The yin-yang of hormones: cytokinin and auxin interactions in plant development

Abstract

The phytohormones auxin and cytokinin interact to regulate many plant growth and developmental processes. Elements involved in the biosynthesis, inactivation, transport, perception, and signaling of these hormones have been elucidated, revealing the variety of mechanisms by which signal output from these pathways can be regulated. Recent studies shed light on how these hormones interact with each other to promote and maintain plant growth and development. In this review, we focus on the interaction of auxin and cytokinin in several developmental contexts, including its role in regulating apical meristems, the patterning of the root, the development of the gynoecium and female gametophyte, and organogenesis and phyllotaxy in the shoot.

Figure 1.

Key Elements of Auxin and Cytokinin Pathways. Elements of the auxin and cytokinin pathways involved in biosynthesis, degradation, transport, and signaling are shown. Points of activating (+) or suppressing (−) crosstalk for the respective pathways are indicated by orange circles (auxin) or green circles (cytokinin). See text for additional details.

Figure 2.

Cell Patterning in the Globular Stage Embryo. The top images depict the cell types in early embryos with the colors corresponding to the indicated cell type. The upper image to the left shows a cross section through the embryo, and the four vascular initial cells represent a template similar to that used previously (De Rybel et al., 2014). The upper image to the right shows the asymmetric cell division of the hypophysis to generate the upper lens-shaped cell and the larger basal cell. This was shown to be controlled by both auxin and cytokinin (Müller and Sheen, 2008). The asterisks show the WUS-expressing domain in the embryo. The lower two images depict the relative cytokinin and auxin concentrations shaded in the indicated colors (Müller and Sheen, 2008; De Rybel et al., 2014). Note that in the cross section of the embryo, cytokinin activity is not depicted as this has not as yet been determined.

Figure 3.

Cell Patterning in the Growing Root. The central panels depict the cell types in various root tissues, with the cell types depicted in the indicated colors. A close-up of the root tip stem cell niche is boxed in green. The root cross section (boxed in red) shows the bisymmetric cellular pattern. The top panel boxed in blue depicts the some of the stages of lateral root organogenesis with E representing an emerged root. In the image of a stage III LRP, the anticlinal faces are marked in red and periclinal faces are marked in blue. The three panels on the right depict the relative levels of auxin or cytokinin signaling, depicted by the indicated colors, as measured by various reporters (based on results of Blilou et al., 2005b; Bishopp et al., 2011b; Della Rovere et al., 2013; Zürcher et al., 2013; Tian et al., 2014). See text for additional details. The lateral root image (top panel) is reproduced from Bishopp and Bennett (2014) (Figure 2).

Figure 4.

Regulatory Networks Controlling Vascular Development. Models of the regulatory networks incorporated within two mathematical models of vascular development. Solid lines show activation or repression of targets. One key difference between these two models is the way in which cytokinin modulates PIN activity. In the model of vascular patterning by Muraro et al. (2014), PIN7 transcription is promoted by cytokinin response. In the model of vascular tissue formation by De Rybel et al. (2014), cytokinin inhibits the localization of PIN on the membrane independently of cytokinin response. Furthermore, in this model, there is an additional regulation on PIN polarity whereby auxin in neighboring cells polarizes auxin toward the membrane. In both models, the PINs transport auxin out of the cell and therefore reduce auxin concentration within the cell (dashed lines) and auxin inhibits cytokinin response (either through AHP6 or other as yet unidentified components). The regulation of cytokinin synthesis by auxin (via ARF5, TMO5, LHW, and LOG4) is a linear pathway, and as such De Rybel et al. didn’t model the components individually. However, the complete pathway is shown alongside in blue, so that the reader can see how these components are included within the regulatory network.

Figure 5.

Patterning of the Shoot Apical Meristem. (A) Organization of the SAM showing locations of the OC, CZ, PZ, and rib zone (RZ). A transverse cross section is shown along with a surface view to illustrate phyllotaxy with the primordia labeled P1 through P5. (B) Auxin and cytokinin activity at the SAM. Maxima of auxin (purple) and cytokinin (blue) activity based on DR5:VENUS and TCS:GFP reporter analysis, respectively (Murray et al., 2012; Zürcher et al., 2013; Besnard et al., 2014). The cytokinin maximum is found at the OC, whereas auxin maxima are found at locations of primordia formation. (C) A model of the circuitry by which auxin and cytokinin regulate WUS expression at the OC. The transcriptional regulator WUS promotes the expression of the signaling peptide CLV3, which interacts with the receptor kinase CLV1 in the CZ to negatively regulate WUS expression. The transcription factor HEC promotes stem cell proliferation in the CZ.