Spatial regulation of plant hormone action

Abstract

Although many plant cell types are capable of producing hormones, and plant hormones can in most cases act in the same cells in which they are produced, they also act as signaling molecules that coordinate physiological responses between different parts of the plant, indicating that their action is subject to spatial regulation. Numerous publications have reported that all levels of plant hormonal pathways, namely metabolism, transport, and perception/signal transduction, can help determine the spatial ranges of hormone action. For example, polar auxin transport or localized auxin biosynthesis contribute to creating a differential hormone accumulation across tissues that is instrumental for specific growth and developmental responses. On the other hand, tissue specificity of cytokinin actions has been proposed to be regulated by mechanisms operating at the signaling stages. Here, we review and discuss current knowledge about the contribution of the three levels mentioned above in providing spatial specificity to plant hormone action. We also explore how new technological developments, such as plant hormone sensors based on FRET (fluorescence resonance energy transfer) or single-cell RNA-seq, can provide an unprecedented level of resolution in defining the spatial domains of plant hormone action and its dynamics.

Keywords: Metabolism; plant hormone sensor; plant hormones; signaling; spatial regulation; transport.

Fig. 1.

Vascular patterning in the embryonic Arabidopsis root. Proto- and metaxylem identities are established by high levels of auxin and low sensitivity to cytokinins. Procambium identity is associated with high cytokinin levels transported from the xylem, and low auxin levels—facilitated by the activity of PIN auxin efflux carriers. Red color indicates auxin, blue indicates cytokinins. PC, procambium; PX, protoxylem; MX, metaxylem.

Fig. 2.

Regulation of SAM functions by local hormone action in Arabidopsis. (A) Maintenance of meristem identity by local production of active cytokinins from precursors transported from roots. (B) The role of gibberellins during the transition to flowering. Gibberellins are maintained outside the SAM during the vegetative phase, but at the onset of flowering there is a transient increase to support a change in the SAM to accommodate new organs, which is due to long-distance transport and local synthesis at the flanks of the meristem. (C) Distinct domains of auxin and cytokinin responses generate a robust phyllotactic pattern for the emergence of new organ primordia in a regular manner. Red color, auxin; blue, cytokinin; purple, AHP6 expression domains. P1, P2, and P3 are previously formed primordia; I1 and I2 are the site where the next primordia will appear and the incipient primordia, respectively.

Fig. 3.

Hormone-mediated spatial regulation of organ growth in response to shade in Arabidopsis. (A) The elongation of the hypocotyl is stimulated by shade through the local action of auxin in the epidermis, which is transported from the cotyledons through the vasculature and translocated thanks to the PIN efflux carriers. (B) Cotyledon growth is arrested under shade conditions by the increase of auxin in the vasculature, which induces the expression of CKX that reduces cytokinin levels and thus cell division. (C) Hyponasty is caused by differential petiole elongation in response to shade, which is due to the combined effect of transported auxin and local gibberellin synthesis. Asymmetric hormone accumulation causes preferential elongation of the abaxial side of the organ by stimulating the activity of the transcription factors PIF and ARF. Red, auxin; blue, cytokinins.

Fig. 4.

Hormone-mediated shaping of the root in response to water availability. Left, a schematic of a primary root under different situations of water availability (more water, blue; less/no water, white). Right: hypothetical models of the cellular and molecular mechanisms underlying these responses. Red color indicates auxin levels; red arrows, auxin transport; blue arrows, water flow through plasmodesmata; gray boxes, closed plasmodesmata due to ABA signaling; S-ARF7, sumoylated ARF7; ep, epidermis; co, cortex; en, endodermis, pe, pericycle; vas, vasculature; endoR, endoreduplication. For an explanation of mechanisms, please read the main text.