Genome analyses provide insights into Engelhardia's adaptation to East Asia summer monsoon

doi:10.1016/j.pld.2025.07.003

Plant Diversity ›› 2025, Vol. 47 ›› Issue (05): 718-732.DOI: 10.1016/j.pld.2025.07.003

• Articles • Previous Articles Next Articles

Genome analyses provide insights into Engelhardia's adaptation to East Asia summer monsoon

Min Li^a,k, Jing-Jing Wu^b, Ren-Ping Su^a,k, Ou-Yan Fang^a,k, Xiang Cai^a,k, Pei-Han Huang^a,k, Xiao-Yang Gao^c, Xin-Xing Fu^d, Xiao-Hui Ma^b, Lin-Yue H^b, Yi-Gang Song^e, Guo-Xiong Hu^f, Shi-Shun Zhou^j, Yun-Hong Tan^j, Yves Van de Peer^g,h,i, Jie Li^a, Sheng-Dan Wu^b, Hong-Hu Meng^a,j,l

a. Plant Phylogenetics and Conservation Group, Center for Integrative Conservation, and Yunnan Key Laboratory for Conservation of Tropical Rainforests and Asian Elephants, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China;
b. State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, College of Ecology, Lanzhou University, Lanzhou 730000, Gansu, China;
c. CAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science, Mengla 666303, Yunnan, China;
d. College of Life Sciences, Northwest Normal University, Lanzhou 730070, Gansu, China;
e. Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai 201602, China;
f. College of Life Sciences, Guizhou University, Guiyang 550025, Guizhou, China;
g. VIB-UGent Center for Plant Systems Biology & Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent 9052, Belgium;
h. Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria 0028, South Africa;
i. College of Horticulture, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing 210095, Jiangsu, China;
j. Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Nay Pyi Taw 05282, Myanmar;
k. University of Chinese Academy of Sciences, Beijing 100049, China;
l. Yunnan International Joint Laboratory for the Conservation and Utilization of Tropical Timber Tree Species, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China

Received:2025-07-14 Revised:2025-07-18 Online:2025-09-29 Published:2025-09-29
Contact: Yves Van de Peer,E-mail:yvpee@psb.vib-ugent.be;Jie Li,E-mail:jieli@xtbg.ac.cn;Sheng-Dan Wu,E-mail:wusd@lzu.edu.cn;Hong-Hu Meng,E-mail:menghonghu@xtbg.ac.cn
Supported by:
We thank the Supercomputing Center of Lanzhou University for providing the research cyberinfrastructure resources and service. This work was supported by the National Natural Science Foundation of China (No. 42171063); Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (No. Y4ZK111B01); the Special Fund for Scientific Research of Shanghai Landscaping & City Appearance Administrative Bureau (G242414, G242416); the “Yunnan Revitalization Talent Support Program” in Yunnan Province (XDYC-QNRC-2022-0028); Yunnan Revitalization Talent Support Program “Innovation Team” Project (202405AS350019); the CAS “Light of West China” Program; the 14th Five-Year Plan of Xishuangbanna Tropical Botanical Garden, Chinese Academy Sciences (XTBG-1450303); the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (No. 833522); and Ghent University (Methusalem funding, BOF.MET.2021.0005.01).

Genome analyses provide insights into Engelhardia's adaptation to East Asia summer monsoon

a. Plant Phylogenetics and Conservation Group, Center for Integrative Conservation, and Yunnan Key Laboratory for Conservation of Tropical Rainforests and Asian Elephants, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China;
b. State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems, College of Ecology, Lanzhou University, Lanzhou 730000, Gansu, China;
c. CAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science, Mengla 666303, Yunnan, China;
d. College of Life Sciences, Northwest Normal University, Lanzhou 730070, Gansu, China;
e. Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai 201602, China;
f. College of Life Sciences, Guizhou University, Guiyang 550025, Guizhou, China;
g. VIB-UGent Center for Plant Systems Biology & Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent 9052, Belgium;
h. Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria 0028, South Africa;
i. College of Horticulture, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing 210095, Jiangsu, China;
j. Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Nay Pyi Taw 05282, Myanmar;
k. University of Chinese Academy of Sciences, Beijing 100049, China;
l. Yunnan International Joint Laboratory for the Conservation and Utilization of Tropical Timber Tree Species, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China

