Comparative Chloroplast Genomes of Zosteraceae Species Provide Adaptive Evolution Insights Into Seagrass.

Jun Chen,Shuai Shang,Meiling Zhu,Shuo Liang,Xuexi Tang,Yu Zang,Ying Wang

doi:10.3389/fpls.2021.741152

Abstract

Seagrasses are marine flowering plants found in tropical and sub-tropical areas that live in coastal regions between the sea and land. All seagrass species evolved from terrestrial monocotyledons, providing the opportunity to study plant adaptation to sea environments. Here, we sequenced the chloroplast genomes (cpGenomes) of three Zostera species, then analyzed and compared their cpGenome structures and sequence variations. We also performed a phylogenetic analysis using published seagrass chloroplasts and calculated the selection pressure of 17 species within seagrasses and nine terrestrial monocotyledons, as well as estimated the number of shared genes of eight seagrasses. The cpGenomes of Zosteraceae species ranged in size from 143,877 bp (Zostera marina) to 152,726 bp (Phyllospadix iwatensis), which were conserved and displayed similar structures and gene orders. Additionally, we found 17 variable hotspot regions as candidate DNA barcodes for Zosteraceae species, which will be helpful for studying the phylogenetic relationships and interspecies differences between seagrass species. Interestingly, nine genes had positive selection sites, including two ATP subunit genes (atpA and atpF), two ribosome subunit genes (rps4 and rpl20), two DNA-dependent RNA polymerase genes (rpoC1 and rpoC2), as well as accD, clpP, and ycf2. These gene regions may have played key roles in the seagrass adaptation to diverse environments. The Branch model analysis showed that seagrasses had a higher rate of evolution than terrestrial monocotyledons, suggesting that seagrasses experienced greater environmental pressure. Moreover, a branch-site model identified positively selected sites (PSSs) in ccsA, suggesting their involvement in the adaptation to sea environments. These findings are valuable for further investigations on Zosteraceae cpGenomes and will serve as an excellent resource for future studies on seagrass adaptation to sea environments.

Highlights

Seagrasses are marine flowering plants in class Monocotyledoneae that form vast meadows, and flower and seed underwater
The cpGenome sizes of the three species and Z. marina of family Zosteraceae ranged from 143,877 bp in Z. marina to 152,726 bp in P. iwatensis, which were composed of four regions, including an large single-copy (LSC) and small single-copy (SSC) region separated by two inverted repeats (IRs) (Figure 1 and Table 1)
There were 132 genes in P. iwatensis, 131 in Z. nigricaulis, 127 in Z. japonica, and 116 in Z. marina, which had the lowest number of genes

Summary

Introduction

Seagrasses are marine flowering plants in class Monocotyledoneae that form vast meadows, and flower and seed underwater. As opposed to lower plants such as macroalgae (seaweeds), seagrasses are higher angiosperms that can live fully in seawater. They have terrestrial plant origins and reentered the sea millions of years ago (Orth et al, 2006). The ancestors of seagrasses separated from terrestrial monocotyledons 70–100 million years ago and have since adapted to submerged marine life (Waycott et al, 2007). During this process, a series of adaptive changes took place in their morphological structures and physiological ecology (Ye, 2002). In 2016, the complete genome of Z. muelleri was sequenced and it was found that, to adapt to the marine environment, genes related to hormone biosynthesis, signal transduction, and cell wall catabolism were either lost or modified (Lee et al, 2016)

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