Research advances and molecular mechanism on SPL
 transcription factors in regulating plant flower development

doi:10.3969/j.issn.1000-2006.201708015

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2018, Vol. 42 ›› Issue (03): 159-166.doi: 10.3969/j.issn.1000-2006.201708015

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Research advances and molecular mechanism on SPL transcription factors in regulating plant flower development

TIAN Jing, ZHAO Xueyuan, XIE Longsheng, QUAN Jinyi, YAO Lianmei, WANG Guodong, ZHENG Yaoqang, LIU Xuemei^*

College of Life Science, Northeast Forestry University, Harbin 150040, China

Online:2018-06-06 Published:2018-06-06

Abstract

Abstract: Abstract: SPL(squamosa promoter-binding protein-like)transcription factor is a kind of gene family unique to plants. It is widely found in green plants and plays an important role in plant growth and development. Flower development is the most important process in plant reproductive development, including changes in the different developmental patterns, such as flowering determination, flower evocation, and floral organ development. This paper summarized the structure and function of SPL transcriptional factors, and in particular described the molecular mechanism and biological function of the SPL gene during plant flower development. Finally, we concluded that SPL transcription factors can be directly or indirectly involved in the photoperiod pathway, gibberellin pathway, and age pathway to control the flowering time in plants. The SPL gene can directly activate the downstream floral meristem identity genes,such as LEAFY(LFY), which regulate the flowering transition in plants. The SPL gene can regulate floral organ and fertility development by the interaction of downstream floral organ identity genes, such as controlling the length and shape of the inflorescence and pedicel, and the size of floral organ. The SPL gene can also regulate plant microsporogenesis and megasporogenesis, male and female gametophyte development. According to related research results with Arabidopsis, we have preliminarily mapped the molecular mechanism of Arabidopsis flowering regulation.

CLC Number:

Q943.2

TIAN Jing, ZHAO Xueyuan, XIE Longsheng, QUAN Jinyi, YAO Lianmei, WANG Guodong, ZHENG Yaoqang, LIU Xuemei. Research advances and molecular mechanism on SPL transcription factors in regulating plant flower development[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2018, 42(03): 159-166.

