Novel insights into chloroplast genome evolution in the green macroalgal genus Ulva (Ulvophyceae, Chlorophyta)

Feng Liu; Nansheng Chen; Hongshu Wang; Jiamin Li; Jing Wang; Fan Qu

doi:10.3389/fpls.2023.1126175

Novel insights into chloroplast genome evolution in the green macroalgal genus Ulva (Ulvophyceae, Chlorophyta)

Front Plant Sci. 2023 Apr 18:14:1126175. doi: 10.3389/fpls.2023.1126175. eCollection 2023.

Authors

Feng Liu^{1

2

3}, Nansheng Chen^{1

2

3}, Hongshu Wang^{1

2

3}, Jiamin Li^{1

2

3}, Jing Wang^{1

2

3}, Fan Qu⁴

Affiliations

¹ CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences (IOCAS), Qingdao, Shandong, China.
² Marine Ecology and Environmental Science Laboratory, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, Shandong, China.
³ Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, Shandong, China.
⁴ Harbin University of Science and Technology, Weihai, Shandong, China.

Abstract

To understand the evolutionary driving forces of chloroplast (or plastid) genomes (plastomes) in the green macroalgal genus Ulva (Ulvophyceae, Chlorophyta), in this study, we sequenced and constructed seven complete chloroplast genomes from five Ulva species, and conducted comparative genomic analysis of Ulva plastomes in Ulvophyceae. Ulva plastome evolution reflects the strong selection pressure driving the compactness of genome organization and the decrease of overall GC composition. The overall plastome sequences including canonical genes, introns, derived foreign sequences and non-coding regions show a synergetic decrease in GC content at varying degrees. Fast degeneration of plastome sequences including non-core genes (minD and trnR3), derived foreign sequences, and noncoding spacer regions was accompanied by the marked decrease of their GC composition. Plastome introns preferentially resided in conserved housekeeping genes with high GC content and long length, as might be related to high GC content of target site sequences recognized by intron-encoded proteins (IEPs), and to more target sites contained by long GC-rich genes. Many foreign DNA sequences integrated into different intergenic regions contain some homologous specific orfs with high similarity, indicating that they could have been derived from the same origin. The invasion of foreign sequences seems to be an important driving force for plastome rearrangement in these IR-lacking Ulva cpDNAs. Gene partitioning pattern has changed and distribution range of gene clusters has expanded after the loss of IR, indicating that genome rearrangement was more extensive and more frequent in Ulva plastomes, which was markedly different from that in IR-containing ulvophycean plastomes. These new insights greatly enhance our understanding of plastome evolution in ecologically important Ulva seaweeds.

Keywords: GC content; Ulvophyceae; chloroplast genome; comparative genomics; genome rearrangement; group I/II intron.

Grants and funding

This work was financially supported by the National Natural Science Foundation of China (No. 42276133/41876165), the Strategic Priority Research Program of Chinese Academy of Sciences (No. XDA23050302/XDA23050403), the Key Research Program of Frontier Sciences, Chinese Academy of Sciences (No. QYZDB-SSW-DQC023), the Science and Technology Basic Resources Investigation Program of China (No. 2018FY100200), the Major Scientific and Technological Innovation Project of Shandong Province (No. 2019JZZY020706), and Natural Science Foundation of Shandong Province for Young Scholars (No. ZR2022QD066).