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Transcriptome-Wide Characterization of the MADS-Box Family in Pinesap Monotropa hypopitys Reveals Flowering Conservation in Non-photosynthetic Myco-Heterotrophs

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Abstract

Pinesap Monotropa hypopitys is a myco-heterotrophic non-photosynthetic higher angiosperm perennial plant devoid of vegetative organs and with standard flower arrangement. The MADS-domain transcription factor family has multiple regulatory functions in plant life cycle and is implicated in flower evolution and diversity. This study is the first to describe the MADS-box genes in a myco-heterotrophic eudicot. By performing the M. hypopitys transcriptome-wide analysis, we identified 30 MADS-box genes belonging to the major clades in the MIKCc and MIKC* lineages. Among them, MhyMADS18 is suggested as an ancestral gene of the cluster comprising AP1/FUL, FLC, SEP, and AGL6 clades. The RNA-seq profiling of the MhyMADS expression in the flowering plant revealed mRNAs specific to bracts, flowers, and roots with adventitious buds. Our results represent systematic and expression analysis of the pinesap MADS-box genes that may be involved in seed dormancy regulation, flowering time control, and flower organ identity specification. The obtained data should further our understanding of the roles played by the MADS-box genes in developmental regulation of myco-heterotrophic plants.

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References

  • Álvarez-Buylla ER, Ambrose BA, Flores-Sandoval E, Englund M, Garay-Arroyo A, García-Ponce B, de la Torre-Bárcena E, Espinosa-Matías S, Martínez E, Piñeyro-Nelson A, Engström P, Meyerowitz EM (2010) B-function expression in the flower center underlies the homeotic phenotype of Lacandonia schismatica (Triuridaceae). Plant Cell 22(11):3543–3559

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In Proceedings of the second international conference on intelligent systems for molecular biology, AAAI Press, Menlo Park, pp. 28–36

  • Balanzà V, Martínez-Fernández I, Ferrándiz C (2014) Sequential action of FRUITFULL as a modulator of the activity of the floral regulators SVP and SOC1. J Exp Bot 65(4):1193–1203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Basler D, Körner C (2014) Photoperiod and temperature responses of bud swelling and bud burst in four temperate forest tree species. Tree Physiol 34(4):377–388

    Article  PubMed  Google Scholar 

  • Behrend A, Borchert T, Hohe A (2015) “The usual suspects"- analysis of transcriptome sequences reveals deviating B gene activity in C. vulgaris bud bloomers. BMC Plant Biol 15:8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beletsky AV, Filyushin MA, Gruzdev EV, Mazur AM, Prokhortchouk EB, Kochieva EZ, Mardanov AV, Ravin NV, Skryabin KG (2017) De novo transcriptome assembly of the mycoheterotrophic plant Monotropa hypopitys. Genom Data 11:60–61

    Article  PubMed  Google Scholar 

  • Bemer M, Heijmans K, Airoldi C, Davies B, Angenent GC (2010) An atlas of type I MADS box gene expression during female gametophyte and seed development in Arabidopsis. Plant Physiol 154(1):287–300

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen WH, Li PF, Chen MK, Lee YI, Yang CH (2015a) FOREVER YOUNG FLOWER negatively regulates ethylene response DNA-binding factors by activating an ethylene-responsive factor to control Arabidopsis floral organ senescence and abscission. Plant Physiol 168(4):1666–1683

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen R, Shen LP, Wang DH, Wang FG, Zeng HY, Chen ZS, Peng YB, Lin YN, Tang X, Deng MH, Yao N, Luo JC, Xu ZH, Bai SN (2015b) A gene expression profiling of early rice stamen development that reveals inhibition of photosynthetic genes by OsMADS58. Mol Plant 8(7):1069–1089

    Article  PubMed  CAS  Google Scholar 

  • Cho S, Jang S, Chae S, Chung KM, Moon Y, An G, Jung SK (1999) Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol Biol 40:419–429

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353(6339):31–37

    Article  PubMed  CAS  Google Scholar 

  • Corbesier L, Coupland G (2006) The quest for florigen: a review of recent progress. J Exp Bot 57(13):3395–3403

    Article  PubMed  CAS  Google Scholar 

  • Davies B, Egea-Cortines M, de Andrade Silva E, Saedler H, Sommer H (1996) Multiple interactions amongst floral homeotic MADS box proteins. EMBO J 15(16):4330–4343

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Folter S, Busscher J, Colombo L, Losa A, Angenent GC (2004) Transcript profiling of transcription factor genes during silique development in Arabidopsis. Plant Mol Biol 56(3):351–366

