INVITED REVIEWS
Research Progress of Spatiotemporal Transcriptomes
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- 1Guangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Life Sciences, South China Agricultural University, Guangzhou 510642, China
2State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen 518083, China
3Shenzhen Branch of Guangdong Laboratory for Lingnan Modern Agriculture, Shenzhen 518083, China
Received date: 2022-09-12
Accepted date: 2023-01-10
Online published: 2023-01-10
Abstract
Spatiotemporal heterogeneity is a key factor for functional differentiation in different tissues and plays an important role in regulating cell fate. Spatiotemporal transcriptomic sequencing (stRNA-seq) is an emerging omics technology that combines quantitative transcriptome with high-resolution tissue imaging. It anchors expression data to the physical map of a target organ or tissue and molecularly characterizes tissue sections and cell layers via unbiased bioinformatic analysis, which reflects the spatiotemporal heterogeneity of gene expression abundances within specific cells. Benefiting from the rapid development of high-throughput sequencing, the spatiotemporal heterogeneity of gene expression in various cells can be explored by new experimental approaches. In this review, we first briefly introduce the principle and development process of stRNA-seq, providing readers an overview on the characteristics, advantages and disadvantages of different stRNA-seq techniques. Then, we summarize the applications of stRNA-seq in animals, plants and microorganisms, which provide theoretical references for the systematic research of stRNA-seq in future.
Cite this article
Yubin Xiao, Zixu Zhang, Yuzhu Wang, Huan Liu, Letian Chen . Research Progress of Spatiotemporal Transcriptomes[J]. Chinese Bulletin of Botany, 2023 , 58(2) : 214 -232 . DOI: 10.11983/CBB22220
References
| [1] | 操利超, 巴颖, 张核子 (2022). 单细胞测序方法研究进展. 生物信息学 20, 91-99. |
| [2] | 崔桂忠, 彭广敦, 景乃禾 (2020). 高精度时空转录组揭示小鼠早期胚胎三胚层细胞谱系发生过程. 中国细胞生物学学报 42, 1-8. |
| [3] | 牛艳丽, 柏胜龙, 王麒云, 刘凌云 (2017). 单细胞组学技术及其在植物保卫细胞研究中的应用. 植物学报 52, 788-796. |
| [4] | 邱丹丹, 蒋松 (2022). 空间转录组技术在肾脏疾病研究中的应用. 肾脏病与透析肾移植杂志 31, 256-260. |
| [5] | 项铮, 苏存锦, 潘杰 (2022). 空间转录物组学技术进展及其在神经科学领域中的应用. 中国生物化学与分子生物学报 38, 1486-1492. |
| [6] | 杨佳凤, 陈鹏璐, 龚熹 (2021). 单细胞转录组测序技术在细胞分类中的应用. 中国细胞生物学学报 43, 476-483. |
| [7] | 赵宇豪, 李永盛, 央茂, 王许安, 吴文广, 刘颖斌 (2022). 空间转录组测序技术在肿瘤发生发展机制中的应用及前景. 中华医学杂志 102, 1551-1554. |
| [8] | 朱彬彬, 刘亚慧, 齐大屯, 程倩倩, 李高寒, 高传玉 (2022). 单细胞测序和空间转录组学在心血管疾病研究中的进展. 中国心血管病研究 20, 497-502. |
| [9] | Andersson A, Larsson L, Stenbeck L, Salmén F, Ehinger A, Wu SZ, Al-Eryani G, Roden D, Swarbrick A, Borg ?, Frisén J, Engblom C, Lundeberg J (2021). Spatial deconvolution of HER2-positive breast cancer delineates tumor-associated cell type interactions. Nat Commun 12, 6012. |
| [10] | Asp M, Bergenstr?hle J, Lundeberg J (2020). Spatially resolved transcriptomes-next generation tools for tissue exploration. Bioessays 42, 1900221. |
| [11] | Asp M, Giacomello S, Larsson L, Wu CL, Fürth D, Qian XY, W?rdell E, Custodio J, Reimeg?rd J, Salmén F, ?sterholm C, St?hl PL, Sundstr?m E, ?kesson E, Bergmann O, Bienko M, M?nsson-Broberg A, Nilsson M, Sylvén C, Lundeberg J (2019). A spatiotemporal organ-wide gene expression and cell atlas of the developing human heart. Cell 179, 1647-1660. |
