AbstractRheum pumilum stands as both a quintessential alpine plant and a significant traditional Chinese and Tibetan medicinal herb. Unraveling the molecular intricacies of seed germination in Rh. pumilum not only unveils the genetic foundations of plant seed germination strategies in high-altitude environments but also offers insights for cultivating Rh.

摘要细叶大黄既是一种典型的高山植物，也是一种重要的中藏药。解开Rh.pumilum种子萌发的分子复杂性不仅揭示了高海拔环境中植物种子萌发策略的遗传基础，而且为培养Rh提供了见解。

pumilum medicinal materials. Employing transcriptome sequencing and the Weighted Gene Co-expression Network Analysis, this study delved into the shifts in gene expression levels across various stages of seed germination in Rh. pumilum. The process of seed germination in Rh. pumilum entails a cascade of complex physiological events.

pumilum药材。本研究采用转录组测序和加权基因共表达网络分析，探讨了短小Rh种子萌发不同阶段基因表达水平的变化。短小Rh.种子萌发过程需要一系列复杂的生理事件。

Six hormones (ABA, IAA, ETH, GA, BR, CK) emerged as pivotal players in seeds breaking in shells and the facilitation of rapid seed germination in Rh. pumilum. Fourteen transcription factor families (LOB, GRAS, B3, bHLH, bZIP, EIL, MYB, MYB related, NAC, TCP, WRKY, HSF, PLATZ, and SBP) along with four key genes (E2.4.1.13, EIN3, BZR, and BIN2) were identified that may be associated with both biotic and abiotic environmental stress.

六种激素（ABA，IAA，ETH，GA，BR，CK）成为种子破壳和促进短小Rh种子快速萌发的关键因素。十四个转录因子家族（LOB，GRAS，B3，bHLH，bZIP，EIL，MYB，MYB相关，NAC，TCP，WRKY，HSF，PLATZ和SBP）以及四个关键基因（E2.4.1.13，EIN3，BZR和BIN2）被鉴定可能与生物和非生物环境胁迫有关。

The ETR, ACACA and ATPeV0C genes were linked with energy accumulation during the initial stages of seed germination, CYP707A may play an important role in breaking seed dormancy, while the BRI1 gene may be correlated with swift seed germination. Additionally, several unidentified genes were recognized to play key roles in seed germination of Rh.

ETR、ACACA和ATPeV0C基因与种子萌发初期的能量积累有关，CYP707A可能在打破种子休眠中起重要作用，而BRI1基因可能与种子快速萌发有关。此外，一些未鉴定的基因被认为在Rh的种子萌发中起关键作用。

pumilum, warranting further investigation. Moreover, Rh. pumilum demonstrates full activation of crucial physiological functions such as energy metabolism, signal transduction, and responses to biological and abiotic stresses during the seed breaking in shells. This study provides molecular evidence elucidating the swift se.

pumilum，值得进一步调查。此外，Rh.pumilum在种子破壳过程中表现出能量代谢，信号转导以及对生物和非生物胁迫的反应等关键生理功能的完全激活。这项研究提供了阐明swift se的分子证据。

IntroductionRheum pumilum Maxim is a perennial herbaceous plant belonging to the genus Rheum in the Polygonaceae family1. This species is endemic to the Qinghai-Tibetan Plateau (QTP), and serves as a distinctive representative of the local flora on the QTP2. It thrives primarily in habitats such as sparse shrubbery forests, forest edges, and wet meadows at altitudes ranging from 2800 to 4700 m1.

引言细叶大黄是多年生草本植物，属于蓼科大黄属1。该物种是青藏高原（QTP）特有的，是QTP2上当地植物区系的独特代表。它主要在海拔2800至4700 m1的稀疏灌木林，森林边缘和潮湿草地等栖息地繁衍生息。

Its stem is typically short, measuring only 5–25 cm, an adaptation to the harsh alpine environment characterized by low temperatures, intense ultraviolet light, strong winds, and drought3,4,5. Rh. pumilum is also one of several fundamental varieties of Tibetan medicine Rhubarb, with its dried roots and rhizomes utilized in Tibetan medicine under the name Qumamei6.

