Abstract
Nucleolus was regarded as a mere ribosome-producing factory for many decades however, in the past two decades; this has come to the light that it is a plurifunctional nuclear domain which plays vital role in many cellular processes. Despite many advances, much remains to be revealed about the nucleolus association with cellular processes. While exploring the chromosomal diversity in the high altitude plants of the Indian cold desert region in North West Himalayas we came across 140 wild plants, out of these, pollen mother cell (PMC) in 31 plants showed the occurrence of additional nucleoli. Coincidently, all these plants also depicted the phenomenon of cytomixis i.e. inter-PMC chromatin material extrusion/transfer among/between adjacent meiocytes. Interestingly, it was noticed that nucleolus accompanied the chromatin material during process of cytomixis. During, and after the migration of nucleolus, change in its shape, size and number has also been discussed. So the current paper here in correlated the inter-PMC migration of nucleolus to the occurrence of cytomixis.
Acknowledgements
The authors are thankful to the University Grants Commission (UGC), New Delhi, for providing financial assistance under the DRS SAP I, II & III, ASIST programme, and Dr. D.S. Kothari Postdoctoral Fellowship to Dr. Puneet Kumar [award letter no. F.4-2/2006(BSR)/13-427/2011(BSR)]. The authors are very grateful to the head of the Department of Botany, Punjabi University, Patiala and Dr. Paramjit Singh, Director, Botanical Survey of India, Headquarters Kolkata and Joint Director, Dr. S.K. Srivastava, NRC, Dehradun, for necessary laboratory, library and internet facilities.
References
Anastassova-Kristeva M. 1977. The nucleolar cycle in man. J. Cell Sci. 25: 103–110.10.1242/jcs.25.1.103Search in Google Scholar PubMed
Anastassova-Kristeva M., Nicoloff H., Kunzel G. & Rieger R. 1977. Nucleolus formation in structurally reconstructed barley karyotypes with six satellite chromosomes. Chromosoma 62: 111–117.10.1007/BF00292633Search in Google Scholar
Arnoldy W. 1900. Beitraegezurmorphologie der Gymnospermen. IV. Was sind die “Keimblaschen” oder “Hofmeisters_Korperchen” in der Eizelle der Abietineen? Flora 87: 194–204.Search in Google Scholar
Basavaiah T. & Murthy T.C.S. 1987. Cytomixis in pollen mother cells of Urochloa panicoides P. Beauv. (Poaceae). Cytologia 52: 69–74.10.1508/cytologia.52.69Search in Google Scholar
Bedi Y.S. 1990. Cytomixis in woody species. Proc. Indian Natl. Sci. Acad. (Plant Sci.) 100B: 233–238.10.1007/BF03053475Search in Google Scholar
Belling J. 1921. On counting chromosomes in pollen mother cells. Am. Nat. 55: 573–574.10.1086/279843Search in Google Scholar
Bellucci M., Roscini C. & Mariani A. 2003. Cytomixis in pollen mother cells of Medicago sativa L. J. Hered. 94: 512–516.10.1093/jhered/esg096Search in Google Scholar PubMed
Bhandari N. N., Tandon S.L. & Jain S. 1969. Some observations on the cytology and cytomixis in Canavalia DC. Cytologia 34: 22–28.10.1508/cytologia.34.22Search in Google Scholar
Bhat T.A., Parveen S. & Khan A.H. 2006. MMS-Induced cytomixis in pollen mother cells of broad bean (Vicia faba L.). Turk. J. Bot. 30: 273–279.Search in Google Scholar
Bustamante F.O., Rocha L.C., Torres A.G., Davide L.C., Mittelmann A. & Techio V.H. 2014. Distribution of rDNA in diploid and polyploid Lolium multiflorum Lam. and fragile sites in 45s rDNA regions. Crop Sci. 54: 1–9.10.2135/cropsci2013.05.0325Search in Google Scholar
Chakravorti A.K. 1960. Idiogram studies with special reference to chromosome nucleolus relationship and its bearing on the cytogenetics of Heliconia. Nucleus 3: 225–250.Search in Google Scholar
