Spatial Pattern of Genetic Diversity and Demographic History Revealed by Population Genomic Analysis: Resilience to Climate Fluctuations of Acer truncatum Bunge

As functional units of heredity, plant genetic resources are genetic materials of actual or potential value [1] and are important basic materials for genetic breeding [2]. Better understanding of the genetic diversity and spatial pattern of a species is useful for evaluating its genetic resources and provides a theoretical basis for development of conservation strategies and sustainable innovative utilization of genetic resources. Global climate oscillations and geological events have a crucial impact on the distribution pattern of species, further driving genetic differentiation and shaping current spatial patterns [3,4,5,6]. Many paleo-species disappeared during and following the Pliocene (5–1.7 Million years ago) as a result of climatic deterioration. Plants in central Europe had little opportunity to migrate southward due to the east–west structure of the mountains. In contrast, vast areas in China and wide-open plains of eastern Asia offered plants the opportunity to retreat before the advancing ice sheets [7]. During the Quaternary glaciation, extreme low temperature forced some species to survive in some refuges [8,9], while sheltered plants could expand and resettled under more favorable conditions during the inter-glacial or post-glacial warming. Ginkgo biloba L. survived in three refuges located in eastern, southern and southwestern China during the glacial period and expanded towards the northern regions during the post-glacial periods [10]. Loropetalum chinense var. rubrum Yieh contracted within the refuge in Nanling of China during the last glacial maximum and then expanded northward [11]. Therefore, the current distribution pattern of species does not represent their historical distribution. Inferring the demographic history of species based on genetic information can provide insights into important historical events, including population bottlenecks, expansions and contractions. The unique evolutionary history of each species affects the level and distribution of genetic diversity [12,13]. Thus, understanding the demographic history of species and exploring the mechanisms of the spatial patterns of genetic diversity are essential to the development of conservation strategies for plants’ genetic resources.

Acer truncatum Bunge, a deciduous tree of the genus Acer in Sapindaceae, is widely distributed in northern China, as well as in Russia, Japan and Korea [7,14]. A. truncatum is not only of ornamental value but also of timber and medicinal value. With its beautiful crown shape and autumn foliage color, it is an excellent landscape species suitable for use as a shade and street tree [15]. The wood of A. truncatum is of good quality and can be used in construction, furniture and sculpture, etc., and its bark fiber can also be used in papermaking and replacing cotton [16,17]. The leaves are rich in flavonoids, chlorogenic acid, vitamin E and tannins [18,19,20] and the bark contains anti-tumor active substances such as catechin, procyanidin B2/B3, and procyanidin C1/C2 [21]. Furthermore, the seed of A. truncatum contains 5%–6% nervonic acid [22], which is utilized to treat various brain diseases, such as Zellweger syndrome, Adrenoleukodystrophy and Alzheimer [23,24,25,26]. The discovery of nervonic acid in A. truncatum was regarded as an epoch-making outstanding achievement in the field of human brain medicine.

A. truncatum has been planted on a large scale as an economic tree species since 1970 and was approved as a new resource for food by the National Ministry of Health in 2011 (http://www.nhc.gov.cn/sps/s7891/201103/cffd9def6007444ea271189c18063b54.shtml, access on 18 March 2024). In 2020, A. truncatum was listed as an important species in the National Reserve Forest Project for development and utilization. At present, nearly 80 institutes have carried out research on A. truncatum, including cultivation, breeding and active substance extraction [27]. A. truncatum is a national treasure species in China, which is highly favored by the market, with increasing demand and expanding planting bases. However, the natural populations of A. truncatum have been seriously threatened due to anthropogenic interference and habitat degradation, and it has been listed as a near-threatened species in China Species Red List [28]. Recent studies reported the genetic diversity of A. truncatum is high. Qiao et al. [29] revealed a high genetic diversity in 15 populations of A. truncatum (H = 0.252, I = 0.394) from eight provinces, using 240 sequence-related amplified polymorphism (SRAP) markers. The study of 250 individuals in A. truncatum from nine different regions using 11 simple sequence repeat (SSR) markers revealed a high genetic diversity of population (H_e = 0.719, I = 2.05) [30]. However, as one of the Acer species distributed in the northern margin, it is unclear that how A. truncatum has responded to climate oscillations through genetic diversity and demographic history of natural populations over its long evolutionary history. Therefore, studies on genetic diversity of A. truncatum can provide theoretical guidance for the conservation and sustainable utilization of genetic resources.

Single nucleotide polymorphism (SNP) markers developed through whole genome re-sequencing have abundant loci and present a high level of genetic stability [31,32,33], so they are suitable to study population genetics [34]. Meanwhile, the first genome assembly of A. truncatum was in 2020, with 13 chromosomes and a genome size of 633.28 Mb [35] to provide a basis for studying the population genetic structure of A. truncatum. Consequently, the spatial pattern of genetic diversity and demographic history of A. truncatum were analyzed by the explored SNP using whole genome re-sequencing to provide a theoretical basis for developing conservation strategies and exploiting excellent germplasm and innovative utilization of germplasm.