它的茎通常很短，只有5-25厘米，适应了以低温、强烈紫外线、强风和干旱为特征的恶劣阿尔卑斯环境3,4,5。右侧。pumilum也是藏药大黄的几个基本品种之一，其干燥的根和根茎在藏药中被称为Qumamei6。

In recent years, escalating demand for traditional Chinese and Tibetan medicines has led to the overexploitation of wild rhubarb, resulting in a significant decline in its resources7. For instance, Lu and Lan (2016) noted an increase in the endangered status of Rh. pumilum from level 3 to level 2 during their assessment of endangered plant resources in Lhasa8.

近年来，对中药和藏药的需求不断上升，导致野生大黄的过度开采，导致其资源显着下降7。例如，Lu和Lan（2016）在评估拉萨濒危植物资源时指出，短小Rh.的濒危状态从3级增加到2级。

Similarly, Sun et al. (2018) found a decline in wild Rhubarb resources during their investigation of Tibetan medicinal plants in Qinghai Province9. Consequently, there is an urgent need for research on rhubarb germplasm resources and artificial domestication.In natural environments, seed germination strategy is crucial for plant distribution and abundance10.

同样，Sun等人（2018）在青海省藏药植物调查期间发现野生大黄资源减少9。因此，迫切需要对大黄种质资源和人工驯化进行研究。在自然环境中，种子萌发策略对植物的分布和丰度至关重要10。

Seed dormancy is an important strategy for controlling germination time in plants11. The current classification system categorizes seed dormancy into five types: morphological dormancy (MD), physiological dormancy (PD), morphophysiological dormancy (MPD), physical dormancy (PY), and a combinational dormancy (.

种子休眠是控制植物发芽时间的重要策略11。目前的分类系统将种子休眠分为五种类型：形态休眠（MD），生理休眠（PD），形态生理休眠（MPD），物理休眠（PY）和组合休眠（。

Comprehensive analysis of the transcriptome revealed a pronounced similarity in the germination process of Rh. pumilum seeds during the LB and MY stages. In the Principal Component Analysis of DEGs, there was substantial overlap between the DEGs in the LB and MY stages (Fig. 3A). Similarly, the functional enrichment analysis of DEGs indicated minimal alteration in functional categories between LB and MY stages, except for slight variations in DEGs quantities (Fig.

转录组的综合分析显示，在LB和MY阶段，短小Rh种子的萌发过程具有明显的相似性。在DEG的主成分分析中，LB和MY阶段的DEG之间存在大量重叠（图3A）。类似地，DEGs的功能富集分析表明LB和MY阶段之间的功能类别变化最小，除了DEGs数量的轻微变化（图）。

S2). Similar germination patterns were observed in Meconopsis integrifolia37, also an alpine plant, and Cinnamomum migao, a traditional Chinese medicine38, suggesting they may employ comparable germination strategies.Furthermore, the survey of Transcription Factors (TFs) revealed identical TF families between LB and MY stages, with no significant disparity in their numbers (Fig. 5A).

S2）。在高山植物Meconopsis integrifolia37和中药肉桂38中观察到类似的发芽模式，表明它们可能采用类似的发芽策略。此外，转录因子（TFs）的调查显示，LB和MY阶段之间的TF家族相同，数量没有显着差异（图5A）。

While multiple genes associated with six hormones exhibited significant expression differences between LB and DZ stages, no such disparities were noted between LB and MY stages (Fig. 4). Hormones and transcription factors play pivotal roles in seed germination, and the expression patterns observed here may represent a unique strategy specific to alpine plants.

