A ligand-independent origin of abscisic acid perception

First author: Yufei Sun; Affiliations: The Hebrew University of Jerusalem (耶路撒冷希伯来大学): Rehovot, Israel

Corresponding author: Assaf Mosquna

Land plants are considered monophyletic, descending from a single successful colonization of land by an aquatic algal ancestor. The ability to survive dehydration to the point of desiccation is a key adaptive trait enabling terrestrialization. In extant land plants, desiccation tolerance depends on the action of the hormone abscisic acid (ABA) that acts through a receptor-signal transduction pathway comprising a PYRABACTIN RESISTANCE 1-like (PYL)–PROTEIN PHOSPHATASE 2C (PP2C)–SNF1-RELATED PROTEIN KINASE 2 (SnRK2) module. Early-diverging aeroterrestrial algae mount a dehydration response that is similar to that of land plants, but that does not depend on ABA: Although ABA synthesis is widespread among algal species, ABA-dependent responses are not detected, and algae lack an ABA-binding PYL homolog. This raises the key question of how ABA signaling arose in the earliest land plants. Here, we systematically characterized ABA receptor-like proteins from major land plant lineages, including a protein found in the algal sister lineage of land plants. We found that the algal PYL-homolog encoded by Zygnema circumcarinatum has basal, ligand-independent activity of PP2C repression, suggesting this to be an ancestral function. Similarly, a liverwort receptor possesses basal activity, but it is further activated by ABA. We propose that co-option of ABA to control a preexisting PP2C-SnRK2-dependent desiccation-tolerance pathway enabled transition from an all-or-nothing survival strategy to a hormone-modulated, competitive strategy by enabling continued growth of anatomically diversifying vascular plants in dehydrative conditions, enabling them to exploit their new environment more efficiently.

陆地植物被认为是单系起源，源自于单个成功殖民陆地的水生藻类植物祖先。能够在某个特定干燥点下脱水生存是陆地化成功的一个关键适应性性状。在现存的陆地植物中，脱水耐受性依赖于植物激素脱落酸ABA介导的一个受体信号转导通路，包含着一个PYL-PP2C-SnRK2模块。早期分化出来的绿藻具有类似于陆地植物的脱水响应，但并不依赖于ABA；尽管ABA合成在藻类植物中广泛存在，但并未检测到ABA依赖性的响应，并且绿藻缺少一个ABA结合PYL同源物。这引出了一个关键的问题，即ABA信号转导如何在早期陆地植物中出现的。本文中，作者系统性研究了主要陆地植物支系的ABA类受体蛋白，包括一个在陆地植物的藻类姊妹支中发现的蛋白。作者发现藻类Zygnema circumcarinatum中PYL同源物具有基础的、独立于配体的PP2C抑制活性，说明这可能是一个古老的功能。同样，一个地钱受体拥有基础的活性，但其会被ABA进一步激活。作者假设通过对ABA的共选择来控制一个预先存在的PP2C-SnRK2依赖性脱水耐受性通路，从全有或全无的生存策略过渡到激素调节的竞争策略，该过程主要是通过使得结构上多样化的维管植物在干燥条件下持续性的生长，使其能够更加有效地开发他们新的生存环境。

通讯：Assaf Mosquna (https://plantscience.agri.huji.ac.il/assafmosquna)

研究方向：植物对环境胁迫的响应；植物中的ABA信号转导通路和相关的细胞、生理胁迫响应。

doi: https://doi.org/10.1073/pnas.1914480116

Journal: PNAS

First Published: November 19, 2019