Auxin-dependent acceleration of cell division rates regulates root growth at elevated temperature

Abstract

Roots are highly plastic organs enabling plants to acclimate to a changing below-ground environment. In addition to abiotic factors like nutrients or mechanical resistance, plant roots also respond to temperature variation. Below the heat stress threshold, Arabidopsis thaliana seedlings react to elevated temperature by promoting primary root growth, possibly to reach deeper soil regions with potentially better water saturation. While above-ground thermomorphogenesis is enabled by thermo-sensitive cell elongation, it was unknown how temperature modulates root growth. We here show that roots are able to sense and respond to elevated temperature independent of shoot-derived signals. An unknown root thermosensor seems to employ auxin as a messenger to promote primary root growth. Growth is primarily achieved by accelerating cell division rates in the root apical meristem, likely maintained via temperature-sensitive organization of the polar auxin transport system. Hence, the primary cellular target of elevated ambient temperature differs fundamentally between root and shoot tissues, while the messenger auxin that relays temperature information to elongating or dividing cells, respectively, remains the same.

Warm temperature and mild water stress cooperatively promote root elongation

“…In an effort to establish a molecular pathway for the control of mild osmotic stress and warm temperatureinduced root elongation, we tested mutants of genes that have established roles in shoot temperature signalling. The detached roots of plants deficient in PIF1, 3, 4, 5 and 7 (pifq/pif7-1) behaved very similarly to the wild type (Figure 3SA), confirming early reports that these genes are not required for local root responses to warm temperature 10,11 . We also found that the roots of mutants lacking phyA and phyB were very similar to wild type roots (Figure S3B).…”

“…These results reveal COP1 to be a repressor of warm temperature / water stress signalling in roots. Most studies into warm temperature-induced root elongation are performed in the light 3,7,10,15,16 . This result could therefore explain why multiple groups have reported warm temperature-induced elongation in the absence of water stress, and why warm temperatureenhanced root elongation is reduced or lost in short photoperiod conditions 15,16 .…”

Temperature Sensing in Plants

“…This raises the question of how local temperature information is sensed and integrated, and whether there are systemic temperature signals within the plant. Interestingly, it appears that roots sense temperature independently of shoots in Arabidopsis, and known shoot thermomorphogenesis regulators, phytochromes and ELF3, are not primarily involved in the response (1,12). In aerial tissues, the heat shock response is particularly strongly induced in the shoot apical meristem, suggesting that specific cell types have different responses to temperature (101).…”

Temperature changes in the root ecosystem affect plant functionality

“…Nowadays, climate change is leading to more frequent high-temperature extremes, such as heat waves, that aggravate the negative impact of heat on plant development and agricultural yield ( Gray and Brady, 2016 ; Miller et al., 2021 ). In comparison with shoot responses, root responses to high temperatures have been understudied, and the majority of studies have focused on the response to warming, which induced thermomorphogenesis responses, rather than heat stress ( Nagel et al., 2009 ; Bellstaedt et al., 2019 ; Gaillochet et al., 2020 ; Lee et al., 2021b ; Ai et al., 2022 ). However, there is an increasing interest in deciphering the role of roots in plant adaptation to heat stress ( Huang et al., 2012 ; Calleja-Cabrera et al., 2020 ; Tiwari et al., 2022 ), driven primarily by general concerns about how climate change might affect crop production in agricultural systems ( Fahad et al., 2017 ).…”