    Article  PubMed  CAS  Google Scholar 

  • Delgado Sandoval SDC, Abraham Juárez MJ, Simpson J (2012) Agave tequilana MADS genes show novel expression patterns in meristems, developing bulbils and floral organs. Sex Plant Reprod 25(1):11–26

    Article  Google Scholar 

  • Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14(21):1935–1940

    Article  PubMed  CAS  Google Scholar 

  • Dreni L, Zhang D (2016) Flower development: the evolutionary history and functions of the AGL6 subfamily MADS-box genes. J Exp Bot 67(6):1625–1638

    Article  PubMed  CAS  Google Scholar 

  • Espinosa-Soto C, Immink RG, Angenent GC, Alvarez-Buylla ER, de Folter S (2014) Tetramer formation in Arabidopsis MADS domain proteins: analysis of a protein-protein interaction network. BMC Syst Biol 8:9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fan Z, Li J, Li X, Wu B, Wang J, Liu Z, Yin H (2015) Genome-wide transcriptome profiling provides insights into floral bud development of summer-flowering Camellia azalea. Sci Rep 5:9729

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fernandez DE, Wang CT, Zheng Y, Adamczyk BJ, Singhal R, Hall PK, Perry SE (2014) The MADS-domain factors AGAMOUS-LIKE15 and AGAMOUS-LIKE18, along with SHORT VEGETATIVE PHASE and AGAMOUS-LIKE24, are necessary to block floral gene expression during the vegetative phase. Plant Physiol 165(4):1591–1603

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ferrándiz C, Fourquin C (2014) Role of the FUL-SHP network in the evolution of fruit morphology and function. J Exp Bot 65(16):4505–4513

    Article  PubMed  CAS  Google Scholar 

  • Filyushin MA, Kochieva EZ, Skryabin KG (2015) 5.8S rRNA sequence and secondary structure in Monotropa hypopitys and related Ericaceae species. Dokl Biochem Biophys 463:264–267

    Article  PubMed  CAS  Google Scholar 

  • García-Luís A, Kanduser M, Santamarina P, Guardiola JL (1992) Low temperature influence on flowering in citrus. The separation of inductive and bud dormancy releasing effects. Physiol Plant 86(4):648–682

    Article  Google Scholar 

  • Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8(13):1548–1560

    Article  PubMed  CAS  Google Scholar 

  • Gramzow L, Ritz MS, Theissen G (2010) On the origin of MADS-domain transcription factors. Trends Genet 26(4):149–153

    Article  PubMed  CAS  Google Scholar 

  • Gramzow L, Weilandt L, Theißen G (2014) MADS goes genomic in conifers: towards determining the ancestral set of MADS-box genes in seed plants. Ann Bot 114(7):1407–1429

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gruzdev EV, Mardanov AV, Beletsky AV, Kochieva EZ, Ravin NV, Skryabin KG (2016) The complete chloroplast genome of parasitic flowering plant Monotropa hypopitys: extensive gene losses and size reduction. Mitochondrial DNA 1(1):212–213

    Article  Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, Macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, Leduc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512

    Article  PubMed  CAS  Google Scholar 

  • Hemming MN, Trevaskis B (2011) Make hay when the sun shines: the role of MADS-box genes in temperature-dependent seasonal flowering responses. Plant Sci 180(3):447–453

    Article  PubMed  CAS  Google Scholar 

  • Hill K, Wang H, Perry SE (2008) A transcriptional repression motif in the MADS factor AGL15 is involved in recruitment of histone deacetylase complex components. Plant J 53(1):172–185

    Article  PubMed  CAS  Google Scholar 

  • Hoenicka H, Nowitzki O, Hanelt D, Fladung M (2008) Heterologous overexpression of the birch FRUITFULL-like MADS-box gene BpMADS4 prevents normal senescence and winter dormancy in Populus tremula L. Planta 227:1001–1011

    Article  PubMed  CAS  Google Scholar 

  • Hsu HF, Huang CH, Chou LT, Yang CH (2003) Ectopic expression of an orchid (Oncidium Gower Ramsey) AGL6-like gene promotes flowering by activating flowering time genes in Arabidopsis thaliana. Plant Cell Physiol 44(8):783–794

    Article  PubMed  CAS  Google Scholar 

  • Immink RGH, Tonaco IAN, de Folter S, Shchennikova A, van Dijk ADJ, Busscher-Lange J, Borst JW, Angenent GC (2009) SEPALLATA3: the ‘glue’ for MADS box transcription factor complex formation. Genome Biol 10:R24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jaakola L, Poole M, Jones MO, Kämäräinen-Karppinen T, Koskimäki JJ, Hohtola A, Häggman H, Fraser PD, Manning K, King GJ, Thomson H, Seymour GB (2010) A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiol 153(4):1619–1629

