Advertisement

Molecular Biology Reports

, Volume 46, Issue 2, pp 2067–2084 | Cite as

Comparative RNA editing profile of mitochondrial transcripts in cytoplasmic male sterile and fertile pigeonpea reveal significant changes at the protein level

  • Tanvi Kaila
  • Swati Saxena
  • G. Ramakrishna
  • Anshika Tyagi
  • Kishor U. Tribhuvan
  • Harsha Srivastava
  • Sandhya
  • Ashok Chaudhury
  • Nagendra Kumar Singh
  • Kishor GaikwadEmail author
Original Article

Abstract

RNA editing is a process which leads to post-transcriptional alteration of the nucleotide sequence of the corresponding mRNA molecule which may or may not lead to changes at the protein level. Apart from its role in providing variability at the transcript and protein levels, sometimes, such changes may lead to abnormal expression of the mitochondrial gene leading to a cytoplasmic male sterile phenotype. Here we report the editing status of 20 major mitochondrial transcripts in both male sterile (AKCMS11) and male fertile (AKPR303) pigeonpea genotypes. The validation of the predicted editing sites was done by mapping RNA-seq reads onto the amplified mitochondrial genes, and 165 and 159 editing sites were observed in bud tissues of the male sterile and fertile plant respectively. Among the resulting amino acid alterations, the most frequent one was the conversion of hydrophilic amino acids to hydrophobic. The alterations thus detected in our study indicates differential editing, but no major change in terms of the abnormal protein structure was detected. However, the above investigation provides an insight into the behaviour of pigeonpea mitochondrial genome in native and alloplasmic state and could hold clues in identification of editing factors and their role in adaptive evolution in pigeonpea.

Keywords

RNA editing Mitochondria Cytoplasmic male sterility Cajanus scarabaeoides Cajanus cajan 

Notes

Acknowledgements

We acknowledge the financial support received from ICAR-National Research Centre on Plant Biotechnology, New Delhi, India.

Author contributions

TK carried out the experiments, prepared the library for sequencing run and wrote the manuscript. SS and AT were involved in sequencing run. TK, SS, AT, KUT and HS were involved in result interpretation, data analysis and finalization of the manuscript. GR maintained the fields of pigeonpea throughout the experiment and contributed to the manuscript. S, AC, and NKS contributed in data analysis and manuscript finalisation. KG conceived the study, designed the experiments, and coordinated the work. All the authors have read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

11033_2019_4657_MOESM1_ESM.docx (681 kb)
Supplementary material 1 (DOCX 680 KB)

