Molecular foundation underlying the formation of highly productive isobilateral leaves in mangroves.

Abstract

Photosynthesis in mangroves contributes to one of the most carbon-rich ecosystems on Earth and plays a significant role in mitigating global climate change. However, the mechanisms underlying the high productivity of mangroves remain largely unexplored. Through anatomical analyses, we found that mangrove species with higher biomass production, such as Sonneratia apetala, exhibit isobilateral leaves, which enhance light harvesting and reduce light inhibition, resulting in higher photosynthetic yields. Transcriptomic and genomic analyses revealed the molecular processes underlying the formation of isobilateral leaves. We found that auxin is rapidly synthesized and works in coordination with gibberellin and brassinosteroid in the isobilateral leaves of S. apetala. Interestingly, we identified a group of genes related to adaxial-abaxial leaf polarity in S. apetala, with upregulated genes associated with chlorophyll synthesis, adaxial cell identity and erect leaf growth, while genes related to the recognition of adaxial cell boundaries-possibly related to the lower palisade tissues-were downregulated. Additionally, we identified amino acid substitutions and changes in promoter cis-acting elements in Indole-3-acetic acid carboxylmethyltransferase 1 (IAMT1) in Sonneratia species. These findings provide new insights into the formation of isobilateral leaves in mangroves and their adaptation to intertidal high-light coastal conditions.