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Hemleben V, Grierson D, Borisjuk N, et al. Personal Perspectives on Plant Ribosomal RNA Genes Research: From Precursor-rRNA to Molecular Evolution. Front Plant Sci. 2021;12:797348doi: 10.3389/fpls.2021.797348.
Hemleben, V., Grierson, D., Borisjuk, N., Volkov, R. A., & Kovarik, A. (2021). Personal Perspectives on Plant Ribosomal RNA Genes Research: From Precursor-rRNA to Molecular Evolution. Frontiers in plant science, 12797348. https://doi.org/10.3389/fpls.2021.797348
Hemleben, Vera, et al. "Personal Perspectives on Plant Ribosomal RNA Genes Research: From Precursor-rRNA to Molecular Evolution." Frontiers in plant science vol. 12 (2021): 797348. doi: https://doi.org/10.3389/fpls.2021.797348
Hemleben V, Grierson D, Borisjuk N, Volkov RA, Kovarik A. Personal Perspectives on Plant Ribosomal RNA Genes Research: From Precursor-rRNA to Molecular Evolution. Front Plant Sci. 2021 Dec 21;12:797348. doi: 10.3389/fpls.2021.797348. eCollection 2021. PMID: 34992624; PMCID: PMC8724763.
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Front Plant Sci. 2021 Dec 21;12:797348. doi: 10.3389/fpls.2021.797348. eCollection 2021.

Personal Perspectives on Plant Ribosomal RNA Genes Research: From Precursor-rRNA to Molecular Evolution.

Frontiers in plant science

Vera Hemleben, Donald Grierson, Nikolai Borisjuk, Roman A Volkov, Ales Kovarik

Affiliations

  1. Center of Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany.
  2. Plant and Crop Sciences Division, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, United Kingdom.
  3. School of Life Sciences, Huaiyin Normal University, Huai'an, China.
  4. Department of Molecular Genetics and Biotechnology, Yuriy Fedkovych Chernivtsi National University, Chernivtsi, Ukraine.
  5. Laboratory of Molecular Epigenetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, Brno, Czechia.

PMID: 34992624 PMCID: PMC8724763 DOI: 10.3389/fpls.2021.797348

Abstract

The history of rDNA research started almost 90 years ago when the geneticist, Barbara McClintock observed that in interphase nuclei of maize the nucleolus was formed in association with a specific region normally located near the end of a chromosome, which she called the nucleolar organizer region (NOR). Cytologists in the twentieth century recognized the nucleolus as a common structure in all eukaryotic cells, using both light and electron microscopy and biochemical and genetic studies identified ribosomes as the subcellular sites of protein synthesis. In the mid- to late 1960s, the synthesis of nuclear-encoded rRNA was the only system in multicellular organisms where transcripts of known function could be isolated, and their synthesis and processing could be studied. Cytogenetic observations of NOR regions with altered structure in plant interspecific hybrids and detailed knowledge of structure and function of rDNA were prerequisites for studies of nucleolar dominance, epistatic interactions of rDNA loci, and epigenetic silencing. In this article, we focus on the early rDNA research in plants, performed mainly at the dawn of molecular biology in the 60 to 80-ties of the last century which presented a prequel to the modern genomic era. We discuss - from a personal view - the topics such as synthesis of rRNA precursor (35S pre-rRNA in plants), processing, and the organization of 35S and 5S rDNA. Cloning and sequencing led to the observation that the transcribed and processed regions of the rRNA genes vary enormously, even between populations and species, in comparison with the more conserved regions coding for the mature rRNAs. Epigenetic phenomena and the impact of hybridization and allopolyploidy on rDNA expression and homogenization are discussed. This historical view of scientific progress and achievements sets the scene for the other articles highlighting the immense progress in rDNA research published in this special issue of Frontiers in Plant Science on "Molecular organization, evolution, and function of ribosomal DNA."

Copyright © 2021 Hemleben, Grierson, Borisjuk, Volkov and Kovarik.

Keywords: epigenetics; hybridization; molecular evolution; nucleolar dominance; polyploidy; rDNA research history; rRNA precursor; rRNA processing

