Shoot-to-Root Mobile Transcription Factor HY5 Coordinates Plant Carbon and Nitrogen Acquisition

Abstract

Coordination of shoot photosynthetic carbon fixation with root inorganic nitrogen uptake optimizes plant performance in a fluctuating environment [1]. However, the molecular basis of this long-distance shoot-root coordination is little understood. Here we show that Arabidopsis ELONGATED HYPOCOTYL5 (HY5), a bZIP transcription factor that regulates growth in response to light [2, 3], is a shoot-to-root mobile signal that mediates light promotion of root growth and nitrate uptake. Shoot-derived HY5 auto-activates root HY5 and also promotes root nitrate uptake by activating NRT2.1, a gene encoding a high-affinity nitrate transporter [4]. In the shoot, HY5 promotes carbon assimilation and translocation, whereas in the root, HY5 activation of NRT2.1 expression and nitrate uptake is potentiated by increased carbon photoassimilate (sucrose) levels. We further show that HY5 function is fluence-rate modulated and enables homeostatic maintenance of carbon-nitrogen balance in different light environments. Thus, mobile HY5 coordinates light-responsive carbon and nitrogen metabolism, and hence shoot and root growth, in a whole-organismal response to ambient light fluctuations.

Seedling Establishment: A Dimmer Switch-Regulated Process between Dark and Light Signaling

“…The role for HY5 in Arabidopsis root development has been known for a long time, as HY5-deficient mutants show defects in root hair development, gravitropism, lateral root outgrowth, and elongation (Oyama et al, 1997;Sibout et al, 2006). The HY5 protein is, as was discovered recently, translocated via the phloem toward the root, with root-specific HY5 and HYH transcription, and promoted root development as a consequence (Chen et al, 2016;Zhang et al, 2017; Fig. 3D).…”

“…3D). By quickly enhancing root elongation and lateral root outgrowth upon seedling establishment, the young photoautotrophic plant can start the uptake of water and nutrients such as nitrate to fuel growth (Chen et al, 2016). cycles of variable duration and light intensity depending on the latitude and time of the year.…”

Light Signaling, Root Development, and Plasticity

“…Stem-piped light can activate root-expressed phyB, which on its turn regulates HY5 in the Arabidopsis root (Lee et al, 2016). HY5 is involved in root growth in response to light, modulating, for example, root gravitropism and nitrogen uptake (Cluis et al, 2004;Lee et al, 2007;Huang et al, 2015;Chen et al, 2016). Therefore, stem-piped light might communicate information about the aboveground light environment to the root (Fig.…”

“…The transcription factor HY5 is a key integrator of photomorphogenesis and is involved in light, hormone, and stress signaling (Cluis et al, 2004;Lee et al, 2007;Gangappa and Botto, 2016). HY5 was recently shown to be transported upon light activation from the shoot to the root (Chen et al, 2016). In the root system, HY5 activates its own expression and that of HYH, creating a positive feedback loop after shoot-to-root transport of HY5 .…”

“…One clear functional example is that HY5 can stimulate nitrate uptake via NRT2;1 and will do so upon light-activation in the shoot (Chen et al, 2016;Fig. 3).…”