Abstract
Both light and temperature have dramatic effects on plant development. Phytochrome photoreceptors regulate plant responses to the environment in large part by controlling the abundance of PHYTOCHROME INTERACTING FACTOR (PIF) transcription factors. However, the molecular determinants of this essential signaling mechanism still remain largely unknown. Here, we present evidence that the BLADE-ON-PETIOLE (BOP) genes, which have previously been shown to control leaf and flower development in Arabidopsis, are involved in controlling the abundance of PIF4. Genetic analysis shows that BOP2 promotes photo-morphogenesis and modulates thermomorphogenesis by suppressing PIF4 activity, through a reduction in PIF4 protein level. In red-light-grown seedlings PIF4 ubiquitination was reduced in the bop2 mutant. Moreover, we found that BOP proteins physically interact with both PIF4 and CULLIN3A and that a CULLIN3-BOP2 complex ubiquitinates PIF4 in vitro. This shows that BOP proteins act as substrate adaptors in a CUL3BOP1/BOP2 E3 ubiquitin ligase complex, targeting PIF4 proteins for ubiquitination and subsequent degradation.
Highlights
A key element of plant adaptive responses is their ability to make morphological changes by adjusting the regulatory processes controlling their growth and development patterns in response to environmental stimuli such as changes in light and temperature
As observed for hypocotyl elongation, the pif4bop1bop2 triple mutants had the same cotyledon separation phenotype as the pif4 single mutant (Figure 2c). These results show that pif4 is epistatic over bop2 and that PIF4 is necessary for the BOP2-mediated suppression of hypocotyl elongation and promotion of cotyledon separation
We tested whether BOP2 could mediate the interaction of PIF4 to a CUL3 complex by coexpressing HA-CUL3A, myc-BOP2 and HA-PIF4 in protoplasts followed by immunoprecipitation with anti-myc antibodies (Covance, Princeton, USA). Both HA-CUL3A and HA-PIF4 could be pulled down by BOP2 (Figure 4f), suggesting that all three proteins may act in the same complex. These results demonstrate that the BOP proteins physically interact with PIF4 and serve as substrate adaptors in a CUL3BOP1/BOP2 E3 ubiquitin ligase complex potentially targeting PIF4 for ubiquitination and subsequent degradation
Summary
A key element of plant adaptive responses is their ability to make morphological changes by adjusting the regulatory processes controlling their growth and development patterns in response to environmental stimuli such as changes in light and temperature. Members of the phytochrome light receptor family have the unique ability to sense red (R) and far-red (FR) light. They control germination, early seedling development, stem and internode elongation, the balance between leaf lamina and petiole formation (part of the shade avoidance syndrome) and the transition to flowering (Franklin and Quail, 2010). All higher plants possess multiple phytochromes (phyA-phyE in Arabidopsis) with phyB being the primary photoreceptor mediating seedling de-etiolation in red light. A major function of phyB is to prevent the shade-avoidance syndrome (SAS) in sunlight, an environment that is rich in red light and leading to phyB activation. It was shown that phyB can integrate light and temperature signals by acting as a thermosensor (Jung et al, 2016; Legris et al, 2016)
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