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APETALA2 like genes from Picea abies show functional similarities to their Arabidopsis homologues

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Abstract

In angiosperm flower development the identity of the floral organs is determined by the A, B and C factors. Here we present the characterisation of three homologues of the A class gene APETALA2 (AP2) from the conifer Picea abies (Norway spruce), Picea abies APETALA2 LIKE1 (PaAP2L1), PaAP2L2 and PaAP2L3. Similar to AP2 these genes contain sequence motifs complementary to miRNA172 that has been shown to regulate AP2 in Arabidopsis. The genes display distinct expression patterns during plant development; in the female-cone bud PaAP2L1 and PaAP2L3 are expressed in the seed-bearing ovuliferous scale in a pattern complementary to each other, and overlapping with the expression of the C class-related gene DAL2. To study the function of PaAP2L1 and PaAP2L2 the genes were expressed in Arabidopsis. The transgenic PaAP2L2 plants were stunted and flowered later than control plants. Flowers were indeterminate and produced an excess of floral organs most severely in the two inner whorls, associated with an ectopic expression of the meristem-regulating gene WUSCHEL. No homeotic changes in floral-organ identities occurred, but in the ap2-1 mutant background PaAP2L2 was able to promote petal identity, indicating that the spruce AP2 gene has the capacity to substitute for an A class gene in Arabidopsis. In spite of the long evolutionary distance between angiosperms and gymnosperms and the fact that gymnosperms lack structures homologous to sepals and petals our data supports a functional conservation of AP2 genes among the seed plants.

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Abbreviations

miRNA:

microRNA

RACE:

Rapid amplification of cDNA ends

SEM:

Scanning electron microscopy

RT–PCR:

Reverse transcriptase polymerase chain reaction

TBR:

Tree-bisection-reconnection

SAM:

Shoot apical meristem

References

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730-2741

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658-1653

    Article  PubMed  CAS  Google Scholar 

  • Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619

    Article  PubMed  CAS  Google Scholar 

  • Carlsbecker A, Sundstrom J, Tandre K, Englund M, Kvarnheden A, Johanson U, Engstrom P (2003) The DAL10 gene from Norway spruce (Picea abies) belongs to a potentially gymnosperm-specific subclass of MADS-box genes and is specifically active in seed cones and pollen cones. Evol Dev 5(6):551–561

    Article  PubMed  CAS  Google Scholar 

  • 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). Plant J 40:546–557

    Article  PubMed  CAS  Google Scholar 

  • Carroll SB (2000) Endless forms: the evolution of gene regulation and morphological diversity. Cell 101:577–580

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    Article  PubMed  CAS  Google Scholar 

  • Cheung WY, Hubert N, Landry BS (1993) A simple and rapid DNA microextraction method for plant, animal, and insect suitable for RAPD and other PCR analyses. PCR Methods Appl 3:69–70

    PubMed  CAS  Google Scholar 

  • Chuck G, Meeley RB, Hake S (1998) The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. Genes Dev 12:1145–1154

    PubMed  CAS  Google Scholar 

  • Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–2067

    CAS  Google Scholar 

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

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914

    Article  PubMed  CAS  Google Scholar 

  • Florin R (1951) Evolution in cordaites and conifers. Acta Horti Bergiani 15:285–388

    Google Scholar 

  • Florin R (1954) The female reproductive organs of conifers and taxads. Biol Rev 29:367–389

    Article  Google Scholar 

  • Friedman WE, Floyd SK (2001) Perspective: the origin of flowering plants and their reproductive biology-a tale of two phylogenies. Evolution Int J Org Evolution 55:217–231

    PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Jackson D (1991) Molecular plant pathology. In situ hybridisations in plants. Oxford University Press, Oxford, pp 163–174

    Google Scholar 

  • 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 5:842–854

    Article  Google Scholar 

  • Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225

    Article  PubMed  CAS  Google Scholar 

  • Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. PNAS 102:3117–3122

    Article  PubMed  CAS  Google Scholar 

  • Keck EM, McSteen P, Carpenter R, Coen E (2003) Separation of genetic functions controlling organ identity in flowers. EMBO J 22:1058–1066

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Soltis PS, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23:107–120

    Article  PubMed  CAS  Google Scholar 

  • Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet: 383–396

  • Kramer EM, Jaramillo MA, Di Stilio VS (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 2:1011–1023

    Article  Google Scholar 

  • Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 9:688–698

    Article  Google Scholar 

  • Krizek BA, Prost V, Macias A (2000) AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. Plant Cell 8:1357–1366

    Article  Google Scholar 

  • Lauter N, Kampani A, Carlson S, Goebel M, Moose SP (2005) microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. PNAS 102:9412–9417

