Aquatic plants, a specialized evolutionary group adapted to life in water, play significant roles in food and medicinal supply (e.g., lotus root, foxnut), industrial raw materials (e.g., reed), and ecological restoration. While most aquatic lineages independently evolved from their terrestrial ancestors, the genomic dynamisms underlying this adaptation remain largely unexplored.

Recently, a collaborative investigation from the Wuhan Botanical Garden and China Pharmaceutical University, sheds new light on this mechanism. Their research, published in Current Biology titled "The convergent genomic dynamism for aquatic adaptation in vascular plants", integrates whole-genome assemblies from 122 vascular plant species  with morphological analyses (including stomata, vascular bundles, and aerenchyma), waterlogging experiments, and transcriptome sequencing. This study uncovers convergent genomic dynamisms addressing the plant adaptation to aquatic environments.

The "Accelerated Pace" of Genome Evolution in Aquatic Plants

By comparing the evolutionary rates of genes among species with different life forms (terrestrial, emergent/floating-leaved, freshwater submerged, and seagrasses), the results showed that aquatic plants-particularly submerged species and seagrasses-exhibited significantly higher evolutionary rates both in their nuclear, mitochondrial, and chloroplast genes compared to their terrestrial relatives. This suggests that aquatic environments did not "slow down" evolution, instead, have probably accelerated genomic changes through ecological constrains (e.g., low light, hypoxia, salinity fluctuations) that increase mutation rates, or through small population effects that promoted genetic drift.

Convergent Expansion of Functional Gene Families

Contrary to the widely held belief that aquatic plants primarily adapt to water via gene loss and streamlined genome, this study revealed extensive convergent expansions of gene families across various aquatic plant lineages. These expanded genes are closely associated with key adaptive traits such as iron ion homeostasis, aerenchyma formation, photosynthesis enhancement, and osmoregulation. For instance, the transcription factor bHLH115 responsible for iron deficiency-responsive have remarkably expanded in submerged species, likely contributing to their adaptive capacity to iron-deficient aquatic environments.

Specific Phenotypes Are Closely Associated with Gene Copy Number

Microscopic observations and controlled experiments revealed significant differences in stomatal development and aerenchyma formation among various aquatic plants. Submerged plants typically lack stomata or exhibit reduced stomata on their underwater leaves, yet some species can rapidly develop stomata when exposed to air, demonstrating strong phenotypic plasticity. Further analysis showed a significant positive correlation between the copy numbers of 13 key genes involved in stomatal development and the total stomatal area per unit leaf area. 

Diverged Transcriptional Responses to Flooding

By comparing gene expression variation between submerged and aerial conditions in 12 representative species (including terrestrial, emergent/floating-leaved, and submerged types), the study found that emergent/floating-leaved species and terrestrial ones activated a specific gene set (e.g., ethylene synthesis, hypoxia tolerance, aerenchyma formation) to "resist" or "escape" stress from flooding. In contrast, submerged plants exhibited a markedly different expression pattern: genes related to stomatal development and cell wall synthesis were significantly upregulated when leaves were exposed to air, and these pathways were suppressed when grown under water. It indicated that submerged plants may have shift from "stress response" to "fully adaptation" after long-term evolution. 

Global climate change is leading to more frequent  and severe flooding events, posing a serious threat on food security. By understanding the genomic mechanisms that allow aquatic plants to thrive in water, researchers can potentially develop strategies to enhance the resilience of crops to flooding and ensure a more stable food supply in the face of climate change.