Mitochondrial regulation of flower development

Mitochondrion

Volumn 8, Issue 1, 2008, Pages 74-86

  Carlsson, Jenny ^a   Leino, Matti ^a   Sohlberg, Joel ^a   Sundström, Jens F ^a   Glimelius, Kristina ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Alloplasmic lines; Cytoplasmic male sterility (CMS); Floral homeotic genes; Nuclear mitochondrial interactions; Pentatricopeptide repeat (PPR); Restorer of fertility

Indexed keywords

ARTICLE; BRASSICA; CARROT; CYTOPLASMIC MALE STERILITY; FLOWER DEVELOPMENT; GENE EXPRESSION; GENE INTERACTION; GENE REPRESSION; GENETIC REGULATION; HOMEOBOX; MITOCHONDRIAL GENE; MITOCHONDRIAL RESPIRATION; MOLECULAR CLONING; NONHUMAN; PHENOTYPE; PLANT GENETICS; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TOBACCO; WHEAT;

BRASSICA; DAUCUS CAROTA; FLOWERS; GENES, HOMEOBOX; GENES, PLANT; GENOME, MITOCHONDRIAL; MITOCHONDRIA; PLANT INFERTILITY; TOBACCO; TRITICUM;

BRASSICA; DAUCUS CAROTA; NICOTIANA TABACUM; TRITICUM AESTIVUM;

EID: 37349131062     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2007.09.006     Document Type: Article

References (131)

1. Abad A.R., Mehrtens B.J., and Mackenzie S.A. Specific expression in reproductive tissues and fate of a mitochondrial sterility-associated protein in cytoplasmic male-sterile bean. Plant Cell 7 (1995) 271-285
2. Ainsworth C., Parker J., and Buchanan-Wollaston V. Sex determination in plants. Curr. Top. Dev. Biol. 38 (1998) 167-223
3. Albert V.A., Gustafsson M.H.G., and Di Laaurenzio L. Ontogenetic systematics, molecular genetics and the angiosperm petal. In: Soltis D.E., Soltis P.S., and Doyle J.J. (Eds). Molecular Systematics of Plants II (1998), Kluwer Academic Publishers, Boston 349-374
4. APG-II, 2003. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants. Bot. J. Linn. Soc. 141, 339-436.
5. Banga S.S., Deol J.S., and Banga S. Alloplasmic male-sterile Brassica juncea with Enarthrocarpus lyratus cytoplasm and the introgression of gene(s) for fertility restoration from cytoplasm donor species. Theor. Appl. Genet. 106 (2003) 1390-1395
6. Bannerot H., Loulidard L., Cauderon Y., and Tempe J. Transfer of cytoplasmic male sterility from Raphanus sativus to Brassica oleracea. Cruciferae 1974 Eucarpia meeting (1974) 52-54
7. Bentolila S., Alfonso A.A., and Hanson M.R. A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. USA 99 16 (2002) 10887-10892
8. Bereterbide A., Hernould M., Castera S., and Mouras A. Inhibition of cell proliferation, cell expansion and differentiation by the Arabidopsis SUPERMAN gene in transgenic tobacco plants. Planta 214 (2001) 22-29
9. Bereterbide A., Hernould M., Farbos I., Glimelius K., and Mouras A. Restoration of stamen development and production of functional pollen in an alloplasmic CMS tobacco line by ectopic expression of the Arabidopsis thaliana SUPERMAN gene. Plant J. 29 5 (2002) 607-615
10. Bergman P., Edqvist J., Farbos I., and Glimelius K. Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Mol. Biol. 42 (2000) 531-544
11. Bonhomme S., Budar F., Férault M., and Pelletier G. A 2.5 kb NcoI fragment of Ogura radish mitochondrial DNA is correlated with cytoplasmic male-sterility in Brassica cybrids. Curr. Genet. 19 (1991) 121-127
12. Bonhomme S., Budar F., Lancelin D., Small I., Defrance M.-C., and Pelletier G. Sequence and transcription analysis of the Nco2.5 Ogura-specific fragment correlated with cytoplasmic male sterility in Brassica hybrids. Mol. Gen. Genet. 235 (1992) 340-348
