Cycloartenol-derived triterpenoid pathway genes alter the root metabolome and microbiome in tomato

IF 5.7 2区生物学 Q1 PLANT SCIENCES

Plant Physiology and Biochemistry Pub Date : 2025-10-01 DOI:10.1016/j.plaphy.2025.110584

Alessandra Guerrieri , Davar Abedini , Fred White , Jurre Bleeker , Gertjan Kramer , Lemeng Dong

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引用次数: 0

Abstract

Plant triterpenoids derived from cycloartenol are central to sterol homeostasis and specialized metabolite production, yet their roles in shaping rhizosphere interactions remain poorly understood. Here, we investigated the function of key cycloartenol-derived triterpenoid biosynthetic genes in tomato (Solanum lycopersicum) by transiently silencing CYCLOARTENOL SYNTHASE 1 (SlCAS1), STEROL METHYLTRANSFERASE 1 (SlSMT1), STEROL SIDE CHAIN REDUCTASE 2 (SlSSR2), and PHYTOENE DESATURASE (SlPDS). SlCAS1 suppression caused severe growth inhibition, confirming the essential role of cycloartenol for plant development. Silencing of SlSMT1 and SlSSR2 altered root sterol composition, with SlSMT1 reducing β-sitosterol and stigmasterol, and SlSSR2 causing decreases in cholesterol as well as significant reductions in steroidal glycoalkaloids (SGAs) and steroidal saponins (SAs). By contrast, SlPDS silencing unexpectedly led to elevated sterol levels and broad metabolome shifts. Untargeted metabolomics revealed gene-specific alterations in root and exudate profiles, while molecular networking highlighted the rapid loss of SGAs in exudates, suggesting microbial degradation. Integration of metabolomic and 16S rRNA sequencing data showed that changes in sterols, SGAs, and saponins were associated with distinct bacterial families, including Comamonadaceae and Sphingomonadaceae. Together, these findings demonstrate that cycloartenol-derived triterpenoid pathway genes strongly influence root metabolite composition and shape the assembly of tomato root-associated microbial communities.

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环arten醇衍生的三萜途径基因改变番茄根代谢组和微生物组

由环蒿烯醇衍生的植物三萜是固醇稳态和专门代谢物生产的核心，但它们在形成根际相互作用中的作用仍然知之甚少。本研究通过对番茄（Solanum lycopersicum）中环artenol合成酶1 （SlCAS1）、甾醇甲基转移酶1 （SlSMT1）、甾醇侧链还原酶2 （SlSSR2）和PHYTOENE去饱和酶（SlPDS）的瞬时沉默，研究了环artenol衍生的关键三萜生物合成基因的功能。SlCAS1的抑制引起了严重的生长抑制，证实了环蒿烯醇在植物发育中的重要作用。SlSMT1和SlSSR2的沉默改变了根固醇组成，SlSMT1减少了β-谷甾醇和豆甾醇，SlSSR2导致胆固醇降低以及甾体糖生物碱（SGAs）和甾体皂苷（SAs）的显著减少。相比之下，SlPDS沉默意外地导致胆固醇水平升高和广泛的代谢组变化。非靶向代谢组学揭示了根和渗出物谱的基因特异性改变，而分子网络强调了渗出物中SGAs的快速损失，表明微生物降解。代谢组学和16S rRNA测序数据的整合显示，甾醇、SGAs和皂苷的变化与不同的细菌科有关，包括Comamonadaceae和Sphingomonadaceae。总之，这些发现表明，环artenol衍生的三萜途径基因强烈影响根代谢物组成，并塑造番茄根相关微生物群落的组装。

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来源期刊

Plant Physiology and Biochemistry 生物-植物科学

CiteScore

11.10

自引率

3.10%

发文量

410

审稿时长

33 days

期刊介绍： Plant Physiology and Biochemistry publishes original theoretical, experimental and technical contributions in the various fields of plant physiology (biochemistry, physiology, structure, genetics, plant-microbe interactions, etc.) at diverse levels of integration (molecular, subcellular, cellular, organ, whole plant, environmental). Opinions expressed in the journal are the sole responsibility of the authors and publication does not imply the editors'' agreement. Manuscripts describing molecular-genetic and/or gene expression data that are not integrated with biochemical analysis and/or actual measurements of plant physiological processes are not suitable for PPB. Also "Omics" studies (transcriptomics, proteomics, metabolomics, etc.) reporting descriptive analysis without an element of functional validation assays, will not be considered. Similarly, applied agronomic or phytochemical studies that generate no new, fundamental insights in plant physiological and/or biochemical processes are not suitable for publication in PPB. Plant Physiology and Biochemistry publishes several types of articles: Reviews, Papers and Short Papers. Articles for Reviews are either invited by the editor or proposed by the authors for the editor''s prior agreement. Reviews should not exceed 40 typewritten pages and Short Papers no more than approximately 8 typewritten pages. The fundamental character of Plant Physiology and Biochemistry remains that of a journal for original results.