Two antagonistic gene regulatory networks drive Arabidopsis root hair growth at low temperature

Abstract

The root hair (RH) cells can elongate to several hundred times their initial size, and are an ideal model system for investigating cell size control. Their development is influenced by both endogenous and external signals, which are combined to form an integrative response. Surprisingly, a low temperature condition of 10{degrees}C causes an increased RH growth in Arabidopsis and in several monocots, even when the development of the rest of the plant are halted. Previously, we demonstrated a strong correlation between the RH growth response and a significant decrease in nutrient availability in the medium under low temperature conditions. However, the molecular basis responsible for receiving and transmitting signals related to the availability of nutrients in the soil, and their relation to plant development, remain largely unknown. In this study, we have discovered two antagonic gene regulatory networks (GRNs) controlling RH early transcriptome responses to low temperature. One GNR enhances RH growth and it is commanded by the transcription factors (FTs) ROOT HAIR DEFECTIVE 6 (RHD6), HAIR DEFECTIVE 6-LIKE 2 and 4 (RSL2-RSL4) and a member of the homeodomain leucine zipper (HD-Zip I) group I 16 (AtHB16). On the other hand, a second GRN was identified as a negative regulator of RH growth at low temperature and it is composed by the trihelix TF GT2-LIKE1 (GTL1) and the associated DF1, a previously unidentified MYB-like TF (AT2G01060) and several members of HD-Zip I group (AtHB3, AtHB13, AtHB20, AtHB23). Functional analysis of both GRNs highlights a complex regulation of RH growth response to low temperature, and more importantly, these discoveries enhance our comprehension of how plants synchronize the RH growth in response to variations in temperature at the cellular level. Significance StatementRoot hair (RH) cells may expand hundreds of times, making them a useful cell size model. Integrated endogenous and exogenous cues affect their development. Even when plant development ceases, Arabidopsis and other monocots grow RH at 10{degrees}C. We previously established a strong correlation between growth response and a substantial medium nutrition reduction at low temperature. Receiving and transmitting soil nutrient signals and their impact on plant development are unknown molecularly. Our study identified two opposing gene regulatory networks (GRN) that govern early transcriptome responses linked to RH growth at low temperature. Functional analysis shows a complex regulation of the transcriptional cascade to influence the low-temperature RH growth. These results explain how cells coordinate RH formation in response to temperature.