| [12] | Baccin C, Al-Sabah J, Velten L, Helbling PM, Grünschl?ger F, Hernández-Malmierca P, Nombela-Arrieta C, Steinmetz LM, Trumpp A, Haas S (2020). Combined single-cell and spatial transcriptomics reveal the molecular, cellular and spatial bone marrow niche organization. Nat Cell Biol 22, 38-48. |
| [13] | Boisset JC, Vivié J, Grün D, Muraro MJ, Lyubimova A, van Oudenaarden A (2018). Mapping the physical network of cellular interactions. Nat Methods 15, 547-553. |
| [14] | Boyd DF, Allen EK, Randolph AG, Guo XZJ, Weng YC, Sanders CJ, Bajracharya R, Lee NK, Guy CS, Vogel P, Guan WD, Li YM, Liu XQ, Novak T, Newhams MM, Fabrizio TP, Wohlgemuth N, Mourani PM, PALISI Pediatric Intensive Care Influenza PICFLU Investigators, Wight TN, Schultz-Cherry S, Cormier SA, Shaw-Saliba K, Pekosz A, Rothman RE, Chen KF, Yang ZF, Webby RJ, Zhong NS, Crawford JC, Thomas PG (2020). Exuberant fibroblast activity compromises lung function via ADAMTS4. Nature 587, 466-471. |
| [15] | Butler D, Mozsary C, Meydan C, Foox J, Rosiene J, Shaiber A, Danko D, Afshinnekoo E, MacKay M, Sedlazeck FJ, Ivanov NA, Sierra M, Pohle D, Zietz M, Gisladottir U, Ramlall V, Sholle ET, Schenck EJ, Westover CD, Hassan C, Ryon K, Young B, Bhattacharya C, Ng DL, Granados AC, Santos YA, Servellita V, Federman S, Ruggiero P, Fungtammasan A, Chin CS, Pearson NM, Langhorst BW, Tanner NA, Kim Y, Reeves JW, Hether TD, Warren SE, Bailey M, Gawrys J, Meleshko D, Xu D, Couto-Rodriguez M, Nagy-Szakal D, Barrows J, Wells H, O'Hara NB, Rosenfeld JA, Chen Y, Steel PAD, Shemesh AJ, Xiang J, Thierry-Mieg J, Thierry- Mieg D, Iftner A, Bezdan D, Sanchez E, Campion TR Jr, Sipley J, Cong L, Craney A, Velu P, Melnick AM, Shapira S, Hajirasouliha I, Borczuk A, Iftner T, Salvatore M, Loda M, Westblade LF, Cushing M, Wu SX, Levy S, Chiu C, Schwartz RE, Tatonetti N, Rennert H, Imielinski M, Mason CE (2021). Shotgun transcriptome, spatial omics, and isothermal profiling of SARS-CoV-2 infection reveals unique host responses, viral diversification, and drug interactions. Nat Commun 12, 1660. |
| [16] | Cao JY, Packer JS, Ramani V, Cusanovich DA, Huynh C, Daza R, Qiu XJ, Lee C, Furlan SN, Steemers FJ, Adey A, Waterston RH, Trapnell C, Shendure J (2017). Comprehensive single-cell transcriptional profiling of a multicellular organism. Science 357, 661-667. |
| [17] | Carlberg K, Korotkova M, Larsson L, Catrina AI, St?hl PL, Malmstr?m V (2019). Exploring inflammatory signatures in arthritic joint biopsies with spatial transcriptomics. Sci Rep 9, 18975. |
| [18] | Chen A, Liao S, Cheng MN, Ma KL, Wu L, Lai YW, Qiu XJ, Yang J, Xu JS, Hao SJ, Wang X, Lu HF, Chen X, Liu X, Huang X, Li Z, Hong Y, Jiang YJ, Peng J, Liu S, Shen MZ, Liu CY, Li QS, Yuan Y, Wei XY, Zheng HW, Feng WM, Wang ZF, Liu Y, Wang ZH, Yang YZ, Xiang HT, Han L, Qin BM, Guo PC, Lai GY, Mu?oz-Cánoves P, Maxwell PH, Thiery JP, Wu QF, Zhao FX, Chen BC, Li M, Dai X, Wang S, Kuang HY, Hui JH, Wang LQ, Fei JF, Wang O, Wei XF, Lu HR, Wang B, Liu SP, Gu Y, Ni M, Zhang WW, Mu F, Yin Y, Yang HM, Lisby M, Cornall RJ, Mulder J, Uhlén M, Esteban MA, Li YX, Liu LQ, Xu X, Wang J (2022). Spatiotemporal transcriptomic atlas of mouse organogenesis using DNA nanoball-patterned arrays. Cell 185, 1777-1792. |
| [19] | Chen J, Suo SB, Tam PPL, Han JDJ, Peng GD, Jing NH (2017). Spatial transcriptomic analysis of cryosectioned tissue samples with Geo-seq. Nat Protoc 12, 566-580. |
| [20] | Chen KH, Boettiger AN, Moffitt JR, Wang SY, Zhuang XW (2015). Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348, aaa6090. |
