Cytokinins

Abstract

Cytokinins are phytohormones involved in the regulation of many physiological and developmental processes in plants. Generally, they stimulate cell division and help to control root and shoot meristem activity, but they further exert control on processes related to leaf senescence, nutrient uptake and pathogen resistance. In flowering plants, the cytokinin system has evolved to a high degree of complexity and the key elements of cytokinin biosynthesis, activation, inactivation, degradation and perception are well understood on a molecular level. Cytokinin activity is interconnected with many other signalling pathways including those of other hormones. Cytokinin signalling already appears at the evolutionary level of early divergent land plants. There is evidence that in future crop plant properties and productivity improvements could be achieved by making use of the increasing knowledge of the cytokinin regulatory network.

Key Concepts

  • Cytokinins are N6 derivatives of adenine with aromatic or isoprenoid side chains which vary in abundance and biological activity.
  • Cytokinin biosynthesis is mediated by two types of isopentenyl transferases (IPTs), directly via isoprenylation of ATP or indirectly via modification of tRNA and their subsequent breakdown.
  • Homeostasis of cytokinin activity can be achieved by degradation involving cytokinin oxidase/dehydrogenases (CKX), conjugation by glycosyltransferases or by transport.
  • Cytokinin perception is mediated by sensor histidine kinases (CHK) which initiate a multistep phosphorelay to histidine phosphotransfer proteins (HPT) and from there to type‐B response regulators (RRBs). These act as transcription factors and modulate the expression rate of cytokinin responsive genes. Type‐A response regulators (RAA) are strongly upregulated and play a role as negative regulators of cytokinin action.
  • Cytokinin responsive genes were detected by means of microarray and RNAseq‐based methodologies and address areas of stress and defence (drought, pathogens), redox status (oxidative burst), protein degradation and modification, signalling (including light, nutrients and hormonal interactions), cell wall, development (cell proliferation and differentiation) and secondary metabolism (flavonoids, lignin, anthocyanin and alkaloids). Cytokinin homeostasis genes can also be subject of cytokinin action.
  • Cytokinin signalling is interconnected to other signalling pathways on the level of biosynthesis, metabolism and signalling forming complex regulatory networks. Many crosstalk connections, antagonistic and synergistic ones, have been described for auxin, but important interactions exist as well with respect to signalling by other hormones such as gibberellin, ethylene, abscisic acid and strigolactone.
  • The cytokinin system has been described in Arabidopsis and a few other flowering plants in detail. However, there is increasing evidence that cytokinin‐based regulation is already functional on the evolutionary level of bryophytes.
  • Increasing experimental evidence makes it likely that the cytokinin regulatory system can be subject in targeted breeding approaches on crop plants in order to improve productivity‐related plant properties.

Keywords: phytohormone; plant growth regulation; zeatin; isopentenyltransferase; cytokinin oxidase; two‐component system; signalling

Figure 1. N6‐Isopentenyladenine (iP), trans‐zeatin (tZ) and cis‐zeatin (cZ) are natural isoprenoid cytokinins. Benzyladenine (BA) is a natural aromatic cytokinin, while thidiazuron (TDZ) is a synthetic diphenylurea‐type cytokinin.
Figure 2. Simplified scheme of cytokinin biosynthesis and activation in flowering plants. Biosynthesis: A‐IPTs: adenylate‐isopentenyltransferases, tRNA‐IPTs: tRNA isopentenyltransferases (Miyawaki et al., ). Activation: CYP735 cytochrome P450 monooxygenase (Takei et al., ), LOG: cytokinin nucleotide 5′‐monophosphoribohydrolase (Kuroha et al., ). Red: free bases, blue: ribosides (R), green: nucleotides (RTP, RDP and RMP). iP, isopentenyladenine; tZ, trans‐zeatin; cZ, cis‐zeatin.
Figure 3. Cytokinin inactivation exemplarily for trans‐zeatin (tZ). Inactivation can either be achieved by formation of inactive cytokinin glucosides (left) or by irreversible degradation by cytokinin dehydrogenase/oxidase (CKX) (right). tZOG, trans‐zeatin‐O‐glucoside; tZ7G, trans‐zeatin‐7‐glucoside; tZ9G, trans‐zeatin‐9‐glucoside.
Figure 4. (a) Long‐distance transport of cytokinins through the vascular system (adapted from Hirose et al., and Kudo et al., ). (b) Model of cytokinin transport across the plasma membrane mediated by transport proteins (Kudo et al., ; Zhang et al., ).
Figure 5. Simplified scheme of the two‐component cytokinin signalling based on sensor histidine kinases binding cytokinin bases and thereby triggering the multistep phosphorelay, which results in alterations of the expression of many cytokinin‐regulated genes.
Figure 6. Phenotypic convergence caused by cytokinin‐related mutations affecting signalling, degradation or biosynthesis in Arabidopsis. In comparison to wild type grown under the same conditions, each of the mutants shows a severe inhibition of growth in the aerial part. ahk2,3, double knockout mutant for cytokinin receptors (Nishimura et al., ), 35S:CKX1: overexpression of CKX (Werner et al., ), ipt1,3,5,7 quadruple knockout mutant for cytokinin biosynthesis (Miyawaki et al., ). Figure was kindly provided by T. Werner (FU‐Berlin).
Figure 7. Scheme of origin of selected cytokinin‐specific genes during the evolution of photosynthetic organisms. Depicted by gene name is the first confirmed homologue in whole‐genome sequences. Colours represent their conservation during plant evolution. Adapted from Gruhn and Heyl 2013.
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Further Reading

Borghi L, Kang J, Ko D, Lee Y and Martinoia E (2015) The role of ABCG‐type ABC transporters in phytohormone transport. Biochemical Society Transactions 43: 924–930.

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Lindner, Ann‐Cathrin, and von Schwartzenberg, Klaus(Nov 2016) Cytokinins. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020095.pub2]