References

  1. 1.
    Knoop V (2013) Plant mitochondrial genome peculiarities evolving in the earliest vascular plant lineages. J Syst Evol 51:1–12CrossRefGoogle Scholar
  2. 2.
    Palmer JD, Adams KL, Cho Y, Parkinson CL, Qiu YL, Song K (2000) Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc Natl Acad Sci USA 97(13):6960–6966.  https://doi.org/10.1073/pnas.97.13.6960 CrossRefPubMedGoogle Scholar
  3. 3.
    Gualberto JM, Mileshina D, Wallet C, Niazi AK, Weber-Lotfi F, Dietrich A (2014) The plant mitochondrial genome: dynamics and maintenance. Biochimie 100(1), 107–120.  https://doi.org/10.1016/j.biochi.2013.09.016 CrossRefPubMedGoogle Scholar
  4. 4.
    Marienfeld J, Unseld M, Brennicke A (1999) The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci 4:495–502.  https://doi.org/10.1016/S1360-1385(99)01502-2 CrossRefPubMedGoogle Scholar
  5. 5.
    Levings iii CS, Brown GG (1989) Molecular biology of plant mitochondria. Cell 56:171–179.  https://doi.org/10.1016/0092-8674(89)90890-8 CrossRefGoogle Scholar
  6. 6.
    Zhang T, Fang Y, Wang X, Deng X, Zhang X, Hu S (2012) The complete chloroplast and mitochondrial genome sequences of boea hygrometrica: insights into the evolution of plant organellar genomes. PLoS ONE 7(1):e30531.  https://doi.org/10.1371/journal.pone.0030531 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Gott JM (2003) Expanding genome capacity via RNA editing. C R Biol 326:901–908CrossRefGoogle Scholar
  8. 8.
    Mallela A, Nishikura K (2012) A-to-I editing of protein coding and noncoding RNAs. Crit Rev Biochem Mol Biol 47:493–501CrossRefGoogle Scholar
  9. 9.
    Mahendran R, Spottswood MR, Miller DL (1991) RNA editing by cytidine insertion in mitochondria of Physarum polvcephalum. Nature 349:434–438CrossRefGoogle Scholar
  10. 10.
    Cattaneo R, Kaelin K, Baczko K, Billeter MA (1989) Measles virus editing provides an additional cysteine-rich protein. Cell 56(5):759–764.  https://doi.org/10.1016/0092-8674(89)90679-X CrossRefPubMedGoogle Scholar
  11. 11.
    Benne R, van den Burg J, Brakenhoff JP (1986) Major transcript of the frame shifted coxll gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46:819–826CrossRefGoogle Scholar
  12. 12.
    Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341:662–666CrossRefGoogle Scholar
  13. 13.
    Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341(6243):660–662.  https://doi.org/10.1038/341660a0 CrossRefPubMedGoogle Scholar
  14. 14.
    Hiesel R, Wissinger B, Schuster W, Brennicke A (1989) RNA editing in plant mitochondria. Science 246(4937):1632–1634.  https://doi.org/10.1126/science.2480644 CrossRefPubMedGoogle Scholar
  15. 15.
    Begu D, Graves PV, Domec C, Arselin G, Litvak S, Araya A (1990) RNA editing of wheat mitochoodrial ATP synthase subunit 9: direct protein and cDNA sequencing. Plant Cell 2:1238–1290Google Scholar
  16. 16.
    Graves PV, Begu D, Velours J, Neau E, Belloc F, Litvak S, Araya A (1990) Direct protein sequencing of wheat mitochondrial ATP synthase subunit 9 confirms RNA editing in plants. J Mol Biol 214:1–6CrossRefGoogle Scholar
  17. 17.
    Takenaka M, Zehrmann A, Verbitskiy D, Härtel B, Brennicke A (2013) RNA editing in plants and its evolution. Annu Rev Genet 47(1):335–352.  https://doi.org/10.1146/annurev-genet-111212-133519 CrossRefPubMedGoogle Scholar
  18. 18.
    Mower JP, Palmer JD (2006) Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris. Mol Gen Genom 276:285–293CrossRefGoogle Scholar
  19. 19.
    Giegé P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 96:15324–15329.  https://doi.org/10.1073/pnas.96.26.15324 CrossRefPubMedGoogle Scholar
  20. 20.
    Castandet B, Choury D, Bégu D, Jordana X, Araya A (2010) Intron RNA editing is essential for splicing in plant mitochondria. Nucleic Acids Res 38(20):7112–7121.  https://doi.org/10.1093/nar/gkq591 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genom 268(4):434–445.  https://doi.org/10.1007/s00438-002-0767-1 CrossRefGoogle Scholar
  22. 22.
    Bentolila S, Oh J, Hanson MR, Bukowski R (2013) Comprehensive high-resolution analysis of the role of an Arabidopsis gene family in RNA editing. PLoS Genet 9(6):e1003584.  https://doi.org/10.1371/journal.pgen.1003584 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Ichinose M, Sugita M (2017) RNA editing and its molecular mechanism in plant organelles. Genes 8:5.  https://doi.org/10.3390/genes8010005 CrossRefGoogle Scholar
  24. 24.
