PDS5基因突变增强拟南芥TAD样结构域的形成-动脉网

Mutations of PDS5 genes enhance TAD-like domain formation Arabidopsis thaliana

Nature 等信源发布 2024-10-29 12:47

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AbstractIn eukaryotes, topologically associating domains (TADs) organize the genome into functional compartments. While TAD-like structures are common in mammals and many plants, they are challenging to detect in Arabidopsis thaliana. Here, we demonstrate that Arabidopsis PDS5 proteins play a negative role in TAD-like domain formation.

摘要在真核生物中，拓扑关联域（TAD）将基因组组织成功能区室。虽然TAD样结构在哺乳动物和许多植物中很常见，但它们在拟南芥中很难检测到。在这里，我们证明拟南芥PDS5蛋白在TAD样结构域形成中起负面作用。

Through Hi-C analysis, we show that mutations in PDS5 genes lead to the widespread emergence of enhanced TAD-like domains throughout the Arabidopsis genome, excluding pericentromeric regions. These domains exhibit increased chromatin insulation and enhanced chromatin interactions, without significant changes in gene expression or histone modifications.

通过Hi-C分析，我们表明PDS5基因的突变导致整个拟南芥基因组中广泛出现增强的TAD样结构域，不包括着丝粒周围区域。这些结构域表现出增加的染色质绝缘和增强的染色质相互作用，而基因表达或组蛋白修饰没有显着变化。

Our results suggest that PDS5 proteins are key regulators of genome architecture, influencing 3D chromatin organization independently of transcriptional activity. This study provides insights into the unique chromatin structure of Arabidopsis and the broader mechanisms governing plant genome folding..

我们的结果表明，PDS5蛋白是基因组结构的关键调节因子，独立于转录活性影响3D染色质组织。这项研究为拟南芥独特的染色质结构和控制植物基因组折叠的更广泛机制提供了见识。。

IntroductionThe three-dimensional organization of chromatin is essential for gene expression, DNA replication, and damage repair. In mammals, Hi-C studies have revealed hierarchical genome structures, notably identifying topologically associating domains (TADs) as key features1. TADs are characterized by strong internal chromatin interactions and reduced contacts with neighboring regions1.

引言染色质的三维组织对于基因表达，DNA复制和损伤修复至关重要。在哺乳动物中，Hi-C研究揭示了分层的基因组结构，特别是将拓扑关联域（TADs）确定为关键特征1。TAD的特征在于强烈的内部染色质相互作用和与邻近区域的接触减少1。

Genes residing within the confines of a single TAD often exhibit similar expression patterns, enabling coordinated regulatory control. TAD boundaries, marked by insulators, prevent unnecessary interactions between elements like enhancers in adjacent TADs, ensuring precise gene regulation. The spatial proximity within TADs enhances interactions among genes and regulatory elements, affecting chromatin accessibility and gene transcription2.

位于单个TAD范围内的基因通常表现出相似的表达模式，从而能够进行协调的调控。由绝缘体标记的TAD边界可以防止相邻TAD中增强子等元素之间不必要的相互作用，从而确保精确的基因调控。TAD内的空间接近增强了基因和调控元件之间的相互作用，影响了染色质的可及性和基因转录2。

Disruptions in TAD distribution, often due to genomic rearrangements, can lead to misregulated genes and are linked to diseases such as cancer and developmental disorders3,4,5. There are two mechanisms for establishing TADs. The first type, which shows particularly strong chromatin contacts between TAD borders, involves cohesin and CTCF protein complexes.

TAD分布的破坏，通常是由于基因组重排，可能导致基因失调，并与癌症和发育障碍等疾病有关3,4,5。建立TAD有两种机制。。

They create looped structures by extruding chromatin loops until they reach a pair of oppositely oriented CTCF binding sites overlapping with TAD boundaries6,7,8,9. The second type of TAD, where the boundary and intra-TAD contact strengths are similar, is shaped by gene expression, especially at TAD borders.

