Advances of the Flowering Genes of Gymnosperms

Authors

  • Dun MAO Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Jiabao YE Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Feng XU Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)

DOI:

https://doi.org/10.15835/nbha47111343

Keywords:

floral development, flowering gene, Gymnosperms, juvenile period, reproductive growth

Abstract

Flowering is an important stage in the life cycle of plants and also a turning point from vegetative growth to reproductive growth. This process is affected by many exogenous and endogenous factors. Some examples of the latter are endogenous hormones, plant growth status, nutrient composition, and flowering regulatory genes. Many gymnosperms have a long juvenile period. Previous studies attempted to shorten this period using traditional asexual propagation methods, but significant results have not been achieved. In recent years, molecular biology is used to study the flowering regulatory gene to obtain transgenic plants with early flowering trait. Thus, the production of gymnosperms is hastened, and economic efficiency is improved. Studies have shown that the flowering genes of plants act synergistically to form a complex network. In this paper, we reviewed the recent development in the study of the regulation of the flowering genes of gymnosperms, that is, from the floral meristem-specific gene, floral organ-specific gene, genes that inhibit plant flowering, and microRNA regulation of flowering. We provide a reference for the in-depth study on the genetic improvement of the flowering gene.

References

Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant Cell 9(6): 841-857.

Alvarez J, Guli CL, Yu X, Smyth DR (1992). Terminal flower: a gene affecting inflorescence development in Arabidopsis thaliana. The Plant Journal 2(1):103-116.

Angenent GC, Colombo L (1996). Molecular control of ovule development. Trends in Plant Science 1(7):228-232.

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(11):2730-2741.

Banfield MJ, Brady RL (2000). The structure of Antirrhinum centroradialis protein (CEN) suggests a role as a kinase regulator. Journal of Molecular Biology 297(5):1159-1170.

Bartel DP (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281-297.

Becker A, Saedler H, Theissen G (2003). Distinct MADS-box gene expression patterns in the reproductive cones of the gymnosperm Gnetum gnemon. Development genes and evolution 213(11):567-572.

Blázquez MA, Soowal LN, Lee I, Weigel D (1997). LEAFY expression and flower initiation in Arabidopsis. Development 124(19):3835-3844.

Bowman JL, Smyth DR, Meyerowitz EM (1991). Genetic interactions among floral homeotic genes of Arabidopsis. Development 112(1):1-20.

Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E (1996). Control of inflorescence architecture in Antirrhinum. Nature 379(6568):791.

Calonje M, Sanchez R, Chen L, Sung ZR (2008). EMBRYONIC FLOWER1 participates in polycomb group-mediated AG gene silencing in Arabidopsis. The Plant Cell 20(2):277-291.

Carlsbecker A, Tandre K, Johanson U, Englund M, Engström P (2004). The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies). The Plant Journal 40(4):546-557.

Chen H, Yang Z, Xu H, Wu D, Luo Q, Bai T (2015). Molecular cloning and expression analysis of PmLFY and PmNLY genes in Pinus massoniana. Molecular Plant Breeding 13(11):2491-2499.

Chen L, Cheng JC, Castle L, Sung ZR (1997). EMF genes regulate Arabidopsis inflorescence development. The Plant Cell 9(11):2011-2024.

Chen M, Penfield S (2018). Feedback regulation of COOLAIR expression controls seed dormancy and flowering time. Science 360(6392):1014-1017.

Cheng SY, Cheng JH, Xu F, Ye JB, Wang XH (2016). Molecular cloning and expression analysis of a putative E class MADS-box gene, GbSEP, from Ginkgo biloba. Journal of Animal and Plant Sciences 26:253-260.

Chi X, Yang Q, Chen X, Wang J, Pan L, Chen M, Yang Z, He Y, Liang X, Yu S (2011). Identification and characterization of microRNAs from peanut (Arachis hypogaea L.) by high-throughput sequencing. PLoS One 6(11):e27530.

