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CNEReg Interprets Ruminant-specific Conserved Non-coding Elements by Developmental Gene Regulatory Network

Genomics, Proteomics & Bioinformatics 2023年第3期21卷 632-648页

作者： Xiangyu Pan Zhaoxia Ma Xinqi Sun Hui Li Tingting Zhang Chen Zhao Nini Wang rasmus heller Wing Hung Wong Wen Wang Yu Jiang Yong Wang Key Laboratory of Animal Genetics Breeding and Reproduction of Shaanxi ProvinceCollege of Animal Science and TechnologyNorthwest A&F UniversityYangling 712100China Department of Medical Research Guangdong Provincial People’s HospitalGuangdong Academy of Medical SciencesGuangzhou 510080China Guangdong Cardiovascular Institute Guangdong Provincial People’s HospitalGuangdong Academy of Medical SciencesGuangzhou 510080China Academy of Mathematics and Systems Science Chinese Academy of SciencesBeijing 100190China School of Mathematics University of Chinese Academy of SciencesBeijing 100049China State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources College of Animal Science and TechnologyGuangxi UniversityNanning 530005China Section for Computational and RNA Biology Department of BiologyUniversity of CopenhagenCopenhagen DK-2100Denmark Department of Statistics Department of Biomedical Data ScienceBio-X ProgramStanford UniversityStanfordCA 94305USA Center for Ecological and Environmental Sciences Northwestern Polytechnical UniversityXi’an 710072China State Key Laboratory of Genetic Resources and Evolution Kunming Institute of ZoologyChinese Academy of SciencesKunming 650223China Center for Excellence in Animal Evolution and Genetics Chinese Academy of SciencesKunming 650223China Key Laboratory of Systems Health Science of Zhejiang Province School of Life ScienceHangzhou Institute for Advanced StudyUniversity of Chinese Academy of SciencesHangzhou 310024China

The genetic information coded in DNA leads to trait innovation via a gene regulatory network(GRN)in development.Here,we developed a conserved non-coding element interpretation method to integrate multi-omics data into gene regulatory network(CNEReg)to investigate the ruminant multi-chambered stomach innovation.We generated paired expression and chromatin accessibility data during rumen and esophagus development in sheep,and revealed 1601 active ruminantspecific conserved non-coding elements(active-RSCNEs).To interpret the function of these activeRSCNEs,we defined toolkit transcription factors(TTFs)and modeled their regulation on rumenspecific genes via batteries of active-RSCNEs during development.Our developmental GRN revealed 18 TTFs and 313 active-RSCNEs regulating 7 rumen functional modules.Notably,6 TTFs(OTX1,SOX21,HOXC8,SOX2,TP63,and PPARG),as well as 16 active-RSCNEs,functionally distinguished the rumen from the esophagus.Our study provides a systematic approach to understanding how gene regulation evolves and shapes complex traits by putting evo-devo concepts into practice with developmental multi-omics data.

关键词： Trait innovation Gene regulatory network Conserved non-coding element Toolkit transcription factor Ruminant

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Single-cell transcriptomic landscape of the sheep rumen provides insights into physiological programming development and adaptation of digestive strategies

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Zoological Research 2022年第4期43卷 634-647页

作者： Yuan Yuan Da-Ming Sun Tao Qin Sheng-Yong Mao Wei-Yun Zhu Yu-Yang Yin Jie Huang rasmus heller Zhi-Peng Li Jun-Hua Liu Qiang Qiu School of Ecology and Environment Northwestern Polytechnical UniversityXi’anShaanxi 710072China Ruminant Nutrition and Feed Engineering Technology Research Center College of Animal Science and TechnologyNanjing Agricultural UniversityNanjingJiangsu 210095China Laboratory of Gastrointestinal Microbiology Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal HealthNational Center for International Research on Animal Gut NutritionCollege of Animal Science and TechnologyNanjing Agricultural UniversityNanjingJiangsu 210095China Huzhou Academy of Agricultural Sciences HuzhouZhejiang 313000China Section for Computational and RNA Biology Department of BiologyUniversity of CopenhagenCopenhagen DK-2200Denmark College of Animal Science and Technology Jilin Agricultural UniversityChangchunJilin 130118China