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kanno A, Nakada M, Akita Y, Hirai M (2007) Class B gene expression and the modified ABC model in nongrass monocots. Sci World J 7:268–279

    Article  CAS  Google Scholar 

  • Koo SC, Bracko O, Park MS, Schwab R, Chun HJ, Park KM, Seo JS, Grbic V, Balasubramanian S, Schmid M, Godard F, Yun DJ, 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(5):807–816

    Article  PubMed  CAS  Google Scholar 

  • Kozlowski LP (2016) IPC—isoelectric point calculator. Biol Direct 11:55. https://doi.org/10.1186/s13062-016-0159-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  PubMed  CAS  Google Scholar 

  • Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Leake JR (1994) The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol 127:171–216

    Article  Google Scholar 

  • Leake JR, McKendrick SL, Bidartondo M, Read DJ (2004) Symbiotic germination and development of the myco-heterotroph Monotropa hypopitys in nature and its requirement for locally distributed Tricholoma spp. New Phytol 163(2):405–423

    Article  Google Scholar 

  • Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61(9):2247–2254

    Article  PubMed  CAS  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li D, Liu C, Shen L, Wu Y, Chen H, Robertson M, Helliwell CA, Ito T, Meyerowitz E, Yu H (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15(1):110–120

    Article  PubMed  Google Scholar 

  • Liu C, Zhang J, Zhang N, Shan H, Su K, Zhang J, Meng Z, Kong H, Chen Z (2010) Interactions among proteins of floral MADS-box genes in basal eudicots: implications for evolution of the regulatory network for flower development. Mol Biol Evol 27:1598–1611

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Kim YJ, Müller R, Yumul RE, Liu C, Pan Y, Cao X, Goodrich J, Chen X (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins. Plant Cell 23(10):3654–3670

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu C, Teo ZW, Bi Y, Song S, Xi W, Yang X, Yin Z, Yu H (2013) A conserved genetic pathway determines inflorescence architecture in Arabidopsis and rice. Dev Cell 24(6):612–622

    Article  PubMed  CAS  Google Scholar 

  • Logacheva MD, Schelkunov MI, Shtratnikova VY, Matveeva MV, Penin AA (2016) Comparative analysis of plastid genomes of non-photosynthetic Ericaceae and their photosynthetic relatives. Sci Rep 6:30042

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luo HL, Chen SM, Jiang JF, Chen Y, Chen FD, Teng NJ, Yin DM, Huang CB (2011) The expression of floral organ identity genes in contrasting water lily cultivars. Plant Cell Rep 30:1909–1918

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Yanofsky MF, Meyerowitz EM (1991) AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5:484–495

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Yanofsky MF (1995) The Arabidopsis AGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell 7(11):1763–1771

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17(1):10–12

    Article  Google Scholar 

  • Matsubara K, Shimamura K, Kodama H, Kokubun H, Watanabe H, Basualdo IL, Ando T (2008) Green corolla segments in a wild Petunia species caused by a mutation in FBP2, a SEPALLATA-like MADS box gene. Planta 228(3):401–409

    Article  PubMed  CAS  Google Scholar 

  • McAtee PA, Richardson AC, Nieuwenhuizen NJ, Gunaseelan K, Hoong L, Chen X, Atkinson RG, Burdon JN, David KM, Schaffer RJ (2015) The hybrid non-ethylene and ethylene ripening response in kiwifruit (Actinidia chinensis) is associated with differential regulation of MADS-box transcription factors. BMC Plant Biol 15:304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McCarthy EW, Mohamed A, Litt A (2015) Functional divergence of APETALA1 and FRUITFULL is due to changes in both regulation and coding sequence. Front Plant Sci 6:1076

    Article  PubMed  PubMed Central  Google Scholar 

  • Melzer R, Theissen G (2011) MADS and more: transcription factors that shape the plant. Methods Mol Biol 754:3–18

    Article  PubMed  CAS  Google Scholar 

  • Merckx VSFT., Freudenstein JV, Kissling J, Christenhusz MJM, Stotler RE, Crandall-Stotler B, Wickett N, Rudall PJ, Maas-van de Kamer H, Maas PJM (2013) Taxonomy and classification. In: Merckx VSFT (ed) Mycoheterotrophy: the biology of plants living on fungi. Springer, New York, pp 73–83

