Mitochondrion role in molecular basis of cytoplasmic male sterility

Mitochondrion

Volumn 19, Issue PB, 2014, Pages 198-205

  Horn, Renate ^a   Gupta, Kapuganti J ^b   Colombo, Noemi ^c  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

Author keywords

ATP level; Chimeric open reading frame; Cytoplasmic male sterility; Mitochondria; Reactive oxygen species; Restorer of fertility

Indexed keywords

MITOCHONDRIAL DNA;

FERTILITY; GENE REARRANGEMENT; GENETICS; MITOCHONDRIAL GENE; MITOCHONDRIAL GENOME; MITOCHONDRION; PHYSIOLOGY; PLANT; PLANT GAMETOGENESIS; PLANT PHYSIOLOGY;

DNA, MITOCHONDRIAL; FERTILITY; GAMETOGENESIS, PLANT; GENE REARRANGEMENT; GENES, MITOCHONDRIAL; GENOME, MITOCHONDRIAL; MITOCHONDRIA; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS;

EID: 84914107251     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2014.04.004     Document Type: Review

References (124)

1. Akagi H., Nakamura A., Yokozeki-Misono Y., Inagaki A., Takahashi H., Mori K., Fujimura T. Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theor. Appl. Genet. 2004, 108:1449-1457.
2. Ashutosh, Kumar P., Dinesh Kumar V., Sharma P.C., Prakash S., Bhat S.R. A novel orf108 co-transcribed with the atpA gene is associated with cytoplasmic male sterility in Brassica juncea carrying Moricandia arvensis cytoplasm. Plant Cell Physiol. 2008, 49(2):284-289.
3. Bailey-Serres J., Hanson D.K., Fox T.D., Leaver C.J. Mitochondrial genome rearrangement leads to extension and relocation of cytochrome c oxidase subunit I gene in Sorghum. Cell 1986, 47:567-576.
4. Balk J., Leaver C.J. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 2001, 13:1803-1818.
5. Baranwal V.K., Mikkilineni V., Zehr U.B., Tyagi A.K., Kapoor S. Heterosis: emerging ideas about hybrid vigour. J. Exp. Bot. 2012, 18:6309-6314.
6. Barr C.M., Fishman L. The nuclear component of a cytonuclear hybrid incompatibility in Mimulus maps to a cluster of pentatricopeptide repeat genes. Genetics 2010, 184:455-465.
7. Bellaoui M., Grelon M., Pelltier G., Budar F. The restorer Rfo gene acts post-translationally on the stability of the ORF138 OGURA CMS-associated protein in reproductive tissues of rapeseed cybrids. Plant Mol. Biol. 1999, 40:893-902.
8. Bentolila S., Stefanov S. A reevaluation of rice mitochondrial evolution based on the complete sequence of male-fertile and male-sterile mitochondrial genomes. Plant Physiol. 2012, 158(2):996-1017.
9. Bentolila S., Alfonso A.A., Hanson M.R. A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10887-10892.
10. Bonhomme S., Budar F., Lancelin D., Small I., Defrance M.C., Pelletier G. Sequence and transcript analysis of the Nco2.5 Ogura-specific fragment correlated with cytoplasmic male-sterility in Brassica cybrids. Mol. Gen. Genet. 1992, 235:340-348.
11. Brown G.G., Formanova N., Jin H., Wargachuk R., Dendy C., Patil P., Laforest M., Zhang J., Cheung W.Y., Landry B.S. The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 2003, 35:262-272.
12. Castandet B., Araya A. The nucleo-cytoplasmic conflict, a driving force for the emergence of plant orgenellar RNA editing. IUBMB Life 2012, 64:120-125.
13. Chang S., Yang T., Du T., Huang Y., Chen J., Yan J., He J., Guan R. Mitochondrial genome sequencing helps show the evolutionary mechanism of mitochondrial genome formation in Brassica. BMC Genomics 2011, 12:497.
14. Chase C.D. Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 2007, 23(2):81-90.
15. Chase C.D., Gabay-Laughnan S., Springer Verlag Cytoplasmic male sterility and fertility restoration by nuclear genes. Molecular Biology and Biotechnology of Organelles 2004, 593-622. Springer, Verlag. H. Daniell, C.D. Chase (Eds.).
