Abstract
MADS-box genes encode a family of transcription factors, which control developmental processes in flowering plants ranging from flower to root development. During the last few years increasing evidence point to more general roles of these factors not only in the control of flowering time, but also in other reproductive processes. However, they are also expressed in roots, stems and leaves. These results suggest that their function may be much more diverse than those involved in flowering, and the possibility of uncovering new roles for MADS-box genes in plant development. Here, we specifically explore the role of the STMADS subfamily in development of vegetative structures. This subfamily continues to grow, providing new insight into the vegetative development of other plant species and how it is distinct from the one in Arabidopsis is investigated.
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E.R. Alvarez-Buylla S.J. Liljegren S. Pelaz S.E. Gold C. Burgeff G.S. Ditta F. Vergara-Silva M.F. Yanofsky (2000a) ArticleTitleMADS-box gene evolution beyond flowers: expression in pollen, endospermguard cells, roots and trichomes Plant J. 24 457–466 Occurrence Handle10.1046/j.1365-313x.2000.00891.x
E.R. Alvarez-Buylla S. Pelaz S.J. Liljegren S.E. Gold C. Burgeff G.S. Ditta L.R. De Pouplana L. Martínez-Castilla M.F. Yanofsky (2000b) ArticleTitleAn ancestral MADS-box gene duplication occurred before the divergence of plants and animals Proc. Natl. Acad. Sci. 97 5328–5333 Occurrence Handle10.1073/pnas.97.10.5328
C.R. Aswath S.Y. Mo S.H. Kim D.H. Kim (2004) ArticleTitleIbMADS4 regulates the vegetative shoot development in transgenic chrysanthemum (Dendrathema grandiflora (Ramat.) Kitamura) Plant Sci. 166 847–854 Occurrence Handle10.1016/j.plantsci.2003.11.030
E.P. Beers C. Zhao (2001) Arabidopsis as a model for investigating gene activity and function in vascular tissues Molecular Breeding of Woody Plants Elsevier Science B.V. Blacksburg, Virginia 43–52
A. Becker K.U. Winter B. Meyer H. Saedler G. Theißen (2000) ArticleTitleMADS-Box gene diversity in seed plants 300 million years ago Mol. Biol. Evol. 17 1425–1434 Occurrence Handle11018150
M.J. Carmona N. Ortega F. Garcia-Maroto (1998) ArticleTitleIsolation and molecular characterization of a new vegetative MADS-box gene from Solanum tuberosum L Planta 207 181–188 Occurrence Handle10.1007/s004250050471 Occurrence Handle9951721
N. Chaffey (2002) ArticleTitleWhy is there so little research into the cell biology of the secondary vascular system of trees? New Plytol. 153 213–223 Occurrence Handle10.1046/j.0028-646X.2001.00311.x
L. Colombo A.J. Van Tunen H.J.M. Dons G.C. Angenent (1997) Molecular control of flower development in Petunia hybrida J.A. Callow (Eds) Advances in Botanical Research Vol. 26 Academic Press London 229–250
L.J. Cseke J. Zheng G.K. Podila (2003) ArticleTitleCharacterization of PTM5 in aspen trees: a MADS-box gene expressed during woody vascular development Gene 318 55–67 Occurrence Handle10.1016/S0378-1119(03)00765-0 Occurrence Handle14585498
L. Cseke G. Podila (2004) ArticleTitleMADS-box genes in Dioecious Aspen II: A review of MADS-box genes from trees and their potential in forest biotechnology Physiol. Mol. Biol. Plants 10 7–28
B. Davies M. Egea-Cortines E. deAndrade Silva H. Saedler H. Sommer (1996) ArticleTitleMultiple interactions amongst floral homeotic MADS box proteins EMBO J. 15 4330–4343 Occurrence Handle8861961
