Evolution of isoform‐level gene expression patterns across tissues during lotus species divergence

Abstract

Both gene duplication and alternative splicing (AS) drive the functional diversity of gene products in plants, yet the relative contributions of the two key mechanisms to the evolution of gene function are largely unclear.Here, we studied AS in two closely related lotus plants, Nelumbo lutea and Nelumbo nucifera, and the outgroup Arabidopsis thaliana, for both single-copy and duplicated genes. We show that most splicing events evolved rapidly between orthologs and that the origin of lineage-specific splice variants or isoforms contributed to gene functional changes during species divergence within Nelumbo. Single-copy genes contain more isoforms, have more AS events conserved across species, and show more complex tissue-dependent expression patterns than their duplicated counterparts. This suggests that expression divergence through isoforms is a mechanism to extend the expression breadth of genes with low copy numbers. As compared to isoforms of local, small-scale duplicates, isoforms of whole-genome duplicates are less conserved and display a less conserved tissue bias, pointing towards their contribution to subfunctionalization. Through comparative analysis of isoform expression networks, we identified orthologous genes of which the expression of at least some of their isoforms displays a conserved tissue bias across species, indicating a strong selection pressure for maintaining a stable expression pattern of these isoforms. Overall, our study shows that both AS and gene duplication contributed to the diversity of gene function during the evolution of lotus.

Genome-Wide Identification and Co-Expression Networks of WOX Gene Family in Nelumbo nucifera

“…A previous study revealed that the expression patterns of genes in lotus were different in multiple tissues [ 32 ], which enabled further investigation of the tissue expression level of the NnWOX genes. Interestingly, we only found similar tissue expression patterns between the duplicated NnWOX13a/b genes in the ancient clade.…”

“…Due to the minimum sample size and correlation of gene modules and tissue, weight gene co-expression network analysis (WGCNA) was widely used for identifying the co-expressed gene pairs in different plant tissues or experimental treatment samples [ 59 , 60 , 61 ]. Previous transcriptomic research on lotus has constructed a gene-level network involved in only six tissues and a transcript-level co-expression network including eleven tissues using WGCNA [ 32 , 62 ]. In this study, we used the same pipeline of WGCNA to construct the gene co-expression networks for each NnWOX gene ( Figure 5 ).…”

“…With specific purposes of artificial domestication, the cultural lotuses were divided into three taxonomic groups, i.e., rhizome, seed, and flower lotus [ 29 ]. Based on the well-assembled reference genome of lotus [ 30 ], recent transcriptomic and proteomic research on sacred lotus was carried out to reveal the molecular mechanism of regulating the development of tissues [ 31 , 32 , 33 ]. According to previous studies, a single whole-genome duplication event occurred in ancestors of the N. nucifera during the K-Pg boundary [ 30 ], similar to the basal eudicot Amborella trichopoda [ 34 ].…”