Cho LH, Yoon J, An G (2016). The control of flowering time by environmental factors. Plant Journal for Cell & Molecular Biology 90(4):708.

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

Coen ES, Romero J, Doyle S, Elliott R, Murphy G, Carpenter R (1990). Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63(6):1311-1322.

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. The Plant Cell 7(11):1859-1868.

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

Dornelas MC, Rodriguez APM (2005). A FLORICAULA/LEAFY gene homolog is preferentially expressed in developing female cones of the tropical pine Pinus caribaea var. caribaea. Genetics and Molecular Biology 28(2):299-307.

Dou J, Wang L, Yan J, Fu M, Zhang X, Xu F (2017). Molecular cloning and expression analysis of a AGAMOUS-like 66 gene (GbAGL66) in Ginkgo biloba. Biotechnology 16(3):100-107.

Eckardt NA (2005). A time to grow, a time to flower. The Plant Cell 17(10):2615-2617.

Falkowski PG, Dubinsky Z (1981). Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289(5794):172.

Frohlich MW, Parker DS (2000). The mostly male theory of flower evolutionary origins: from genes to fossils. Systematic Botany 25(2):155-170.

Glazinska P, Zienkiewicz A, Wojciechowski W, Kopcewicz J (2009). The putative miR172 target gene InAPETALA2-like is involved in the photoperiodic flower induction of Ipomoea nil. Journal of Plant Physiology 166(16):1801-1813.

Guo CL, Chen LG, He XH, Dai Z, Yuan HY (2005). Expressions of LEAFY homologous genes in different organs and stages of Ginkgo biloba. Hereditas (Beijing) 27(2):241.

Himi S, Sano R, Nishiyama T, Tanahashi T, Kato M, Ueda K, Hasebe M (2001). Evolution of MADS-box gene induction by FLO/LFY genes. Journal of Molecular Evolution 53(4-5):387-393.

Jack T (2004). Molecular and genetic mechanisms of floral control. The Plant Cell 16(Suppl 1):S1-S17.

Jager M, Hassanin A, Manuel M, Guyader HL, Deutsch J (2003). MADS-box genes in Ginkgo biloba and the evolution of the AGAMOUS family. Molecular Biology and Evolution 20(5):842-854.

Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007). The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. The Plant Cell 19(9):2736-2748.

Karlgren A, Gyllenstrand N, Källman T, Sundström JF, Moore D, Lascoux M, Lagercrantz U (2011). Evolution of the PEBP Gene Family in Plants: Functional Diversification in Seed Plant Evolution. Plant Physiology 156(4):1967-1977.

Katahata SI, Futamura N, Igasaki T, Shinohara K (2014). Functional analysis of soc1-like and agl6-like mads-box genes of the gymnosperm Cryptomeria japonica. Tree Genetics & Genomes 10(2):317-327.

Kelly AJ, Bonnlander MB, Meeks-Wagner DR (1995). NFL, the tobacco homolog of FLORICAULA and LEAFY, is transcriptionally expressed in both vegetative and floral meristems. The Plant Cell 7(2):225-234.

Khodorova NV, Michèle BC (2013). The role of temperature in the growth and flowering of geophytes. Plants 2(4):699-711.

Kotoda N, Iwanami H, Takahashi S, Abe K (2006). Antisense expression of MdTFL1, a TFL1-like gene, reduces the juvenile phase in apple. Journal of the American Society for Horticultural Science 131(1):74-81.

Kyozuka J, Konishi S, Nemoto K, Izawa T, Shimamoto K (1998). Down-regulation of RFL, the FLO/LFY homolog of rice, accompanied with panicle branch initiation. Proceedings of the National Academy of Sciences USA 95(5):1979-1982.

Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes and Development 14(18):2366-2376.

Levy YY, Dean C (1998). The transition to flowering. The Plant Cell 10(12):1973-1989.

