Skip to main content
SpringerLink
Log in

Instability in mitochondrial membranes in Polima cytoplasmic male sterility of Brassica rapa ssp. chinensis

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Cytoplasmic male sterility (CMS) is an important factor to observe heterosis in Brassica rapa. Although several studies have documented the rearrangements of mitochondrial DNA and dysfunction in the mitochondria have been observed in most types of CMS, the basis of the molecular mechanisms involved in these processes and other effects on CMS remain unclear. In this study, suppression subtractive hybridization was performed in the flowers of an alloplasmic Polima CMS system from B. rapa ssp. chinensis to identify genes that are differentially expressed between fertile and sterile plants. A total of 443 clones were isolated (156 were upregulated in fertile buds, and 287 were upregulated in sterile ones). Real-time RT-PCR further demonstrated the credibility of SSH. Among these genes, many membrane protein genes (LTP12, PIP2A, and GRP14) were inhibited in the sterile male line. Mitochondrial membrane potential (MMP) assay was then performed. Results showed that the sterile MMP was unstable and failed to create a potential difference; thus, mitochondrial dysfunction occurred. Moreover, abnormal microtubules and photosynthetic pathways were found in sterile male cells. Unstable MMP, nutritional deficiency, and abnormal microtubules were the causes of Polima CMS in Brassica campestris. H2O2, MDA, and O2–, accumulated as byproducts of energy metabolism disorder in sterile male cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alberts B, Johnson A, Lewis JI, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell. 4th edition. Chapter 14. Garland Science, New York

    Google Scholar 

  • Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bang S, Tsutsui K, Shim S, Kaneko Y (2011) Production and characterization of the novel CMS line of radish (Raphanus sativus) carrying Brassica maurorum cytoplasm. Plant Breed 130:410–412

    Article  Google Scholar 

  • Barsby TL, Yarrow SA, Kemble RJ, Grant I (1987) The transfer of cytoplasmic male sterility to winter-type oilseed rape (Brassica napus L.) by protoplast fusion. Plant Sci 53:243–248

    Article  Google Scholar 

  • Bergman P, Edqvist J, Farbos I, Glimelius K (2000) Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Mol Biol 42:531–544

    Article  CAS  PubMed  Google Scholar 

  • Budar F, Pelletier G (2001) Male sterility in plants: occurrence, determinism, significance and use. Comptes rendus de l'Academie des sciences Serie III, Sciences de la vie 324:543–550

    Article  CAS  PubMed  Google Scholar 

  • Cai G, Moscatelli A, Cresti M (1997) Cytoskeletal organization and pollen tube growth. Trends Plant Sci 2:86–91

    Article  Google Scholar 

  • Carlsson J, Lagercrantz U, Sundstrom J, Teixeira R, Wellmer F, Meyerowitz EM, Glimelius K (2007) Microarray analysis reveals altered expression of a large number of nuclear genes in developing cytoplasmic male sterile Brassica napus flowers. Plant J 49:452–462

    Article  CAS  PubMed  Google Scholar 

  • Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial–nuclear interactions. Trends Genet 23:81–90

    Article  CAS  PubMed  Google Scholar 

  • Chaumont F, Bernier B, Buxant R, Williams ME, Levings CS 3rd, Boutry M (1995) Targeting the maize T-urf13 product into tobacco mitochondria confers methomyl sensitivity to mitochondrial respiration. Proc Natl Acad Sci U S A 92:1167–1171

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen C, Marcus A, Li W, Hu Y, Calzada JPV, Grossniklaus U, Cyr RJ, Ma H (2002) The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129:2401–2409

    Article  CAS  PubMed  Google Scholar 

  • Curtiss J, Turley RB, Stewart JM, Zhang JF (2012) Identification of differentially expressed genes in semigametic pima cotton by differential display. Plant Mol Biol Rep 30:643–653

    Article  CAS  Google Scholar 

  • Datta R, Chamusco KC, Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130:1645–1656

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Deng X, Hu ZA, Wang HX (1999) mRNA differential display visualized by silver staining tested on gene expression in resurrection plant Boea hygrometrica. Plant Mol Biol Rep 17:279–279

