The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria.
The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria.
复制标题
DOI：
10.7554/elife.02478
复制
发表时间：
2014-06-16
期刊：
影响因子：
7.7
通讯作者：
Gowik U
中科院分区：
文献类型：
--
作者：
Mallmann J;Heckmann D;Bräutigam A;Lercher MJ;Weber AP;Westhoff P;Gowik U
C4光合作用代表了一个复杂性状的收敛进化的最显著的例子，其中包括数千个基因的表达模式的重新编程。解剖学、生理学和系统发育分析以及计算机模拟表明，光呼吸碳泵(称为C2光合作用)的建立是C4进化的先决条件。然而，目前还缺乏一个机制模型来解释C4和C2光合作用进化之间的紧密联系。在这里，我们通过对密切相关的C3、C3-C4和C4物种进行比较转录和生化分析，结合通过碳固定机制模型限制的通量平衡分析来解决这个问题。我们发现，C2光合作用在束鞘和叶肉细胞之间造成了氮代谢的失衡。重新平衡氮代谢需要至少部分类似于基本C4循环的逆转录反应。因此，我们的发现表明，C2光合作用代表着C4系统的预适应，C2系统的进化建立了重要的C4成分作为副作用。DOI：http://dx.doi.org/10.7554/eLife.02478.001环境压力有时会导致不同的有机体独立进化相同的特征。这种现象的一个戏剧性的例子被称为收敛进化，可以从植物在光合作用过程中将空气中的二氧化碳转化为淀粉的模式中看到。早期的植物生活在空气中二氧化碳含量较高的环境中。随着时间的推移，二氧化碳水平下降，因此植物进化出更有效的光合作用类型来应对。一种非常有效的光合作用，称为C4光合作用，本质上代表了一种二氧化碳浓缩机制。它已经在19个不同的开花植物家族中独立进化了至少62次。科学家们已经证明，一种不那么先进、效率较低的光合作用二氧化碳浓度，称为C2光合作用，是C4光合作用的垫脚石。众所周知，C4光合作用的进化需要改变数千个基因的表达模式，但从C2光合作用到C4光合作用的确切机制尚不清楚。为了更详细地探讨这一点，Mallmann，Heckmann等人。研究了黄花属植物，它与向日葵和紫锥花属于同一科。在相同的温室条件下，种植使用三种不同光合作用途径-C3光合作用、C4光合作用或两者之间的中间途径的植物，并比较它们的基因表达模式。计算机模拟被用来模拟依赖C2光合作用的植物的新陈代谢。根据模型，C2光合作用似乎改变了对光合作用至关重要的两种类型细胞之间的氮代谢平衡。为了重新平衡氮，表达了几个基因来触发氨循环机制。同样的基因在C4光合作用过程中被激活，这种循环机制包括C4过程的一部分。Mallmann，Heckmann等人的发现。这表明C4光合作用的最初步骤是为了防止氮素失衡而进化的。随着时间的推移，这种机制被增选为更有效的光合作用的一部分，这可能解释了为什么这么多不同的植物从C2光合作用进化到C4光合作用。DOI：http://dx.doi.org/10.7554/eLife.02478.002
C4 photosynthesis represents a most remarkable case of convergent evolution of a complex trait, which includes the reprogramming of the expression patterns of thousands of genes. Anatomical, physiological, and phylogenetic and analyses as well as computational modeling indicate that the establishment of a photorespiratory carbon pump (termed C2 photosynthesis) is a prerequisite for the evolution of C4. However, a mechanistic model explaining the tight connection between the evolution of C4 and C2 photosynthesis is currently lacking. Here we address this question through comparative transcriptomic and biochemical analyses of closely related C3, C3–C4, and C4 species, combined with Flux Balance Analysis constrained through a mechanistic model of carbon fixation. We show that C2 photosynthesis creates a misbalance in nitrogen metabolism between bundle sheath and mesophyll cells. Rebalancing nitrogen metabolism requires anaplerotic reactions that resemble at least parts of a basic C4 cycle. Our findings thus show how C2 photosynthesis represents a pre-adaptation for the C4 system, where the evolution of the C2 system establishes important C4 components as a side effect. DOI: http://dx.doi.org/10.7554/eLife.02478.001 Environmental pressures sometimes cause different organisms to independently evolve the same traits. A dramatic example of this phenomenon, which is called convergent evolution, can be seen in the modes used by plants to convert carbon dioxide from the air into starch during photosynthesis. Early plants existed in an environment with high levels of carbon dioxide in the air. Over time, carbon dioxide levels decreased, so plants evolved more efficient types of photosynthesis to cope. A very efficient type of photosynthesis, called C4 photosynthesis essentially represents a carbon dioxide concentration mechanism. It has evolved at least 62 times independently in 19 different families of flowering plants. Scientists have shown that a less advanced, low-efficiency version of photosynthetic carbon dioxide concentration, called C2 photosynthesis, is a stepping-stone to C4 photosynthesis. It is also known that the evolution of C4 photosynthesis required changes to the expression patterns of thousands of genes, but the exact mechanism that leads from C2 photosynthesis to C4 photosynthesis is not clear. To explore this in greater detail, Mallmann, Heckmann et al. studied plants from the genus Flaveria, which belongs to the same family as sunflowers and asters. Under identical greenhouse conditions, plants that use three different photosynthetic pathways—C3 photosynthesis, C4 photosynthesis, or an intermediate between the two—were grown and their gene expression patterns were compared. Computer simulations were used to model the metabolism of plants that relied on C2 photosynthesis. Based on the modeling, it appears that C2 photosynthesis shifts the balance of nitrogen metabolism between two types of cell that are critical to photosynthesis. To rebalance the nitrogen, several genes are expressed to trigger an ammonia recycling mechanism. The same genes are turned on during C4 photosynthesis, and this recycling mechanism include parts of the C4 process. The findings of Mallmann, Heckmann et al. suggest that the initial steps in C4 photosynthesis evolved to prevent nitrogen imbalance. Over time, this mechanism was co-opted to become part of a more efficient form of photosynthesis, which may explain why so many different plants evolved from C2 to C4 photosynthesis. DOI: http://dx.doi.org/10.7554/eLife.02478.002