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Biochem J. 1980 Oct 1;191(1):165-71 - PubMed
  2. Comp Cytogenet. 2018 Dec 13;12(4):493-513 - PubMed
  3. Nat Biotechnol. 2000 Dec;18(12):1303-6 - PubMed
  4. Plant Mol Biol. 1993 Jan;21(2):381-4 - PubMed
  5. Plant Physiol. 1975 Mar;55(3):496-501 - PubMed
  6. J Mol Biol. 1970 May 14;49(3):671-80 - PubMed
  7. Plant J. 2017 Feb;89(3):617-635 - PubMed
  8. J Mol Biol. 1972 Jan 14;63(1):57-73 - PubMed
  9. J Biol Chem. 2002 Aug 30;277(35):31577-84 - PubMed
  10. Curr Opin Genet Dev. 2004 Apr;14(2):210-7 - PubMed
  11. J Cell Biol. 1981 Dec;91(3 Pt 2):3s-14s - PubMed
  12. Arch Mikrobiol. 1973;90(3):213-22 - PubMed
  13. Plant Mol Biol. 2004 Oct;56(3):439-63 - PubMed
  14. Mol Phylogenet Evol. 2003 Nov;29(2):187-202 - PubMed
  15. Genome Biol Evol. 2017 Feb 1;9(2):380-397 - PubMed
  16. Genetics. 2004 Apr;166(4):1935-46 - PubMed
  17. Plant Mol Biol. 1993 Sep;22(6):1153-6 - PubMed
  18. Plant Mol Biol. 1994 Nov;26(4):1167-79 - PubMed
  19. J Mol Biol. 1969 Dec 14;46(2):281-303 - PubMed
  20. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3442-7 - PubMed
  21. J Mol Biol. 1988 Dec 5;204(3):523-34 - PubMed
  22. Nat Commun. 2021 Jan 15;12(1):387 - PubMed
  23. Genome. 1994 Apr;37(2):271-9 - PubMed
  24. Z Naturforsch C Biosci. 1979 Mar-Apr;34(3-4):253-8 - PubMed
  25. Chromosoma. 2000 Jun;109(3):161-72 - PubMed
  26. Plant J. 2016 Feb;85(3):362-77 - PubMed
  27. BMC Plant Biol. 2010 Aug 16;10:176 - PubMed
  28. Eur J Biochem. 1974 May 15;44(2):501-7 - PubMed
  29. Results Probl Cell Differ. 1994;20:3-24 - PubMed
  30. J Biosci. 2006 Mar;31(1):5-12 - PubMed
  31. Z Naturforsch C J Biosci. 1989 Nov-Dec;44(11-12):1029-34 - PubMed
  32. Mol Biol Cell. 2017 May 15;28(10):1285-1287 - PubMed
  33. Mol Biol Rep. 2010 Apr;37(4):1897-912 - PubMed
  34. Genes Dev. 2006 May 15;20(10):1283-93 - PubMed
  35. Front Genet. 2019 Apr 05;10:290 - PubMed
  36. Mol Gen Genet. 1988 Jun;212(3):548-54 - PubMed
  37. Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14891-6 - PubMed
  38. Heredity (Edinb). 2002 Jan;88(1):19-25 - PubMed
  39. BMC Plant Biol. 2009 Apr 08;9:42 - PubMed
  40. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2158-62 - PubMed
  41. Gene. 1988;62(1):165-9 - PubMed
  42. Mol Phylogenet Evol. 2011 Nov;61(2):321-32 - PubMed
  43. Plant Mol Biol. 1987 Sep;9(5):509-20 - PubMed
  44. Eur J Biochem. 1975 Aug 15;56(2):403-11 - PubMed
  45. Heredity (Edinb). 2013 Jul;111(1):23-33 - PubMed
  46. Mol Cell Biol. 1988 Oct;8(10):4282-8 - PubMed
  47. Genetics. 2007 Feb;175(2):477-85 - PubMed
  48. Plant Mol Biol. 1986 Sep;6(5):339-45 - PubMed
  49. Genes Dev. 1997 Aug 15;11(16):2124-36 - PubMed
  50. Eur J Biochem. 1988 Mar 15;172(3):767-76 - PubMed
  51. Theor Appl Genet. 1988 Jul;76(1):108-12 - PubMed
  52. Mol Biol Evol. 1999 Mar;16(3):311-20 - PubMed
  53. Heredity (Edinb). 2012 Jun;108(6):640-6 - PubMed
  54. Theor Appl Genet. 1993 Feb;85(6-7):801-8 - PubMed
  55. Front Plant Sci. 2021 Jun 24;12:678689 - PubMed
  56. Chromosoma. 2012 Aug;121(4):389-94 - PubMed
  57. Nucleic Acids Res. 2010 Jul;38(13):4487-502 - PubMed
  58. Nature. 1968 Aug 3;219(5153):454-63 - PubMed
  59. J Mol Biol. 1988 Dec 5;204(3):535-48 - PubMed
  60. Plant Physiol. 2005 Sep;139(1):275-86 - PubMed
  61. Tsitol Genet. 2014 Jan-Feb;48(1):3-9 - PubMed
  62. Plant Cell Physiol. 2012 Feb;53(2):267-76 - PubMed
  63. Biochem J. 1969 Jun;113(1):131-8 - PubMed
  64. Front Plant Sci. 2020 Feb 10;11:41 - PubMed
  65. Protoplasma. 2017 Mar;254(2):791-801 - PubMed
  66. Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6 - PubMed
  67. New Phytol. 2007;175(4):756-763 - PubMed
