Does physiological innovation change the fundamental relationships between growth and survival?

“活得快，死得早”是对摇滚明星和好莱坞演员的著名描述，但也概括了一个重要的生物学原理。生长和繁殖快的动植物更有可能被天敌或极端环境杀死。我们通常用能量来解释这种生物权衡：花在生长上的能量越多，就意味着花在防御敌人、获取基本资源或储存以在不利条件下生存的能量越少。这一解释的一个合乎逻辑的延伸是，如果可以用更少的能源实现同样的增长，那么就可以有更多的能源用于防御、资源捕获和储存，从而提高生存能力。然而，尽管这一预测对生物学至关重要，但仍未经验证。与祖先的C3型光合作用相比，在70多个植物谱系中，C4光合作用的进化提高了在高光和高温下的光合能量转换效率。为了了解光合效率的提高是如何影响生长的，我们开发了一种实验方法，能够比较数百种植物在相同环境条件下的生长情况。我们发现C4光合作用在促进更快生长的直接生理作用之外，C4叶片的密度出乎意料地低于C3，进一步提高了生长效率。这使得C4植物更大，更多的生长投入到根部，这使我们假设它们可能能够积累更多的储存，并且在干旱时比C3植物更好地获得水分。总之，这些假设的影响预计会增加反复落叶和干旱事件后植物的存活率。如果有实验证据支持，C3和C4植物之间的这些生态差异将对植物群落对环境变化和土地管理的响应具有重要的全球意义。我们建议使用三个大型比较实验来检验这些假设，利用我们最近在开发高通量实验筛选方法方面的进展。我们能够在相同的实验装置中测量数千种植物的生长，根与芽的分配，储存和存活，并开发了新的统计方法来分析大量的结果数据集。我们也是第一个成功应用代谢组学方法鉴定和量化多种野生植物物种的储存化合物的团队。我们提出的工作策略是将这些方法结合起来，研究70种生态上重要的草种在实验施加干旱或反复落叶的情况下的存活率，这些草种代表了C4光合作用及其C3姐妹分类群的7个独立进化起源。其他假设的生存机制将通过使用不同年龄的植物来操纵大小来测试。由于C4光合作用对植物水分利用也有直接的生理影响，我们将在干旱试验中通过减小气孔孔径对植物水力学进行详细测量。这三个实验的结果将使我们能够测试C4和C4物种中更大的储存、更深的生根、更低的植物水分利用和更大的植物尺寸对生存的相对重要性，并获得对该系统的整体理解。这项工作将增强我们对重大生理创新如何改变生长-生存关系并使植物探索新的表型空间的机制理解。在整个项目中，我们将与数学建模人员合作，确保实验产生的数据有助于开发关于全球植被如何储存碳和影响气候的改进模型。

"Live fast, die young" famously describes the wild excesses of rock stars and Hollywood actors, but also encapsulates an important biological principle. Animals and plants that grow and reproduce quickly are more likely to be killed by natural enemies or environmental extremes. We usually explain this biological trade-off in terms of energy: more energy spent on growth means less energy invested in defence against enemies, the capture of essential resources, or into stores for surviving adverse conditions. A logical extension of this explanation is that, if the same growth could be achieved using less energy, more would be available for defence, resource capture and storage, thereby increasing survival. However, this prediction remains untested, despite its central importance for biology.The evolution of C4 photosynthesis in more than seventy plant lineages has increased the efficiency of photosynthetic energy conversion at high light and hot temperatures, in comparison with the ancestral C3 type of photosynthesis. To understand how this increase in photosynthetic efficiency influences growth, we have developed an experimental approach capable of comparing growth among hundreds of plant species in the same environmental conditions. We have discovered that, as well as a direct physiological effect of C4 photosynthesis in promoting faster growth, C4 leaves are unexpectedly less dense than C3 ones, further increasing growth efficiency. This allows C4 plants to be larger, with more growth invested in roots, which leads us to hypothesize that they may be able to accumulate greater storage, and have better access to water during drought than their C3 counterparts. Together, these hypothesized effects are expected to increase plant survival following repeated defoliation and drought events. If supported by experimental evidence, these ecological differences between C3 and C4 plants would have important global scale implications for the responses of plant communities to environmental change and land management.We propose to test these hypothesis using three large comparative experiments, capitalizing on our recent advances in developing high-throughput experimental screening methods. We are able to measure growth, allocation to roots verses shoots, storage and survival on thousands of plants in the same experimental set-up, and have developed novel statistical methods to analyze the large resultant datasets. We are also the first group to successfully apply metabolomic methods to identify and quantify storage compounds across multiple wild plant species. Our strategy for the proposed work will be to combine these approaches, investigating survival of experimentally imposed drought or repeated defoliation in seventy ecologically important grass species, representing seven independent evolutionary origins of C4 photosynthesis and their C3 sister taxa. Alternative hypothesized survival mechanisms will be tested by using plants of different ages to manipulate size. Since C4 photosynthesis also has a direct physiological effect on plant water use, by reducing stomatal aperture, we will make detailed measurements of plant hydraulics during the drought experiment. Findings from the three experiments will allow us to test the relative importance to survival of greater storage, deeper rooting, lower plant water use, and greater plant size in C4 then C4 species, and to gain a holistic understanding of the system. The work will enhance our mechanistic understanding of how a major physiological innovation changed growth-survival relationships and enabled plants to explore new phenotypic space. Throughout the project, we will work with mathematical modelers to ensure that the experiments will generate data that are useful for developing improved models of how global vegetation stores carbon and influences climate.