它们通过挤出染色质环来创建环状结构，直到它们到达一对与TAD边界重叠的相反方向的CTCF结合位点6,7,8,9。第二种类型的TAD，其边界和TAD内接触强度相似，由基因表达形成，特别是在TAD边界处。

This type of TAD also correlates with the epigenomic landscape10,11.Surprisingly, TADs, which typically range in size from dozens to hundreds of kilobase pairs, are not prominent in the Arabidopsis genome12,13,14. Nonetheless, with deep sequencing of Arabidopsis Hi-C libraries, or alternative app.

。尽管如此，通过对拟南芥Hi-C文库或替代应用程序进行深度测序。

pds5 mutantsCohesin complexes in plants and animals have conserved function in regulating chromosome segregation during cell division22. In mammals, cohesin is also indispensable to define 3D genome organization. We conducted Hi-C experiments to assess the potential impact of the perturbation in cohesin activities on the Arabidopsis 3D genome (Supplementary Data 1).

植物和动物中的pds5突变体色素复合物在调节细胞分裂过程中的染色体分离方面具有保守功能22。在哺乳动物中，粘着蛋白对于定义3D基因组组织也是必不可少的。我们进行了Hi-C实验，以评估粘着蛋白活性扰动对拟南芥3D基因组的潜在影响（补充数据1）。

Since loss-of-function mutants of Arabidopsis cohesin subunits SMC1 and SMC3 are not viable, we selected mutants that potentially affect cohesin-chromatin interactions23. To this end, wapl1 wapl2 double mutants (hereafter referred to as wapl1/2) and pds5a pds5b pds5c pds5e quadruple mutants (hereafter referred to as pds5a/b/c/e) were used for Hi-C experiments8,24,25.At the chromosomal level, the Hi-C maps of wapl1/2, pds5a/b/c/e, and wild-type (WT) appeared similar (Supplementary Fig. 1a and Supplementary Fig. 2).

由于拟南芥粘着蛋白亚基SMC1和SMC3的功能丧失突变体不可行，我们选择了可能影响粘着蛋白-染色质相互作用的突变体23。为此，将wapl1 wapl2双突变体（以下称为wapl1/2）和pds5a pds5b pds5c pds5e四重突变体（以下称为pds5a/b/c/e）用于Hi-c实验8,24,25。在染色体水平上，wapl1/2，pds5a/b/c/e和野生型（WT）的Hi-c图谱似乎相似（补充图1a和补充图2）。

However, closer inspection of the diagonal revealed striking differences in local chromatin contacts (i.e., contacts that span distances up to a few hundred kilobase pairs) in the pds5a/b/c/e mutants (Fig. 1a, Supplementary Figs. 1a–c). In pds5a/b/c/e, TAD-like domains were clearly visible and widely distributed through the genome, except in the pericentromeric regions, which remained constitutive heterochromatin.

然而，仔细检查对角线发现，在pds5a/b/c/e突变体中，局部染色质接触（即跨越数百千碱基对的接触）存在显着差异（图1a，补充图1a-c）。在pds5a/b/c/e中，TAD样结构域清晰可见，并在基因组中广泛分布，但在着丝粒周围区域除外，该区域仍然是组成型异染色质。

Consistently, chromatin interaction decay plots showing how contact strength decreases with genomic distance revealed specific changes in chromosome arm regions of pds5a/b/c/e compared to WT, indicating that the former adopted distinct chromatin packing patterns (Supplementary Fig. 1d).Fig. 1: Analysis of TAD-like domains in pds5a/b/c/e.a Prominent TAD-like structures in pds5a/b/c/e, showcased by a representative 1 Mb genomic region.

一致地，显示接触强度如何随基因组距离降低的染色质相互作用衰减图显示，与WT相比，pds5a/b/c/e的染色体臂区域发生了特定变化，表明前者采用了不同的染色质堆积模式（补充图1d）。图1:pds5a/b/c/e中TAD样结构域的分析。pds5a/b/c/e中突出的TAD样结构，由代表性的1Mb基因组区域显示。

b Comparison of insulation score profile of a 1 Mb regi.

b比较1 Mb区域的绝缘评分曲线。

pds5 TAD-like domains do not alter other chromatin featuresGiven that PDS5s redundantly regulate Arabidopsis seedling development27 and that pds5a/b/c/e exhibited the most altered transcriptome profile (Supplementary Fig. 4 and Supplementary Data 4–7), we presumed that chromatin organization was most affected in pds5a/b/c/e compared to other lower-order mutants.