Cohn N.S. 1969. Elements of Cytology. New York, Harcourt, Brace and World.Search in Google Scholar
Darvey N.L. & Driscoll C.J. 1972. Nucleolar behaviour in Triticum. Chromosoma 36: 131–139.10.1007/BF00285208Search in Google Scholar
De Paula Wilson B.M., San-Martin J.A.B., Boneventi P., Torezan J.M.D. & Vanzela A.L.L. 2005. Functionality of major and minor 45S rDNA sites in different diploid wild species and varieties of sunflowers. Caryologia 58: 374–379.10.1080/00087114.2005.10589476Search in Google Scholar
Falistocco E., Tosti N. & Falcinelli M. 1995. Cytomixis in pollen mother cells of diploid Dactylis, one of the origins of 2n gametes. J. Hered. 86: 448–453.10.1093/oxfordjournals.jhered.a111619Search in Google Scholar
Fankhauser G. & Humphrey R.R. 1943. Relation between number of nucleoli and number of chromosome sets in animal cells. Proc. Natl. Acad. Sci. USA 29: 344–350.10.1073/pnas.29.11.344Search in Google Scholar PubMed PubMed Central
Farley K.I., Surovtseva Y., Merkel J. & Baserga S.J. 2015. Determinants of mammalian nucleolar architecture. Chromosoma 124: 323–331.10.1007/s00412-015-0507-zSearch in Google Scholar PubMed PubMed Central
Frank D.J. & Roth M.B. 1998. ncl-1 is required for the regulation of cell size and ribosomal RNA synthesis in Caenorhabditis elegans. J. Cell Biol. 140: 1321–1329.10.1083/jcb.140.6.1321Search in Google Scholar PubMed PubMed Central
Frank D.J., Edgar B.A. & Roth M.B 2002. The Drosophila melanogaster gene brain tumor negatively regulates cell growth and ribosomal RNA synthesis. Development 129: 399–407.10.1242/dev.129.2.399Search in Google Scholar PubMed
Gates R.R. 1911. Pollen formation in Oenotheragigas. Ann. Bot. 25: 909–940.10.1093/oxfordjournals.aob.a089373Search in Google Scholar
George S.A. & Lennartz M.R. 1980. Methods for determining ploidy in amphibians: nucleolar number and erythroeyte size 1. Experientia 36: 687–688.10.1007/BF01970141Search in Google Scholar
Grummt I. 2013. The nucleolus – guardian of cellular homeostasis and genome integrity. Chromosoma 122: 487–497.10.1007/s00412-013-0430-0Search in Google Scholar PubMed
Guan J.Z., Wang J.J., Cheng Z.H., Liu Y. & Li Z.Y. 2012. Cytomixis and meiotic abnormalities during microsporogenesis are responsible for male sterility and chromosome variations in Houttuynia cordata. Genet. Mol. Res. 11: 121–130.10.4238/2012.January.17.2Search in Google Scholar PubMed
Heitz E. 1931. Die Ursache der gesetzmässigen Zahl, Lage, Form, und Grösse pflanzlicher Nucleolen. Planta 12: 774–844.10.1007/BF01912443Search in Google Scholar
Jiménez R., Burgos M. & Diaz de la Guardia R. 1988. A study of the silver staining significance in mitotic NORs. Heredity 60: 125–127.10.1038/hdy.1988.18Search in Google Scholar PubMed
Kachroo P. & Koul A.K. 1999. Progress in Cytogenetics: Professor A.K. Koul commemoration volume. Dehra Dun, India, Bishen Singh Mahendra Pal Singh, 368 pp.Search in Google Scholar
Koernicke M. 1901. Uberortsveranderung von Zellkarnern. S.B. Niederhein Ges Natur-U Heilkunde, Bonn A, pp. 14–25.Search in Google Scholar
Kumar P. 2010. Exploration of cytomorphological diversity in the members of Polypetalae from Lahaul-Spiti and adjoining areas. Ph.D thesis, Punjabi University, Patiala, Punjab, India http://hdl.handle.net/10603/2872. Accessed on 27th February, 2016Search in Google Scholar
Kumar P. & Singhal V.K. 2011a. Chromosome number, male meiosis and pollen fertility in selected angiosperms of the cold deserts of Lahaul-Spiti and adjoining areas (Himachal Pradesh, India). Plant Syst. Evol. 297: 271–297.10.1007/s00606-011-0516-1Search in Google Scholar
