Molecular attributes of the tropical tree Avicennia schaueriana involved in the response and tolerance to low temperatures

Abstract

Mangroves are coastal ecosystems of great socioenvironmental importance that are highly threatened by human activities. Mangrove trees live under harsh environmental conditions, which makes them sensitive to extreme weather events, particularly freezing events. Such events are unpredictable and have catastrophic consequences for mangrove trees; therefore, understanding and anticipating the impacts of such events are essential for directing future mitigation measures. Freezing cold currently limits the distribution of mangroves to tropical and subtropical latitudes worldwide. Mangrove trees are seriously affected by freezing conditions and suffer severe metabolic fluctuations due to photosystem and cellular structure damage. However, land plants more broadly have developed sophisticated mechanisms of resistance to freezing during their evolution, and the central molecular mechanisms involved in this process are consistent. However, the known information is restricted to models of herbaceous plants, such as Arabidopsis thaliana, that are native to temperate habitats, and there is a research gap regarding tropical trees such as mangroves. This work aimed to improve the understanding of the molecular aspects of the response and tolerance to freezing in mangrove trees using Avicennia schaueriana as a model. This species occurs within the colder range limits of South American mangroves and shows evidence of the existence of two functional groups that are locally adapted to the equatorial (EQ) and subtropical (ST) portions of the Brazilian coast. We investigated the transcriptional profiles of seedlings from both functional groups under freezing shock (-4{degrees}C) in a time series. We analyzed transcriptomic data by combining differential expression, coexpression network and protein interaction data. Our results allowed us to describe the profile of the molecular response of A. schaueriana to freezing and the divergence in the behavior of the EQ and ST functional groups. In EQ plants, the response strongly depended on the action of abscisic acid (ABA) and stress signals throughout the experiment. Notably, ABA negatively affects plant growth and promotes the accumulation of carotenoids, anthocyanins and lipids through chlorophyll degradation. On the other hand, in the ST, there were fewer hormones active in the process of primary growth maintenance and metabolic normalization. The accumulation of substances is mainly based on sucrose, anthocyanin and lipid levels, and lipid synthesis is not dependent on chlorophyll degradation. Based on these results, we hypothesize that susceptibility to freezing damage is greater in EQ mangroves than in ST mangroves. Therefore, we recommend that this fact be considered when managing this species, especially at higher latitudes, which are more prone to lower temperatures and extreme freezing events.