Abstract
Species of the genus Brachiaria comprise plants with different modes of reproduction, sexual and apomictic. In apomixis, the embryo sac differentiates from an unreduced cell, and the embryo develops in the absence of egg cell fertilisation. In this work, the characterisation and expression analyses of a MADS-box gene from Brachiaria brizantha, named BbrizAGL6, was described in sexual and apomictic plants. Phylogenetic analyses indicated that BbrizAGL6 belongs to the AGL6-like subfamily of proteins and clusters together with the AGL6-like protein of other monocots. BbrizAGL6 and AGL6 show conservation of the protein complex. Furthermore, BbrizAGL6 expressed preferentially in reproductive tissues and corresponding transcripts were detected in anthers and ovules. In ovules of B. brizantha, where the main differences among sexual and apomictic reproduction occur, BbrizAGL6 was differentially modulated. Transcripts of BbrizAGL6 were localised in the megaspore mother cell of ovaries from apomictic and sexual plants and, additionally, in the region where aposporic initial cells differentiate, in the nucellus of apomictic plants. For the first time, a role of an AGL6-like gene in megasporogenesis of apomictic and sexual plants is suggested.
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References
Alves ER, Carneiro VTC, Araujo ACG (2001) Direct evidence of pseudogamy in an apomictic Brachiaria brizantha (Poaceae). Sex Plant Reprod 14:207–212
Alves ER, Carneiro VTC, Dusi DMA (2007) In situ localization of three cDNA sequences associated with the later stages of aposporic embryo sac development of Brachiaria brizantha. Protoplasma 231:161–171
Araujo ACG, Mukhambetzhanov S, Pozzobon MT, Santana EF, Carneiro VTC (2000) Female gametophyte development in apomictic and sexual Brachiaria brizantha (Poaceae). Rév de Cytol Biol Végétales - Le Botaniste Tome 23:13–28
Asker SE, Jerling L (1992) Apomixis in plants. Boca Raton, Florida, USA: CRC Press, Inc 298 p
Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20
Brambilla V, Battaglia R, Colombo M, Masiero S, Bencivenga S, Kater MM, Colombo L (2007) Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell 19:2544–2556
Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37
Davies B, Schwarz-Sommer Z (1994) Control of floral organ identity by homeotic MADS-box transcription factors. Results Probl Cell Differ 20:235–258
de Folter S, Immink RG, Kieffer M, Parenicova L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17:1424–1433
Dusi DMA, Willemse MTM (1999) Apomixis in Brachiaria decumbens Stapf: gametophytic development and reproductive calendar. Acta Biol Cracov Ser Bot 41:151–162
Egea-Cortines M, Saedler H, Sommer H (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J 18:5370–5379
Favaro R, Immink RG, Ferioli V, Bernasconi B, Byzova M, Angenent GC, Kater M, Colombo L (2002) Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants. Mol Genet Genomics 268:152–159
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
Gramzow L, Theissen G (2010) A hitchhiker's guide to the MADS world of plants. Genome Biol 11:214
Guerin J, Rossel JB, Robert S, Tsuchiya T, Koltunow AMG (2000) A DEFICIENS homologue is down-regulated during apomictic initiation in ovules of Hieracium. Planta 210:914–920
Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529
Hou X-J, Liu S-R, Khan M, Hu C-G, Zhang J-Z (2013) Genome-wide identification, classification, expression profiling, and SSR marker development of the MADS-box gene family in Citrus. Plant Mol Biol Rep 1–14
Immink R, Tonaco I, de Folter S, Shchennikova A, van Dijk A, Busscher-Lange J, Borst J, Angenent G (2009) SEPALLATA 3: the 'glue' for MADS box transcription factor complex formation. Genome Biol 10:R24
Jager M, Hassanin A, Manuel M, Le Guyader H, Deutsch J (2003) MADS-box genes in Ginkgo biloba and the evolution of the AGAMOUS family. Mol Biol Evol 20:842–854
Jang S, An K, Lee S, An G (2002) Characterization of tobacco MADS-box genes involved in floral initiation. Plant Cell Physiol 43:230–238
Koltunow AMG, Grossniklaus U (2003) Apomixis: a developmental perspective. Ann Rev Plant Biol 54:547–574
