Highly degenerate plastomes in two hemiparasitic dwarf mistletoes: Arceuthobium chinense and A. pini (Viscaceae)

Abstract

The leafless and endophytic habitat may significantly relax the selection pressure on photosynthesis, and plastid transcription and translation, causing the loss/pseudogenization of several essential plastid-encoding genes in dwarf mistletoes. Dwarf mistletoes (Arceuthobium spp., Viscaceae) are the most destructive plant parasites to numerous conifer species worldwide. In this study, the plastid genomes (plastomes) of Arceuthobium chinense Lecomte and A. pini Hawksworth and Wiens were sequenced and characterized. Although dwarf mistletoes are hemiparasites capable of photosynthesis, their plastomes were highly degenerated, as indicated by the smallest plastome size, the lowest GC content, and relatively very few intact genes among the Santalales hemiparasites. Unexpectedly, several essential housekeeping genes (rpoA, rpoB, rpoC1, and rpoC2) and some core photosynthetic genes (psbZ and petL), as well as the rpl33 gene, that is indispensable for plants under stress conditions, were deleted or pseudogenized in the Arceuthobium plastomes. Our data suggest that the leafless and endophytic habit, which heavily relies on the coniferous hosts for nutrients and carbon requirement, may largely relax the selection pressure on photosynthesis, as well as plastid transcription and translation, thus resulting in the loss/pseudogenization of such essential plastid-encoding genes in dwarf mistletoes. Therefore, the higher level of plastome degradation in Arceuthobium species than other Santalales hemiparasites is likely correlated with the evolution of leafless and endophytic habit. A higher degree of plastome degradation in Arceuthobium. These findings provide new insights into the plastome degeneration associated with parasitism in Santalales and deepen our understanding of the biology of dwarf mistletoes.