MicroRNA-mediated regulation of flower development in grasses

• Authors: Aleksandra Smoczynska , Zofia Szweykowska-Kulinska
• Languages of publication: EN

Abstracts

EN

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 plays an important role during flower opening. The 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 carried out to answer the question whether this model could be applicable in the case of monocots. Genes from all classes found in eudicots have been also identified 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 the case of Arabidopsis thaliana also takes place in monocots. MiRNA172, miRNA159, miRNA171 and miRNA396 regulate expression of floral organ identity genes in barley, rice and maize, affecting various features of the flower structure, ranging from formation of lemma and palea to the development of reproductive organs. A model of floral development in grasses and its genetic regulation is not yet fully characterized. Further studies on both, the 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.

Keywords

EN

miRNA; grasses; flower development; ABCDE model

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2016
• Volume: 63
• Issue: 4
• Pages: 687-692

Dates

published

2016

received

2016-06-06

revised

2016-06-25

accepted

2016-07-19

(unknown)

2016-11-04

Contributors

author

Aleksandra Smoczynska

• Department of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznan, Poznań, Poland

author

Zofia Szweykowska-Kulinska

• Department of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznan, Poznań, Poland

References

• Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131: 3357-3365. https://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. https://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. https://doi.org/10.1105/tpc.016238.
• Barciszewska-Pacak M, Milanowska K, Knop K, Bielewicz D, Nuc P, Plewka P, Pacak AM, 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. https://doi.org/10.3389%2Ffpls.2015.00410.
• Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233. doi: 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 comparative exploration of plant pri-miRNA expression data. Nucleic Acids Res 40: D191-D197. https://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 pri-miRNAs enhance miRNA biogenesis. EMBO Reports 14: 622-628. https://doi.org/10.1038/embor.2013.62.
• Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218: 683-692. https://doi.org/10.1007/s00425-004-1203-z.
• Bommert P, Satoh-Nagasawa N, Jackson D, Hirano HY (2005) Genetics and evolution of inflorescence and flower development in grasses. Plant Cell Physiol 46: 69-78. https://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. https://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. https://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. https://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. Nat Genet 39: 1517-1521. https://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. https://doi.org/doi10.1007/s00497-011-0175-y.
• 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 https://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. https://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. https://doi.org/10.1186/1471-2229-12-120.
• 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. https://doi.org/10.1111/j.1365-313X.2007.03272.x.
• 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. https://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 https://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. https://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 number control in rice. Dev Biol 359: 277-288. https://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. https://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. https://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. https://doi.org/10.1105/tpc.112.097105.
• Kramer EM, Jaramillo MA, Di Stilio VS (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166: 1011-1023. https://doi.org/10.1534/166.2.1011.
• 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. J Exp Bot 65: 6123-6135. https://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: 1664-1672. https://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 architecture and floral meristem establishment in rice. Plant J 69: 445-461. https://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. https://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: 659-670. https://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: 843-854. https://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. https://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. https://doi.org/10.1104/pp.114.235564.
• Lord EM (1981) Cleistogamy: A tool for the study of floral morphogenesis, function and evolution. Bot Rev 47: 421-449
• Mena M, Ambrose BA, Meeley RB, Briggs SP, Yanofsky MF, Schmidt RJ (1996) Diversification of C-function activity in maize flower development. Science 274: 1537-1540. https://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. https://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. https://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. https://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 https://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. https://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 https://doi.org/doi:10.1038/35012103.
• Phipps IF (1928) Heritable characters in maize. XXXI. Tassel-seed4. J Hered 19: 399-404
• 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 https://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. https://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. https://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. Plant J 64: 668-678. https://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. https://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. https://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. https://doi.org/10.4161/psb.26955.
• Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, 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: 427-444. https://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. https://doi.org/10.1007/s00122-004-1673-1.
• Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669-87. https://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: e1000818 https://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. https://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. https://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. https://doi.org/10.1371/journal.pone.0095972.
• 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. https://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. https://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 Cell Physiol 49: 853-857. https://doi.org/10.1093/pcp/pcn050.
• Yuan Z, Gao S, Xue DW, Luo D, Li LT, Ding SY, Yao X, Wilson ZA, Qian Q, Zhang DB (2009) RETARDED PALEA1 controls palea development and floral zygomorphy in rice. Plant Physiol 149: 235-244. https://doi.org/10.1104%2Fpp.108.128231.
• Zhu QH, 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 https://doi.org/10.1186/1471-2229-9-149.

Identifiers

DOI

10.18388/abp.2016_1358