16. Chase C.D., Ortega V.M. Organization of atpA coding and 3'-flanking sequences associated with cytoplasmic male sterility in Phaseolus vulgaris L. Curr. Genet. 1992, 22:147-153.
17. Chen L., Liu Y.-G. Male sterility and fertility restoration in crops. Annu. Rev. Plant Biol. 2014, 65(5):5.1-5.28.
18. Cui X., Wise R.P., Schnable P.S. The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 1996, 272:1334-1335.
19. Dahan J., Mireau H. The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol. 2013, 10:1-8.
20. Das S., Sen S., Chakraborty A., Chakraborti P., Maiti M.K., Basu A., Basu D., Sen S.K. An unedited 1.1kb mitochondrial orfB gene transcript in the wild abortive cytoplasmic male sterility (WA-CMS) system of Oryza sativa L. subsp. indica. BMC Plant Biol. 2010, 10:39.
21. De la Canal L., Crouzillat D., Quetier F., Ledoigt G. A transcriptional alteration on the atp9 gene is associated with a sunflower male-sterile cytoplasm. Theor. Appl. Genet. 2001, 102:1185-1189.
22. Deng M.H., Wen J.F., Huo J.L., Zhu H.S., Dai X.Z., Zhang Z.Q., Zhou H., Zou X.X. Relationship of metabolism of reactive oxygen species with cytoplasmic male sterility in pepper (Capsicum annuum L.). Sci. Hortic. 2012, 134:232-236.
23. Desloire S., Gherbi H., Laloui W., Marhadour S., Clouet V., Cattolico L., Falentin C., Giancola S., Renard M., Budar F., Small I., Caboch M., Delourme R., Bendahmane A. Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep. 2003, 4:588-594.
24. Dewey R.E., Timothy D.H., Levings C.S. A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc. Natl. Acad. Sci. 1987, 84:5374-5378.
25. Dieterich J.H., Braun H.P., Schmitz U.K. Alloplasmic male sterility in Brassica napus (CMS "Tournefortii-Stiewe") is associated with a special gene arrangement around a novel atp9 gene. Mol. Gen. Genomics. 2003, 269:723-731.
26. Ducos E., Touzet P., Boutry M. The male sterile G cytoplasm of wild beet displays modified mitochondrial respiratory complexes. Plant J. 2001, 26:171-180.
27. Duroc Y., Hiard S., Vrielynck N., Ragu S., Budar F. The Ogura sterility-inducing protein forms a large complex without interfering with the oxidative phosphorylation components in rapeseed mitochondria. Plant Mol. Biol. 2009, 70:123-137.
28. Engelke T., Tatlioglu T. The fertility restorer genes X and T alter the transcripts of a novel mitochondrial gene implicated in CMS1 in chives (Allium schoenoprasum L.). Mol. Gen. Genomics 2004, 271:150-160.
29. European Commission Sustainable Food Consumption and Production in a Resource-Constrained World - The 3rd SCAR Foresight Exercise 2011, Publications Office of the European Union - XVI, Luxembourg, (232 pp.).
30. Fernie A.R., Carrari F., Sweetlove L.J. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 2004, 7:254-261.
31. Fujii S., Toriyama K. Suppressed expression of RETROGRADE-REGULATED MALE STERILITY restores pollen fertility in cytoplasmic male sterile rice plants. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9513-9518.
32. Fujii S., Bond C.S., Small I.D. Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1723-1728.
33. Gabay-Laughnan S., Laughnan J. Male sterility and restorer genes in maize. The Maize Handbook 1994, 418-423. Springer, New York. M. Freeling, V. Walbot (Eds.).
34. Gabay-Laughnan S., Kuzmin E.V., Monroe J., Roark L., Newton K.J. Characterization of a novel thermosensitive restorer of fertility for cytoplasmic male sterility in maize. Genetics 2009, 182:91-103.
35. Gagliardi D., Leaver C.J. Polyadenylation accelerates the degradation of the mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. EMBO J. 1999, 18:3757-3766.