Koltunow AMG, Johnson SD, Rodrigues JCM, Okada T, Hu Y, Tsuchiya T, Wilson S, Fletcher P, Ito K, Suzuki G, Mukai Y, Fehrer J, Bicknell RA (2011) Sexual reproduction is the default mode in apomictic Hieracium subgenus Pilosella, in which two dominant loci function to enable apomixis. Plant J 66:890–902
Koo SC, Bracko O, Park MS, Schwab R, Chun HJ, Park KM, Seo JS, Grbic V, Balasubramanian S, Schmid M, Godard F, Yun D-J, Lee SY, Cho MJ, Weigel D, Kim MC (2010) Control of lateral organ development and flowering time by the Arabidopsis thaliana MADS-box Gene AGAMOUS-LIKE6. Plant J 62:807–816
Li H, Liang W, Hu Y, Zhu L, Yin C, Xu J, Dreni L, Kater MM, Zhang D (2011) Rice MADS6 interacts with the floral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13, and DROOPING LEAF in specifying floral organ identities and meristem fate. Plant Cell 23:2536–2552
Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) Shatterproof MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770
Liu X, Anderson J, Pijut P (2010) Cloning and characterization of Prunus serotina AGAMOUS, a putative flower homeotic gene. Plant Mol Biol Rep 28(2):193–203
Liu T, Li Y, Zhang C, Qian Y, Wang Z, Hou X (2012a) Overexpression of FLOWERING LOCUS C, isolated from non-heading Chinese cabbage (Brassica campestris ssp. chinensis Makino), influences fertility in Arabidopsis. Plant Mol Biol Rep 30:1444–1449
Liu Y, Kong J, Li T, Wang Y, Wang A, Han Z (2012b) Isolation and characterization of an APETALA1-like gene from pear (Pyrus pyrifolia). Plant Mol Biol Rep 1–9
Matias-Hernandez L, Battaglia R, Galbiati F, Rubes M, Eichenberger C, Grossniklaus U, Kater MM, Colombo L (2010) VERDANDI is a direct target of the MADS domain ovule identity complex and affects embryo sac differentiation in Arabidopsis. Plant Cell 22:1702–1715
Mena M, Mandel MA, Lerner DR, Yanofsky MF, Schmidt RJ (1995) A characterization of the MADS-box gene family in maize. Plant J 8:845–854
Moon YH, Kang HG, Jung JY, Jeon JS, Sung SK, An G (1999) Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol 120:1193–1204
Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195
Nogler GA (1984) Gametophytic apomixis. In: Johri BM (ed) Embriology of angiosperms. Springer-Verlag, Berlin, pp 475–518
Ohmori S, Kimizu M, Sugita M, Miyao A, Hirochika H, Uchida E, Nagato Y, Yoshida H (2009) MOSAIC FLORAL ORGANS1, an AGL6-Like MADS box gene, regulates floral organ identity and meristem fate in rice. Plant Cell 21:3008–3025
Oliveira R, Chalfun-Junior A, Paiva L, Andrade A (2010) In silico and quantitative analyses of MADS-Box genes in Coffea arabica. Plant Mol Biol Rep 28(3):460–472
Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada J-P (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–632
Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538–1551
Pessino SC, Espinoza F, Martinez EJ, Ortiz JP, Valle EM, Quarin CL (2001) Isolation of cDNA clones differentially expressed in flowers of apomictic and sexual Paspalum notatum. Hereditas 134:35–42
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
Polegri L, Calderini O, Arcioni S, Pupilli F (2010) Specific expression of apomixis-linked alleles revealed by comparative transcriptomic analysis of sexual and apomictic Paspalum simplex Morong flowers. J Exp Bot 61:1869–1883
Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140:345–356
Reinheimer R, Kellogg EA (2009) Evolution of AGL6-like MADS box genes in grasses (Poaceae): ovule expression is ancient and palea expression is new. Plant Cell 21:2591–2605
Riechmann JL, Krizek BA, Meyerowitz EM (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci U S A 93:4793–4798
Rijpkema AS, Zethof J, Gerats T, Vandenbussche M (2009) The petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant J 60:1–9
Rodrigues JCM, Cabral GB, Dusi DMA, Mello LV, Rigden D, Carneiro VTC (2003) Identification of differentially expressed cDNA sequences in ovaries of sexual and apomictic plants of Brachiaria brizantha. Plant Mol Biol 53:745–757
Rodriguez-Leal D, Vielle-Calzada J-P (2012) Regulation of apomixis: learning from sexual experience. Curr Opin Plant Biol 15(5):549–555
