Isopentenyltransferase-1 (IPT1) knockout in Physcomitrella together with phylogenetic analyses of IPTs provide insights into evolution of plant cytokinin biosynthesis
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
24692654
PubMed Central
PMC4036517
DOI
10.1093/jxb/eru142
PII: eru142
Knihovny.cz E-resources
- Keywords
- Bryophyte, cytokinin, isopentenyladenosine, isopentenyltransferases, moss, tRNA.,
- MeSH
- Alkyl and Aryl Transferases genetics metabolism MeSH
- Biological Evolution * MeSH
- Chloroplasts enzymology genetics MeSH
- Cytokinins biosynthesis MeSH
- Phylogeny * MeSH
- Gene Knockout Techniques MeSH
- Bryopsida classification enzymology genetics MeSH
- Molecular Sequence Data MeSH
- RNA, Transfer genetics metabolism MeSH
- Plant Proteins genetics metabolism MeSH
- Plants classification enzymology genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- adenylate isopentenyltransferase MeSH Browser
- Alkyl and Aryl Transferases MeSH
- Cytokinins MeSH
- RNA, Transfer MeSH
- Plant Proteins MeSH
The moss Physcomitrella patens is part of an early divergent clade of land plants utilizing the plant hormone cytokinin for growth control. The rate-limiting step of cytokinin biosynthesis is mediated by isopentenyltransferases (IPTs), found in land plants either as adenylate-IPTs or as tRNA-IPTs. Although a dominant part of cytokinins in flowering plants are synthesized by adenylate-IPTs, the Physcomitrella genome only encodes homologues of tRNA-IPTs. This study therefore looked into the question of whether cytokinins in moss derive from tRNA exclusively. Targeted gene knockout of ipt1 (d|ipt1) along with localization studies revealed that the chloroplast-bound IPT1 was almost exclusively responsible for the A37 prenylation of tRNA in Physcomitrella. Ultra-performance liquid chromatography-tandem mass spectrometry (UPLC-MS/MS)-based cytokinin profiling demonstrated that the total amount of all free cytokinins in tissue was almost unaffected. However, the knockout plants showed increased levels of the N (6) -isopentenyladenine (iP)- and trans-zeatin (tZ)-type cytokinins, considered to provide active forms, while cis-zeatin (cZ)-type cytokinins were reduced. The data provide evidence for an additional and unexpected tRNA-independent cytokinin biosynthetic pathway in moss. Comprehensive phylogenetic analysis indicates a diversification of tRNA-IPT-like genes in bryophytes probably related to additional functions.
See more in PubMed
Akiyoshi DE, Regier DA, Jen G, Gordon MP. 1985. Cloning and nucleotide sequence of the tzs gene from Agrobacterium tumefaciens strain T37. Nucleic Acids Research 13, 2773–2788 PubMed PMC
Barry GF, Rogers SG, Fraley RT, Brand L. 1984. Identification of a cloned cytokinin biosynthetic gene. Proceedings of the National Academy of Sciences, USA 81, 4776–4780 PubMed PMC
Bartels S, Gonzalez Besteiro MA, Lang D, Ulm R. 2010. Emerging functions for plant MAP kinase phosphatases. Trends in Plant Science 15, 322–329 PubMed
Beaty JS, Powell GK, Lica L, Regier DA, Macdonald EMS, Hommes NG, Morris RO. 1986. Tzs, a nopaline Ti plasmid gene from Agrobacterium tumefaciens associated with trans-zeatin biosynthesis. Molecular and General Genetics 203, 274–280
Boyd EF, Almagro-Moreno S, Parent MA. 2009. Genomic islands are dynamic, ancient integrative elements in bacterial evolution. Trends in Microbiology 17, 47–53 PubMed
Brugiere N, Humbert S, Rizzo N, Bohn J, Habben JE. 2008. A member of the maize isopentenyl transferase gene family, Zea mays isopentenyl transferase 2 (ZmIPT2), encodes a cytokinin biosynthetic enzyme expressed during kernel development. Plant Molecular Biology 67, 215–229 PubMed
Caillet J, Droogmans L. 1988. Molecular cloning of the Escherichia coli miaA gene involved in the formation of Δ2-isopentenyl adenosine in tRNA. Journal of Bacteriology 170, 4147–4152 PubMed PMC