    Article  Google Scholar 

  • Deng XH, Zhang SN, Hou XL, Yang Y (2007) Studies on biochemical characteristics of PolCMS line and its maintainer line of Brassica rapa ssp. chinensis. Acta Agriculturae Universitatis Jiangxiensis 4:522–525 (in Chinese)

    Google Scholar 

  • Dewey RE, Levings IIICS, Timothy DH (1986) Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell 44:439–449

    Article  CAS  PubMed  Google Scholar 

  • Dieterich JH, Braun HP, Schmitz UK (2003) Alloplasmic male sterility in Brassica napus (CMS 'Tournefortii-Stiewe') is associated with a special gene arrangement around a novel atp9 gene. Mol Gen Genomics 269:723–731

    Article  CAS  Google Scholar 

  • Dorion S, Lalonde S, Saini HS (1996) Induction of male sterility in wheat by meiotic-stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiol 111:137–145

    CAS  PubMed Central  PubMed  Google Scholar 

  • Downey R, Rimmer S (1993) Agronomic improvement in oilseed Brassicas. Adv Agron 50:1–66

    Article  Google Scholar 

  • Ducos E, Touzet P, Boutry M (2001) The male sterile G cytoplasm of wild beet displays modified mitochondrial respiratory complexes. Plant J 26:171–180

    Article  CAS  PubMed  Google Scholar 

  • Duroc Y, Gaillard C, Hiard S, Defrance MC, Pelletier G, Budar F (2005) Biochemical and functional characterization of ORF138, a mitochondrial protein responsible for Ogura cytoplasmic male sterility in Brassiceae. Biochimie 87:1089–1100

    Article  CAS  PubMed  Google Scholar 

  • Eckardt NA (2006) Cytoplasmic male sterility and fertility restoration. Plant Cell 18:515–517

    Article  CAS  PubMed Central  Google Scholar 

  • Erickson L, Grant I, Beversdorf W (1986) Cytoplasmic male sterility in rapeseed (Brassica napus L.). Theor Appl Genet 72:151–157

    Article  CAS  PubMed  Google Scholar 

  • Foissner I, Grolig F, Obermeyer G (2002) Reversible protein phosphorylation regulates the dynamic organization of the pollen tube cytoskeleton: effects of calyculin A and okadaic acid. Protoplasma 220:1–15

    Article  CAS  PubMed  Google Scholar 

  • Frank SA, Barr CM (2003) Programmed cell death and hybrid incompatibility. J Hered 94:181–183

    Article  CAS  PubMed  Google Scholar 

  • Glover J, Grelon M, Craig S, Chaudhury A, Dennis E (1998) Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis. Plant J 15:345–356

    Article  CAS  PubMed  Google Scholar 

  • Gorska-Brylass A, Butowt R, Rodriguez-Garcia M (1997) Distribution of loosely-bound calcium in the vegetative and generative cells of the pollen grains in Chlorophytum elatum. Biol Plant 40:169–181

    Article  CAS  Google Scholar 

  • 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 31:5907–5916

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanson MR (1991) Plant mitochondrial mutations and male sterility. Annu Rev Genet 25:461–486

    Article  CAS  PubMed  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Havey MJ (2004) The use of cytoplasmic male sterility for hybrid seed production. In: Molecular Biology and Biotechnology of Plant Organelles. edn. pp. 623-634. Springer

  • He S, Abad AR, Gelvin SB, Mackenzie SA (1996) A cytoplasmic male sterility-associated mitochondrial protein causes pollen disruption in transgenic tobacco. Proc Natl Acad Sci U S A 93:11763–11768

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Horn R, Köhler RN, Zetsche K (1991) A mitochondrial 16-kDa protein is associated with cytoplasmic male sterility in sunflower. Plant Mol Biol 17:29–36

    Article  CAS  PubMed  Google Scholar 

  • Hsieh K, Huang AH (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19:582–596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang J, Struck F, Matzinger DF, Levings CS (1994) Flower-enhanced expression of a nuclear-encoded mitochondrial respiratory protein is associated with changes in mitochondrion number. Plant Cell 6:439–448

