Skip to main content

Advertisement

SpringerLink
Log in

Maize Male sterile 8 (Ms8), a putative β-1,3-galactosyltransferase, modulates cell division, expansion, and differentiation during early maize anther development

  • Original Article
  • Published:
Plant Reproduction Aims and scope Submit manuscript

Abstract

Precise somatic and reproductive cell proliferation and differentiation in anthers are crucial for male fertility. Loss of function of the Male sterile 8 (Ms8) gene causes male sterility with multiple phenotypic defects first visible in the epidermal and tapetal cells. Here, we document the cloning of Ms8, which is a putative β-1,3-galactosyltransferase. Ms8 transcript is abundant in immature anthers with a peak at the meiotic stage; RNA expression is highly correlated with protein accumulation. Co-immunoprecipitation coupled with mass spectrometry sequencing identified several MS8-associated proteins, including arabinogalactan proteins, prohibitins, and porin. We discuss the hypotheses that arabinogalactan protein might be an MS8 substrate and that MS8 might be involved in maintenance of mitochondrial integrity.

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

Abbreviations

Ms8 :

Male sterile 8

AGP:

Arabinogalactan proteins

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Borderies G, le Béchec M, Rossignol M, Lafitte C, Le Deunff E, Beckert M, Dumas C, Elisabeth MR (2004) Characterization of proteins secreted during maize microspore culture: arabinogalactan proteins (AGPs) stimulate embryo development. Eur J Cell Biol 83:205–212

    Article  PubMed  CAS  Google Scholar 

  • Chen L, Miao Y, Wang C, Su P, Li T, Wang R, Hao X, Yang G, He G, Gao C (2012) Characterization of a novel pollen-specific promoter from wheat (Triticum aestivum L.). Plant Mol Biol Rep 30:1426–1432

    Article  CAS  Google Scholar 

  • Conley C, Hanson M (1994) Tissue-specific protein expression in plant mitochondria. Plant Cell 6:85–91

    PubMed  CAS  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469

    Article  Google Scholar 

  • Dereeper A, Audic S, Claverie JM, Blanc G (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 10:1–6

    Google Scholar 

  • Duvick DN, Smith JSC, Cooper M (2004) Long term selection in a commercial hybrid maize breeding program. In: Janick J (ed) Plant Breeding Reviews, Part 2: Long-term selection: crops, animals, and bacteria. Wiley, New York, pp 109–151

    Google Scholar 

  • Forsthoefel NR, Vernon DM (2011) Effect of sporophytic PIRL9 genotype on post-meiotic expression of the Arabidopsis pirl1:pirl9 mutant phenotype. Planta 233:423–431

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T, Yano K, Yamaki S, Tsuda K, Nagata T, Niihama M, Kato H, Kikuchi S, Hamada K, Mochizuki T, Ishimizu T, Iwai H, Tsutsumi N, Kurata N (2010) Rice expression atlas in reproductive development. Plant Cell Physiol 51:2060–2081

    Article  PubMed  CAS  Google Scholar 

  • Golubovskaya I, Grebennikova ZK, Avalkina NA, Sheridan WF (1993) The role of the ameiotic1 gene in the initiation of meiosis and in subsequent meiotic events in maize. Genet 135:1151–1166

    CAS  Google Scholar 

  • Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312

    Article  PubMed  CAS  Google Scholar 

  • Hamilton DA, Schwarz YH, Mascarenhas JP (1998) A monocot pollen-specific promoter contains separable pollen-specific and quantitative elements. Plant Mol Biol 38:663–669

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hu L, Tan H, Liang W, Zhang D (2010) The post-meiotic deficient anther 1 (PDA1) gene is required for post-meiotic anther development in rice. J Genet Genomics 37:37–46

    Article  PubMed  CAS  Google Scholar 

  • Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D (2011) Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23:515–533

    Article  PubMed  CAS  Google Scholar 

  • Isaac PG, Brennicke A, Dunbar SM, Leaver CJ (1985) The mitochondrial genome of fertile maize (Zea mays L.) contains two copies of the gene encoding the α-subunit of the F1-ATPase. Current Genet 10:321–328

