Origin and co-evolution of land plant-fungal symbioses through the "greening of the Earth"

大约475年前陆生植物对陆地的殖民是地球历史上影响最深远的篇章之一。在陆地植物进化树中，Liverworts占据着关键的位置，各种各样的证据支持这些非维管植物是最基础的陆生光合生物，也是最早的陆地殖民者之一，大约在475年前。最近的分子遗传学证据支持这样一种观点，即苔类菌根的关联是一种基础和祖先特征，陆地植物从单一的共同祖先进化而来，在根进化之前与真菌伴侣形成共生关系。至少在过去的30年里，普遍的范式一直是AMfungi是所有植物-真菌共生体的祖先形式，与最早的陆地植物共同进化。AM关联菌是最常见的菌根类型，目前在超过70%的陆地植物物种中发现，包括简单和复杂的菌体苔类植物。然而，项目团队成员（MB， JGD， SP）报告的新证据表明，现存最基础的肝菌类群Haplomitriopsida与最基础的植物共生真菌类群endogonales完全相关。我们现在第一次有证据表明真菌群在它们与陆地植物的营养共生初期的身份。这为研究共生如何促进陆地生物圈的出现打开了一扇非凡的新窗口。我们的建议利用这些发现，解决了与植物“地球绿化”初始阶段有关的三个基本进化问题：(1)地物与内源性真菌物种之间的关联在功能上是否与AM真菌伴侣形成的关联相同？(2)真菌伴侣从兼性腐殖性内生内生真菌到专性生物营养性AM真菌的转变是由植物和真菌的互惠互利增加驱动的吗？(3)土壤有机质的积累是否有利于专性生物营养型am真菌而不是兼性腐养型内啡肽向植物提供矿物质营养？我们精心挑选了7种与真菌相关的苔类，提供了一个强大的模型系统光谱，适用于C交换、营养关系和真菌特异性的实验和定量功能分析。我们所有的目标生物都可以从孢子或胚芽中培养出来，为植物提供有或没有真菌共生体的植物。这为在3年的项目中定量真菌定殖对配子体生长、营养和生殖输出的影响提供了一个可靠的方法。我们的实验项目将在：(1)田间采集的成熟种群(和(2)由芽孢/孢子生长的共生与非共生植物上进行。田间收集的种群将用于从地茅到真菌伴侣的c分配和通过真菌向植物相互吸收营养的功能研究。来自芽孢/孢子的种群将用于调查真菌共生体对苔类生长和繁殖产量的净成本/收益，以及真菌伙伴的生物量和范围。分子鉴定和超结构研究将在这两组植物上进行，以确定真菌内共生体的身份，植物-真菌界面的性质，以及这些与功能和宿主特异性的关系。总体而言，该项目将为陆地植物和真菌之间的古老共生关系的黎明提供基础知识和理解，这种共生关系在陆地生态系统的进化中发挥了基础性作用——这一主题与NERC的地球系统科学主题高级挑战“改善相互作用的当前知识”密切相关

Colonization of the land by terrestrial plants ca. 475 Ma was one of themost far-reaching chapters in Earth's history. Liverworts occupy thepivotal position in the land plant evolutionary tree with a wide variety ofevidence supporting these non-vascular plants as the most basal terrestrialphotosynthetic organisms and amongst the earliest colonizers of the land ca.475 Ma. Recent molecular genetic evidence supports the view thatmycorrhiza-like associations in liverworts are a basal and ancestral trait,and land plants evolved from a single common ancestor that formed symbioticassociations with fungal partners before roots evolved. For at least the past 30 years, the prevailing paradigm has been that AMfungi are the ancestral form of all plant-fungal symbioses co-evolving withthe earliest land plants. AM associations are the most common type ofmycorrhiza, and are currently found in over 70% of land plant speciesincluding simple and complex thalloid liverworts. However, new evidencereported by members of the project team (MB, JGD, SP) has revealed that themost basal extant groups of liverworts, the Haplomitriopsida, exclusivelyform associations with the most basal group of plant-symbiotic fungi - theEndogonales. For the first time, we now have evidence pointing to theidentity of the fungal group at the dawn of their nutritional symbiosis withland plants. This opens a remarkable new window for functionalinvestigations into how the symbiosis facilitated the emergence of theterrestrial biosphere. Our proposal exploits these findings by addressing three fundamentalevolutionary questions relating to the initial phase of plants 'greening ofthe Earth':(1) Are the associations between liverworts and species of Endogonefunctionally equivalent to those formed with AM fungal partners? (2) Was the switching of fungal partners from facultatively saprotrophicEndogone to obligately biotrophic AM fungi through the evolutionary advanceof basal liverworts driven by increasing mutualistic benefits to the plantsand fungi?(3) Did the accumulation of soil organic matter favour obligately biotrophicAM fungi over facultatively saprotrophic Endogone in supplying mineralnutrients to the plants?We have carefully selected 7 liverwort species with fungal associations thatprovide a powerful spectrum of model systems amenable to experimentation andquantitative functional analyses of C exchange, nutrient relationships andfungal specificity. All of our target organisms can all be cultured eitherfrom spores or gemmae to provide plants with and without fungal symbionts.This provides a robust approach for enabling quantification of fungalcolonization on gametophyte growth, nutrition and reproductive output withina 3 yr project.Our experimental programme will be conducted on (1) mature field-collectedpopulations (and (2) symbiotic vs. asymbiotic plants grown fromgemmae/spores. Field collected populations will be used for functionalstudies of C-allocation from liverworts to their fungal partners andreciprocal uptake of nutrients into the plants via the fungi. Populationsfrom gemmae/spores will be used for investigating the net costs/benefits ofthe fungal symbionts on the growth and reproductive output of the liverwortsand the biomass and extent of the fungal partners. Molecular identificationand ultra-structural studies will be undertaken on both sets of plants toestablish the identity of the fungal endosymbionts, the nature of theplant-fungal interfaces, and how these relate to function and hostspecificity.Overall, this project will contribute fundamental knowledge andunderstanding to the dawn of an ancient symbiosis between land plants andfungi that played a founding role in the evolution of terrestrial ecosystems- a topic closely aligned to NERC's Earth System Science Theme high-levelchallenge "improving current knowledge of the interaction b