虽然与六种激素相关的多个基因在LB和DZ阶段之间表现出显着的表达差异，但在LB和MY阶段之间没有发现这种差异（图4）。激素和转录因子在种子萌发中起着关键作用，这里观察到的表达模式可能代表了高山植物特有的独特策略。

These results underscore the pivotal role of the LB stage in the germination process of Rh. pumilum seeds. Analysis of DEGs functional enrichment during the LB stage revealed the initiation of crucial metabolic activities including energy metabolism, MAPK signal transduction, hormone signal transduction, lipid metabolism, and amino acid metabolism (Fig.

这些结果强调了LB阶段在短小Rh种子萌发过程中的关键作用。对LB阶段DEGs功能富集的分析揭示了关键代谢活动的开始，包括能量代谢、MAPK信号转导、激素信号转导、脂质代谢和氨基酸代谢（图）。

S2). These metabolic processes furnish the substrates, energy, and informational foundation necessary for Rh. pumilum seed germination. Similar functional enrichment results were observed in M. integrifolia and C. migao, sugg.

S2）。这些代谢过程为短小Rh.pumilum种子萌发提供了必要的底物，能量和信息基础。在M.integrifolia和C.migao，sugg中观察到类似的功能富集结果。

Data availability

数据可用性

The transcriptome sequencing data were deposited in the NCBI Sequence Read Archive (SRA) under accession numbers SRR28033215, SRR28033216, SRR28033217, SRR28033218, SRR28033219, SRR28033220, SRR28033221, SRR28033222, SRR28033223.

转录组测序数据以登录号SRR28033215，SRR28033216，SRR28033217，SRR28033218，SRR28033219，SRR28033220，SRR28033221，SRR28033222，SRR28033223保存在NCBI序列读取档案（SRA）中。

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Download referencesFundingThis work was supported by the National Natural Science Foundation of China [Grant Number 32070355]; and Shandong Provincial Natural Science Foundation [Grant Number ZR2020MC030].Author informationAuthor notesThese authors contributed equally: Ailan Wang and Wenjie Guo.Authors and AffiliationsSchool of Life Sciences, Ludong University, Yantai, Shandong, ChinaAilan Wang, Wenjie Guo, Shimeng Wang, Yanfang Wang, Dongrui Kong & Weiwei LiAuthorsAilan WangView author publicationsYou can also search for this author in.

下载参考文献资助这项工作得到了国家自然科学基金（批准号32070355）的支持；和山东省自然科学基金[批准号ZR2020MC030]。作者信息作者注意到这些作者做出了同样的贡献：王爱兰和郭文杰。作者和附属机构鲁东大学生命科学学院，山东烟台，中国王爱兰，郭文杰，王世梦，王燕芳，孔东瑞和魏伟作者王赛兰观点作者出版物您也可以在中搜索这位作者。

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PubMed Google ScholarContributionsA.W. conceived the experiment and wrote the original draft. W.G. and S.W. executed the experiment. Y.W. and D.K. analyzed data. W.L. contributed to analyzing data, visualizing, reviewing and editing the manuscript.Corresponding authorCorrespondence to.

PubMed谷歌学术贡献。W、 构思了这个实验并写了初稿。W、 G.和S.W.进行了实验。Y、 W.和D.K.分析了数据。W、 L.有助于分析数据，可视化，审阅和编辑手稿。对应作者对应。

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Reprints and permissionsAbout this articleCite this articleWang, A., Guo, W., Wang, S. et al. Transcriptome analysis unveiled the genetic basis of rapid seed germination strategies in alpine plant Rheum pumilum.

转载和许可本文引用本文Wang，A.，Guo，W.，Wang，S。等人。转录组分析揭示了高山植物小黄快速种子萌发策略的遗传基础。

Sci Rep 14, 19194 (2024). https://doi.org/10.1038/s41598-024-70320-xDownload citationReceived: 30 April 2024Accepted: 14 August 2024Published: 19 August 2024DOI: https://doi.org/10.1038/s41598-024-70320-xShare this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

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Keywords

关键词

Rheum pumilum

细叶大黄

Transcriptome sequencingSeed germinationHormonesTranscription factors

转录组测序种子发芽激素转录因子

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