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Complex regulatory network of Betula BplSPL8 in planta

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Abstract

SQUAMOSA-promoter binding protein-like (SPL) proteins are plant-specific transcription factors and participate in different pathways, including the vegetative to reproductive transition, male sterility, biosynthesis of gibberellic acid (GA), plant morphogenesis and response to environmental stress. In this study, we generated transgenic Arabidopsis that overexpressed Betula BplSPL8 and confirmed that BplSPL8 is a transcription factor with transcriptional activation activity and is located in the nucleus. Functional analysis of BplSPL8 showed that it is involved in regulating different development processes: (1) BplSPL8 can delay flowering by reducing sensitivity to GA under short days; (2) BplSPL8 controls the number and morphogenesis of leaves, including up-rolling leaves under long days and folded leaves mediated by GA under short days; (3) BplSPL8 can promote root elongation during late development of roots and inhibit lateral root formation; (4) BplSPL8 may be involved in regulating carotenoid biosynthesis and secretion metabolism. These results show that there is a complex regulatory network for the SPL family genes that is mediated by other components and may provide a new insights for the functional research of SPL genes.

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References

  • Arazi T, Talmor-Neiman M, Stav R, Riese M, Huijser P, Baulcombe DC (2005) Cloning and characterization of micro-RNAs from moss. Plant J 43(6):837–848

    Article  CAS  PubMed  Google Scholar 

  • Cardon GH, Hohmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12(2):367–377

    Article  CAS  PubMed  Google Scholar 

  • Cardon G, Hohmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237(1):91–104

    Article  CAS  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 2(11):113–116

    Article  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  CAS  PubMed  Google Scholar 

  • Dinneny JR, Benfey PN (2008) Plant stem cell niches: standing the test of time. Cell 132(4):553–557

    Article  CAS  PubMed  Google Scholar 

  • Gayomba SR, Jung HI, Yan J, Danku J, Rutzke MA, Bernal M, Kramer U, Kochian LV, Salt DE, Vatamaniuk OK (2013) The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana. Metallomics 5(9):1262–1275

    Article  CAS  PubMed  Google Scholar 

  • Jung JH, Ju Y, Seo PJ, Lee JH, Park CM (2012) The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. Plant J 69(4):577–588

    Article  CAS  PubMed  Google Scholar 

  • Keller CP, Van Volkenburgh E (1997) Auxin-induced epinasty of tobacco leaf tissues (a nonethylene-mediated response). Plant Physiol 113(2):603–610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250(1):7–16

    CAS  PubMed  Google Scholar 

  • Krizek BA, Lewis MW, Fletcher JC (2006) RABBIT EARS is a second-whorl repressor of AGAMOUS that maintains spatial boundaries in Arabidopsis flowers. Plant J 45(3):369–383

    Article  CAS  PubMed  Google Scholar 

  • Li C, Lu S (2014) Molecular characterization of the SPL gene family in Populus trichocarpa. BMC Plant Biol 14:131

    Article  PubMed  PubMed Central  Google Scholar 

  • Li S, Yang X, Wu F, He Y (2012) HYL1 controls the miR156-mediated juvenile phase of vegetative growth. J Exp Bot 63(7):2787–2798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Hou H, Li X, Xiang J, Yin X, Gao H, Zheng Y, Bassett CL, Wang X (2013) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus x domestica Borkh.). Plant Physiol Biochem 70:100–114

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Yang C (2006) Temporal characteristics of developmental cycles of female and male flowers in Betula platyphylla in Northeastern China. Sci Silvaec Sin 42(12):28–32

    Google Scholar 

  • Macdonald AD, Mothersill DH (1987) Shoot development in Betula papyrifera. VI. Development of the reproductive structures. Can J Bot 65(3):466–475

    Article  Google Scholar 

  • Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124(1):33–44

    CAS  PubMed  Google Scholar 

  • Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M, Reed JW (2000) AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123(2):563–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nath U, Crawford BC, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299(5611):1404–1407