V. Decroocq X. Zhu M. Kauffman J. Kyozuka W.J. Peacock E.S. Dennis D.J. Llewellyn (1999) ArticleTitleA TM3-like MADS-box gene from Eucalyptus expressed in both vegetative and reproductive tissues Gene 228 155–160 Occurrence Handle10.1016/S0378-1119(98)00613-1 Occurrence Handle10072768
M. Egea-Cortines H. Saedler H. Sommer (1999) ArticleTitleTernary complex formation between the MADS-box proteins SQUAMOSADEFICIENSGLOBOSA is involved in the control of floral architecture in Anthirrinum majus EMBO J. 18 5370–5379 Occurrence Handle10.1093/emboj/18.19.5370 Occurrence Handle10508169
F. Fornara G. Marziani L. Mizzi M. Kater L. Colombo (2003) ArticleTitleMADS-box genes controlling flower development in rice Plant Biol. 5 16–22 Occurrence Handle10.1055/s-2003-37975
A. Gamboa J. Paéz-Valencia G.F. Acevedo L. Vázquez-Moreno R.E. Alvarez-Buylla (2001) ArticleTitleFloral transcription factor agamous interacts in vitro with a leucine-rich repeat and an acid phosphatase complex Bioch. Biophy. Resear. Comm. 288 1018–1026 Occurrence Handle10.1006/bbrc.2001.5875
F. Garcia-Maroto M.J. Carmona J.A. Garrido M. Vilches-Ferron J. Rodriguez-Ruiz D. Lopez Alonso (2002) ArticleTitleNew roles for MADS-box genes in higher plants Biol. Planta. 46 321–330 Occurrence Handle10.1023/A:1024353514081
F. Garcia-Maroto N. Ortega R. Lozano M.J. Carmona (2000) ArticleTitleCharacterization of the potato MADS-box gene STMADS16expression analysis in tobacco transgenic plants Plant Mol. Biol. 42 499–513 Occurrence Handle10.1023/A:1006397427894 Occurrence Handle10798619
Q. Gu C. Ferrandiz M.F. Yanofsky R. Martienssen (1998) ArticleTitleThe FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development Development 125 1509–1517 Occurrence Handle9502732
U. Hartmann S. Hohmann K. Nettesheim E. Wisman H. Saedler P. Huijser (2000) ArticleTitleMolecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis Plant J. 21 351–360 Occurrence Handle10.1046/j.1365-313x.2000.00682.x Occurrence Handle10758486
H. Huang M. Tudor T. Su Y. Zhang Y. Hu H. Ma (1996) ArticleTitleDNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation Plant Cell 8 81–94 Occurrence Handle10.1105/tpc.8.1.81 Occurrence Handle8597661
J. Heard M. Caspi K. Dunn (1997) ArticleTitleEvolutionary diversity of symbiotically induced nodule MADS box genes: characterization of nmhC5a member of a novel subfamily Mol. Plant–Microb. Interact. 10 665–676
K. Henschel R. Kofuji M. Hasebe H. Seadler T. Munster G. Theißen (2002) ArticleTitleTwo ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens Mol. Biol. Evol. 19 801–814 Occurrence Handle12032236
S.R. Hepworth F. Valverde D. Ravenscroft A. Mouradov G. Coupland (2002) ArticleTitleAntagonistic regulation of flowering-time gene SOC1 by CONSTANSFLC via separate promoter motifs EMBO J. 21 4327–4337 Occurrence Handle10.1093/emboj/cdf432 Occurrence Handle12169635
T. Honma K. Goto (2001) ArticleTitleComplexes of MADS-box proteins are sufficient to convert leaves into floral organs Nature 409 525–529 Occurrence Handle10.1038/35054083 Occurrence Handle11206550
H. Huang M. Tudor C.A. Weiss Y. Hu H. Ma (1995) ArticleTitleThe Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein Plant Mol. Biol. 28 549–567 Occurrence Handle10.1007/BF00020401 Occurrence Handle7632923