pds5 TAD样结构域不会改变其他染色质特征鉴于PDS5s冗余调节拟南芥幼苗发育27，并且pds5a/b/c/e表现出改变最多的转录组谱（补充图4和补充数据4-7），我们推测与其他低阶突变体相比，染色质组织在pds5a/b/c/e中受影响最大。

Thus, we deep-sequenced the Hi-C libraries from pds5a/b/c/e for further analyzes (Supplementary Data 1). When compared to WT, approximately 15% of the chromatin in pds5a/b/c/e exhibited AB compartment swaps, indicating mild rewiring of genome topology at the chromosomal level (Supplementary Figs. 5a–d and Supplementary Data 8).

因此，我们对来自pds5a/b/C/e的Hi-C文库进行了深度测序，以进行进一步分析（补充数据1）。。

Interestingly, these AB compartment swaps were not associated with changes in active (e.g., H3K4me3) or repressive (e.g., H3K27me3 and H3K9me2) histone marks, which were enriched in A and B compartment regions, respectively (Supplementary Fig. 5b–f and Supplementary Data 9-14). Furthermore, while A and B compartment identities are typically linked to active and inactive gene expression, the switch in compartment identity in pds5a/b/c/e occurred independently of transcriptomic changes (Supplementary Figs. 5g, h).Next, we examined the newly emerged local chromatin contact patterns on the Hi-C map of pds5a/b/c/e.

有趣的是，这些AB区室交换与活性（例如H3K4me3）或抑制性（例如H3K27me3和H3K9me2）组蛋白标记的变化无关，这些标记分别富集在A和B区室区域（补充图5b-f和补充数据9-14）。此外，虽然A和B区室身份通常与活性和非活性基因表达相关，但pds5a/B/c/e中的区室身份转换独立于转录组学变化而发生（补充图5g，h）。接下来，我们检查了pds5a/b/C/e的Hi-C图上新出现的局部染色质接触模式。

By calculating insulation scores, we identified genomic regions within pds5a/b/c/e that exhibited strong chromatin insulation (Fig. 1b and Supplementary Data 15). Notably, most of the insulated regions in pds5a/b/c/e already displayed weak insulation patterns in WT plants (Fig. 1c–e). Consistent with a recent report, these insulated regions were enriched with 5’ flanking regions of gene transcription start sites16 (Supplementary Fig. 6).

通过计算绝缘分数，我们确定了pds5a/b/c/e中表现出强烈染色质绝缘的基因组区域（图1b和补充数据15）。。与最近的报道一致，这些绝缘区域富含基因转录起始位点16的5'侧翼区域（补充图6）。

We also annotated TAD-like domains in pds5a/b.

我们还在pds5a/b中注释了TAD样域。

Along with the emergence of TAD-like domains, extensive changes in local chromatin contacts occurred in pds5a/b/c/e. To better understand the chromatin interaction network in pds5a/b/c/e, we identified chromatin contacts with statistical significance (referred to as “chromatin loops”) in WT and mutant plants31.

随着TAD样结构域的出现，pds5a/b/c/e中局部染色质接触发生了广泛变化。为了更好地了解pds5a/b/c/e中的染色质相互作用网络，我们在WT和突变植物中鉴定了具有统计学意义的染色质接触（称为“染色质环”）31。

Both genotypes exhibited similar chromatin loops at short distances (<10 kb), but the fraction of shared chromatin loops decreased dramatically at longer distances (10–100 kb) (Fig. 2a). Among the long-distance chromatin loops (10–100 kb), approximately 40% of loop-forming regions in WT plants overlapped with protein-coding genes, whereas this percentage rose to 65% in pds5a/b/c/e mutants, partly due to a lower occurrence of transposons overlapping with pds5a/b/c/e loops (Fig. 2a, b).Fig.

