Ruperti Benedetto, Botton Alessandro, Populin Francesca, Eccher Giulia, Brilli Matteo, Quaggiotti Silvia, Trevisan Sara, Cainelli Nadia, Guarracino Paola, Schievano Elisabetta, Meggio Franco
Department of Agronomy, Food, Natural Resources, Animals and Environment, University of Padova, Legnaro, Italy.
Interdepartmental Research Centre for Viticulture and Enology, University of Padova, Conegliano, Italy.
Front Plant Sci. 2019 Mar 26;10:339. doi: 10.3389/fpls.2019.00339. eCollection 2019.
Studies on model plants have shown that temporary soil flooding exposes roots to a significant hypoxic stress resulting in metabolic re-programming, accumulation of toxic metabolites and hormonal imbalance. To date, physiological and transcriptional responses to flooding in grapevine are poorly characterized. To fill this gap, we aimed to gain insights into the transcriptional and metabolic changes induced by flooding on grapevine roots (K5BB rootstocks), on which cv Sauvignon blanc ( L.) plants were grafted. A preliminary experiment under hydroponic conditions enabled the identification of transiently and steadily regulated hypoxia-responsive marker genes and drafting a model for response to oxygen deprivation in grapevine roots. Afterward, over two consecutive vegetative seasons, flooding was imposed to potted vines during the late dormancy period, to mimick the most frequent waterlogging events occurring in the field. Untargeted transcriptomic and metabolic profiling approaches were applied to investigate early responses of grapevine roots during exposure to hypoxia and subsequent recovery after stress removal. The initial hypoxic response was marked by a significant increase of the hypoxia-inducible metabolites ethanol, GABA, succinic acid and alanine which remained high also 1 week after recovery from flooding with the exception of ethanol that leveled off. Transcriptomic data supported the metabolic changes by indicating a substantial rearrangement of primary metabolic pathways through enhancement of the glycolytic and fermentative enzymes and of a subset of enzymes involved in the TCA cycle. GO and KEGG pathway analyses of differentially expressed genes showed a general down-regulation of brassinosteroid, auxin and gibberellin biosynthesis in waterlogged plants, suggesting a general inhibition of root growth and lateral expansion. During recovery, transcriptional activation of gibberellin biosynthetic genes and down-regulation of the metabolic ones may support a role for gibberellins in signaling grapevine rootstocks waterlogging metabolic and hormonal changes to the above ground plant. The significant internode elongation measured upon budbreak during recovery in plants that had experienced flooding supported this hypothesis. Overall integration of these data enabled us to draft a first comprehensive view of the molecular and metabolic pathways involved in grapevine's root responses highlighting a deep metabolic and transcriptomic reprogramming during and after exposure to waterlogging.
对模式植物的研究表明，土壤短期淹水会使根系遭受严重的缺氧胁迫，从而导致代谢重新编程、有毒代谢物积累和激素失衡。迄今为止，葡萄对淹水的生理和转录反应的特征尚不明确。为了填补这一空白，我们旨在深入了解淹水对葡萄根系（K5BB砧木）诱导的转录和代谢变化，赤霞珠（L.）植株嫁接到该砧木上。水培条件下的初步实验能够鉴定出瞬时和稳定调控的缺氧响应标记基因，并绘制出葡萄根系对缺氧响应的模型。之后，在连续两个生长季节中，在休眠后期对盆栽葡萄进行淹水处理，以模拟田间最常见的涝灾事件。采用非靶向转录组学和代谢谱分析方法，研究葡萄根系在缺氧暴露期间及胁迫解除后的早期恢复反应。最初的缺氧反应表现为缺氧诱导代谢物乙醇、γ-氨基丁酸、琥珀酸和丙氨酸显著增加，除乙醇水平趋于平稳外，淹水恢复1周后这些代谢物水平仍保持较高。转录组数据通过表明初级代谢途径通过糖酵解和发酵酶以及参与三羧酸循环的一部分酶的增强而发生大量重排，支持了代谢变化。对差异表达基因的GO和KEGG通路分析表明，淹水植物中油菜素内酯、生长素和赤霉素生物合成普遍下调，这表明根系生长和侧向扩展受到普遍抑制。在恢复过程中，赤霉素生物合成基因的转录激活和代谢基因的下调可能支持赤霉素在向地上部植株传递葡萄砧木涝渍代谢和激素变化信号方面的作用。在经历淹水的植株恢复期间芽萌发时测得的显著节间伸长支持了这一假设。这些数据的整体整合使我们能够初步全面了解葡萄根系响应所涉及的分子和代谢途径，突出了淹水期间和之后的深度代谢和转录组重编程。
