Skip Navigation

This Article
Right arrow Full Text Freely available
Right arrow Print PDF (564K) Freely available
Right arrow Supplementary Material
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (67)
Right arrowRequest Permissions
Right arrow Commercial Re-use Guidelines
for Open Access NAR Content
Google Scholar
Right arrow Articles by Vandenbussche, M.
Right arrow Articles by Gerats, T.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Vandenbussche, M.
Right arrow Articles by Gerats, T.
Social Bookmarking
 Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

Nucleic Acids Research, 2003, Vol. 31, No. 15 4401-4409
© 2003 Oxford University Press

Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations

Michiel Vandenbussche*, Günter Theissen1, Yves Van de Peer and Tom Gerats

Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium and 1 Lehrstuhl for Genetics, Friedrich Schiller University of Jena, Philosophenweg 12, D-07743 Jena, Germany

*To whom correspondence should be addressed. Tel: +32 92645191; Fax: +32 92645349; Email: mibus{at}gengenp.rug.ac.be
Present address:
Tom Gerats, Department of Experimental Botany, University of Nijmegen, Toernooiveld 1, 6525ED, Nijmegen, The Netherlands

Frameshift mutations generally result in loss-of-function changes since they drastically alter the protein sequence downstream of the frameshift site, besides creating premature stop codons. Here we present data suggesting that frameshift mutations in the C-terminal domain of specific ancestral MADS-box genes may have contributed to the structural and functional divergence of the MADS-box gene family. We have identified putative frameshift mutations in the conserved C-terminal motifs of the B-function DEF/AP3 subfamily, the A-function SQUA/AP1 subfamily and the E-function AGL2 subfamily, which are all involved in the specification of organ identity during flower development. The newly evolved C-terminal motifs are highly conserved, suggesting a de novo generation of functionality. Interestingly, since the new C-terminal motifs in the A- and B-function subfamilies are only found in higher eudicotyledonous flowering plants, the emergence of these two C-terminal changes coincides with the origin of a highly standardized floral structure. We speculate that the frameshift mutations described here are examples of co-evolution of the different components of a single transcription factor complex. 3' terminal frameshift mutations might provide an important but so far unrecognized mechanism to generate novel functional C-terminal motifs instrumental to the functional diversification of transcription factor families.


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
Mol Biol EvolHome page
H. Shan, L. Zahn, S. Guindon, P. K. Wall, H. Kong, H. Ma, C. W. dePamphilis, and J. Leebens-Mack
Evolution of Plant MADS Box Transcription Factors: Evidence for Shifts in Selection Associated with Early Angiosperm Diversification and Concerted Gene Duplications
Mol. Biol. Evol., October 1, 2009; 26(10): 2229 - 2244.
[Abstract] [Full Text] [PDF]


Home page
J Exp BotHome page
S. K. Broholm, E. Pollanen, S. Ruokolainen, S. Tahtiharju, M. Kotilainen, V. A. Albert, P. Elomaa, and T. H. Teeri
Functional characterization of B class MADS-box transcription factors in Gerbera hybrida
J. Exp. Bot., September 18, 2009; (2009) erp279v1.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
R. Reinheimer and E. A. Kellogg
Evolution of AGL6-like MADS Box Genes in Grasses (Poaceae): Ovule Expression Is Ancient and Palea Expression Is New
PLANT CELL, September 1, 2009; 21(9): 2591 - 2605.
[Abstract] [Full Text] [PDF]


Home page
Plant Cell PhysiolHome page
Y.-Y. Chang, Y.-F. Chiu, J.-W. Wu, and C.-H. Yang
Four Orchid (Oncidium Gower Ramsey) AP1/AGL9-like MADS Box Genes Show Novel Expression Patterns and Cause Different Effects on Floral Transition and Formation in Arabidopsis thaliana
Plant Cell Physiol., August 1, 2009; 50(8): 1425 - 1438.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
M. Vandenbussche, A. Horstman, J. Zethof, R. Koes, A. S. Rijpkema, and T. Gerats
Differential Recruitment of WOX Transcription Factors for Lateral Development and Organ Fusion in Petunia and Arabidopsis
PLANT CELL, August 1, 2009; 21(8): 2269 - 2283.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
G. Xu, H. Ma, M. Nei, and H. Kong
Evolution of F-box genes in plants: Different modes of sequence divergence and their relationships with functional diversification
PNAS, January 20, 2009; 106(3): 835 - 840.
[Abstract] [Full Text] [PDF]


