The diverse roles of cytokinins in regulating leaf development

Abstract

Leaves provide energy for plants, and consequently for animals, through photosynthesis. Despite their important functions, plant leaf developmental processes and their underlying mechanisms have not been well characterized. Here, we provide a holistic description of leaf developmental processes that is centered on cytokinins and their signaling functions. Cytokinins maintain the growth potential (pluripotency) of shoot apical meristems, which provide stem cells for the generation of leaf primordia during the initial stage of leaf formation; cytokinins and auxins, as well as their interaction, determine the phyllotaxis pattern. The activities of cytokinins in various regions of the leaf, especially at the margins, collectively determine the final leaf morphology (e.g., simple or compound). The area of a leaf is generally determined by the number and size of the cells in the leaf. Cytokinins promote cell division and increase cell expansion during the proliferation and expansion stages of leaf cell development, respectively. During leaf senescence, cytokinins reduce sugar accumulation, increase chlorophyll synthesis, and prolong the leaf photosynthetic period. We also briefly describe the roles of other hormones, including auxin and ethylene, during the whole leaf developmental process. In this study, we review the regulatory roles of cytokinins in various leaf developmental stages, with a focus on cytokinin metabolism and signal transduction processes, in order to shed light on the molecular mechanisms underlying leaf development.

Fig. 1. Schematic model of cytokinin (CK) biosynthesis, metabolism, degradation, and signal transduction.

The names of the genes in up panels are shown in ovals, and in low panel are shown in the capsule shapes (see the text for further details). DMAPP: dimethylallyl pyrophosphate; iPRMP: isopentenyladenosine-5-monophosphate; tZRMP, trans-zeatin riboside 5′-monophosphate; cZRMP, cis-zeatin riboside 5′-monophosphate; iP, N6-(Δ2-isopentenyl)adenine; tZ: trans-zeatin; cZ: cis-zeatin; Ade: adenine; IPT, isopentenyltransferases; tRNA-IPT, tRNA-isopentenyltransferase; CYP735A, cytochrome P450 monooxygenase; LOG, LONELY GUY; GT, glycosyltransferase; CKX, cytokinin oxidase/dehydrogenase; ABCG, g subfamily ATP-binding cassette; PUP, purine permeases; ENT, equilibrative nucleoside transporters; HKs, histidine kinase; HPTs, histidine phosphotransfer proteins; ARR, response regulator, CRF, cytokinin response factor. Other abbreviations are as defined in the text

Fig. 2. Schematic diagram of cytokinin (CK) regulation of leaf primordium initiation.

Cells in the shoot apical meristem (SAM) are arranged into the L1, L2, and L3 layers and four distinct zones: the central zone (CZ), peripheral zone (PZ), organizing center (OC), and rib zone (RZ). KNOX is expressed in almost the entire SAM. KNOX positively regulates the synthesis of cytokinins and keeps their levels high. Cytokinins promote the expression of WUS through signal transduction and transcription factors, which maintain a high cell division rate in the OC. ERECTA blocks the effect of cytokinins and promotes the transport of auxin. In areas with higher auxin concentrations, the leaf primordium begins to form. In the early stage of leaf development, KNOX, which is highly expressed in the marginal blastozone, changes the leaf morphology by promoting cytokinin synthesis to form compound leaves. Solid lines indicate direct relationships that have been confirmed; dashed lines represent potential mechanisms. The abbreviations are as defined in the text

Fig. 3. Schematic diagram of cytokinin functions in different stages of leaf development.

The gray dashed lines divide the three stages of leaf development; the bright green area represents cells in the proliferation stage; the green area represents cells in the expansion stage; and the yellow-green area represents the senescence stage. The terms inside the red rounded rectangles are biological functions; the genes in the blue box are involved in chlorophyll synthesis. The solid arrows and blocked bars indicate activation and suppression, respectively