    Article  PubMed  CAS  Google Scholar 

  • Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96

    PubMed  CAS  Google Scholar 

  • Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165(2):821–833

    PubMed  CAS  Google Scholar 

  • Maes T, Van Montagu M, Gerats T (1999) The inflorescence architecture of Petunia hybrida is modified by the Arabidopsis thaliana Ap2 gene. Dev Genet 25:199–208

    Article  PubMed  CAS  Google Scholar 

  • Mayer KFX, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815

    Article  PubMed  CAS  Google Scholar 

  • Moose SP, Sisco PH (1996) Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev 10:3018–3027

    PubMed  CAS  Google Scholar 

  • 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. Dev Genet 25(3):245–252

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rutledge R, Regan S, Nicolas O, Fobert P, Cote C, Bosnich W, Kauffeldt C, Sunohara G, Seguin A, Stewart D (1998) Characterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis. Plant J 15:625–634

    Article  PubMed  CAS  Google Scholar 

  • Savard L, Li P, Strauss SH, Chase MW, Michaud M, Bousquet J (1994) Chloroplast and nuclear gene sequences indicate late Pennsylvanian time for the last common ancestor of extant seed plants. PNAS 91:5163–5167

    Article  PubMed  CAS  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527

    Article  PubMed  CAS  Google Scholar 

  • Shigyo M, Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes. Dev Genes Evol 214:105–114

    Article  PubMed  CAS  Google Scholar 

  • Shigyo M, Hasebe M, Ito M (2006) Molecular evolution of the AP2 subfamily. Gene 2:256–265

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sundström J, Carlsbecker A, Svensson ME, Johansson 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. Dev Genet 25:253–266

    Article  PubMed  Google Scholar 

  • Swofford D (2001) PAUP* 4.0b10: phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, Mass In

  • Tandre K, Albert VA, Sundås A, Engström P (1995) Conifer homologues to genes that control floral development in angiosperms. Plant Mol Biol 27:69–78

    Article  PubMed  CAS  Google Scholar 

  • Tandre K, Svenson M, Svensson ME, Engström P (1998) Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J 15:615–623

    Article  PubMed  CAS  Google Scholar 

  • Vahala T, Oxelman B, von Arnold S (2001) Two APETALA2-like genes of Picea abies are differentially expressed during development. J Exp Bot 52:1111–1115

    Article  PubMed  CAS  Google Scholar 

  • Winter KU, Becker A, Munster T, Kim JT, Saedler H, Theissen G (1999) MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. PNAS 96:7342–7347

    Article  PubMed  CAS  Google Scholar 

  • Winter KU, Saedler H, Theissen G (2002) On the origin of class B floral homeotic genes: functional substitution and dominant inhibition in Arabidopsis by expression of an orthologue from the gymnosperm Gnetum. Plant J 31:457–475

    Article  PubMed  CAS  Google Scholar 

  • Würschum T, Gross-Hardt R, Laux T (2006) APETALA2 Regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 18:295–307

    Article  PubMed  Google Scholar 

  • 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 346:35–39

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant miRNA genes. Plant J 46:243–259

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Tan HT, Pwee KH, Kumar PP (2004) Conservation of class C function of floral organ development during 300 million years of evolution from gymnosperms to angiosperms. Plant J 4:566–577

    Article  Google Scholar 

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Acknowledgments

We thank Laleh Paran, Agneta Ottosson, Gunilla Swärdh, Gun-Britt Berglund and Marie Englund for technical help with transformation, culture and analysis of the plant material, Gary Wife for assistance with the SEM analysis and Dr. Stefan Gunnarsson for technical assistance with the light microscope. We thank Kim et al. (2006; Department of Botany University of Florida, Gainsville, USA) for the nucleotide matris over AP2 genes and acknowledge NASC for ap2-1 seeds. The work was financially supported by the Swedish Council for Forestry and Agricultural Research, Carl Trygger Foundation for Scientific Research and The Royal Swedish Academy of Agriculture and Forestry.

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Authors and Affiliations

  1. Department of Physiological Botany, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, 752 36, Uppsala, Sweden

    Lars Nilsson, Annelie Carlsbecker & Annika Sundås-Larsson

  2. Department of Plant Biology and Forest Genetics, SLU, P.O. Box 7080, 750 07, Uppsala, Sweden

    Tiina Vahala

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  1. Lars Nilsson
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  2. Annelie Carlsbecker
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  3. Annika Sundås-Larsson
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  4. Tiina Vahala
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Correspondence to Annika Sundås-Larsson.

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Nilsson, L., Carlsbecker, A., Sundås-Larsson, A. et al. APETALA2 like genes from Picea abies show functional similarities to their Arabidopsis homologues. Planta 225, 589–602 (2007). https://doi.org/10.1007/s00425-006-0374-1

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