    Chapter  Google Scholar 

  • Mizzotti C, Ezquer I, Paolo D, Rueda-Romero P, Guerra RF, Battaglia R, Rogachev I, Aharoni A, Kater MM, Caporali E, Colombo L (2014) SEEDSTICK is a master regulator of development and metabolism in the Arabidopsis seed coat. PLoS Genet 10(12):e1004856

    Article  PubMed  PubMed Central  Google Scholar 

  • Murai K (2013) Homeotic genes and the ABCDE model for floral organ formation in wheat. Plants (Basel) 2(3):379–395

    Article  CAS  Google Scholar 

  • Niu Q, Li J, Cai D, Qian M, Jia H, Bai S, Hussain S, Liu G, Teng Y, Zheng X (2016) Dormancy-associated MADS-box genes and microRNAs jointly control dormancy transition in pear (Pyrus pyrifolia white pear group) flower bud. J Exp Bot 67(1):239–257

    Article  PubMed  CAS  Google Scholar 

  • Ohmori S, Kimizu M, Sugita M, Miyao A, Hirochika H, Uchida E, Nagato Y, Yoshida H (2009) MOSAIC FLORAL ORGANS 1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice. Plant Cell 21:3008–3025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pabón-Mora N, Hidalgo O, Gleissberg S, Litt A (2013) Assessing duplication and loss of APETALA1/FRUITFULL homologs in Ranunculales. Front Plant Sci 4:358

    Article  PubMed  PubMed Central  Google Scholar 

  • Parenicová 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pina C, Pinto F, Feijo´ JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756

    Article  PubMed  PubMed Central  CAS  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(6944):85–88

    Article  PubMed  CAS  Google Scholar 

  • Piwarzyk E, Yang Y, Jack T (2007) Conserved C-terminal motifs of the Arabidopsis proteins APETALA3 and PISTILLATA are dispensable for floral organ identity function. Plant Physiol 45(4):1495–1505

    Article  CAS  Google Scholar 

  • Ravin NV, Gruzdev EV, Beletsky AV, Mazur AM, Prokhortchouk EB, Filyushin MA, Kochieva EZ, Kadnikov VV, Mardanov AV, Skryabin KG (2016) The loss of photosynthetic pathways in the plastid and nuclear genomes of the non-photosynthetic mycoheterotrophic eudicot Monotropa hypopitys. BMC Plant Biol 16(Suppl 3):238

    Article  PubMed  CAS  Google Scholar 

  • Rijpkema AS, Royaert S, Zethof J, van der Weerden G, Gerats T, Vandenbussche M (2006) Analysis of the Petunia TM6 MADS box gene reveals functional divergence within the DEF/AP3 lineage. Plant Cell 18(8):1819–1832

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shchennikova AV, Beletsky AV, Shulga OA, Mazur AM, Prokhortchouk EB, Kochieva EZ, Ravin NV, Skryabin KG (2016) Deep-sequence profiling of miRNAs and their target prediction in Monotropa hypopitys. Plant Mol Biol 91(4–5):441–458

    Article  PubMed  CAS  Google Scholar 

  • Sung S, Amasino RM (2004) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7(1):4–10

    Article  PubMed  CAS  Google Scholar 

  • Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K, Münster T, Theissen G, Nozaki H, Ito M (2005) Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc Natl Acad Sci USA 102(7):2436–2441

    Article  PubMed  CAS  Google Scholar 

  • Tani E, Polidoros AN, Flemetakis E, Stedel C, Kalloniati C, Demetriou K, Katinakis P, Tsaftaris AS (2009) Characterization and expression analysis of AGAMOUS-like, SEEDSTICK-like, and SEPALLATA-like MADS-box genes in peach (Prunus persica) fruit. Plant Physiol Biochem 47(8):690–700

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, Saedler H (2001) Plant biology: floral quartets. Nature 409:469–471

    Article  PubMed  CAS  Google Scholar 

  • Vandelook F, Van Assche JA (2009) Temperature conditions control embryo growth and seed germination of Corydalis solida (L.) Clairv., a temperate forest spring geophyte. Plant Biol (Stuttg) 11(6):899–906

    Article  CAS  Google Scholar 

  • Vandenbussche M, Theissen G, Van de Peer Y, Gerats T (2003) Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res 31:4401–4409

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Varkonyi-Gasic E, Moss SM, Voogd C, Wu R, Lough RH, Wang YY, Hellens RP (2011) Identification and characterization of flowering genes in kiwifruit: sequence conservation and role in kiwifruit flower development. BMC Plant Biol 11:72