References

[1] SHI Q, ZHOU L, WANG Y, et al. A strategy for screening monoclonal antibodies for Arabidopsis flowers[J]. Front Plant Sci, 2017, 8: 270. DOI:10.3389/fpls.2017.00270.
[2] MATSUOKA D, YASUFUKU T, FURUYA T, et al. An abscisic acid inducible Arabidopsis MAPKKK, MAPKKK18 regulates leaf senescence via its kinase activity[J]. Plant Mol Biol, 2015, 87(6): 565-575. DOI:10.1007/s11103-015-0295-0.
[3] SMYTH J B, WANG J H, BARLOW R M, et al. Experimental acute selenium intoxication in lambs[J]. J Comp Pathol, 1990, 102(2): 197-209. DOI:10.1016/s0021-9975(08)80125-9.
[4] COEN E S, MEYEROWITZ E M. The war of the whorls: genetic interactions controlling flower development[J]. Nature, 1991, 353(6339): 31-37. DOI:10.1038/353031a0.
[5] THEISSEN G. Development of floral organ identity: stories from the MADS house[J]. Curr Opin Plant Biol, 2001, 4(1): 75-85. DOI:10.1016/s1369-5266(00)00139-4.
[6] RIECHMANN J L, HEARD J, MARTIN G, et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes[J]. Science, 2000, 290(5499): 2105-2110.
[7] INITIATIVE T A G, COPENHAVER G P. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana TAGI ‘The Arabidopsis Genome Initiative'[J]. Nature, 2000, 408:796-815 10.1038/35048692 11130711. 2000, 408: 796-815.
[8] CARDON GH, HÖHMANN S, NETTESHEIM K, et al. Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition[J]. Plant J, 1997, 12(2): 367-377. DOI:10.1046/j.1365-313x.1997.12020367.x.
[9] CARDON G, HÖHMANN S, KLEIN J, et al. Molecular characterisation of the Arabidopsis SBP-box genes[J]. Gene, 1999, 237(1): 91-104. DOI:10.1016/s0378-1119(99)00308-x.
[10] KLEIN J, SAEDLER H, HUIJSER P. A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA[J]. Mol Gen Genet, 1996, 250(1): 7-16. DOI:10.1007/bf02191820.
[11] MANNING K, TÖR M, POOLE M, et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening[J]. Nat Genet, 2006, 38(8): 948-952. DOI:10.1038/ng1841.
[12] LÄNNENPÄÄ M, JÄNÖNEN I, HÖLTTÄ-VUORI M, et al. A new SBP-box gene BpSPL1 in silver birch(Betula pendula)[J]. Physiol Plant, 2004, 120(3): 491-500. DOI:10.1111/j.0031-9317.2004.00254.x.
[13] KROPAT J, TOTTEY S, BIRKENBIHL R P, et al. A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element[J]. Proceedings of the National Academy of Sciences, 2005, 102(51): 18730-18735. DOI:10.1073/pnas.0507693102.
[14] ARAZI T, TALMOR-NEIMAN M, STAV R, et al. Cloning and characterization of micro-RNAs from moss[J]. Plant J, 2005, 43(6): 837-848. DOI:10.1111/j.1365-313X.2005.02499.x.
[15] ERIKSSON EM, BOVY A, MANNING K, et al. Effect of the Colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening[J]. Plant Physiol, 2004, 136(4): 4184-4197. DOI:10.1104/pp.104.045765.
[16] MORENO M A, HARPER L C, KRUEGER R W, et al. liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis[J]. Genes Dev, 1997, 11(5): 616-628. DOI:10.1101/gad.11.5.616.
[17] RIESE M, HÖHMANN S, SAEDLER H, et al. Comparative analysis of the SBP-box gene families in P. patens and seed plants[J]. Gene, 2007, 401(1/2): 28-37. DOI:10.1016/j.gene.2007.06.018.
[18] HOU H, LI J, GAO M, et al. Genomic organization, phylogenetic comparison and differential expression of the SBP-box family genes in grape[J]. PLoS ONE, 2013, 8(3): e59358. DOI:10.1371/journal.pone.0059358.
[19] HULTQUIST J F, DORWEILER J E. Feminized tassels of maize mop1 and ts1 mutants exhibit altered levels of miR156 and specific SBP-box genes[J]. Planta, 2008, 229(1): 99-113. DOI:10.1007/s00425-008-0813-2.
[20] 陈晓博. 参与番茄花柄离区发育的转录因子SPL3的基因功能研究[D]. 北京:中国农业科学院, 2010.
[21] XING S, SALINAS M, HÖHMANN S, et al. miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis[J]. Plant Cell, 2010, 22(12): 3935-3950. DOI:10.1105/tpc.110.079343.
[22] GANDIKOTA M, BIRKENBIHL R P, HÖHMANN S, et al. The miRNA156/157 recognition element in the 3' UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings[J]. Plant J, 2007, 49(4): 683-693. DOI:10.1111/j.1365-313X.2006.02983.x.