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang PL, Wang CS, Hsu CM, Jauh GY, Tzen JT (2007) Stable oil bodies sheltered by a unique oleosin in lily pollen. Plant Cell Physiol 48:812–821

    Article  CAS  PubMed  Google Scholar 

  • Jing B, Heng S, Tong D, Wan Z, Fu T, Tu J, Ma C, Yi B, Wen J, Shen J (2012) A male sterility-associated cytotoxic protein ORF288 in Brassica juncea causes aborted pollen development. J Exp Bot 63:1285–1295

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Karklelienė R, Bobinas Č, Stanienė G (2005) Combining ability of morphological traits and biochemical parameters in carrot (Daucus sativus Röhl.) CMS lines. Biologija 3:15–18

    Google Scholar 

  • Knabe W, Kuhn HJ (1996) The role of microtubules and microtubule-organising centres during the migration of mitochondria. J Anat 189:383–391

    PubMed Central  PubMed  Google Scholar 

  • Ku S, Yoon H, Suh HS, Chung YY (2003) Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta 217:559–565

    Article  CAS  PubMed  Google Scholar 

  • Lee SLJ, Warmke H (1979) Organelle size and number in fertile and T-cytoplasmic male-sterile corn. Am J Bot 66:141–148

    Article  Google Scholar 

  • León G, Holuigue L, Jordana X (2007) Mitochondrial complex II is essential for gametophyte development in Arabidopsis. Plant Physiol 143:1534–1546

    Article  PubMed Central  PubMed  Google Scholar 

  • Li X, Wang X, Yang Y, Li R, He Q, Fang X, Luu DT, Maurel C, Lin J (2011) Single-molecule analysis of PIP2; 1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23:3780–3797

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Linke B, Nothnagel T, Börner T (2003) Flower development in carrot CMS plants: mitochondria affect the expression of MADS box genes homologous to GLOBOSA and DEFICIENS. Plant J 34:27–37

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Butow RA (2006) Mitochondrial retrograde signaling. Annu Rev Genet 40:159–185

    Article  CAS  PubMed  Google Scholar 

  • Liu ZG, Yang YL, Hu TM, Wang YL, Xu R, Lei YN, He J (2012) antioxidant and osmoregulation substance properties of flower buds in Platycodon grandiflorus male sterile lines. Acta Prataculturae sinica 21:77–82 (in Chinese)

    Google Scholar 

  • Mackenzie SA, Chase CD (1990) Fertility restoration is associated with loss of a portion of the mitochondrial genome in cytoplasmic male-sterile common bean. Plant Cell 2:905–912

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Makaroff CA, Palmer JD (1988) Mitochondrial DNA rearrangements and transcriptional alterations in the male-sterile cytoplasm of Ogura radish. Mol Cell Biol 8:1474–1480

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mathilde G, Ghislaine G, Daniel V, Georges P (2003) The Arabidopsis MEI1 gene encodes a protein with five BRCT domains that is involved in meiosis-specific DNA repair events independent of SPO11-induced DSBs. Plant J 35:465–475

    Article  CAS  PubMed  Google Scholar 

  • Mayfield JA, Preuss D (2000) Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat Cell Biol 2:128–130

    Article  CAS  PubMed  Google Scholar 

  • Mazzafera P (1991) Biochemical characterization of anthers from male-sterile coffee plants. Revista Brasileira de Genética (Brasil) 14:413–423

    CAS  Google Scholar 

  • Mihr C, Baumgärtner M, Dieterich JH, Schmitz UK, Braun HP (2001) Proteomic approach for investigation of cytoplasmic male sterility (CMS) in Brassica. J Plant Physiol 158:787–794

    Article  CAS  Google Scholar 

  • Murata T, Goshima F, Daikoku T, Inagaki-Ohara K, Takakuwa H, Kato K, Nishiyama Y (2000) Mitochondrial distribution and function in herpes simplex virus-infected cells. J Gen Virol 81:401–406