13. Bonnett H.T., Djurberg I., Fajardo M., and Glimelius K. A mutation causing variegation and abnormal development in tobacco is associated with an altered mitochondrial DNA. Plant J. 3 4 (1993) 519-525
14. Bonnett H.T., Kofer W., Håkansson G., and Glimelius K. Mitochondrial involvement in petal and stamen development studied by sexual and somatic hybridization of Nicotiana species. Plant Sci. 80 (1991) 119-130
15. Bowman J.L., Sakai H., Jack T., Weigel D., Mayer U., and Meyerowitz E.M. SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114 (1992) 599-615
16. Bowman J.L., Smyth D.R., and Meyerowitz E.M. Genes directing flower development in Arabidopsis. Plant Cell 1 1 (1989) 37-52
17. Bowman J.L., Smyth D.R., and Meyerowitz E.M. Genetic interactions among floral homeotic genes of Arabidopsis. Development 112 1 (1991) 1-20
18. Bradley D., Carpenter R., Sommer H., Hartley N., and Coen E. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72 1 (1993) 85-95
19. Brown G.G., Formanová N., Jin H., Wargachuk R., Dendy C., Patil P., Laforest M., Zhang J., Cheung W.Y., and Landry B.S. The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 35 (2003) 262-272
20. Burns J.A., Gerstel D.U., and Sand S.A. Cytoplasmic male sterility in Nicotiana, restoration of fertility, and the nucleolus. II. N. debneyi cytoplasm. Genetics 90 (1978) 151-159
21. Butow R.A., and Avadhani N.G. Mitochondrial signaling: the retrograde response. Mol. Cell 14 (2004) 1-15
22. Carlsson J., Lagercrantz U., Sundström J., Teixeira R., Wellmer F., Meyerowitz E.M., and Glimelius K. Microarray analysis reveals altered expression of a large number of nuclear genes in developing cytoplasmic male sterile Brassica napus flowers. Plant J. 49 (2007) 452-462
23. Carlsson J., Leino M., and Glimelius K. Mitochondrial genotypes with variable parts of Arabidopsis thaliana DNA affect development in Brassica napus lines. Theor. Appl. Genet. 115 (2007) 627-641
24. Clifton S.W., Minx P., Fauron C.M.-R., Gibson M., Allen J.O., Sun H., Thompson M., Barbazuk W.B., Kanuganti S., Tayloe C., Meyer L., Wilson R.K., and Newton K.J. Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol. 136 (2004) 3486-3503
25. Coen E.S., and Meyerowitz E.M. The war of the whorls: genetic interactions controlling flower development. Nature 353 6339 (1991) 31-37
26. Conley C.A., and Hanson M.R. Tissue-specific protein expression in plant mitochondria. Plant Cell 6 (1994) 85-91
27. Cui X., Wise R.P., and Schnable P.S. The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272 (1996) 1334-1336
28. Davies B., Motte P., Keck E., Saedler H., Sommer H., and Schwarz-Sommer Z. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. Embo J. 18 14 (1999) 4023-4034
29. de Martino G., Pan I., Emmanuel E., Levy A., and Irish V.F. Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18 8 (2006) 1833-1845
30. Delph L.F., Touzet P., and Bailey M.F. Merging theory and mechanism in studies of gynodioecy. Trends Ecol. Evol. (Amst.) 22 1 (2007) 17-24
31. Desloire S., Gherbi H., Laloui W., Marhadour S., Clouet V., Cattolico L., Falentin C., Giancola S., Renard M., Budar F., Small I., Caboche M., Delourme R., and Bendahmane A. Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptiderepeat protein family. EMBO Rep. 4 6 (2003) 588-594
32. Dill C.L., Wise R.P., and Schnable P.S. Rf8 and Rf* mediate unique T- urf13-transcript accumulation, revealing a conserved motif associated with RNA processing and restoration of pollen fertility in T-cytoplasm maize. Genetics 147 (1997) 1367-1379