[23] WANG Y, HU Z, YANG Y, et al. Function annotation of an SBP-box gene in Arabidopsis based on analysis of co-expression networks and promoters[J]. Int J Mol Sci, 2009, 10(1): 116-132. DOI:10.3390/ijms10010116.
[24] WU G. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3[J]. Development, 2006, 133(18): 3539-3547. DOI:10.1242/dev.02521.
[25] USAMI T, HORIGUCHI G, YANO S, et al. The more and smaller cells mutants of Arabidopsisthaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty[J]. Development, 2009, 136(6): 955-964. DOI:10.1242/dev.028613.
[26] JIAO Y, WANG Y, XUE D, et al. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice[J]. Nat Genet, 2010, 42(6): 541-544. DOI:10.1038/ng.591.
[27] WANG H, NUSSBAUM-WAGLER T, LI B, et al. The origin of the naked grains of maize[J]. Nature,2005, 436(7051): 714-719. DOI:10.1038/nature03863.
[28] UNTE U S, SORENSEN A M, PESARESI P, et al. SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis[J]. Plant Cell, 2003, 15(4): 1009-1019. DOI:10.1105/tpc.010678.
[29] ZHANG Y, SCHWARZ S, SAEDLER H, et al. SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis[J]. Plant Mol Biol, 2007, 63(3): 429-439. DOI:10.1007/s11103-006-9099-6.
[30] STONE J M, LIANG X, NEKL E R, et al. Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1[J]. Plant J, 2005, 41(5): 744-754. DOI:10.1111/j.1365-313X.2005.02334.x.
[31] GUO J, SONG J, WANG F, et al. Genome-wide identification and expression analysis of rice cell cycle genes[J]. Plant Mol Biol, 2007, 64(4): 349-360. DOI:10.1007/s11103-007-9154-y.
[32] YAMASAKI K, KIGAWA T, INOUE M, et al. A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors[J]. J Mol Biol, 2004, 337(1): 49-63. DOI:10.1016/j.jmb.2004.01.015.
[33] BIRKENBIHL RP, JACH G, SAEDLER H, et al. Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains[J]. J Mol Biol, 2005, 352(3): 585-596. DOI:10.1016/j.jmb.2005.07.013.
[34] ALVAREZ-BUYLLA E R, BENÍTEZ M, CORVERA-POIRÉ A, et al. Flower development[J/OL]. The Arabidopsis Book, 2010, 8: e0127. DOI:10.1199/tab.0127.
[35] JACK T. Molecular and genetic mechanisms of floral control[J]. Plant Cell, 2004, 16: 17. DOI:10.1105/tpc.017038.
[36] TEOTIA S, TANG G. To bloom or not to bloom: role of microRNAs in plant flowering[J]. Mol Plant,2015, 8(3): 359-377. DOI:10.1016/j.molp.2014.12.018.
[37] LEE J, OH M, PARK H, et al. SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy[J]. Plant J, 2008, 55(5): 832-843. DOI:10.1111/j.1365-313X.2008.03552.x.
[38] SCHMID M, UHLENHAUT N H, GODARD F, et al. Dissection of floral induction pathways using global expression analysis[J]. Development, 2003, 130(24): 6001-6012. DOI:10.1242/dev.00842.
[39] JUNG J H, JU Y, SEO P J, et al. The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis[J]. Plant J, 2012, 69(4): 577-588. DOI:10.1111/j.1365-313X.2011.04813.x.
[40] LAL S, PACIS L B, SMITH H M. Regulation of the SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE genes/microRNA156 module by the homeodomain proteins PENNYWISE and POUND-FOOLISH in Arabidopsis[J]. Mol Plant, 2011, 4(6): 1123-1132. DOI:10.1093/mp/ssr041.
[41] PRESTON J C, HILEMAN L C. SQUAMOSA-PROMOTER BINDING PROTEIN 1 initiates flowering in Antirrhinum majus through the activation of meristem identity genes[J]. Plant J, 2010, 62(4): 704-712. DOI:10.1111/j.1365-313X.2010.04184.x.
[42] YU S, GALVAO V C, ZHANG Y C, et al. Gibberellin regulates the Arabidopsis floral transitionthrough miR156-Targeted SQUAMOSA PROMOTER BINDING-LIKE transcription factors[J]. The Plant Cell, 2012, 24(8): 3320-3332. DOI:10.1105/tpc.112.101014.
[43] YU S, CAO L, ZHOU C M, et al. Sugar is an endogenous cue for juvenile-to-adult phase transition in plants[J]. eLife, 2013, 2. DOI:10.7554/elife.00269.
[44] CHUCK G, CIGAN A M, SAETEURN K, et al. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA[J]. Nat Genet, 2007, 39(4): 544-549. DOI:10.1038/ng2001.