| [21] | Chen XY, Sun YC, Church GM, Lee JH, Zador AM (2018). Efficient in situ barcode sequencing using padlock probe- based BaristaSeq. Nucleic Acids Res 46, e22. |
| [22] | Cho CS, Xi JY, Si YC, Park SR, Hsu JE, Kim M, Jun G, Kang HM, Lee JH (2021). Microscopic examination of spatial transcriptome using Seq-Scope. Cell 184, 3559-3572. |
| [23] | Codeluppi S, Borm LE, Zeisel A, La Manno G, van Lunteren JA, Svensson CI, Linnarsson S (2018). Spatial organization of the somatosensory cortex revealed by osmFISH. Nat Methods 15, 932-935. |
| [24] | Combs PA, Eisen MB (2013). Sequencing mRNA from cryo-sliced Drosophila embryos to determine genome-wide spatial patterns of gene expression. PLoS One 8, e71820. |
| [25] | Costa V, Angelini C, De Feis I, Ciccodicola A (2010). Uncovering the complexity of transcriptomes with RNA- Seq. J Biomed Biotechnol 2010, 853916. |
| [26] | Downes DJ, Cross AR, Hua P, Roberts N, Schwessinger R, Cutler AJ, Munis AM, Brown J, Mielczarek O, de Andrea CE, Melero I, COvid-19 Multi-Omics Blood ATlas COMBAT Consortium, Gill DR, Hyde SC, Knight JC, Todd JA, Sansom SN, Issa F, Davies JOJ, Hughes JR (2021). Identification of LZTFL1as a candidate effector gene at a COVID-19 risk locus. Nat Genet 53, 1606-1615. |
| [27] | Eisenstein M (2022). Seven technologies to watch in 2022. Nature 601, 658-661. |
| [28] | Emmert-Buck MR, Bonner RF, Smith PD, Chuaqui RF, Zhuang ZP, Goldstein SR, Weiss RA, Liotta LA (1996). Laser capture microdissection. Science 274, 998-1001. |
| [29] | Eng CHL, Lawson M, Zhu Q, Dries R, Koulena N, Takei Y, Yun JN, Cronin C, Karp C, Yuan GC, Cai L (2019). Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH+. Nature 568, 235-239. |
| [30] | Fawkner-Corbett D, Antanaviciute A, Parikh K, Jagielowicz M, Gerós AS, Gupta T, Ashley N, Khamis D, Fowler D, Morrissey E, Cunningham C, Johnson PRV, Koohy H, Simmons A (2021). Spatiotemporal analysis of human intestinal development at single-cell resolution. Cell 184, 810-826. |
| [31] | Fazal FM, Han S, Parker KR, Kaewsapsak P, Xu J, Boettiger AN, Chang HY, Ting AY (2019). Atlas of subcellular RNA localization revealed by APEX-seq. Cell 178, 473-490. |
| [32] | Femino AM, Fay FS, Fogarty K, Singer RH (1998). Visualization of single RNA transcripts in situ. Science 280, 585-590. |
| [33] | Fu XN, Sun L, Chen JY, Dong RZ, Lin Y, Palmiter RD, Lin S, Gu LC (2021). Continuous polony gels for tissue mapping with high resolution and RNA capture efficiency. BioRxiv doi: 10.1101/2021.03.17.435795. |
| [34] | Fu XN, Sun L, Dong RZ, Chen JY, Silakit R, Condon LF, Lin Y, Lin S, Palmiter RD, Gu LC (2022). Polony gels enable amplifiable DNA stamping and spatial transcriptomics of chronic pain. Cell 185, 4621-4633. |
| [35] | Fürth D, Hatini V, Lee JH (2019). In situ transcriptome accessibility sequencing (INSTA-seq). BioRxiv doi: 10 1101/ 722819. |
| [36] | Gao SW, Shi Q, Zhang YF, Liang GX, Kang ZX, Huang BF, Ma DY, Wang L, Jiao JW, Fang XD, Xu CR, Liu LQ, Xu X, G?ttgens B, Li C, Liu F (2022). Identification of HSC/MPP expansion units in fetal liver by single-cell spatiotemporal transcriptomics. Cell Res 32, 38-53. |
| [37] | Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T, James JJ, Maysuria M, Mitton JD, Oliveri P, Osborn JL, Peng T, Ratcliffe AL, Webster PJ, Davidson EH, Hood L, Dimitrov K (2008). Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26, 317-325. |
| [38] | Giacomello S, Lundeberg J (2018). Preparation of plant tissue to enable spatial transcriptomics profiling using barcoded microarrays. Nat Protoc 13, 2425-2446. |