通讯作者: Yves Van de Peer,E-mail:yvpee@psb.vib-ugent.be;Jie Li,E-mail:jieli@xtbg.ac.cn;Sheng-Dan Wu,E-mail:wusd@lzu.edu.cn;Hong-Hu Meng,E-mail:menghonghu@xtbg.ac.cn
基金资助:
We thank the Supercomputing Center of Lanzhou University for providing the research cyberinfrastructure resources and service. This work was supported by the National Natural Science Foundation of China (No. 42171063); Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (No. Y4ZK111B01); the Special Fund for Scientific Research of Shanghai Landscaping & City Appearance Administrative Bureau (G242414, G242416); the “Yunnan Revitalization Talent Support Program” in Yunnan Province (XDYC-QNRC-2022-0028); Yunnan Revitalization Talent Support Program “Innovation Team” Project (202405AS350019); the CAS “Light of West China” Program; the 14th Five-Year Plan of Xishuangbanna Tropical Botanical Garden, Chinese Academy Sciences (XTBG-1450303); the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (No. 833522); and Ghent University (Methusalem funding, BOF.MET.2021.0005.01).

Abstract

Abstract: Genetic information has been instrumental in elucidating the relationship between the East Asian Summer Monsoon (EASM) and subtropical evergreen broad-leaved forests (EBLFs). However, how the genomic insights of EBLFs' species correspond to environmental shifts induced by the EASM remains limited. In this study, we investigated the adaptive mechanisms of evergreen Engelhardia species in response to the EASM through genome sequencing and comparative genomic analyses from the de novo genome assemblies of five closely related Engelhardia taxa and one Rhoiptelea species. Our findings revealed that the divergence of evergreen trees from their sister deciduous species is closely associated with the onset and intensification of the EASM. This genomic transition may have coincided with a significant expansion of the terpene synthase (TPS) gene family in E. fenzelii, driven by four distinct modes of gene duplication. This expansion enhances the biosynthesis of terpene volatiles, providing a defensive mechanism against potential herbivory in EASM affected environments. We also identified a shared whole-genome duplication (WGD) event across Engelhardia, along with substantial differences in transposable element (TE) composition and activity, which contributed to genome size variation between E. fenzelii and E. roxburghiana. In addition, demographic analyses revealed a continuous population decline over the past 10 million years, further exacerbated by recent human disturbance, underscoring the conservation urgency for these species. These results not only provide preliminary insights into the complex evolutionary dynamics within the Engelhardia genus from genomic insights (e.g., the intricate relationships between genomic variations, environmental changes, and adaptive responses driven by significant climatic events such as the EASM), but also provides valuable insights into the conservation significance of EBLFs.

Key words: Engelhardia, Comparative genomics, Genome evolution, EBLFs, TPS, EASM

摘要： Genetic information has been instrumental in elucidating the relationship between the East Asian Summer Monsoon (EASM) and subtropical evergreen broad-leaved forests (EBLFs). However, how the genomic insights of EBLFs' species correspond to environmental shifts induced by the EASM remains limited. In this study, we investigated the adaptive mechanisms of evergreen Engelhardia species in response to the EASM through genome sequencing and comparative genomic analyses from the de novo genome assemblies of five closely related Engelhardia taxa and one Rhoiptelea species. Our findings revealed that the divergence of evergreen trees from their sister deciduous species is closely associated with the onset and intensification of the EASM. This genomic transition may have coincided with a significant expansion of the terpene synthase (TPS) gene family in E. fenzelii, driven by four distinct modes of gene duplication. This expansion enhances the biosynthesis of terpene volatiles, providing a defensive mechanism against potential herbivory in EASM affected environments. We also identified a shared whole-genome duplication (WGD) event across Engelhardia, along with substantial differences in transposable element (TE) composition and activity, which contributed to genome size variation between E. fenzelii and E. roxburghiana. In addition, demographic analyses revealed a continuous population decline over the past 10 million years, further exacerbated by recent human disturbance, underscoring the conservation urgency for these species. These results not only provide preliminary insights into the complex evolutionary dynamics within the Engelhardia genus from genomic insights (e.g., the intricate relationships between genomic variations, environmental changes, and adaptive responses driven by significant climatic events such as the EASM), but also provides valuable insights into the conservation significance of EBLFs.