    CAS  PubMed  Google Scholar 

  • Nakajima Y, Yamamoto T, Muranaka T, Oeda K (2001) A novel orfB-related gene of carrot mitochondrial genomes that is associated with homeotic cytoplasmic male sterility (CMS). Plant Mol Biol 46:99–107

    Article  CAS  PubMed  Google Scholar 

  • Nakashima H (1978) Physiological and morphological studies on the cytoplasmic male sterility of some crops. Journal of the Faculty of Agriculture, Hokkaido University 59:17–58

    CAS  Google Scholar 

  • Namasivayam PHD (2006) Identification of differentially expressed sequences in pre-embryonic tissue of oilseed rape by suppression subtractive hybridization (SSH). Plant Cell Tiss Org Cult 86:417–421

    Article  CAS  Google Scholar 

  • Papini A, Mosti S, Brighigna L (1999) Programmed-cell-death events during tapetum development of angiosperms. Protoplasma 207:213–221

    Article  Google Scholar 

  • Paulmann W, Röbbelen G (1988) Effective transfer of cytoplasmic male sterility from radish (Raphanus sativus L.) to Rape (Brassiest napus L.). Plant Breed 100:299–309

    Article  Google Scholar 

  • Pelletier G, Budar F (2007) The molecular biology of cytoplasmically inherited male sterility and prospects for its engineering. Curr Opin Biotechnol 18:121–125

    Article  CAS  PubMed  Google Scholar 

  • Perez-Prat E, van Lookeren Campagne MM (2002) Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci 7:199–203

    Article  CAS  PubMed  Google Scholar 

  • Picault N, Hodges M, Palmieri L, Palmieri F (2004) The growing family of mitochondrial carriers in Arabidopsis. Trends Plant Sci 9:138–146

    Article  CAS  PubMed  Google Scholar 

  • Pierson ES, Cresti M (1992) Cytoskeleton and cytoplasmic organization of pollen and pollen tubes. Int Rev Cytol 140:73–125

    Article  CAS  Google Scholar 

  • Piffanelli P, Murphy DJ (1998) Novel organelles and targeting mechanisms in the anther tapetum. Trends Plant Sci 3:250–252

    Article  Google Scholar 

  • Pruvot JC, Kräling K, Charne D, Tulsieram L (1999) Development of low glucosinolate restorer and Ogu CMS winter rape hybrid. Proceedings of 10th International Rapeseed Congress, Canberra Australia

  • Reddy TV, Kaur J, Agashe B, Sundaresan V, Siddiqi I (2003) The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein. Development 130:5975–5987

    Article  CAS  PubMed  Google Scholar 

  • Rhoads DM, Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7:177–194

    Article  CAS  PubMed  Google Scholar 

  • Robison MM, Wolyn DJ (2006) Petaloid-type cms in carrot is not associated with expression of atp8 (orfB). Theor Appl Genet 112:1496–1502

    Article  CAS  PubMed  Google Scholar 

  • Sabar M, Gagliardi D, Balk J, Leaver CJ (2003) ORFB is a subunit of F1FO-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep 4:381–386

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sakata T, Higashitani A (2008) Male sterility accompanied with abnormal anther development in plants—genes and environmental stresses with special reference to high temperature injury. Int J Plant Dev Biol 2:42–51

    Google Scholar 

  • Sane AP, Nath P, Sane PV (1997) Differences in kinetics of F1 ATPases of cytoplasmic male sterile, maintainer and fertility restored lines of sorghum. Plant Sci 130:19–25

    Article  CAS  Google Scholar 

  • Satoh Y, Nagai M, Mikami T, Kinoshita T (1993) The use of mitochondrial DNA polymorphism in the classification of individual onion plants by cytoplasmic genotypes. Theor Appl Genet 86:345–348

    CAS  PubMed  Google Scholar 

  • Saumitou-Laprade P, Cuguen J, Vernet P (1994) Cytoplasmic male sterility in plants: molecular evidence and the nucleocytoplasmic conflict. Trends Ecol Evol 9:431–435

