Systemic transport of trans-zeatin and its precursor have differing roles in Arabidopsis shoots

Abstract

Organ-to-organ signal transmission is essential for higher organisms to ensure coordinated biological reactions during metabolism and morphogenesis. Similar to organs in animals, plant organs communicate by various signalling molecules. Among them, cytokinins, a class of phytohormones, play a key role as root-to-shoot long-distance signals, regulating various growth and developmental processes in shoots. Previous studies have proposed that trans-zeatin-riboside, a type of cytokinin precursor, is a major long-distance signalling form in xylem vessels and its action depends on metabolic conversion via the LONELY GUY enzyme in proximity to the site of action. Here we report an additional long-distance signalling form of cytokinin: trans-zeatin, an active form. Grafting between various cytokinin biosynthetic and transportation mutants revealed that root-to-shoot translocation of trans-zeatin, a minor component of xylem cytokinin, controls leaf size but not meristem activity-related traits, whereas that of trans-zeatin riboside is sufficient for regulating both traits. Considering the ratio of trans-zeatin to trans-zeatin-riboside in xylem and their delivery rate change in response to environmental conditions, this dual long-distance cytokinin signalling system allows plants to fine-tune the manner of shoot growth to adapt to fluctuating environments.

Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways

“…Following its nitrate-induced synthesis in the root, cytokinin acts as a long-distance (systemic) signal, conveying information about the root’s nitrogen status that influences shoot metabolism and growth [12,27,28,29,30]. Cytokinin translocation via xylem in this systemic nitrogen response system is mediated by the cytokinin transporter ABCG14, and recent transcriptomic analysis indicates that its target could be the glutamate/glutamine metabolism machinery in the shoot [20,31]. Recent findings also show that long-distance transport of the cytokinin precursor t ZR (which has low activity) can account for nitrate availability-mediated adjustments of shoot apical meristem size and organogenesis rates through modulating the expression of WUSCHEL [32].…”

Cytokinin signaling: from the ER or from the PM? That is the question!

“…80%), but also tZ in a lower proportion ( c . 15%), which have both been shown to be active in the shoot (Hirose et al ., ; Kuroha et al ., ; Osugi et al ., ). In principle, we may distinguish two different cytokinin signaling pathways for these two metabolites as outlined in the following.…”

“…The activity of the other root‐derived cytokinin, tZR, depends strictly on LOG enzymes (Osugi et al ., ) implying that their biological activity requires the metabolic conversion of cytokinins in the cytoplasm and, therefore, their uptake in the cell. For tZR, another family of transporters exists named equilibrative nucleoside transporter (ENT) (Wormit et al ., ; Hirose et al ., ).…”

Connecting the pieces: uncovering the molecular basis for long‐distance communication through plant grafting

“…a,e). Additional support for a model involving cytokinins as mobile root‐to‐shoot signals comes from previous work showing that cytokinins synthesized in the root are transported through the xylem into the shoot, and serve a necessary function in regulating shoot growth (Osugi et al ., ).…”

“…Low‐N conditions induce the expression of C‐ TERMINALLY ENCODED PEPTIDE ( CEP ) peptides in roots (a), which were shown to travel into the shoot where they bind CEP receptors (c; highlighted in blue) and trigger the expression of CEP ‐ DOWNSTREAM ( CEPD ) response peptides (highlighted in pink) that move back down into the root to induce NRT 2.1 expression in a nitrate‐dependent manner (d) (Tabata et al ., ; Ohkubo et al ., ). High‐nitrate conditions in roots activate the production of trans ‐Zeatin cytokinin precursors (highlighted in purple), which were shown, through genetic grafting experiments (e), to move through the xylem into shoots where they participate in the regulation of shoot apical meristem (SAM) size (Osugi et al ., ; Landrein et al ., ). Note that (b–e) illustrate key reciprocal grafting experiments that were used to demonstrate the movement of long‐distance N signals, but are not meant to illustrate all grafting experiments used in the discoveries described.…”