Flowering genes identification, network analysis, and database construction for 837 plants

Abstract

Flowering is one of the most important biological phenomena in the plant kingdom, which not only has important ecological significance, but also has substantial horticultural ornamental value. In this study, we undertook an exhaustive review of the advancements in our understanding of plant flowering genes. We delved into the identification and conducted comparative analyses of flowering genes across virtually all sequenced angiosperm plant genomes. Furthermore, we established an extensive angiosperm flowering atlas, encompassing a staggering 183 720 genes across eight pathways, along with 10 155 ABCDE mode genes, which play a pivotal role in plant flowering regulation. Through the examination of expression patterns, we unveiled the specificities of these flowering genes. An interaction network between flowering genes of the ABCDE model and their corresponding upstream genes offered a blueprint for comprehending their regulatory mechanisms. Moreover, we predicted the miRNA and target genes linked to the flowering processes of each species. To culminate our efforts, we have built a user-friendly web interface, named the Plant Flowering-time Gene Database (PFGD), accessible at http://pfgd.bio2db.com/. We firmly believe that this database will serve as a cornerstone in the global research community, facilitating the in-depth exploration of flowering genes in the plant kingdom. In summation, this pioneering endeavor represents the first comprehensive collection and comparative analysis of flowering genes in plants, offering valuable resources for the study of plant flowering genetics.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32172583), Natural Science Foundation for Distinguished Young Scholars of Hebei Province (C2022209010), Natural Science Foundation of Hebei (C2021209005), and Key Laboratory of Nucleic Research, Tangshan (2022TS003b).

Author contributions

X.S. conceived the project and was responsible for the project initiation. X.S., T.W., and X.M. supervised and managed the project and research. The data collection and bioinformatic analyses were led by X.S., T.W., Q.Y., X.M., Y.B., and R.C. The database construction was led by X.S., Z.L., T.Y., F.N., and X.M. The manuscript was organized, written and revised by X.S., T.W., X.M., Y.B., and R.Z. All authors read and approved the manuscript.

Data availability

All materials and related datasets in this study are available in our PFGD database (http://pfgd.bio2db.com).

Conflict of interest statement

The authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1] Song X, Duan W, Huang Z. et al. Comprehensive analysis of the flowering genes in Chinese cabbage and examination of evolutionary pattern of CO-like genes in plant kingdom. Sci Rep. 2015; 5:14631

[2] He Y, Chen T, Zeng X. Genetic and epigenetic understanding of the seasonal timing of flowering. Plant Commun. 2020; 1:100008

[3] Song YH, Ito S, Imaizumi T. Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci. 2013; 18:575-83

[4] Luo X, He Y. Experiencing winter for spring flowering: a molecular epigenetic perspective on vernalization. J Integr Plant Biol. 2020; 62:104-17

[5] Biswal DP, Panigrahi KCS. Light- and hormone-mediated development in non-flowering plants: An overview. Planta. 2021; 253:1

[6] Wei Q, Ma C, Xu Y. et al. Control of chrysanthemum flowering through integration with an aging pathway. Nat Commun. 2017; 8:829

[7] Fornara F, de Montaigu A, Coupland G. SnapShot: control of flowering in Arabidopsis. Cell. 2010; 141:550-550.e2

[8] Bouché F, Lobet G, Tocquin P. et al. FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res. 2016; 44:D1167-71

[9] Song YH, Shim JS, Kinmonth-Schultz HA. et al. Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol. 2015; 66:441-64

[10] Kong DY, Chen SJ, Zhou LG. et al. Research progress of photoperiod regulated genes on flowering time in rice. Yi Chuan. 2016; 38:532-42

[11] Zhou R, Liu P, Li D. et al. Photoperiod response-related gene SiCOL1 contributes to flowering in sesame. BMC Plant Biol. 2018; 18:343

[12] Zeng X, Liu H, Du H. et al. Soybean MADS-box gene GmAGL1 promotes flowering via the photoperiod pathway. BMC Genomics. 2018; 19:51

[13] Li L, Li X, Liu Y. et al. Flowering responses to light and temperature. Sci China Life Sci. 2016; 59:403-8

