MicroRNA-mediated regulation of flower development in grasses

  • Aleksandra Smoczynska Department of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznan
  • Zofia Szweykowska-Kulinska
Keywords: miRNA, grasses, flower development, ABCDE model


Flower structure in grasses is very unique. There are no petals or sepals like in eudicots but instead flowers develop bract-like structures –palea and lemma. Reproductive organs are enclosed by round lodicule that not only protects reproductive organs but also play important role during flower opening. First genetic model for floral organ development was proposed 25 years ago and it was based on the research on model eudicots. Since then studies have been made to answer the question whether this model could be applicable in case of monocots. Genes from all found in eudicots classes have been also indentified in genomes of such monocots like rice, maize or barley. What’s more it seems that miRNA-mediated regulation of floral organ genes that was observed in case of Arabidopsis thaliana also has a place in monocots. MiRNA172, miRNA159, miRNA171 and miRNA396 regulate expression of floral organ identity genes in barley, rice and maize affecting various features of flower structure from formation of lemma and palea to development of reproductive organs. Model of floral development in grasses and its genetic regulation in not yet fully characterized. Further studies on both model eudicots and grasses are needed to unravel this topic. This review provides general overview of genetic model of flower organ identity specification in monocots and it’s miRNA-mediated regulation.


Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357-3365 http://dx.doi.org/10.1242/dev.01206

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. http://dx.doi.org/10.1016/S1097-2765(00)80450-5

Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. The Plant Cell 15:2730-2741 http://dx.doi.org/10.1105/tpc.016238

Barciszewska-Pacak M, Milanowska K, Knop K, Bielewicz D, Nuc P, Plewka P, Pacak AM, Franck Vazquez F, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2015) Arabidopsis microRNA expression regulation in a wide range of abiotic stress responses. Front. Plant Sci 6:410 http://dx.doi.org/10.3389%2Ffpls.2015.00410

Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell. 136:215–33. http://dx.doi.org/doi: 10.1016/j.cell.2009.01.002.

Bielewicz D, Dolata J, Zielezinski A, Alaba S, Szarzynska B, Szczesniak MW. Jarmolowski A, Szweykowska-Kulinska Z, Karlowski W (2012). mirEX: a platform for 12 comparative exploration of plant pri-miRNA expression data. Nucleic Acids Res. 40:191–197. http://dx.doi.org/10.1093/nar/gkr878

Bielewicz D, Kalak M, Kalyna M, Windels D, Barta A, Vazquez F, Szweykowska-Kulinska Z, Jarmolowski A (2013). Introns of plant primiRNAs enhance miRNA biogenesis. EMBO Reports 14:622–628.

Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta. 218:683-692 http://dx.doi.org/10.1007/s00425-004-1203-z

Bommert P, Satoh-Nagasawa N, Jackson D, Hirano H-Y (2005) Genetics and evolution of inflorescence and flower development in grasses. Plant Cell Physiol 46:69–78 http://dx.doi.org/10.1093/pcp/pci504

Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022-2025 http://dx.doi.org/10.1126/science.1088060

Cheng PC, Greyson RI, Walden DB (1983) Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am. J. Bot. 70:450–462 http://dx.doi.org/10.2307/2443252

Chuck G, Meeley R, Hake S (2008) Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1 and sid1. Development 135: 3013-3019 http://dx.doi.org/10.1242/dev.024273

Chuck G, Meeley R, Irish E, Sakai H, Hake S (2007) The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nature 39: 1517 – 1521 http://dx.doi.org/doi:10.1038/ng.2007.20

Ciaffi C, Paolacci AR (2011) Molecular aspects of flower development in grasses. Sex Plant Reprod 24:247-282 http://dx.doi.org/doi10.1007/s00497-011-0175-y 13

Clifford H T (1987). Spikelet and floral morphology. In Grass Systematics and Evolution. TR Soderstrom, KW Hilu, CS Campbell, ME Barkworth eds, pp.21-30. Washington Smithsonian Institute Press

Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31-37 http://dx.doi.org/10.1038/353031a0

Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, van Tunen AJ (1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7: 1859–1868 http://dx.doi.org/10.1105/tpc.7.11.1859

Curaba J, Spriggs A, Taylor J, Li Z, Helliwell C (2012) miRNA regulation in the early development of barley seed. BMC Plant Biol. 12:120 http://dx.doi.org/10.1186/1471-2229-12-120.