Kumar P. & Singhal V.K. 2011b. Male meiosis, morphometric analysis and distribution pattern of 2x and 4x cytotypes of Ranunculus hirtellus Royle, 1834 (Ranunculaceae) from the cold regions of northwest Himalayas (India). Comp. Cytogenet. 5: 143–161.10.3897/compcytogen.v5i3.1359Search in Google Scholar
Kumar P., Singhal V.K., Kaur D. & Kaur S. 2010. Cytomixis and associated meiotic abnormalities affecting pollen fertility in Clematis orientalis. Biol. Plant. 54: 181–184.10.1007/s10535-010-0031-1Search in Google Scholar
Kumar P., Singhal V.K., Rana P.K., Kaur S. & Kaur D. 2011. Cytology of Ranunculus laetus Wall. ex Royle from cold desert regions and adjoining hills of North-west Himalayas. Caryologia 64: 25–32.10.1080/00087114.2011.589761Search in Google Scholar
Kumar P., Singhal V.K. & Kaur D. 2012. Impaired male meiosis due to irregular synapsis coupled with cytomixis in a new diploid cytotype of Dianthus angulatus (Caryophyllaceae) from Indian cold deserts. Folia Geobot. 47: 59–68.10.1007/s12224-011-9107-8Search in Google Scholar
Kumar P., Rana P.K., Himshikha., Singhal V.K. & Gupta R.C. 2014. Cytogeography and phenomenon of cytomixis in Silene vulgaris from cold regions of Northwest Himalayas (India). Plant Syst. Evol. 300: 831–842.10.1007/s00606-013-0922-7Search in Google Scholar
Kumar R., Rana P.K., Himshikha., Kaur D., Kaur M., Singhal V.K., Gupta R.C. & Kumar P. 2015. Structural heterozygosity and cytomixis driven pollen sterility in Anemone rivularis Buch.-Ham. ex DC. from Western Himalaya (India). Caryologia 68: 246–253.10.1080/00087114.2015.1032615Search in Google Scholar
Lam Y.W. & Trinkle-Mulcahy L. 2015. New insights into nucleolar structure and function. F1000 Prime Rep. 7: 48.10.12703/P7-48Search in Google Scholar PubMed PubMed Central
Lattoo S.K., Khan S., Bamotra S. & Dhar A.K. 2006. Cytomixis imparis meiosis and influences reproductive success in Chlorophytum comosum (Thunb) Jacq. – An additional strategy and possible implications. J. Biosci. 31: 629–637.10.1007/BF02708415Search in Google Scholar PubMed
Levin D.A. 1973. Accessory nucleoli in microsporocytes of hybrid Phlox. Chromosoma 41: 413.10.1007/BF00396499Search in Google Scholar
Liu Y., Hui R.K., Deng R.N., Wang J.J., Wang M. & Li Z.Y. 2012. Abnormal male meiosis explains pollen sterility in the polyploid medicinal plant Pinellia ternata (Araceae). Genet. Mol. Res. 11: 112–120.10.4238/2012.January.17.1Search in Google Scholar PubMed
Marks G.E. 1957. The cytology of Oxalis dispar. Chromosoma. 8: 650–670.10.1007/BF01259525Search in Google Scholar PubMed
Maszewski J. & Kwiatkowska M. 1984. Number, size, and transcriptional activity of nucleoli during different periods of interphase in antheridial filaments of Chara vulgaris L. Folia Histochem. Cytobiol. 22: 9–19.Search in Google Scholar
Miglani G.S. 2009. Developmental Genetics. New Delhi, I.K. Publishing House Pvt, Ltd., 780 pp.Search in Google Scholar
Montiel E.S., Manrique–Poyato M.I., Rocha–Sanchez S., Lopez–Leon Maria D., Cabrero J., Pe Fectti F. & Camacho JP. 2012. Nucleolus size varies with sex, ploidy and gene dosage in Insects. Physiol. Entomol. pages 1–8 DOI: 10.1111/j.1365–3032.2011.00822.x10.1111/j.1365–3032.2011.00822.xSearch in Google Scholar
Montgomery. T.H. 1898. Comparative cytological studies, with special regard to the morphology of the nucleolus. J. Morph. 15: 265–282.10.1002/jmor.1050150204Search in Google Scholar
Mursalimov S.R. & Deineko E.V. 2011. An ultrastructural study of cytomixis in tobacco pollen mother cells. Protoplasma 248: 717–724.10.1007/s00709-010-0234-5Search in Google Scholar PubMed
Mursalimov S.R. & Deineko E.V. 2015. How cytomixis can form unreduced gametes in tobacco. Plant Syst. Evol. 301: 293–1297.10.1007/s00606-014-1150-5Search in Google Scholar