33. Endress P.K., and Igersheim A. The reproductive structures of the basal angiosperm Amborella trichopoda (Amborellaceae). Int. J. Plant Sci. 161 (2000) 237-248
34. Erickson E.H., Garment M.B., and Peterson C.E. Structure of cytoplasmic male-sterile and fertile carrot flowers. J. Am. Soc. Hortic. Sci. 107 (1982) 698-706
35. Fan Z., and Stefansson B.R. Influence of temperature on sterility of two cytoplasmic malesterility systems in rape (Brassica napus L.). Can. J. Plant Sci. 66 (1986) 221-227
36. Fan Z., Stefansson B.R., and Sernyk J.L. Maintainers and restores for three male-sterility inducing cytoplasms in rape (Brassica napus L.). Can. J. Plant Sci. 66 (1986) 229-234
37. Farbos I., Mouras A., Bereterbide A., and Glimelius K. Defective cell proliferation in the floral meristem of alloplasmic plants of Nicotiana tabacum leads to abnormal floral organ development and male sterility. Plant J. 26 2 (2001) 131-142
38. Forsberg J., Dixelius C., Lagercrantz U., and Glimelius K. UV dose-dependent DNA elimination in asymmetric somatic hybrids between Brassica napus and Arabidopsis thaliana. Plant Sci. 131 (1998) 65-76
39. Gaut B.S. Evolutionary dynamics of grass genomes. New Phytol. 154 (2002) 15-28
40. Geddy R., and Brown G.G. Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection. BMC Genomics 8 130 (2007) 130
41. Geddy R., Mahé L., and Brown G.G. Cell-specific regulation of a Brassica napus CMS associated gene by a nuclear restorer with related effects on a floral homeotic gene promoter. Plant J. 41 (2005) 333-345
42. Gerstel D.U., Burns J.A., and Burk L.G. Cytoplasmic male sterility in Nicotiana, restoration of fertility, and the nucleolus. Genetics 89 (1978) 157-169
43. Goto K., and Meyerowitz E.M. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8 13 (1994) 1548-1560
44. Gourret J.-P., Delourme R., and Renard M. Expression of ogu cytoplasmic male sterility in cybrids of Brassica napus. Theor. Appl. Genet. 83 (1992) 549-556
45. Hama E., Takumi S., Ogihara Y., and Murai K. Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218 (2004) 712-720
46. Handa H. The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napusL.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res. 31 20 (2003) 5907-5916
47. Hanson M.R., and Bentolila S. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16 (2004) S154-S169
48. Hattori M., Miyake H., and Sugita M. A pentatricopeptide repeat protein is required for RNA processing of clpP pre-mRNA in moss chloroplasts. J. Biol. Chem. 282 14 (2007) 10773-10782
49. Havey M.J. The use of cytoplasmic male sterility for hybrid seed production. In: Daniell H., and Chase C. (Eds). Molecular Biology and Biotechnology of Plant Organelles (2004), Springer, Dordrecht 623-634
50. Hernandez-Hernandez T., Martinez-Castilla L.P., and Alvarez-Buylla E.R. Functional diversification of B MADS-box homeotic regulators of flower development: adaptive evolution in protein-protein interaction domains after major gene duplication events. Mol. Biol. Evol. 24 2 (2007) 465-481
51. Hernould M., Bereterbide A., Farbos I., Glimelius K., and Mouras A. Cytoplasmic male sterility in tobacco: a plant genetic disease curable by gene therapy. Flowering Newslett. 34 (2002) 1-10
52. Hileman L.C., Sundstrom J.F., Litt A., Chen M., Shumba T., and Irish V.F. Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol. Biol. Evol. 23 11 (2006) 2245-2258
53. Irish V.F. Variations on a theme: flower development and evolution. Genome Biol. 1 2 (2000) reviews 1015
54. Jack T., Brockman L.L., and Meyerowitz E.M. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68 4 (1992) 683-697