36. Gaikwad K., Baldev A., Kirti P.B., Mohapatra T., Bhat S.R., Chopra V.L., Prakash S. Organization and expression of the mitochondrial genome in CMS (Moricandia) Brassica juncea: nuclear-mitochondrial incompatibility results in differential expression of the atpα gene. Plant Breed. 2006, 125:623-628.
37. Gallagher L.J., Betz S.K., Chase C.D. Mitochondrial RNA editing truncates a chimeric open reading frame associated with S male-sterility in maize. Curr. Genet. 2002, 42:179-184.
38. Gillman J.D., Bentolila S., Hanson M.R. The petunia restorer of fertility protein is part of a large mitochondrial complex that interacts with transcripts of the CMS associated locus. Plant J. 2007, 49:217-227.
39. Glaser E., Soll J. Targeting signals and import machinery of plastids and plant mitochondria. Molecular Biology and Biotechnology of Plant Organelles: Chloroplasts and Mitochondria 2004, 385-418. Kluwer Academic Publishers. H. Daniell, C. Chase (Eds.).
40. Gulyas G., Shin Y., Kim H., Lee J.-S., Hirata Y. Altered transcript reveals an orf507 sterility-related gene in chili pepper (Capsicum annuum L.). Plant Mol. Biol. Report. 2010, 28:605-612.
41. Gutierres S., Sabar M., Lelandais C., Chetrit P., Diolez P., Degand H., Boutry M., Vedel F., de Kouchkovsky Y., de Paepe R. Lack of mitochondrial and nuclear-encoded subunits of complex I and alterations of the respiratory chain in Nicotiana sylvestris mitochondrial deletions mutants. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:3436-3441.
42. Handa H., Gualberto J.M., Grienenberger J.M. Characterization of the mitochondrial orfB and its derivate, orf224, a chimeric open reading frame specific to one mitochondrial genome of the "Polima" male-sterile cytoplasm in rapeseed (Brassica napus L.). Curr. Genet. 1995, 28:546-552.
43. Hanson M.R., Bentolila S. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 2004, 16:154-169.
44. Hernould M., Suharsono S., Litvak S., Araya A., Mouras A. Male-sterility induction in transgenic tobacco plants with an unedited atp9 mitochondrial gene from wheat. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:2370-2374.
45. Horn R. Molecular diversity of male sterility inducing and male-fertile cytoplasms in the genus Helianthus. Theor. Appl. Genet. 2002, 104:562-570.
46. Horn R. Cytoplasmic male sterility and fertility restoration in higher plants. Prog. Bot. 2006, 67:31-52.
47. Howad W., Kempken F. Cell type-specific loss of atp6 RNA editing in cytoplasmic male sterile Sorghum bicolor. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:11090-11095.
48. Howad W., Tang H.V., Pring D.R., Kempken F. Nuclear genes from Tx CMS maintainer lines are unable to maintain atp6 RNA editing in any anther cell-type in the Sorghum bicolor A3 cytoplasm. Curr. Genet. 1999, 36:62-68.
49. Hu L., Liang W., Yin C., Cui X., Zong J., Wang X., Hu J., Zhang D. Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 2011, 23:515-533.
50. Hu J., Wang K., Huang W., Liu G., Gao Y., Wang J., Huang Q., Ji Y., Quin X., Wan L., Zhu R., Li S., Yang D., Zhu Y. The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 2012, 24:109-122.
51. Hu J., Yi R., Zhang H., Ding Yi Nucleo-cytoplasmic interactions affect RNA editing of cox2, atp6 and atp9 in alloplasmic male-sterile rice (Oryza sativa L.) lines. Mitochondrion 2013, 13:87-95.
52. Igarashi K., Kazama T., Motomura K., Toriyama K. Whole genomic sequencing of RT98 mitochondria derived from Oryza rufipogon and northern blot analysis to uncover a cytoplasmic male sterility-associated gene. Plant Cell Physiol. 2013, 54:237-243.
