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Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats

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Abstract

Class-B floral homeotic genes are involved in specifying petal and stamen identity during flower development in plant species. Homeotic transformation of stamens into pistil-like structures (called pistillody) has been observed in alloplasmic lines of bread wheat (Triticum aestivum L.) having the cytoplasm of a wild relative species, Aegilops crassa Boiss. To obtain information about the molecular mechanism underlying pistillody induction, we isolated two PISTILLATA (PI)-type class-B MADS-box genes, WPI1 (wheat PI STILLATA # 1) and WPI2, from wheat. Phylogenetic reconstruction indicated that WPI1 is orthologous to OsMADS4 and that WPI2 is probably an ortholog of OsMADS2. Both OsMADS4 and OsMADS2 genes were suggested to be PI orthologs in rice, and the function of OsMADS4 as a class-B gene was proven by the transgenic study. An in situ hybridization study demonstrated that the WPI1 gene is expressed in primordia of lodicules and stamens in developing florets in wheat. In the alloplasmic wheat line exhibiting pistillody, the WPI1 transcripts were not detected in the primordia of pistil-like stamens, whereas WPI1 was expressed in the lodicules. The wheat APETALA3 (AP3)-type class-B MADS-box gene WAP3 (wheat AP3)/TaMADS#82 showed an expression pattern similar to that of WPI1. These results suggest that pistillody in alloplasmic wheats is caused by alterations to the expression pattern of class-B MADS-box genes.

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Abbreviations

AG :

AGAMOUS

AP1 :

APETALA1

AP2 :

APETALA2

AP3 :

APETALA3

CMS :

Cytoplasmic male sterility

CS :

Chinese Spring

EST :

Expressed sequence tag

N26 :

Norin 26

P :

PISTILLATA

SEP1 :

SEPALLATA1

SEP2 :

SEPALLATA2

SEP3 :

SEPALLATA3

SUP :

SUPERMAN

WAP3 :

Wheat APETALA3

WPI1 :

Wheat PISTILLATA#1

WPI2 :

Wheat PISTILLATA#2

References

  • Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569–579

    CAS  PubMed  Google Scholar 

  • Angenent GC, Colombo L (1996) Molecular control of ovule development. Trends Plant Sci 1:228–232

    Article  Google Scholar 

  • Bereterbide A, Hernould M, Farbos I, Glimelius K, Mouras A (2002) 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 29:607–615

    Article  CAS  PubMed  Google Scholar 

  • Chung Y-Y, Kim S-R, Kang H-G, Noh Y-S, Park MC, Finkel D, An G (1995) Characterization of two rice MADS box genes homologous to GLOBOSA. Plant Sci 109:45–56

    CAS  Google Scholar 

  • Davies B, Schwarz-Sommer Z (1994) Control of floral organ identity by homeotic MADS-box transcription factors. In: Nover L (ed) Plant promoters and transcription factors. Springer, Berlin Heidelberg New York, pp 235–258

  • Feldman M (2001) Origin of cultivated wheat. In: Bonjean AP, Angus WJ (eds) The world wheat book. A history of wheat breeding. Lavoisier, Paris, pp 3–56

  • Farbos I, Mouras A, Bereterbide A, Glimelius K (2001) Defective cell proliferation in the floral meristem of alloplasmic plants of Nicotiana tabacum leads to abnormal floral organ development and male sterility. Plant J 26:131–142

    Article  CAS  PubMed  Google Scholar 

  • Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1560

    CAS  PubMed  Google Scholar 

  • Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529

    CAS  PubMed  Google Scholar 

  • Jack T, Brockman LL, Meyerowitz EM (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683–697

    CAS  PubMed  Google Scholar 

  • Johansen B, Pedersen LB, Skipper M, Frederiksen S (2002) MADS-box gene evolution—structure and transcription patterns. Mol Phylogenet Evol 23:458–480

    CAS  PubMed  Google Scholar 

  • Kang H-G, Jeon J-S, Lee S, An G (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol Biol 38:1021–1029

    CAS  PubMed  Google Scholar 

  • Kaul MLH (1988) Male sterility in higher plants. Monographs of Theor Appl Genet, vol 10. Springer, Berlin Heidelberg New York

  • Kramer EM, Dorit RL, Irish VF (1998) Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149:765–783

    CAS  PubMed  Google Scholar 

  • Kyozuka J, Shimamoto K (2002) Ectopic expression of OsMADS3, a rice ortholog of AGAMOUS, caused a homeotic transformation of lodicules to stamens in transgenic rice plants. Plant Cell Physiol 43:130–135

    CAS  PubMed  Google Scholar 

  • Kyozuka J, Kobayashi T, Morita M, Shimamoto K (2000) Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol 41:710–718

    CAS  PubMed  Google Scholar 

  • Linke B, Nothnagel T, Borner 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

    CAS  PubMed  Google Scholar 

  • Ma H (1994) The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev 8:745–756

    CAS  PubMed  Google Scholar 

  • McGonigle B, Bouhidel K, Irish VF (1996) Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes Dev 10:1812–1821

    CAS  PubMed  Google Scholar 

  • Meguro A, Takumi S, Ogihara Y, Murai K (2003) WAG, a wheat AGAMOUS homolog, is associated with development of pistil-like stamens in alloplasmic wheats. Sex Plant Reprod 15:221–230

    CAS  Google Scholar 

  • Moon Y-H, Jung J-Y, Kang H-G, An G (1999) Identification of a rice APETALA3 homologue by yeast two-hybrid screening. Plant Mol Biol 40:167–177

