Abstract
Main conclusion
The hierarchical architecture of chromatins affects the gene expression level of glandular secreting trichomes and the artemisinin biosynthetic pathway-related genes, consequently bringing on huge differences in the content of artemisinin and its derivatives of A. annua.
Abstract
The plant of traditional Chinese medicine "Qinghao" is called Artemisia annua L. in Chinese Pharmacopoeia. High content and the total amount of artemisinin is the main goal of A. annua breeding, nevertheless, the change of chromatin organization during the artemisinin synthesis process has not been discovered yet. This study intended to find the roles of chromatin structure in the production of artemisinin through bioinformatics and experimental validation. Chromosome conformation capture analysis was used to scrutinize the interactions among chromosomes and categorize various scales of chromatin during artemisinin synthesis in A. annua. To confirm the effect of the changes in chromatin structure, Hi-C and RNA-sequencing were performed on two different strains to find the correlation between chromatin structure and gene expression levels on artemisinin synthesis progress and regulation. Our results revealed that the frequency of intra-chromosomal interactions was higher in the inter-chromosomal interactions between the root and leaves on a high artemisinin production strain (HAP) compared to a low artemisinin production strain (LAP). We found that compartmental transition was connected with interactions among different chromatins. Interestingly, glandular secreting trichomes (GSTs) and the artemisinin biosynthetic pathway (ABP) related genes were enriched in the areas which have the compartmental transition, reflecting the regulation of artemisinin synthesis. Topologically associated domain boundaries were associated with various distributions of genes and expression levels. Genes associated with ABP and GST in the adjacent loop were highly expressed, suggesting that epigenetic regulation plays an important role during artemisinin synthesis and glandular secreting trichomes production process. Chromatin structure could show an important status in the mechanisms of artemisinin synthesis process in A. annua.
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Data availability
The data reported in this article have been deposited in NCBI Sequence Read Archive (SRA) under Accession Number PRJNA991086.
Abbreviations
- ABP:
-
Artemisinin biosynthetic pathway
- DEG:
-
Differentially expressed gene
- GST:
-
Glandular secreting trichome
- HAN1:
-
A. annua From Hainan
- HAP:
-
High artemisinin production strain
- LAP:
-
Low artemisinin production strain
- LQ-9:
-
A. annua From Linqing
- TAD:
-
Topological associated domain
References
Abranches R, Santos AP, Wegel E, Williams S, Castilho A, Christou P, Shaw P, Stoger E (2000) Widely separated multiple transgene integration sites in wheat chromosomes are brought together at interphase. Plant J 24(6):713–723. https://doi.org/10.1111/j.1365-313X.2000.00908.x
Aftab T, Khan M, Idrees M, Naeem M, Moinuddin HN (2011) Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L. Protoplasma 248(3):601–612. https://doi.org/10.1007/s00709-010-0218-5
Appalasamy S, Lo K, Ch’ng S, Nornadia K, Othman A, Chan L (2014) Antimicrobial activity of artemisinin and precursor derived from in vitro plantlets of Artemisia annua L. BioMed Res Int. https://doi.org/10.1155/2014/215872
Arsenault PR, Vail D, Wobbe KK, Erickson K, Weathers PJ (2010) Reproductive development modulates gene expression and metabolite levels with possible feedback inhibition of artemisinin in Artemisia annua. Plant Physiol 154(2):958–968. https://doi.org/10.1104/pp.110.162552
Boya R, Yadavalli AD, Nikhat S, Kurukuti S, Palakodeti D, Pongubala JMR (2017) Developmentally regulated higher-order chromatin interactions orchestrate B cell fate commitment. Nucleic Acids Res 45(19):11070–11087. https://doi.org/10.1093/nar/gkx722
Brown GD (1994) Cadinanes from Artemisia annua that may be intermediates in the biosynthesis of artemisinin. Phytochemistry 36(3):637–641. https://doi.org/10.1016/S0031-9422(00)89788-5
