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Journal of Plant Growth Regulation

, Volume 38, Issue 2, pp 416–430 | Cite as

Identification and Characterization of ATP/ADP Isopentenyltransferases (ATP/ADP PpIPTs) Genes in Peach

  • Min-ji Li
  • Qin-ping Wei
  • Fu-tian PengEmail author
  • Wen Yu
  • Jing-jing Luo
  • Yong-fei Zhao
Article
  • 123 Downloads

Abstract

ATP/ADP isopentenyltransferase (IPTs) genes encode key enzymes involved in cytokinin synthesis. In this study, the functions of ATP/ADP PpIPTs in peach were investigated. According to the genome sequence, we have found and verified that there are four members of this gene family in peach, namely, PpIPT1, PpIPT3, PpIPT5, and PpIPT7. Overexpression of each of these genes in Arabidopsis resulted in increased levels of cytokinins in the transgenic plants, confirming their roles in cytokinin synthesis. Numerous altered phenotypes were observed in the transgenic plants, including vigorous growth and enhanced salt resistance. ATP/ADP PpIPTs were expressed in tissues throughout the plant, but the expression patterns differed between the genes. Only PpIPT3 was upregulated within 2 h after the application of nitrate to N-deprived peach seedlings, and the increase was resistant to pre-treatment of a specific nitrate metabolism inhibitor. Results showed that ATP/ADP PpIPT expression levels decreased significantly in pulp within 2 weeks after flowering and remained low. However, pulp cytokinin levels were quite high during this time. Only PpIPT5 in seed increased significantly within 2 weeks after flowering, which was consistent with cytokinin levels during early fruit development, suggesting that PpIPT5 in seed is the key gene for cytokinin biosynthesis during early fruit development. ATP/ADP PpIPT expression also increased significantly during later fruit development in seed.

Keywords

ATP/ADP PpIPTs Peach (Prunus persicaFruit Tissue-specific expression Plant hormone Nitrate 