Rozen S, Skaletsky JH (2000) Primer3 on the WWW for general users and for biologist programmers In: Krawetz S MSe, editor. Bioinformatics methods and protocols: methods in molecular biology. Totowa: Humana Press, pp 365–386
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Sharbel TF, Voigt M-L, Corral JM, Galla G, Kumlehn J, Klukas C, Schreiber F, Vogel H, Rotter B (2010) Apomictic and sexual ovules of Boechera display heterochronic global gene expression patterns. Plant Cell 22:655–671
Silveira ED, Alves-Ferreira M, GuimarãeS LA, da Silva FR, Carneiro VTC (2009) Selection of reference genes for quantitative real-time PCR expression studies in the apomictic and sexual grass Brachiaria brizantha. BMC Plant Biol 9:84
Silveira ED, Guimarães LA, Dusi DMA, da Silva FR, Martins NF, do Carmo Costa M, Alves-Ferreira M, Carneiro VTC (2012) Expressed sequence-tag analysis of ovaries of Brachiaria brizantha reveals genes associated with the early steps of embryo sac differentiation of apomictic plants. Plant Cell Rep 31(2):403–16
Simon P (2003) Q-gene: processing quantitative real-time RT–PCR data. Bioinformatics 19:1439–1440
Singh M, Goel S, Meeley RB, Dantec C, Parrinello H, Michaud C, Leblanc O, Grimanelli D (2011) Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23:443–458
Song J-J, Ma W, Tang Y-J, Chen Z-Y, Liao J-P (2010) Isolation and characterization of three MADS-box genes from Alpinia hainanensis (Zingiberaceae). Plant Mol Biol Rep 28(2):264–276
Southerton SG, Marshall H, Mouradov A, Teasdale RD (1998) Eucalypt MADS-box genes expressed in developing flowers. Plant Physiol 118:365–372
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Theissen G, Saedler H (2001) Plant biology floral quartets. Nature 409:469–471
Theissen G, Kim JT, Saedler H (1996) Classification 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
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Thompson BE, Bartling L, Whipple C, Hall DH, Sakai H, Schmidt R, Hake S (2009) Bearded-ear encodes a MADS box transcription factor critical for maize floral development. Plant Cell 21:2578–2590
Vandenbussche M, Zethof J, Royaert S, Weterings K, Gerats T (2004) The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. Plant Cell 16:741–754
Viaene T, Vekemans D, Becker A, Melzer S, Geuten K (2010) Expression divergence of the AGL6 MADS domain transcription factor lineage after a core eudicot duplication suggests functional diversification. BMC Plant Biol 10:148
Wang Y-Q, Melzer R, Theißen G (2010) Molecular interactions of orthologues of floral homeotic proteins from the gymnosperm Gnetum gnemon provide a clue to the evolutionary origin of ‘floral quartets’. Plant J 64(2):177–190
Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis DE, de Pamphilis CW, Ma H (2005) The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209–2223
Zhang J, Nallamilli BR, Mujahid H, Peng Z (2010) OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J 64:604–617
Zhang D, Hu C, Ouyang Y, Yao J (2012) Construction of a full-length cDNA library and analysis of expressed sequence tags from inflorescence of apomictic sabaigrass (Eulaliopsis binata). Plant Mol Biol Rep 30:46–54
Acknowledgements
The authors acknowledge Ana L.M. Lacerda and Andrea D. Koehler for technical help in RNA extraction and Flávia S. Ferreira for dissecting ovaries. This work was supported by the National Council for Scientific and Technological Development-CNPq (490749/2008-9–VTCC) and the Brazilian Agricultural Research Corporation-Embrapa (0209020010.000- VTCC). This work is part of LAG’s PhD thesis from Pós-Graduação em Biologia Molecular, University of Brasilia-UnB, Brazil, with a partial fellowship from CNPq and Embrapa. CNPq also provided a 1-year fellowship for LAG at Università degli Studi di Milano, Italy.
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Guimarães, L.A., de A. Dusi, D.M., Masiero, S. et al. BbrizAGL6 Is Differentially Expressed During Embryo Sac Formation of Apomictic and Sexual Brachiaria brizantha Plants. Plant Mol Biol Rep 31, 1397–1406 (2013). https://doi.org/10.1007/s11105-013-0618-8
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DOI: https://doi.org/10.1007/s11105-013-0618-8