Skip to main content
SpringerLink
Log in

Hierarchical Structures and Dissected Functions of MADS-Box Transcription Factors in Rice Development

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Floral organ development and regulation of flowering time in rice is closely associated with MADS-box transcriptional factors (TFs). MADS-box proteins contain a conserved 60 amino acid MADS-box motif for a sequence-specific DNA-binding activity that also functions in dimerization and accessory factor binding. A systematic understanding of this MADS-box TF subfamily is needed to explain the functional complexity among the gene family members. In total, the function of 33 out of 75 MADS-box TFs in rice has been characterized. Meta-anatomical expression data based on a large collection of spatiotemporal microarray data integrated to the phylogenetic tree context was very effective at explaining the functional complexity or specificity among a large gene family. Subsequently, a cluster of MADS-box TFs consisting of 15 gene members showed preferred expression in floral organs, and their expression patterns are well correlated with previously identified functions in floral organ identity. In addition, the hierarchical structure of a group of MADS-box TFs, based on the expression patterns, was well supported by the genetic studies. OsMADS1 functions in the earliest step of floral organ development and affects the overall floral organ development by identifying downregulation of nine members in the same clade in osmads1 mutant and observed phenotypic changes. The combination of hierarchical structure and possible hetero-dimerization among MADS-box TFs allows for understanding the molecular and genetic regulatory model for floral organ development in rice. This work provides a comprehensive understanding of the functions of MADS-box TFs and will be a useful guide for further studies.

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

  • Ali Z, Raza Q, Atif RM, Aslam U, Ajmal M, Chung G (2019) Genetic and molecular control of floral organ identity in cereals. Int J Mol Sci 20:2743

    CAS  PubMed Central  Google Scholar 

  • Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genom 8:242

    Google Scholar 

  • Bastow R, Mylne J, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167

    CAS  PubMed  Google Scholar 

  • Becker A, Theissen G (2003) A novel MADS-box gene subfamily with a sister group relationship to class B floral homeotic genes. Mol Genet Genom 266:942–950

    Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20

    CAS  PubMed  Google Scholar 

  • Callens C, Tucker MR, Zhang D, Wilson ZA (2018) Dissecting the role of MADS-box genes in monocot floral development and diversity. J Exp Bot 69:2435–2459

    CAS  PubMed  Google Scholar 

  • Cao PJ, Bartley LE, Jung KH, Ronald PC (2008) Construction of a rice glycosyltransferase phylogenomic database and identification of rice-diverged glycosyltransferases. Mol Plant 1:858–877

    CAS  PubMed  Google Scholar 

  • Castelán-Muñoz N, Herrera J, Cajero-Sánchez W, Arrizubieta M, Trejo C, García-Ponce B, de la Paz Sánchez M, Álvarez-Buylla ER, Garay-Arroyo A (2019) MADS-box genes are key components of genetic regulatory networks involved in abiotic stress and plastic developmental responses in plants. Front Plant Sci 10:853

    PubMed  PubMed Central  Google Scholar 

  • Chandran AKN, Yoo YH, Cao P, Sharma R, Sharma M, Dardick C, Ronald PC, Jung KH (2016) Updated Rice kinase database RKD 20: enabling transcriptome and functional analysis of rice kinase genes. Rice 9:40

    PubMed  PubMed Central  Google Scholar 

  • Chandran AKN, Hong W, Abhijith B, Lee J, Kim YJ, Park SK, Jung KH (2020) Rice Male Gamete Expression Database (RMEDB): a web resource for functional genomic studies of rice male organ development. J Plant Biol 63:421–430

    Google Scholar 

  • Ciaffi M, Paolacci AR, Tanzarella OA, Porceddu E (2011) Molecular aspects of flower development in grasses. Sex Plant Reprod 24:247–282

    CAS  PubMed  Google Scholar 

  • Colombo L, Franken J, Van der Krol AR, Wittich PE, Dons HJ, Angenent GC (1997) Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development. Plant Cell 9:703–715

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dinneny JR, Yanofsky MF (2005) Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned. BioEssays 27:42–49

    CAS  PubMed  Google Scholar 

  • Dinneny JR, Weigel D, Yanofsky MF (2005) A genetic framework for fruit patterning in Arabidopsis thaliana. Development 132:4687–4696

    CAS  PubMed  Google Scholar 

  • Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk PB, An G, Colombo L, Kater MM (2007) The d-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant J 52:690–699

