Evolution of receptor signalling specificity for symbiosis and development

地球上复杂生命进化的一个关键事件是植物从水到陆地的转变。为了征服陆地环境，植物必须制定策略，利用最初原始的根前体来获取土壤养分。从那时起，植物就与提供营养的有益真菌共生。今天，丛枝菌根(AM)共生是地球上最常见的有益植物-真菌相互作用，有助于植物适应性、植物生物多样性和全球营养循环。然而，我们才刚刚开始揭示导致这种密切联系的建立的分子过程，并为现代作物育种控制它。Paszkowski研究小组发现，一种名为Dwarf 14 like(D14L)的α/β水解酶受体对于根际真菌对水稻的感知是必不可少的。这种受体的激活对于解除基因程序的阻碍是必要的，这些基因程序能够实现共生发展并诱导植物激素strigolacone的产生(Gutjahr等人，《科学》2015；Choi等人，NAT Commun 2020)。该受体存在于整个植物界，具有多种功能，包括检测烟雾成分karrikin和调节幼苗发育等。然而，来自不同植物物种的D14L受体在功能上并不一定相同。Paszkowski实验室最近发现，拟南芥的D14L同源物只能补充水稻d14L突变体的发育表型，但不能恢复AM共生。由于D14L受体存在于陆地植物中，包括早期的分叉植物，甚至轮藻，它们可能具有明显的和连续的多样化，以获得我们今天观察到的信号作用。我们现在希望重现进化轨迹，以便定义决定信号特异性的蛋白质特征，并更好地理解它们的出现。利用指数增长的基因组序列资源，我们在这里提出了一种高分辨率的元基因组学方法，使用和开发的计算工具明显优于传统做法。这包括开发新的算法步骤，使计算速度比以前的方法快10,000倍。在计算机实验中获得的结果随后在大米中进行功能验证，以确认它们与活体的相关性。这里产生的见解对于理解受体功能如何整合和指定不同的信号信号至关重要。通过这样做，这将开辟计算和植物生物学研究的新领域，并提供一个可以评估信号传递过程的其他例子的范例。

A key event in the evolution of complex life on earth is the transition of plants from water to land. To conquer the terrestrial environment plants had to develop strategies for the acquisition of soil nutrients with initially primitive root precursors. Ever since, plants have lived in symbioses with nutrient-delivering beneficial fungi. Today, the arbuscular mycorrhizal (AM) symbiosis is the most commonly occurring beneficial plant-fungal interaction on Earth, contributing to plant fitness, plant biodiversity and global nutrient cycles. Yet, we are only beginning to unveil the molecular processes leading to the establishment of this intimate association and to control it for modern crop breeding. The Paszkowski group has found that an alpha/beta hydrolase receptor, called DWARF 14 LIKE (D14L), is essential for fungal perception of rice in the rhizosphere. The activation of this receptor is necessary for the unblocking of genetic programmes that enable symbiosis development and induce production of the phytohormone strigolactone (Gutjahr et al., Science 2015; Choi et al., Nat Commun 2020). The receptor is present across the plant kingdom and serves multifunctional roles, including the detection of the smoke constituent karrikin and the modulation of seedling development amongst others. However, D14L receptors from different plant species are functionally not necessarily equivalent. The Paszkowski lab recently found that the D14L homologue from Arabidopsis thaliana was only able to complement the developmental phenotype of rice d14l mutants, but failed to restore AM symbiosis.As D14L receptors are present across terrestrial plants, including early divergent plants and even Charophyte algae, they may have distinctly and successively diversified to acquire the signalling roles we observe today. We now wish to reproduce the evolutionary trajectory in order to define the protein features that condition signalling specificity, and to better understand their emergence. Exploiting the exponentially growing genome sequence resource, we propose here a high-resolution metagenomics approach, employing and developing computational tools that are significantly superior relative to conventional practices. This includes the development of new algorithmic steps enabling 10,000-fold computational acceleration compared to previous approaches. Results obtained from these in silico efforts are then functionally validated in rice to confirm their relevance in vivo.Insights generated here are vital for understanding how receptor functioning integrates and specifies different signalling cues. In doing so, this will open up new areas of research in computational and plant biology and provide a paradigm for which other examples of signalling processes can be assessed.