两种基因型在短距离（<10kb）处均表现出相似的染色质环，但在较长距离（10-100kb）处，共享染色质环的比例急剧下降（图2a）。在长距离染色质环（10-100kb）中，WT植物中大约40%的环形成区域与蛋白质编码基因重叠，而在pds5a/b/c/e突变体中，这一百分比上升到65%，部分原因是转座子与pds5a/b/c/e环重叠的发生率较低（图2a，b）。图。

2: Comparison of epigenetic features associated with chromatin loops and gene expression between WT and pds5a/b/c/e.a Proportion of chromatin loop sizes in WT and pds5a/b/c/e. Loops smaller than 10 kb, between 10 and 50 kb, and bigger than 50 kb are included. Blue scaled bars indicate those loops in pds5a/b/c/e which are also identified in wild-type plants.

2： WT和pds5a/b/c/e之间与染色质环和基因表达相关的表观遗传特征的比较.WT和pds5a/b/c/e中染色质环大小的比例。包括小于10kb，10-50kb和大于50kb的环。蓝色刻度条表示pds5a/b/c/e中的那些环，这些环也在野生型植物中被鉴定。

b, c Genomic features at regions annotated with chromatin loops, which are illustrated as the green area in each plot. The blue and black curves refer to individual loop anchor regions. d–h Enrichment of epigenetic marks around chromatin regions that form loops with protein-coding genes. These regions are divided into five groups according to expression levels of their interacting protein-coding genes.

b、 c用染色质环注释的区域的基因组特征，其在每个图中显示为绿色区域。蓝色和黑色曲线表示单个循环锚点区域。d–h富集染色质区域周围的表观遗传标记，这些区域与蛋白质编码基因形成环。根据它们相互作用的蛋白质编码基因的表达水平，将这些区域分为五组。

The color gradient from blue via gray to red represents ascending gene expression.Full size imageFor the long-distance chromatin loops in pds5a/b/c/e, we examined their epigenetic profiles in relation to gene expression. Curren.

从蓝色到灰色到红色的颜色梯度代表上升的基因表达。。科伦。

Data availability

数据可用性

Data supporting the findings of this work are available within the paper and its Supplementary Information files. A reporting summary for this article is available as a Supplementary Information file. Short read data of in situ Hi-C, ChIP-seq, ATAC-seq, and RNA-seq are publicly available at NCBI Sequence Read Archive under accession number PRJNA1043456.

本文及其补充信息文件中提供了支持这项工作结果的数据。本文的报告摘要可作为补充信息文件提供。原位Hi-C，ChIP-seq，ATAC-seq和RNA-seq的短读数据可在NCBI Sequence read Archive上公开获得，登录号为PRJNA1043456。

Large datasets, such as normalized Hi-C matrices and BigWig ChIP-seq and ATAC-seq track files are available in the Figshare repository [https://doi.org/10.6084/m9.figshare.24533263.v1]. The epigenetic profile of various histone marks is available from our previous publication43. Source data are provided with this paper..

Figshare存储库中提供了大型数据集，例如标准化的Hi-C矩阵以及BigWig ChIP-seq和ATAC-seq轨迹文件[https://doi.org/10.6084/m9.figshare.24533263.v1]。各种组蛋白标记的表观遗传学特征可从我们之前的出版物43中获得。本文提供了源数据。。

Code availability

代码可用性

The code for Hi-C read mapping, filtering, and matrix normalization is available in the GitHub repository [https://github.com/changliu325/Arabidopsis_crwn1_chromatin/tree/master/HiC]. The code for TAD-like domain calling and insulation score computation is also available in the GitHub repository [https://github.com/changliu325/pds5_chromatin]..

GitHub存储库中提供了用于Hi-C读取映射、过滤和矩阵规范化的代码[https://github.com/changliu325/Arabidopsis_crwn1_chromatin/tree/master/HiC]。GitHub存储库中还提供了类似TAD的域调用和绝缘分数计算代码[https://github.com/changliu325/pds5_chromatin]。。

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Download referencesAcknowledgementsWe thank Manuela Knauft and Jaqueline Pohl for their excellent technical assistance during Hi-C library preparation and sequencing. We thank Arp Schnittger for providing us wapl1/2 mutants. We thank computing support by the High Performance and Cloud Computing Group at the Zentrum für Datenverarbeitung of the University of Tübingen, the state of Baden-Württemberg through bwHPC and the German Research Foundation (DFG) through grant no.