[45] ZHANG T, WANG J, ZHOU C. The role of miR156 in developmental transitions in Nicotiana tabacum[J]. Sci China Life Sci, 2015, 58(3): 253-260. DOI:10.1007/s11427-015-4808-5.
[46] XIE K, WU C, XIONG L. Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice[J]. Plant Physiol, 2006, 142(1): 280-293. DOI:10.1104/pp.106.084475.
[47] HYUN Y, RICHTER R, VINCENT C, et al. Multi-layered regulation of SPL15 and cooperation with SOC1 integrate endogenous flowering pathways at the Arabidopsis shoot meristem[J]. Dev Cell, 2016, 37(3): 254-266. DOI:10.1016/j.devcel.2016.04.001.
[48] WU G, PARK M Y, CONWAY S R, et al. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis[J]. Cell, 2009, 138(4): 750-759. DOI:10.1016/j.cell.2009.06.031.
[49] HYUN Y, RICHTER R, COUPLAND G. Competence to flower: age-controlled sensitivity to environmental cues[J]. Plant Physiology, 2016, 173(1): 36-46. DOI:10.1104/pp.16.01523.
[50] AUKERMAN MJ, SAKAI H. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes[J]. Plant Cell, 2003, 15(11): 2730-2741. DOI:10.1105/tpc.016238.
[51] JUNG J H, SEO Y H, SEO P J, et al. The GIGANTEA-regulated MicroRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis[J]. The Plant Cell Online, 2007, 19(9): 2736-2748. DOI:10.1105/tpc.107.054528.
[52] MAY P, LIAO W, WU Y, et al. The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development[J]. Nat Commun, 2013, 4: 2145. DOI:10.1038/ncomms3145.
[53] KIM J J, LEE J H, KIM W, et al. The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis[J]. Plant Physiol, 2012, 159(1): 461-478. DOI:10.1104/pp.111.192369.
[54] POETHIG R S. Phase change and the regulation of developmental timing in plants[J]. Science, 2003, 301(5631): 334-336. DOI:10.1126/science.1085328.
[55] BÄURLE I, DEAN C. The timing of developmental transitions in plants[J]. Cell, 2006, 125(4): 655-664. DOI:10.1016/j.cell.2006.05.005.
[56] HUIJSER P, SCHMID M. The control of developmental phase transitions in plants[J]. Development,2011, 138(19): 4117-4129. DOI:10.1242/dev.063511.
[57] JUNG J H, SEO P J, KANG S K, et al. miR172 signals are incorporated into the miR156 signaling pathway at the SPL3/4/5 genes in Arabidopsis developmental transitions[J]. Plant Mol Biol, 2011, 76(1/2): 35-45. DOI:10.1007/s11103-011-9759-z.
[58] YAMAGUCHI A, WU M F, YANG L, et al. The MicroRNA-regulated SBP-Box transcription factor SPL3 Is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1[J]. Developmental Cell,2009, 17(2): 268-278. DOI:10.1016/j.devcel.2009.06.007.
[59] GOU JY, FELIPPES FF, LIU CJ, et al. Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor[J]. Plant Cell, 2011, 23(4): 1512-1522. DOI:10.1105/tpc.111.084525.
[60] PROVENIERS M. Sugars speed up the circle of life[J]. eLife, 2013, 2: e00625. DOI:10.7554/eLife.00625.
[61] YANG L, CONWAY S R, POETHIG R S. Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156[J]. Development, 2011, 138(2): 245-249. DOI:10.1242/dev.058578.
[62] YANG L, XU M, KOO Y, et al. Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C[J]. eLife, 2013, 2: e00260. DOI:10.7554/eLife.00260.
[63] KING R W, HISAMATSU T, GOLDSCHMIDT E E, et al. The nature of floral signals in Arabidopsis. I. photosynthesis and a far-red photoresponse independently regulate flowering by increasing expression of FLOWERING LOCUS T(FT)[J]. Journal of Experimental Botany, 2008, 59(14): 3811-3820. DOI:10.1093/jxb/ern231.
[64] IRISH V F. The flowering of Arabidopsis flower development[J]. Plant J, 2010, 61(6): 1014-1028. DOI:10.1111/j.1365-313X.2009.04065.x.
[65] GOLDBERG RB, DE PAIVA G, YADEGARI R. Plant embryogenesis: zygote to seed[J]. Science, 1994, 266(5185): 605-614. DOI:10.1126/science.266.5185.605.
[66] LORD E M, RUSSELL S D. The mechanisms of pollination and fertilization in plants[J]. Annu Rev Cell Dev Biol, 2002, 18: 81-105. DOI:10.1146/annurev.cellbio.18.012502.083438.