53. Itabashi E., Iwata N., Fujii S., Kazama T., Toriyama K. The fertility restorer gene, Rf2, for Lead Rice-type cytoplasmic male sterility of rice encodes a mitochondrial glycine rich protein. Plant J. 2011, 65:359-367.
54. Iwabuchi M., Koizuka N., Fujimoto H., Takako S., Imamura J. Identification and expression of the kosena radish (Raphanus sativus cv. Kosena) homologue of the ogura radish CMS-associated gene, orf138. Plant Mol. Biol. 1999, 39:183-188.
55. Janska H., Mackenzie S. Physical mapping of the mitochondrial genome in CMS common bean and the nature of spontaneous reversion to fertility. Plant Mitochondria 1993, 393-401. Springer Verlag, Weinheim, New York. A. Brennicke, U. Kück (Eds.).
56. Janska H., Sarria R., Woloszynska M., Arrietal-Montiel M., Mackenzie S. Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 1998, 10:1163-1180.
57. o-ATPase dysfunction in peppers (Capsicum annuum L.) with cytoplasmic male sterility and its association with orf507 and Ψatp6-2 genes. Int. J. Mol. Sci. 2013, 14(1):1050-1068.
58. o-ATP synthase complex. Mol. Biol. Cell 2007, 18:1897-1908.
59. Jiang P., Zhang X., Zhu Y., Zhu W., Xie H., Wang X. Metabolism of reactive oxygen species in cotton cytoplasmic male sterility and its restoration. Plant Cell Rep. 2007, 26:1617-1634.
60. Jiang W., Yang S., Yu D., Gai J. A comparative study of ATPase subunit 9 (atp9) gene between cytoplasmic male sterile line and its maintainer line in soybeans. Afr. J. Biotech. 2011, 10:10387-10392.
61. Jing B., Heng S., Tong D., Wan Z., Fu T., Tu J., Ma C., Yi B., Wen J., Shen J. A male sterility-associated cytotoxic protein ORF288 in Brassica juncea causes aborted pollen development. J. Exp. Bot. 2012, 63:1285-1295.
62. Johns C., Lu M.Q., Lyznik A., Mackenzie S. A mitochondrial DNA sequence is associated with abnormal pollen development in cytoplasmic male sterile bean plants. Plant Cell 1992, 4:435-449.
63. Jordan D.R., Mace E.S., Henzell R.G., Klein P.E., Klein R.R. Molecular mapping and candidate gene identification of the Rf2 gene for pollen fertility restoration in sorghum [Sorghum bicolor (L.) Moench.]. Theor. Appl. Genet. 2010, 120:1279-1287.
64. Jordan D.R., Klein R.R., Sakrewski K.G., Henzell R.G., Klein P.E., Mace E.S. Mapping and characterization of Rf5: a new gene conditioning pollen fertility restoration in A1 and A2 cytoplasm in sorghum (Sorghum bicolor (L.) Moench). Theor. Appl. Genet. 2011, 123:383-396.
65. Kazama T., Toriyama K. A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett. 2003, 544(1-3):99-102.
66. Kim D.H., Kim B.D. The organization of mitochondrial atp6 gene region in male fertile and CMS lines of pepper (Capsicum annuum L.). Curr. Genet. 2006, 49:59-67.
67. Kim D.H., Kang J.G., Kim B.D. Isolation and characterization of the cytoplasmic male sterility-associated orf456 gene in chili pepper (Capsicum annuum L.). Plant Mol. Biol. 2007, 63:519-532.
68. Kim S.R., Yang J.I., Moon S., Ryu C.H., An K., Kim K.M., Yim J., An G. Rice OGRI encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J. 2009, 59:738-749.
69. Klein R.R., Klein P.E., Mullet J.E., Minx P., Rooney W.L., Schertz K.F. Fertility restorer locus Rf1 of sorghum (Sorghum bicolor L.) encodes a pentatricopeptide repeat protein not present in the colinear region of rice chromosome 12. Theor. Appl. Genet. 2005, 111:994-1012.
70. Kofer W., Glimelius K., Bonnett H.T. Modifications of mitochondrial DNA cause changes in floral development in homeotic-like mutants of tobacco. Plant Cell 1991, 3:759-769.