    Tseng CC, Lee CJ, Chung YT, Sung TY, Hsieh MH (2013) Differential regulation of Arabidopsis plastid gene expression and RNA editing in non-photosynthetic tissues. Plant Mol Biol 82:375–392CrossRefGoogle Scholar
  25. 25.
    Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31:5907–5916CrossRefGoogle Scholar
  26. 26.
    Picardi E, Horner DS, Chiara M, Schiavon R, Valle G, Pesole G (2010) Large-scale detection and analysis of RNA editing in grape mtDNA by RNA deep-sequencing. Nucleic Acids Res 38(14):4755–4767.  https://doi.org/10.1093/nar/gkq202 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Grimes BT, Sisay AK, Carroll HD, Cahoon AB (2014) Deep sequencing of the tobacco mitochondrial transcriptome reveals expressed ORFs and numerous editing sites outside coding regions. BMC Genom 15(1):1–10.  https://doi.org/10.1186/1471-2164-15-31 CrossRefGoogle Scholar
  28. 28.
    Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc Natl Acad Sci USA 104:8178–8183CrossRefGoogle Scholar
  29. 29.
    Zehrmann A, Verbitskiy D, Van Der Merwe JA, Brennicke A, Takenaka M (2009) A DYW domain-containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell 21:558–567CrossRefGoogle Scholar
  30. 30.
    Aubourg S, Boudet N, Kreis M, Lecharny A (2000) In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants. Plant Mol Biol 42:603–613.  https://doi.org/10.1023/A:1006352315928 CrossRefPubMedGoogle Scholar
  31. 31.
    Small ID, Peeters N (2000) The PPR motif–a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25(99):45–47.  https://doi.org/10.1016/S0968-0004)01520-0.CrossRefGoogle Scholar
  32. 32.
    Fujii S, Small I (2011) The evolution of RNA editing and pentatricopeptide repeat genes. N Phytol 191:37–47CrossRefGoogle Scholar
  33. 33.
    Shikanai T (2015) RNA editing in plants: machinery and flexibility of site recognition. Biochim Biophys Acta 1847:779–785CrossRefGoogle Scholar
  34. 34.
    Schallenberg-Rüdinger M, Knoop V (2016) Coevolution of organelle RNA editing and nuclear specificity factors in early land plants. Adv Bot Res 78:1–57Google Scholar
  35. 35.
    Sun T, Bentolila S, Hanson M (2016) The unexpected diversity of plant organelle RNA editosomes. Trends Plant Sci 21:962–973CrossRefGoogle Scholar
  36. 36.
    Kim SR, Yang JI, Moon S, Ryu CH, An K, Kim KM, Yim J, An G (2009) Rice OGR1 encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J 59:738–749.  https://doi.org/10.1111/j.1365-313X.2009.03909.x CrossRefPubMedGoogle Scholar
  37. 37.
    Laser KD, Lersten NR (1972) Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot Rev 38, 425–454.  https://doi.org/10.1007/BF02860010 CrossRefGoogle Scholar
  38. 38.
    Small ID, Rackham O, Filipovska A (2013) Organelle transcriptomes: products of a deconstructed genome. Curr Opin Microbiol 16:652e658CrossRefGoogle Scholar
  39. 39.
    Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23:81e90CrossRefGoogle Scholar
  40. 40.
    Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99:10887–10892CrossRefGoogle Scholar
  41. 41.
    Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J et al (2006) Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Agriculture 18:676–687.  https://doi.org/10.1105/tpc.105.038240.2 CrossRefGoogle Scholar
  42. 42.
    Dahan J, Mireau H (2013) The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol 10:1469e1476CrossRefGoogle Scholar
  43. 43.
    Uyttewaal M, Arnal N, Quadrado M, Martin-Canadell A, Vrielynck N, Hiard S, Gherbi H, Bendahmane A, Budar F, Mireau H (2008) Characterization of Raphanus sativus pentatricopeptide repeat proteins encoded by the fertility restorer locus for ogura cytoplasmic male sterility. Plant Cell Online 20(12):3331–3345.  https://doi.org/10.1105/tpc.107.057208 CrossRefGoogle Scholar
  44. 44.
    Iwabuchi M, Kyozuka J, Shimamoto K (1993) Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male-sterile rice. EMBO J 12:1437–1446CrossRefGoogle Scholar
  45. 45.
    Araya A, Bégu D, Litvak S (1994) RNA editing in plants. Physiol Plant 91:543–550CrossRefGoogle Scholar
  46. 46.
    Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24(3):133–141CrossRefGoogle Scholar
  47. 47.
    Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5(1):16–18.  https://doi.org/10.1038/nmeth1156 CrossRefPubMedGoogle Scholar
  48. 48.
    Mardis ER (2008) Next-generation DNA sequencing methods. Annu Rev Genom Hum Genet 9:387–402CrossRefGoogle Scholar
  49. 49.