| [39] | Giacomello S, Salmén F, Terebieniec BK, Vickovic S, Navarro JF, Alexeyenko A, Reimeg?rd J, McKee LS, Mannapperuma C, Bulone V, St?hl PL, Sundstr?m JF, Street NR, Lundeberg J (2017). Spatially resolved transcriptome profiling in model plant species. Nat Plants 3, 17061. |
| [40] | Giolai M, Verweij W, Lister A, Heavens D, Macaulay I, Clark MD (2019). Spatially resolved transcriptomics reveals plant host responses to pathogens. Plant Methods 15, 114. |
| [41] | Gough A, Stern AM, Maier J, Lezon T, Shun TY, Chennubhotla C, Schurdak ME, Haney SA, Taylor DL (2017). Biologically relevant heterogeneity: metrics and practical insights. SLAS Discov 22, 213-237. |
| [42] | Gurazada SGR, Cox KL Jr, Czymmek KJ, Meyers BC (2021). Space: the final frontier-achieving single-cell, spatially resolved transcriptomics in plants. Emerg Top Life Sci 5, 179-188. |
| [43] | Hou XL, Yang Y, Li P, Zeng ZP, Hu WL, Zhe RL, Liu XQ, Tang DE, Ou ML, Dai Y (2021). Integrating spatial transcriptomics and single-cell RNA-seq reveals the gene expression profling of the human embryonic liver. Front Cell Dev Biol 9, 652408. |
| [44] | Ji AL, Rubin AJ, Thrane K, Jiang SZ, Reynolds DL, Meyers RM, Guo MG, George BM, Mollbrink A, Bergenstr?hle J, Larsson L, Bai YH, Zhu BK, Bhaduri A, Meyers JM, Rovira-Clavé X, Hollmig ST, Aasi SZ, Nolan GP, Lundeberg J, Khavari PA (2020). Multimodal analysis of composition and spatial architecture in human squamous cell carcinoma. Cell 182, 497-514. |
| [45] | Junker JP, No?l ES, Guryev V, Peterson KA, Shah G, Huisken J, McMahon AP, Berezikov E, Bakkers J, van Oudenaarden A (2014). Genome-wide RNA tomography in the zebrafish embryo. Cell 159, 662-675. |
| [46] | Ke RQ, Mignardi M, Pacureanu A, Svedlund J, Botling J, W?hlby C, Nilsson M (2013). In situ sequencing for RNA analysis in preserved tissue and cells. Nat Methods 10, 857-860. |
| [47] | Kolodziejczyk AA, Kim JK, Svensson V, Marioni JC, Teichmann SA (2015). The technology and biology of single-cell RNA sequencing. Mol Cell 58, 610-620. |
| [48] | Kulasinghe A, Tan CW, dos Santos Miggiolaro AFR, Monkman J, SadeghiRad H, Bhuva DD, da Silva Motta Junior J, Vaz de Paula CB, Nagashima S, Baena CP, Souza-Fonseca-Guimaraes P, de Noronha L, McCulloch T, Rossi GR, Cooper C, Tang B, Short KR, Davis MJ, Souza-Fonseca-Guimaraes F, Belz GT, O'Byrne K (2022). Profiling of lung SARS-CoV-2 and influenza virus infection dissects virus-specific host responses and gene signatures. Eur Respir J 59, 2101881. |
| [49] | Lee JH, Daugharthy ER, Scheiman J, Kalhor R, Yang JL, Ferrante TC, Terry R, Jeanty SSF, Li C, Amamoto R, Peters DT, Turczyk BM, Marblestone AH, Inverso SA, Bernard A, Mali P, Rios X, Aach J, Church GM (2014). Highly multiplexed subcellular RNA sequencing in situ. Science 343, 1360-1363. |
| [50] | Lee JK, Wang JG, Sa JK, Ladewig E, Lee HO, Lee IH, Kang HJ, Rosenbloom DS, Camara PG, Liu ZQ, van Nieuwenhuizen P, Jung SW, Choi SW, Kim J, Chen A, Kim KT, Shin S, Seo YJ, Oh JM, Shin YJ, Park CK, Kong DS, Seol HJ, Blumberg A, Lee JI, Iavarone A, Park WY, Rabadan R, Nam DH (2017). Spatiotemporal genomic architecture informs precision oncology in glioblastoma. Nat Genet 49, 594-599. |
| [51] | Lein E, Borm LE, Linnarsson S (2017). The promise of spatial transcriptomics for neuroscience in the era of molecular cell typing. Science 358, 64-69. |