55. Kapoor M., Tsuda S., Tanaka Y., Mayama T., Okuyama Y., Tsuchimoto S., and Takatsuji H. Role of petunia pMADS3 in determination of floral organ and meristem identity, as revealed by its loss of function. Plant J. 32 1 (2002) 115-127
56. Kaul M.L.H. Male Sterility in Higher Plants (1988), Springer-Verlag, Berlin, Heidelberg, New York, London, Paris, Tokyo
57. Kirti P.B., Banga S.S., Prakash S., and Chopra V.L. Transfer of Ogu cytoplasmic male sterility to Brassica juncea and improvement of the male sterile line through somatic cell fusion. Theor. Appl. Genet. 91 (1995) 517-521
58. Klein R.R., Klein P.E., Mullet J.E., Minx P., Rooney W.L., and 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. 111 (2005) 994-1012
59. Kofer W., Glimelius K., and Bonnett H.T. Modifications of mitochondrial DNA cause changes in floral development in homeotic-like mutants of tobacco. Plant Cell 3 (1991) 759-769
60. Koizuka N., Imai R., Fujimoto H., Hayakawa T., Kimura Y., Kohno-Murase J., Sakai T., Kawasaki S., and Imamura J. Genetic characterization of pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J. 34 (2003) 407-415
61. Kotera E., Tasaka M., and Shikanai T. A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433 (2005) 326-330
62. Kramer E.M., Dorit R.L., and Irish V.F. Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149 2 (1998) 765-783
63. Kramer E.M., and Irish V.F. Evolution of genetic mechanisms controlling petal development. Nature 399 6732 (1999) 144-148
64. Kramer E.M., Jaramillo M.A., and Di Stilio V.S. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166 2 (2004) 1011-1023
65. Cys(GCA). Nucleic Acids Res. 28 (2000) 2571-2576
66. Leino M., Landgren M., and Glimelius K. Alloplasmic effects on mitochondrial transcriptional activity and RNA turnover result in accumulated transcripts of Arabidopsis orfs in cytoplasmic male-sterile Brassica napus. Plant J. 42 4 (2005) 469-480
67. Leino M., Teixeira R., Landgren M., and Glimelius K. Brassica napus lines with rearranged Arabidopsis mitochondria display CMS and a range of developmental aberrations. Theor. Appl. Genet. 106 (2003) 1156-1163
68. Leino M., Thyselius S., Landgren M., and Glimelius K. Arabidopsis thaliana chromosome III restores fertility in a cytoplasmic male-sterile Brassica napus line with A. thaliana mitochondrial DNA. Theor. Appl. Genet. 109 (2004) 272-279
69. Li X.-Q., Jean M., Landry B.S., and Brown G.G. Restorer genes for different forms of Brassica cytoplasmic male sterility map to a single nuclear locus that modifies transcripts of several mitochondrial genes. Proc. Natl. Acad. Sci. USA 95 (1998) 10032-10037
70. Linke B., and Börner T. Mitochondrial effects on flower and pollen development. Mitochondrion 5 (2005) 389-402
71. Linke B., Nothnagel T., and Börner T. Morphological characterization of modified flower morphology of three novel alloplasmic male sterile carrot sources. Plant Breed. 118 (1999) 543-548
72. Linke B., Nothnagel T., and Börner T. Flower development in carrot CMS plants: mitochondria affect the expression of MADS box genes homologous to GLOBOSA and DEFICIENS. Plant J. 34 4 (2003) 27-37
73. Litt A., and Irish V.F. Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165 2 (2003) 821-833
74. Liu Z., and Butow R.A. Mitochondrial retrograde signaling. Annu. Rev. Genet. 40 (2006) 159-185
75. Livers R.W. Fertility restoration and its inheritance in cytoplasmic male-sterile wheat. Science 144 (1964) 420