关键词: Engelhardia, Comparative genomics, Genome evolution, EBLFs, TPS, EASM

Min Li, Jing-Jing Wu, Ren-Ping Su, Ou-Yan Fang, Xiang Cai, Pei-Han Huang, Xiao-Yang Gao, Xin-Xing Fu, Xiao-Hui Ma, Lin-Yue H, Yi-Gang Song, Guo-Xiong Hu, Shi-Shun Zhou, Yun-Hong Tan, Yves Van de Peer, Jie Li, Sheng-Dan Wu, Hong-Hu Meng. Genome analyses provide insights into Engelhardia's adaptation to East Asia summer monsoon[J]. Plant Diversity, 2025, 47(05): 718-732.

References

Abrusan, G., Grundmann, N., DeMester, L., et al., 2009. TEclass--a tool for automated classification of unknown eukaryotic transposable elements. Bioinformatics 25, 1329-1330.
Bai, W.N., Yan, P.C., Zhang, B.W., et al., 2018. Demographically idiosyncratic responses to climate change and rapid Pleistocene diversification of the walnut genus Juglans (Juglandaceae) revealed by whole-genome sequences. New Phytol. 217, 1726-1736.
Bailly-Bechet, M., Haudry, A., Lerat, E., 2014. "One code to find them all": a perl tool to conveniently parse RepeatMasker output files. Mobile Dna-Uk 5, 860-921.
Benson, G., 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580.
Burge, C., Karlin S., 1997. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94.
Celedon, J.M., Bohlmann, J., 2019. Oleoresin defenses in conifers: chemical diversity, terpene synthases and limitations of oleoresin defense under climate change. New Phytol. 224, 1444-1463.
Chang, C.Y., Brautigam, K., Huner, N.P.A., et al., 2021. Champions of winter survival: cold acclimation and molecular regulation of cold hardiness in evergreen conifers. New Phytol. 229, 675-691.
Chen, Y.X., Chen, Y.S., Shi, C.M., et al., 2018. SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. GigaScience 7, 1-6.
Chen, Z., Zhou, Z., Guo, Z.M., et al., 2023. Historical development of karst evergreen broadleaved forests in East Asia has shaped the evolution of a hemiparasitic genus Brandisia (Orobanchaceae). Plant Divers. 45, 501-512.
Cheng, H., Concepcion, G.T., Feng, X.,et al., 2021. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat. Methods 18, 170-175.
De Bie, T., Cristianini, N., Demuth, J.P., et al., 2006. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269-1271.
Ding, Y.M., Pang, X.X., Cao, Y., et al., 2023. Genome structure-based Juglandaceae phylogenies contradict alignment-based phylogenies and substitution rates vary with DNA repair genes. Nat. Commun. 14, 617.
Doležel, J., Bartoš, J., 2005. Plant DNA flow cytometry and estimation of nuclear genome size. Ann. Bot. 95, 99–110.
Dudchenko, O., Batra, S.S., Omer, A.D., et al., 2017. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92-95.
Edwards, E.J., Chatelet, D.S., Chen, B.C., et al., 2017. Convergence, Consilience, and the Evolution of Temperate Deciduous Forests. Am. Nat. 190, S87-S104.
Ellinghaus, D., Kurtz, S., Willhoeft, U., 2008. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9, 18.
Emms, D.M., Kelly, S., 2015. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157.
Feng, X., Chen, Q.P., Wu, W.H., et al., 2024. Genomic evidence for rediploidization and adaptive evolution following the whole - genome triplication. Nat Commun. 15,1635.
Flynn, J.M., Hubley, R., Goubert, C., et al., 2020. RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl. Acad. Sci. U.S.A. 117, 9451–9457.
Garcia-Hernandez, M., Berardini, T.Z., Chen, G.H., et al., 2002. TAIR: a resource for integrated Arabidopsis data. Funct. Integr. Genomic. 2, 239-253.
Haas, B.J., Delcher, A.L., Mount, S.M., et al., 2003. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654-5666.
Haas, B.J., Papanicolaou, A., Yassour, M., et al., 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512.
Haas, B.J., Salzberg, S.L., Zhu, W., et al., 2008. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol 9, R7.
Hai, L.S., Li, X. Q., Zhang, J.B., et al., 2022. Assembly dynamics of East Asian subtropical evergreen broadleaved forests: New insights from the dominant Fagaceae trees. J. Integr. Plant Biol. 64, 2126-2134.
Hansen, J., Sato, M., Russell, G., Kharecha, P., 2013. Climate sensitivity, sea level and atmospheric carbon dioxide. Philos. Trans. A Math. Phys. Eng. Sci. 371, 20120294.