[14] Song YH. The effect of fluctuations in photoperiod and ambient temperature on the timing of flowering: time to move on natural environmental conditions. Mol Cells. 2016; 39:715-21

[15] Kushanov FN, Buriev ZT, Shermatov SE. et al. QTL mapping for flowering-time and photoperiod insensitivity of cotton Gossypium darwinii Watt. PLoS One. 2017; 12:e0186240

[16] Xiao D, Shen HR, Zhao JJ. et al. Genetic dissection of flowering time in Brassica rapa responses to temperature and photoperiod. Plant Sci. 2019; 280:110-9

[17] Adeyemo OS, Hyde PT, Setter TL. Identification of FT family genes that respond to photoperiod, temperature and genotype in relation to flowering in cassava (Manihot esculenta, Crantz). Plant Reprod. 2019; 32:181-91

[18] Zhu Y, Klasfeld S, Jeong CW. et al. TERMINAL FLOWER 1-FD complex target genes and competition with FLOWERING LOCUS T. Nat Commun. 2020; 11:5118

[19] Nakamichi N, Kudo T, Makita N. et al. Flowering time control in rice by introducing Arabidopsis clock-associated PSEUDO-RESPONSE REGULATOR 5. Biosci Biotechnol Biochem. 2020; 84:970-9

[20] Muntha ST, Zhang L, Zhou Y. et al. Phytochrome A signal transduction 1 and CONSTANS-LIKE 13 coordinately orchestrate shoot branching and flowering in leafy Brassica juncea. Plant Biotechnol J. 2019; 17:1333-43

[21] Rychel-Bielska S, Plewiński P, Kozak B. et al. Photoperiod and vernalization control of flowering-related genes: a case study of the narrow-leafed Lupin (Lupinus angustifolius L.). Front Plant Sci. 2020; 11:572135

[22] Mathieu AS, Périlleux C, Jacquemin G. et al. Impact of vernalization and heat on flowering induction, development and fertility in root chicory (Cichorium intybus L. var. sativum). J Plant Physiol. 2020; 254:153272

[23] Motoki K, Kinoshita Y, Hosokawa M. Non-vernalization flowering and seed set of cabbage induced by grafting onto radish rootstocks. Front Plant Sci. 2019; 9:1967

[24] Lazaro A, Zhou Y, Giesguth M. et al. PERPETUAL FLOWERING2 coordinates the vernalization response and perennial flowering in Arabis alpina. J Exp Bot. 2019; 70:949-61

[25] Qi HD, Lin Y, Ren QP. et al. RNA splicing of FLC modulates the transition to flowering. Front Plant Sci. 2019; 10:1625

[26] Whittaker C, Dean C. The FLC Locus: a platform for discoveries in epigenetics and adaptation. Annu Rev Cell Dev Biol. 2017; 33:555-75

[27] Son GH, Park BS, Song JT. et al. FLC-mediated flowering repression is positively regulated by sumoylation. J Exp Bot. 2014; 65:339-51

[28] Royo C, Dreisigacker S, Soriano JM. et al. Allelic variation at the vernalization response (Vrn-1) and photoperiod sensitivity (Ppd-1) genes and their association with the development of durum wheat landraces and modern cultivars. Front Plant Sci. 2020; 11:838

[29] Chen S, Wang J, Deng G. et al. Interactive effects of multiple vernalization (Vrn-1)- and photoperiod (Ppd-1)-related genes on the growth habit of bread wheat and their association with heading and flowering time. BMC Plant Biol. 2018; 18:374

[30] Li Y, Xiong H, Guo H. et al. Identification of the vernalization gene VRN-B1 responsible for heading date variation by QTL mapping using a RIL population in wheat. BMC Plant Biol. 2020; 20:331

[31] Xu T, Liu N, Wu C. et al. Intron-retained alternatively spliced VIN3-LIKE 2 gene from Chimonanthus praecox promotes flowering in transgenic Arabidopsis. Hortic Plant J. 2023; 9:789-800

[32] Kiss T, Balla K, Veisz O. et al. Allele frequencies in the VRN-A1, VRN-B1 and VRN-D 1 vernalization response and PPD-B1 and PPD-D1 photoperiod sensitivity genes, and their effects on heading in a diverse set of wheat cultivars (Triticum aestivum L.). Mol Breed. 2014; 34:297-310

