Summary
Mature leaf area (LA) is a showcase of diversity – varying enormously within and across species, and associated with the productivity and distribution of plants and ecosystems. Yet, it remains unclear how developmental processes determine variation in LA.
We introduce a mathematical framework pinpointing the origin of variation in LA by quantifying six epidermal ‘developmental traits’: initial mean cell size and number (approximating values within the leaf primordium), and the maximum relative rates and durations of cell proliferation and expansion until leaf maturity. We analyzed a novel database of developmental trajectories of LA and epidermal anatomy, representing 12 eudicotyledonous species and 52 Arabidopsis experiments.
Within and across species, mean primordium cell number and maximum relative cell proliferation rate were the strongest developmental determinants of LA. Trade-offs between developmental traits, consistent with evolutionary and metabolic scaling theory, strongly constrain LA variation. These include trade-offs between primordium cell number vs cell proliferation, primordium mean cell size vs cell expansion, and the durations vs maximum relative rates of cell proliferation and expansion. Mutant and wild-type comparisons showed these trade-offs have a genetic basis in Arabidopsis.
Analyses of developmental traits underlying LA and its diversification highlight mechanisms for leaf evolution, and opportunities for breeding trait shifts.
摘要
叶片大小(即叶面积)是植物最基本目最重要的持征，直接影响作物产量、植物分布和生态系统生产力。叶面积能够充分反映物种多样性，在种内和种间存在着巨大的变异，然而，叶面积的大小如何被发育过程调控的原理，尚未明确。
本研究提出了一个新的理论框架，通过量化表皮的六个“发育性状”来分析叶面积变异的根源。这六个动态发育性状主要包括:初始细胞大小和细胞数量(理论上可以视为叶原基细胞的大小和数量)、细胞增殖(cell proliferation)的最大相对速率和持续时间、以及细胞扩展(cell expansion)最大相对速率和持续时间。研究模拟了从叶原基到成熟叶片的发育过程，并分析了12种双子叶植物和52个拟南芥基因型实验的叶片表皮发育过程。
研究表明，无论是在种间还是种内，叶原基细胞数量和细胞增殖速率是叶面积发育的主要决定因素。发育性状之间存在显著权衡关系，这些权衡很大程度上约束了叶面积的变异范围，而且这种权衡关系符合进化原理和异速生长理论的基本推断。具体来说，存在四个主要的权衡关系：叶原基细胞数量与细胞增殖之间的权衡、叶原基细胞大小与细胞扩展之间的权衡、细胞增殖最大相对速率与持续时间之间的权衡、细胞扩展最大相对速率与持续时间之间的权衡。通过拟南芥突变体和野生型的比较分析，发现这些发育权衡具有遗传学基础，这样就可通过基因来调节这些权衡关系，进而获得理想的叶面积。
该研究提出了“发育性状”(developmental traits)，阐明了叶面积发育过程中的基本原理，揭示了叶片大小多样性 及其进化机制，为下一代植物育种开辟了新的方向。
