Editors' ChoicePlant biology

Stress signals in plants

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Science Signaling  18 Apr 2017:
Vol. 10, Issue 475, eaan4524
DOI: 10.1126/scisignal.aan4524

Selective autophagy mediates the cross-talk between plant growth and stress signaling pathways.

In living organisms, there is often an energetic trade-off between growth and stress responses, and regulation of this balance is especially important in plants, which cannot adapt to stresses by moving to a new location. Plant growth is promoted by brassinosteroid (BR) hormones, which inhibit the GSK3-like kinase BIN2, preventing BIN2 from deactivating transcription factors, including the “master regulator” BES1. Nolan et al. found that selective autophagy of BES1 was required to slow plant growth to enable survival under drought, starvation, and osmotic stress. Experiments with specific pharmacological inhibitors in mutant and wild-type Arabidopsis thaliana demonstrated that BES1 was degraded by autophagy. BES1 interacted with DSK2, a ubiquitin-binding receptor, and DSK2 was required for the localization of BES2 to the autophagosome and for its degradation. Under glucose starvation or osmotic stress, the growth of DSK2-knockdown mutants was less sensitive to inhibition of BR than was the growth of wild-type plants, indicating that DSK2 was linked to changes in BR-dependent growth signaling under stress. DSK2 was phosphorylated by BIN2, which promoted the association of DSK2 with ATG8, which targets proteins for autophagy. Plant mutants defective for autophagy or with constitutively active BR signaling died in response to drought, whereas wild-type plants and plants with a loss-of-function mutation in the BR signaling pathway survived. BES1 abundance was reduced in response to dehydration in wild-type plants, whereas BES1 accumulated in DSK2-knockdown plants without any accompanying changes in BES1 transcription. DSK2-knockdown plants and plants with constitutive BR signaling showed similar sets of genes that were differentially expressed compared with those in wild-type plants in response to drought. A similar set of responses, including gene expression profiles and effects on BES1 abundance, was observed under carbon starvation. Thus, BIN2 negatively regulates BES1 by phosphorylation and through targeting BES1 for autophagy by enabling DSK2-ATG8 interactions. This study helps elucidate the mechanistic basis of trade-offs between growth and stress responses. In an accompanying paper, Yang et al. investigated additional, light-dependent mechanisms controlling BES1 stability and degradation and therefore the regulation of plant growth. Together, these studies describe how BES1 mediates BR signaling regulation in response to environmental conditions.

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