71. Köhler R.H., Horn R., Lössl A., Zetsche K. Cytoplasmic male sterility in sunflower is correlated with the co-transcription of a new open reading frame with the atpA gene. Mol. Gen. Genet. 1991, 227:369-376.
72. Koizuka N., Imai R., Fujimoto H., Hayakawa T., Kimura Y., Kohno-Murase J., Sakai T., Kawasaki S., Imamura J. Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J. 2003, 34:407-415.
73. Komori T., Ohta S., Murai N., Takakura Y., Kuraya Y., Suzuki S., Hiei Y., Imaseki H., Nitta N. Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J. 2004, 37:315-325.
74. Krishnasamy S., Makaroff C.A. Characterization of the radish mitochondrial orfB locus: possible relationship with male sterility in Ogura radish. Curr. Genet. 1993, 24:156-163.
75. Kubo T., Newton K.J. Angiosperm mitochondrial genomes and mutations. Mitochondrion 2008, 8:5-14.
76. Kubo T., Kitazaki K., Matsunaga M., Kagami H., Mikami T. Male sterility-inducing mitochondrial genomes: how do they differ?. Crit. Rev. Plant Sci. 2011, 30(4):378-400.
77. Kumar P., Vasupalli N., Srinivasan R., Bhat S.R. An evolutionarily conserved mitochondrial orf108 is associated with cytoplasmic male sterility in different alloplasmic lines of Brassica juncea and induces male sterility in transgenic Arabidopsis thaliana. J. Exp. Bot. 2012, 63:2921-2932.
78. L'Homme Y., Stahl R.J., Li X.-Q., Hameed A., Brown G.G. Brassica nap cytoplasmic male sterility is associated with expression of a mtDNA region containing a chimeric gene similar to the pol CMS-associated orf224 gene. Curr. Genet. 1997, 31:325-335.
79. Laser K.D., Lersten N.R. Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot. Rev. 1972, 33:337-346.
80. Lázaro J.J., Jiménez A., Camejo D., Iglesia-Baena I., del Carmen Marti M., Lázaro-Payo A., Barranco-Medina S., Sevilla F. Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation. Front. Plant Sci. 2013, 4:460.
81. Li J., Pandeya D., Jo Y.D., Liu W.Y., Kang B.C. Reduced activity of ATP synthase in mitochondria causes cytoplasmic male sterility in chili pepper. Planta 2013, 237(4):1097-1109.
82. Liu F., Cui X., Horner H.T., Weiner H., Schnable P. Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 2001, 13:1063-1078.
83. Logan D.C. Plant mitochondrial dynamics. Biochim. Biophys. Acta 2006, 1763:430-441.
84. Luo D., Xu H., Liu Z., Guo J., Li H., Chen L., Fang C., Zhang Q., Bai M., Yao N., Wu H., Wu H., Ji C., Zheng H., Chen Y., Ye S., Li X., Zhao X., Li R., Li Y.G. A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat. Genet. 2013, 45:573-577.
85. Matsuhira H., Kagami H., Kurata M., Kitazaki K., Matsunaga M., Hamaguchi Y., Hagihara E., Ueda M., Harada M., Muramatsu A., Yui-Kurino R., Taguchi K., Tamagake H., Mikami T., Kubo T. Unusual and typical features of a novel restorer-of-fertility gene of sugar beet (Beta vulgaris L.). Genetics 2012, 192:1347-1358.
86. Menassa R., L'Homme Y., Brown G.G. Posttranscriptional and developmental regulation of a CMS-associated mitochondrial gene region by a nuclear restorer gene. Plant J. 1999, 17:491-499.
87. Millar A.H., Whelan J., Soole K.L., Day D.A. Organization and regulation of mitochondrial respiration in plant. Annu. Rev. Plant Biol. 2011, 62:79-104.
88. Mittler R., Vanderauwera S., Suzuki N., Miller G., Tognetti V.B., Vandepoele K., Gollery M., Shulaev V., Van Breusegem F. ROS signaling: the new wave?. Trends Plant Sci. 2011, 18:300-309.
