Early increased expression of a cyclin-dependant protein kinase (LtCDKA1;1) during inflorescence initiation of the long day grass Lolium temulentum
Greg F. W. Gocal A B C and Rod W. King B D
+ Author Affiliations
- Author Affiliations
A Department of Botany and Zoology, The Australian National University, GPO Box 475, Canberra, ACT 2601, Australia.
B Commonwealth Scientific and Industrial Research Organisation (CSIRO), Division of Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.
C Present address: Cibus US LLC, 6455 Nancy Ridge Drive, San Diego, CA 92121, USA.
D Corresponding author. Email: rwerking@gmail.com
Functional Plant Biology 40(10) 986-995 https://doi.org/10.1071/FP12294
Submitted: 4 October 2012 Accepted: 25 March 2013 Published: 4 June 2013
Abstract
Knowing where and when different genes express at the shoot apex during the transition to flowering will help in understanding this developmental switch. The CDKA family of serine/threonine kinase genes are appropriate candidates for such developmental switching as they are involved in the regulation of the G1/S and G2/M boundaries of the cell cycle (see review by Dudits et al. 2007) and so could regulate increases of cell division associated with flowering. Furthermore, in rice stems the gibberellin (GA) class of plant growth regulators rapidly upregulate CDKA expression and cell division. Thus, CDKA expression might be linked to the florigenic action of GA as a photoperiodically-generated, signal. For the grass Lolium temulentum L., we have isolated an LtCDKA1;1 gene, which is upregulated in shoot apices collected soon after the start of a single florally inductive long day (LD). In contrast to weak expression of LtCDKA1;1 in the vegetative shoot apex, in situ and PCR-based mRNA assays and immunological studies of its protein show very rapid increases in the apical dome at the time that florigenic signals arrive at the apex (<6 h after the end of the LD). By ~54 h LtCDKA1;1 mRNA is localised to the floral target cells, the spikelet primordia. Later both LtCDKA1;1 mRNA and protein are most evident in floret meristems. Only ~10% of cells within the apical dome are dividing at any time but the LD increase in LtCDKA1;1 may reflect an early transient increase in the mitotic index (Jacqmard et al. 1993) as well as a later increase when spikelet primordia form. Increased expression of an AP1-like gene (LtMADS2) follows that of LtCDKA1;1. Overall, LtCDKA1;1 is a useful marker of both early florigenic signalling and of later morphological/developmental aspects of the floral transition.
Additional keywords: CDKA, cell division, flower development, inflorescence initiation, Lolium temulentum, serine/threonine kinase.
References
Bell MH, Halford NG, Ormrod JC, Francis D (1993) Tobacco plants transformed with CDC25, a mitotic inducer gene from fission yeast. Plant Molecular Biology 23, 445–451.| Tobacco plants transformed with CDC25, a mitotic inducer gene from fission yeast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXks12jtw%3D%3D&md5=9144ceb8739bffd18174c880ce3d074fCAS | 8219080PubMed |
Bernier G, Kinet J-M, Sachs RM (1981) Age and flower initiation. In ‘The physiology of flowering.’ p. 106. (CRC Press: Boca Raton, FL, USA)
Besnard-Wibaut C, Cochet T, Noin M (1989) Photoperiod and gibberellic acid – control of the cell cycle in Silene armeria and its effect on flowering. Physiologia Plantarum 77, 352–358.
| Photoperiod and gibberellic acid – control of the cell cycle in Silene armeria and its effect on flowering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXpsFKmsQ%3D%3D&md5=5d67291f9f4b1c5c9c7b7f066eb2a1f3CAS |
Bonhomme F, Kurz B, Meltzer S, Bernier G, Jacqmard A (2000) Cytokinin and gibberellin activate SaMADS A, a gene apparently involved in the floral transition in Sinapis alba. The Plant Journal 24, 103–111.
| Cytokinin and gibberellin activate SaMADS A, a gene apparently involved in the floral transition in Sinapis alba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvVeqsrY%3D&md5=736401d91c065cd6530e7e26f08ffa82CAS | 11029708PubMed |
Chang S, Puryear J, Cairney K (1993) A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11, 113–116.
| A simple and efficient method for isolating RNA from pine trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslKqurs%3D&md5=88dae88320409df314fed5647f08a102CAS |
Chung SK, Parish RW (1995) Studies on the promoter of the Arabidopsis thaliana cdc2a gene. FEBS Letters 362, 215–219.
