Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities

Joseph Hahm,Keunhwa Kim,Yongjian Qiu,Meng Chen

doi:10.1038/s41467-020-15526-z

Joseph Hahm, Keunhwa Kim + Show 2 more

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https://doi.org/10.1038/s41467-020-15526-z

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Journal: Nature Communications	Publication Date: Apr 3, 2020
Citations: 72	License type: open-access

Affiliation: University of California, Riverside

Abstract

Warm temperature is postulated to induce plant thermomorphogenesis through a signaling mechanism similar to shade, as both destabilize the active form of the photoreceptor and thermosensor phytochrome B (phyB). At the cellular level, shade antagonizes phyB signaling by triggering phyB disassembly from photobodies. Here we report temperature-dependent photobody localization of fluorescent protein-tagged phyB (phyB-FP) in the epidermal cells of Arabidopsis hypocotyl and cotyledon. Our results demonstrate that warm temperature elicits different photobody dynamics than those by shade. Increases in temperature from 12 °C to 27 °C incrementally reduce photobody number by stimulating phyB-FP disassembly from selective thermo-unstable photobodies. The thermostability of photobodies relies on phyB’s photosensory module. Surprisingly, elevated temperatures inflict opposite effects on phyB’s functions in the hypocotyl and cotyledon despite inducing similar photobody dynamics, indicative of tissue/organ-specific temperature signaling circuitry either downstream of photobody dynamics or independent of phyB. Our results thus provide direct cell biology evidence supporting an early temperature signaling mechanism via dynamic assembly/disassembly of individual photobodies possessing distinct thermostabilities.

Highlights

Warm temperature is postulated to induce plant thermomorphogenesis through a signaling mechanism similar to shade, as both destabilize the active form of the photoreceptor and thermosensor phytochrome B
PBs have been characterized extensively using transgenic lines expressing phytochrome B (phyB)-FP36,39,40,44–46,54,55, and to examine the dynamics of phyB tagged with a fluorescent protein (phyB-FP) PBs induced by temperature changes, we went back to the phyB-FP lines, including PBG, which expresses functional phyB-GFP to complement the null phyB-5 mutant in the Landsberg erecta (Ler) background[36], and PBC, which expresses phyB-CFP to complement the null phyB-9 mutant in Col-046,55
PBG and PBC lines showed reduced hypocotyl responses with a 1.4-fold dynamic range for both lines. They retained similar temperature effects on phyB signaling as Ler and Col-0, respectively—that is, warmer temperatures attenuated the function of phyB or enhanced hypocotyl elongation in all four lines (Fig. 1a, b)

Summary

Introduction

Warm temperature is postulated to induce plant thermomorphogenesis through a signaling mechanism similar to shade, as both destabilize the active form of the photoreceptor and thermosensor phytochrome B (phyB). Besides the stress-tolerant responses induced by extreme freezing or scorching conditions[1,2,3], changes in the range of ambient growth temperatures (12–27 °C for Arabidopsis4) can dramatically alter the rate of shoot and root growth and thereby plant architecture[5,6], adjust cell differentiation patterns and developmental transitions such as reproductive organ formation[7,8,9], and modulate plant immunity[10,11,12] These phenomena are collectively called thermomorphogenesis[13,14]. Temperature signaling by phyB is thought to be mediated by a similar mechanism as that of shade[14,18,19]

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