Transcriptome sequencing of three Ranunculus species (Ranunculaceae) reveals candidate genes in adaptation from terrestrial to aquatic habitats

Abstract

Adaptation to aquatic habitats is a formidable challenge for terrestrial angiosperms that has long intrigued scientists. As part of a suite of work to explore the molecular mechanism of adaptation to aquatic habitats, we here sequenced the transcriptome of the submerged aquatic plant Ranunculus bungei, and two terrestrial relatives R. cantoniensis and R. brotherusii, followed by comparative evolutionary analyses to determine candidate genes for adaption to aquatic habitats. We obtained 126,037, 140,218 and 114,753 contigs for R. bungei, R. cantoniensis and R. brotherusii respectively. Bidirectional Best Hit method and OrthoMCL method identified 11,362 and 8,174 1:1:1 orthologous genes (one ortholog is represented in each of the three species) respectively. Non-synonymous/synonymous (dN/dS) analyses were performed with a maximum likelihood method and an approximate method for the three species-pairs. In total, 14 genes of R. bungei potentially involved in the adaptive transition from terrestrial to aquatic habitats were identified. Some of the homologs to these genes in model plants are involved in vacuole protein formation, regulating ‘water transport process’ and ‘microtubule cytoskeleton organization’. Our study opens the door to understand the molecular mechanism of plant adaptation from terrestrial to aquatic habitats.

Insights into the strategy of micro-environmental adaptation: Transcriptomic analysis of two alvinocaridid shrimps at a hydrothermal vent

“…Multiple testing correction was performed via false discovery rate (FDR) estimation. Orthologous pairs with an FDR>0.05, Ks<0.01, Ks>1, or Ka>1 were discarded [36]. Ka/Ks>1 indicated strong positive selection.…”

Development of EST‐derived microsatellite markers in the aquatic macrophyte Ranunculus bungei (Ranunculaceae)

“…A mixture of tissues from roots, stems, and leaves was used for the transcriptome sequencing of R. bungei , conducted by Chen et al (2015) using the Illumina HiSeq 2000 sequencer (Illumina, San Diego, California, USA). A total of 5,312,841 clean reads of R. bungei deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (accession no.…”

“…A total of 5,312,841 clean reads of R. bungei deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (accession no. SRR1822529; Chen et al, 2015) were used for de novo transcriptome assembly using Trinity version 2.1.0 with default parameters (Grabherr et al, 2011). The longest sequence was chosen for transcripts with several isoforms, as identified with a perl script (available at https://github.com/jinweiwu/perl/blob/master/ extract).…”

“…(section Batrachium DC., Ranunculaceae) is a perennial submerged plant that can proliferate vegetatively through rhizomes or sexually via selfing or outcrossing (Cook, 1966). Ranunculus bungei is widely distributed in heterogeneous environments within the temperate and alpine regions of China and is significant for studies of the adaptation to aquatic habitats in angiosperms (Chen et al, 2015). In recent years, investigations have been carried out to examine genetic variation and population structure in R. bungei with intersimple sequence repeat (ISSR) markers or chloroplast noncoding spacers (Wang et al, 2010; Chen et al, 2014), but these markers are less powerful in studies on reproductive system, hybridization, patterns of gene flow, and fine-scale population structure.…”

Expansin gene loss is a common occurrence during adaptation to an aquatic environment

“…Aquatic inhabitance has multiple independent origins within angiosperms, and is characterized by species with highly adaptive morphologies (Hillman, ; Boeger and Poulson, ; Sulman et al , ; Chen et al , ; Carretero‐Paulet et al , ; Carretero‐Paulet et al , ; Du et al , ; Shtein et al , ). Although only representing 1–2% of all flowering plants, ~17% of angiosperm families contain aquatic members (Les et al , ).…”