    Bahn JH, Lee JH, Li G, Greer C, Peng G, Xiao X (2012) Accurate identification of A-to-I RNA editing in human by transcriptome sequencing. Genome Res 22:142–150.  https://doi.org/10.1101/gr.124107.111.142 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Singh NK, Gupta DK, Jayaswal PK, Mahato AK, Dutta S, Singh S, Bhutani S, Dogra V, Singh BP, Kumawat G (2012) The first draft of the pigeonpea genome sequence. J Plant Biochem Biotechnol 21(1):98–112.  https://doi.org/10.1007/s13562-011-0088-8 CrossRefPubMedGoogle Scholar
  51. 51.
    Sharma D, Green JM (1980) Pigeonpea. In Fehr WR, Hadley HH (eds) Hybridization of crop plants. WI: American Society of Agronomy and Crop Science Society of America, Madison, pp 471–481Google Scholar
  52. 52.
    Saxena KB, Kumar RV, Rao PV (2002) Pigeonpea nutrition and its improvement. J Crop Prod 5:227–260CrossRefGoogle Scholar
  53. 53.
    Odeny D, Ferguson M, Hoisington DA (2007) Development characterization and utilization of microsatellite markers in pigeonpea [Cajanus cajan (L.) Millsp.]. Plant 126:130–136.  https://doi.org/10.1111/j.1439-0523.2007.01324.x CrossRefGoogle Scholar
  54. 54.
    Bohra A, Mallikarjuna N, Saxena KB, Upadhyaya HD, Vales I, Varshney RK (2010) Harnessing the potential of crop wild relatives through genomics tools for pigeonpea improvement. J Plant Biol 37:1–16Google Scholar
  55. 55.
    Saxena KB, Sultana R, Mallikarjuna N, Saxena RK, Kumar RV, Sawargaonkar SL, Varshney RK (2010) Male-sterility systems in pigeonpea and their role in enhancing yield. Plant Breed 129(2):125–134.  https://doi.org/10.1111/j.1439-0523.2009.01752.x CrossRefGoogle Scholar
  56. 56.
    Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter J, Donoghue MT, Azam S, Fan G, Whaley AM (2011) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol 30(1):83–89.  https://doi.org/10.1038/nbt.2022 CrossRefPubMedGoogle Scholar
  57. 57.
    Tuteja R, Saxena RK, Davila J, Shah T, Chen W, Xiao YL, Fan G, Saxena KB, Alverson AJ, Spillane C et al (2013) Cytoplasmic male sterility-associated chimeric open reading frames identified by mitochondrial genome sequencing of four cajanus genotypes. DNA Res 20(5):485–495.  https://doi.org/10.1093/dnares/dst025 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Kaila T, Chaduvla PK, Saxena S, Bahadur K, Gahukar SJ, Chaudhury A, Sharma TR, Singh NK, Gaikwad K (2016) Chloroplast genome sequence of pigeonpea (Cajanus cajan (L.) Millspaugh) and Cajanus scarabaeoides (L.) Thouars: genome organization and comparison with other legumes. Front Plant Sci 7:1847.  https://doi.org/10.3389/fpls.2016.01847 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Kemble GW, McCormick AL, Pereiram L, Mocarski ES (1987) A cytomegalovirus protein with properties of herpes simplex virus ICPS: partial purification of the polypeptide and map position of the gene. J Virol 61:3143–3151PubMedPubMedCentralGoogle Scholar
  60. 60.
    Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15Google Scholar
  61. 61.
    Mower JP (2005) PREP-Mt: predictive RNA editor for plant mitochondrial genes. BMC Bioinform 6:96CrossRefGoogle Scholar
  62. 62.
    Chou PY, Fasman GD (1974) Conformational parameters for amino acids in helical, β-sheet, and random coil regions calculated from proteins. Biochemistry 13:211–222.  https://doi.org/10.1021/bi00699a001 CrossRefPubMedGoogle Scholar
  63. 63.
    Chou PY, Fasman GD (1974) Prediction of protein conformation. Biochemistry 13:222–245.  https://doi.org/10.1021/bi00699a002 CrossRefPubMedGoogle Scholar
  64. 64.
    Käll L, Krogh A, Sonnhammer ELL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036.  https://doi.org/10.1016/j.jmb.2004.03.016 CrossRefPubMedGoogle Scholar
  65. 65.
    Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858CrossRefGoogle Scholar
  66. 66.
    The PyMOL Molecular Graphics System, Version 2.0 Schrödinger, LLCGoogle Scholar
  67. 67.
    Takenaka M, Brennicke A (2007) RNA editing in plant mitochondria: assays and biochemical approaches. Methods Enzymol 424:439–458CrossRefGoogle Scholar
  68. 68.
    Kazakoff SH, Imelfort M, Edwards D, Koehorst J, Biswas B, Batley J, Scott PT, Gresshoff PM (2012) Capturing the biofuel wellhead and powerhouse: the chloroplast and mitochondrial genomes of the leguminous feedstock tree Pongamia pinnata. PLoS ONE 7:1–12.  https://doi.org/10.1371/journal.pone.0051687 CrossRefGoogle Scholar
  69. 69.