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180

    Article  Google Scholar 

  • Shi Y, Zhao S, Yao J (2009) Premature tapetum degeneration: a major cause of abortive pollen development in photoperiod sensitive genic male sterility in rice. J Integr Plant Biol 51:774–781

    Article  PubMed  Google Scholar 

  • Shinjyo C (1969) Cytoplasmic-genetic male sterility in cultivated rice, Oryza sativa L. II. The inheritance of male sterility 1. Idengaku zasshi 44:149–156

    Google Scholar 

  • Sovero M (1987) Cytoplasmic male sterility in turnip-rape (Brassica campestris L.). Dissertation, p:132, University of Manitoba

  • Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG (1997) TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124:2645–2657

    CAS  PubMed  Google Scholar 

  • Stephens J, Holland R (1954) Cytoplasmic male-sterility for hybrid sorghum seed production. Agron J 46:20–23

    Article  Google Scholar 

  • Stevens R, Grelon M, Vezon D, Oh J, Meyer P, Perennes C, Domenichini S, Bergounioux C (2004) A CDC45 homolog in Arabidopsis is essential for meiosis, as shown by RNA interference–induced gene silencing. Plant Cell 16:99–113

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Teixeira RT, Farbos I, Glimelius K (2005a) Expression levels of meristem identity and homeotic genes are modified by nuclear-mitochondrial interactions in alloplasmic male-sterile lines of Brassica napus. Plant J 42:731–742

    Article  CAS  PubMed  Google Scholar 

  • Teixeira RT, Knorpp C, Glimelius K (2005b) Modified sucrose, starch, and ATP levels in two alloplasmic male-sterile lines of B. napus. J Exp Bot 56:1245–1253

    Article  CAS  PubMed  Google Scholar 

  • Tian HQ, Kuang A, Musgrave ME, Russell SD (1998) Calcium distribution in fertile and sterile anthers of a photoperiod-sensitive genic male-sterile rice. Planta 204:183–192

    Article  CAS  Google Scholar 

  • Tsuwamoto R, Fukuoka H, Takahata Y (2007) Identification and characterization of genes expressed in early embryogenesis from microspores of Brassica napus. Planta 225:641–652

    Article  CAS  PubMed  Google Scholar 

  • Wang YY, Lu D, Wei DM, Lin WX, Tian HQ (2006a) The distribution of ATPase in developmental anther of rice. J Plant Physiol Mol Biol 32:113–122 (in Chinese)

    CAS  Google Scholar 

  • 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 YG (2006b) 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 18:676–687

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Warmke H, Lee SLJ (1977) Mitochondrial degeneration in Texas cytoplasmic male-sterile corn anthers. J Hered 68:213–222

    Google Scholar 

  • Wei YT, Zhang L, Zhang DX, Liang SL (2011) Studies on the substances metabolism during the development of male sterile microspores in radish. Liaoning Agric Sci 4:8–10 (in Chinese)

    Google Scholar 

  • Wen L, Liu G, Li SQ, Wan CX, Tao J, Xu KY, Zhang ZJ, Zhu YG (2007) Proteomic analysis of anthers from Honglian cytoplasmic male sterility line rice and its corresponding maintainer and hybrid. Bot Stud 48:293–309

    CAS  Google Scholar 

  • Wu HM, Cheun AY (2000) Programmed cell death in plant reproduction. Plant Mol Biol 44:267–281

    Article  PubMed  Google Scholar 

  • Wu JY, Yamg GS (2008) Meiotic abnormality in dominant genic male sterile Brassica napus. Mol Biol 42:645–651

    CAS  Google Scholar 

  • Xu J, Yang C, Yuan Z, Zhang D, Gondwe MY, Ding Z, Liang W, Wilson ZA (2010) The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. Plant Cell 22:91–107

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamashita K-i, Tashiro Y (2004) Seed productivity test of CMS lines of Japanese bunching onion (Allium fistulosum L.) possessing the cytoplasm of a wild species, A. galanthum Kar. et Kir. Euphytica 136:327–331