| Studies on the promoter of the Arabidopsis thaliana cdc2a gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkvVagtbg%3D&md5=c2b8fe535e5d67d2d784ad61d348f432CAS | 7720875PubMed |
Colasanti J, Tyers M, Sundaresan V (1991) Isolation and characterization of cDNA clones encoding a functional p34cdc2 homologue from Zea mays. Proceedings of the National Academy of Sciences of the United States of America 88, 3377–3381.
| Isolation and characterization of cDNA clones encoding a functional p34cdc2 homologue from Zea mays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmt1Gjt74%3D&md5=069bdc5718015c0e50fe57f32d2daf32CAS | 2014258PubMed |
D’Aloia M, Tamseddak K, Bonhomme D, Bonhomme F, Bernier G, Périlleux C (2009) Gene activation cascade triggered by a single photoperiodic cycle inducing flowering in Sinapis alba. The Plant Journal 59, 962–973.
| Gene activation cascade triggered by a single photoperiodic cycle inducing flowering in Sinapis alba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1yrsrnM&md5=799260c9cbda7ce358e879d8e84ce59fCAS | 19473326PubMed |
Dudits D, Cserháti M, Miskolcsi P, Horváth GV (2007) The growing family of plant cyclin-dependent kinases with multiple functions in cellular and developmental regulation. Annual Plant Reviews 32, 1–30.
Evans LT (1964a) Inflorescence initiation in Lolium temulentum L. V. The role of auxins and gibberellins. Australian Journal of Biological Sciences 7, l0–l23.
Evans LT (1964b) Infloresence initiation in Lolium temulentum L. VI. Effects of some inhibitors of nucleic acid, protein, and steroid biosynthesis. Australian Journal of Biological Sciences 7, 24–35.
Evans LT, Blundell C (1996) The acceleration of primordium initiation as a component of floral evocation in Lolium temulentum L. Australian Journal of Plant Physiology 23, 569–576.
| The acceleration of primordium initiation as a component of floral evocation in Lolium temulentum L.Crossref | GoogleScholarGoogle Scholar |
Evans LT, King RW (1985) Lolium temulentum. In ‘CRC handbook of flowering. Vol. III’. (Ed. AH Halevy) pp. 306–323. (CRC Press: Boca Raton, FL, USA)
Evans LT, Rijven AHGC (1967) Inflorescence initiation in Lolium temulentum L. XI. Early increases in the incorporation of 32P and 35S by shoot apices during induction. Australian Journal of Biological Sciences 20, 1033–1042.
Fobert PR, Gaudin V, Lunness P, Coen ES, Doonan JH (1996) Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plants. The Plant Cell 8, 1465–1476.
Francis D, Lyndon RF (1985) The control of the cell cycle in relation to floral induction. In ‘The cell cycle in plants’. (Eds J Bryant, D Francis) pp. 199–215. (Cambridge University Press: Cambridge, UK)
Gocal GFW (1997) Molecular biology of floral evocation in Lolium temulentum. PhD thesis. The Australian National University, Canberra, Australia.
Gocal GFW, Poole AT, Gubler F, Watts RJ, Blundell C, King RW (1999) Long-day up-regulation of a GAMYB gene during Lolium temulentum inflorescence formation. Plant Physiology 119, 1271–1278.
| Long-day up-regulation of a GAMYB gene during Lolium temulentum inflorescence formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFymu7c%3D&md5=71d513cf64834ddfc9de5ab56fe49e99CAS |
Gocal GFW, King RW, Blundell C, Schwartz OM, Andersen CH, Weigel D (2001a) Evolution of floral meristem identity genes: analysis of Lolium genes related to APETALA1 and LEAFY of Arabidopsis. Plant Physiology 125, 1788–1801.
| Evolution of floral meristem identity genes: analysis of Lolium genes related to APETALA1 and LEAFY of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKqtLs%3D&md5=2eb1235ac860ab41abf32a52d3b1b36eCAS |
Gocal GFW, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish RW, Dennis ES, Weigel D, King RW (2001b) GAMYB-like genes and gibberellin signalling in Arabidopsis. Plant Physiology 127, 1682–1693.