下载参考文献致谢我们感谢Manuela Knauft和Jaqueline Pohl在Hi-C文库制备和测序过程中提供的出色技术帮助。我们感谢Arp Schnittger为我们提供wapl1/2突变体。我们感谢蒂宾根大学Zentrum für Datenverabeitung的高性能和云计算小组通过bwHPC和德国研究基金会（DFG）通过第号赠款提供的计算支持。

INST 37/935-1 FUGG. This work was supported by DFG under grants No. JI347/6-1 and LI 2862/8-1, the Federal Ministry of Education and Research (BMBF) under grant No. 100489995, and the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No.

仪器37/935-1 FUGG。这项工作得到了DFG的资助，资助号为JI347/6-1和LI 2862/8-1，联邦教育与研究部（BMBF）的资助号为100489995，以及欧盟地平线2020研究与创新计划（资助协议号为。

757600).FundingOpen Access funding enabled and organized by Projekt DEAL.Author informationAuthor notesThese authors contributed equally: Anna-Maria Göbel, Sida Zhou.Authors and AffiliationsDepartment of Epigenetics, Institute of Biology, University of Hohenheim, Garbenstrasse 30, Stuttgart, GermanyAnna-Maria Göbel, Zhidan Wang, Sofia Tzourtzou & Chang LiuInstitute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str.

757600）。资金开放获取资金由Projekt交易启用和组织。作者信息作者注意到这些作者做出了同样的贡献：Anna Maria Göbel，Sida Zhou。作者和附属机构霍恩海姆大学生物研究所表观遗传学系，斯图加特Garbenstrasse 30，GermanyAnna Maria Göbel，Zhidan Wang，Sofia Tzoutzou＆Chang Liu波茨坦大学生物化学与生物学研究所，Karl-Liebknecht-Str。

24-25, Potsdam-Golm, GermanySida Zhou, Shiwei Zheng & Hua JiangLeibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, GermanySida Zhou, Axel Himmelbach, Shiwei Zheng & Hua JiangMax Planck Institute of Molecular Plant Physiology, Potsdam-Golm, GermanySida Zhou, Shiwei Zheng & Hua JiangDepartamento de Genética, Fisiología y Microbiología, Facultad de Ciencias Biológicas, Universidad Complutense, Madrid, SpainMónica PradilloAuthorsAnna-Maria GöbelView author publicationsYou can also search for this author in.

24-25岁，波茨坦-戈尔姆，GermanySida Zhou，Shiwei Zheng&Hua JiangLeibniz植物遗传学和作物植物研究所（IPK），Gatersleben，GermanySida Zhou，Axel Himmelbach，Shiwei Zheng&Hua JiangMax-Planck分子植物生理学研究所，波茨坦-戈尔姆，GermanySida Zhou，Shiwei Zheng&Hua JiangLeibniz Genética，Fisiologia Microbiologia，Facultad de Ciencias Biológicas，Universidad Complutense，Madrid，SpainMónica PradilloAuthorsAnna Maria GöbelView作者出版物您也可以在中搜索此作者。

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PubMed Google ScholarContributionsH.J. and C.L. conceived and designed the experiments. A.M.G., H.J., and C.L. wrote the manuscript. A.M.G., S.Z., Z.W., S.T., S.Z., M.P., A.H. executed the experimental procedures. All authors discussed the results and commented on the manuscript.Corresponding authorsCorrespondence to.

PubMed谷歌学术贡献。J、。A、 M.G.，H.J。和C.L.撰写了手稿。A、 M.G.，S.Z.，Z.W.，S.T.，S.Z.，M.P.，A.H.执行了实验程序。所有作者都讨论了结果并对稿件进行了评论。通讯作者通讯。

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Reprints and permissionsAbout this articleCite this articleGöbel, AM., Zhou, S., Wang, Z. et al. Mutations of PDS5 genes enhance TAD-like domain formation Arabidopsis thaliana.

转载和许可本文引用本文Göbel，AM。，Zhou，S。，Wang，Z。等人。PDS5基因的突变增强了拟南芥TAD样结构域的形成。

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