When plants transitioned from aquatic to terrestrial environments, they faced severe challenges, including dehydration and increased ultraviolet radiation. To cope with these stresses, plants evolved hydrophobic barriers such as cuticles and pollen coats that protect tissues and maintain water balance. While the chemical composition of these barriers has been well documented, how their formation is regulated across diverse tissues—including leaves, fruits, glandular trichomes, and reproductive organs—remains poorly understood. In particular, it is unclear how plants achieved tissue-specific barrier functions while preserving robustness and redundancy at the molecular level. Based on these challenges, there is a clear need to conduct in-depth research into how hydrophobic barrier biosynthesis diversified during plant evolution.
Researchers from Zhejiang University reported (DOI: 10.1093/hr/uhaf114) on 28 April 2025 in Horticulture Research, a comprehensive analysis of how hydrophobic barriers are established across tomato tissues. By integrating genetic, biochemical, ultrastructural, and evolutionary approaches, the study demonstrates that SlLACS1 and SlLACS2 regulate cuticle formation in leaves, fruits, and distinct glandular trichomes, while redundantly ensuring pollen viability. The work reveals how conserved metabolic enzymes were redeployed through evolution to meet the protective demands of increasingly complex plant organs.
The study focused on SlLACS1 and SlLACS2, two genes encoding long-chain acyl-CoA synthetases that activate fatty acids for cutin biosynthesis. Transcriptome-guided screening combined with targeted genome editing showed that the two genes exhibit striking tissue specificity. Loss of SlLACS1 selectively compromised cuticle integrity in type I/IV glandular trichomes, whereas disruption of SlLACS2 affected type VI trichomes. Microscopic and chemical analyses confirmed that these defects were associated with reduced cutin deposition and increased permeability.
Despite this specialization, the genes function redundantly in other tissues. Plants lacking both SlLACS1 and SlLACS2 displayed severely thinned cuticles in leaves and fruits, leading to enhanced water loss and reduced surface protection. Unexpectedly, the double mutants also showed a dramatic decline in pollen viability. Ultrastructural observations revealed that the pollen coat—a lipid-rich hydrophobic layer essential for fertilization—was largely absent, linking these genes to reproductive success.
Phylogenetic analysis across more than 200 plant species showed that LACS1 and LACS2 originated from a gene duplication event associated with plant terrestrialization. While their enzymatic activity remained conserved, diversification of tissue-specific expression enabled the evolution of multiple, specialized hydrophobic barriers.
“This study illustrates how plants solved diverse protection challenges using a shared molecular framework,” said the corresponding author. “Instead of evolving new enzymes, plants duplicated an existing gene and diversified its spatial deployment.” The findings highlight how functional redundancy and specialization can coexist, allowing plants to maintain essential barriers while tailoring protection to specific tissues. Such genetic flexibility likely played a crucial role in enabling plants to colonize land and develop complex organs without compromising survival.
Understanding how hydrophobic barriers are regulated across plant tissues has important implications for agriculture and crop improvement. Insights into the roles of SlLACS1 and SlLACS2 may inform strategies to enhance drought tolerance, reduce post-harvest water loss, and improve reproductive stability under environmental stress. In crops such as tomato, fine-tuning barrier formation could contribute to improved fruit quality and shelf life. More broadly, the evolutionary framework established in this study provides a foundation for exploring barrier-related traits in other plant species, supporting breeding efforts aimed at resilience in increasingly challenging climates.
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References
DOI
10.1093/hr/uhaf114
Original Source URL
https://doi.org/10.1093/hr/uhaf114
Funding information
This study was funded by the National Natural Science Foundation of China (grant no. 32472718), National Key Research and Development Project of China (grant no. 2024YFD2001003), Natural Science Foundation of Zhejiang province (grant no. LZ22C150005), and the Starry Night Science Fund of Zhejiang University Shanghai Institute for Advanced Study (SN-ZJU-SIAS-0011).
About Horticulture Research
Horticulture Research is an open access journal of Nanjing Agricultural University and ranked number one in the Horticulture category of the Journal Citation Reports ™ from Clarivate, 2023. The journal is committed to publishing original research articles, reviews, perspectives, comments, correspondence articles and letters to the editor related to all major horticultural plants and disciplines, including biotechnology, breeding, cellular and molecular biology, evolution, genetics, inter-species interactions, physiology, and the origination and domestication of crops.