National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.
College of Horticulture and Landscape Architecture, Yangzhou University, Yangzhou, 225009, China.
Plant Physiol. 2024 Sep 2;196(1):634-650. doi: 10.1093/plphys/kiae327.
Citrus is one of the most important fruit crop genera in the world, but many Citrus species are vulnerable to cold stress. Ichang papeda (Citrus ichangensis), a cold-hardy citrus species, holds great potential for identifying valuable metabolites that are critical for cold tolerance in Citrus. However, the metabolic changes and underlying mechanisms that regulate Ichang papeda cold tolerance remain largely unknown. In this study, we compared the metabolomes and transcriptomes of Ichang papeda and HB pummelo (Citrus grandis "Hirado Buntan", a cold-sensitive species) to explore the critical metabolites and genes responsible for cold tolerance. Metabolomic analyses led to the identification of common and genotype-specific metabolites, consistent with transcriptomic alterations. Compared to HB pummelo under cold stress, Ichang papeda accumulated more sugars, flavonoids, and unsaturated fatty acids, which are well-characterized metabolites involved in stress responses. Interestingly, sphingosine and chlorogenic acid substantially accumulated only in Ichang papeda. Knockdown of CiSPT (C. ichangensis serine palmitoyltransferase) and CiHCT2 (C. ichangensis hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyltransferase2), two genes involved in sphingosine and chlorogenic acid biosynthesis, dramatically decreased endogenous sphingosine and chlorogenic acid levels, respectively. This reduction in sphingosine and chlorogenic acid notably compromised the cold tolerance of Ichang papeda, whereas exogenous application of these metabolites increased plant cold tolerance. Taken together, our findings indicate that greater accumulation of a spectrum of metabolites, particularly sphingosine and chlorogenic acid, promotes cold tolerance in cold-tolerant citrus species. These findings broaden our understanding of plant metabolic alterations in response to cold stress and provide valuable targets that can be manipulated to improve Citrus cold tolerance.
柑橘是世界上最重要的水果作物之一，但许多柑橘物种易受低温胁迫的影响。宜昌橙（Citrus ichangensis）是一种耐寒的柑橘物种，具有鉴定对柑橘耐寒性至关重要的有价值代谢物的巨大潜力。然而，宜昌橙耐寒性的代谢变化和调控机制在很大程度上尚不清楚。在这项研究中，我们比较了宜昌橙和 HB 柚（Citrus grandis "Hirado Buntan"，一种对低温敏感的物种）的代谢组和转录组，以探讨与耐寒性相关的关键代谢物和基因。代谢组学分析导致了共同和基因型特异性代谢物的鉴定，与转录组变化一致。与低温胁迫下的 HB 柚相比，宜昌橙积累了更多的糖、类黄酮和不饱和脂肪酸，这些都是参与应激反应的特征代谢物。有趣的是，只有在宜昌橙中，神经酰胺和绿原酸大量积累。下调两个参与神经酰胺和绿原酸生物合成的基因 CiSPT（C. ichangensis serine palmitoyltransferase）和 CiHCT2（C. ichangensis hydroxycinnamoyl-CoA:shikimate hydroxycinnamoyltransferase2），分别显著降低了内源神经酰胺和绿原酸的水平。这种神经酰胺和绿原酸的减少显著降低了宜昌橙的耐寒性，而这些代谢物的外源应用则提高了植物的耐寒性。总之，我们的研究结果表明，更多谱代谢物的积累，特别是神经酰胺和绿原酸，促进了耐寒柑橘物种的耐寒性。这些发现拓宽了我们对植物代谢变化响应低温胁迫的理解，并提供了有价值的靶点，可以通过操纵这些靶点来提高柑橘的耐寒性。