Cho SH, von Schwartzenberg K, Quatrano R. 2009. The role of abscisic acid in stress tolerance. Annual Plant Reviews Volume 36: the moss Physcomitrella patens. Oxford: Wiley-Blackwell, 282–297
Clamp M, Cuff J, Searle SM, Barton GJ. 2004. The Jalview Java alignment editor. Bioinformatics 20, 426–427 PubMed
Cove D, Ashton N. 1984. The hormonal regulation of gametophytic development in bryophytes. In: Dyer AF, Duckett JG, eds. The experimental biology of bryophytes. London: Academic Press, 177–201
Decker EL, Frank W, Sarnighausen E, Reski R. 2006. Moss systems biology en route: phytohormones in Physcomitrella development. Plant Biology 8, 397–405 PubMed
Dihanich ME, Najarian D, Clark R, Gillman EC, Martin NC, Hopper AK. 1987. Isolation and characterization of MOD5, a gene required for isopentenylation of cytoplasmic and mitochondrial tRNAs of Saccharomyces cerevisiae . Molecular and Cellular Biology 7, 177–184 PubMed PMC
Eichinger L, Pachebat JA, Glockner G, et al. 2005. The genome of the social amoeba Dictyostelium discoideum . Nature 435, 43–57 PubMed PMC
Faiss M, Zalubilova J, Strnad M, Schmülling T. 1997. Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signaling in whole tobacco plants. The Plant Journal 12, 401–415 PubMed
Frebort I, Kowalska M, Hluska T, Frebortova J, Galuszka P. 2011. Evolution of cytokinin biosynthesis and degradation. Journal of Experimental Botany 62, 2431–2452 PubMed
Galichet A, Hoyerova K, Kaminek M, Gruissem W. 2008. Farnesylation directs AtIPT3 subcellular localization and modulates cytokinin biosynthesis in Arabidopsis. Plant Physiology 146, 1155–1164 PubMed PMC
Gillman EC, Slusher LB, Martin NC, Hopper AK. 1991. MOD5 translation initiation sites determine N6-isopentenyladenosine modification of mitochondrial and cytoplasmic tRNA. Molecular and Cellular Biology 11, 2382–2390 PubMed PMC
Golovko A, Hjalm G, Sitbon F, Nicander B. 2000. Cloning of a human tRNA isopentenyl transferase. Gene 258, 85–93 PubMed
Golovko A, Sitbon F, Tillberg E, Nicander B. 2002. Identification of a tRNA isopentenyltransferase gene from Arabidopsis thaliana . Plant Molecular Biology 49, 161–169 PubMed
Goodstein DM, Shu S, Howson R, et al. 2012. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178–D1186 PubMed PMC
Howe K, Bateman A, Durbin R. 2002. QuickTree: building huge Neighbour-Joining trees of protein sequences. Bioinformatics 18, 1546–1547 PubMed
Hunter S, Jones P, Mitchell A, et al. 2012. InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Research 40, D306–D312 PubMed PMC
Kakimoto T. 2001. Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant and Cell Physiology 42, 677–685 PubMed
Kakimoto T. 2003. Biosynthesis of cytokinins. Journal of Plant Research 116, 233–239 PubMed
Kamada-Nobusada T, Sakakibara H. 2009. Molecular basis for cytokinin biosynthesis. Phytochemistry 70, 444–449 PubMed
Kamisugi Y, Schlink K, Rensing SA, Schween G, von Stackelberg M, Cuming AC, Reski R, Cove DJ. 2006. The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration. Nucleic Acids Research 34, 6205–6214 PubMed PMC
Kasahara H, Takei K, Ueda N, Hishiyama S, Yamaya T, Kamiya Y, Yamaguchi S, Sakakibara H. 2004. Distinct isoprenoid origins of cis- and trans-zeatin biosyntheses in Arabidopsis. Journal of Biological Chemistry 279, 14049–14054 PubMed
Knight CD, Cove D, Boyd PJ, Ashton N. 1988. The isolation of biochemical and developmental mutants in Physcomitrella patens . In: Glime JM, ed. Methods in Bryology: Proceedings of the Bryology Methods Workshop, Mainz. Hattori Botanical Laboratory, Nichinan, Japan, 47–58
Konevega AL, Soboleva NG, Makhno VI, Peshekhonov AV, Katunin VI. 2006. The effect of modification of tRNA nucleotide-37 on the tRNA interaction with the P- and A-site of the 70S ribosome Escherichia coli . Molecular Biology 40, 669–683 PubMed
Kopecna M, Blaschke H, Kopecny D, Vigouroux A, Koncitikova R, Novak O, Kotland O, Strnad M, Morera S, von Schwartzenberg K. 2013. Structure and function of nucleoside hydrolases from Physcomitrella and maize catalyzing hydrolysis of purine, pyrimidine and cytokinin ribosides. Plant Physiology 163, 1568–1583 PubMed PMC