    Google Scholar 

  • Yanada KI, Yamada K, Matsuzawa A, Tanaka I, Shiota H (2010) Lilly pollen protoplast system for functional analysis of plant aquaporins [abstract]. Proceedings of 21st International Conference On Arabidopsis Research

  • Yang M, Hu Y, Lodhi M, McCombie WR, Ma H (1999) The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proc Natl Acad Sci U S A 96:11416–11421

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang X, Makaroff CA, Ma H (2003) The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 15:1281–1295

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang JH, Zhang MF, Yu JQ (2008) Relationship between cytoplasmic male sterility and SPL-like gene expression in stem mustard. Physiol Plant 133:426–434

    Article  CAS  PubMed  Google Scholar 

  • Young EG, Hanson MR (1987) A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 50:41–49

    Article  CAS  PubMed  Google Scholar 

  • Yui R, Iketani S, Mikami T, Kubo T (2003) Antisense inhibition of mitochondrial pyruvate dehydrogenase E1alpha subunit in anther tapetum causes male sterility. Plant J 34:57–66

    Article  CAS  PubMed  Google Scholar 

  • Zhang JY, Li Y, Shi GJ, Chen XF, Wang JJ, Hou XL (2009) Characterization of α-tubulin gene distinctively presented in a cytoplasmic male sterile and its maintainer line of non-heading Chinese cabbage. J Sci Food Agric 89:274–280

    Article  CAS  Google Scholar 

  • Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154:149–162

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao D, Han T, Risseeuw E, Crosby WL, Ma H (2003) Conservation and divergence of ASK1 and ASK2 gene functions during male meiosis in Arabidopsis thaliana. Plant Mol Biol 53:163–173

    Article  CAS  PubMed  Google Scholar 

  • Zhou MB, Yang P, Gao PJ, Tang DQ (2011) Identification of differentially expressed sequence tags in rapidly elongating Phyllostachys pubescens internodes by suppressive subtractive hybridization. Plant Mol Biol Rep 29:224–231

    Article  Google Scholar 

  • Zou J, Lin WH, Luo HB, Sun LZ, Liu C (2009) Relationship between contents of soluble sugar, soluble protein and free proline and C-cytoplasmic male sterility in maize. J Hunan Agric Univ 35:249–251 (in Chinese)

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31272173, 31301782), the National High Technology Research and Development Program of China (863 Program, 2012AA100101, 2012AA100202), the Natural Science Foundation of Jiangsu Province (BK2011643, BK20130673), and the Science and Technology Innovation Fund of Nanjing Agricultural University (KYZ201111, KJ2013015).

Author information

Authors and Affiliations

  1. College of Horticulture, Nanjing Agricultural University, Weigang 1#, Xuanwu district, Nanjing, Jiangsu, 210095, China

    Ying Li, Tongkun Liu, Weike Duan, Xiaoming Song, Gongjun Shi, Jingyi Zhang, Xiaohui Deng, Shuning Zhang & Xilin Hou

  2. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China

    Ying Li, Tongkun Liu, Weike Duan, Xiaoming Song, Shuning Zhang & Xilin Hou

  3. Key laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    Ying Li, Tongkun Liu, Weike Duan, Xiaoming Song, Shuning Zhang & Xilin Hou

Authors
  1. Ying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tongkun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Weike Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoming Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gongjun Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jingyi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaohui Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shuning Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xilin Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xilin Hou.

Additional information

Ying Li and Tongkun Liu contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. S1

Analysis of subtraction efficiency by PCR. (DOC 163 kb)

Supplementary Table S1

Putative identities of cDNA clones from forward SSH library. (XLS 68 kb)

Supplementary Table S2

Putative identities of cDNA clones from reverse SSH library. (XLS 44 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, Y., Liu, T., Duan, W. et al. Instability in mitochondrial membranes in Polima cytoplasmic male sterility of Brassica rapa ssp. chinensis . Funct Integr Genomics 14, 441–451 (2014). https://doi.org/10.1007/s10142-014-0368-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-014-0368-1

Keywords

Search

Navigation