Engstrom EM (2011) Phylogenetic analysis of GRAS proteins from moss, lycophyte and vascular plant lineages reveals that GRAS genes arose and underwent substantial diversification in the ancestral lineage common to bryophytes and vascular plants. Plant Signal Behav. 6:850-854 http://dx.doi.org/10.4161/psb.6.6.15203

Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15: 2603–2611 http://dx.doi.org/10.1105/tpc.015123

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 http://dx.doi.org/10.1105/tpc.12.6.871

Jin Y, Luo Q, Tong H, Wang A, Cheng Z, Tang J, Li D, Zhao X, Li X, Wan J, Jiao Y, Chu C, Zhu L (2011) An AT-hook gene is required for palea formation and fl oral organ 14 number control in rice. Dev Biol 359:277–288 http://dx.doi.org/10.1016/j.ydbio.2011.08.023

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 α-Amylase Expression in Aleurone and Flower Development. Plant Cell. 16:33-44 http://dx.doi.org/10.1105/tpc.017327

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 http://dx.doi.org/10.1023/A:1006051911291

Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, Kimizu M, Yoshida 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 http://dx.doi.org/10.1105/tpc.112.097105

Kruszka K, Pacak A, Swida-Barteczka A, Nuc P, Alaba S, Wroblewska Z, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2014) Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley. Journal of Experimental Botany 65: 6123-35 http://dx.doi.org/10.1093/jxb/eru353

Kruszka K, Pieczynski M, Windels D, Bielewicz D, Jarmolowski A, Szweykowska-Kulinska Z, Vazquez F (2012) Role of microRNAs and other sRNAs of plants in their changing environments. J Plant Physiol 169:1664-72 http://dx.doi.org/10.1016/j.jplph.2012.03.009

Lee D, An G (2012) Two AP2 family genes, SUPERNUMERARY BRACT (SNB) and OsINDETERMINATE SPIKELET 1 (OsIDS1), synergistically control inflorescence 15 architecture and floral meristem establishment in rice. Plant J 69 445–461 http://dx.doi.org/10.1111/j.1365-313X.2011.04804.x

Lee DY, Lee J, Moon S, Park SY, An G (2007) The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem. Plant J. 49: 64-78 http://dx.doi.org/10.1111/j.1365-313X.2006.02941.x.

Lee MH, Kim B, Song SK, Heo JO, Yu NI, Lee SA, Kim M, Kim DG, Sohn SO, Lim CE, Chang KS, Lee MM, Lim J (2008) Large-scale analysis of the GRAS gene family in Arabidopsis thaliana. Plant Mol Biol. 67:659-70 http://dx.doi.org/10.1007/s11103-008-9345-1

Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 75:843–54. http://dx.doi.org/10.1016/0092-8674(93)90529-Y.

Liang G, He H, Li Y, Wang F, Yu D (2014) Molecular Mechanism of microRNA396 Mediating Pistil Development in Arabidopsis1. Plant Physiol. 164:249–258 http://dx.doi.org/10.1104/pp.113.225144

Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: Implications for the evolution of floral development. Genetics 165: 821–833

Liu H, Guo S, Xu Y, Li C, Zhang Z, Zhang D, Xu S, Zhang C, Chong K (2014) OsmiR396d-Regulated OsGRFs Function in Floral Organogenesis in Rice through Binding to Their Targets OsJMJ706 and OsCR41. Plant Physiol. 165:160–174 http://dx.doi.org/10.1104/pp.114.235564

Lord EM (1981) Cleistogamy: A tool for the study of floral morphogenesis, function and evolution. The Botanical Review 47: 421-449 16

Mena M, Ambrose BA, Meeley RB, BriggsSP, Yanofsky MF, Schmitt RJ (1996) Diversification of C-function activity in maize flower development. Science 274:1537–1540 http://dx.doi.org/10.1016/S1360-1385(97)82558-7

Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–721 http://dx.doi.org/10.1105%2Ftpc.104.027920

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: 705–718 http://dx.doi.org/doi:10.1242/dev.00294

Nair S, Wang N, Turuspekov Y, Pourkheirandish M, Sinsuwongwat S, Chen G, Sameri M, Tagiri A, Honda I, Watanabe Y, Kanamori H, Wicker T, Stein N, Nagamura Y, Matsumoto T, Komatsuda T (2010) Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage. PNAS 107:490-495 http://dx.doi.org/doi:10.1073/pnas.0909097107