Lang D, Eisinger J, Reski R, Rensing SA. 2005. Representation and high-quality annotation of the Physcomitrella patens transcriptome demonstrates a high proportion of proteins involved in metabolism in mosses. Plant Biology 7, 238–250 PubMed
Lang D, Weiche B, Timmerhaus G, Richardt S, Riano-Pachon DM, Correa LG, Reski R, Mueller-Roeber B, Rensing SA. 2010. Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biology and Evolution 2, 488–503 PubMed PMC
Lang D, Zimmer AD, Rensing SA, Reski R. 2008. Exploring plant biodiversity: the Physcomitrella genome and beyond. Trends in Plant Science 13, 542–549 PubMed
Lichtenstein C, Klee H, Montoya A, Garfinkel D, Fuller S, Flores C, Nester E, Gordon M. 1984. Nucleotide sequence and transcript mapping of the tmr gene of the pTiA6NC octopine Ti-plasmid: a bacterial gene involved in plant tumorigenesis. Journal of Molecular and Applied Genetics 2, 354–362 PubMed
Maass H, Klämbt D. 1981. On the biogenesis of cytokinins in roots of Phaseolus vulgaris . Planta 151, 353–358 PubMed
Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T. 2006. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proceedings of the National Academy of Sciences, USA 103, 16598–16603 PubMed PMC
Mok DWS, Mok MC. 2001. Cytokinin metabolism and action. Annual Review of Plant Physiology and Plant Molecular Biology 52, 89–118 PubMed
Murai N. 1994. Cytokinin biosynthesis in tRNA and cytokinin incorporation into plant RNA. In: Mok DWS, Mok MC, eds Cytokinins: chemistry, activity, and function. Boca Raton, FL: CRC Press, 87–99
Newell CA, Natesan SK, Sullivan JA, Jouhet J, Kavanagh TA, Gray JC. 2012. Exclusion of plastid nucleoids and ribosomes from stromules in tobacco and Arabidopsis. The Plant Journal 69, 399–410 PubMed
Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. Journal of Molecular Biology 302, 205–217 PubMed
Novák O, Hauserova E, Amakorova P, Doležal K, Strnad M. 2008. Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69, 2214–2224 PubMed
Novák O, Tarkowski P, Tarkowská D, Doležal K, Lenobel R, Strnad M. 2003. Quantitative analysis of cytokinins in plants by liquid chromatography–single-quadrupole mass spectrometry. Analytica Chimica Acta 480, 207–218
Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K. 2009. The evolution of nuclear auxin signalling. BMC Evolutionary Biology 9, 126. PubMed PMC
Patil G, Nicander B. 2013. Identification of two additional members of the tRNA isopentenyltransferase family in Physcomitrella patens . Plant Molecular Biology 82, 417–426 PubMed
Pils B, Heyl A. 2009. Unraveling the evolution of cytokinin signaling. Plant Physiology 151, 782–791 PubMed PMC
Prigge MJ, Bezanilla M. 2010. Evolutionary crossroads in developmental biology. Physcomitrella patens . Development 137, 3535–3543 PubMed
Rensing SA, Lang D, Zimmer AD, et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64–69 PubMed
Reski R, Abel WO. 1985. Induction of budding on chloronemata and caulonemata of the moss, Physcomitrella patens, using isopentenyladenine. Planta 165, 354–358 PubMed
Reutter K, Atzorn R, Hadeler B, Schmulling T, Reski R. 1998. Expression of the bacterial ipt gene in Physcomitrella rescues mutations in budding and in plastid division. Planta 206, 196–203
Richter H, Lieberei R, Strnad M, Novak O, Gruz J, Rensing SA, von Schwartzenberg K. 2012. Polyphenol oxidases in Physcomitrella: functional PPO1 knockout modulates cytokinin-dependent development in the moss Physcomitrella patens . Journal of Experimental Botany 63, 5121–5135 PubMed PMC
Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 PubMed
Sakakibara H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annual Review of Plant Biology 57, 431–449 PubMed
Sakamoto T, Sakakibara H, Kojima M, Yamamoto Y, Nagasaki H, Inukai Y, Sato Y, Matsuoka M. 2006. Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiology 142, 54–62 PubMed PMC
