A Mobile Auxin Signal Connects Temperature Sensing in Cotyledons with Growth Responses in Hypocotyls

Abstract

Plants have a remarkable capacity to adjust their growth and development to elevated ambient temperatures. Increased elongation growth of roots, hypocotyls, and petioles in warm temperatures are hallmarks of seedling thermomorphogenesis. In the last decade, significant progress has been made to identify the molecular signaling components regulating these growth responses. Increased ambient temperature utilizes diverse components of the light sensing and signal transduction network to trigger growth adjustments. However, it remains unknown whether temperature sensing and responses are universal processes that occur uniformly in all plant organs. Alternatively, temperature sensing may be confined to specific tissues or organs, which would require a systemic signal that mediates responses in distal parts of the plant. Here, we show that Arabidopsis (Arabidopsis thaliana) seedlings show organ-specific transcriptome responses to elevated temperatures and that thermomorphogenesis involves both autonomous and organ-interdependent temperature sensing and signaling. Seedling roots can sense and respond to temperature in a shoot-independent manner, whereas shoot temperature responses require both local and systemic processes. The induction of cell elongation in hypocotyls requires temperature sensing in cotyledons, followed by the generation of a mobile auxin signal. Subsequently, auxin travels to the hypocotyl, where it triggers local brassinosteroidinduced cell elongation in seedling stems, which depends upon a distinct, permissive temperature sensor in the hypocotyl.

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

“…Auxin signaling output is tightly connected to its transport within and across tissues (reviewed in (Benjamins and Scheres, ). During shoot responses to temperature, auxin is produced in the cotyledons and transported to the hypocotyl to promote cell elongation (Bellstaedt et al, 2019). Furthermore, the modulation of auxin long-distance transport from the shoot to the root can regulate root developmental responses to environmental light conditions (Sassi et al, 2012).…”

“…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 (Wang et al, 2016).Although root and shoot thermomorphogenesis occur simultaneously during early seedling development (Bellstaedt et al, 2019), it is still unclear whether these responses are coordinated at the whole plant level. In this study, we leveraged a genetic approach combined with comprehensive phenotypic analyses, transcriptional profiling and metabolic measurements to further characterize the molecular circuits mediating root thermomorphogenesis.…”

“…Although root and shoot thermomorphogenesis occur simultaneously during early seedling development (Bellstaedt et al, 2019), it is still unclear whether these responses are coordinated at the whole plant level. In this study, we leveraged a genetic approach combined with comprehensive phenotypic analyses, transcriptional profiling and metabolic measurements to further characterize the molecular circuits mediating root thermomorphogenesis.…”

PHYTOCHROME INTERACTING FACTOR 7 is important for early responses to elevated temperature in Arabidopsis seedlings

“…Hypocotyl elongation in response to shade and temperature elevation also depends on other phytohormones including gibberellic acid (GA) and brassinosteroids (BR) (Quint et al, 2016;Legris et al, 2017;Casal & Balasubramanian, 2019). BR acts in the hypocotyl while auxin biosynthesis mainly occurs in cotyledons before being transported to the hypocotyl to promote elongation (Stavang et al, 2009;Oh et al, 2012;Kohnen et al, 2016;Procko et al, 2016;Ibanez et al, 2018;Martinez et al, 2018;Bellstaedt et al, 2019).…”

Rapid systemic signaling during abiotic and biotic stresses: is the ROS wave master of all trades?

“…Because many of the systemic signals were shown to involve plant hormones, such as jasmonic acid (JA) or methyl jasmonate (MJ), ethylene, abscisic acid (ABA), auxin (IAA) and others (e.g. Devireddy et al , ; Mittler and Blumwald, ; Choudhury et al , ; Zhang et al , ; Bellstaedt et al , ; Marcec et al , ), crosstalk between these hormones could play a key role in systemic signaling. In addition, many of these hormones, especially those that accumulate at a very rapid rate in systemic tissues (e.g.…”