Palatnik JF, Allen E, Wu XL, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263 http://dx.doi.org/10.1038/nature01958

Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495 http://dx.doi.org/10.1016/S0960-9822(02)01017-5

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 http://dx.doi.org/doi:10.1038/35012103

Phipps IF (1928) Heritable characters in maize. XXXI. Tassel-seed4. J. Hered. 19: 399–404 17

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 http://dx.doi.org/doi:10.1038/nature01741

Prasad K, Vijayraghavan U (2003) Double-stranded RNA interference of a rice PI/GLO paralog, OsMADS2, uncovers its second-whorl-specific function in floral organ patterning. Genetics 165:2301-2305

Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130:6001-6012. http://dx.doi.org/doi:10.1242/dev.00842

Schreiber AW, Shi BJ, Huang CY, Langridge P, Baumann U (2011) Discovery of barley miRNAs through deep sequencing of short reads. BMC Genomics. 12:129. http://dx.doi.org/10.1186/1471-2164-12-129

Schulze S, Schäfer BN, Parizotto EA, Voinnet O, Theres K (2010) LOST MERISTEMS genes regulate cell differentiation of central zone descendants in Arabidopsis shoot meristems. The Plant Journal 64:668-678 http://dx.doi.org/10.1111/j.1365-313X.2010.04359.x

Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527 http://dx.doi.org/10.1016/j.devcel.2005.01.018

Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4:447–456 http://dx.doi.org/10.1016/S1369-5266(00)00199-0

Szweykowska-Kulinska Z., Jarmolowski, A, Vazquez F (2013). The crosstalk between plant microRNA biogenesis factors and the spliceosome. Plant Signal. Behav. 8:e26955. http://dx.doi.org/10.4161/psb.26955 18

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

Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H, Ashikari M, Matsuoka M (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J. 47:427-44 http://dx.doi.org/10.1111/j.1365-313X.2006.02795.x

Turuspekov Y, Mano Y, Honda I, Kawada N, Watanabe Y, Komatsuda T (2004) Identification and mapping of cleistogamy genes in barley. Theor Appl Genet 109:480–487 http://dx.doi.org/10.1007/s00122-004-1673-1

Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell. 136:669–87. http://dx.doi.org/10.1016/j.cell.2009.01.046.

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(1):e1000818 http://dx.doi.org/doi:10.1371/journal.pgen.1000818

Wang L, Mai YX, Zhang YC, Luo Q, Yang HQ (2010) MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IV genes regulate shoot branching in Arabidopsis. Mol Plant. 3:794-806 http://dx.doi.org/10.1093/mp/ssq042

Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ (2004) Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 131: 6083-6091 http://dx.doi.org/10.1242/dev.01523

Windels D, Bielewicz D, Ebneter M, Jarmolowski A, Szweykowska-Kulinska Z, Vazquez F (2014) miR393 Is Required for Production of Proper Auxin Signalling Outputs. PLoS One 9:e95972. http://dx.doi.org/10.1371/journal.pone.0095972 19

Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano HY (2006) Functional diversification of the two C-class genes OsMADS3 and OsMADS58 in Oryza sativa. Plant Cell 18:15–28 http://dx.doi.org/10.1105/tpc.105.037200

Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16: 500–509 http://dx.doi.org/10.1105%2Ftpc.018044

Yao SG, Ohmori S, Kimizu M, Yoshida H (2008) Unequal genetic redundancy of rice PISTILLATA orthologs, OsMADS2 and OsMADS4, in lodicule and stamen development. Plant and Cell Physiology 49:853-857 http://dx.doi.org/10.1093/pcp/pcn050

Yuan Z, Gao S, Xue D-W, Luo D, Li L-T, Ding S-Y, Yao X, Wilson ZA, Qian Q, Zhang D-B (2009) RETARDED PALEA1 controls palea development and floral zygomorphy in rice. Plant Physiol 149:235–244 http://dx.doi.org/10.1104%2Fpp.108.128231

Zhu Q-H, Upadhyaya NM, Gubler F, Helliwell CA (2009) Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biology 9:149 http://dx.doi.org/10.1186/1471-2229-9-149