| GAMYB-like genes and gibberellin signalling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVWmug%3D%3D&md5=905eb2fd52b6224d36268feb5e83d57cCAS |
Goodall GJ, Filipowicz W (1989) The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell 58, 473–483.
| The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlsVOrsro%3D&md5=9fbd300f01bebacd7a291e11b85761d2CAS | 2758463PubMed |
Goodall GJ, Kiss T, Filipowicz W (1991) Nuclear RNA splicing and small nuclear RNAs and their genes in higher plants. In ‘Oxford surveys of plant molecular and cell biology, 7’. (Ed. BJ Miflin) pp. 255–296. (Oxford University Press: Oxford, UK)
Guo J, Song J, Wang F, Zhang XS (2007) Genome-wide identification and expression analysis of rice cell cycle genes. Plant Molecular Biology 64, 349–360.
| Genome-wide identification and expression analysis of rice cell cycle genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvFarsL0%3D&md5=e86304939bf44cb082a0bad9be3db2eeCAS | 17443292PubMed |
Hashimoto J, Hirabayashi T, Hayano Y, Haya S, Ohashi Y, Suzuka I, Utsugi T, Toh EA, Kikuchi Y (1992) Isolation and characterization of cDNA clones encoding CDC2 homologues from Oryza sativa: a functional homologue and cognate variants. Molecular & General Genetics 233, 10–16.
| Isolation and characterization of cDNA clones encoding CDC2 homologues from Oryza sativa: a functional homologue and cognate variants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkt1ems7w%3D&md5=35858b02097043b08a0c97ba1f585f07CAS |
Hirayama T, Imajuku Y, Anai T, Matsui M, Oka A (1991) Identification of two cell-cycle-controlling CDC2 gene homologs in Arabidopsis thaliana. Gene 105, 159–165.
| Identification of two cell-cycle-controlling CDC2 gene homologs in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xls1Gjt74%3D&md5=8690e453cf8fcf1a1c0cfc90a1af1c6fCAS | 1937013PubMed |
Jacqmard A, Bomans J, Ormrod JC, Bernier G (1993) Early increase in the mitotic index in the shoot apex of Lolium temulentum cv. Ceres during the floral transition. Journal of Experimental Botany 44, 1407–1409.
| Early increase in the mitotic index in the shoot apex of Lolium temulentum cv. Ceres during the floral transition.Crossref | GoogleScholarGoogle Scholar |
John PCL, Sek FJ, Lee MG (1989) A homolog of the cell cycle control protein p34cdc2 participates in the division cycle of Chlamydomonas, and a similar protein is detectable in higher plants and remote taxa. Plant Cell 1, 1185–119.
Joubès J, Chevalier C, Dudits D, Heberle-Bors E, Inze D, Umeda M, Renaudin J (2000) CDK-related protein kinases in plants. Plant Molecular Biology 43, 607–620.
| CDK-related protein kinases in plants.Crossref | GoogleScholarGoogle Scholar | 11089864PubMed |
King RW (2012) Mobile signals in daylength-regulated flowering: gibberellins, FT and sucrose. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 59, 479–490.
| Mobile signals in daylength-regulated flowering: gibberellins, FT and sucrose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1Cru7o%3D&md5=bbb40daa81adead8e4c1d8c77ce676b6CAS |
King RW, Evans LT (2003) Gibberellins and flowering of grasses and cereals: prizing open the lid of the ‘florigen’ black box. Annual Review of Plant Biology 54, 307–328.
| Gibberellins and flowering of grasses and cereals: prizing open the lid of the ‘florigen’ black box.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFSgu7k%3D&md5=dbc3a42a4eb6da9637f5de99fb139362CAS | 14502993PubMed |
King RW, Moritz T, Evans LT, Junttila O, Herlt AJ (2001) Long-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex. Plant Physiology 127, 624–632.
| Long-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslGlu78%3D&md5=eb979b251612bc3be9f95995485627b1CAS | 11598236PubMed |
King RW, Moritz T, Evans LT, Martin J, Andersen CH, Blundell C, Kardailsky I, Chandler PM (2006) Gibberellin biosynthesis and the regulation of flowering in the long day grass, Lolium temulentum L. by gibberellins and the gene FLOWERING LOCUS T. Plant Physiology 141, 498–507.
| Gibberellin biosynthesis and the regulation of flowering in the long day grass, Lolium temulentum L. by gibberellins and the gene FLOWERING LOCUS T.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aktrc%3D&md5=58f1642a6845284b04684d75003f90eeCAS | 16581877PubMed |
Knox RB, Evans LT (1968) Inflorescence initiation in Lolium temulentum L. XII. An autoradiographic study of evocation in the shoot apex. Australian Journal of Biological Sciences 21, 1083–1094.