89. Monéger F., Smart C.J., Leaver C.J. Nuclear restoration of cytoplasmic male sterility in sunflower is associated with tissue-specific regulation of a novel mitochondrial gene. EMBO J. 1994, 13:8-17.
90. Nakamura T., Yagi Y., Kobayashi K. Mechanistic insight into pentatricopeptide repeat proteins as sequence-specific RNA-binding proteins for organellar RNAs in plants. Plant Cell Physiol. 2012, 53:1171-1179.
91. Nizampatnam N.R., Doodhi H., Narasimham Y.K., Mulpuri S., Viswanathaswamy D.K. Expression of sunflower cytoplasmic male sterility-associated open reading frame orfH522 induces male sterility in transgenic tobacco plants. Planta 2009, 229:987-1001.
92. Park J.Y., Lee Y.P., Lee J., Choi B.S., Kim S., Yang T.J. Complete mitochondrial genome sequence and identification of a candidate gene responsible for cytoplasmic male sterility in radish (Raphanus sativus L.) containing DCGMS cytoplasm. Theor. Appl. Genet. 2013, 126:1763-1774.
93. Peng X., Wang K., Hu C., Zhu Y., Wang T., Yang J., Tong J., Li S., Zhu Y. The mitochondrial gene orfH79 plays a critical role in impairing both male gametophyte development and root growth in CMS-Honglian rice. BMC Plant Biol. 2010, 10:125.
94. Potz H., Tatlioglu T. Molecular analysis of cytoplasmic male sterility in chives (Allium schoenoprasum L.). Theor. Appl. Genet. 1993, 87:439-445.
95. Rhoads D.M., Levings C.S.I.I.I., Siedow J.N. URF13, a ligand-gated, pore-forming receptor for T-toxin in the inner membrane of cms-T mitochondria. J. Bioenerg. Biomembr. 1995, 27:437-445.
96. Roads D.M. Plant mitochondrial retrograde regulation. Plant Mitochondria 2011, 411-437. Springer, New York. F. Kempken (Ed.).
97. 0-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep. 2003, 4:1-6.
98. Schmitz-Linneweber C., Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 2008, 13:663-670.
99. Schnable P.S., Wise R.P. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci. 1998, 3(5):175-180.
100. Schwarzländer M., Finkemeier I. Mitochondrial energy and redox signaling in plants. Antioxid. Redox Signal. 2013, 18:2122-2144.
101. Senda M., Harada T., Mikami T., Sugiura M., Kinoshita T. Genomic organization and sequence analysis of the cytochrome oxidase subunit II gene from normal and male-sterile mitochondria in sugar beet. Curr. Genet. 1991, 19:175-181.
102. Shaya F., Gaiduk S., Keren I., Shevtsov S., Zemah H., Belausov E., Evenor D., Reuveni M., Ostersetzer-Biran O. Expression of mitochondrial gene fragments within the tapetum induce male sterility by limiting the biogenesis of the respiratory machinery in transgenic tobacco. J. Integr. Plant Biol. 2012, 54:115-130.
103. Sugiyama Y., Watase Y., Nagase M., Makita N., Yagura S., Hirai A., Sugiura M. The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of the mitochondrial genomes in higher plants. Mol. Gen. Genomics. 2005, 272:603-615.
104. Suzuki H., Yu J., Ness S.A., O'Connell M.A., Zhang J. 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. Genomics 2013, 288:445-457.
105. Tanaka Y., Tsuda M., Yasumoto K., Yamagishi H., Terachi T. A complete mitochondrial genome sequence of ogura-type male-sterile cytoplasm and its comparative analysis with that of normal cytoplasm in radish (Raphanus sativus L.). BMC Genomics 2012, 13:352.
106. Tang H.V., Pring D.R., Shaw L.C., Salazar R.A., Muza F.R., Yan B., Schertz K.F. Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J. 1996, 10(1):123-133.
107. Taylor R.W., Turnbull D.M. Mitochondrial DNA mutations in human disease. Nat. Rev. Genet. 2005, 6:389-402.
108. Uyttewaal M., Arnal N., Quadrado M., Martin-Canadell A., Vrielynck N., Hiard S., Gherbi H., Bendahmane A., Budar F., Mireau H. Characterization of Raphanus sativus pentatricopeptide repeat proteins encoded by the fertility restorer locus for Ogura cytoplasmic male sterility. Plant Cell 2008, 20:3331-3345.