76. Lurin C., Andrés C., Aubourg S., Bellaoui M., Bitton F., Bruyère C., Caboche M., Debast C., Gualberto J., Hoffman B., Lecharny A., Ret M.L., Martin-Magniette M.-L., Mireau H., Peeters N., Renou J.-P., Szurek B., Taconnat L., and Small I. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16 (2004) 2089-2103
77. Malik M., Vyas P., Rangaswamy N.S., and Shivanna K.R. Development of two new cytoplasmic male-sterile lines in Brassica juncea through wide hybridisation. Plant Breed. 118 (1999) 75-78
78. Marienfeld J.R., Unseld M., Brandt P., and Brennicke A. Mosaic open reading frames in the Arabidopsis thaliana mitochondrial genome. Biol. Chem. 378 (1997) 859-862
79. McCollum G.D. Sterility in successive backcrosses of Raphanobrassica (2n = 4x = 36) with recurrent Brassica oleracea (2n = 2x = 18). Can. J. Genet. Cytol. 21 (1979) 479-485
80. McCollum G.D. Induction of an alloplasmic male-sterile Brassica oleracea by substituting cytoplasm from 'Early Scarlet Globe' radish (Raphanus sativus). Euphytica 30 (1981) 855-859
81. Mena M., Ambrose B.A., Meeley R.B., Briggs S.P., Yanofsky M.F., and Schmidt R.J. Diversification of C-function activity in maize flower development. Science 274 5292 (1996) 1537-1540
82. Meur G., Gaikwad K., Bhat S.R., Prakash S., and Kirti P.B. Homeotic-like modifications of stamens to petals is associated with aberrent mitochondrial gene expression in cytoplasmic male sterile Ogura Brassica juncea. J. Genet. 85 2 (2006) 133-139
83. Meyerowitz E.M. Plants compared to animals: the broadest comparative study of development. Science 295 5559 (2002) 1482-1485
84. Murai K., Takumi S., Koga H., and Ogihara Y. Pistillody, homeotic transformation of stamens into pistil-like structures, caused by nuclear-cytoplasm interaction in wheat. Plant J. 29 2 (2002) 169-181
85. Murai K., and Tsunewaki K. Photoperiod-sensitive cytoplasmic male sterility in wheat with Aegilops crassa cytoplasm. Euphytica 67 1-2 (1993) 41-48
86. Murai K., and Tsunewaki K. Genetic analysis on the fertility restoration by Triticum aestivum cv. Chinese Spring against photoperiod-sensitive cytoplasmic male sterility. Jpn. J. Genet. 69 (1994) 195-202
87. Newton K.J., and Coe E.H. Mitochondrial DNA changes in abnormal growth (nonchromosomal stripe) mutants of maize. Proc. Natl. Acad. Sci. USA 83 (1986) 7363-7366
88. Newton K.J., Gabay-Laughnan S., and De Paepe R. Mitochondrial mutations in plants. In: Day D.A., Millar A.H., and Whelan J. (Eds). Plant Mitochondria: From Genome to Function (2004), Kluwer Academic Publishers, Dordrecht/Boston/London 121-141
89. Nothnagel T., Straka P., and Linke B. Male sterility in populations of Daucus and the development of alloplasmic male-sterile lines of carrot. Plant Breed. 119 (2000) 145-152
90. Notsu Y., Masood S., Nishikawa T., Kubo N., Akiduki G., Nakazono M., Hirai A., and Kadowaki K. 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. Genomics 268 (2002) 434-445
91. Ogihara Y., Yamazaki Y., Murai K., Kanno A., Terachi T., Shiina T., Miyashita N., Nasuda S., Nakamura C., Mori N., Takumi S., Murata M., Futo S., and Tsunewaki K. Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res. 33 19 (2005) 6235-6250
92. Ogura H. Studies on the new male-sterility in Japanese radish, with special reference to the utilization of this sterility towards the practical raising of hybrid seeds. Mem. Fac. Agric. Kagoshima Univ. 6 (1968) 39-78
93. Okuda K., Nakamura T., Sugita M., Shimizu T., and Shikanai T. A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J. Biol. Chem. 281 49 (2006) 37661-37667