T. Jack (2001) ArticleTitlePlant development going MADS Plant Mol. Biol. 46 515–520 Occurrence Handle10.1023/A:1010689126632 Occurrence Handle11516144
B. Johansen L.B. Pedersen M. Skipper S. Frederiksen (2002) ArticleTitleMADS-box gene evolution-structure and transcription patterns Mol. Phylogenet. Evol. 23 458–480 Occurrence Handle10.1016/S1055-7903(02)00032-5 Occurrence Handle12099799
M.M. Kater J. Franken K.J. Carney L. Colombo G.C. Angenent (2001) ArticleTitleSex determination in the monoecious species cucumber is confined to specific floral whorls Plant Cell 13 481–493 Occurrence Handle10.1105/tpc.13.3.481 Occurrence Handle11251091
K. Kaufmann R. Melzer G. Theißen (2005) ArticleTitleMICK-type MADS domain proteins: structural modularity, protein interactions and network evolution in land plants Gene 347 183–198 Occurrence Handle10.1016/j.gene.2004.12.014 Occurrence Handle15777618
S.A. Kempin B. Savidge M.F. Yanofsky (1995) ArticleTitleMolecular basis of the cauliflower phenotype in Arabidopsis Science 267 522–525 Occurrence Handle7824951
S.H. Kim K. Mizuno T. Fujimura (2002) ArticleTitleIsolation of MADS-box genes from sweet potatoe (Ipomoea batatas (L.) Lam.) expressed specifically in vegetative tissue Plant Cell. Physiol. 43 314–322 Occurrence Handle10.1093/pcp/pcf043 Occurrence Handle11917086
T.T. Kozlowski S.G. Pallardy (1997) Physiology of Woody Plants Academic Press New York
N.T. Krogan N.W. Ashton (2000) ArticleTitleAncestry of plant MADS-box genes revealed by bryophyte (Physcomitrella patens) homologues New Phytol. 147 505–517 Occurrence Handle10.1046/j.1469-8137.2000.00728.x
S.J. Liljegren G.S. Ditta Y. Eshed B. Savidge J.L. Bowman M.F. Yanofsky (2000) ArticleTitleSHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis Nature 404 766–770 Occurrence Handle10.1038/35008089 Occurrence Handle10783890
R. Lozano T. Angosto P. Gomez C. Payan J. Capel P. Huijser J. Salinas J.M. Martinez-Zapater (1998) ArticleTitleTomato flower abnormalities induced by low temperatures are associated with changes of expression of MADS-Box genes Plant Physiol. 117 91–100 Occurrence Handle10.1104/pp.117.1.91 Occurrence Handle9576778
H. Ma M.F. Yanofsky E.M. Meyerowitz (1991) ArticleTitleAGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes Genes Dev. 5 484–495 Occurrence Handle1672119
M.A. Mandel C. Gustafson-Brown B. Savidge M.F. Yanofsky (1992) ArticleTitleMolecular characterization of the Arabidopsis floral homeotic gene APETALA1 Nature 360 273–277 Occurrence Handle10.1038/360273a0 Occurrence Handle1359429
L. Mao D. Begum H.-W. Chuang M.A. Budiman E.J. Szymkowiak E.E. Irish R.A. Wing (2000) ArticleTitleJOINTLESS is a MADS-box gene controlling tomato flower abscission zone development Nature 406 910–913 Occurrence Handle10.1038/35022611 Occurrence Handle10972295
E.M. Meyerowitz (1997) ArticleTitleGenetic control of cell division patterns in developing plants Cell 88 299–308 Occurrence Handle10.1016/S0092-8674(00)81868-1 Occurrence Handle9039256
Y.H. Moon H.G. Kang J.Y. Jung J.S. Jeon S.K. Sung G. An (1999) ArticleTitleDetermination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast twohybrid system Plant Physiol. 120 1193–1203 Occurrence Handle10.1104/pp.120.4.1193 Occurrence Handle10444103
T. Münster J. Pahnke A. Di Rosa J.T. Kim W. Martin H. Saedler G. Theißen (1997) ArticleTitleFloral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestors of ferns and seed plants Proc. Natl. Acad. Sci. 94 2415–2420 Occurrence Handle10.1073/pnas.94.6.2415 Occurrence Handle9122209