Li K, Yang J, Liu J, Du X, Wei C, Su W, He G, Zhang Q, Hong F, Qian X (2006). Cloning, characterization and tissue-specific expression of a cDNA encoding a novel EMBRYONIC FLOWER 2 gene (OsEMF2) in Oryza sativa. DNA Sequence 17(1):74-78.

Liljegren SJ, Gustafson-Brown C, Pinyopich A, Ditta GS, Yanofsky MF (1999). Interactions among APETALA1, LEAFY, and TERMINAL FLOWER 1 specify meristem fate. The Plant Cell 11(6):1007-1018.

Liu MS, Chen LFO, Lin CH, Lai YM, Huang JY, Sung ZR (2012). Molecular and functional characterization of broccoli Embryonic flower 2 genes. Plant and Cell Physiology 53(7):1217-1231.

Mallory AC, Dugas DV, Bartel DP, Bartel B (2004). MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Current Biology 14(12):1035-1046.

Mellerowicz EJ, Horgan K, Walden A, Coker A, Walter C (1998). PRFLL–a Pinus radiata homologue of FLORICAULA and LEAFY is expressed in buds containing vegetative shoot and undifferentiated male cone primordia. Planta 206(4):619-629.

Michaels SD, Amasino RM (2001). Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. The Plant Cell 13(4):935-941.

Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005). Integration of flowering signals in winter-annual Arabidopsis. Plant Physiology 137(1):149-156.

Millar AA, Gubler F (2005). The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. The Plant Cell 17(3):705-721.

Moon YH, Chen L, Pan RL, Chang HS, Zhu T, Maffeo DM, Sung ZR (2003). EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. The Plant Cell 15(3):681-693.

Mouradov A, Glassick T, Hamdorf B, Murphy L, Fowler B, Marla S, Teasdale RD (1998). NEEDLY, a Pinus radiata ortholog of FLORICAULA/LEAFY genes, expressed in both reproductive and vegetative meristems. Proceedings of the National Academy of Sciences USA 95(11):6537-6542.

Mouradov A, Hamdorf B, Teasdale RD, Kim JT, Winter KU, Theissen G (1999). A DEF/GLO?like MADS?box gene from a gymnosperm: Pinus radiata contains an ortholog of angiosperm B class floral homeotic genes. Developmental Genetics 25(3):245-252.

Nag A, Jack T (2010). Sculpting the flower; the role of microRNAs in flower development. In: Current Topics in Developmental Biology 91:349-378.

Nakagawa M, Shimamoto K, Kyozuka J (2002). Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. The Plant Journal 29(6):743-750.

Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998). A genetic framework for floral patterning. Nature 395(6702):561.

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(6783):200.

Peña L, Martín-Trillo M, Juárez J, Pina JA, Navarro L, Martínez-Zapater JM (2001). Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nature Biotechnology 19(3):263.

Pillitteri LJ, Lovatt CJ, Walling LL (2004). Isolation and characterization of a TERMINAL FLOWER homolog and its correlation with juvenility in citrus. Plant Physiology 135(3):1540-1551.

Quinn CR, Iriyama R, Fernando DD (2015). Computational predictions and expression patterns of conserved microRNAs in loblolly pine (Pinus taeda). Tree Genetics & Genomes 11(1):806.

Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002). MicroRNAs in plants. Genes & Development 16(13):1616-1626.

Rounsley SD, Ditta GS, Yanofsky MF (1995). Diverse roles for MADS box genes in Arabidopsis development. The Plant Cell 7(8):1259-1269.

Rutledge R, Regan S, Nicolas O, Fobert P, Côté C, Bosnich W, … Stewart D (1998). Characterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis. The Plant Journal 15(5):625-634.

Schultz EA, Haughn GW (1991). LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. The Plant Cell 3(8):771-781.

Serrano-Mislata A, Goslin K, Zheng B, Rae L, Wellmer F, Graciet E, Madueño F (2017). Regulatory interplay between LEAFY, APETALA1/CAULIFLOWER and TERMINAL FLOWER 1: New insights into an old relationship. Plant Signaling and Behavior 12(10):e1370164.

