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A king and vassals' tale: Molecular signatures of clonal integration in Posidonia oceanica under chronic light shortage
Journal of Ecology ( IF 5.3 ) Pub Date : 2020-07-27 , DOI: 10.1111/1365-2745.13479
Miriam Ruocco 1 , Laura Entrambasaguas 1 , Emanuela Dattolo 1 , Alfonsina Milito 1, 2 , Lazaro Marín‐Guirao 1, 3 , Gabriele Procaccini 1
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  1. Under unfavourable conditions, clonal plants benefit from physiological integration among ramets, sharing resources and information. Clonal integration can buffer against environmental changes and lets the plant clone work as a ‘macro’ organism. Molecular signals that regulate this phenomenon are completely unknown in marine plants.
  2. Here we present a first comprehensive study providing insights into the metabolic role of different types of ramets (i.e. apical vs. vertical) in the foundation species Posidonia oceanica. Plants were exposed to 80% diminishing irradiance level (LL) in a controlled mesocosm system. Subsequent multiscale variations in whole transcriptome expression, global DNA methylation level, photo‐physiology, morphology and fitness‐related traits, were explored at different exposure times. We tested the hypothesis that vertical shoots (the ‘vassals’) can provide vital resources to apical shoots (the ‘kings’) under energy shortage, thus safeguarding the whole clone survival.
  3. Whole transcriptome analysis of leaves and shoot‐apical meristems (SAMs) emphasized signatures of molecular integration among ramets, which strongly correlated with higher organization‐level responses. In both shoots types, the exposure to LL resulted in a growth slowdown throughout the experiment, which started from immediate signals in SAMs. In apical shoots, this was linked to an acclimative response, where they were suffering a mild stress condition, while in vertical ones it fell in a more severe stress response. Yet, they suffered from sugar starvation and showed a clear cellular stress response in terms of protein refolding and DNA repair mechanisms. Several epigenetic mechanisms modulated the observed gene‐expression patterns and the cross‐talk between DNA methylation and the cellular energetic status appeared to regulate shoot metabolism under LL.
  4. Synthesis. Our results demonstrate a high level of specialization of integrated ramets within seagrass clones and a ‘division of labour’ under adverse conditions. Vertical shoots appear to do ‘most of the job’ especially in terms of resource providing, whereas activated functions in apical shoots were restricted to few important processes, according to an ‘energy‐saving’ strategy. The response of vertical shoots could be seen as a ‘sacrificing response’ allowing the survival of ‘the king’ that is key for ensuring propagation and population maintenance, and for the colonization of new environments.


中文翻译:

国王与诸侯的故事:慢性光短缺下大洋波塞冬克隆克隆整合的分子特征

  1. 在不利条件下,克隆植物受益于分株之间的生理整合,共享资源和信息。克隆整合可以缓冲环境变化,并使植物克隆像“宏”生物一样起作用。调节这种现象的分子信号在海洋植物中是完全未知的。
  2. 在这里,我们提出了第一个全面的研究,提供了对基础物种波西多尼亚大洋洲中不同类型的分株(即顶端与垂直)的代谢作用的见解。在受控的中观宇宙系统中,将植物暴露于80%的降低辐照度(LL)。在不同的暴露时间,探索了整个转录组表达,总体DNA甲基化水平,光生理学,形态学和适应性相关性状的随后多尺度变化。我们测试了以下假设,即垂直枝条(“附庸国”)可以在能源短缺的情况下为顶端枝条(“国王”)提供重要资源,从而保护整个克隆的生存。
  3. 叶片和茎尖分生组织(SAMs)的整个转录组分析强调了分株间分子整合的特征,这与较高的组织水平响应密切相关。在这两种类型的芽中,暴露于LL导致整个实验的生长减慢,这从SAM中的即时信号开始。在顶端的芽中,这与适应性反应有关,在这种情况下,它们承受的是轻度的胁迫条件,而在垂直的芽中,其适应性更强。然而,他们患有糖饥饿症,并且在蛋白质复性和DNA修复机制方面表现出明显的细胞应激反应。
  4. 综合。我们的结果表明,在不利条件下,海草克隆中整合分株的高度专业化和“分工”。根据“节能”策略,垂直枝条似乎完成了“大部分工作”,尤其是在资源提供方面,而顶端枝条的激活功能仅限于几个重要的过程。垂直芽的反应可被视为“牺牲反应”,使“国王”得以生存,这是确保繁殖和种群维持以及新环境定殖的关键。
更新日期:2020-07-27
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