A case study ofWhirly1(WHY1) evolution in the angiosperms: altered sequence, splicing, and expression in a clade of early-transitional mycoheterotrophic orchids

Author:

Muti Rachel M.,Barrett Craig F.ORCID,Sinn Brandon T.ORCID

Abstract

AbstractThe plastid-targeted transcription factorWhirly1(WHY1) has been implicated in chloroplast biogenesis, plastid genome stability, and fungal defense response, which together represent characteristics of interest for the study of autotrophic losses across the angiosperms. While gene loss in the plastid and nuclear genomes has been well studied in mycoheterotrophic plants, the evolution of the molecular mechanisms impacting genome stability are completely unknown. Here we characterize the evolution ofWHY1in four early-transitional mycoheterotrophic orchid species in the genusCorallorhizaby synthesizing the results of phylogenetic, transcriptomic, and comparative genomic analyses withWHY1genomic sequences sampled from 21 orders of angiosperms. We found an increased number of non-canonicalWHY1isoforms assembled from all but the greenestCorallorhizaspecies, including intron retention in some isoforms. WithinCorallorhiza, phylotranscriptomic analyses revealed the presence of tissue-specific differential expression ofWHY1in only the most photosynthetically capable species and a coincident increase in the number of non-canonicalWHY1isoforms assembled from fully mycoheterotrophic species. Gene- and codon-level tests ofWHY1selective regimes did not infer significant signal of either relaxed selection or episodic diversifying selection inCorallorhiza, but did so for relaxed selection in the late-stage full mycoheterotrophic orchidsEpipogium aphyllumandGastrodia elata. Taken together, this study provides the most comprehensive view ofWHY1evolution in angiosperms to date. Our analyses reveal that splicing alteration and decreased expression ofWHY1are coincident with deceased plastome stability in a group of early-transitional mycoheterotrophic orchids and that these changes may precede the selective shifts observed in late-stage mycoheterotrophic species.

Publisher

Cold Spring Harbor Laboratory

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