Genomic Adaptive Evolution of Sand Rice (Agriophyllum squarrosum) and Its Implications for Desert Ecosystem Restoration

Abstract

Natural selection is a significant driver of population divergence and speciation of plants. Due to local adaptation to geographic regions with ecological gradients, plant populations harbored a wide range of adaptive genetic variation to enable them to survive the heterogeneous habitats. This is all the more necessary for desert plants, as they must tolerant more striking gradients of abiotic stresses. However, the genomic mechanism by which desert plants adapt to ecological heterogeneity remains unclear, which could help to guide the sustainability of desert ecosystems. Here, using restriction-site-associated DNA sequencing in 38 natural populations, we investigated the genomic divergence and environmental adaptation of sand rice, Agriophyllum squarrosum, an annual pioneer species that covers sand dunes in northern China. Population genetic structure analyses showed that sand rice could be divided into three geographically distinct lineages, namely, Northwest, Central, and East. Phylogeographic analyses revealed that the plant might originate locally in Bergen County and further differentiated into the East lineage and then the Central lineage. Ecological niche modeling found that different lineages occupied distinct ecological niches, suggesting that the ecological gradient would have triggered genomic differentiation among sand rice lineages. Ecological association study supported that the three SNPs under divergent selection were closely correlated with precipitation gradients, indicating that precipitation might be the most important stress trigger for lineage diversity in sand rice. These adaptive SNPs could be used to genotype suitable germplasms for the ecological restoration of specific desertified lands. Further analyses found that genetic structure could significantly overestimate the signals for balancing selection. Within the Central lineage, we still found that 175 SNPs could be subject to balancing selection, which could be the means by which sand rice maintains genetic diversity and adapts to multiple stresses across heterogeneous deserts and sandy lands. From a genomic point of view, this study highlighted the local and global adaptation patterns of a desert plant to extreme and heterogeneous habitats. Our data provide molecular guidance for the restoration of desertified lands in the arid and semi-arid regions of China and could facilitate the marker assistant breeding of this potential crop to mitigate climate change.

Variations in Flavonoid Metabolites Along Altitudinal Gradient in a Desert Medicinal Plant Agriophyllum squarrosum

“…Previous studies showed that there was no significant divergence among the altitudinal wild populations in neutral molecular genetic markers (nrITS and chloroplast DNA; Qian et al, 2016 , 2021 ). However, non-target metabolomics analysis supported that the accumulations of a couple of flavonoids, such as hesperetin, quercetin, and apigenin, were significantly enriched in the ecotype with high altitude (unpublished data).…”

Integrated metabolomics and transcriptomics insights on flavonoid biosynthesis of a medicinal functional forage, Agriophyllum squarrosum (L.), based on a common garden trial covering six ecotypes

“…Sandrice [ Agriophyllum squarrosum (L.)] is an edible and medicinal resource psammophyte of Chenopodiaceae, which is widely distributed in the vast arid and semi-arid sandy lands in Central Asia, the Caucasus, Mongolia, Siberia, and Northern China ( Qian et al, 2016 ). Sandrice is a pioneer species on mobile sands, being able to adapt to the cruel environment in deserts like extreme temperature, dehydration, and sand burial, and was proved to have a wide range of genetic and phenotypic variation among different populations, which was derived from local adaptation to their original marginal habitats ( Yin et al, 2016 ; Zhao et al, 2017 , 2022 ; Qian et al, 2021 ). Although this underutilized feed crop has not been domesticated, the seeds of sandrice have a long consumption history and are rich in essential amino acids, crude fiber, polyunsaturated fatty acids, etc., and tender stems and leaves of sandrice are wild feedings for livestock in the sandy areas, making it an ideal functional food and natural feed crop ( Li et al, 1992 ; Chen et al, 2014 ; Wang Q. et al, 2019 ; Han et al, 2021 ; Zhao et al, 2021 ).…”

Precipitation and local environment shape the geographic variation of seed size across natural populations of sand rice (Agriophyllum squarrosum)

“…7D–F ), indicating that the plasticity of seed size is heritable and potentially adaptive. Population genetic analyses have consistently indicated that genetic divergence mainly occurs between populations from the eastern sand fields and those from the central and western deserts in Northern China ( Qian et al ., 2016 , 2021 ). Our previous haplotype analysis of a seed size candidate gene, DA1-Related , also showed a similar divergence pattern among natural populations of sand rice ( Zhao et al , 2017 ).…”