    Article  CAS  Google Scholar 

  • Ito T, Shinozaki K (2002) The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol 43:1285–1292

    Article  PubMed  CAS  Google Scholar 

  • Izhar S, Frankel R (1971) Mechanism of male sterility in Petunia: the relationship between Ph, callose activity in the anthers and the breakdown of the microsporogenesis. Theor Applied Genet 41:104–108

    Google Scholar 

  • Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Hahm BH, An G (2005) Rice undeveloped tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722

    Article  PubMed  CAS  Google Scholar 

  • Jung KH, Han MJ, Lee D, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18:3015–3032

    Article  PubMed  CAS  Google Scholar 

  • Kalantidis K, Wilson ZA, Mulligan BJ (2002) Mitochondrial gene expression in stamens is differentially regulated during male gametogenesis in Arabidopsis. Sex Plant Reprod 14:299–304

    Article  CAS  Google Scholar 

  • Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, Matsuoka M (2004) Loss-of-function mutations of the rice GAMYB gene impair amylase expression in aleurone and flower development. Plant Cell 16:33–44

    Article  PubMed  CAS  Google Scholar 

  • Kasashima K, Ohta E, Kagawa Y, Endo H (2006) Mitochondrial functions and estrogen receptor-dependent nuclear translocation of pleiotropic human prohibitin 2. J Biol Chem 281:36401–36410

    Article  PubMed  CAS  Google Scholar 

  • Kelliher T, Walbot V (2012) Hypoxia triggers meiotic fate acquisition in maize. Science 337:345–348

    Article  PubMed  CAS  Google Scholar 

  • Lang Z, Zhou P, Yu J, Ao G, Zhao Q (2008) Functional characterization of the pollen-specific SBgLR promoter from potato (Solanum tuberosum L.). Planta 227:387–396

    Article  PubMed  CAS  Google Scholar 

  • Laver H, Reynolds S, Monéger F, Leaver C (1991) Mitochondrial genome organisation and expression associated with cytoplasmic male sterility in sunflower (Helianthus annuus). Plant J 1:185–193

    Article  PubMed  CAS  Google Scholar 

  • Li XQ, Zhang M, Brown GG (1996) Cell-specific expression of mitochondrial transcripts in maize seedlings. Plant Cell 8:1961–1975

    PubMed  CAS  Google Scholar 

  • Li N, Zhang D, Liu H, Yin C, Li X, Liang W, Yuan Z, Xu B, Chu H, Wang J, Wen T, Huang H, Luo D, Ma H, Zhang D (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014

    Article  PubMed  CAS  Google Scholar 

  • Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D (2011a) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630

    Article  PubMed  CAS  Google Scholar 

  • Li X, Gao X, Wei L, Deng L, Ouyang Y, Chen G, Li X, Zhang Q, Wu C (2011b) Rice APOPTOSIS INHIBITOR5 coupled with two DEAD-Box adenosine 59-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant Cell 23:1416–1434

    Article  PubMed  CAS  Google Scholar 

  • Logan DC, Millar AH, Sweetlove LJ, Hill SA, Leaver CJ (2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiol 125:662–672

    Article  PubMed  CAS  Google Scholar 

  • Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Skibbe DS, Fernandes J, Walbot V (2008) Male reproductive development: gene expression profiling of maize anther and pollen ontogeny. Genome Biol 9:R181

    Article  PubMed  Google Scholar 

  • Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of Arabinogalactan proteins in plant development. Plant Physiol 122:3–9

    Article  PubMed  CAS  Google Scholar 

  • May BP, Liu H, Vollbrecht E, Senior L, Rabinowicz PD, Roh D, Pan X, Stein L, Freeling M, Alexander D, Martienssen R (2003) Maize-targeted mutagenesis: a knockout resource for maize. Proc Natl Acad Sci USA 100:11541–11546

