Evolutionary diversification of acyl-CoA synthetases underpins hydrophobic barrier formation across diverse tomato tissues and beyond

Abstract

The transition of plants from aquatic to terrestrial environments required effective barriers against water loss and UV damage. The plant cuticle, a hydrophobic barrier covering aerial surfaces, emerged as a critical innovation, yet how its biosynthesis is regulated in specialized structures remains poorly understood. This study identifies two long-chain acyl-CoA synthetases, SlLACS1 and SlLACS2, that exhibit both distinct and overlapping functions in cuticle formation across tomato tissues. These genes show striking specificity in different trichome types: SlLACS1 functions in type I/IV trichomes, while SlLACS2 is required for type VI trichome cuticle integrity. However, they act redundantly in leaf epidermal and fruit cuticle formation, as revealed by analysis of single and double mutants. Unexpectedly, simultaneous disruption of both genes severely compromises pollen viability through defective pollen coat formation. Biochemical characterization demonstrates that SlLACS1 and SlLACS2 maintain their ancestral enzymatic function of activating long-chain fatty acids, an activity conserved from algal LACS homologs. These findings reveal how gene duplication and diversification facilitated the development of specialized hydrophobic barrier functions in distinct tissues while maintaining redundancy in fundamental protective structures, representing a sophisticated adaptation to terrestrial life.

Acknowledgments

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). We thank Gaurav Moghe from Cornell University for his insightful feedback and helpful discussions for this work.

Author Contributions

J.J. and P.F. designed the experiments; J.J., Q.H., X.F., J.W., and T.L. performed most of the experiments; J.C. and X.S. performed phylogenetic analysis; J.J., J.P. and S.F. performed cutin monomer and terpenoid measurement; R.L., J.Y., and X.S. provided guidance for the experiment design; J.J. wrote the first draft of the manuscript; P.F. and R.L. revised the manuscript with input from all the authors.

Data availability

All data are incorporated into the article and its online supplementary material.

Conflict of interest statement

All authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

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