Shoot and root thermomorphogenesis are linked by a developmental trade-off

Abstract

Temperature is one of the most impactful environmental factors to which plants adjust their growth and development. While the regulation of temperature signaling has been extensively investigated for the aerial part of plants, much less is known and understood about how roots sense and modulate their growth in response to fluctuating temperatures. Here we found that shoot and root growth responses to high ambient temperature are coordinated during early seedling development. A shoot signaling module that includes HY5, the phytochromes and the PIFs exerts a central function in coupling these growth responses and control auxin levels in the root. In addition to the HY5/PIF-dependent shoot module, a regulatory axis composed of auxin biosynthesis and auxin perception factors controls root responses to high ambient temperature. Together, our findings show that shoot and root developmental responses to temperature are tightly coupled during thermomorphogenesis and suggest that roots integrate energy signals with local hormonal inputs.genes including YUC8 Gangappa and Kumar, 2017). Both HY5 and PIF4 expression levels and protein abundance are tightly regulated by a plethora of factors (reviewed in (Lau and Deng, 2012;Quint et al., 2016)). Among those, CONSTITUTIVE PHOTOMORPHOGENESIS PROTEIN1 (COP1) and DEETIOLATED1 (DET1) trigger HY5 degradation and promote both PIF4 expression and protein stabilization (Gangappa and Kumar, 2017;Osterlund et al., 2000;Saijo et al., 2003;Yanagawa et al., 2004). The collective genetic activity of PIF4, HY5, COP1 and DET1 defines an intertwined regulatory module that acts at the interface between light and temperature signalling Gangappa and Kumar, 2017). Interestingly, HY5 protein has also been shown to translocate from the shoot to the root and to coordinate carbon fixation with nitrogen uptake (Chen et al., 2016). Importantly, roots can autonomously sense and respond to temperature (Bellstaedt et al., 2019), which might allow them to reach deeper and cooler layers of the soil under warm surface conditions (Illston and Fiebrich, 2017). However, in contrast to the shoot, the molecular mechanisms underlying plant root thermo-responses have so far remained elusive. Similarly tothe shoot, maintenance of auxin homeostasis is critical for the root response to temperature (Wang et al., 2016). In line with this idea, auxin signaling increases upon perception of higher ambient temperature (Hanzawa et al., 2013;Wang et al., 2016). In this context the auxin efflux transporters PIN2 and PILS6 mediate auxin transport and local accumulation at the root, which in turn triggers developmental response to temperature in the root (Feraru et al., 2019;Hanzawa et al., 2013). Furthermore, the auxin receptors TIR1 and AFB2 are stabilized upon increased ambient temperature by forming a protein complex with HEAT SHOCK PROTEIN 90 (HSP90) and its co-chaperone SUPPRESSOR OF G2 ALLELE SKP1 (SGT1). The accumulation of TIR1 and AFB2 subsequently activates auxin signaling and mediates root thermo-sensory elongation (...

Local HY5 Activity Mediates Hypocotyl Growth and Shoot-to-Root Communication

“…Surprisingly, we found that CAB3p : DOF-HY5 could also rescue the hy5 root growth defects ( Figure 2D ), indicating that HY5 mobility is not required for HY5-dependent shoot-to-root communication. These results are consistent with the finding that HY5 can trigger an unknown signal in the shoot to control root thermomorphogenesis ( Gaillochet et al, 2020 ). HY5 expression in the shoot and the root was weaker in CER6p : DOF-HY5 line number 9 than that in other lines derived from this construct ( Figure 1D and Supplemental Figure 3A ).…”

“…In addition to the communication between shoot cell layers, communication between aerial and underground organs is crucial for coordinating growth and development between these tissues ( van Gelderen et al, 2018b ). Disrupting this communication by severing aerial and underground portions of a plant leads to decreased growth of both the shoot and roots, and the accumulation of chlorophyll in roots ( Kobayashi et al, 2017 ; Bellstaedt et al, 2019 ; Gaillochet et al, 2020 ). However, as mechanical perturbations are quite severe, the combined effects of the wounding response and the loss of all mobile signals make specific effects difficult to discern.…”