94. Ouyang S., Zhu W., Hamilton J., H L., Campbell M., Childs K., Thibaud-Nissen F., Malek R.L., Lee Y., Zheng L., Orvis J., Haas B., Wortman J., and Buell C.R. The TIGR rice genome annotation resource: improvements and new features. Nucleic acids Res. 35 (2007) D883-D887
95. Pathania A., Bhat S.R., Dinesh Kumar V., Ashutosh, Kirti P.B., Prakash S., and Chopra V.L. Cytoplasmic male sterility in alloplasmic Brassica juncea carrying Diplotaxis catholica cytoplasm: molecular characterization and genetics of fertility restoration. Theor. Appl. Genet. 107 (2003) 455-461
96. Pelletier G., and Budar F. The molecular biology of cytoplasmically inherited male sterility and prospect for its engineering. Curr. Opin. Biotechnol. 18 (2007) 121-125
97. Pelletier G., Primard C., Vedel F., Chetrit P., Remy R., Rousselle, and Renard M. Intergeneric cytoplasmic hybridization in cruciferae by protoplast fusion. Mol. Gen. Genet. 191 (1983) 244-250
98. Polowick P.L., and Sawhney V.K. A scanning electron microscopic study on the influence of temperature on the expression of cytoplasmic male sterility in Brassica napus. Can. J. Bot. 65 (1987) 807-814
99. Polowick P.L., and Sawhney V.K. Microsporogenesis in a normal line and in the ogu cytoplasmic male-sterile line of Brassica napus I. The influence of high temperatures. Sex. Plant Reprod. 3 (1990) 263-276
100. Polowick P.L., and Sawhney V.K. Microsporogenesis in a normal line and in the ogu cytoplasmic male-sterile line of Brassica napus II. The influence of intermediate and low temperatures. Sex. Plant Reprod. 4 (1991) 22-27
101. Prakash S., Ahuja I., Upreti H.C., Dinesh Kumar V., Bhat S.R., Kirti P.B., and Chopra V.L. Expression of male sterility in alloplasmic Brassica juncea with Erucastrum canariense cytoplasm and the development of a fertility restoration system. Plant Breed. 120 (2001) 479-482
102. Rhoads D.M., and Subbaiah C.C. Mitochondrial retrograde regulation in plants. Mitochondrion 7 (2007) 177-194
103. Sabar M., Gagliardi D., Balk J., and Leaver C.J. ORFB is a subunit of F1F0-ATP synthase: insight into the basis of cytoplasmic male-sterility in sunflower. EMBO Rep. 4 4 (2003) 381-386
104. Sakai H., Medrano L.J., and Meyerowitz E.M. Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378 (1995) 199-203
105. Sakamoto W., Kondo H., Murata M., and Motoyoshi F. Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell 8 (1996) 1377-1390
106. Schmitz-Linneweber C., Williams-Carrier R., and Barkan A. RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 59 region of mRNAs whose translation it activates. Plant Cell 17 (2005) 2791-2804
107. Schmitz-Linneweber C., Williams-Carrier R.E., Williams-Voelker P.M., Kroeger T.S., Vichas A., and Barkan A. A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18 (2006) 2650-2663
108. Schultz E.A., Pickett F.B., and Haughn G.W. The FL010 gene product regulates the expression domain of homeotic genes AP3 and PI in Arabidopsis flowers. Plant Cell 3 (1991) 1221-1237
109. Schwarz-Sommer Z., Huijser P., Nacken W., Saedler H., and Sommer H. Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250 (1990) 931-936
110. Smart C.J., Monéger F., and Leaver C.J. Cell-specific regulation of gene expression in mitochondria during anther development in sunflower. Plant Cell 6 (1994) 811-825
111. Smyth D.R., Bowman J.L., and Meyerowitz E.M. Early flower development in Arabidopsis. Plant Cell 2 (1990) 755-767
112. Sommer H., Beltran J.P., Huijser P., Pape H., Lonnig W.E., Saedler H., and Schwarz-Sommer Z. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J. 9 3 (1990) 605-613