109. Virmani S.S. Advances in hybrid rice research and development in the tropics. Proc. 4th Int. Symp. on Hybrid Rice 2003, 7-20. IRRI, Manila. S.S. Virmani, C.X. Mao, B. Hardy (Eds.).
110. Wang Y., Ma S., Wang M., Zheng X., Gu M., Hu S. Sequence analysis of the gene correlated with cytoplasmic male sterility (CMS) in rapeseed (Brassica napus) Polima and Shaan 2A. Chin. Sci. Bull. 2002, 47:124-128.
111. Wang Z., Zou Y., Li X., Zhang Q., Chen L., Wu H., Su D., Chen Y., Guo J., Luo D., Long Y., Zhong Y., Liu Y.G. 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. Plant Cell 2006, 18:676-687.
112. Wang K., Gao F., Ji Y., Liu Y., Dan Z., Yang P., Zhu Y., Li S. ORFH79 impairs mitochondrial function via interaction with a subunit of electron transport chain complex III in Honglian cytoplasmic male sterile rice. New Phytol. 2013, 198:408-418.
113. Wang K., Peng X., Ji Y., Yang P., Zhu Y., Li S. Gene, protein, and network of male sterility in rice. Front. Plant Sci. 2013, 4:1-10.
114. Wang Z.W., Wang C., Gao L., Mei S.Y., Zhou Y., Xiang C.P., Wang T. Heterozygous alleles restore male fertility to cytoplasmic male-sterile radish (Raphanus sativus L.): a case of overdominance. J. Exp. Bot. 2013, 64:2041-2048.
115. Wen L., Ruesch K.L., Ortega V.M., Kamps T.L., Gabay-Laughnan S., Chase C.D. A nuclear restorer-of-fertility mutation disrupts accumulation of mitochondrial ATP synthase subunit in developing pollen of S male-sterile maize. Genetics 2003, 165:771-779.
116. Wise R.P., Gobelman W.K., Pei D., Dill C.L., Schnable P.S. Mitochondrial transcript processing and restoration of male fertility in T-cytoplasm maize. J. Hered. 1999, 90:380-385.
117. Wise R.P., Broson C.R., Schnable P.S., Homer H.T. The genetics, pathology, and molecular biology of T-cytoplasm male sterility in maize. Adv. Agron. 1999, 65:79-130.
118. Xu X.B., Liu Z.X., Zhang D.F., Liu Y., Song W.B., Li J.S., Dai J.R. Isolation and analysis of rice Rf1-orthologous PPR genes co-segregating with Rf3 in maize. Plant Mol. Biol. Report. 2009, 27:511-551.
119. Yamamoto M.P., Kubo T., Mikami T. The 5'-leader sequence of sugar beet mitochondrial atp6 encodes a novel polypeptide that is characteristic of Owen cytoplasmic male sterility. Mol. Gen. Genomics. 2005, 273:342-349.
120. Yamamoto M.P., Shinada H., Onodera Y., Komaki C., Mikami T., Kubo T. A male sterility-associated mitochondrial protein in wild beets causes pollen distribution in transgenic plants. Plant J. 2008, 54:1027-1036.
121. Yi P., Wang L., Sun Q.P., Zhu Y. Discovery of mitochondrial chimeric-gene associated with cytoplasmic male sterility of HL-rice. Chin. Sci. Bull. 2002, 47(9):744-747.
122. Young E.G., Hanson M.R. A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 1987, 50:41-49.
123. Zabala G., Gabay-Laughnan S., Laughnan J.R. The nuclear Rf3 affects the expression of the mitochondrial chimeric sequence R implicated in the S-type male sterility in maize. Genetics 1997, 147:847-850.
124. Zabaleta E., Mouras A., Hernould M., Suharsono S., Araya A. Transgenic male-sterile plant induced by an unedited atp9 gene is restored to fertility by inducing its expression with antisense RNA. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11259-11263.