| [52] | Liao J, Lu XY, Shao X, Zhu L, Fan XH (2021). Uncovering an organ's molecular architecture at single-cell resolution by spatially resolved transcriptomics. Trends Biotechnol 39, 43-58. |
| [53] | Lieben L (2017). Spatial transcriptomics in plants. Nat Rev Genet 18, 394. |
| [54] | Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523-536. |
| [55] | Liu C, Li R, Li Y, Lin XM, Zhao KC, Liu Q, Wang SW, Yang XQ, Shi XY, Ma YT, Pei CY, Wang H, Bao WD, Hui JH, Yang T, Xu ZC, Lai TT, Berberoglu MA, Sahu SK, Esteban MA, Ma KL, Fan GY, Li YX, Liu SP, Chen A, Xu X, Dong ZQ, Liu LQ (2022a). Spatiotemporal mapping of gene expression landscapes and developmental trajectories during zebrafish embryogenesis. Dev Cell 57, 1284-1298. |
| [56] | Liu Y, Yang MY, Deng YX, Su G, Enninful A, Guo CC, Tebaldi T, Zhang D, Kim D, Bai ZL, Norris E, Pan A, Li JT, Xiao Y, Halene S, Fan R (2020). High-spatial-resolution multi-omics sequencing via deterministic barcoding in tissue. Cell 183, 1665-1681. |
| [57] | Liu YY, Li CH, Han Y, Li RC, Cui F, Zhang H, Su XS, Liu XW, Xu GX, Wan SB, Li GW (2022b). Spatial transcriptome analysis on peanut tissues shed light on cell heterogeneity of the peg. Plant Biotechnol J 20, 1648-1650. |
| [58] | Lovatt D, Ruble BK, Lee J, Dueck H, Kim TK, Fisher S, Francis C, Spaethling JM, Wolf JA, Grady MS, Ulyanova AV, Yeldell SB, Griepenburg JC, Buckley PT, Kim J, Sul JY, Dmochowski IJ, Eberwine J (2014). Transcriptome in vivo analysis (TIVA) of spatially defined single cells in live tissue. Nat Methods 11, 190-196. |
| [59] | Lubeck E, Coskun AF, Zhiyentayev T, Ahmad M, Cai L (2014). Single-cell in situ RNA profiling by sequential hybridization. Nat Methods 11, 360-361. |
| [60] | Ma?no N, Hauling T, Cappi G, Madaboosi N, Dupouy DG, Nilsson M (2019). A microfluidic platform towards automated multiplexed in situ sequencing. Sci Rep 9, 3542. |
| [61] | Maniatis S, ?ij? T, Vickovic S, Braine C, Kang K, Mollbrink A, Fagegaltier D, Andrusivová ?, Saarenp?? S, Saiz-Castro G, Cuevas M, Watters A, Lundeberg J, Bonneau R, Phatnani H (2019). Spatiotemporal dynamics of molecular pathology in amyotrophic lateral sclerosis. Science 364, 89-93. |
| [62] | Marks RA, Hotaling S, Frandsen PB, VanBuren R (2021). Representation and participation across 20 years of plant genome sequencing. Nat Plants 7, 1571-1578. |
| [63] | Marx V (2021). Method of the year: spatially resolved transcriptomics. Nat Methods 18, 9-14. |
| [64] | Maynard KR, Collado-Torres L, Weber LM, Uytingco C, Barry BK, Williams SR, Catallini II JL, Tran MN, Besich Z, Tippani M, Chew J, Yin YF, Kleinman JE, Hyde TM, Rao N, Hicks SC, Martinowich K, Jaffe AE (2021). Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex. Nat Neurosci 24, 425-436. |
| [65] | Medaglia C, Giladi A, Stoler-Barak L, De Giovanni M, Salame TM, Biram A, David E, Li HJ, Iannacone M, Shulman Z, Amit I (2017). Spatial reconstruction of immune niches by combining photoactivatable reporters and scRNA-seq. Science 358, 1622-1626. |
| [66] | Merritt CR, Ong GT, Church SE, Barker K, Danaher P, Geiss G, Hoang M, Jung J, Liang Y, McKay-Fleisch J, Nguyen K, Norgaard Z, Sorg K, Sprague I, Warren C, Warren S, Webster PJ, Zhou Z, Zollinger DR, Dunaway DL, Mills GB, Beechem JM (2020). Multiplex digital spatial profiling of proteins and RNA in fixed tissue. Nat Biotechnol 38, 586-599. |