    Article  PubMed  CAS  Google Scholar 

  • Mihara K, Sato R (1985) Molecular cloning and sequencing of cDNA for yeast porin, an outer mitochondrial membrane protein: a search for targeting signal in the primary structure. EMBO J 4:769–774

    PubMed  CAS  Google Scholar 

  • Monéger F, Smart CJ, Leaver CJ (1994) Nuclear restoration of cytoplasmic male sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. EMBO J 13:8–17

    PubMed  Google Scholar 

  • Muschietti J, Dircks L, Vancanneyt G, McCormick S (1994) LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J 6:321–338

    Article  PubMed  CAS  Google Scholar 

  • Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80

    Article  CAS  Google Scholar 

  • Qu Y, Egelund J, Gilson PR, Houghton F, Gleeson PA, Schultz CJ, Bacic A (2008) Identification of a novel group of putative Arabidopsis thaliana β-(1,3)-galactosyltransferases. Plant Mol Biol 68:43–59

    Article  PubMed  CAS  Google Scholar 

  • Raizada MN, Benito MI, Walbot V (2001) The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs. Plant J 25:1–15

    Article  Google Scholar 

  • Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh herbarium and mummified plant tissues. Plant Mol Biol 5:69–76

    Article  CAS  Google Scholar 

  • Schindler T, Bergfeld R, Schopfer P (1995) Arabinogalactan proteins in maize coleoptiles: developmental relationship to cell death during xylem differentiation but not to extension growth. Plant J 7:25–36

    Article  PubMed  CAS  Google Scholar 

  • Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417

    Article  PubMed  CAS  Google Scholar 

  • Skibbe DS, Fernandes JF, Medzihradszky KF, Burlingame AL, Walbot V (2009) Mutator transposon activity reprograms the transcriptomes and proteomes of developing maize anthers. Plant J 59:622–633

    Article  PubMed  CAS  Google Scholar 

  • Smart CJ, Monéger F, Leaver CJ (1994) Cell-specific regulation of gene expression in mitochondria during anther development in sunflower. Plant Cell 6:811–825

    PubMed  CAS  Google Scholar 

  • Sorensen AM, Krober S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423

    Article  PubMed  CAS  Google Scholar 

  • Strasser R, Bondili JS, Vavra U, Schoberer J, Svoboda B, Glossl J, Leonard R, Stadlmann J, Altmann F, Steinkellner H, Mach L (2007) A unique β-1,3-galactosyltransferase is indispensable for the biosynthesis of N-Glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19:2278–2292

    Article  PubMed  Google Scholar 

  • Subbaiah CC, Palaniappan A, Duncan K, Rhoads DM, Huber SC, Sachs MM (2006) Mitochondrial localization and putative signaling function of sucrose synthase in maize. J Biol Chem 281:15625–15635

    Article  PubMed  CAS  Google Scholar 

  • Tang W, Ezcurra I, Muschietti J, McCormick S (2002) A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 14:2277–2287

    Article  PubMed  CAS  Google Scholar 

  • Tao J, Zhang L, Chong K, Wang T (2007) OsRAD21-3, an orthologue of yeast rad21, is required for pollen development in Oryza sativa. Plant J 51:919–930

    Article  PubMed  CAS  Google Scholar 

  • Tatsuta T, Model K, Langer T (2005) Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 16:248–259

    Article  PubMed  CAS  Google Scholar 

  • Twell D, Wing R, Yamaguchi J, McCormick S (1989) Isolation and expression of an anther-specific gene from tomato. Mol Gen Genet 217:240–245

    Article  PubMed  CAS  Google Scholar 

  • Twell D, Yamaguchi J, McCormick S (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Dev 109:705–713

    CAS  Google Scholar 

  • Walbot V, Qüesta J (2013) Plant Transposable Elements: Methods and Protocols in the Methods in Molecular Biology series. Humana Press Inc, New York

    Google Scholar 

  • Walbot V, Rudenko GN (2002) MuDR/Mu transposons of maize. In: Craig NL, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II. Amer. Soc, Microbiology, Washington, D. C, pp 533–564