Mursalimov S.R., Sidorchuk Y.V., Deineko E.V. 2013. New insights into cytomixis: specific cellular features and prevalence in higher plants. Planta 238: 415–423.10.1007/s00425-013-1914-0Search in Google Scholar PubMed
Mursalimov S., Permyakova N., Deineko E., Houben A. & Demidov D. 2015. Cytomixis doesn’t induce obvious changes in chromatin modifications and programmed cell death in tobacco male meiocytes. Front. Plant Sci. 6: 846.10.3389/fpls.2015.00846Search in Google Scholar PubMed PubMed Central
Olson M.O. & Dundr M. 2015. Nucleolus: structure and function. eLS. 1–9. DOI: 10.1002/9780470015902.a0005975.pub310.1002/9780470015902.a0005975.pub3Search in Google Scholar
Paredes S. & Maggert K.A. 2009. Ribosomal DNA contributes to global chromatin regulation. Proc. Natl. Acad. Sci. USA 106: 17829–17834.10.1073/pnas.0906811106Search in Google Scholar PubMed PubMed Central
Pederson T. 2010. The nucleolus. Cold Spring Harb. Perspect. Biol. 3: a000638.10.1101/cshperspect.a000638Search in Google Scholar PubMed PubMed Central
Popp W. & Wachtler F. 1983. Changes in nucleolar structure, number and size in cellular activation and inactivation. Observations in human phytohaemagglutinin-treated lymphocytes. Cell Tissue Res. 234: 377–388.10.1007/BF00213775Search in Google Scholar PubMed
Ranjbar M., Roya K. & Samineh N. 2011. Impact of cytomixis on meiosis in Astragalus cyclophyllos Beck (Fabaceae) from Iran. Caryologia 64: 256–264.10.1080/00087114.2011.10589791Search in Google Scholar
Schubert I. & Kunzel G. 1990. Position-dependent NOR activity in barley. Chromosoma 99: 352–359.10.1007/BF01731723Search in Google Scholar
Shaw P. & Brown J. 2012. Nucleoli: composition, function, and dynamics. Plant Physiol. 158: 44–51.10.1104/pp.111.188052Search in Google Scholar PubMed PubMed Central
Shaw P.J. & Jordan E.G. 1995. The nucleolus. Ann. Rev. Cell Dev. Biol. 11: 93–121.10.1146/annurev.cb.11.110195.000521Search in Google Scholar PubMed
Singhal V.K. & Kumar P. 2008. Impact of cytomixis on meiosis, pollen viability and pollen size in wild populations of Himalayan poppy (Meconopsis aculeate Royle). J. Biosci. 33: 371–380.10.1007/s12038-008-0057-0Search in Google Scholar PubMed
Singhal V.K., Rana P.K., Kumar P. & Kaur D. 2011. Persistent occurrence of meiotic abnormalities in a new hexaploid cytotype of Thalictrum foetidum L. from Indian cold deserts. Biologia 66: 458–464.10.2478/s11756-011-0033-2Search in Google Scholar
Smetana K. & Busch H. 1974. The nucleolus and nucleolar DNA. In: Busch H. (ed.), The Nucleus. New York, Academic Press.10.1016/B978-0-12-147601-4.50010-5Search in Google Scholar
Stępński D. 2014. Functional ultrastructure of the plant nucleolus. Protoplasma 251: 1285–1306.10.1007/s00709-014-0648-6Search in Google Scholar PubMed PubMed Central
Sybenga J. 1972. General Cytogenetics. Amsterdam, North-Holland Publishing Co.Search in Google Scholar
Verma R.C. & Raina S.N. 1981. Cytogenetics of Crotalaria V. Supernumerary nucleoli in C. agatiflora (Leguminosae). Genetica 56: 75–80.10.1007/BF00126933Search in Google Scholar
Vilhar B., Vidic T., Jogan N. & Dermastia M. 2002. Genome size and the nucleolar number as estimators of ploidy level in Dactylis glomerata in the Slovenian Alps. Plant Syst. Evol. 234: 1–13.10.1007/s00606-002-0186-0Search in Google Scholar
Warburton D., Atwood K.C. & Henderson A.S. 1976. Variation in the number of genes rDNA among human acrocentric chromosomes: Correlation with frequency of satellite association. Cytogenet. Cell Genet. 17: 221–230.10.1159/000130715Search in Google Scholar PubMed
©2016 Institute of Botany, Slovak Academy of Sciences
Articles in the same Issue
- Cellular and Molecular Biology
- Molecular detection of Mycobacterium tuberculosis complex in the 8th century skeletal remains from the territory of Slovakia