Notes

Acknowledgements

This work was supported by China Agriculture Research System; CARS-31-3-03; http://119.253.58.231/.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abe I, Tanaka H, Abe T, Noguchi H (2007) Enzymatic formation of unnatural cytokinin analogs by adenylate isopentenyltransferase from mulberry. Biochem Biophys Res Commun 355:795–800CrossRefGoogle Scholar
  2. Ando S, Asano T, Tsushima S, Kamchi S, Hagio T, Tabei Y (2005) Changes in gene expression of putative isopentenyltransferase during clubroot development in Chinese cabbage (Brassica rapa L.). Physiol Mol Plant Pathol 67:59–67CrossRefGoogle Scholar
  3. Arnau JA, Tadeo FR, Guerri J, Primo-Millo E (1999) Cytokinins in peach: endogenous levels during early fruit development. Plant Physiol Biochem 37(10):741–750CrossRefGoogle Scholar
  4. Arús P, Verde I, Sosinski B, Zhebentyayeva T, Abbott AG (2012) The peach genome. Tree Genet Genomes 8:531–547CrossRefGoogle Scholar
  5. Ashikari M, Sakakibara H, Lin S et al (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745CrossRefGoogle Scholar
  6. Atkins CA, Pigeaire A (1993) Application of cytokinins to flowers to increase pod set in Lupinus angustifolius. Aust J Agr Res 44:1799–1819CrossRefGoogle Scholar
  7. Blackwell JR, Horgan R (1994) Cytokinin biosynthesis by extracts of Zea mays. Phytochemistry 35:339–342CrossRefGoogle Scholar
  8. Bouchard JN, Yamasaki H (2008) Heat stress stimulates nitric oxide production in symbiodinium microadriaticum: a possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol 49(4):641–652CrossRefGoogle Scholar
  9. Castaings L, Marchive C, Meyer C, Krapp A (2011) Nitrogen signalling in Arabidopsis: how to obtain insights into a complex signalling network. J Exp Bot 62:1391–1397CrossRefGoogle Scholar
  10. Crane JC (1964) Growth substances in fruit setting and development. Annu Rev Plant Physiol 15:303–326CrossRefGoogle Scholar
  11. Dobrev PI, Kaminek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950:21–29CrossRefGoogle Scholar
  12. Dragovoz IV, Kots SY, Chekhun TI, Yavorskaya VK, Volkogon NV (2002) Complex growth regulator increases alfalfa seed production. Russ J Plant Physiol 49:823–827CrossRefGoogle Scholar
  13. Dyer DJ, Carlson DR, Cotterman CD, Sikorski JA, Ditson SL (1987) Soybean pod set enhancement with synthetic cytokinin analogs. Plant Physiol 84:240–243CrossRefGoogle Scholar
  14. Emery RJN, Ma Q, Atkins CA (2000) The forms and sources of cytokinins in developing white lupine seeds and fruits. Plant Physiol 123:1593–1604CrossRefGoogle Scholar
  15. Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452CrossRefGoogle Scholar
  16. Golovko A, Sitbon F, Tillberg E, Nicander B (2002) Identification of a tRNA isopentenyl-transferase gene from arabidopsis thaliana. Plant Mol Biol 49(2):161–169CrossRefGoogle Scholar
  17. Haberer G, Kieber JJ (2002) Cytokinins. New insights into a classic phytohormone. Plant Physiol 128(2):354–362CrossRefGoogle Scholar
  18. Hernandez Miñana FM, Primo Millo E, Primo Millo J (1989) Endogenous cytokinins in developing fruits of seeded and seedless Citrus cultivars. J Exp Bot 40(10):1127–1134CrossRefGoogle Scholar
  19. Immanen J, Nieminen K, Silva HD, Rojas FR, Meisel LA, Silva H, Albert VA, Hvidsten TR, Helariutta Y (2013) Characterization of cytokinin signaling and homeostasis gene families in two hardwood tree species: Populus trichocarpa and Prunus persica. BMC Genom 14:885CrossRefGoogle Scholar
  20. Jameson PE, Song J (2016) Cytokinin: a key driver of seed yield. J Exp Bot 67(3):593CrossRefGoogle Scholar
  21. Kakimoto T (2001) Identification of plant Cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685CrossRefGoogle Scholar
  22. 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. J Biol Chem 279:14049–14054CrossRefGoogle Scholar
  23. Le DT, Nishiyama R, Watanabe Y et al (2012) Identification and expression analysis of cytokinin metabolic genes in soybean under normal and drought conditions in relation to cytokinin levels. PLoS ONE 7(8):e42411CrossRefGoogle Scholar
  24. Liu Y, Wang SH et al (2011) Auxin inhibits the outgrowth of tiller buds in rice (Oryza sativa L.) by downregulating OsIPT expression and cytokinin biosynthesis in nodes. Aust J Crop Sci 5:169–174Google Scholar
  25. Liu YD, Yin ZJ, Yu JW et al (2012) Improved salt tolerance and delayed leaf senescence in transgenic cotton expressing the Agrobacterium IPT gene. Biol Plant 56:237–246CrossRefGoogle Scholar
  26. McCab MS, Garratt LC, Schepers F et al (2001) Effects of P-SAG12-IPT gene expression on development and senescence in transgenic lettuce. Plant Physiol 127:505–516CrossRefGoogle Scholar
  27. Merewitz EB, Gianfagna T, Huang et al (2011) Photosynthesis, water use, and root viability under water stress as affected by expression of SAG12-ipt controlling cytokinin synthesis in Agrostis stolonifera. J Exp Bot 62:383–395CrossRefGoogle Scholar
  28. Miyawaki K, Kitano MM, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37:128–138CrossRefGoogle Scholar
  29. Miyawaki K, Tarkowski P, Kitano MM, Kato T et al (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103:44CrossRefGoogle Scholar
  30. Mochida K, Yoshida T, Sakurai T et al (2010) Genome-wide analysis of two-component systems and prediction of stress-responsive two-component system members in soybean. DNA Res 17(5):303–324CrossRefGoogle Scholar
