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Integrative omics studies revealed synergistic link between sucrose metabolic isogenes and carbohydrates in poplar roots infected by Fusarium wilt

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Abstract

Advances in carbohydrate metabolism prompted its essential role in defense priming and sweet immunity during plant-pathogen interactions. Nevertheless, upstream responding enzymes in the sucrose metabolic pathway and associated carbohydrate derivatives underlying fungal pathogen challenges remain to be deciphered in Populus, a model tree species. In silico deduction of genomic features, including phylogenies, exon/intron distributions, cis-regulatory elements, and chromosomal localization, identified 59 enzyme genes (11 families) in the Populus genome. Spatiotemporal expression of the transcriptome and the quantitative real-time PCR revealed a minuscule number of isogenes that were predominantly expressed in roots. Upon the pathogenic Fusarium solani (Fs) exposure, dynamic changes in the transcriptomics atlas and experimental evaluation verified Susy (PtSusy2 and 3), CWI (PtCWI3), VI (PtVI2), HK (PtHK6), FK (PtFK6), and UGPase (PtUGP2) families, displaying promotions in their expressions at 48 and 72 h of post-inoculation (hpi). Using the gas chromatography-mass spectrometry (GC–MS)-based non-targeted metabolomics combined with a high-performance ion chromatography system (HPICS), approximately 307 metabolites (13 categories) were annotated that led to the quantification of 46 carbohydrates, showing marked changes between three compared groups. By contrast, some sugars (e.g., sorbitol, L-arabitol, trehalose, and galacturonic acid) exhibited a higher accumulation at 72 hpi than 0 hpi, while levels of α-lactose and glucose decreased, facilitating them as potential signaling molecules. The systematic overview of multi-omics approaches to dissect the effects of Fs infection provides theoretical cues for understanding defense immunity depending on fine-tuned Suc metabolic gene clusters and synergistically linked carbohydrate pools in trees.

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Acknowledgements

The authors would like to thank the National Natural Science Foundation of China, the Natural Science Foundation of Jiangsu Province Priority, and the Academic Program Development of Jiangsu Higher Education Institutions. Thanks to Dr. Sebastian Wolf for the support with the final revision of the manuscript.

Funding

This research is supported by the Scientific and TechnologicalInnovation 2030-Major Project of the Biological Breeding in Agriculture (2023ZD04056), the National Natural Science Foundation of China (31870589; 31700525), the Natural Science Foundation of Jiangsu Province (BK20170921), and the Undergraduate Innovation and Entrepreneurship Training Programs in Nanjing Forestry University (202010298064Z).

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Conceptualization, T.S. and M.H.; methodology, X.X. and HK. W.; software, X.X., HK.W., and H.W.; validation, X.X., K.Y., and T.H.; formal analysis, X.X., H.W., and K.Y.; investigation, X.X.; resources, H.W. and K.Y.; data curation, X.X., H.W., and K.Y.; writing—original draft preparation, X.X., HK.W., and K.Y.; writing—review and editing, T.S. and M.H.; visualization, H.W., K.Y., and T.H.; supervision, T.S., and M.H; project administration, T.S., M.H., and F.C.; funding acquisition, T.S. and M.H. All authors read and commented on the manuscript.

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Correspondence to Mei Han or Tao Su.

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Xu, X., Wei, H., Yao, K. et al. Integrative omics studies revealed synergistic link between sucrose metabolic isogenes and carbohydrates in poplar roots infected by Fusarium wilt. Plant Mol Biol 114, 29 (2024). https://doi.org/10.1007/s11103-024-01426-z

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  • DOI: https://doi.org/10.1007/s11103-024-01426-z

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