Home page
Plant Cell PhysiolHome page
M.-K. Chen, I-C. Lin, and C.-H. Yang
Functional Analysis of Three Lily (Lilium longiflorum) APETALA1-like MADS Box Genes in Regulating Floral Transition and Formation
Plant Cell Physiol., May 1, 2008; 49(5): 704 - 717.
[Abstract] [Full Text] [PDF]


Home page
Plant Physiol.Home page
E. Piwarzyk, Y. Yang, and T. Jack
Conserved C-Terminal Motifs of the Arabidopsis Proteins APETALA3 and PISTILLATA Are Dispensable for Floral Organ Identity Function
Plant Physiology, December 1, 2007; 145(4): 1495 - 1505.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
M. Ueda, M. Fujimoto, S.-i. Arimura, N. Tsutsumi, and K.-i. Kadowaki
Evidence for Transit Peptide Acquisition through Duplication and Subsequent Frameshift Mutation of a Preexisting Protein Gene in Rice
Mol. Biol. Evol., December 1, 2006; 23(12): 2405 - 2412.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
L. C. Hileman, J. F. Sundstrom, A. Litt, M. Chen, T. Shumba, and V. F. Irish
Molecular and Phylogenetic Analyses of the MADS-Box Gene Family in Tomato
Mol. Biol. Evol., November 1, 2006; 23(11): 2245 - 2258.
[Abstract] [Full Text] [PDF]


Home page
Plant Physiol.Home page
R. Benlloch, I. d'Erfurth, C. Ferrandiz, V. Cosson, J. P. Beltran, L. A. Canas, A. Kondorosi, F. Madueno, and P. Ratet
Isolation of mtpim Proves Tnt1 a Useful Reverse Genetics Tool in Medicago truncatula and Uncovers New Aspects of AP1-Like Functions in Legumes
Plant Physiology, November 1, 2006; 142(3): 972 - 983.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
N. A. Eckardt
Functional Divergence of AP3 Genes in the MAD World of Flower Development
PLANT CELL, August 1, 2006; 18(8): 1779 - 1781.
[Full Text] [PDF]


Home page
Plant CellHome page
A. S. Rijpkema, S. Royaert, J. Zethof, G. van der Weerden, T. Gerats, and M. Vandenbussche
Analysis of the Petunia TM6 MADS Box Gene Reveals Functional Divergence within the DEF/AP3 Lineage
PLANT CELL, August 1, 2006; 18(8): 1819 - 1832.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
G. de Martino, I. Pan, E. Emmanuel, A. Levy, and V. F. Irish
Functional Analyses of Two Tomato APETALA3 Genes Demonstrate Diversification in Their Roles in Regulating Floral Development
PLANT CELL, August 1, 2006; 18(8): 1833 - 1845.
[Abstract] [Full Text] [PDF]


Home page
J Exp BotHome page
C. P. Scutt, M. Vinauger-Douard, C. Fourquin, C. Finet, and C. Dumas
An evolutionary perspective on the regulation of carpel development
J. Exp. Bot., July 1, 2006; 57(10): 2143 - 2152.
[Abstract] [Full Text] [PDF]