Shannon S, Meeks-Wagner DR (1991). A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. The Plant Cell 3(9):877-892.

Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000). The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proceedings of the National Academy of Sciences USA 97(7):3753-3758.

Shindo S, Ito M, Ueda K, Kato M, Hasebe M (1999). Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evolution and Development 1(3):180-190.

Shindo S, Sakakibara K, Sano R, Ueda K, Hasebe M (2001). Characterization of a FLORICAULA/LEAFY homologue of Gnetum parvifolium and its implications for the evolution of reproductive organs in seed plants. International Journal of Plant Sciences 162(6):1199-1209.

Singh B, Kaur P, Singh RD, Ahuja PS (2008). Biology and chemistry of Ginkgo biloba. Fitoterapia 79(6):401-418.

Sommer H, Beltran JP, Huijser P, Pape H, Lönnig WE, Saedler H, Schwarz?Sommer Z (1990). Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. The EMBO Journal 9(3):605-613.

Spanudakis E, Jackson S (2014). The role of microRNAs in the control of flowering time. Journal of Experimental Botany 65(2):365-380.

Sun R, Guo T, Cobb J, Wang Q, Zhang B (2015). Role of microRNAs during flower and storage root development in sweet potato. Plant Molecular Biology Reporter 33(6):1731-1739.

Sundström J, Carlsbecker A, Svensson ME, Svenson M, Johanson U, Theissen G, Engström P (1999). MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B?class floral homeotic genes in angiosperms. Developmental Genetics 25(3):253-266.

Sundström J, Engström P (2002). Conifer reproductive development involves B-type MADS-box genes with distinct and different activities in male organ primordia. The Plant Journal 31(2):161-169.

Sung ZR, Belachew A, Shunong B, Bertrand-Garcia R (1992). EMF, an Arabidopsis gene required for vegetative shoot development. Science 258(5088):1645-1647.

Sung ZR, Chen LJ, Moon YH, Yoshida Y (2003). Molecular Mechanism of Shoot determinancy and flowering in Arabidopsis. HortScience 38(7):1325-1327.

Tandre K, Albert VA, Sundås A, Engström P (1995). Conifer homologues to genes that control floral development in angiosperms. Plant Molecular Biology 27(1):69-78.

Theissen G (2001). Development of floral organ identity: stories from the MADS house. Current Opinion in Plant Biology 4(1):75-85.

Theissen G, Saedler H (2001). Plant biology: floral quartets. Nature 409(6819):469.

Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig WE, Schwarz-Sommer Z (1992). GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. The EMBO Journal 11(13):4693-4704.

Van der Linden CG, Vosman B, Smulders MJM (2002). Cloning and characterization of four apple MADS box genes isolated from vegetative tissue. Journal of Experimental Botany 53(371):1025-1036.

Vázquez-Lobo A, Carlsbecker A, Vergara?Silva F, Alvarez-Buylla ER, Piñero D, Engström P (2007). Characterization of the expression patterns of LEAFY/FLORICAULA and NEEDLY orthologs in female and male cones of the conifer genera Picea, Podocarpus, and Taxus: implications for current evo-devo hypotheses for gymnosperms. Evolution and Development 9(5):446-459.

Wang L, Yan J, Meng X, Ye J, Zhang W, Xu F (2017). Cloning and expression analysis of Constans-like 16 (GbCOL16) gene from Ginkgo biloba. Biotechnology 16(3):92-99.

Wang L, Zhao J, Luo K, Cui J, He Q, Xia X, Lu Z, Li W, Jin B (2016). Deep sequencing discovery and profiling of conserved and novel miRNAs in the ovule of Ginkgo biloba. Trees 30(5):1557-1567.