Hesse, U., 2023. K-mer-based genome size estimation in theory and practice. Methods Mol. Biol. 2672, 79-113.
Hoffmann, A.A., Sgro, C.M., 2011. Climate change and evolutionary adaptation. Nature 470, 479-485.
Hu, J., Fan, J., Sun, Z., Liu, S., 2020. NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics 36, 2253-2255.
Huang, H.R., Liu, X., Arshad, R., et al., 2023. Telomere-to-telomere haplotype-resolved reference genome reveals subgenome divergence and disease resistance in triploid Cavendish banana. Hortic Res. 10, uhad153.
Jiao, Y., Leebens-Mack, J., Ayyampalayam, S., et al., 2012. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13, R3.
Jiang, H., Wan, S., Ma, X., et al., 2017. End-member modeling of the grain-size record of Sikouzi fine sediments in Ningxia (China) and implications for temperature control of Neogene evolution of East Asian winter monsoon. PLoS One 12, e0186153.
Kanehisa, M., Sato, Y., Kawashima, M., et al., 2016. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 44, 457-462.
Katoh, K., Standley, D.M., 2013. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 30, 772-780.
Keilwagen, J., Wenk, M., Erickson, J.L.,et al., 2016. Using intron position conservation for homology-based gene prediction. Nucleic Acids Res. 44, e89.
Kim, D., Langmead, B., Salzberg, S.L., 2015. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 121-357.
Kovaka, S., Zimin, A.V., Pertea, G.M., et al., 2019. Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biol. 20, 278.
Landi, M., Shah, T., Falquet, L., et al,. 2023. Haplotype-resolved genome of heterozygous African cassava cultivar TMEB117 (Manihot esculenta). Sci. Data. 10, 887.
Licht, A., van Cappelle, M., Abels, H. A., et al., 2014. Asian monsoons in a late Eocene greenhouse world. Nature 513, 501-506.
Li, H., Durbin, R., 2011. Inference of human population history from individual whole-genome sequences. Nature 475, 493-496.
Li, X.Q., Xiang, X.G., Jabbour, F., et al., 2022. Biotic colonization of subtropical East Asian caves through time. Proc. Natl. Acad. Sci. U.S.A. 119, e2207199119.
Li, M., Su, R.P., Cai, X., et al., 2025. Is it time to abandon the flow cytometry in the estimation of genome size when the K-mer analysis is available? A case from Engelhardia species. Genomics Commun. 2, e014.
Liang, Q., Lin, X., Liu, J., et al., 2022. Genome-wide identification of MAPKK and MAPKKK gene family members and transcriptional profiling analysis during bud dormancy in pear (Pyrus x bretschneideri). Plants 11, 1731.
Lin, L., Jiang, X.L., Guo, K.Q., et al., 2023. Climate change impacts the distribution of Quercus section Cyclobalanopsis (Fagaceae), a keystone lineage in East Asian evergreen broadleaved forests. Plant Divers. 45, 552-568.
Liu, L., Jin, X., Chen, N., et al., 2015. Phylogeny of Morella rubra and its relatives (Myricaceae) and genetic resources of Chinese bayberry using RAD sequencing. PLoS One 10, e0139840.
Liu, X., Zhang, H., Zhao, Y., et al., 2013. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 110, 15485-15490.
Love, M.I., Huber, W., Anders, S., 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550.
Lynch, M., Conery, J.S., 2000. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155.
Ma, X., Ru, D., Morales-Briones, D.F., et al., 2023. Genome sequence and salinity adaptation of the desert shrub Nitraria sibirica (Nitrariaceae, Sapindales). DNA Res. 30, dsad011.
Majoros, W.H., Pertea, M., Salzberg, S.L., 2004. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878-2879.
Mapleson, D., Accinelli, G.G., Kettleborough, G., et al., 2017. KAT: a K-mer analysis toolkit to quality control NGS datasets and genome assemblies. Bioinformatics 33, 574-576.
Marcais, G., Kingsford, C., 2011. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764-770.
Marques, A., Martins, I.S., Kastner, T., et al., 2019. Increasing impacts of land use on biodiversity and carbon sequestration driven by population and economic growth. Nat. Ecol. Evol. 3, 628-637.
Meng, H.H., Gao, X.Y., Song, Y.G., et al., 2021. Biodiversity arks in the Anthropocene. Reg. Sustain. 2, 109-115.