Home page
Plant Physiol.Home page
A. Berbel, C. Navarro, C. Ferrandiz, L. A. Canas, J.-P. Beltran, and F. Madueno
Functional Conservation of PISTILLATA Activity in a Pea Homolog Lacking the PI Motif
Plant Physiology, September 1, 2005; 139(1): 174 - 185.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. M. Zahn, H. Kong, J. H. Leebens-Mack, S. Kim, P. S. Soltis, L. L. Landherr, D. E. Soltis, C. W. dePamphilis, and H. Ma
The Evolution of the SEPALLATA Subfamily of MADS-Box Genes: A Preangiosperm Origin With Multiple Duplications Throughout Angiosperm History
Genetics, April 1, 2005; 169(4): 2209 - 2223.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
Y. Tanabe, M. Hasebe, H. Sekimoto, T. Nishiyama, M. Kitani, K. Henschel, T. Munster, G. Theissen, H. Nozaki, and M. Ito
Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes
PNAS, February 15, 2005; 102(7): 2436 - 2441.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
R. C. Moore, S. R. Grant, and M. D. Purugganan
Molecular Population Genetics of Redundant Floral-Regulatory Genes in Arabidopsis thaliana
Mol. Biol. Evol., January 1, 2005; 22(1): 91 - 103.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
C. J. Whipple, P. Ciceri, C. M. Padilla, B. A. Ambrose, S. L. Bandong, and R. J. Schmidt
Conservation of B-class floral homeotic gene function between maize and Arabidopsis
Development, December 15, 2004; 131(24): 6083 - 6091.
[Abstract] [Full Text] [PDF]


Home page
Plant Physiol.Home page
F. Fornara, L. Parenicova, G. Falasca, N. Pelucchi, S. Masiero, S. Ciannamea, Z. Lopez-Dee, M. M. Altamura, L. Colombo, and M. M. Kater
Functional Characterization of OsMADS18, a Member of the AP1/SQUA Subfamily of MADS Box Genes
Plant Physiology, August 1, 2004; 135(4): 2207 - 2219.
[Abstract] [Full Text] [PDF]


Home page
Plant Physiol.Home page
V. F. Irish and P. N. Benfey
Beyond Arabidopsis. Translational Biology Meets Evolutionary Developmental Biology
Plant Physiology, June 1, 2004; 135(2): 611 - 614.
[Abstract] [Full Text] [PDF]


Home page
Plant Physiol.Home page
A. V. Shchennikova, O. A. Shulga, R. Immink, K. G. Skryabin, and G. C. Angenent
Identification and Characterization of Four Chrysanthemum MADS-Box Genes, Belonging to the APETALA1/FRUITFULL and SEPALLATA3 Subfamilies
Plant Physiology, April 1, 2004; 134(4): 1632 - 1641.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
T.-Y. Tzeng, H.-C. Liu, and C.-H. Yang
The C-terminal Sequence of LMADS1 Is Essential for the Formation of Homodimers for B Function Proteins
J. Biol. Chem., March 12, 2004; 279(11): 10747 - 10755.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
M. Vandenbussche, J. Zethof, S. Royaert, K. Weterings, and T. Gerats
The Duplicated B-Class Heterodimer Model: Whorl-Specific Effects and Complex Genetic Interactions in Petunia hybrida Flower Development
PLANT CELL, March 1, 2004; 16(3): 741 - 754.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
J. Nam, J. Kim, S. Lee, G. An, H. Ma, and M. Nei
Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms
PNAS, February 17, 2004; 101(7): 1910 - 1915.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
E. M. Kramer, M. A. Jaramillo, and V. S. Di Stilio
Patterns of Gene Duplication and Functional Evolution During the Diversification of the AGAMOUS Subfamily of MADS Box Genes in Angiosperms
Genetics, February 1, 2004; 166(2): 1011 - 1023.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
M. Vandenbussche, J. Zethof, E. Souer, R. Koes, G. B. Tornielli, M. Pezzotti, S. Ferrario, G. C. Angenent, and T. Gerats
Toward the Analysis of the Petunia MADS Box Gene Family by Reverse and Forward Transposon Insertion Mutagenesis Approaches: B, C, and D Floral Organ Identity Functions Require SEPALLATA-Like MADS Box Genes in Petunia
PLANT CELL, November 1, 2003; 15(11): 2680 - 2693.
[Abstract] [Full Text] [PDF]



Disclaimer: Please note that abstracts for content published before 1996 were created through digital scanning and may therefore not exactly replicate the text of the original print issues. All efforts have been made to ensure accuracy, but the Publisher will not be held responsible for any remaining inaccuracies. If you require any further clarification, please contact our Customer Services Department.