    CAS  PubMed  Google Scholar 

  • Duan K, Li L, Xu SP, Xu ZH, Xue HW (2006) A brassinolide-suppressed rice MADS-box transcription factor, OsMDP1, has a negative regulatory role in BR signaling. Plant J 47(4):519–531

    CAS  PubMed  Google Scholar 

  • Garay-Arroyo A, Ortiz-Moreno E, de la Paz SM, Murphy AS, Garcia-Ponce B, Marsch-Martinez N, de Folter S, Corvera-Poire A, Jaimes-Miranda F, Pacheco-Escobedo MA, Dubrovsky JG, Pelaz S, Alvarez-Buylla ER (2013) The MADS transcription factor XAL2/AGL14 modulates auxin transport during Arabidopsis root development by regulating PIN expression. EMBO J 32:2884–2895

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1556

    CAS  PubMed  Google Scholar 

  • Guo S, Xu Y, Liu H, Mao Z, Zhang C, Ma Y, Zhang Q, Meng Z, Chong K (2013) The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat Commun 4:1566

    PubMed  Google Scholar 

  • Han P, Garcia-Ponce B, Fonseca-Salazar G, Alvarez-Buylla ER, Yu H (2008) AGAMOUS-LIKE 17, a novel flowering promoter, acts in a FT-independent photoperiod pathway. Plant J 55:253–265

    CAS  PubMed  Google Scholar 

  • Heijmans K, Ament K, Rijpkema AS, Zethof J, Wolters-Arts M, Gerats T, Vandenbussche M (2012) Redefining C and D in the petunia ABC. Plant Cell 24:2305–2317

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Huang F, Xu G, Chi Y, Liu H, Xue Q, Zhao T, Gai J, Yu D (2014) A soybean MADS-box protein modulates floral organ numbers, petal identity and sterility. BMC Plant Biol 14:89

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon JS, Jang S, Lee S, Nam J, Kim C, Lee SH, Chung YY, Kim SR, Lee YH, Cho YG, An G (2000) leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell 12:871–884

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jung KH, Cao P, Seo YS, Dardick C, Ronald PC (2010) The Rice Kinase Phylogenomics Database: a guide for systematic analysis of the rice kinase super-family. Trends Plant Sci 15:595–599

    CAS  PubMed  Google Scholar 

  • Jung KH, Cao P, Sharma R, Jain R, Ronald PC (2015) Phylogenomics databases for facilitating functional genomics in rice. Rice 8:60

    PubMed  Google Scholar 

  • Kang HG, Jang S, Chung JE, Cho YG, An G (1997) Characterization of two rice MADS box genes that control flowering time. Mol Cells 7:559–566

    CAS  PubMed  Google Scholar 

  • Kang HG, Jeon JS, 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 

  • Kater MM, Dreni L, Colombo L (2006) Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. J Exp Bot 57:3433–3444

    CAS  PubMed  Google Scholar 

  • Khanday I, Yadav SR, Vijayraghavan U (2013) Rice LHS1/OsMADS1 controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways. Plant Physiol 161:1970–1983

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khong GN, Pati PK, Richaud F, Parizot B, Bidzinski P, Mai CD, Bès M, Bourrié I, Meynard D, Beeckman T, Selvaraj MG, Manabu I, Genga AM, Brugidou C, Do VN, Guiderdoni E, Morel JB, Gantet P (2015) OsMADS26 negatively regulates resistance to pathogens and drought tolerance in rice. Plant Physiol 169:2935–2949

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SL, Lee S, Kim HJ, Nam HG, An G (2007) OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiol 145:1484–1494

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, Kimizu M, Yohshida H, Nagamura Y, Kyozuka J (2012) Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-Like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell 24:1848–1859

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee Y, An G (2015) Complex regulatory networks of flowering time in rice. Rice Res 3:141

    Google Scholar 

  • Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14:2366–2376

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Kim J, Son JS, Nam J, Jeong DH, Lee K, Jang S, Yoo J, Lee J, Lee DY, Kang HG, An G (2003) Systematic reverse genetic screening of T-DNA tagged genes in rice for functional genomic analyses: MADS-box genes as a test case. Plant Cell Physiol 44:1403–1411

    CAS  PubMed  Google Scholar 

  • Lee S, Choi SC, An G (2008) Rice SVP-group MADS-box proteins, OsMADS22 and OsMADS55, are negative regulators of brassinosteroid responses. Plant J 54:93–105

    CAS  PubMed  Google Scholar 

  • Lewis MW, Leslie ME, Liljegren SJ (2006) Plant separation: 50 ways to leave your mother. Curr Opin Plant Biol 9:59–65