T. Münster W. Faigl H. Saedler G. Theißen (2002) ArticleTitleEvolutionary aspects of MADS-box genes in the eusporangiate fern Ophioglossum Plant Biol. 4 474–483 Occurrence Handle10.1055/s-2002-34130
N. Ori M.T. Juarez D. Jackson J. Yamaguchi G.M. Banowetz S. Hake (1999) ArticleTitleLeaf senescence is delayed in tobacco plants expressing the maize homeobox gene knotted1 under the control of a senescence-activated promoter Plant Cell 11 1073–1080 Occurrence Handle10.1105/tpc.11.6.1073 Occurrence Handle10368178
L. Parenicova S. Folter M. Kieffer D.S. Horner C. Favalli J. Busscher H.E. Cook R.M. Ingram M.M. Kater B. Davies G.C. Angenent L. Colombo (2003) ArticleTitleMolecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world Plant Cell 15 1538–1551 Occurrence Handle10.1105/tpc.011544 Occurrence Handle12837945
A.P. Prakash P.P. Kumar (2002) ArticleTitlePkMADS1 is a novel MADS box gene regulating adventitious shoot induction and vegetative shoot development in Paulownia kawakamii Plant J. 29 141–151 Occurrence Handle10.1046/j.0960-7412.2001.01206.x Occurrence Handle11851917
A.P. Prakash A. Kush P. Lakshmanan P.P. Kumar (2003) ArticleTitleCytosine methylation occurs in a CDC48 homologue and a MADS-box gene during adventitious shoot induction in Petunia leaf explants J. Emp. Bot. 54 1361–1371 Occurrence Handle10.1093/jxb/erg155
M.D. Purugganan S.D. Rounsley R.J. Schmidt M.F. Yanofsky (1995) ArticleTitleMolecular evolution of flower development: diversification of the plant MADS-box regulatory gene family Genetics 140 345–356 Occurrence Handle7635298
J.L. Riechmann B.A. Krizek E.M. Meyerowitz (1996) ArticleTitleDimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1APETALA3PISTILLATAAGAMOUS Proc. Natl. Acad. Sci. 93 4793–4798 Occurrence Handle10.1073/pnas.93.10.4793 Occurrence Handle8643482
J.L. Riechmann E.M. Meyerowitz (1997) ArticleTitleMADS domain proteins in plant development Biol. Chem. 378 1079–1101 Occurrence Handle9372178
S.D. Rounsley G.S. Ditta M.F. Yanofsky (1995) ArticleTitleDiverse roles for MADS box genes in Arabidopsis development Plant Cell 7 1259–1269 Occurrence Handle10.1105/tpc.7.8.1259 Occurrence Handle7549482
R. Rutledge S. Regan O. Nicolas P. Fobert C. Cote W. Bosnich C. Kauffeldt G. Sunohara A. Seguin D. Stewart (1998) ArticleTitleCharacterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis Plant J. 15 625–634 Occurrence Handle10.1046/j.1365-313x.1998.00250.x Occurrence Handle9778845
T. Sakamoto A. Nishimura M. Tamaoki M. Kuba H. Tanaka S. Iwahori M. Matsuoka (1999) ArticleTitleThe conserved KNOX domain mediates specificity of tobacco KNOTTED1-type homeodomain proteins Plant Cell 11 1419–1432 Occurrence Handle10.1105/tpc.11.8.1419 Occurrence Handle10449577
A. Samach H. Onouchi S.E. Gold G.S. Ditta Z. Schwarz-Sommer M.F. Yanofsky G. Coupland (2000) ArticleTitleDistinct roles of CONSTANS target genes in reproductive development of Arabidopsis Science 288 1613–1616 Occurrence Handle10.1126/science.288.5471.1613 Occurrence Handle10834834
J. Schmitz R. Franzen T.H. Ngyuen F. Garcia-Maroto C. Pozzi F. Salamini W. Rohde (2000) ArticleTitleCloning, mapping and expression analysis of barley MADS-box genes Plant Mol. Biol. 42 899–913 Occurrence Handle10.1023/A:1006425619953 Occurrence Handle10890536
