Genetic and evolutionary analyses of plastomes of the subfamily Cactoideae (Cactaceae) indicate relaxed protein biosynthesis and tRNA import from cytosol

Abstract

Cactaceae arose ca. 30–35 million years ago (Mya) and comprises keystone species of arid and semiarid biomes. Various specific features related to morphology, anatomy, and CAM metabolism have likely favored diversification and expansion under arid environments. The plastome of most cactus species also undergone several evolutionary features to adapt growth and development under adverse environmental conditions. Aiming to enhance the understanding of the plastid evolution in the subfamily Cactoideae, we sequenced and analyzed in detail the plastome of Rhipsalis teres (Vell.) Steud., an epiphytic species from the Atlantic forest. The plastome of R. teres contains the two main rearrangements found in other plastomes of the subfamily Cactoideae. Our structural analyses suggested that the ancestral plastome architecture served as the basic structure for homologous recombination-mediated diversification of the IR boundaries found in them. Cactoideae plastomes show several polymorphic RNA editing sites, which are mainly distributed in genes related to gene expression machinery. Interestingly, the loss of rpl33 and rpl36 genes suggests a relaxed plastid biosynthesis in these species. Also, the absence of the trnV-UAC gene indicates the emergence of a tRNA import mechanism given that, for steric reasons, all valine codons cannot be read by the tRNAVal(GAC). Finally, our data indicate that the environment imposed several evolutionary features in the plastomes of Cactoideae during evolution under arid and semiarid biomes allowing adaptation and diversification.