As an important evolutionary innovation and unique organ,the rumen has played a crucial role in ruminant adaptation to complex ecological environments.However,the cellular basis of its complex morphology and function remains largely unknown.In this study,we identified eight major cell types from seven representative prenatal and postnatal rumen samples using~56600 single-cell transcriptomes.We captured the dynamic changes and high heterogeneity in cellular and molecular profiles before,during,and after the appearance of keratinized stratified squamous epithelium with neatly arranged papillae and functional maturity.Basal cells,keratinocytes,differentiating keratinocytes,terminally differentiated keratinocytes,and special spinous cells provided the cellular basis for rumen epithelium formation.Notably,we obtained clear evidence of two keratinization processes involved in early papillogenesis and papillae keratinization and identified TBX3 as a potential marker gene.Importantly,enriched stratum spinosum cells played crucial roles in volatile fatty acid(VFA)metabolism and immune response.Our results provide a comprehensive transcriptional landscape of rumen development at single-cell resolution,as well as valuable insight into the interactions between dietary metabolism and the rumen.

关键词： Rumen scRNA-seq Ruminal epithelium Keratinization

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Modes of genetic adaptations underlying functional innovations in the rumen

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Science China(Life Sciences) 2021年第1期64卷 1-21页

作者： Xiangyu Pan Yudong Cai Zongjun Li Xianqing Chen rasmus heller Nini Wang Yu Wang Chen Zhao Yong Wang Han Xu Songhai Li Ming Li Cunyuan Li Shengwei Hu Hui Li Kun Wang Lei Chen Bin Wei Zhuqing Zheng Weiwei Fu Yue Yang Tingting Zhang Zhuoting Hou Yueyang Yan Xiaoyang Lv Wei Sun Xinyu Li Shisheng Huang Lixiang Liu Shengyong Mao Wenqing Liu Jinlian Hua Zhipeng Li Guojie Zhang Yulin Chen Xihong Wang Qiang Qiu Brian PDalrymple Wen Wang Yu Jiang Key Laboratory of Animal Genetics Breeding and Reproduction of Shaanxi ProvinceCollege of Animal Science and TechnologyNorthwest A&F UniversityYangling712100China School of Ecology and Environment Northwestern Polytechnical UniversityXi’an710072China Section for Computational and RNA Biology Department of BiologyUniversity of CopenhagenCopenhagenDK-2100Denmark University of Chinese Academy of Sciences Beijing100049China Center for Excellence in Animal Evolution and Genetics Chinese Academy of SciencesKunming650223China CEMS NCMISMDISAcademy of Mathematics and Systems ScienceChinese Academy of SciencesBeijing100080China Marine Mammal and Marine Bioacoustics Laboratory Institute of Deep-sea Science and EngineeringChinese Academy of SciencesSanya572000China College of Life Sciences Shihezi UniversityShihezi832003China State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources College of Animal Science and TechnologyGuangxi UniversityNanning530005China College of Animal Science and Technology Yangzhou UniversityYangzhou225009China Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China Yangzhou UniversityYangzhou225009China Key Laboratory for Major Obstetric Diseases of Guangdong Province The Third Affiliated Hospital of Guangzhou Medical UniversityGuangzhou510150China School of Life Science and Technology Shanghai Tech UniversityShanghai201210China College of Animal Science and Technology Nanjing Agricultural UniversityNanjing210095China College of Veterinary Medicine Shaanxi Centre of Stem Cells Engineering&TechnologyNorthwest A&F UniversityYangling712100China Department of Special Economic Animal Nutrition and Feed Science Institute of Special Animal and Plant SciencesChinese Academy of Agricultural SciencesChangchun130112China Section for Ecology and Evolution Department of BiologyUniversity of CopenhagenCopenhagenDK-2100Denmark China National GeneBank BGI-ShenzhenShen

