The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions

Abstract

Cytokinins (CKs) are well-established as important phytohormonal regulators of plant growth and development. An increasing number of studies have also revealed the function of these hormones in plant responses to biotic and abiotic stresses. While the function of certain CK classes, including trans-zeatin and isopentenyladenine-type CKs, have been studied in detail, the role of cis-zeatin-type CKs (cZs) in plant development and in mediating environmental interactions is less well defined. Here we provide a comprehensive summary of the current knowledge about abundance, metabolism and activities of cZs in plants. We outline the history of their analysis and the metabolic routes comprising cZ biosynthesis and degradation. Further we provide an overview of changes in the pools of cZs during plant development and environmental interactions. We summarize studies that investigate the role of cZs in regulating plant development and defence responses to pathogen and herbivore attack and highlight their potential role as 'novel' stress-response markers. Since the functional roles of cZs remain largely based on correlative data and genetic manipulations of their biosynthesis, inactivation and degradation are few, we suggest experimental approaches using transgenic plants altered in cZ levels to further uncover their roles in plant growth and environmental interactions and their potential for crop improvement.

Keywords: Abiotic stress; c-io6A37-tRNA; cis-zeatin; herbivory; pathogen; plant growth; prenylated tRNA..

Figure 1. Overview of cis-zeatin metabolism

tRNA-isopentenyltransferases (tRNA-IPTs) catalyze the prenylation of adenine (A) 37 on specific (UNN-)tRNAs leading to the formation of isopentenyl adenine (IP)-containing tRNA. In A. thaliana, the isopentenyl group is derived from the mevalonate (MVA) pathway in the cytosol; but predicted localization of enzymes in other plants suggest the use of isoprene moieties derived from the methylerythritol phosphate (MEP) pathway (broken arrow). The MEP pathway also contributes to IP and trans-zeatin (tZ) biosynthesis. Once isoprenylated tRNA is synthesized, it can be further modified and the CKs can be released by unknown enzymes (“?” in a black box; e.g. tRNA degrading enzymes). Hydroxylation of the prenyl side chain is suggested to occur on the IP-containing tRNA (i⁶A37-tRNA), leading to the formation of cZ-containing tRNA (c-io⁶A37-tRNA). Inactivation and catabolism of cZ is mediated by cZ-O-glucosyltransferases (cZOGT), cZ-N-glucosyltransferases (cZNGT), and cytokinin oxidase/dehydrogenase (CKX). Glucosylated forms of cZ-type CKs: cZOG (cZ-O-glucoside), cZROG (cZ-riboside-O-glucoside) and cZ7G/cZ9G (cZ-N9/N7-glucosides). Multiple arrows indicate multiple biochemical steps; dotted-lines show unexplored metabolic flow. DMAPP (dimethylallyl-diphosphate), IPR (IP-riboside), cZR (cZ-riboside), A (adenine).

Figure 2. cis-zeatins as potential regulators of plant development and stress responses.

cis-zeatin (cZ) and its riboside (cZR) are reported to accumulate in particular under various conditions characterized by limited growth, during particular developmental stages, but also in response to abiotic and biotic stresses. cZ/cZR were shown to be involved in the regulation of the plant development and to be able to modulate plant defense responses. Based on their distribution patterns, they were additionally proposed to sustain a minimum cytokinin (CK) activity under growth-limiting conditions, to prevent the redirection of resources e.g., from stress adaptation processes to plant growth and for a means by which phytophagous organisms could manipulate the plant’s physiology and morphology for their bbenefit. However, an experimental confirmation of this hypothesis is still missing.