Wang T, Pan H, Wang J, Yang W, Cheng T, Zhang Q (2014). Identification and profiling of novel and conserved microRNAs during the flower opening process in Prunus mume via deep sequencing. Molecular Genetics and Genomics 289(2):169-183.

Wang X, Cheng J, XU F, Li X, Zhang W, Liao Y, Cheng SY, Li X (2015). Molecular cloning and expression analysis of a MADS-Box gene (GbMADS2) from Ginkgo biloba. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 43(1):19-24.

Wang ZJ, Huang JQ, Huang YJ, Li Z, Zheng BS (2012). Discovery and profiling of novel and conserved microRNAs during flower development in Carya cathayensis via deep sequencing. Planta 236(2):613-621.

Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1993). LEAFY controls floral meristem identity in Arabidopsis. Cell 69(5):843-859.

Weigel D, Nilsson O (1995). A developmental switch sufficient for flower initiation in diverse plants. Nature 377(6549):495.

William DA, Su Y, Smith MR, Lu M, Baldwin DA, Wagner D (2004). Genomic identification of direct target genes of LEAFY. Proceedings of the National Academy of Sciences USA 101(6):1775-1780.

Winter KU, Becker A, Münster T, Kim JT, Saedler H, Theissen G (1999). MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proceedings of the National Academy of Sciences USA 96(13):7342-7347.

Wu G (2013). Plant microRNAs and development. Journal of Genetics and Genomics 40(5):217-230.

Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009). The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750-759.

Wu G, Poethig RS (2006). Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539-3547.

Xia R, Xu J, Arikit S, Meyers BC (2015). Extensive families of miRNAs and PHAS loci in Norway spruce demonstrate the origins of complex phasiRNA networks in seed plants. Molecular Biology and Evolution 32(11):2905-2918.

Yakovlev IA, Fossdal CG, Johnsen Ø (2010). Micrornas, the epigenetic memory and climatic adaptation in Norway spruce. New Phytologist 187(4):1154-1169.

Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano HY (2006). Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa. The Plant Cell 18(1):15-28.

Yan J, Mao D, Liu X, Wang L, Xu F, Wang G, Zhang W, Liao Y (2017). Isolation and functional characterization of a circadian-regulated CONSTANS homolog (GbCO) from Ginkgo biloba. Plant Cell Reports 36(9):1387-1399.

Yang CH, Chen LJ, Sung ZR (1995). Genetic regulation of shoot development in Arabidopsis: role of the EMF genes. Developmental Biology 169(2):421-435.

Yang F, Xu F, Wang X, Liao Y, Chen Q, Meng X (2016). Characterization and functional analysis of a mads-box transcription factor gene (GbMADS9) from Ginkgo biloba. Scientia Horticulturae 212:104-114.

Yang L, Conway SR, Poethig RS (2011). Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156. Development 138(2):245-249.

Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990). The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346(6279):35.

Zhang J, Chen L, Hu X, He X (2002). GinNdly gene cloned from the male gametophyte of Ginkgo biloba. Chinese Journal of Cell Biology 24(3):189-191.

Zhang J, Chen L, Hu X, He X (2002). LEAFY homologous gene cloned in maidenhair tree (Ginkgo biloba L.). Scientia Silvae Sinicae 38(4):167-170.

Zhang X, Wang LL, Yan JP, Fu MY, Dou JS, Xu F (2017). Characterization and expression analysis of an AP2 gene from Ginkgo biloba. Biotechnology 16(3):108-115.

Zhou CM, Zhang TQ, Wang X, Yu S, Lian H, Tang H, Feng ZY, Zozomova-Lihová J, Wang JW (2013). Molecular basis of age-dependent vernalization in cardamine flexuosa. Science 340(6136):1097-1100.

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2018-11-23

How to Cite

MAO, D., YE, J., & XU, F. (2018). Advances of the Flowering Genes of Gymnosperms. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 47(1), 1–9. https://doi.org/10.15835/nbha47111343

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DOI: 10.15835/nbha47111343

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