964 Dosage compensation and sex-chromatin in non-mammals;Genet. Res. Comb 5 354–365
Cooper D N 1983 Eukaryotic DNA methylation;Hum. Genet. 64 315–333
Darlington C D and Ha Cour L F 1938 Differential reactivity of the chromosomes;Ann. Bot, (N.S.) 2 615–625
Davies K 1991 The essence of inactivity;Nature (London) 349 15–16
Dawson P S and Hollingsworth N N 1982 Sex-linkage of glucose-6-phosphate dehydrogenase locus in the flour beetleTribolium castaneum;Can. J. Genet. Cytol. 24 267–271
Dawson P S and Samollow P B 1985 Chromosome evolution inTribolium flour beetles: Evidences from linkage of hexokinase-1 and malic enzyme loci inT. castaneum andT. confusum;Evolution 39 220–223
Donald J A and Cooper D W 1977 Studies on metatherian sex chromosomes III. The use of tritiated uridine-induced aberrations to distinguish active and inactive X chromosomes;Aust. J. Biol. Sci..30 103–114
Dutrillaux B 1976 Study of human X chromosome with 5-BrdU acridine orange techniques. Application to X chromosome pathology; inChromosomes today (eds) P H Pearson and K R Lewis (New York John Wiley) Vol 5, pp 395–402
Gartler S M and Andina R J 1976 Mammalian X-chromosome inactivation;Adv. Hum. Genet,7 99–140
Gartler S B and Riggs A D 1983 Mammalian X-chromosome inactivation;Annu. Rev. Genet,17 155–190
Ghosh S N, Bhattacharya M and Rao SRV 1987 DNA replication in the spermatogonial cells ofGryllotalpa fossor and Schistocerca gregaria;Insect Sci. Appl. 8 359–364
Graves JAB 1987 The evolution of mammalian sex chromosomes and dosage compensation: Clues from marsupials and monotremes:Trends Genet. 3 252–256
Hannah-Alava 1965 The premeiotic stages of spermatogenesis;Adv. Genet. 13 157–226
Hebbert D R 1984 Dosage compensation of the sex-linked enzyme phosphoglucomutase in the Orthoptera;Heredity 53 361–369
Henning W, Brand R C, Hackstein J, Hochstenbach R, Kremer H, Laukenau D-H, Lankenau S, Miedema K and Potgens A 1989 Y chromosomal fertility genes ofDrosophila: a new type of eukaryotic genes;Genome 31 561–571.
Imms A D 1971A general text book of entomology. 9th edition. Revised by O W Richards and R G Davis (London: The English Language Book Society and Chapman and Hall Ltd.)
Jaffe E and Laird C 1986 Dosage compensation inDrosophila;Trends Genet. 2 316–321
Jones K W 1984 The evolution of sex chromosomes and gene dosage compensation; inGenetics: Newfrontiers (eds) V L Chopra, B C Joshi, R P Sharma and H C Bansal (New Delhi: Oxford University Press) Vol 1,pp 187–194
Klevecz R R and Hsu T C 1964 The differential capacity for RNA synthesis among chromosomes. A cytological approach;Proc. Natl. Acad. Sci. USA 52 811–817
Koduru P R K, Grace J R and Rao B K 1985 Karyotype, heterochromatin content and meiotic feature ofPoecilocera pieta (Orthoptera, Acrididae);Genetica 67 31–37
Lindsley D L, Sandler L, Baker B B, Carpenter A T C, Danell R E, Hall J C, JaCobs P A, Miklos G L G, Davis B K, Gethmann R C, Hardy R W, Hessler A, Miller S M, Nozawa H, Parry D B and Gould-Somero B 1972 Segmental aneuploidy and genetic gross structure of theDrosophila geonome;Genetics 71 157–184
Lifschytz E and Lindsley D L L972 The role of X-chromosome inactivation during spermatogenesis;Proc. Natl. Acod. Sci. USA 69 182–186
Lucchesi J C 1973 Dosage compensation inDrosophila;Annu. Rev. Genet. 7 225–237
Lyon R F 1961 Gene action in the X chromosome of the mouse(Mus musculus L.);Nature (London) 190 372–373
Meyer B J and Casson. L P 1986Caenorhabditis elegans compensates for the differences in X chromosome dosage between sexes by regulating transcript level;Cell 47 871–881
