Avalilação PREreview de Rapid evolution of gene expression patterns in flowering plants

Peer review of ‘Rapid evolution of gene expression patterns in flowering plants.’  

       Zhongyu Huang, Ashley Mansour, and Sunil Kumar Kenchanmane Raju

This is a well-written manuscript by Christoph Schuster et al. The study explores the evolution of gene expression patterns in flowering plants using high-throughput whole-transcriptome sequencing (RNA-seq). By analyzing both protein-coding genes and long non-coding RNAs (lncRNAs),  focusing on orthologous genes across nine plant organs in seven angiosperm species, the authors aim to understand how gene expression varies between different organs and between different species. The authors show that gene expression patterns diverge more significantly across species than across organs, particularly in reproductive tissues such as stamens and pollen. These tissues show a high degree of evolutionary plasticity, likely reflecting adaptations to different reproductive strategies or environmental conditions. In contrast, vegetative tissues such as leaves and meristems exhibit more conserved gene expression profiles. The study also finds that lncRNAs evolve rapidly and are largely lineage-specific, suggesting they may contribute to species-specific traits. Importantly, the authors compare these findings to mammalian gene expression patterns and highlight the distinct evolutionary dynamics in plants, which may be due to their strong ability to adapt to new environments. Overall, this article provides valuable insights into the molecular basis of plant diversity and demonstrates how transcriptome evolution may have played a crucial role in angiosperm diversification.

Major concerns or issues 

A. While this article provides valuable results on gene expression patterns in flowering plants, we would like to highlight sampling bias in species selection. The study focuses on seven angiosperms, four of which belong to the Brassicaceae family, and only one represents monocots. This distribution raises the question of whether the findings can be generalized to all flowering plants. Given the vast diversity within angiosperms, especially between monocots and eudicots, a more balanced representation of plant lineages could strengthen the conclusions and provide a more comprehensive understanding of transcriptomic evolution across the clade.

B. In the article, the authors reported low conservation of orthologous lncRNAs across species, but this conclusion is based on only eight selected lncRNAs, which may limit the interpretation. While the observed pattern may reflect rapid evolution and lineage-specific expression, it could also result from differences in genome annotation quality—especially in non-model plants where non-coding regions are often poorly annotated. Misannotation or missing data may lead to an underestimation of conservation. Improved annotation and cross-species alignment tools may be necessary to better understand the evolution of plant lncRNA. Deng et al. (2017)  proposed assessing collinearity using the nearest upstream and downstream coding genes (within a three-gene distance), offering a useful strategy for identifying orthologous lncRNAs. Recently developed tools, such as PlantLncBoost (Wu et al., 2022), will further enhance the accuracy of finding IncRNAs.

C. The use of the phrase “almost cell-type specific resolution” to refer to the pollen data does not feel appropriate. Given that it is a general feature of pollen to exhibit only two cell types, and this study does not uniquely isolate these cell types, we believe this phrase is unnecessary and does not contribute to the analysis of the paper. Focusing instead on the spatial and developmental nature of the data, as well as the number of species used, highlights the true strengths of this paper. 

D. The mention of the two Angiosperm diversification events in the discussion does not seem to be linked to the paper text or organism choice. If the argument is that these diversification bursts correspond with the phylogenetic tree at the beginning, then a specific time frame should be mentioned for the second burst, so it can be coordinated with the tree, and a more detailed explanation of the intended link to the expression patterns discussed in the body of the paper. 

E. If Angiosperm diversification can also be linked to the importance of insect pollinators, then that would provide a clear reason for the increased speed of evolutionary diversification in pollen and stamens, as evolution in these mechanisms could be easily influenced by insect species preference.

(as demonstrated in this paper (Hernández-Hernández and Wiens 2020)

F. The authors compare and contrast their results with those of Brawand et al, which showed samples from the same tissues in distantly related species clustered together. One possibility is that the plant species selected here have evolved much faster compared to the mammalian species (Brawand et al. 2011). We are also curious about the role of alternative splicing in mammals. Merkin et al. have shown that while tissue-specific gene expression programs are largely conserved, alternative splicing is frequently lineage-specific and conserved in only a few tissue types (Merkin et al. 2012). This raises the question of whether the fundamental differences in gene expression regulation in mammals (alternative splicing, alternate exon usage etc) and plants (cis-regulatory element evolution in duplicate paralogs regulating tissue/lineage specific gene expression etc) could explain some of the differences in this study? 

Acknowledgement: 

This preprint was discussed in the BPSC 240 course offered by Sunil K. Kenchanmane Raju in the Department of Botany and Plant Sciences at the University of California, Riverside, in Spring 2025. The authors thank the participants of the course for the detailed discussions, particularly Angel Morris and Skyler Wong. 

References: 

Deng, P., Liu, S., Nie, X., Weining, S., & Wu, L. (2017). Conservation analysis of long non-coding RNAs in plants. Science China Life Sciences, 61(2), 190–198. 

Wu, P., Qin, Q., Zhang, J., Zhang, H., Li, X., Wang, H., & Meng, Q. (2022). The invasion process of the entomopathogenic fungus Ophiocordyceps sinensis into the larvae of ghost moths (Thitarodes xiaojinensis) using a GFP-labeled strain. Frontiers in Microbiology, 13. 

Hernández-Hernández, T., & Wiens, J. J. (2020). Why are there so many flowering plants? A multiscale analysis of plant diversification. The American Naturalist, 195(6), 948–963. 

Brawand, D., Soumillon, M., Necsulea, A., Julien, P., Csárdi, G., Harrigan, P., ... & Kaessmann, H. (2011). The evolution of gene expression levels in mammalian organs. Nature, 478(7369), 343-348.

Merkin, J., Russell, C., Chen, P., & Burge, C. B. (2012). Evolutionary dynamics of gene and isoform regulation in Mammalian tissues. Science, 338(6114), 1593-1599.

Competing interests

The authors declare that they have no competing interests.