The interaction between strigolactones and other plant hormones in the regulation of plant development

Abstract

Plant hormones are small molecules derived from various metabolic pathways and are important regulators of plant development. The most recently discovered phytohormone class comprises the carotenoid-derived strigolactones (SLs). For a long time these compounds were only known to be secreted into the rhizosphere where they act as signaling compounds, but now we know they are also active as endogenous plant hormones and they have been in the spotlight ever since. The initial discovery that SLs are involved in the inhibition of axillary bud outgrowth, initiated a multitude of other studies showing that SLs also play a role in defining root architecture, secondary growth, hypocotyl elongation, and seed germination, mostly in interaction with other hormones. Their coordinated action enables the plant to respond in an appropriate manner to environmental factors such as temperature, shading, day length, and nutrient availability. Here, we will review the current knowledge on the crosstalk between SLs and other plant hormones-such as auxin, cytokinin, abscisic acid (ABA), ethylene (ET), and gibberellins (GA)-during different physiological processes. We will furthermore take a bird's eye view of how this hormonal crosstalk enables plants to respond to their ever changing environments.

Keywords: auxin; cytokinin; ethylene; gibberellins; hormone crosstalk; phenotypic plasticity; root and shoot architecture; strigolactone.

Figure 1

Strigolactone and ABA biosynthetic pathways share a common origin at β-carotene. Adapted and modified from Ruyter-Spira et al. (2013).

Figure 2

An overview of auxin, SL, and CK transport within the plant (left) and hormone interactions during the regulation of shoot and root development (right). Auxin, strigolactone (SL), and cytokinin (CK) transport are represented by black, red, and blue dotted line, respectively. For hormone interactions (right), arrows represent promotion, while flat-ended lines indicate inhibition. (A) Auxin, produced in the shoot apical meristem (SAM) and young leaves, is transported basipetally through the stem in the polar auxin transport (PAT) stream toward the root apical meristem (RAM). Here, but probably also throughout the entire vasculature of the plant, it positively regulates SL biosynthesis (Hayward et al., 2009). As shown by GR24 feeding experiments, SLs transported through the xylem from the root to the shoot down-regulate the free auxin level in young leafs in a MAX2-dependent manner hereby controlling their development (Ruyter-Spira et al., 2011). SLs in the vasculature negatively affect PAT capacity (Crawford et al., 2010), as observed for NPA (Ljung et al., 2001), which negatively feeds back on auxin levels at the sites of biosynthesis. This long distance SL-auxin feedback mechanism, affects plant developmental processes as described below. (B) During the regulation of bud outgrowth, SLs reduce the capacity of the PAT stream in the main stem, leading to enhanced competition between buds to release their auxin into the stem (Crawford et al., ; Shinohara et al., 2013). On the other hand, SLs and CK are transported acropetally through the xylem and act directly in the buds to control their outgrowth through the joint regulation of TCP transcription factor BRC1 (Braun et al., ; Dun et al., 2012). (C) SLs have a direct positive effect on secondary growth by activating cell division in the vascular cambium in which they act downstream of auxin. The fact that the max1 mutant still displays some residual cambium activity might point to a SL independent response to auxin. However, this remaining activity could also be due to residual SLs in these mutants (Agusti et al., 2011). (D) Hormone interactions during primary root (PR) elongation, lateral root (LR) initiation and development (1) and root hair (RH) elongation (2). (1) Auxin imported from the main PAT stream into the root stimulates SL production. SL export into the xylem and down regulation of the PAT stream feedback on auxin levels in the shoot as described under (A). SL biosynthesis genes are specifically expressed in vascular tissue and the cortex of the proximal meristem of the root, through which the lateral auxin reflux toward the main PAT stream takes place. Therefore it is likely that locally synthesized SLs are controlling the efficiency of this reflux. Primary root elongation and lateral root initiation are determined by the auxin gradient inside the root tip, which is determined by auxin levels imported through the PAT stream, auxin synthesized in the root tip, and local auxin transport, including the auxin lateral reflux. Lateral root development and emergence are controlled by auxin derived from the shoot for which the SL controlled PAT stream capacity and lateral auxin influx into the developing lateral root primordia (LRP) are the main determinants. Although in the flow diagram auxin is depicted as a positive regulator of root growth, auxin displays a dose-response curve with an optimum, such that supra-optimal auxin concentrations will have a negative effect (Ruyter-Spira et al., 2011). (2) The effect of SLs on RH elongation is dependent on both auxin and ethylene (ET) biosynthesis and signaling. It has been suggested that SLs negatively regulate auxin efflux (Koltai et al., 2010). If this would specifically occur in RH cells this would result in increased local auxin levels which stimulates RH elongation. This local action of SLs has not been proven yet. Alternatively, it may be that SLs affect auxin transport in the PAT stream and/or the root tip hereby indirectly affecting the auxin concentration in RH cells. ET acts downstream of SLs and has a direct effect on RH elongation but also interacts with the auxin pathway (Kapulnik et al., 2011b). Abbreviations: P, primordium; DM, distal meristem; PM, proximal meristem; AM, apical meristem; BM, basal meristem; TZ, transition zone; EZ, elongation zone; DZ, differentiation zone; FC, founder cell.