  31. Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118CrossRefGoogle Scholar
  32. Nagel L, Brewster R, Riedell WE, Reese RN (2001) Cytokinin regulation of flower and pod set in soybeans (Glycine max (L.) Merr.). Ann Bot 88:27–31CrossRefGoogle Scholar
  33. Nitsch JP (1970) Hormonal factors in growth and development. Biochem Fruits Prod 2:427–472Google Scholar
  34. Nobusada TK, Makita N, Kojima M, Sakakibara H (2013) Nitrogen-dependent regulation of de novo cytokinin biosynthesis in rice: the role of glutamine metabolism as an additional signal. Plant Cell Physiol 54:1881–1893CrossRefGoogle Scholar
  35. Pace J, McDermott EE (1952) Methionine sulphoximine and some enzyme systems involving glutamine. Nature 169(4297):415–416CrossRefGoogle Scholar
  36. Powell AF, Paleczny AR, Olechowski H, Emery RJN (2013) Changes in cytokinin form and concentration in developing kernels correspond with variation in yield among field-grown barley cultivars. Plant Physiol Biochem 64:33–40CrossRefGoogle Scholar
  37. Qiu WM, Liu MY, Qiao GR et al (2012) An isopentyl transferase gene driven by the stress-inducible rd29a promoter improves salinity stress tolerance in transgenic tobacco. Plant Mol Biol Rep 30:519–528CrossRefGoogle Scholar
  38. Ren XQ, Xu K, Li H et al (2013) Expression analysis of the adenylate-isopentenyl transferase(a-ipt) genes in apple(malus × domestica borkh.). J China Agric Univ 18(6):120–125Google Scholar
  39. Rivero RM, Kojima M, Gepstein A et al (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636CrossRefGoogle Scholar
  40. Sakakibara H (2003) Nitrate-specific and cytokinin-mediated nitrogen signaling pathways in plants. J Plant Res 116:253–257CrossRefGoogle Scholar
  41. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation[J]. Annu Rev Plant Biol 57:431–449CrossRefGoogle Scholar
  42. Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Plant Sci 11:440–448CrossRefGoogle Scholar
  43. Sakamoto T, Sakakibara H, Kojima M, Yamamoto Y, Naagasaki H, Inukai Y, Sato Y, Matsuoka M (2006) Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol 142:54–62CrossRefGoogle Scholar
  44. Sakano Y, Okada Y, Matsunaga A, Suwama T, Kaneko T, Ito K, Noguchi H, Abe I (2004) Molecular cloning, expression, and characterization of adenylate isopentyltransferase from hop (Humulus lupulus L.). Phytochemistry 65:2439–2446CrossRefGoogle Scholar
  45. Samuelson ME, Larsson CM (1993) Nitrate regulation of zeatin riboside levels in barley roots: effects of inhibitors of N assimilation and comparison with ammonium. Plant Sci 93:77–84CrossRefGoogle Scholar
  46. Schäfer M, Brütting C, Mezacanales ID et al (2015) The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions. J Exp Bot 66(16):4873CrossRefGoogle Scholar
  47. Smigocki AC, Owens LD (1988) Cytokinin gene fused with a strong promoter enhances shoot organogenesis and zeatin levels in transformed plant cells. Proc Natl Acad Sci USA 85:5131–5135CrossRefGoogle Scholar
  48. Stern RA, Shargal A, Flaishman MA (2003a) Thidiazuron increases fruit size of ‘Spadona’and ‘Coscia’ pear (Pyrus communis L.). J Hortic Sci Biotechnol 78:51–55CrossRefGoogle Scholar
  49. Stern RA, Ben-Arie R, Neria O, Flaishman M (2003b) CPPU and BA increase fruit size of ‘Royal Gala’ (Malus domestica) apple in a warm climate. J Hortic Sci Biotechnol 78:297–302CrossRefGoogle Scholar
  50. Takei K, Sakakibara H, Sugiyama T (2001a) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276:26405–26410CrossRefGoogle Scholar
  51. Takei K, Sakakibara H, Taniguchi M, Sugiyama T (2001b) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42:85–93CrossRefGoogle Scholar
  52. Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53:971–977CrossRefGoogle Scholar
  53. Tanaka M, Takei K, Kojima M, Sakakibara H, Mori H (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J 45:1028–1036CrossRefGoogle Scholar
  54. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F et al (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494CrossRefGoogle Scholar
  55. Wang X, Zhao P, Liu X et al (2014) Quantitative profiling method for phytohormones and betaines in algae by liquid chromatography electrospray ionization tandem mass spectrometry. Biomed Chromatogr 28(2):275–280CrossRefGoogle Scholar
  56. Ye CJ, Wu SW, Kong FN, Zhou CJ, Yang QK, Sun Y, Wang B (2006) Identification and characterization of an isopentenyl-transferase (IPT) gene in soybean(Glycine max L.). Plant Sci 170:542–550CrossRefGoogle Scholar
  57. Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16(4):227–233CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Min-ji Li
    • 1
  • Qin-ping Wei
    • 1
  • Fu-tian Peng
    • 2
    Email author
  • Wen Yu
    • 2
  • Jing-jing Luo
    • 2
  • Yong-fei Zhao
    • 2
  1. 1.Beijing Academy of Forestry and Pomology Sciences, Beijing Academy of Agriculture & Forestry Sciences/Key Laboratory of Urban Agriculture (North China)Ministry of AgricultureBeijingPeople’s Republic of China
  2. 2.College of Horticulture Science and Engineering/State Key Laboratory of Crop BiologyShandong Agricultural UniversityTai’anPeople’s Republic of China

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