COST1 regulates autophagy to control plant drought tolerance

First author: Yan Bao; Affiliations: Iowa State University (爱荷华州立大学): Ames, USA

Corresponding author: Diane C. Bassham

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.

植物通过一个响应于外部环境的复杂调控通路来平衡生长与胁迫抗性之间的竞争关系。作者鉴定了一个植物特异性的基因COST1，该基因作用于正常的植物生长，但通过影响自噬（autophagy）途径负调控干旱抗性。拟南芥的cost1突变体的生长水平下降，但干旱抗性水平上升，同时还出现组成型的自噬以及干旱响应相关基因的表达上调，另外过表达COST1赋予了植株对于干旱的超敏以及自噬减少。COST1蛋白在植物脱水时会降解，而在利用26S蛋白酶体抑制剂或自噬通路抑制剂处理时，COST1蛋白的降解会明显减少。cost1突变体的干旱抗性依赖于自噬通路的激活，但是独立于其它已知的干旱信号通路，表明COST1是通过自噬通路发挥作用的。另外，COST1与自噬体标记ATG8e以及自噬接头蛋白NBR1共定位于自噬体，且通过与ATG8e的物理互作直接影响ATG8e的蛋白水平，说明了COST1蛋白能够直接作用于自噬的调控。作者提出了一个模型，其中COST1蛋白会在植物处于最适环境条件下抑制自噬，所以使得植株正常生长。而当植物遭受干旱胁迫时，COST1蛋白被降解，自噬通路被激活，从而抑制生长，增强植株的干旱抗性。本文的研究鉴定了COST1作为一个重要的调控因子，通过直接调控植物中的自噬通路参与植物生长与胁迫响应之间的平衡调控。

Significance

干旱是对全球作物可持续生产的最具破坏性的威胁之一。自噬是植物响应包括干旱在内的多种胁迫时的重要生理进程，但目前在植物的干旱耐受性与自噬之间直接的分子关联仍不清楚。本文报道了一个植物特异性蛋白COST1，该蛋白能够在植物处于最优生长条件下时降低植株体内的自噬，从而能够控制植物生长与胁迫抗性之间的平衡。除了拓宽了我们对于植物自噬调控的理解，cost1突变体的优越抗旱能力以及植物界COST蛋白的高度保守表明未来作物育种中可以通过针对COST蛋白的人为改造来增强作物的胁迫抗性。

通讯：Diane C. Bassham (https://www.ipb.iastate.edu/people/diane-bassham)

个人简介：1990年，伯明翰大学，学士；1993年，沃里克大学，博士。

研究方向：植物液泡的生物发生及功能。

doi: https://doi.org/10.1073/pnas.1918539117

Journal: PNAS

First Published: March 13, 2020