    PubMed  Google Scholar 

  • Li H, Liang W, Jia R, Yin C, Zong J, Kong H, Zhang D (2010) The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice. Cell Res 20:299–313

    CAS  PubMed  Google Scholar 

  • Liu Y, Cui S, Wu F, Yan S, Lin X, Du X, Chong K, Schilling S, Theißen G, Meng Z (2013) Functional conservation of MIKC*-type MADS box genes in Arabidopsis and rice pollen maturation. Plant Cell 25:1288–1303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Dee ZP, Wittich P, Pe ME, Rigola D, Del Buono I, Sari-Gorla M, Kater MM, Colombo L (1999) OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev Genet 25:237–244

    CAS  PubMed  Google Scholar 

  • Malcomber ST, Kellogg EA (2005) SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 10:427–435

    CAS  PubMed  Google Scholar 

  • Menzel G, Apel K, Melzer S (1996) Identification of two MADS box genes that are expressed in the apical meristem of the long-day plant Sinapis alba in transition to flowering. Plant J 9(3) 399–408. https://doi.org/10.1046/j.1365-313X.1996.09030399.x

    Article  CAS  PubMed  Google Scholar 

  • Moon S, Hong W, Kim Y, Chandran AKN, Gho Y, Yoo Y, Nguyen VNT, An G, Park SK, Jung KH (2020) Comparative transcriptome analysis reveals gene regulatory mechanism of UDT1 on anther development. J Plant Biol 63:289–296

    CAS  Google Scholar 

  • Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130(4):705–718

    CAS  PubMed  Google Scholar 

  • Nayar S, Sharma R, Tyagi AK, Kapoor S (2013) Functional delineation of rice MADS29 reveals its role in embryo and endosperm development by affecting hormone homeostasis. J Exp Bot 64:4239–4253

    CAS  PubMed  PubMed Central  Google Scholar 

  • Norman C, Runswick M, Pollock R, Treisman R (1988) Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55:989–1003

    CAS  PubMed  Google Scholar 

  • Ó’Maoiléidigh DS, Graciet E, Wellmer F (2014) Gene networks controlling Arabidopsis thaliana flower development. New Phytol 201:16–30

    PubMed  Google Scholar 

  • Passmore S, Maine GT, Elble R, Christ C, Tye BK (1988) Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of MAT alpha cells. J Mol Biol 204:593–606

    CAS  PubMed  Google Scholar 

  • Paul P, Dhatt BK, Miller M, Flsom JJ, Wang Z, Krassovskaya I, Liu K, Sandhu J, Yu H, Zhang C, Obata T, Staswick P, Walia H (2020) MADS78 and MADS79 are essential regulators of early seed development in rice. Plant Physiol 182:933–948

    CAS  PubMed  Google Scholar 

  • Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424:85–88

    CAS  PubMed  Google Scholar 

  • Puig J, Meynard D, Khong GN, Pauluzzi G, Guiderdoni E, Gantet P (2013) Analysis of the expression of the AGL17-like clade of MADS-box transcription factors in rice. Gene Expr Patterns 13:160–170

    CAS  PubMed  Google Scholar 

  • Ryu CH, Lee S, Cho LH, Kim SL, Lee YS, Choi SC, Jeong HJ, Yi J, Park SJ, Han CD, An G (2009) OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant Cell Environ 32:1412–1427

    CAS  PubMed  Google Scholar 

  • Sabelli PA, Larkins B (2009) The development of endosperm in grasses. Plant Physiol 149:14–26

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sang X, Li Y, Luo Z, Ren D, Fang L, Wang N, Zhao F, Ling Y, Yang Z, Liu Y, He G (2012) CHIMERIC FLORAL ORGANS1, encoding a monocot-specific MADS box protein, regulates floral organ identity in rice. Plant Physiol 160:788–807

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sato H, Yoshida K, Mitsuda N, Ohme-Takagi M, Takamiro T (2012) Male-sterile and cleistogamous phenotypes in tall fescue induced by chimeric repressors of SUPERWOMAN1 and OsMADS58. Plant Sci 183:183–189

    CAS  PubMed  Google Scholar 

  • Sharma R, Cao P, Jung K-H, Sharma MK, Ronald PC (2013) Construction of a rice glycoside hydrolase phylogenomic database and identification of targets for biofuel research. Front Plant Sci 4:1–15

    CAS  Google Scholar 

  • Sommer H, Beltran JP, Huijser P, Pape H, Lonnig WE, 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  PubMed Central  Google Scholar 

