Genetic dissection of signaling processes regulating response to elevated ambient temperatures in Arabidopsis thaliana

• Applicant: Professor Dr. Marcel Quint
• Subject Area: Plant Physiology ; Plant Genetics and Genomics
• Term: from 2012 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 223862977

• Final Report Year: 2022

Final Report Abstract

This project aimed to identify novel regulators that mediate morphological plant responses to warm temperatures (termed thermomorphogenesis) and to characterize their function within the known framework of molecular regulators that centers around the transcription factor PIF4. Using a forward genetic approach, we previously have isolated mutants which are compromised in their ability to elongate hypocotyls in response to elevated temperatures. Identification of the genes that cause the altered phenotype resulted in two promising candidates: D6PK and SMAX1. While SMAX1 function in thermomorphogenesis has recently been published by another group, we were able to show that D6PK is required for temperature-induced auxin to translocate from cotyledons into the hypocotyl to induce cell elongation. In a second approach, we aimed to specifically identify transcription factors that contribute to thermomorphogenesis regulation using the available TRANSPLANTA collection which allows inducible overexpression of hundreds of transcription factor genes. Here, several promising candidate genes were identified that caused hypersensitive or reduced temperature responses. While characterization of their potential role in thermomrophogenesis is ongoing for several of the identified TFs, we focused specifically on a group of (b)HLH transcription factors, some of which have previously been implicated as regulators of cell elongation. For several members of this TF family, a tripartite level of antagonistic regulation has been implicated in response to several stimuli. This tri-antagonistic system involves the actual bHLH transcriptional regulators which can be repressed by binding to a HLH repressor. The repressor can be scavenged by binding of a secondary HLH repressor which thereby de-represses the inhibition of the actual transcriptional regulator. We were able to show that PIF4 function at warm ambient temperature can be modulated by PAR repressors and PRE secondary repressors and that loss of the respective genes affects thermomorphogenesis. Furthermore, PIF4 can bind to the promoter of its secondary repressor PRE1 which suggests a feed-forward regulation by which PIF4 can prevent its inhibition via PARs by inducing a secondary repressor (PREs) to scavenge the repressor (PARs).

Publications

• (2014) The DET1-COP1-HY5 pathway constitutes a multipurpose signaling module regulating plant photomorphogenesis and thermomorphogenesis. Cell Reports 9:1983-1989
  Delker C, Sonntag L, Velikkakam James G, Janitza P, Ibañez C, Ziermann H, Peterson T, Denk K, Mull S, Ziegler J, Davis SJ, Schneeberger K, Quint M
  
• (2015) Natural Variants of ELF3 Affect Thermomorphogenesis by Transcriptionally Modulating PIF4- Dependent Auxin Response Genes. BMC Plant Biology 15:197
  Raschke A, Ibañez C, Ullrich KK, Anwer MU, Becker S, Glöckner A, Trenner J, Denk K, Saal B, Sun X, Ni M, Davis SJ, Delker C, Quint M
  
• (2016) Molecular and genetic control of plant thermomorphogenesis. Nature Plants 2:15190
  Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, van Zanten M
  
• (2018). Brassinosteroids dominate hormonal regulation of plant thermomorphogenesis via BZR1. Current Biology 28:303-310
  Ibañez C, Delker C, Martinez C, Bürstenbinder K, Janitza P, Lippmann R, Ludwig W, Sun H, James GV, Klecker M, Grossjohann A, Schneeberger K, Prat S, Quint M
  
• (2019). A mobile auxin signal connects temperature sensing in cotyledons with growth responses in hypocotyls. Plant Physiology 180:757–766
  Bellstaedt J, Trenner J, Lippmann R, Poeschl Y, Zhang X, Friml J, Quint M, Delker C
  
• (2019). Development of wild and cultivated plants under global warming conditions. Current Biology 29:R1326-R1338
  Lippmann R, Babben S, Menger A, Delker C, Quint M
  
• (2020) Cut and paste - Temperature-enhanced cotyledon micrografting for Arabidopsis thaliana seedlings. Plant Methods 16:12
  Bartusch K, Trenner J, Melnyk CW, Quint M
  
• (2021) High and low temperature signalling and response. Journal of Experimental Botany 72:7339-7344
  de Smet I, Quint M, van Zanten M
  
• (2021) On the evolution of plant thermomorphogenesis. Journal of Experimental Botany 72:7345–7358
  Ludwig W, Hayes S, Trenner J, Delker C, Quint M
  
• (2022) High temperature perception in leaves promotes vascular regeneration and graft formation in distant tissues. Development 149:dev200079
  Serivichyaswat PT, Bartusch K, Leso M, Musseau C, Iwase A, Chen Y, Sugimoto K, Quint M, Melnyk CW