P. Shore A.D. Sharrocks (1995) ArticleTitleThe MADS-box family of transcription factors Eur. J. Biochem. 229 1–13 Occurrence Handle10.1111/j.1432-1033.1995.tb20430.x Occurrence Handle7744019
N.R. Sinha R. Williams S. Hake (1993) ArticleTitleOverexpression of the maize homeobox gene KNOTTED1 causes a switch from determinate to indeterminate cell fate Genes Dev. 7 787–795 Occurrence Handle7684007
J. Sundstrom P. Engstrom (2002) ArticleTitleConifer reproductive development involves B-type MADS-box genes with distinct and different activities in male organ primordial Plant J. 31 161–169 Occurrence Handle10.1046/j.1365-313X.2002.01343.x Occurrence Handle12121446
M. Takemura R. Sawai M. Kaneko A. Yokota T. Kohchi (2004) ArticleTitleAnalysis of MADS-box protein complexes including AGL24 in Arabidopsis Plant Cell Physiol. 45 S72
K. Tandre V.A. Albert A. Sundas P. Engstreom (1995) ArticleTitleConifer homologues to genes that control floral development in angiosperms Plant Mol. Biol. 27 69–78 Occurrence Handle10.1007/BF00019179 Occurrence Handle7865797
G. Theißen (2000) ArticleTitleShattering developments Nature 404 711–713 Occurrence Handle10783869
G. Theißen J.T. Kim H. Saedler (1996) ArticleTitleClassification 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 Occurrence Handle8875863
W. Tröbner L. Ramirez P. Motte I. Hue P. Huijser W. Lonning H. Saedler Z. Schwarz-Sommer (1992) ArticleTitleGLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis EMBO J. 11 4693–4704 Occurrence Handle1361166
K.U. Winter A. Becker T. Munster J.T. Kim H. Saedler G. Theißen (1999) ArticleTitleMADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants Proc. Natl Acad. Sci. USA 96 7342–7347 Occurrence Handle10.1073/pnas.96.13.7342 Occurrence Handle10377416
S. Yalovsky M. Rodriguez-Concepcion K. Bracha G. Toledo-Ortiz W. Gruissem (2000) ArticleTitlePrenylation of the floral transcription factor APETALA1 modulates its function Plant Cell 12 1257–1266 Occurrence Handle10.1105/tpc.12.8.1257 Occurrence Handle10948247
Y. Yang L. Fanning T. Jack (2003) ArticleTitleThe K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3PISTILLATA Plant J. 33 47–59 Occurrence Handle10.1046/j.0960-7412.2003.01473.x Occurrence Handle12943540
Y. Yang T. Jack (2004) ArticleTitleDefining subdomains of the K domain important for protein–protein interactions of plant MADS proteins Plant Mol. Biol. 55 45–59 Occurrence Handle10.1007/s11103-004-0416-7 Occurrence Handle15604664
H. Yu Y. Xu E.L. Tan P.P. Kumar (2002) ArticleTitleAGAMOUS-LIKE24a dosage-dependent mediator of the flowering signals Proc. Natl. Acad. Sci. 99 16336–16341 Occurrence Handle10.1073/pnas.212624599 Occurrence Handle12451184
S. Zachgo E.D. Silva P. Motte W. Trobner H. Saedler Z. Schwarzsommer (1995) ArticleTitleFunctional analysis of the Antirrhinum floral homeotic deficiens gene in vivoin vitro by using a temperature-sensitive mutant Development 121 2861–2875 Occurrence Handle7555713
H. Zhang B.G. Forde (1998) ArticleTitleAn Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture Science 279 407–409 Occurrence Handle10.1126/science.279.5349.407 Occurrence Handle9430595
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Aswath, C., Kim, S. Another Story of MADS-Box Genes – their Potential in Plant Biotechnology. Plant Growth Regul 46, 177–188 (2005). https://doi.org/10.1007/s10725-005-8482-7
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DOI: https://doi.org/10.1007/s10725-005-8482-7