    Suzuki H, Yu J, Ness SA, O’Connell MA, Zhang J (2013) RNA editing events in mitochondrial genes by ultra-deep sequencing methods: a comparison of cytoplasmic male sterile, fertile and restored genotypes in cotton. Mol Genet Genom 288(9):445–457.  https://doi.org/10.1007/s00438-013-0764-6 CrossRefGoogle Scholar
  70. 70.
    Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T (2000) The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNACys(GCA). Nucleic Acids Res 28(13):2571–2576.  https://doi.org/10.1093/nar/28.13.2571 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Salmans ML, Chaw SM, Lin CP, Shih AC, Wu YW, Mulligan RM (2010) Editing site analysis in a gymnosperm mitochondrial genome reveals similarities with angiosperm mitochondrial genomes. Curr Genet 56:439–446CrossRefGoogle Scholar
  72. 72.
    Lu B, Hanson MRR (1994) A single homogeneous form of ATP6 protein accumulates in petunia mitochondria despite the presence of differentially edited atp6 transcripts. Plant Cell 6:1955–1968.  https://doi.org/10.1105/tpc.6.12.1955 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57–61CrossRefGoogle Scholar
  74. 74.
    Fang Y, Wu H, Zhang T, Yang M, Yin Y, Pan L, Yu X, Zhang X, Hu S, Al-Mssallem IS et al (2012) A complete sequence and transcriptomic analyses of date palm (Phoenix dactylifera L.) mitochondrial genome. PLoS ONE 7(5):e37164.  https://doi.org/10.1371/journal.pone.0037164 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Yura K, Go M (2008) Correlation between amino acid residues converted by RNA editing and functional residues in protein three-dimensional structures in plant organelles. BMC Plant Biol 8:1–11.  https://doi.org/10.1186/1471-2229-8-79 CrossRefGoogle Scholar
  76. 76.
    Mungpakdee S, Shinzato C, Takeuchi T, Kawashima T, Koyanagi R, Hisata K, Tanaka M, Goto H, Fujie M, Lin S et al (2014) Massive gene transfer and extensive rna editing of a symbiotic dinoflagellate plastid genome. Genome Biol Evol 6(6):1408–1422.  https://doi.org/10.1093/gbe/evu109 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Moreira S, Valach M, Aoulad-Aissa M, Otto C, Burger G (2016) Novel modes of RNA editing in mitochondria. Nucleic Acids Res 44:4907–4919.  https://doi.org/10.1093/nar/gkw188 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Yan C, Wu F, Jernigan RL, Dobbs D, Honavar V (2008) Characterization of protein–protein interfaces. Protein J 27(1):59–70.  https://doi.org/10.1007/s10930-007-9108-x CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Begu D, Graves PV, Domec C, Arselin G, Litvak S, Araya A (1990) RNA editing of wheat mitochondrial ATP synthase subunit 9: direct protein and cDNA sequencing. Plant Cell 2:1238–1290Google Scholar
  80. 80.
    Kurek I, Ezra D, Begu D, Erel N, Litvak S, Breiman A (1997) Studies on the effects of nuclear background and tissue specificity on RNA editing of the mitochondrial ATP synthase subunits a, 6 and 9 in fertile and cytoplasmic male-sterile (CMS) wheat. Theor. Appl Genet 95:1305–1311CrossRefGoogle Scholar
  81. 81.
    Tang HV, Chen W, Pring DR (1999) Mitochondrial orf107 transcription, editing, and nucleolytic cleavage conferred by the gene Rf3 are expressed in sorghum pollen. Sex Plant Reprod 12:53–55CrossRefGoogle Scholar
  82. 82.
    Howad W, Tang HV, Pring DR, Kempken F (1999) Nuclear genes from T × CMS maintainer lines are unable to maintain atp6 editing in any anther cell-type in the Sorghum bicolor A3 cytoplasm. Curr Genet 36:62–68CrossRefGoogle Scholar
  83. 83.
    Pring DR, Chen W, Tang HV, Howad W, Kempken F (1998) Interaction of mitochondrial RNA editing and nucleolytic processing in the restoration of male fertility in sorghum. Curr Genet 33:429–436CrossRefGoogle Scholar
  84. 84.
    Gallagher LJ, Betz SK, Chase CD (2002) Mitochondrial RNA editing truncates a chimeric open reading frame associated with S male-sterility in maize. Curr Genet 42:179–184CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Tanvi Kaila
    • 1
    • 2
  • Swati Saxena
    • 1
  • G. Ramakrishna
    • 1
  • Anshika Tyagi
    • 1
  • Kishor U. Tribhuvan
    • 1
  • Harsha Srivastava
    • 1
  • Sandhya
    • 1
  • Ashok Chaudhury
    • 2
  • Nagendra Kumar Singh
    • 1
  • Kishor Gaikwad
    • 1
    Email author
  1. 1.ICAR-National Research Centre on Plant BiotechnologyNew DelhiIndia
  2. 2.Department of Bio & NanotechnologyGuru Jambheshwar University of Science & TechnologyHisarIndia

Personalised recommendations