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——这是其他生命所依赖的。当植物不受环境胁迫时，光合作用很好，但当植物太热或干旱胁迫时，这个过程就变得低效了。植物在环境胁迫下进化出了两种主要的光合作用途径：CAM和C4光合作用。C4和CAM都经历了多次进化，人们认为C4是为了应对高温而进化的，CAM是为了应对干旱而进化的。同样，这两种途径被认为在细胞和遗传水平上是不相容的。然而，已经发现了一种C4-CAM植物：马齿苋，它通常进行C4光合作用，但在干旱情况下进行CAM。本项目旨在了解C4-CAM光合系统的功能和生态意义。研究小组将发现C4-CAM在葡状叶中进化了多少次，并将确定两种途径在叶子中的空间结构。他们将确定调控这两种途径的基因，并将C4-CAM物种的生态范围与没有这种特征的近亲进行比较。最后，他们将调查其他植物，以确定这种新型光合作用类型的其他起源。这项研究可能有助于作物改良——例如，将C4基因改造为水稻，将CAM基因改造为杨树。C4-CAM作物在水资源充足时可能高产，但在缺水时却抗旱。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光合作用是经过多次进化的两种代谢途径。尽管生物化学上相似，但每条途径都需要一套独特的解剖特征才能有效地工作，传统观点认为这些特征是拮抗的，因此有利于高效C4的解剖结构同时会不利于CAM的代谢。然而，这种被广泛接受的观点并不适用于马齿苋，它是目前已知的唯一在一片叶子中同时进行C4和CAM循环的植物。最近的研究表明，马齿苋的祖先是一种兼性CAM植物，在进化C4系统的同时至少三次保持CAM能力。拟议的研究将验证这一假设，并将马齿苋作为研究C4和CAM途径进化连通性的模型谱系。本项目旨在：1)确认马齿苋所有主要系中兼性CAM的存在，并在代表所有C4起源的7个种中表征CAM和C4的生化循环及差异基因表达；2)利用原位杂交和蛋白质免疫定位技术，确定叶片内C4和CAM循环的空间构型；3)利用最近设计的靶向基因富集诱饵（HybSeq）对整个马蹄苋的关键光合（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趋同分子适应；4) C4-CAM Portulaca和C3-CAM相关谱系所占气候包络的特征和对比；5)启动系统发育生理学调查，在其他分支中发现更多的C4-CAM植物。该奖项由美国国家科学基金会生物学理事会联合资助，由综合生物系统部的综合生态生理学、环境生物学部的系统学和生物多样性科学以及新兴领域共同资助。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值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.