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Physiological, transcriptomic, and metabolomic analyses reveal that Pantoea sp. YSD J2 inoculation improves the accumulation of flavonoids in Cyperus esculentus L. var. sativus.

ABSTRACT: Plant growth-promoting microorganisms (PGPMs), such as Pantoea sp. YSD J2, promote plant development and stress resistance, while their role in flavonoids accumulation still needs to be further understood. To investigate the complex flavonoid biosynthesis pathway of Cyperus esculentus L. var. sativus (tigernut), we compared Pantoea sp. YSD J2 inoculation (YSD J2) and water inoculation (CK) groups. YSD J2 significantly elevated the content of indole-3-acetic acid (IAA) and orientin. Furthermore, when analyzing flavonoid metabolome, YSD J2 caused increased levels of uralenol, petunidin-3-O-glucoside-5-O-arabinoside, luteolin-7-O-glucuronide-(2 → 1)-glucuronide, kaempferol-3-O-neohesperidoside, cyanidin-3-O-(2″-O-glucosyl)glucoside, kaempferol-3-O-glucuronide-7-O-glucoside, quercetin-3-O-glucoside, luteolin-7-O-glucuronide-(2 → 1)-(2″-sinapoyl)glucuronide, and quercetin-4'-O-glucoside, which further enhanced antioxidant activity. We then performed RNA-seq and LC-MS/MS, aiming to validate key genes and related flavonoid metabolites under YSD J2 inoculation, and rebuild the gene-metabolites regulatory subnetworks. Furthermore, the expression patterns of the trans cinnamate 4-monooxygenase (CYP73A), flavonol-3-O-L-rhamnoside-7-O-glucosyltransferase (UGT73C6), shikimate O-hydroxycinnamoyltransferase (HCT), chalcone isomerase (CHI), flavonol synthase (FLS), and anthocyanidin synthase (ANS) genes were confirmed by qRT-PCR. Additionally, 4 transcription factors (TF) (especially bHLH34, Cluster-37505.3) under YSD J2 inoculation are also engaged in regulating flavonoid accumulation. Moreover, the current work sheds new light on studying the regulatory effect of Pantoea sp. YSD J2 on tigernut development and flavonoid biosynthesis.

SUBMITTER: Wang S

PROVIDER: S-EPMC11367128 | biostudies-literature | 2024 Aug

REPOSITORIES: biostudies-literature

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Physiological, transcriptomic, and metabolomic analyses reveal that Pantoea sp. YSD J2 inoculation improves the accumulation of flavonoids in Cyperus esculentus L. var. sativus.

Wang Saisai S Huang Yanna Y Sun Yu Y Wang Jinbin J Tang Xueming X

Heliyon 20240808 16

Plant growth-promoting microorganisms (PGPMs), such as Pantoea sp. YSD J2, promote plant development and stress resistance, while their role in flavonoids accumulation still needs to be further understood. To investigate the complex flavonoid biosynthesis pathway of Cyperus esculentus L. var. sativus (tigernut), we compared Pantoea sp. YSD J2 inoculation (YSD J2) and water inoculation (CK) groups. YSD J2 significantly elevated the content of indole-3-acetic acid (IAA) and or ...[more]

PMID: 39224290

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Project description:BackgroundYellow nutsedge (Cyperus esculentus, known as 'YouShaDou' in China, YSD) and purple nutsedge (Cyperus rotundus, known as 'XiangFuZi' in China, XFZ), closely related Cyperaceae species, exhibit significant differences in triacylglycerol (TAG) accumulation within their tubers, a key factor in carbon flux repartitioning that highly impact the total lipid, carbohydrate and protein metabolisms. Previous studies have attempted to elucidate the carbon anabolic discrepancies between these two species, however, a lack of comprehensive genome-wide annotation has hindered a detailed understanding of the underlying molecular mechanisms.ResultsThis study utilizes transcriptomic analyses, supported by a comprehensive YSD reference genome, and metabolomic profiling to uncover the mechanisms underlying the major carbon perturbations between the developing tubers of YSD and XFZ germplasms harvested in Yunnan province, China, where the plant biodiveristy is renowned worldwide and may contain more genetic variations relative to their counterparts in other places. Our findings indicate distinct expression patterns of key regulatory genes involved in TAG biosynthesis and lipid droplet formation, including transcriptional factors and structural genes such as ABI3 transcriptional factor, rate-limiting enzymes GPAT3/6/9 and DGAT2/3, and oleosin and caleosin homologs. Furthermore, our omics data suggest that these differences in gene expression are not the sole contributors to the diverse tuber compositions. Instead, complex interactions among highly regulated catalytic reactions, governing carbohydrate, protein, and species-specific metabolite metabolisms, such as starch and sucrose metabolic pathways, flavonoid and amino acids biosynthetic pathways, collectively contribute to the pronounced carbon anabolic differentiation primarily evident in TAG accumulation, as well as the starch properties in mature tubers.ConclusionThis study offers new metabolic insights into the high-value underground non-photosynthetic tissues of Cyperaceae species, which harbors not only high biomass productivity but also abundant nutrients as favorable food or industrial sources in the modern agriculture. The detailed omics analyses aim to deepen our understanding of the Cyperaceae species, which may potentially broaden their application values and facilitate the molecular breeding of better varieties to ameliorate the food safety problem.

Dataset Information

Physiological, transcriptomic, and metabolomic analyses reveal that Pantoea sp. YSD J2 inoculation improves the accumulation of flavonoids in Cyperus esculentus L. var. sativus.

Publications

Physiological, transcriptomic, and metabolomic analyses reveal that <i>Pantoea</i> sp. YSD J2 inoculation improves the accumulation of flavonoids in <i>Cyperus esculentus</i> L. var. sativus.

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