- Cellular and Molecular Biology
- First report of microorganisms of Caucasus glaciers (Georgia)
- Cellular and Molecular Biology
- Codon optimization of Aspergillus niger feruloyl esterase and its expression in Pichia pastoris
- Botany
- Response of lichens Cladonia arbuscula subsp. mitis and Cladonia furcata to nitrogen excess
- Botany
- No confirmation for previously suggested presence of diploid cytotypes of Sesleria (Poaceae) on the Balkan Peninsula
- Botany
- RCD1 homologues and their constituent WWE domain in plants: analysis of conservation through phylogeny methods
- Botany
- Nucleoli migration coupled with cytomixis
- Cellular and Molecular Biology
- Evaluation of appropriate reference gene for normalization of microRNA expression by real-time PCR in Lablab purpureus under abiotic stress conditions
- Zoology
- The fractal nature of the latitudinal biodiversity gradient
- Zoology
- A new species of Neoribates (Neoribates) (Acari: Oribatida: Parakalummidae) with key to the Neotropical species of the subgenus
- Zoology
- Diversity patterns of aquatic specialists and generalists: contrasts among two spring-fen mesohabitats and nearby streams
- Zoology
- Heteroptera (Insecta: Hemiptera) of the peat bogs of Belarusian Lakeland
- Cellular and Molecular Biology
- Cloning of monoacylglycerol o-acyltransferase 2 cDNA from a silkworm, Bombyx mori
- Zoology
- Biological aspect of the surface structure of the tongue in the adult red kangaroo (Macropus rufus) — light and scanning electron microscopy
- Zoology
- Status of the rose-ringed parakeet Psittacula krameri in Lisbon, Portugal
- Zoology
- Considerations on the vulnerability of the Eurasian water shrew Neomys fodiens to the presence of introduced brown trout Salmo trutta
Articles in the same Issue
- Cellular and Molecular Biology
- Molecular detection of Mycobacterium tuberculosis complex in the 8th century skeletal remains from the territory of Slovakia
- Cellular and Molecular Biology
- First report of microorganisms of Caucasus glaciers (Georgia)
- Cellular and Molecular Biology
- Codon optimization of Aspergillus niger feruloyl esterase and its expression in Pichia pastoris
- Botany
- Response of lichens Cladonia arbuscula subsp. mitis and Cladonia furcata to nitrogen excess
- Botany
- No confirmation for previously suggested presence of diploid cytotypes of Sesleria (Poaceae) on the Balkan Peninsula
- Botany
- RCD1 homologues and their constituent WWE domain in plants: analysis of conservation through phylogeny methods
- Botany
- Nucleoli migration coupled with cytomixis
- Cellular and Molecular Biology
- Evaluation of appropriate reference gene for normalization of microRNA expression by real-time PCR in Lablab purpureus under abiotic stress conditions
- Zoology
- The fractal nature of the latitudinal biodiversity gradient
- Zoology
- A new species of Neoribates (Neoribates) (Acari: Oribatida: Parakalummidae) with key to the Neotropical species of the subgenus
- Zoology
- Diversity patterns of aquatic specialists and generalists: contrasts among two spring-fen mesohabitats and nearby streams
- Zoology
- Heteroptera (Insecta: Hemiptera) of the peat bogs of Belarusian Lakeland
- Cellular and Molecular Biology
- Cloning of monoacylglycerol o-acyltransferase 2 cDNA from a silkworm, Bombyx mori
- Zoology
- Biological aspect of the surface structure of the tongue in the adult red kangaroo (Macropus rufus) — light and scanning electron microscopy
- Zoology
- Status of the rose-ringed parakeet Psittacula krameri in Lisbon, Portugal
- Zoology
- Considerations on the vulnerability of the Eurasian water shrew Neomys fodiens to the presence of introduced brown trout Salmo trutta