    Google Scholar 

  • Wang D, Oses-Prieto JA, Li KH, Fernandes J, Burlingame AL, Walbot V (2010) The Male sterile 8 mutation of maize disrupts the temporal progression of the transcriptome and results in the mis-regulation of metabolic functions. Plant J 63:939–951

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Skibbe DS, Walbot V (2011) Maize csmd1 exhibits pre-meiotic somatic and post-meiotic microspore and somatic defects but sustains anther growth. Sex Plant Reprod 24:297–306

    Article  PubMed  CAS  Google Scholar 

  • Wang CR, Nan GL, Kelliher T, Timofejeva L, Vernoud V, Golubovskaya IN, Harper L, Egger R, Walbot V, Cande WZ (2012a) Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Dev 139:2594–2603

    Article  CAS  Google Scholar 

  • Wang D, Adams CM, Fernandes JF, Egger RL, Walbot V (2012b) A low molecular weight proteome comparison of fertile and Male sterile 8 anthers of Zea mays. Plant Biotech J 10:925–935

    Article  Google Scholar 

  • Warmke HE, Overman MA (1972) Cytoplasmic male sterility in sorghum. I. Callose behaviour in fertile and sterile anther. J Hered 63:103–108

    Google Scholar 

  • Wilson ZA, Zhang D (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492

    Article  PubMed  CAS  Google Scholar 

  • Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD finger family of transcription factors. Plant J 28:27–39

    Article  PubMed  CAS  Google Scholar 

  • Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 4:759–771

    PubMed  CAS  Google Scholar 

  • Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19:3530–3548

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zeth K, Thein M (2010) Porins in prokaryotes and eukaryotes: common themes and variations. Biochem J 431:13–22

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Dev 133:3085–3095

    Article  CAS  Google Scholar 

  • Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX, Huang H, Xia HJ, Yang ZN (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52:528–538

    Article  PubMed  CAS  Google Scholar 

  • Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1045–1062

    Google Scholar 

  • Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Zhang GQ, Chang YH, Li XC, Yang J, Huang XY, Yu QB, Chen H, Wu TL, Yang ZN (2010) AtMYB103 is a key regulator for several pathways during Arabidopsis anther development. Sci China (C) 53:1112–1122

    Article  CAS  Google Scholar 

  • Zhu J, Lou Y, Xu X, Yang Z (2011) A genetic pathway for tapetum development and function in Arabidopsis. J of Integrative Plant Biol 53:892–900

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Professors Matt Ritter and Jeffrey Wong of Cal Poly-San Luis Obispo for organizing the summer screening field and assisting in the training of undergraduate field staff to conduct the screen of directed Mu transposon tagging of ms8. We thank Dr. Jung-Gun Kim in Mary Beth Mudgett’s laboratory for help with Western blotting and the Co-IP assays; Dr. Christopher M. Adams at the Vincent Coates Foundation Mass-spectrometry Laboratory at Stanford University conducted the protein sequencing. We are also grateful to the editor and two anonymous reviewers for advice on this paper. Research supported by a grant from the National Science Foundation (PGRP 07-01880).

Author information

Author notes

  1. Dongxue Wang

    Present address: Department of Biology, Emory University, Atlanta, GA, 30322, USA

  2. David S. Skibbe

    Present address: Syngenta, 317 330th Street, Stanton, MN, 55018, USA

Authors and Affiliations

  1. Department of Biology, Stanford University, Stanford, CA, 94305-5020, USA

    Dongxue Wang, David S. Skibbe & Virginia Walbot

Authors
  1. Dongxue Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David S. Skibbe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Virginia Walbot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dongxue Wang.

Additional information

Communicated by H. G. Dickinson.

Dongxue Wang and David S. Skibbe have contributed equally to this study.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, D., Skibbe, D.S. & Walbot, V. Maize Male sterile 8 (Ms8), a putative β-1,3-galactosyltransferase, modulates cell division, expansion, and differentiation during early maize anther development. Plant Reprod 26, 329–338 (2013). https://doi.org/10.1007/s00497-013-0230-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-013-0230-y

Keywords

Search

Navigation