Mikkelsen M 1976 Identification of active and inactive X chromosomes by BrdU incorporation and fluorochrome staining; inChromosomes today (eds) P H Pearson and K R Lewis (New York: John Wiley) Vol 5, pp 409–414
Mukherjee A S 1990 Dosage compensation inDrosophila and mammals: A review of the past and speculation for the future; inTrends in chromosome research (ed.) T Sharma (New Delhi: Narosa Publishing House) 90–109
Muller H J 1950 Evidence of the precision of genetic adaptation:Harvey Lect. 43 165–229
Ohno S 1967 Sexchromosomes and sex-linked genes (New York: Springer-Verlag)
Ohno S 1974 Conservation of ancient linkage groups in evolution and some insights into the genetic regulatory mechanism of X inactivation;Cold Spring Harbor Symp. Quant. Biol. 38 155–164
Ohno S, Kaplan W D and Kinosita R 1959 Formation of the sex chromatin by a single X chromosome in liver cells ofRattus norvegicus;Exp. CellRes. 18 415–418
Padmaja M 1988Linkage studies and X-chromosome regulation in Gryllotalpa fossor, Ph.D. thesis, University of Delhi, Delhi
Raman M K and Rao SRV 1975a Chromosomes of the mole cricketGryllotalpa fossor Scudder (Orthoptera); CumSki. 44 777–778
Raman M K and Rao SRV 1975b3H-Uridine autoradiographic study of spermatogenesis in the mole cricket,Gryllotalpa fossor Scudder;Nucleus 19 137–140
Rao SRV and Ali S 1982 Insect sex chromosomes VI. A presumptive hyperactivation of the male X chromosome inAche domesticus (L);Chromosoma (Berl.) 86 325–339
Rao SRV and Arora P 1978 Insect sex chromosomes: Part I—Differential response to 5-bromodeoxyuridine of the two X chromosomes in females of the mole cricketGryllotalpa fossor (Scudder);Indian. J. Expo, Biol. 16 870–872
Rao SRV and Arora P 1979 Insect sex chromosomes. III. Differential susceptibility of homologous X chromosomes ofGryllotalpa fossor to3H-urd-induced aberrations;Chromosoma 74 241–252
Rao SRV and Bhattacharya M 1984 Insect sex chromosomes: IX. X chromosome linkage of glucose-6-phosphate dehydrogenase (G-6-PD) locus inGryllotalpa fossor (Orthoptera);.Heredity 53 235–238
Rasch E M, Cassidy J D and King R O 1977 Evidence for dosage compensation in parthenogenetic hymenoptera;Chromosoma 59 323–340
Razin A and Riggs A D 1980 DNA methylation and gene function;Science 210 604–610
Ross H H 1965Text book of entomology 4th edition (Toppan: Wiley and Sons)
Sarkar S 1987Gnome organization in the mole cricket Gryllotalpa fossor, Ph.D. thesis, University of Delhi, Delhi
Sarkar S, Gupta V S, Hendre and Rao SRV 1992 5-methyl-cytosine content inGryllotalpa fossor (Scudder) (Orthoptera);Genome 35 163–166
Schmid W 1967 Heterochromatin in mammals;Arch-Klause-Stiff Vereb. Forsch. 42 1–60
Stern C 1929 Uber die additive Wirkung multiple Allele;Biol. Zentr. 49 261–290
White M J D 1973Animal cytology and evolution 3rd edition (New York: Cambridge University Press)
Young W J., Porter J E and Childs B 1964 Glucose-6-phosphate dehydrogenase inDrosophila: X-linked variants;Science 143 140–141
Zakharov A F and Egolina N A 1972 Differential spiralization along mammalian chromosomes I. BrdU revealed differentiation in Chinese hamster chromosomes;Chromosoma (Berl.) 38 341–365
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Based on the presidential address delivered at the XII Annual Cell Biology Conference and Cell Biology Symposium in Hyderabad (December 27–29, 1989). Dedicated to Prof. B R Seshachar, on his 85th birthday.
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Rao, S.R.V., Padmaja, M. Mammalian-type dosage compensation mechanism in an insect —Gryllotalpa fossor (Scudder) — Orthoptera. J Biosci 17, 253–273 (1992). https://doi.org/10.1007/BF02703153
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DOI: https://doi.org/10.1007/BF02703153