[67] CHAUDHURY A M, MING L, MILLER C, et al. Fertilization-independent seed development in Arabidopsis thaliana[J]. Proceedings of the National Academy of Sciences, 1997, 94(8): 4223-4228. DOI:10.1073/pnas.94.8.4223.
[68] OHAD N, YADEGARI R, MARGOSSIAN L, et al. Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization[J]. Plant Cell, 1999, 11(3): 407-416. DOI:10.1105/tpc.11.3.407.
[69] AUNG B, GRUBER M Y, AMYOT L, et al. MicroRNA156 as a promising tool for alfalfa improvement[J]. Plant Biotechnol J, 2015, 13(6): 779-790. DOI:10.1111/pbi.12308.
[70] FERREIRA E SILVA GF, SILVA EM, AZEVEDO Mda S, et al. microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development[J]. Plant J, 2014, 78(4): 604-618. DOI:10.1111/tpj.12493.
[71] XING S, SALINAS M, GARCIA-MOLINA A, et al. SPL8 and miR156-targeted SPL genes redundantly regulate Arabidopsis gynoecium differential patterning[J]. Plant J, 2013, 75(4): 566-577. DOI:10.1111/tpj.12221.
[72] WANG Y, WANG Z, AMYOT L, et al. Ectopic expression of miR156 represses nodulation and causes morphological and developmental changes in Lotus japonicus[J]. Mol Genet Genomics, 2015, 290(2): 471-484. DOI:10.1007/s00438-014-0931-4.
[73] SHIKATA M, KOYAMA T, MITSUDA N, et al. Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase[J]. Plant Cell Physiol, 2009, 50(12): 2133-2145. DOI:10.1093/pcp/pcp148.
[74] KRIZEK B A, ANDERSON JT. Control of flower size[J]. J Exp Bot, 2013, 64(6): 1427-1437. DOI:10.1093/jxb/ert025.
[75] HEPWORTH J, LENHARD M. Regulation of plant lateral-organ growth by modulating cell number and size[J]. Curr Opin Plant Biol, 2014, 17: 36-42. DOI:10.1016/j.pbi.2013.11.005.
[76] WANG Z, WANG Y, KOHALMI SE, et al. SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 2 controls floral organ development and plant fertility by activating ASYMMETRIC LEAVES 2 in Arabidopsis thaliana[J]. Plant Mol Biol, 2016, 92(6): 661-674. DOI:10.1007/s11103-016-0536-x.
[77] KANRAR S, BHATTACHARYA M, ARTHUR B, et al. Regulatory networks that function to specify flower meristems require the function of homeobox genes PENNYWISE and POUND-FOOLISH in Arabidopsis[J]. Plant J, 2008, 54(5): 924-937. DOI:10.1111/j.1365-313X.2008.03458.x.
[78] HAY A, TSIANTIS M. KNOX genes: versatile regulators of plant development and diversity[J]. Development, 2010, 137(19): 3153-3165. DOI:10.1242/dev.030049.
[79] GUO M, THOMAS J, COLLINS G, et al. Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis[J]. Plant Cell, 2008, 20(1): 48-58. DOI:10.1105/tpc.107.056127.
[80] WEIGEL D, NILSSON O. A developmental switch sufficient for flower initiation in diverse plants[J]. Nature, 1995, 377(6549): 495-500. DOI:10.1038/377495a0.
[81] WEIGEL D, ALVAREZ J, SMYTH DR, et al. LEAFY controls floral meristem identity in Arabidopsis[J]. Cell, 1992, 69(5): 843-859. DOI:10.1016/0092-8674(92)90295-n.
[82] YAMAGUCHI N, YAMAGUCHI A, ABE M, et al. LEAFY controls Arabidopsis pedicel length and orientation by affecting adaxial-abaxial cell fate[J]. Plant J, 2012, 69(5): 844-856. DOI:10.1111/j.1365-313X.2011.04836.x.
[83] BEEMSTER G T, FIORANI F, INZÉ D. Cell cycle: the key to plant growth control[J]. Trends Plant Sci,2003, 8(4): 154-158. DOI:10.1016/S1360-1385(03)00046-3.
[84] MIZUKAMI Y. A matter of size: developmental control of organ size in plants[J]. Curr Opin Plant Biol,2001, 4(6): 533-539. DOI:10.1016/s1369-5266(00)00212-0.
[85] LIU N, TU L, WANG L, et al. MicroRNA 157-targeted SPL genes regulate floral organ size and ovule production in cotton[J]. BMC Plant Biol, 2017, 17(1): 7. DOI:10.1186/s12870-016-0969-z.

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Research advances and molecular mechanism on SPL transcription factors in regulating plant flower development

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[13]	ZHANG Kaimin,WANG Yucheng, YANG Guiyan, GAO Caiqiu. Clone and expression analysis of ThPR1 gene in Tamarix hispida [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2013, 37(02): 45-49.