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Viaene T, Vekemans D, Irish VF, Geeraerts A, Huysmans S, Janssens S, Smets E, Geuten K (2009) Pistillata-duplications as a mode for floral diversification in (Basal) asterids. Mol Biol Evol 26(11):2627–2645

    Article  PubMed  CAS  Google Scholar 

  • Voogd C, Wang T, Varkonyi-Gasic E (2015) Functional and expression analyses of kiwifruit SOC1-like genes suggest that they may not have a role in the transition to flowering but may affect the duration of dormancy. J Exp Bot 66(15):4699–4710

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wallace GD (1975) Studies of the Monotropoidiae (Ericaceae): taxonomy and distribution. Wassman J Biol 33:1–88

    Google Scholar 

  • Walworth AE, Chai B, Song GQ (2016) Transcript profile of flowering regulatory genes in VcFT-overexpressing blueberry plants. PLoS ONE 11(6):e0156993

    Article  PubMed  PubMed Central  CAS  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(12):3005–3014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilkinson L (2011) ggplot2: elegant graphics for data analysis by WICKHAM H. Biometrics 67:678–679

    Article  Google Scholar 

  • Wu RM, Walton EF, Richardson AC, Wood M, Hellens RP, Varkonyi-Gasic E (2012) Conservation and divergence of four kiwifruit SVP-like MADS-box genes suggest distinct roles in kiwifruit bud dormancy and flowering. J Exp Bot 63(2):797–807

    Article  PubMed  CAS  Google Scholar 

  • Yalovsky S, Rodríguez-Concepción M, Bracha K, Toledo-Ortiz G, Gruissem W (2000) Prenylation of the floral transcription factor APETALA1 modulates its function. Plant Cell 12(8):1257–1266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang Y, Jack T (2004) Defining subdomains of the K domain important for protein-protein interactions of plant MADS proteins. Plant Mol Biol 55(1):45–59

    Article  PubMed  CAS  Google Scholar 

  • Yoo SK, Wu X, Lee JS, Ahn JH (2011) AGAMOUS-LIKE 6 is a floral promoter that negatively regulates the FLC/MAF clade genes and positively regulates FT in Arabidopsis. Plant J 65(1):62–76

    Article  PubMed  CAS  Google Scholar 

  • Yu X, Duan X, Zhang R, Fu X, Ye L, Kong H, Xu G, Shan H (2016) Prevalent exon-intron structural changes in the APETALA1/FRUITFULL. SEPALLATA, AGAMOUS-LIKE6, and FLOWERING LOCUS C MADS-box gene subfamilies provide new insights into their evolution. Front Plant Sci 7:598

    PubMed  PubMed Central  Google Scholar 

  • Zahn LM, Kong H, Leebens-Mack J, Kim S, Soltis PS, Landherr LL, Soltis DE, Depamphilis 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang JZ, Li ZM, Mei L, Yao JL, Hu CG (2009) PtFLC homolog from trifoliate orange (Poncirus trifoliata) is regulated by alternative splicing and experiences seasonal fluctuation in expression level. Planta 229(4):847–859

    Article  PubMed  CAS  Google Scholar 

  • Zhao S, Luo Y, Zhang Z, Xu M, Wang W, Zhao Y, Zhang L, Fan Y, Wang L (2014) ZmSOC1, a MADS-box transcription factor from Zea mays, promotes flowering in Arabidopsis. Int J Mol Sci 15(11):19987–20037

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This work was supported by a grant from the Russian Science Foundation (14-24-00175), and was done with the use of the experimental climate control facility. The authors thank Dr. Marina Chuenkova for providing language help.

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  1. Olga A. Shulga and Anna V. Shchennikova have contributed equally to this work.

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  1. Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Leninsky Ave. 33, bld. 2, Moscow, 119071, Russia

    Olga A. Shulga, Anna V. Shchennikova, Alexey V. Beletsky, Andrey V. Mardanov, Elena Z. Kochieva, Mikhail A. Filyushin, Nikolay V. Ravin & Konstantin G. Skryabin

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  1. Olga A. Shulga
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Shulga, O.A., Shchennikova, A.V., Beletsky, A.V. et al. Transcriptome-Wide Characterization of the MADS-Box Family in Pinesap Monotropa hypopitys Reveals Flowering Conservation in Non-photosynthetic Myco-Heterotrophs. J Plant Growth Regul 37, 768–783 (2018). https://doi.org/10.1007/s00344-017-9772-9

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  • DOI: https://doi.org/10.1007/s00344-017-9772-9

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