Transcriptomes of Plant Gametophytes Have a Higher Proportion of Rapidly Evolving and Young Genes than Sporophytes

Abstract

Reproductive traits in plants tend to evolve rapidly due to various causes that include plant-pollinator coevolution and pollen competition, but the genomic basis of reproductive trait evolution is still largely unknown. To characterize evolutionary patterns of genome wide gene expression in reproductive tissues in the gametophyte and to compare them to developmental stages of the sporophyte, we analyzed evolutionary conservation and genetic diversity of protein-coding genes using microarray-based transcriptome data from three plant species, Arabidopsis thaliana, rice (Oryza sativa), and soybean (Glycine max). In all three species a significant shift in gene expression occurs during gametogenesis in which genes of younger evolutionary age and higher genetic diversity contribute significantly more to the transcriptome than in other stages. We refer to this phenomenon as “evolutionary bulge” during plant reproductive development because it differentiates the gametophyte from the sporophyte. We show that multiple, not mutually exclusive, causes may explain the bulge pattern, most prominently reduced tissue complexity of the gametophyte, a varying extent of selection on reproductive traits during gametogenesis as well as differences between male and female tissues. This highlights the importance of plant reproduction for understanding evolutionary forces determining the relationship of genomic and phenotypic variation in plants.

Plant organ evolution revealed by phylotranscriptomics in Arabidopsis thaliana

“…3A and Tables S2 and 3 ). This is consistent with previous studies, which reported that young genes tend to contribute more to the transcriptomes of the reproductive tissues compared with the old genes 14 , 16 . Cui, et al .…”

“…3C ; Figure S2A,C and E , Table S4 , 5 , 6 , 7 , 8 , 9 , 10 and 11 ). This pattern is also consistent with previous studies, which reported that plant reproductive tissues tend to have more divergent transcriptomes and less selective pressure 4 , 14 , 16 . But the order of the transcriptomes divergence in the seedling and root is opposite that observed by Yang and Wang, though that could be because of different methods used to estimate the expression divergence and the use of only a single accession of A. thaliana 4 .…”

“…3E and Figure S3 ). This matches previous reports that young genes in reproductive stages tend to have higher expression than old genes 14 , 16 . Additionally, the pattern of TAI is fairly consistent across accessions, with the minor exception of three accessions in which root has the highest average TAI rather than flower.…”

“…The results of TAI and TDI analyses for sense expression indicate that the transcriptome in flower is youngest and has the highest amino acid sequence divergence, the root transcriptome is much older with much lower sequence divergence, and finally the transcriptome in seedling is oldest and most conserved in sequence, experiencing more purifying selection. The result that the transcriptome in flower is youngest is consistent with previous reports that young genes tend to contribute more to the transcriptomes in the reproductive tissues or stages 14 , 16 . This may be consistent with the theory of plant organ evolution and the earliest fossil records of plant organs.…”

“…Although these studies applied the indices TAI and TDI, their application was limited to the examination of the developmental hourglasses in different organisms. More recently, several studies used these two indices to investigate the age of genes and their contributions to transcriptomes in different developmental stages, especially in reproductive tissues, for example, in pollen 14 , seed germination and flower development 15 , and plant reproductive development 16 . However, these reports focused more on comparisons of the reproductive tissues or stages from single accessions from different species, and did not explore the adaptive peaks (over-represented phylostrata) at different stages in their evolutionary history.…”