113. Sugiyama Y., Watase Y., Nagase M., Makita N., Yagura S., Hirai A., and Sugiura M. The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol. Genet. Genomics 272 (2005) 603-615
114. Sundstrom J., Carlsbecker A., Svensson M.E., Svenson M., Johanson U., Theissen G., and Engstrom P. MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms. Dev. Genet. 25 3 (1999) 253-266
115. Tang H.V., Pring D.R., Muza F.R., and Yan B. Sorghum mitochondrial orf25 and a related chimeric configuration of a male-sterile cytoplasm. Curr. Genet. 29 (1996) 265-274
116. Tang H.V., Pring D.R., Shaw L.C., Salazar R.A., Muza F.R., Yan B., and Schertz K.F. Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J. 10 1 (1996) 123-133
117. Teixeira R.T., Farbos I., and Glimelius K. Expression levels of meristem identity and homeotic genes are modified by nuclear-mitochondrial interactions in alloplasmic malesterile lines of Brassica. Plant J. 42 5 (2005) 731-742
118. Teixeira R.T., Knorpp C., and Glimelius K. Modified sucrose, starch, and ATP levels in two alloplasmic male-sterile lines of B. napus. J. Exp. Bot. 56 414 (2005) 1245-1253
119. Theissen G., Becker A., Di Rosa A., Kanno A., Kim J.T., Munster T., Winter K.U., and Saedler H. A short history of MADS-box genes in plants. Plant Mol. Biol. 42 1 (2000) 115-149
120. Unseld M., Marienfeld J.R., Brandt P., and Brennicke A. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat. Genet. 15 (1997) 57-61
121. Vandenbussche M., Zethof J., Royaert S., Weterings K., and Gerats T. The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. Plant Cell 16 3 (2004) 741-754
122. Wang H.-M., Ketela T., Keller W.A., Gleddie S.C., and Brown G.G. Genetic correlation of the orf224/atp6 gene region with Polima CMS in Brassica somatic hybrids. Plant Mol. Biol. 27 (1995) 801-807
123. Wang Z., Zou Y., Li X., Zhang Q., Chen L., Wu H., Su D., Chen Y., Guo J., Luo D., Long Y., Zhong Y., and Liua 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 18 (2006) 676-687
124. Warmke H.E., and Lee S.-L.J. Mitochondrial degeneration in Texas cytoplasmic male-sterile corn anthers. J. Hered. 68 (1977) 213-222
125. Vedel F., Chétrit P., Mathieu C., Pelletier G., and Primard C. Several different mitochondrial DNA regions are involved in intergenomic recombination in Brassica napus cybrid plants. Curr. Genet. 11 (1986) 17-24
126. Wen L., and Chase C.D. Pleiotropic effects of a nuclear restorer-of-fertility locus on mitochondrial transcripts in male-fertile and S male-sterile maize. Curr. Genet. 35 (1999) 521-526
127. Winter K.U., Becker A., Munster T., Kim J.T., Saedler H., and Theissen G. MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc. Natl. Acad. Sci. USA 96 13 (1999) 7342-7347
128. Witt U., Hansen S., Albaum M., and Abel W.O. Molecular analyses of the CMS-inducing 'Polima' cytoplasm in Brassica napus L. Curr. Genet. 19 (1991) 323-327
129. Yanofsky M.F., Ma H., Bowman J.L., Drews G.N., Feldmann K.A., and Meyerowitz E.M. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346 6279 (1990) 35-39
130. Zubko M.K., Zubko E.I., Patskovsky Y.V., Khvedynich O.A., Fisahn J., Gleba Y.Y., and Schieder O. Novel "homeotic" CMS patterns generated in Nicotiana via cybridization with Hyoscyamus and Scopolia. J. Exp. Bot. 47 301 (1996) 1101-1110
131. Zubko M.K., Zubko E.I., Ruban A.V., Adler K., Mock H.-P., Misera S., Gleba Y.Y., and Grimm B. Extensive developmental and metabolic alterations in cybrids Nicotiana tabacum (+ Hyoscyamus niger) are caused by complex nucleo-cytoplasmic incompatibility. Plant J. 25 6 (2001) 627-693