Brown GD (2010) The biosynthesis of artemisinin (Qinghaosu) and the phytochemistry of Artemisia annua L. (Qinghao). Molecules 15(11):7603–7698. https://doi.org/10.3390/molecules15117603
Casewell N, Harrison R, Wüster W, Wagstaff S (2009) Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts. BMC Genomics 10:564. https://doi.org/10.1186/1471-2164-10-564
Chen S, **ang L, Li L, Wu L, Huang L, Zhang D, Sun PJCSB (2017) Global strategy and raw material production on artemisinin resources regeneration. Chin Sci Bull 62:1982–1996
Chuang CH, Belmont AS (2007) Moving chromatin within the interphase nucleus-controlled transitions? Semin Cell Dev Biol 18(5):698–706. https://doi.org/10.1016/j.semcdb.2007.08.012
Consortium EP (2004) The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306(5696):636–640. https://doi.org/10.1126/science.1105136
Covello PS, Teoh KH, Polichuk DR, Reed DW, Nowak G (2007) Functional genomics and the biosynthesis of artemisinin. Phytochemistry 68(14):1864–1871. https://doi.org/10.1016/j.phytochem.2007.02.016
Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nature Rev Genet 2(4):292–301
Dekker J, Mirny L (2016) The 3D genome as moderator of chromosomal communication. Cell 164(6):1110–1121. https://doi.org/10.1016/j.cell.2016.02.007
Delabays N, Simonnet X, Gaudin M (2001) The genetics of artemisinin content in Artemisia annua L. and the breeding of high yielding cultivars. Curr Med Chem 8(15):1795–1801
Deschamps S, Crow JA, Chaidir N, Peterson-Burch B, Kumar S, Lin H, Zastrow-Hayes G, May GD (2021) Chromatin loop anchors contain core structural components of the gene expression machinery in maize. BMC Genomics 22(1):23. https://doi.org/10.1186/s12864-020-07324-0
Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485(7398):376–380. https://doi.org/10.1038/nature11082
Dong P, Tu X, Chu PY, Lü P, Zhu N, Grierson D, Du B, Li P, Zhong S (2017) 3D chromatin architecture of large plant genomes determined by local A/B compartments. Mol Plant 10(12):1497–1509. https://doi.org/10.1016/j.molp.2017.11.005
Duke SO (1994) Glandular trichomes - A focal point of chemical and structural interactions. Int J Plant Sci 155(6):617–620. https://doi.org/10.1086/297200
Duke SO, Paul RN (1993) Development and fine structure of the glandular trichomes of Artemisia annua L. Int J Plant Sci 154(1):107–118. https://doi.org/10.1086/297096
Durand NC, Shamim MS, Machol I, Rao SS, Huntley MH, Lander ES, Aiden EL (2016) Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst 3(1):95–98. https://doi.org/10.1016/j.cels.2016.07.002
Feng S, Cokus SJ, Schubert V, Zhai J, Pellegrini M, Jacobsen SE (2014) Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol Cell 55(5):694–707. https://doi.org/10.1016/j.molcel.2014.07.008
Flyamer IM, Gassler J, Imakaev M, Brandao HB, Ulianov SV, Abdennur N, Razin SV, Mirny LA, Tachibana-Konwalski K (2017) Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature 544(7648):110–114. https://doi.org/10.1038/nature21711
Fortin JP, Hansen KD (2015) Reconstructing A/B compartments as revealed by Hi-C using long-range correlations in epigenetic data. Genome Biol 16(1):180. https://doi.org/10.1186/s13059-015-0741-y
Fraser J, Ferrai C, Chiariello AM, Schueler M, Rito T, Laudanno G, Barbieri M, Moore BL, Kraemer DC, Aitken S, **e SQ, Morris KJ, Itoh M, Kawaji H, Jaeger I, Hayashizaki Y, Carninci P, Forrest AR, Consortium F, Semple CA, Dostie J, Pombo A, Nicodemi M, (2015) Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation. Mol Syst Biol 11 (12):852. doi:https://doi.org/10.15252/msb.20156492
Grob S, Schmid Marc W, Grossniklaus U (2014) Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol Cell 55(5):678–693. https://doi.org/10.1016/j.molcel.2014.07.009
Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B (2008) Domain organization of human chromosomes revealed by map** of nuclear lamina interactions. Nature 453(7197):948–951. https://doi.org/10.1038/nature06947
Imakaev M, Fudenberg G, McCord RP, Naumova N, Goloborodko A, Lajoie BR, Dekker J, Mirny LA (2012) Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat Methods 9(10):999–1003. https://doi.org/10.1038/nmeth.2148
