Xianglei Xu, Haikun Wei, Kejun Yao, Hao Wu, Tingting Huang, Mei Han, Tao Su, Fuliang Cao
{"title":"Integrative omics studies revealed synergistic link between sucrose metabolic isogenes and carbohydrates in poplar roots infected by Fusarium wilt","authors":"Xianglei Xu, Haikun Wei, Kejun Yao, Hao Wu, Tingting Huang, Mei Han, Tao Su, Fuliang Cao","doi":"10.1007/s11103-024-01426-z","DOIUrl":null,"url":null,"abstract":"<p>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 <i>Populus</i>, a model tree species. In silico deduction of genomic features, including phylogenies, exon/intron distributions, <i>cis</i>-regulatory elements, and chromosomal localization, identified 59 enzyme genes (11 families) in the <i>Populus</i> 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 <i>Fusarium solani</i> (Fs) exposure, dynamic changes in the transcriptomics atlas and experimental evaluation verified Susy (<i>PtSusy2</i> and <i>3</i>), CWI (<i>PtCWI3</i>), VI (<i>PtVI2</i>), HK (<i>PtHK6</i>), FK (<i>PtFK6</i>), and UGPase (<i>PtUGP2</i>) 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.</p>","PeriodicalId":20064,"journal":{"name":"Plant Molecular Biology","volume":null,"pages":null},"PeriodicalIF":3.9000,"publicationDate":"2024-03-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Molecular Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1007/s11103-024-01426-z","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
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.
期刊介绍:
Plant Molecular Biology is an international journal dedicated to rapid publication of original research articles in all areas of plant biology.The Editorial Board welcomes full-length manuscripts that address important biological problems of broad interest, including research in comparative genomics, functional genomics, proteomics, bioinformatics, computational biology, biochemical and regulatory networks, and biotechnology. Because space in the journal is limited, however, preference is given to publication of results that provide significant new insights into biological problems and that advance the understanding of structure, function, mechanisms, or regulation. Authors must ensure that results are of high quality and that manuscripts are written for a broad plant science audience.