  68. BMC Plant Biol. 2017 Jan 23;17(1):21 - PubMed
  69. Planta. 1979 Sep;146(4):467-73 - PubMed
  70. Gene. 1991 Mar 1;99(1):63-8 - PubMed
  71. Genome. 1988 Oct;30(5):723-33 - PubMed
  72. Nucleic Acids Res. 1989 Apr 11;17(7):2852 - PubMed
  73. Plant J. 2017 Mar;89(5):1020-1030 - PubMed
  74. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1511-5 - PubMed
  75. Nucleic Acids Res. 1979 Nov 10;7(5):1263-81 - PubMed
  76. Mol Gen Genet. 1998 Aug;259(2):133-41 - PubMed
  77. Trends Plant Sci. 2019 Aug;24(8):700-724 - PubMed
  78. New Phytol. 2007;174(3):658-668 - PubMed
  79. Biochim Biophys Acta. 1977 Apr 4;475(3):424-36 - PubMed
  80. J Mol Biol. 1971 Jan 14;55(1):61-74 - PubMed
  81. Biochem Genet. 1980 Jun;18(5-6):509-17 - PubMed
  82. Curr Opin Plant Biol. 2020 Apr;54:26-33 - PubMed
  83. Ann Bot. 2019 May 20;123(5):767-781 - PubMed
  84. J Biol Chem. 2000 Nov 24;275(47):37173-80 - PubMed
  85. Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5833-8 - PubMed
  86. Cells. 2019 Jun 12;8(6): - PubMed
  87. Proc Natl Acad Sci U S A. 1967 Aug;58(2):673-80 - PubMed
  88. Nat New Biol. 1972 Jan 19;235(55):80-2 - PubMed
  89. Mol Gen Genet. 1988 Oct;214(2):333-42 - PubMed
  90. Plant J. 2018 Dec;96(6):1148-1159 - PubMed
  91. Nucleic Acids Res. 1985 Apr 11;13(7):2293-304 - PubMed
  92. Proc Natl Acad Sci U S A. 1964 Jan;51:139-46 - PubMed
  93. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 - PubMed
  94. Mol Gen Genet. 1993 Jan;236(2-3):155-62 - PubMed
  95. Am J Bot. 2005 Jun;92(6):1006-16 - PubMed
  96. Trends Plant Sci. 2015 Nov;20(11):729-740 - PubMed
  97. Eur J Biochem. 1973 Aug 17;37(2):367-76 - PubMed
  98. Nucleic Acids Res. 2008 Jan;36(Database issue):D377-80 - PubMed
  99. Nucleic Acids Res. 1998 Jan 1;26(1):156-9 - PubMed
  100. Nucleic Acids Res. 1981 Nov 25;9(22):6167-89 - PubMed
  101. Genome Biol. 2017 May 3;18(1):75 - PubMed
  102. Sci Rep. 2020 Nov 5;10(1):19230 - PubMed
  103. J Mol Evol. 1989 Oct;29(4):294-301 - PubMed
  104. Mol Phylogenet Evol. 2001 Nov;21(2):198-217 - PubMed
  105. Plant Physiol. 1976 Nov;58(5):614-7 - PubMed
  106. Nucleic Acids Res. 1992 Jul 25;20(14):3685-91 - PubMed
  107. PLoS Genet. 2017 Sep 15;13(9):e1007006 - PubMed
  108. Biochem J. 1973 May;134(1):249-62 - PubMed
  109. Genes Dev. 2016 Jan 15;30(2):177-90 - PubMed
  110. Plant Cell. 2019 Sep;31(9):1945-1967 - PubMed
  111. Theor Appl Genet. 1988 Nov;76(5):760-6 - PubMed
  112. Curr Biol. 1994 Sep 1;4(9):777-83 - PubMed
  113. Mol Phylogenet Evol. 1998 Apr;9(2):204-19 - PubMed
  114. Nucleic Acids Res. 2011 Jan;39(Database issue):D195-201 - PubMed
  115. Natl Cancer Inst Monogr. 1966 Dec;23:431-47 - PubMed
  116. Plant Cell. 1998 May;10(5):649-57 - PubMed
  117. Theor Appl Genet. 1996 Jun;92(8):1108-11 - PubMed
  118. Nucleic Acids Res. 1989 Aug 11;17(15):6395-6 - PubMed
  119. Nucleic Acids Res. 1990 Mar 11;18(5):1288 - PubMed
  120. FEBS Lett. 2017 Jul;591(13):1801-1850 - PubMed
  121. PLoS Genet. 2010 Nov 24;6(11):e1001225 - PubMed
  122. Chromosoma. 2003 Oct;112(3):152-8 - PubMed
  123. Plant Mol Biol. 1997 Feb;33(3):559-64 - PubMed
  124. Plant Divers. 2016 Dec 24;38(6):264-270 - PubMed
  125. Proc Natl Acad Sci U S A. 2016 Nov 22;113(47):13426-13431 - PubMed
  126. Nature. 1982 Sep 9;299(5879):111-7 - PubMed
  127. Plant Mol Biol. 1997 Nov;35(5):655-60 - PubMed
  128. Chromosoma. 2009 Feb;118(1):85-97 - PubMed
  129. Heredity (Edinb). 2003 Sep;91(3):268-75 - PubMed
  130. Eur J Biochem. 1973 Jul 2;36(1):280-5 - PubMed
  131. Ann Bot. 2008 Apr;101(6):815-23 - PubMed
  132. Genetics. 1972 Oct;72(2):253-66 - PubMed
  133. J Mol Evol. 1993 Feb;36(2):144-52 - PubMed

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