Meng, H.H., Zhang, C.Y., Low, S.L., et al., 2022a. Two new species from Sulawesi and Borneo facilitate phylogeny and taxonomic revision of Engelhardia (Juglandaceae). Plant Divers. 44, 552-564.
Meng, H.H., Zhang, C.Y., Song, Y.G., et al., 2022b. Opening a door to the spatiotemporal history of plants from the tropical Indochina Peninsula to subtropical China. Mol. Phylogenet. Evol. 171, 107458.
Meng, H.H., Song, Y.G., 2023. Biogeographic patterns in Southeast Asia: Retrospectives and perspectives. Biodivers. Conserv. 31, 23261.
Meng, H.H., Song, Y.G., Hu, G.X., et al., 2025. Evolution of East Asian subtropical evergreen broad-leaved forests: When and how? J. Syst. Evol. doi: 10.111/jse.70001.
Mickael, B., Creig, B.S., Sonja, S.Y., 2018. Flow cytometry as tool in plant sciences, with emphasis on genome size and ploidy level assessment. Genet. Appl. 2, 1.
Mirarab, S., Warnow, T., 2015. ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, 44-52.
Mistry, J., Chuguransky, S., Williams, L., et al., 2021 Pfam: The protein families database in 2021. Nucleic Acids Res. 49, D412-D419.
Mumm, R., Posthumus, M.A., Dicke, M., 2008. Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ. 31, 575-585.
Nguyen, L.T., Schmidt, H.A., von Haeseler, A., et al., 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274.
Ou, S., Jiang, N., 2018. LTR_retriever: A highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. 176, 1410–1422.
Pertea, G., Pertea, M., 2020. GFF Utilities: GffRead and GffCompare. F1000Res. 9, 304.
Pertea, M., Pertea, G.M., Antonescu, C.M.,et al., 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290.
Potter, S.C., Luciani, A., Eddy, S.R., et al., 2018. HMMER web server: 2018 update. Nucleic Acids Res. 46, W200-W204.
Qiao, X., Li, Q., Yin, H., et al., 2019. Gene duplication and evolution in recurring polyploidization-diploidization cycles in plants. Genome Biol. 20, 38.
Qiao, X., Zhang, S.L., Paterson, A.H., 2022. Pervasive genome duplications across the plant tree of life and their links to major evolutionary innovations and transitions. Comput. Struct. Biotechnol. J. 20, 3248-3256.
Qin, S.Y., Zuo, Z.Y., Guo, C., et al., 2023. Phylogenomic insights into the origin and evolutionary history of evergreen broadleaved forests in East Asia under Cenozoic climate change. Mol. Ecol. 32, 2850-2868.
Quesneville, H., Bergman, C.M., Andrieu, O., et al., 2005. Combined evidence annotation of transposable elements in genome sequences. PLoS Comput. Biol. 1, 166–175.
Ranallo-Benavidez, T.R., Jaron, K.S., Schatz, M.C., 2020. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat. Commun. 11, 1432.
Razgour, O., Forester, B., Taggart, J.B., et al., 2019. Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections. Proc. Natl. Acad. Sci. U.S.A. 116, 10418-10423.
Ren, R., Wang, H., Guo, C., et al., 2018. Widespread whole genome duplications contribute to genome complexity and species diversity in Angiosperms. Mol. Plant 11, 414-428.
Roach, M.J., Schmidt, S.A., Borneman, A.R., 2018. Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinformatics 19, 460.
Servant, N., Varoquaux, N., Lajoie, B.R., et al., 2015. HiC-Pro: an optimized and flexible pipeline for Hi-C data processing. Genome Biol. 16, 259.
Siepielski, A.M., Morrissey, M.B., Buoro, M., et al., 2017. Precipitation drives global variation in natural selection. Science 355, 959.
Simao, F.A., Waterhouse, R.M., Ioannidis, P., et al., 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210-3212.
Soltis, P.S., Soltis, D.E., 2016. Ancient WGD events as drivers of key innovations in angiosperms. Curr. Opin. Plant Biol. 30, 159-165.
Stanke, M., Diekhans, M., Baertsch, R., et al., 2008. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24, 637-644.
Sun, P., Jiao, B., Yang, Y., et al., 2022. WGDI: A user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes. Mol. Plant 15, 1841-1851.
Sun, X.J., Wang, P.X., 2005. How old is the Asian monsoon system? Palaeobotanical records from China. Palaeogeogr. Palaeocl. Palaeoecol. 222, 181-222.