The rumen is the hallmark organ of ruminants and hosts a diverse ecosystem of microorganisms that facilitates efficient digestion of plant fibers.We analyzed 897 transcriptomes from three Cetartiodactyla lineages:ruminants,camels and cetaceans,as well as data from ruminant comparative genomics and functional assays to explore the genetic basis of rumen functional innovations.We identified genes with relatively high expression in the rumen,of which many appeared to be recruited from other tissues.These genes show functional enrichment in ketone body metabolism,regulation of microbial community,and epithelium absorption,which are the most prominent biological processes involved in rumen innovations.Several modes of genetic change underlying rumen functional innovations were uncovered,including coding mutations,genes newly evolved,and changes of regulatory elements.We validated that the key ketogenesis rate-limiting gene(HMGCS2)with five ruminant-specific mutations was under positive selection and exhibits higher synthesis activity than those of other mammals.Two newly evolved genes(LYZ1 and DEFB1)are resistant to Gram-positive bacteria and thereby may regulate microbial community equilibrium.Furthermore,we confirmed that the changes of regulatory elements accounted for the majority of rumen gene recruitment.These results greatly improve our understanding of rumen evolution and organ evo-devo in general.

关键词： rumen innovations comparative transcriptomics comparative genomics evo-devo evolution of organs

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FungalTraits:a user-friendly traits database of fungi and fungus-like stramenopiles

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Fungal Diversity 2020年第2期107卷 I0001-I0016页

