Evolution and function of an unusual photosynthetic metabolism: Portulaca, the C4-CAM plant

植物进行光合作用，将二氧化碳和阳光转化为储存的化学能-碳水化合物-生命的其余部分依赖于此。当植物没有暴露在环境压力下时，光合作用效果很好，但当植物太热或干旱压力时，这个过程就会变得效率低下。植物已经进化出两条主要的可供选择的光合作用途径来响应环境胁迫，即CAM和C4光合作用。C4和CAM各自进化了多次，C4被认为是对高温的反应，而CAM是对干旱的反应。同样，这两条途径被认为在细胞和遗传水平上是不相容的。然而，人们已经发现了一种C4-CAM植物：马齿苋，它正常进行C4光合作用，但在干旱条件下进行CAM。本项目旨在了解C4-CAM光合作用系统的功能和生态意义。研究小组将发现C4-CAM在Portulaca进化了多少次，并将确定叶内两条路径的空间构型。他们将确定控制这两条途径的基因，并将C4-CAM物种的生态范围与没有这一特征的近亲进行比较。最后，他们将调查其他植物，以确定这种新的光合作用类型的其他来源。这项研究可能有助于作物改良--例如，努力将C4基因改造成水稻，将CAM基因改造成杨树。C4-CAM作物在缺水时可能高产，但在缺水时耐旱。此外，该奖项将支持广泛的教育活动，包括博士后和研究生培训、本科研究、高中教师培训和课程开发。C4和CAM光合作用是两种多次进化的新陈代谢途径。尽管生物化学相似，但每条途径都需要一套独特的解剖学特征才能有效工作，传统观点认为这些特征是拮抗的，因此促进高效C4的解剖结构同时也会对CAM的新陈代谢不利。然而，这种被广泛接受的观点不能适应马齿莲，马齿莲是目前已知的唯一在一片叶子内同时运行C4和CAM循环的植物。最近的研究表明，祖先马齿苋是一种兼性的CAM植物，在进化出C4系统的同时保持了至少三次的CAM能力。这项拟议的研究将检验这一假说，并将马齿莲发展为研究C4和CAM途径进化连通性的模型谱系。本项目的目标是：1)确认兼性CAM在马齿苋所有主要谱系中的存在，并表征代表所有C4起源的7个物种的CAM和C4生化循环和差异基因表达；2)利用原位杂交和蛋白质免疫定位，确定叶片中C4和CAM循环的空间构型；3)利用最近设计的靶向基因浓缩诱饵(HybSeq)对马齿苋中关键的光合作用(和其他)基因进行测序，以提高系统发育分辨率并分析整个群体的收敛分子适应；4)表征和对比与C4-CAM和C3相关谱系有关的气候包络；和5)启动基于系统发育的生理调查，以发现其他分支中更多的C4-CAM植物。该奖项由美国国家科学基金会生物局由综合组织系统司的综合生态生理学、环境生物学司的系统学和生物多样性科学以及新兴前沿共同资助。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

Plants perform photosynthesis to transform carbon dioxide and sunlight into stored chemical energy - carbohydrates - that the rest of life relies upon. Photosynthesis works well when plants are not exposed to environmental stress, but when plants are too hot, or drought stressed, this process becomes inefficient. Plants have evolved two main alternative photosynthetic pathways in response to environmental stresses, CAM and C4 photosynthesis. C4 and CAM have each evolved many times, and it has been thought that C4 evolved in response to hot temperatures and CAM in response to drought. Similarly, these two pathways were assumed to be incompatible at cellular and genetic levels. However, a C4-CAM plant has been discovered: Portulaca, which performs C4 photosynthesis normally, but performs CAM under drought. This project aims to understand the function and ecological significance of a C4-CAM photosynthetic system. The research team will discover how many times C4-CAM evolved in Portulaca, and will identify the spatial configuration of both pathways within the leaf. They will identify the genes that regulate both pathways, and will compare the ecological ranges of C4-CAM species with relatives that do not have this trait. Finally, they will survey other plants to identify additional origins of this novel photosynthesis type. This research may contribute to crop improvement- for example, efforts to engineer C4 into rice, and CAM into poplar. A C4-CAM crop could be highly productive when water is prevalent, but drought-resistant when water is scarce. In addition, this award will support a broad range of educational activities, including post-doctoral and graduate student training, undergraduate research, and high school teacher training and curriculum development.C4 and CAM photosynthesis are two metabolic pathways that have evolved multiple times. Though biochemically similar, each pathway requires a unique suite of anatomical characters in order to work efficiently, and conventional wisdom holds that these characters are antagonistic, such that anatomy that facilitates efficient C4 will simultaneously disadvantage a CAM metabolism. This widely accepted view cannot, however, accommodate Portulaca, the only plants currently known to operate both C4 and CAM cycles within a single leaf. Recent work suggests that ancestral Portulaca was a facultative CAM plant, and evolved a C4 system while maintaining CAM capability at least three times. The proposed research will test this hypothesis and develop Portulaca as a model lineage for investigating the evolutionary connectivity of C4 and CAM pathways. This project aims to: 1) confirm the existence of facultative CAM in all major Portulaca lineages, and characterize CAM and C4 biochemical cycles and differential gene expression in 7 species representing all C4 origins; 2) identify the spatial configuration of C4 and CAM cycles within the leaf, using in situ hybridization and protein immunolocalization; 3) utilize recently designed targeted gene enrichment baits (HybSeq) to sequence key photosynthetic (and other) genes from across Portulaca to improve phylogenetic resolution and analyze convergent molecular adaptation across the group; 4) characterize and contrast the climatic envelopes occupied by C4-CAM Portulaca and C3-CAM related lineages; and 5) initiate phylogenetically-informed physiological surveys to discover additional C4-CAM plants in other clades.This award was co-funded in the Biology Directorate of NSF by Integrative Ecological Physiology in the Integrative Organismal Systems Division, Systematics and Biodiversity Science in the Division of Environmental Biology, and Emerging Frontiers.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.