| [67] | Meylan M, Petitprez F, Becht E, Bougoüin A, Pupier G, Calvez A, Giglioli I, Verkarre V, Lacroix G, Verneau J, Sun CM, Laurent-Puig P, Vano YA, Ela?di R, Méjean A, Sanchez-Salas R, Barret E, Cathelineau X, Oudard S, Reynaud CA, de Reyniès A, Sautès-Fridman C, Fridman WH (2022). Tertiary lymphoid structures generate and propagate anti-tumor antibody-producing plasma cells in renal cell cancer. Immunity 55, 527-541. |
| [68] | Moncada R, Barkley D, Wagner F, Chiodin M, Devlin JC, Baron M, Hajdu CH, Simeone DM, Yanai I (2020). Integrating microarray-based spatial transcriptomics and single-cell RNA-seq reveals tissue architecture in pancreatic ductal adenocarcinomas. Nat Biotechnol 38, 333-342. |
| [69] | Moreno-Villena JJ, Zhou HR, Gilman IS, Tausta SL, Cheung CYM, Edwards EJ (2022). Spatial resolution of an integrated C4+CAM photosynthetic metabolism. Sci Adv 8, eabn2349. |
| [70] | Moses L, Pachter L (2022). Museum of spatial transcriptomics. Nat Methods 19, 534-546. |
| [71] | Nelms B, Walbot V (2019). Defining the developmental program leading to meiosis in maize. Science 364, 52-56. |
| [72] | Okamura-Oho Y, Shimokawa K, Takemoto S, Hirakiyama A, Nakamura S, Tsujimura Y, Nishimura M, Kasukawa T, Masumoto KH, Nikaido I, Shigeyoshi Y, Ueda HR, Song G, Gee J, Himeno R, Yokota H (2012). Transcriptome tomography for brain analysis in the web-accessible anatomical space. PLoS One 7, e45373. |
| [73] | Orozco A (2020). A Spatial Analysis of Norwegian Spruce Cone Developmental Stages. Uppsala: Uppsala University. pp. 1-59. |
| [74] | Ou ZH, Lin ST, Qiu JY, Ding WC, Ren PD, Chen DS, Wang JX, Tong YH, Wu D, Chen A, Deng Y, Cheng MN, Peng T, Lu HR, Yang HM, Wang J, Jin X, Ma D, Xu X, Wang YZ, Li JH, Wu P (2022). Single-nucleus RNA sequencing and spatial transcriptomics reveal the immunological microenvironment of cervical squamous cell carcinoma. Adv Sci 9, 2203040. |
| [75] | Pelka K, Hofree M, Chen JH, Sarkizova S, Pirl JD, Jorgji V, Bejnood A, Dionne D, Ge WH, Xu KH, Chao SX, Zollinger DR, Lieb DJ, Reeves JW, Fuhrman CA, Hoang ML, Delorey T, Nguyen LT, Waldman J, Klapholz M, Wakiro I, Cohen O, Albers J, Smillie CS, Cuoco MS, Wu JY, Su MJ, Yeung J, Vijaykumar B, Magnuson AM, Asinovski N, Moll T, Goder-Reiser MN, Applebaum AS, Brais LK, DelloStritto LK, Denning SL, Phillips ST, Hill EK, Meehan JK, Frederick DT, Sharova T, Kanodia A, Todres EZ, Jané-Valbuena J, Biton M, Izar B, Lambden CD, Clancy TE, Bleday R, Melnitchouk N, Irani J, Kunitake H, Berger DL, Srivastava A, Hornick JL, Ogino S, Rotem A, Vigneau S, Johnson BE, Corcoran RB, Sharpe AH, Kuchroo VK, Ng K, Giannakis M, Nieman LT, Boland GM, Aguirre AJ, Anderson AC, Rozenblatt-Rosen O, Regev A, Hacohen N (2021). Spatially organized multicellular immune hubs in human colorectal cancer. Cell 184, 4734-4752. |
| [76] | Peng GD, Cui GZ, Ke JC, Jing NH (2020). Using single-cell and spatial transcriptomes to understand stem cell lineage specification during early embryo development. Annu Rev Genom Hum Genet 21, 163-181. |
| [77] | Peng GD, Suo SB, Cui GZ, Yu F, Wang R, Chen J, Chen SR, Liu ZW, Chen GY, Qian Y, Tam PPL, Han JDJ, Jing NH (2019). Molecular architecture of lineage allocation and tissue organization in early mouse embryo. Nature 572, 528-532. |
| [78] | Porritt RA, Zemmour D, Abe M, Lee Y, Narayanan M, Carvalho TT, Gomez AC, Martinon D, Santiskulvong C, Fishbein MC, Chen S, Crother TR, Shimada K, Arditi M, Rivas MN (2021). NLRP3 inflammasome mediates immune-stromal interactions in vasculitis. Circ Res 129, e183-e200. |