Schaefer D, Zryd JP, Knight CD, Cove DJ. 1991. Stable transformation of the moss Physcomitrella patens . Molecular and General Genetics 226, 418–424 PubMed
Schaefer DG, Delacote F, Charlot F, Vrielynck N, Guyon-Debast A, Le Guin S, Neuhaus JM, Doutriaux MP, Nogue F. 2010. RAD51 loss of function abolishes gene targeting and de-represses illegitimate integration in the moss Physcomitrella patens . DNA Repair 9, 526–533 PubMed
Schaefer DG, Zryd JP. 1997. Efficient gene targeting in the moss Physcomitrella patens . The Plant Journal 11, 1195–1206 PubMed
Schulz P, Reski R, Maldiney R, Laloue M, von Schwartzenberg K. 2000. Kinetics of cytokinin production and bud formation in Physcomitrella: analysis of wild type, a developmental mutant and two of its ipt transgenics. Journal of Plant Physiology 156, 768–774
Schulz PA, Hofmann AH, Russo VEA, Hartmann E, Laloue M, von Schwartzenberg K. 2001. Cytokinin overproducing ove mutants of Physcomitrella patens show increased riboside to base conversion. Plant Physiology 126, 1224–1231 PubMed PMC
Schween G, Gorr G, Hohe A, Reski R. 2003. Unique tissue-specific cell cycle in Physcomitrella . Plant Biology 5, 50–58
Schween G, Schulte J, Reski R, Hohe A. 2005. Effect of ploidy level on growth, differentiation, and morphology in Physcomitrella patens . Bryologist 108, 27–35
Sonnhammer ELL, Hollich V. 2005. Scoredist: a simple and robust protein sequence distance estimator. BMC Bioinformatics 6, 108. PubMed PMC
Stirk WA, Balint P, Sipos G, Dobrev PI, Novak O, Dolezal K, Strnad M, van Staden J, Ordog V. 2011. Endogenous cytokinins in synchronized Chlorella cultures in relation to light and the cell cycle. European Journal of Phycology 46, 73–73 PubMed
Strnad M. 1997. The aromatic cytokinins. Physiologia Plantarum 101, 674–688
Takei K, Sakakibara H, Sugiyama T. 2001. Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana . Journal of Biological Chemistry 276, 26405–26410 PubMed
Taya Y, Tanaka Y, Nishimura S. 1978. 5′-Amp is a direct precursor of cytokinin in Dictyostelium discoideum . Nature 271, 545–547 PubMed
Thelander M, Olsson T, Ronne H. 2005. Effect of the energy supply on filamentous growth and development in Physcomitrella patens . Journal of Experimental Botany 56, 653–662 PubMed
Vandenbussche F, Fierro AC, Wiedemann G, Reski R, Van Der Straeten D. 2007. Evolutionary conservation of plant gibberellin signalling pathway components. BMC Plant Biology 7, 65. PubMed PMC
von Schwartzenberg K. 2009. Hormonal regulation of development by auxin and cytokinin in moss. Annual Plant Reviews Volume 36: the moss Physcomitrella patens. Oxford: Wiley-Blackwell, 246–281
von Schwartzenberg K, Nunez MF, Blaschke H, Dobrev PI, Novak O, Motyka V, Strnad M. 2007. Cytokinins in the bryophyte Physcomitrella patens: analyses of activity, distribution, and cytokinin oxidase/dehydrogenase overexpression reveal the role of extracellular cytokinins. Plant Physiology 145, 786–800 PubMed PMC
Wang TL, Beutelmann P, Cove DJ. 1981. Cytokinin biosynthesis in mutants of the moss Physcomitrella patens . Plant Physiology 68, 739–744 PubMed PMC
Yamada S, Ohkubo S, Miyashita H, Setoguchi H. 2012. Genetic diversity of symbiotic cyanobacteria in Cycas revoluta (Cycadaceae). FEMS Microbiology Ecology 81, 696–706 PubMed
Yevdakova NA, Motyka V, Malbeck J, Travnickova A, Novak O, Strnad M, von Schwartzenberg K. 2008. Evidence for importance of tRNA-dependent cytokinin biosynthetic pathway in the moss Physcomitrella patens . Journal of Plant Growth Regulation 27, 271–281
Yevdakova NA, von Schwartzenberg K. 2007. Characterisation of a prokaryote-type tRNA-isopentenyltransferase gene from the moss Physcomitrella patens . Planta 226, 683–695 PubMed
Zimmer AD, Lang D, Buchta K, Rombauts S, Nishiyama T, Hasebe M, Van de Peer Y, Rensing SA, Reski R. 2013. Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions. BMC Genomics 14, 498. PubMed PMC