Javierre BM, Burren OS, Wilder SP, Kreuzhuber R, Hill SM, Sewitz S, Cairns J, Wingett SW, Varnai C, Thiecke MJ, Burden F, Farrow S, Cutler AJ, Rehnstrom K, Downes K, Grassi L, Kostadima M, Freire-Pritchett P, Wang F, Consortium B, Stunnenberg HG, Todd JA, Zerbino DR, Stegle O, Ouwehand WH, Frontini M, Wallace C, Spivakov M, Fraser P (2016) Lineage-specific genome architecture links enhancers and non-coding disease vriants to target gene promoters. Cell 167 (5):1369–1384, e1319. doi:https://doi.org/10.1016/j.cell.2016.09.037
Jiang H, Lei R, Ding S-W, Zhu S (2014) Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15(1):1–12
** F, Li Y, Dixon JR, Selvaraj S, Ye Z, Lee AY, Yen CA, Schmitt AD, Espinoza CA, Ren B (2013) A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503(7475):290–294. https://doi.org/10.1038/nature12644
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360. https://doi.org/10.1038/nmeth.3317
Klayman D (1985) Qinghaosu (artemisinin): an antimalarial drug from China. Science 228(4703):1049–1055. https://doi.org/10.1126/science.3887571
Krijger PH, Di Stefano B, de Wit E, Limone F, van Oevelen C, de Laat W, Graf T (2016) Cell-of-origin-specific 3D genome structure acquired during somatic cell reprogramming. Cell Stem Cell 18(5):597–610. https://doi.org/10.1016/j.stem.2016.01.007
Le Dily F, Bau D, Pohl A, Vicent GP, Serra F, Soronellas D, Castellano G, Wright RH, Ballare C, Filion G, Marti-Renom MA, Beato M (2014) Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev 28(19):2151–2162. https://doi.org/10.1101/gad.241422.114
Liang Z, Zhang Q, Ji C, Hu G, Zhang P, Wang Y, Yang L, Gu X (2021) Reorganization of the 3D chromatin architecture of rice genomes during heat stress. BMC Biol 19(1):53. https://doi.org/10.1186/s12915-021-00996-4
Liao B, Hu H, **ao S, Zhou G, Sun W, Chu Y, Meng X, Wei J, Zhang H, Xu J, Chen S (2021a) Global pharmacopoeia genome database is an integrated and mineable genomic database for traditional medicines derived from eight international pharmacopoeias. Sci China Life Sci 65(4):809–817. https://doi.org/10.1007/s11427-021-1968-7
Liao X, Guo S, Yin X, Liao B, Li M, Su H, Li Q, Pei J, Gao J, Lei J, Li X, Huang Z, Xu J, Chen S (2021b) Hierarchical chromatin features reveal the toxin production in Bungarus multicinctus. Chinese Med 16(1):90. https://doi.org/10.1186/s13020-021-00502-6
Liao B, Shen X, **ang L, Guo S, Chen S, Meng Y, Liang Y, Ding D, Bai J, Zhang D, Czechowski T, Li Y, Yao H, Ma T, Howard C, Sun C, Liu H, Liu J, Pei J, Gao J, Wang J, Qiu X, Huang Z, Li H, Yuan L, Wei J, Graham I, Xu J, Zhang B, Chen S (2022) Allele-aware chromosome-level genome assembly of Artemisia annua reveals the correlation between ADS expansion and artemisinin yield. Mol Plant 15(8):1310–1328. https://doi.org/10.1016/j.molp.2022.05.013
Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J (2009) Comprehensive map** of long-range interactions reveals folding principles of the human genome. Science 326(5950):289–293. https://doi.org/10.1126/science.1181369
Lin D, Xu W, Hong P, Wu C, Zhang Z, Zhang S, **ng L, Yang B, Zhou W, **ao Q, Wang J, Wang C, He Y, Chen X, Cao X, Man J, Reheman A, Wu X, Hao X, Hu Z, Chen C, Cao Z, Yin R, Fu ZF, Zhou R, Teng Z, Li G, Cao G (2022) Decoding the spatial chromatin organization and dynamic epigenetic landscapes of macrophage cells during differentiation and immune activation. Nature Comm 13(1):5857. https://doi.org/10.1038/s41467-022-33558-5
Liu C, Wang C, Wang G, Becker C, Zaidem M, Weigel D (2016) Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res 26(8):1057–1068. https://doi.org/10.1101/gr.204032.116
Lommen W, Elzinga S, Verstappen F, Bouwmeester H (2007) Artemisinin and sesquiterpene precursors in dead and green leaves of Artemisia annua L. crops. Planta Medica 73(10):1133–1139. https://doi.org/10.1055/s-2007-981567
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550. https://doi.org/10.1186/s13059-014-0550-8
Luo C, Hajkova P, Ecker JR, (2018) Dynamic DNA methylation: In the right place at the right time. 361 (6409):1336-1340. doi:https://doi.org/10.1126/science.aat6806