    CAS  PubMed  Google Scholar 

  • Münster T, Wingen LU, Faigl W, Werth S, Saedler H, Theissen G (2001) Characterization of three GLOBOSA-like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses. Gene 262:1–13

    Article  PubMed  Google Scholar 

  • Murai K, Tsunewaki K (1993) Photoperiod-sensitive cytoplasmic male sterility in wheat with Aegilops crassa cytoplasm. Euphytica 67:41–48

    Google Scholar 

  • Murai K, Tsunewaki K (1994) Genetic analysis on the fertility restoration by Triticum aestivum cv. Chinese Spring against photoperiod-sensitive cytoplasmic male sterility. Jpn J Genet 69:195–202

    Google Scholar 

  • Murai K, Murai R, Ogihara Y (1997) Wheat MADS box genes, a multigene family dispersed throughout the genome. Genes Genet Syst 72:317–321

    CAS  PubMed  Google Scholar 

  • Murai K, Murai R, Takumi S, Ogihara Y (1998) Cloning and characterization of cDNAs corresponding to the wheat MADS box genes. Proc 9th Int Wheat Genet Symp 1:89–94

    Google Scholar 

  • Murai K, Takumi S, Koga H, Ogihara Y (2002) Pistillody, homeotic transformation of stamens into pistil-like structures, caused by nuclear-cytoplasm interaction in wheat. Plant J 29:169–181

    Article  PubMed  Google Scholar 

  • Ogihara Y, Futami K, Tsuji K, Murai K (1997) Alloplasmic wheats with Aegilops crassa cytoplasm which express photoperiod-sensitive homeotic transformations of anthers, show alterations in mitochondrial DNA structure and transcription. Mol Gen Genet 255:45–53

    Article  CAS  PubMed  Google Scholar 

  • Ogihara Y, Kurihara Y, Futami K, Tsuji K, Murai K (1999) Photoperiod-sensitive cytoplasmic male sterility in wheat: nuclear-mitochondrial incompatibility results in differential processing of the mitochondrial orf25 gene. Curr Genet 36:354–362

    Google Scholar 

  • Ogihara Y, Mochida K, Nemoto Y, Murai K, Yamazaki Y, Shin-I T, Kohara Y (2003) Correlated clustering and virtual display of gene expression patterns in the wheat life cycle by large-scale statistical analyses of expressed sequence tags. Plant J 33:1001–1011

    PubMed  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    CAS  PubMed  Google Scholar 

  • Pelaz S, Tapia-López R, Alvarez-Buylla ER, Yanofsky MF (2001) Conversion of leaves into petals in Arabidopsis. Curr Biol 11:182–184

    CAS  PubMed  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1101

    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 

  • Sommer H, Beltrán J-P, Huijser P, Pape H, Lönnig W-E, Saedler H, Schwarz-Sommer Z (1990) Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J 9:605–613

    CAS  PubMed  Google Scholar 

  • Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85

    CAS  PubMed  Google Scholar 

  • Theissen G, Saedler H (1999) The golden decade of molecular floral development (1990–1999): a cheerful obituary. Dev Genet 25:181–193

    CAS  PubMed  Google Scholar 

  • Theissen G, Kim JT, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43:484–516

    CAS  PubMed  Google Scholar 

  • Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter K-U, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Google Scholar 

  • Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig W-E, Saedler H, Sommer H, Schwarz-Sommer Z (1992) GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11:4693–4704

    PubMed  Google Scholar 

  • Tsuchimoto S, Mayama T, van der Krol A, Ohtsubo E (2000) The whorl-specific action of a petunia class B floral homeotic gene. Genes Cell 5:89–99

    CAS  PubMed  Google Scholar 

  • Tsunewaki K, Wang G-Z, Matsuoka Y (1996) Plasmon analysis of Triticum (wheat) and Aegilops. 1. Production of alloplasmic common wheats and their fertilities. Genes Genet Syst 71:293–311

    CAS  PubMed  Google Scholar 

  • Tsunewaki K, Wang G-Z, Matsuoka Y (2002) Plasmon analysis of Triticum (wheat) and Aegilops. 2. Characterization and classification of 47 plasmons based on their effects on common wheat phenotype. Genes Genet Syst 77:409–427

    CAS  PubMed  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    CAS  PubMed  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. H.-Y. Hirano for valuable suggestions. This work was supported in part by a Grant-in-Aid for Scientific Research (B) from the Ministry of Education, Science and Culture of Japan (No. 12460006 to K.M.) and from the Fukui Prefectural Government (to K.M.).

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  1. Eriko Hama

    Present address: Ishikawa Agricultural Research Center, Saida-machi, 920-3198, Kanazawa, Japan

Authors and Affiliations

  1. Department of Bioscience, Fukui Prefectural University, 4-1-1 Kenjojima, Yoshida-gun, Matsuoka-cho, 910-1195, Fukui, Japan

    Eriko Hama & Koji Murai

  2. Faculty of Agriculture, Kobe University, Rokkodai-cho, Nada-ku, 657-8501, Kobe, Japan

    Shigeo Takumi

  3. Kihara Institute for Biological Research and Graduate School for Integrated Science, Yokohama City University, Maioka-cho, 244-0813, Yokohama, Japan

    Yasunari Ogihara

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  1. Eriko Hama
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  4. Koji Murai
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Correspondence to Koji Murai.

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Hama, E., Takumi, S., Ogihara, Y. et al. Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218, 712–720 (2004). https://doi.org/10.1007/s00425-003-1157-6

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