| [79] | Potter SS (2018). Single-cell RNA sequencing for the study of development, physiology and disease. Nat Rev Nephrol 14, 479-492. |
| [80] | Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S (2008). Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5, 877-879. |
| [81] | Rodriques SG, Stickels RR, Goeva A, Martin CA, Murray E, Vanderburg CR, Welch J, Chen LM, Chen F, Macosko EZ (2019). Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution. Science 363, 1463-1467. |
| [82] | Seyfferth C, Renema J, Wendrich JR, Eekhout T, Seurinck R, Vandamme N, Blob B, Saeys Y, Helariutta Y, Birnbaum KD, De Rybel B (2021). Advances and opportunities in single-cell transcriptomics for plant research. Annu Rev Plant Biol 72, 847-866. |
| [83] | Shah S, Lubeck E, Schwarzkopf M, He TF, Greenbaum A, Sohn CH, Lignell A, Choi HMT, Gradinaru V, Pierce NA, Cai L (2016). Single-molecule RNA detection at depth by hybridization chain reaction and tissue hydrogel embedding and clearing. Development 143, 2862-2867. |
| [84] | Shiroguchi K, Jia TZ, Sims PA, Xie XS (2012). Digital RNA sequencing minimizes sequence-dependent bias and amplification noise with optimized single-molecule barcodes. Proc Natl Acad Sci USA 109, 1347-1352. |
| [85] | Singer RH, Ward DC (1982). Actin gene expression visualized in chicken muscle tissue culture by using in situ hybridization with a biotinated nucleotide analog. Proc Natl Acad Sci USA 79, 7331-7335. |
| [86] | Srivatsan SR, McFaline-Figueroa JL, Ramani V, Saunders L, Cao JY, Packer J, Pliner HA, Jackson DL, Daza RM, Christiansen L, Zhang F, Steemers F, Shendure J, Trapnell C (2020). Massively multiplex chemical transcriptomics at single-cell resolution. Science 367, 45-51. |
| [87] | Srivatsan SR, Regier MC, Barkan E, Franks JM, Packer JS, Grosjean P, Duran M, Saxton S, Ladd JJ, Spielmann M, Lois C, Lampe PD, Shendure J, Stevens KR, Trapnell C (2021). Embryo-scale, single-cell spatial transcriptomics. Science 373, 111-117. |
| [88] | St?hl PL, Salmén F, Vickovic S, Lundmark A, Navarro JF, Magnusson J, Giacomello S, Asp M, Westholm JO, Huss M, Mollbrink A, Linnarsson S, Codeluppi S, Borg ?, Pontén F, Costea PI, Sahlén P, Mulder J, Bergmann O, Lundeberg J, Frisén J (2016). Visualization and analysis of gene expression in tissue sections by spatial transcriptomics. Science 353, 78-82. |
| [89] | Stickels RR, Murray E, Kumar P, Li JL, Marshall JL, Di Bella DJ, Arlotta P, Macosko EZ, Chen F (2021). Highly sensitive spatial transcriptomics at near-cellular resolution with Slide-seq V2. Nat Biotechnol 39, 313-319. |
| [90] | van den Brink SC, Alemany A, van Batenburg V, Moris N, Blotenburg M, Vivié J, Baillie-Johnson P, Nichols J, Sonnen KF, Martinez Arias A, van Oudenaarden A (2020). Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids. Nature 582, 405-409. |
| [91] | Vickovic S, Eraslan G, Salmén F, Klughammer J, Stenbeck L, Schapiro D, ?ij? T, Bonneau R, Bergenstr?hle L, Navarro JF, Gould J, Griffin GK, Borg ?, Ronaghi M, Frisén J, Lundeberg J, Regev A, St?hl PL (2019). High-definition spatial transcriptomics for in situ tissue profiling. Nat Methods 16, 987-990. |
| [92] | Wang MY, Hu QN, Lv TH, Wang YH, Lan Q, Xiang R, Tu ZC, Wei YR, Han K, Shi C, Guo JF, Liu C, Yang T, Du WS, An YR, Cheng MN, Xu JS, Lu HR, Li WS, Zhang SF, Chen A, Chen W, Li YX, Wang XS, Xu X, Hu YH, Liu LQ (2022). High-resolution 3D spatiotemporal transcriptomic maps of developing Drosophila embryos and larvae. Dev Cell 57, 1271-1283. |
