Frequent Tandem Gene Duplications Enhance Stress Resistance and Environmental Adaptation in Extremophilic Apocynum...

Extremophile Apocynum species hold significant economic and ecological value in arid regions. Deciphering their genetic variation is therefore essential for understanding geographic adaptation to abiotic stresses. Here, we assembled a high-quality genome of Apocynum pictum, and, through comparison with the A. venetum genome, identified abundant genome-wide structural variations, particularly tandem gene duplications (TDs). For instance, a key TD spanning 19 tandem SRP genes was found in A. pictum, compared to only four in A. venetum. We further performed whole-genome resequencing of 280 individuals from natural populations of A. venetum and A. pictum that were widely distributed across arid and saline-alkali regions in northern China. We revealed a distinct geographical distribution of six genetic population clusters in the current landscape. Demographic inference identified a severe population decline during the Last Glacial Maximum, while genetic offset analysis forecasted high vulnerability to future climate change in the mountains and Tarim Basin for both species. TDs, for example, tandemly duplicated LRR-RLK, ABCG, and TLP genes, were under significant selection, as revealed by both selective sweep analysis between A. venetum and A. pictum and genome-environment association analysis with temperature and precipitation variables. TLP overexpression in tobacco enhanced drought tolerance by alleviating oxidative damage. Furthermore, a dual-luciferase assay confirmed that the A. pictum TLP promoter haplotypes carrying selection signals exhibited higher transcriptional activity than their counterparts in A. venetum. Our findings highlighted the combined roles of gene dosage effects and regulatory sequence selection of frequent stress-resistant TDs in harsh environments.