Suyama, M., Torrents, D., Bork, P., 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, 609-612.
Svenning, J., Eiserhardt, W.L., Normand, S., et al., 2015. The influence of paleoclimate on present-day patterns in biodiversitv and ecosystems. Annu. Rev. Ecol. Evol. Syst. 46, 551-572.
Tarailo-Graovac, M., Chen, N., 2009. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics Chapter 4, 4.10.1-4.10.14.
Travers, K.J., Patil, C.K., Wodicka, L., et al., 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258.
Vaghela, B., Vashi, R., Rajput, K., et al., 2022. Plant chitinases and their role in plant defense: A comprehensive review. Enzyme Microb. Tech. 159, 110055.
Vurture, G.W., Sedlazeck, F.J., Nattestad, M., et al., 2017. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 33, 2202-2204.
Wan, Q., Huang, K., Chen, S.F., et al., 2023. Fagus diversification in China in relation to East Asian monsoon evolution. Quaternary Sci. Rev. 320.
Wang, D., Zhang, Y.B., Zhang, Z., et al., 2010. KaKs_Calculator 2.0: A Toolkit Incorporating Gamma-Series Methods and Sliding Window Strategies. Genom. Proteom. Bioinf. 8, 77-80.
Wang, Y., Tang, H., Debarry, J.D., et al., 2012. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49.
Wang, M., Li, J., Wang, P., et al., 2021. Comparative genome analyses highlight transposon-mediated genome expansion and the evolutionary architecture of 3D genomic folding in cotton. Mol. Biol. Evol. 38, 3621-3636.
Wang, T.R., Ning, X., Zheng, S.S., et al., 2025. Genomic insights into ecological adaptation of oaks revealed by phylogenomic analysis of multiple species. Plant Divers. 47, 53-67.
Wang, X., Xu, M., Gao, C., et al., 2020. The roles of endomembrane trafficking in plant abiotic stress responses. J. Integr. Plant Biol. 62, 55-69.
Wei, S.G., Li, Lin, Bai, K.D., et al., 2024. Community structure and species diversity dynamics of a subtropical evergreen broad-leaved forest in China: 2005 to 2020. Plant Divers. 46, 70-77.
Westerhold, T., Marwan, N., Drury, A.J., et al., 2020. An astronomically dated record of Earth's climate and its predictability over the last 66 million years. Science 369, 1383.
Wicker, T., Sabot, F., Hua-Van, A., et al., 2007. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973–982.
Wu, F., Fang, X., Yang, Y., et al., 2022. Reorganization of Asian climate in relation to Tibetan Plateau uplift. Nat. Rev. Earth Env. 3, 684-700.
Xu, Q.H., Chen, F.H., Zhang, S.G., et al., 2017. Vegetation succession and East Asian Summer Monsoon changes since the last deglaciation inferred from high-resolution pollen record in Gonghai Lake, Shanxi Province, China. Holocene 27, 835-846.
Xu, Z., Wang, H., 2007. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, 265-268.
Yang, Z.H., 2007. PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591.
Ye, J.W., Tian, B., Li, D.Z., 2022. Monsoon intensification in East Asia triggered the evolution of its flora. Front Plant Sci. 13, 1046538.
Zachos, J.C., Dickens, G.R., Zeebe, R.E., 2008. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451, 279-283.
Zhang, C.Y., Low, S.L., Song, Y.G., et al., 2020. Shining a light on species delimitation in the tree genus Engelhardia Leschenault ex Blume (Juglandaceae). Mol. Phylogenet. Evol. 152, 106918.
Zhang, C.Y., Cao, G.L., Hu, J.L., et al., 2025. The reconstructed evolutionary history of the Engelhardia spicata complex highlights the impact of a three-tiered landform in the Indo-Burma ecoregion. Am. J. Bot. 112, e70077.
Zhang, Y., Duan, M.G., Huang P.H., et al., 2023. Blinded by the bright-Afforestation is affecting widespread sampling deficiency in plant collections. Forest Ecol. Manage. 530, 120765.
Zhao, J., Li, S., Huang, J., et al., 2025. Heterogeneous occurrence of evergreen broad-leaved forests in East Asia: Evidence from plant fossils. Plant Divers. 47, 1-12.
Zulak. K.G., Bohlmann, J., 2010. Terpenoid Biosynthesis and Specialized Vascular Cells of Conifer Defense. J. Integr. Plant Biol. 52, 86-97.
Zvereva, E.L., Kozlov, M.V., 2014. Effects of herbivory on leaf life span in woody plants: a meta-analysis. J. Ecol. 102, 873-881.

