Elucidating the evolutionary dynamics of parasitism in Cuscuta: in-depth phylogenetic reconstruction and extensive plastomes reduction

阐明菟丝子寄生现象的演化动态:深入的系统发育重建和广泛的质体基因组简化

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Abstract

BACKGROUND: The genus Cuscuta L. (Convolvulaceae), commonly known as dodder, is a holoparasite plant that relies on host plants for nutrition, leading to significant genomic changes, particularly in plastomes. This dependency has led to significant reductions and modifications in their plastomes compared to autotrophic plants. In contrast to the well-conserved plastomes of photosynthetic plants, Cuscuta exhibits substantial genomic reductions reflecting the loss of photosynthetic functions and associated genes. RESULT: This study examines eight plastomes within Cuscuta and reconstructs the phylogenetic relationships among 40 Cuscuta taxa using five other genera as an outgroup. The size of plastid genome varies significantly, with the smallest being 60 kb and the largest 121 kb, highlighting extensive genomic reduction. In special cases, the subgenera Cuscuta exhibit the loss of inverted repeats, distinguishing from them other subge within the Cuscuta genus. This reduction is most pronounced in genes related to photosynthesis, such as atp, pet, psa, psb, and ycf genes, particularly in the subg. Grammica (Lour.) Peter. The study also notes the frequent and independent loss of the plastid genes infA, rpl23, rpl32, rps15, and rps16 across various angiosperm lineages, often involving transfer to the nuclear genome. In parasitic plants like Cuscuta, the ndh genes, crucial for photosynthesis, are often lost. The study also highlights that in the subg. Grammica, the matK and rpo genes, along with trnR-ACG genes, are lost in parallel, indicating that these parasitic plants do not need matK and rpo genes after the loss of ndh genes for survival. Analysis of selective relaxation pressure on plastid genes shows a reductive trend, with genes such as atp, pet, psa, psb, rpo, and ycf progressively becoming pseudogenes over time, with housekeeping genes like rpl and rps expected to follow. However, the pseudogenization process is specific to the subg. Grammica, Pachystigma (Engelm.) Baker & C.H.Wright, and Cuscuta, rather than in the subg. Monogynella (Des Moul.) Peter, Engl. & Prantl (ancient clade species). CONCLUSION: The study of Cuscuta plastomes reveals the profound impact of parasitism on genome evolution, highlighting the complex interplay of gene retention and loss through phylogenomic approaches. This research enriches our understanding of plant genome evolution and the intricate host-parasite relationships. It also sheds light on the evolutionary history and genomic adaptations of Cuscuta, illustrating the diverse strategies enabling subg. Grammica, Pachystigma, Cuscuta, and Monogynella thrive as parasitic species. These findings provide valuable insights into the molecular mechanisms underlying parasitism and its impact on plastid genome organization.

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