作者： Sergei Põlme Kessy Abarenkov RHenrik Nilsson Björn D.Lindahl Karina Engelbrecht Clemmensen Havard Kauserud Nhu Nguyen rasmus Kjøller Scott T.Bates Petr Baldrian Tobias Guldberg Frøslev Kristjan Adojaan Alfredo Vizzini Ave Suija Donald Pfister Hans-Otto Baral Helle Järv Hugo Madrid Jenni Nordén Jian-Kui Liu Julia Pawlowska Kadri Põldmaa Kadri Pärtel Kadri Runnel Karen Hansen Karl-Henrik Larsson Kevin David Hyde Marcelo Sandoval-Denis Matthew E.Smith Merje Toome-heller Nalin N.Wijayawardene Nelson Menolli Jr Nicole K.Reynolds Rein Drenkhan Sajeewa S.N.Maharachchikumbura Tatiana B.Gibertoni Thomas Læssøe William Davis Yuri Tokarev Adriana Corrales Adriene Mayra Soares Ahto Agan Alexandre Reis Machado Andrés Argüelles-Moyao Andrew Detheridge Angelina de Meiras-Ottoni Annemieke Verbeken Arun Kumar Dutta Bao-Kai Cui C.K.Pradeep César Marín Daniel Stanton Daniyal Gohar Dhanushka N.Wanasinghe Eveli Otsing Farzad Aslani Gareth W.Griffith Thorsten H.Lumbsch Hans-Peter Grossart Hossein Masigol Ina Timling Inga Hiiesalu Jane Oja John Y.Kupagme József Geml Julieta Alvarez-Manjarrez Kai Ilves Kaire Loit Kalev Adamson Kazuhide Nara Kati Küngas Keilor Rojas-Jimenez Krišs Bitenieks Laszlo Irinyi LászlóGNagy Liina Soonvald Li-Wei Zhou Lysett Wagner M.Catherine Aime MaarjaÖpik María Isabel Mujica Martin Metsoja Martin Ryberg Martti Vasar Masao Murata Matthew PNelsen Michelle Cleary Milan C.Samarakoon Mingkwan Doilom Mohammad Bahram Niloufar Hagh-Doust Olesya Dulya Peter Johnston Petr Kohout Qian Chen Qing Tian Rajasree Nandi Rasekh Amiri Rekhani Hansika Perera Renata dos Santos Chikowski Renato L.Mendes-Alvarenga Roberto Garibay-Orijel Robin Gielen Rungtiwa Phookamsak Ruvishika S.Jayawardena Saleh Rahimlou Samantha C.Karunarathna Saowaluck Tibpromma Shawn P.Brown Siim-Kaarel Sepp Sunil Mundra Zhu-Hua Luo Tanay Bose Tanel Vahter Tarquin Netherway Teng Yang Tom May Torda Varga Wei Li Victor Rafael Matos Coimbra Virton Rodrigo Targino de Oliveira Vitor Xavier de Lima Vladimir S.Mikryukov Yongzhong Lu Yosuke Matsuda Yumiko Miyamoto Urm Institute of Ecology and Earth Sciences University of Tartu14A Ravila50411 TartuEstonia Natural History Museum University of Tartu46 Vanemuise Str51003 TartuEstonia Gothenburg Global Biodiversity Centre Box 46140530 GothenburgSweden Department of Biological and Environmental Sciences University of GothenburgGothenburgSweden Department of Soil and Environment Swedish University of Agricultural SciencesBox 701475007 UppsalaSweden Department of Forest Mycology and Plant Pathology Swedish University of Agricultural SciencesBox 702675007 UppsalaSweden Section for Genetics and Evolutionary Biology(EvoGene) Department of BiosciencesUniversity of OsloP.O.Box 1066BlindernNO-0316 OsloNorway University of Hawaiʻi at Mānoa 3190 Maile WaySt.John 102HonoluluHIUSA Department of Biology University of CopenhagenUniversitetsparken 152100 CopenhagenØDenmark Purdue University Northwest WestvilleIN 46391USA Institute of Microbiology Czech Academy of SciencesVidenska 108314220 Praha 4Czech Republic GLOBE Institute University of CopenhagenØster Farimagsgade 5KH7.2.321353 CopenhagenDenmark Dipartimento di Scienze della Vita e Biologia dei Sistemi Universitàdi TorinoViale Mattioli 2510125 TorinoItaly Department of Organismic and Evolutionary Biology and Farlow Library and Herbarium Harvard University22 Divinity AveCambridgeMA 02138USA Blaihofstr.42 72074 TübingenGermany SYNLAB Estonia Veerenni 53aTallinn 11313Estonia Escuela de Tecnología Médica Universidad Santo TomásLos Carreras 753OsornoChile Centro de Genómica y Bioinformática Universidad MayorCamino La Pirámide 5750HuechurabaSantiagoChile Norwegian Institute for Nature Research(NINA) Sognsveien 680855 OsloNorway School of Life Science and Technology University of Electronic Science and Technology of ChinaChengdu 611731People’s Republic of China Evolutionary Biology Faculty of BiologyBiological and Chemical Research CentreUniversity of Warsawul.Zwirki i Wigury 10102-089 WarsawPoland Department of Botany Swedish Museum of

The cryptic lifestyle of most fungi necessitates molecular identification of the guild in environmental studies.Over the past decades,rapid development and affordability of molecular tools have tremendously improved insights of the fungal diversity in all ecosystems and habitats.Yet,in spite of the progress of molecular methods,knowledge about functional properties of the fungal taxa is vague and interpretation of environmental studies in an ecologically meaningful manner remains challenging.In order to facilitate functional assignments and ecological interpretation of environmental studies we introduce a user friendly traits and character database FungalTraits operating at genus and species hypothesis levels.Combining the information from previous efforts such as FUNGuild and FunFun together with involvement of expert knowledge,we reannotated 10,210 and 151 fungal and Stramenopila genera,respectively.This resulted in a stand-alone spreadsheet dataset covering 17 lifestyle related traits of fungal and Stramenopila genera,designed for rapid functional assignments of environmental stud-ies.In order to assign the trait states to fungal species hypotheses,the scientific community of experts manually categorised and assigned available trait information to 697,413 fungal ITS sequences.On the basis of those sequences we were able to summarise trait and host information into 92,623 fungal species hypotheses at 1%dissimilarity threshold.

关键词： Fungal traits Trophic modes Function Guild Bioinformatics High-throughput sequencing Community ecology

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