[1]	Na-Na Zhang (张娜娜), Gregory W. Stull, Xue-Jie Zhang (张学杰), Shou-Jin Fan (樊守金), Ting-Shuang Yi (伊廷双), Xiao-Jian Qu (曲小健). PlastidHub: An integrated analysis platform for plastid phylogenomics and comparative genomics [J]. Plant Diversity, 2025, 47(04): 544-560.
[2]	Fangdong Geng (耿方东), Miaoqing Liu (刘苗青), Luzhen Wang (王璐珍), Xuedong Zhang (张雪栋), Jiayu Ma (马佳雨), Hang Ye (叶航), Keith Woeste, Peng Zhao (赵鹏). Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya [J]. Plant Diversity, 2025, 47(03): 365-381.
[3]	Gulbar Yisilam, Enting Zheng, Chuanning Li, Zhiyong Zhang, Ying Su, Zhenzhou Chu, Pan Li, Xinmin Tian. The chromosome-scale genome of black wolfberry (Lycium ruthenicum) provides useful genomic resources for identifying genes related to anthocyanin biosynthesis and disease resistance [J]. Plant Diversity, 2025, 47(02): 201-213.
[4]	Jiagang Zhao, Shufeng Li, Jian Huang, Wenna Ding, Mengxiao Wu, Tao Su, Alexander Farnsworth, Paul J. Valdes, Linlin Chen, Yaowu Xing, Zhekun Zhou. Heterogeneous occurrence of evergreen broad-leaved forests in East Asia: Evidence from plant fossils [J]. Plant Diversity, 2025, 47(01): 1-12.
[5]	Zhe Chen, Zhuo Zhou, Ze-Min Guo, Truong Van Do, Hang Sun, Yang Niu. Historical development of karst evergreen broadleaved forests in East Asia has shaped the evolution of a hemiparasitic genus Brandisia (Orobanchaceae) [J]. Plant Diversity, 2023, 45(05): 501-512.
[6]	Hong-Hu Meng, Can-Yu Zhang, Shook Ling Low, Lang Li, Jian-Yong Shen, Nurainas, Yu Zhang, Pei-Han Huang, Shi-Shun Zhou, Yun-Hong Tan, Jie Li. Two new species from Sulawesi and Borneo facilitate phylogeny and taxonomic revision of Engelhardia (Juglandaceae) [J]. Plant Diversity, 2022, 44(06): 552-564.
[7]	MO Xin-Chun. Recent Progress in Model Grass Brachypodium distachyon (Poaceae) [J]. Plant Diversity, 2014, 36(02): 197-207.

Genome analyses provide insights into Engelhardia's adaptation to East Asia summer monsoon

Genome analyses provide insights into Engelhardia's adaptation to East Asia summer monsoon

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 7

Recommended Articles

Metrics

Comments