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COST1 regulates autophagy to control plant drought tolerance

Plants balance their competing requirements for growth and stress tolerance via a sophisticated regulatory circuitry that controls responses to the external environments. We have identified a plant-specific gene, COST1 (constitutively stressed 1), that is required for normal plant growth but negatively regulates drought resistance by influencing the autophagy pathway.

Yan Bao, Wei-Meng Song, Peipei Wang, Xiang Yu, Bei Li, Chunmei Jiang,  View ORCID ProfileShin-Han Shiu, Hongxia Zhang, and Diane C. Bassham

PNAS March 31, 2020 117 (13) 7482-7493

Significance

Drought is one of the most devastating threats to agricultural sustainability worldwide. Autophagy is known to be critical for plant responses to multiple stresses, including drought, but a direct link between drought tolerance and autophagy is still lacking. We report here the identification of a plant-specific protein, COST1 (constitutively stressed 1), which attenuates autophagy under optimal growth conditions, thus controlling the trade-off between plant growth and stress tolerance. In addition to expanding our understanding of the regulation of autophagy in plants, the enhanced drought tolerance of a cost1 mutant and the high conservation of COST proteins throughout the plant kingdom also indicates a potential for engineering COST1 to enhance stress tolerance in crops.

Abstract

Plants balance their competing requirements for growth and stress tolerance via a sophisticated regulatory circuitry that controls responses to the external environments. We have identified a plant-specific gene, COST1 (constitutively stressed 1), that is required for normal plant growth but negatively regulates drought resistance by influencing the autophagy pathway. An Arabidopsis thaliana cost1 mutant has decreased growth and increased drought tolerance, together with constitutive autophagy and increased expression of drought-response genes, while overexpression of COST1 confers drought hypersensitivity and reduced autophagy. The COST1 protein is degraded upon plant dehydration, and this degradation is reduced upon treatment with inhibitors of the 26S proteasome or autophagy pathways. The drought resistance of a cost1 mutant is dependent on an active autophagy pathway, but independent of other known drought signaling pathways, indicating that COST1 acts through regulation of autophagy. In addition, COST1 colocalizes to autophagosomes with the autophagosome marker ATG8e and the autophagy adaptor NBR1, and affects the level of ATG8e protein through physical interaction with ATG8e, indicating a pivotal role in direct regulation of autophagy. We propose a model in which COST1 represses autophagy under optimal conditions, thus allowing plant growth. Under drought, COST1 is degraded, enabling activation of autophagy and suppression of growth to enhance drought tolerance. Our research places COST1 as an important regulator controlling the balance between growth and stress responses via the direct regulation of autophagy.

See https://www.pnas.org/content/117/13/7482

Figure 3:

Expression of COST1 during drought stress. (A) Localization and characteristics of COST1-YFP protein after 3 h of dehydration treatment. (Scale bar, 10 µm.) (B and C) Quantification of fluorescence intensity and punctate structures before and after 3 h of dehydration treatment. Signals were quantified for at least 10 images per replicate, with 3 biological replicates. Asterisks indicate significant differences, compared with no treatment. (D) Immunoblot of COST1-YFP protein after dehydration treatment for the indicated times using antibodies against GFP. The number below indicates the band intensity of COST1-YFP, and Ponceau staining was used as a loading control. (E) Immunoblot of COST1-YFP protein after treatment with DMSO (control), MG132, or ConcA. (F) COST1-YFP was immunoprecipitated after treatment with DMSO, MG132, or ConcA under normal conditions, followed by detection using anti-GFP antibodies. (G) Ubiquitination of COST1-YFP after dehydration of 10-d-old COST1-YFP or YFP transgenic plants for 6 h. After immunoprecipitation with GFP-trap, samples were immunoblotted using antibodies against ubiquitin. Transgenic COST1-YFP plants were generated in cost1 mutant background with full complementation.

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