Cytokinin regulates root meristem activity via modulation of the polar auxin transport

Abstract

Plant development is governed by signaling molecules called phytohormones. Typically, in certain developmental processes more than 1 hormone is implicated and, thus, coordination of their overlapping activities is crucial for correct plant development. However, molecular mechanisms underlying the hormonal crosstalk are only poorly understood. Multiple hormones including cytokinin and auxin have been implicated in the regulation of root development. Here we dissect the roles of cytokinin in modulating growth of the primary root. We show that cytokinin effect on root elongation occurs through ethylene signaling whereas cytokinin effect on the root meristem size involves ethylene-independent modulation of transport-dependent asymmetric auxin distribution. Exogenous or endogenous modification of cytokinin levels and cytokinin signaling lead to specific changes in transcription of several auxin efflux carrier genes from the PIN family having a direct impact on auxin efflux from cultured cells and on auxin distribution in the root apex. We propose a novel model for cytokinin action in regulating root growth: Cytokinin influences cell-to-cell auxin transport by modification of expression of several auxin transport components and thus modulates auxin distribution important for regulation of activity and size of the root meristem.auxin ͉ auxin transport ͉ cytokinin ͉ hormonal crosstalk ͉ root meristem P lant hormones play a crucial role in regulating plant development and the flexible shaping of the plant architecture in response to variable environmental conditions. The final developmental and physiological output of the hormonal signaling in plants is the typical result of combined actions of several hormonal pathways. However, our knowledge of the mechanisms involved in the hormonal crosstalk is still poor.In the regulation of root development, several hormonal pathways are involved, with auxin and cytokinin being the principal players. The whole process of root organogenesis, starting with the initiation of the root pole in embryos (1), positioning and formation of stem cell niche (2, 3), maintenance of mitotic activity in proximal meristem (4-6), and rapid elongation and differentiation of cells leaving the root meristem (7) has been demonstrated to be controlled by auxin. In this context, the differential auxin distribution between cells is crucial (3,8,9). The auxin gradients or local auxin maxima can be generated by auxin metabolic reactions, mainly by local auxin biosynthesis (6, 10, 11) and intercellular auxin transport dependent on the coordinated action of influx carriers of the AUX/LAX family (12), PIN efflux carriers (13,14), and members of the multidrugresistant/P-glycoprotein (MDR/PGP) subfamily B of ATPbinding cassette (ABCB) proteins (15, 16). Accordingly, interference with the polar auxin transport disrupts the auxin distribution and results in dramatic patterning defects in the root meristem (2, 3, 9).Besides auxin, cytokinin (CK) is also involved in root organogenesis. Increase in CK levels by exogen...

Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins

“…4a,b). This phenotype is also consistent with perturbation of cytokinin status, as increase in cytokinin levels normally inhibit root growth and reduce the size of root meristems [22][23][24] . Thus, we speculated that disrupting AtABCG14 may impair root meristem activity.…”

Flavonoids and Auxin Transport Inhibitors Rescue Symbiotic Nodulation in the Medicago truncatula Cytokinin Perception Mutant cre1

“…In the cre1 mutant, rhizobia are unable to inhibit acropetal auxin transport and this is associated with a misregulation of some PIN auxin carrier-encoding gene expression and protein accumulation (Plet et al, 2011). The hypothesis that cytokinin acts upstream of auxin transport regulation is supported by studies from Arabidopsis showing that cytokinin regulates PIN expression, accumulation, selective degradation, and subsequently polar auxin transport (Pernisová et al, 2009;Ruzicka et al, 2009;Marhavý et al, 2011Marhavý et al, , 2014. This is thought to regulate auxin accumulation during lateral root formation (Laplaze et al, 2007;Marhavý et al, 2014).…”

Cytokinin signaling regulates pavement cell morphogenesis in Arabidopsis

“…Indeed our results showed that an increasing Figure S5). Therefore, cytokinin regulation of the fundamental cellular process (cell morphogensis) appears to follow the common theme for the coordination of various developmental and morphogenetic processes in different tissues/organs involving a balancing act between cytokinin and auxin, although detailed mechanisms for the auxin-cytokinin balancing act may differ in different processes [1,5,6,[8][9][10][11]42]. How does cytokinin antagonize the action of auxin in PC morphogenesis?…”

“…At the cellular level, cytokinin is known to promote cell division, stem-cell specification, and chloroplast biogenesis [9][10][11][12]. The major cytokinin biosynthetic pathway is mediated by adenosine phosphate-isopentenyltransferase (IPT), which catalyzes the first and rate-limiting step [13,14].…”