Maes L, Van Nieuwerburgh F, Zhang Y, Reed D, Pollier J, Vande Casteele S, Inzé D, Covello P, Deforce D, Goossens A (2011) Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants. New Phytol 189(1):176–189. https://doi.org/10.1111/j.1469-8137.2010.03466.x
Meaburn KJ, Misteli T (2007) Chromosome territories. Nature 445(7126):379–381
Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, Gribnau J, Barillot E, Bluthgen N, Dekker J, Heard E (2012) Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485(7398):381–385. https://doi.org/10.1038/nature11049
Olsson ME, Olofsson LM, Lindahl A-L, Lundgren A, Brodelius M, Brodelius PE (2009) Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L. Phytochemistry 70(9):1123–1128. https://doi.org/10.1016/j.phytochem.2009.07.009
Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–295. https://doi.org/10.1038/nbt.3122
Quinlan AR (2014) BEDTools: The swiss-army tool for genome feature analysis. Curr Protoc Bioinformatics. https://doi.org/10.1002/0471250953.bi1112s47
Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES, Aiden EL (2014) A 3D map of the human genome at kilobase resolution reveals principles of chromatin loo**. Cell 159(7):1665–1680. https://doi.org/10.1016/j.cell.2014.11.021
Rokyta D, Lemmon A, Margres M, Aronow K (2012) The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genomics 13:312. https://doi.org/10.1186/1471-2164-13-312
Schmitt AD, Hu M, Jung I, Xu Z, Qiu Y, Tan CL, Li Y, Lin S, Lin Y, Barr CL, Ren B (2016) A compendium of chromatin contact maps reveals spatially active regions in the human genome. Cell Rep 17(8):2042–2059. https://doi.org/10.1016/j.celrep.2016.10.061
Schramek N, Wang H, Römisch-Margl W, Keil B, Radykewicz T, Winzenhörlein B, Beerhues L, Bacher A, Rohdich F, Gershenzon J, Liu B, Eisenreich W (2010) Artemisinin biosynthesis in growing plants of Artemisia annua. A 13CO2 study. Phytochemistry 71:179–187. https://doi.org/10.1016/j.phytochem.2009.10.015
Seitan VC, Faure AJ, Zhan Y, McCord RP, Lajoie BR, Ing-Simmons E, Lenhard B, Giorgetti L, Heard E, Fisher AG, Flicek P, Dekker J, Merkenschlager M (2013) Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments. Genome Res 23(12):2066–2077. https://doi.org/10.1101/gr.161620.113
Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, Hoichman M, Parrinello H, Tanay A, Cavalli G (2012) Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148(3):458–472. https://doi.org/10.1016/j.cell.2012.01.010
Shaw PJ, Abranches R, Paula Santos A, Beven AF, Stoger E, Wegel E, González-Melendi P (2002) The architecture of interphase chromosomes and nucleolar transcription sites in plants. J Struct Biol 140(1–3):31–38. https://doi.org/10.1016/s1047-8477(02)00537-3
Su Y, Wang S, Zhang F, Zheng H, Liu Y, Huang T, Ding Y (2017) Phosphorylation of histone H2A at serine 95: A plant-specific mark involved in flowering time regulation and H2A.Z deposition. Plant Cell 29(9):2197–2213. https://doi.org/10.1105/tpc.17.00266
Tanay A, Cavalli G (2013) Chromosomal domains: epigenetic contexts and functional implications of genomic compartmentalization. Curr Opin Genet Dev 23(2):197–203. https://doi.org/10.1016/j.gde.2012.12.009
Tang Z, Luo OJ, Li X, Zheng M, Zhu JJ, Szalaj P, Trzaskoma P, Magalska A, Wlodarczyk J, Ruszczycki B, Michalski P, Piecuch E, Wang P, Wang D, Tian SZ, Penrad-Mobayed M, Sachs LM, Ruan X, Wei CL, Liu ET, Wilczynski GM, Plewczynski D, Li G, Ruan Y (2015) CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163(7):1611–1627. https://doi.org/10.1016/j.cell.2015.11.024
Tappeh K, Hanifian H, Diba K (2012) Comparison of four methods for DNA extraction from Echinococcus granulosus protoscoleces. Turkiye Parazitolojii Dergisi 36(2):100–104. https://doi.org/10.5152/tpd.2012.24
Tiang CL, He Y, Pawlowski WP (2012) Chromosome organization and dynamics during interphase, mitosis, and meiosis in plants. Plant Physiol 158(1):26–34. https://doi.org/10.1104/pp.111.187161
Tomato Genome C (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485(7400):635–641. https://doi.org/10.1038/nature11119