Lewin B (1990) Driving the cell cycle: M phase kinase, its partners, and substrates. Cell 61, 743–752.
| Driving the cell cycle: M phase kinase, its partners, and substrates.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c3mtlSquw%3D%3D&md5=e566ec98aeb17310c7a48e262756fb43CAS | 2160858PubMed |
MacMillan CP, Blundell CA, King RW (2005) Flowering of the grass Lolium perenne L.: effects of vernalization and long days on gibberellin biosynthesis and signalling. Plant Physiology 138, 1794–1806.
| Flowering of the grass Lolium perenne L.: effects of vernalization and long days on gibberellin biosynthesis and signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvV2ksb8%3D&md5=9d327569ba1e85f6eb7f0935b4eb6200CAS | 15980191PubMed |
McDaniel CN, King RW, Evans LT (1991) Floral determination and in vitro floral differentiation in isolated shoot apices of Lolium temulentum L. Planta 185, 9–16.
| Floral determination and in vitro floral differentiation in isolated shoot apices of Lolium temulentum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFGitLY%3D&md5=3d531235dc0dcaef1634868b4b9659cdCAS |
Miao G-H, Hong Z, Verma DPS (1993) Two functional soybean genes encoding p34CDC2 protein kinases are regulated by different developmental pathways. Proceedings of the National Academy of Sciences of the United States of America 90, 943–947.
| Two functional soybean genes encoding p34CDC2 protein kinases are regulated by different developmental pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltlaktbo%3D&md5=efc95f6918383d295a0f2935e6ff6692CAS | 8430109PubMed |
Nurse P (1990) Universal control mechanism regulating onset of M-phase. Nature 344, 503–508.
| Universal control mechanism regulating onset of M-phase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXitFamtrs%3D&md5=84852a11399981bd53d476d7535b6956CAS | 2138713PubMed |
Nurse P (1994) Ordering S phase and M phase in the cell cycle. Cell 79, 547–550.
| Ordering S phase and M phase in the cell cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit1Glu70%3D&md5=8960d3aa826ee359596f119943495c80CAS | 7954820PubMed |
Nurse P, Bisset Y (1981) Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature 292, 558–560.
| Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjsVyr&md5=206713e6beccd1321234dcaf2e338049CAS | 7254352PubMed |
Ormrod JC, Bernier G (1990) Cell cycle patterns in the shoot apex of Lolium temulentum L. cv Ceres during the transition to flowering following a single long day. Journal of Experimental Botany 41, 211–216.
| Cell cycle patterns in the shoot apex of Lolium temulentum L. cv Ceres during the transition to flowering following a single long day.Crossref | GoogleScholarGoogle Scholar |
Rijven AHGC, Evans LT (1967) Inflorescence initiation in Lolium temulentum L. IX. Some chemical changes in the shoot apex at induction. Australian Journal of Biological Sciences 20, 1–20.
Sauter M (1997) Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2 genes from rice during the cell cycle and in response to gibberellin. The Plant Journal 11, 181–190.
| Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2 genes from rice during the cell cycle and in response to gibberellin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitFCktLg%3D&md5=16bab05bcbb93d098d93773d6c1ac38aCAS | 9076986PubMed |
Shaul O, Van Montagu M, Inzé D (1996) Cell cycle control in Arabidopsis. Annals of Botany 78, 283–288.
| Cell cycle control in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtVSrsr0%3D&md5=58fd8e729ac703b8318270ae0513f109CAS |
Taylor M, Francis D (1989) Cell cycle changes in the shoot apex of Silene coeli-rosa during the second and third days of floral induction. Annals of Botany 64, 625–633.
Turck F, Formara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves centre stage. Annual Review of Plant Biology 59, 573–594.
| Regulation and identity of florigen: FLOWERING LOCUS T moves centre stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsbc%3D&md5=9f1f303572a902ec15e9ca00d67fbc59CAS | 18444908PubMed |
