Abstract

SUMMARYTemperature passively affects biological processes involved in plant growth. Therefore, it is challenging to study the dedicated temperature signalling pathways that orchestrate thermomorphogenesis, a suite of elongation growth‐based adaptations that enhance leaf‐cooling capacity. We screened a chemical library for compounds that restored hypocotyl elongation in the pif4‐2–deficient mutant background at warm temperature conditions in Arabidopsis thaliana to identify modulators of thermomorphogenesis. The small aromatic compound ‘Heatin’, containing 1‐iminomethyl‐2‐naphthol as a pharmacophore, was selected as an enhancer of elongation growth. We show that ARABIDOPSIS ALDEHYDE OXIDASES redundantly contribute to Heatin‐mediated hypocotyl elongation. Following a chemical proteomics approach, the members of the NITRILASE1‐subfamily of auxin biosynthesis enzymes were identified among the molecular targets of Heatin. Our data reveal that nitrilases are involved in promotion of hypocotyl elongation in response to high temperature and Heatin‐mediated hypocotyl elongation requires the NITRILASE1‐subfamily members, NIT1 and NIT2. Heatin inhibits NIT1‐subfamily enzymatic activity in vitro and the application of Heatin accordingly results in the accumulation of NIT1‐subfamily substrate indole‐3‐acetonitrile in vivo. However, levels of the NIT1‐subfamily product, bioactive auxin (indole‐3‐acetic acid), were also significantly increased. It is likely that the stimulation of hypocotyl elongation by Heatin might be independent of its observed interaction with NITRILASE1‐subfamily members. However, nitrilases may contribute to the Heatin response by stimulating indole‐3‐acetic acid biosynthesis in an indirect way. Heatin and its functional analogues present novel chemical entities for studying auxin biology.

Highlights

  • Many plant species, including the model system Arabidopsis thaliana, respond to small increases in temperature by adapting their architecture to maximize fitness in suboptimal temperature conditions

  • We demonstrate by genetic means that the NIT1-subfamily of nitrilases promotes hypocotyl elongation in response to high temperature and that Heatin requires these enzymes for its effect on hypocotyl elongation

  • This shows that Heatin treatment phenocopies thermomorphogenesis and acts at least partly genetically downstream of PHYTOCHROME INTERACTING FACTORS 4 (PIF4) or bypasses PIF4 effects

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Summary

Introduction

Many plant species, including the model system Arabidopsis thaliana, respond to small increases in temperature by adapting their architecture to maximize fitness in suboptimal temperature conditions. Central in the regulation of thermomorphogenesis are bHLH transcription factor proteins PHYTOCHROME INTERACTING FACTORS 4 (PIF4) and PIF7 (Chung et al, 2020; Fiorucci et al, 2020; Franklin et al, 2011; van der Woude et al, 2019) Levels of these PIFs increase rapidly in response to high temperature (Chung et al, 2020; Fiorucci et al, 2020; Franklin et al, 2011; van der Woude et al, 2019) and PIFs induce biosynthesis of the bioactive auxin indole-3-acetic acid (IAA) that is required for thermomorphogenesis by binding and activating the promoters of key auxin biosynthesis genes such as TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA1) and the cytochrome P450s genes, CYP79B2 and CYP79B3, as well as the flavin monooxygenase YUCCA8 (YUC8) (Chung et al, 2020; Fiorucci et al, 2020; Franklin et al, 2011; Sun et al, 2012; van der Woude et al, 2019)

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