Towler MJ, Weathers PJ (2015) Variations in key artemisinic and other metabolites throughout plant development in Artemisia annua L. for potential therapeutic use. Ind Crops Products 67:185–191. https://doi.org/10.1016/j.indcrop.2015.01.007
Tu Y (2016) Artemisinin - A gift from traditional Chinese medicine to the world (Nobel Lecture). Angewandte Chemie (international Edn in English) 55(35):10210–10226. https://doi.org/10.1002/anie.201601967
Urreizti R, Garcia-Giralt N, Riancho J, González-Macías J, Civit S, Güerri R, Yoskovitz G, Sarrion P, Mellivobsky L, Díez-Pérez A, Nogués X, Balcells S, Grinberg D (2012) COL1A1 haplotypes and hip fracture. J Bone Miner Res 27(4):950–953. https://doi.org/10.1002/jbmr.1536
Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom DT, Tanay A, Hadjur S (2015) Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep 10(8):1297–1309. https://doi.org/10.1016/j.celrep.2015.02.004
Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, Wysocka J, Lei M, Dekker J, Helms JA, Chang HY (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472(7341):120–124. https://doi.org/10.1038/nature09819
Wang L, Jia G, Jiang X, Cao S, Chen ZJ, Song Q (2021) Altered chromatin architecture and gene expression during polyploidization and domestication of soybean. Plant Cell 33(5):1430–1446. https://doi.org/10.1093/plcell/koab081
**ao L, Tan H, Zhang L (2016) Artemisia annua glandular secretory trichomes: the biofactory of antimalarial agent artemisinin. Sci Bull 61(1):26–36. https://doi.org/10.1007/s11434-015-0980-z
Xu J, Guo S, Yin X, Li M, Su H, Liao X, Li Q, Le L, Chen S, Liao B, Hu H, Lei J, Zhu Y, Qiu X, Luo L, Chen J, Cheng R, Chang Z, Zhang H, Wu NC, Guo Y, Hou D, Pei J, Gao J, Hua Y, Huang Z, Chen S (2022) Genomic, transcriptomic, and epigenomic analysis of a medicinal snake, Bungarus multicinctus, to provides insights into the origin of Elapidae neurotoxins. Acta Pharm Sin B 13(5):2234–2249. https://doi.org/10.1016/j.apsb.2022.11.015
Yadav T, Quivy J-P, Almouzni G (2018) Chromatin plasticity: a versatile landscape that underlies cell fate and identity. Science 361(6409):1332–1336. https://doi.org/10.1126/science.aat8950
Zhang Y, McCord RP, Ho YJ, Lajoie BR, Hildebrand DG, Simon AC, Becker MS, Alt FW, Dekker J (2012) Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148(5):908–921. https://doi.org/10.1016/j.cell.2012.02.002
Zhang X, Pandey MK, Wang J, Zhao K, Ma X, Li Z, Zhao K, Gong F, Guo B, Varshney RK, Yin D (2021) Chromatin spatial organization of wild type and mutant peanuts reveals high-resolution genomic architecture and interaction alterations. Genome Biol 22(1):315. https://doi.org/10.1186/s13059-021-02520-x
Zhou Z, Tan H, Li Q, Li Q, Wang Y, Bu Q, Li Y, Wu Y, Chen W, Zhang L (2020) TRICHOME AND ARTEMISIN REGULATOR2 positively regulates trichome development and artemisinin biosynthesis in Artemisia annua. New Phytol 228(3):932–945. https://doi.org/10.1111/nph.16777
Acknowledgements
The authors thank all members of the group for fruitful discussions. And we thank Y. M. and Y. L. for samples of the various A.annua and J. X. for helpful comments on an ealier vision of this manuscript.
Funding
The study was supported by the NSFC Guizhou Karst Center project “Research on some basic issues of characteristic ethnic medicine in karst areas”—subproject “Research on suitability and protection of characteristic medicinal plant resources” (U1812403-1), the Major National Science and Technology Program of China for Innovative Drug (No. 2019ZX09201005-006-001) and the Open Research Fund of Chengdu University of Traditional Chinese Medicine Key Laboratory of Systematic Research of Distinctive Chinese Medicine Resources in Southwest China (No. 2020GZ2011016).
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Liao, X., Guo, S., Liao, B. et al. Chromatin architecture of two different strains of Artemisia annua reveals the alterations in interaction and gene expression. Planta 258, 74 (2023). https://doi.org/10.1007/s00425-023-04223-y
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DOI: https://doi.org/10.1007/s00425-023-04223-y