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Comparative Plastome Analysis of Root- and Stem-Feeding Parasites of Santalales Untangle the Footprints of Feeding Mode and Lifestyle Transitions

2019; Oxford University Press; Volume: 12; Issue: 1 Linguagem: Inglês

10.1093/gbe/evz271

1759-6653

Xiaoli Chen, Dongming Fang, Chenyu Wu, Bing Liu, Yang Liu, Sunil Kumar Sahu, Bo Song, Shuai Yang, Tuo Yang, Jinpu Wei, Xuebing Wang, Wen Zhang, Qiwu Xu, Hua‐Feng Wang, Lang‐Xing Yuan, Xuezhu Liao, Lipeng Chen, Ziqiang Chen, Yuan Fu, Yue Li Chang, Lihua Lü, Huanming Yang, Jian Wang, Xun Xu, Xin Liu, Susann Wicke, Huan Liu,

Legume Nitrogen Fixing Symbiosis

Abstract In plants, parasitism triggers the reductive evolution of plastid genomes (plastomes). To disentangle the molecular evolutionary associations between feeding on other plants below- or aboveground and general transitions from facultative to obligate parasitism, we analyzed 34 complete plastomes of autotrophic, root- and stem-feeding hemiparasitic, and holoparasitic Santalales. We observed inexplicable losses of housekeeping genes and tRNAs in hemiparasites and dramatic genomic reconfiguration in holoparasitic Balanophoraceae, whose plastomes have exceptionally low GC contents. Genomic changes are related primarily to the evolution of hemi- or holoparasitism, whereas the transition from a root- to a stem-feeding mode plays no major role. In contrast, the rate of molecular evolution accelerates in a stepwise manner from autotrophs to root- and then stem-feeding parasites. Already the ancestral transition to root-parasitism coincides with a relaxation of selection in plastomes. Another significant selectional shift in plastid genes occurs as stem-feeders evolve, suggesting that this derived form coincides with trophic specialization despite the retention of photosynthetic capacity. Parasitic Santalales fill a gap in our understanding of parasitism-associated plastome degeneration. We reveal that lifestyle-genome associations unfold interdependently over trophic specialization and feeding mode transitions, where holoparasitic Balanophoraceae provide a system for exploring the functional realms of plastomes.