| [93] | Wang X, Allen WE, Wright MA, Sylwestrak EL, Samusik N, Vesuna S, Evans K, Liu C, Ramakrishnan C, Liu J, Nolan GP, Bava FA, Deisseroth K (2018). Three-dimensional intact-tissue sequencing of single-cell transcriptional states. Science 361, eaat5691. |
| [94] | Wang Z, Portier BP, Gruver AM, Bui S, Wang HW, Su N, Vo HT, Ma XJ, Luo YL, Budd GT, Tubbs RR (2013). Automated quantitative RNA in situ hybridization for resolution of equivocal and heterogeneous ERBB2 (HER2) status in invasive breast carcinoma. J Mol Diagn 15, 210-219. |
| [95] | Wei RM, He SY, Bai SS, Sei E, Hu M, Thompson A, Chen K, Krishnamurthy S, Navin NE (2022a). Spatial charting of single-cell transcriptomes in tissues. Nat Biotechnol 40, 1190-1199. |
| [96] | Wei XY, Fu SL, Li HB, Liu Y, Wang S, Feng WM, Yang YZ, Liu XW, Zeng YY, Cheng MN, Lai YW, Qiu XJ, Wu L, Zhang NN, Jiang YJ, Xu JS, Su XS, Peng C, Han L, Lou WPK, Liu CY, Yuan Y, Ma KL, Yang T, Pan XY, Gao S, Chen A, Esteban MA, Yang HM, Wang J, Fan GY, Liu LQ, Chen L, Xu X, Fei JF, Gu Y (2022b). Single-cell stereo-seq reveals induced progenitor cells involved in axolotl brain regeneration. Science 377, eabp9444. |
| [97] | Weinstein JA, Regev A, Zhang F (2019). DNA microscopy: optics-free spatio-genetic imaging by a stand-alone chemical reaction. Cell 178, 229-241. |
| [98] | Wendrich JR, Yang BJ, Vandamme N, Verstaen K, Smet W, van de Velde C, Minne M, Wybouw B, Mor E, Arents HE, Nolf J, Van Duyse J, Van Isterdael G, Maere S, Saeys Y, De Rybel B (2020). Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions. Science 370, eaay4970. |
| [99] | Williams CG, Lee HJ, Asatsuma T, Vento-Tormo R, Haque A (2022). An introduction to spatial transcriptomics for biomedical research. Genome Med 14, 68. |
| [100] | Wu DJ, Liu XZ, Zhang JQ, Li L, Wang XD (2021). Significance of single-cell and spatial transcriptomes in cell biology and toxicology. Cell Biol Toxicol 37, 1-5. |
| [101] | Xia KK, Sun HX, Li J, Li JM, Zhao Y, Chen LC, Qin C, Chen RY, Chen ZY, Liu GY, Yin RL, Mu BB, Wang XJ, Xu MY, Li XY, Yuan PS, Qiao YX, Hao SJ, Wang J, Xie Q, Xu JS, Liu SP, Li YX, Chen A, Liu LQ, Yin Y, Yang HM, Wang J, Gu Y, Xu X (2022). The single-cell stereo- seq reveals region-specific cell subtypes and transcriptome profiling in Arabidopsis leaves. Dev Cell 57, 1299-1310. |
| [102] | Yao ZZ, Nguyen TN, Goldy J, Sedeno-Cortes AE, Baftizadeh F, Bertagnolli D, Casper T, Chiang M, Crichton K, Ding SL, Fong O, Garren E, Glandon A, Gouwens NW, Gray J, Graybuck LT, Hawrylycz MJ, Hirschstein D, Kroll M, Lathia K, Lee C, Levi B, McMillen D, Mok S, Pham T, Ren QZ, Rimorin C, Shapovalova N, Sulc J, Sunkin SM, Tieu M, Torkelson A, Tung H, Ward K, Dee N, Smith KA, Tasic B, Zeng HK (2021). A taxonomy of transcriptomic cell types across the isocortex and hippocampal formation. Cell 184, 3222-3241. |
| [103] | Zhang LL, Chen DS, Song DL, Liu XX, Zhang YN, Xu X, Wang XD (2022). Clinical and translational values of spatial transcriptomics. Signal Transduct Target Ther 7, 111. |
| [104] | Zhang M, Eichhorn SW, Zingg B, Yao ZZ, Cotter K, Zeng HK, Dong HW, Zhuang XW (2021a). Spatially resolved cell atlas of the mouse primary motor cortex by MERFISH. Nature 598, 137-143. |
| [105] | Zhang TQ, Chen Y, Liu Y, Lin WH, Wang JW (2021b). Single-cell transcriptome atlas and chromatin accessibility landscape reveal differentiation trajectories in the rice root. Nat Commun 12, 2053. |
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