  • Sugiyama SH, Yasui Y, Ohmori S, Tanaka W, Hirano HY (2019) Rice flower development revisited: regulation of carpel specification and flower meristem determinacy. Plant Cell Physiol 60:1284–1295

    CAS  PubMed  Google Scholar 

  • Tapia-Lopez R, Garcia-Ponce B, Dubrovsky JG, Garay-Arroyo A, Perez-Ruiz RV, Kim SH, Acevedo F, Pelaz S, Alvarez-Buylla ER (2008) An AGAMOUS-related MADS-box gene, XAL1 (AGL12), regulates root meristem cell proliferation and flowering transition in Arabidopsis. Plant Physiol 146:1182–1192

    CAS  PubMed  PubMed Central  Google Scholar 

  • Teo ZWN, Zhou W, Shen L (2019) Dissecting the function of MADS-box transcription factors in orchid reproductive development. Front Plant Sci 10:1474

    PubMed  PubMed Central  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, Melzer R (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann Bot 100:603–619

    PubMed  PubMed Central  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 subfamily in the morphological evolution of eukaryotes. J Mol Evol 43:484–516

    CAS  PubMed  Google Scholar 

  • Wang K, Tang D, Hong L, Xu W, Huang J, Li M, Gu M, Xue Y, Cheng Z (2010) DEP and AFO regulate reproductive habit in rice. PLoS Genet 6:e1000818

    PubMed  PubMed Central  Google Scholar 

  • Wang S, Lu G, Hou Z, Luo Z, Wang T, Li H, Zhang J, Ye Z (2014) Members of the tomato FRUITFULL MADS-box family regulate style abscission and fruit ripening. J Exp Bot 65:3005–3014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu F, Shi X, Lin X, Liu Y, Chong K, Theissen G, Meng Z (2017) The ABCs of flower development: mutational analysis of AP1/FUL-like genes in rice provides evidence for a homeotic (A)-function in grasses. Plant J 89:310–324

    CAS  PubMed  Google Scholar 

  • Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191–203

    CAS  PubMed  Google Scholar 

  • Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano HY (2006) Functional diversification of the two C-class MADS box genes OsMADS3 and OsMADS58 in Oryza sativa. Plant Cell 18:15–28

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto E, Yonemaru J, Yamamoto T, Yano M (2012) OGRO: the overview of functionally characterized genes in rice online database. Rice (n y) 5:26

    Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39

    CAS  PubMed  Google Scholar 

  • Yasui Y, Tanaka W, Sakamoto T, Kurata T, Hirano HY (2017) Genetic enhancer analysis reveals that FLORAL ORGAN NUMBER2 and OsMADS3 co-operatively regulate maintenance and determinacy of the flower meristem in rice. Plant Cell Physiol 58:893–903

    CAS  PubMed  Google Scholar 

  • Yin LL, Xue HW (2012) The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell 24:1049–1065

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon J, Cho LH, Lee S, Pasriga R, Tun W, Yang J, Yoon H, An G (2019) Chromatin interacting factor OsVIL2 is required for outgrowth of axillary buds in rice. Mol Cells 42:858–868

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang G, Xu N, Chen H, Wang G, Huang J (2018) OsMADS25 regulates root system development via auxin signaling in rice. Plant J 95:1004–1022

    CAS  PubMed  Google Scholar 

  • Zhao Y, Zhao H, Wang Y, Zhang X, Zhao X, Yuan Z (2020) Genome-wide identification and expression analysis of MIKC-type MADS-box gene family in Punica granaum L. Plants 10:1197

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported in part by grants from the New Breeding Technology Center Program (PJ01492703 to KHJ) and grant from the National Research Foundation (NRF), Ministry of Education, Science and Technology (NRF- 2021R1A2C2010448 to KHJ); 2020 BK21 FOUR Program of Pusan National University and Pusan National University Research Grant, 2019 to LHC.

Author information

Authors and Affiliations

  1. Department of Plant Bioscience, Pusan National University, Miryang, 50463, Republic of Korea

    Jinmi Yoon & Lae-Hyeon Cho

  2. Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University, Yongin, 17104, Republic of Korea

    Ki-Hong Jung

Authors
  1. Jinmi Yoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lae-Hyeon Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ki-Hong Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lae-Hyeon Cho or Ki-Hong Jung.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoon, J., Cho, LH. & Jung, KH. Hierarchical Structures and Dissected Functions of MADS-Box Transcription Factors in Rice Development. J. Plant Biol. 65, 99–109 (2022). https://doi.org/10.1007/s12374-021-09343-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-021-09343-0

Keywords

Search

Navigation