Hormonal networks involved in apical hook development in darkness and their response to light

Abstract

In darkness, the dicot seedlings produce an apical hook as result of differential cell division and extension at opposite sides of the hypocotyl. This hook protects the apical meristem from mechanical damage during seedling emergence from the soil. In darkness, gibberellins act via the DELLA-PIF (PHYTOCHROME INTERACTING FACTORs) pathway, and ethylene acts via the EIN3/EIL1 (ETHYLENE INSENSITIVE 3/EIN3 like 1)-HLS1 (HOOKLESS 1) pathway to control the asymmetric accumulation of auxin required for apical hook formation and maintenance. These core pathways form a network with multiple points of connection. Light perception by phytochromes and cryptochromes reduces the activity of PIFs and (COP1) CONSTITUTIVE PHOTOMORPHOGENIC 1-both required for hook formation in darkness-, lowers the levels of gibberellins, and triggers hook opening as a component of the switch between heterotrophic and photoautotrophic development. Apical hook opening is thus a suitable model to study the convergence of endogenous and exogenous signals on the control of cell division and cell growth.

Keywords: Arabidopsis; COP1; PIFs; apical hook; auxin; ethylene; gibberellins; photoreceptors.

Figure 1

Apical hook development in dark grown seedlings requires the repressors of photomorphogenesis COP1 and PIFs. Representative photographs of the apical section of the hypocotyls of WT Col, cop1-6 and pifq mutants during the three phases of hook development. Photographs were taken 24 h after germination for the formation phase, 48 h after germination for the maintenance phase and 84 h after germination for the opening phase.

Figure 2

Primary action of auxin (inhibition of cell expansion at the inner side), gibberellins (promotion of cell division and expansion at the outer side) and ethylene (enhanced cell division at the top) during apical hook development. There are interactions not represented here, such as the effects of gibberellins and ethylene on the auxin signaling gradient (see Figure 3). Auxin inhibition of cell growth at the inner side of the hook might be mediated by an enhanced ethylene signaling as auxin levels concentrations above a threshold might enhanced ethylene production and signaling contributing to cell growth inhibition (Abel et al., ; Raz and Ecker, ; Vandenbussche et al., 2010). Arrows: Positive regulation; T-bars: Negative regulation.

Figure 3

Hormone signaling network involved in the inhibition of growth at the inner side of the apical hook by auxin. Established points of action of light during hook opening are indicated. The scheme includes only the components for which specific experimental evidence for a role in apical hook development is available (therefore, for instance, while GID1 should work between Gibberellins and DELLA, this receptor is not included). Lines indicate direct or indirect connections between components. Arrows: Positive regulation; T-bars: Negative regulation. Dotted lines: The expression of TAR2 is promoted by ethylene and the abundance of gibberellins is promoted by ethylene in an EIN2-dependent manner, but whether these responses depend on EIN3 is not demonstrated.

Figure 4

Simplified model of light perception and signaling during de-etiolation. In darkness (left) the photoreceptors are inactive. PIF transcription factors promote skotomorphogenesis. HY5 and other transcription factors that promote photomorphogenesis are ubiquitinated by CUL4-DDB1^COP1-SPA1 E3 ligase complex and degraded in the 26S proteasome. High levels of gibberellins induce degradation of DELLA. Light (right) activates the photoreceptors. In the nucleus, phytochromes (that migrate from the cytoplasm in their active form) and cryptochromes interact with COP1, reducing its activity and allowing the abundance of HY5 to increase. In the nucleus, phytochromes also reduce the activity of PIFs. Gibberellin levels are reduced, DELLA accumulate and bind PIFs further reducing their activity. GA, gibberellins. Arrows: Positive regulation; T-bars: Negative regulation.