    Article  CAS  PubMed  Google Scholar 

  • Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955):257–263

    Article  CAS  PubMed  Google Scholar 

  • Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14(7):399–408

    Article  CAS  PubMed  Google Scholar 

  • Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17(3):354–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salinas M, Xing S, Hohmann S, Berndtgen R, Huijser P (2012) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 235(6):1171–1184

    Article  CAS  PubMed  Google Scholar 

  • Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67(1–2):183–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shikata M, Koyama T, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol 50(12):2133–2145

    Article  CAS  PubMed  Google Scholar 

  • Stone JM, Liang X, Nekl ER, Stiers JJ (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41(5):744–754

    Article  CAS  PubMed  Google Scholar 

  • Taylor-Teeples M, Lin L, de Lucas M, Turco G, Toal TW, Gaudinier A, Young NF, Trabucco GM, Veling MT, Lamothe R, Handakumbura PP, Xiong G, Wang C, Corwin J, Tsoukalas A, Zhang L, Ware D, Pauly M, Kliebenstein DJ, Dehesh K, Tagkopoulos I, Breton G, Pruneda-Paz JL, Ahnert SE, Kay SA, Hazen SP, Brady SM (2015) An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature 517(7536):571–575

    Article  CAS  PubMed  Google Scholar 

  • Toledo-Ortiz G, Huq E, Rodriguez-Concepcion M (2010) Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc Natl Acad Sci USA 107(25):11626–11631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker MR, Laux T (2007) Connecting the paths in plant stem cell regulation. Trends Cell Biol 17(8):403–410

    Article  CAS  PubMed  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Unte US, Sorensen AM, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15(4):1009–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welsch R, Maass D, Voegel T, Dellapenna D, Beyer P (2007) Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol 145(3):1073–1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing S, Salinas M, Hohmann S, Berndtgen R, Huijser P (2010) miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22(12):3935–3950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Nunokawa E, Ishizuka Y, Terada T, Shirouzu M, Osanai T, Tanaka A, Seki M, Shinozaki K, Yokoyama S (2004) A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. J Mol Biol 337(1):49–63

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein-Like7 is a central regulator for copper homeostasis in arabidopsis. Plant Cell 21(1):347–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu N, Cai WJ, Wang S, Shan CM, Wang LJ, Chen XY (2010) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22(7):2322–2335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu S, Galvao VC, Zhang YC, Horrer D, Zhang TQ, Hao YH, Feng YQ, Wang S, Schmid M, Wang JW (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 24(8):3320–3332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu N, Niu QW, Ng KH, Chua NH (2015) The role of miR156/SPLs modules in Arabidopsis lateral root development. Plant J 83(4):673–685

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Schwarz S, Saedler H, Huijser P (2007) SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Mol Biol 63(3):429–439

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Gao Y, Wang Z, Han Y, Zheng D, He J (2015) Lateral root development of related genes in Arabidopsis thaliana. J Heilongjiang Bayi Agric Univ 27(4):19–24

    Google Scholar 

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Acknowledgements

This work was financially supported by the National Science and Technology Program of China (2013AA102704), the National Natural Science Foundation of China (J1210053) and the Fundamental Research Funds for the Central Universities (2572015EA05). We are also grateful to Dr. Beth E. Hazen for critical reading and good advices of the manuscript.

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Correspondence to Xuemei Liu.

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Project funding: This work was financially supported by the National Science and Technology Program of China (2013AA102704), the National Natural Science Foundation of China (J1210053) and the Fundamental Research Funds for the Central Universities (2572015EA05).

The online version is available at http://www.springerlink.com.

Corresponding editor: Chai Ruihai.

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Liu, C., Guan, M., Hu, X. et al. Complex regulatory network of Betula BplSPL8 in planta. J. For. Res. 28, 881–889 (2017). https://doi.org/10.1007/s11676-017-0372-0

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