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Trash to treasure: lactate and protein lactylation in maize root impacts response to drought

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Abstract

Lactate, protein lactylation (Kla), and specifically histone lactylation have recently been shown to regulate antipathogenic immune responses in mammals. Herein, after we confirmed the presence and accumulation of lactate in maize roots under drought conditions, a lactylome profiling analysis revealed that Kla modifications were invariably present in maize roots, that there were obvious differences in the lactylomes of drought-sensitive (B73) vs. drought-tolerant (Jing2416) lines, and that growing Jing2416 under drought conditions caused significant decreases in the lactylation of multiple enzymes responsible for fatty acid degradation. Inspired by findings of histone-Kla based epigenetic regulation of immune functions in animals, we initially discovered 37 Kla sites on 16 histones in the maize genome, and again detected obvious differential histone Kla-mediated trends between two lines by ChIP-Seq. Notably, only 2.7% of genes with differential histone Kla peaks detected during drought stress were commonly present in both lines, a finding demonstrating that abiotic stress triggers distinct epigenetic activities in diverse germplasm while also strongly supporting that a histone Kla layer of regulation is associated with physiological responses to drought stress. Interestingly, exogenous application of spermidine improved the drought tolerance of B73 and substantially altered the levels of lactate, protein lactylation, and histone Kla modification. Thus, beyond extending the known domain of Kla-based biochemical and epigenetic regulation from animal immunity to plant stress physiology, our study suggests the physiological, biochemical, and genetic function of “the best-known metabolic waste”, lactate.

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Data availability

Raw proteomic data generated in this study are available in the Proteomics Identification (PRIDE) database under project accession No. PXD030987. All other data are available in the main text or supplemental materials. Materials are available upon request.

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Acknowledgements

This work was supported by the Beijing Scholars Program (BSP041), Beijing Nova Program (20220484220), the High-level Returned Talents grant from the Ministry of Human Resources and Social Security of the People’s Republic of China, and Science and Technology Xing Meng action focus project of Inner Mongolia Autonomous Region (KJXM2020001). We are grateful to Qinglin Wu and Yiran Jiao for their curiosity while studying the textbook of Biology, which inspired us to conceive this study. We thank Wenyan Wu, Zichen Zhang and Jiarong Wang for providing technical assistance.

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Correspondence to Jiuran Zhao or Wen Ren.

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Shi, Z., Zhou, M., Song, W. et al. Trash to treasure: lactate and protein lactylation in maize root impacts response to drought. Sci. China Life Sci. 66, 1903–1914 (2023). https://doi.org/10.1007/s11427-023-2361-1

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