Adaptive diversification of growth allometry in the plant Arabidopsis thaliana

Seed plants vary tremendously in size and morphology. However, variation and covariation between plant traits may at least in part be governed by universal biophysical laws and biological constants. Metabolic Scaling Theory (MST) posits that whole-organismal metabolism and growth rate are under stabilizing selection that minimizes the scaling of hydrodynamic resistance and maximizes the scaling of resource uptake. This constrains variation in physiological traits and in the rate of biomass accumulation, so that they can be expressed as mathematical functions of plant size with near constant allometric scaling exponents across species. However, observed variation in scaling exponents questions the evolutionary drivers and the universality of allometric equations. We have measured growth scaling and fitness traits of 451 Arabidopsis thaliana accessions with sequenced genomes. Variation among accessions around the scaling exponent predicted by MST correlated with relative growth rate, seed production and stress resistance. Genomic analyses indicate that growth allometry is affected by many genes associated with local climate and abiotic stress response. The gene with the strongest effect, PUB4, has molecular signatures of balancing selection, suggesting that intraspecific variation in growth scaling is maintained by opposing selection on the trade-off between seed production and abiotic stress resistance. Our findings support a core MST prediction and suggest that variation in allometry contributes to local adaptation to contrasting environments. Our results help reconcile past debates on the origin of allometric scaling in biology, and begin to link adaptive variation in allometric scaling to specific genes.

种子植物在体型与形态上存在显著差异。然而植物性状间的变异与协变关系，至少在一定程度上受普适生物物理定律与生物学常数的调控。代谢缩放理论（Metabolic Scaling Theory, MST）提出：全生物代谢与生长速率处于稳定选择作用之下，这种选择会最小化流体动力学阻力的缩放效应，并最大化资源摄取的缩放效应。这限制了生理性状与生物量积累速率的变异，使得这些性状可被表示为植物体型的数学函数，且在不同物种间具有近乎恒定的异速缩放指数。然而，实际观测到的缩放指数变异，对异速方程的进化驱动力与普适性提出了质疑。本研究对451个已测序基因组的拟南芥（Arabidopsis thaliana）生态型的生长缩放与适合度性状进行了测定。各生态型相对于MST预测的缩放指数的变异，与相对生长速率、种子产量及抗逆性存在相关性。基因组分析表明，生长异速性受众多与本地气候及非生物胁迫响应相关的基因调控。效应最强的基因PUB4具有平衡选择的分子特征，这表明生长缩放的种内变异，是通过对种子产量与非生物抗逆性之间权衡的反向选择得以维持的。本研究结果支持MST的核心预测，并表明异速性变异有助于物种适应迥异的本地环境。本研究结果有助于解决此前生物学领域关于异速缩放起源的诸多争论，并首次将异速缩放的适应性变异与特定基因关联起来。