PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating arabidopsis hypocotyl growth

PLoS Genet. 2012;8(3):e1002594. doi: 10.1371/journal.pgen.1002594. Epub 2012 Mar 29.

Abstract

Higher plants adapt their growth to high temperature by a dramatic change in plant architecture. It has been shown that the transcriptional regulator phytochrome-interacting factor 4 (PIF4) and the phytohormone auxin are involved in the regulation of high temperature-induced hypocotyl elongation in Arabidopsis. Here we report that PIF4 regulates high temperature-induced hypocotyl elongation through direct activation of the auxin biosynthetic gene YUCCA8 (YUC8). We show that high temperature co-upregulates the transcript abundance of PIF4 and YUC8. PIF4-dependency of high temperature-mediated induction of YUC8 expression as well as auxin biosynthesis, together with the finding that overexpression of PIF4 leads to increased expression of YUC8 and elevated free IAA levels in planta, suggests a possibility that PIF4 directly activates YUC8 expression. Indeed, gel shift and chromatin immunoprecipitation experiments demonstrate that PIF4 associates with the G-box-containing promoter region of YUC8. Transient expression assay in Nicotiana benthamiana leaves support that PIF4 directly activates YUC8 expression in vivo. Significantly, we show that the yuc8 mutation can largely suppress the long-hypocotyl phenotype of PIF4-overexpression plants and also can reduce high temperature-induced hypocotyl elongation. Genetic analyses reveal that the shy2-2 mutation, which harbors a stabilized mutant form of the IAA3 protein and therefore is defective in high temperature-induced hypocotyl elongation, largely suppresses the long-hypocotyl phenotype of PIF4-overexpression plants. Taken together, our results illuminate a molecular framework by which the PIF4 transcriptional regulator integrates its action into the auxin pathway through activating the expression of specific auxin biosynthetic gene. These studies advance our understanding on the molecular mechanism underlying high temperature-induced adaptation in plant architecture.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Arabidopsis* / genetics
  • Arabidopsis* / growth & development
  • Arabidopsis* / metabolism
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Gene Expression Regulation, Plant
  • Hot Temperature
  • Hypocotyl* / genetics
  • Hypocotyl* / growth & development
  • Indoleacetic Acids / metabolism*
  • Mixed Function Oxygenases / genetics
  • Mixed Function Oxygenases / metabolism*
  • Mutation
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Oxygenases / genetics
  • Oxygenases / metabolism*
  • Plants, Genetically Modified
  • Promoter Regions, Genetic
  • Protein Binding
  • Tobacco / genetics
  • Tobacco / metabolism

Substances

  • Arabidopsis Proteins
  • Basic Helix-Loop-Helix Transcription Factors
  • Indoleacetic Acids
  • Nuclear Proteins
  • PIF4 protein, Arabidopsis
  • SHY2 protein, Arabidopsis
  • Mixed Function Oxygenases
  • YUCCA8 protein, Arabidopsis
  • Oxygenases
  • YUC protein, Arabidopsis