[33] Wu Z, Fang X, Zhu D. et al. Autonomous pathway: FLOWERING LOCUS C repression through an antisense-mediated chromatin-silencing mechanism. Plant Physiol. 2020; 182:27-37

[34] Creux N, Harmer S. Circadian rhythms in plants. Cold Spring Harb Perspect Biol. 2019; 11:a034611

[35] Shim JS, Kubota A, Imaizumi T. Circadian clock and photoperiodic flowering in Arabidopsis: CONSTANS is a hub for signal integration. Plant Physiol. 2017; 173:5-15

[36] Shim JS, Imaizumi T. Circadian clock and photoperiodic response in Arabidopsis: from seasonal flowering to redox homeostasis. Biochem. 2015; 54:157-70

[37] Anwer MU, Davis A, Davis SJ. et al. Photoperiod sensing of the circadian clock is controlled by EARLY FLOWERING 3 and GIGANTEA. Plant J. 2020; 101:1397-410

[38] Li C, Li YH, Li Y. et al. A domestication-associated gene GmPRR3b regulates the circadian clock and flowering time in soybean. Mol Plant. 2020; 13:745-59

[39] Li MW, Lam HM. The modification of circadian clock components in soybean during domestication and improvement. Front Genet. 2020; 11:571188

[40] Toda Y, Kudo T, Kinoshita T. et al. Evolutionary insight into the clock-associated PRR5 transcriptional network of flowering plants. Sci Rep. 2019; 9:2983

[41] Gray JA, Shalit-Kaneh A, Chu DN. et al. The REVEILLE clock genes inhibit growth of juvenile and adult plants by control of cell size. Plant Physiol. 2017; 173:2308-22

[42] Noble JA, Seddon A, Uygun S. et al. The SEEL motif and members of the MYB-related REVEILLE transcription factor family are important for the expression of LORELEI in the synergid cells of the Arabidopsis female gametophyte. Plant Reprod. 2022; 35:61-76

[43] Jin S, Ahn JH. Regulation of flowering time by ambient temperature: repressing the repressors and activating the activators. New Phytol. 2021; 230:938-42

[44] Kumar SV, Lucyshyn D, Jaeger KE. et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature. 2012; 484:242-5

[45] Susila H, Nasim Z, Gawarecka K. et al. PHOSPHORYLETHANOLAMINE CYTIDYLYLTRANSFERASE 1 modulates flowering in a florigen-independent manner by regulating SVP. Development. 2020; 148:dev193870

[46] Wang J, Jiu S, Xu Y. et al. SVP-like gene PavSVP potentially suppressing flowering with PavSEP, PavAP1, and PavJONITLESS in sweet cherries (Prunus avium L.). Plant Physiol Biochem. 2021; 159:277-84

[47] Xie L, Zhang Y, Wang K. et al. TaVrt2, an SVP-like gene, cooperates with TaVrn1 to regulate vernalization-induced flowering in wheat. New Phytol. 2021; 231:834-48

[48] Méndez-Vigo B, Martínez-Zapater JM, Alonso-Blanco C. The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the genetic background. PLoS Genet. 2013; 9:e1003289

[49] Li X, Liu C, Zhao Z. et al. COR27 and COR28 are novel regulators of the COP1-HY 5 regulatory hub and photomorphogenesis in Arabidopsis. Plant Cell. 2020; 32:3139-54

[50] Wang L, Yang T, Lin Q. et al. Receptor kinase FERONIA regulates flowering time in Arabidopsis. BMC Plant Biol. 2020; 20:26

[51] Xie Y, Zhou Q, Zhao Y. et al. FHY3 and FAR1 integrate light signals with the miR156-SPL module-mediated aging pathway to regulate Arabidopsis flowering. Mol Plant. 2020; 13:483-98

[52] Zheng C, Ye M, Sang M. et al. A regulatory network for miR156-SPL module in Arabidopsis thaliana. Int J Mol Sci. 2019; 20:6166

[53] Manuela D, Xu M. Juvenile leaves or adult leaves: determinants for vegetative phase change in flowering plants. Int J Mol Sci. 2020; 21:9753

[54] Ahsan MU, Hayward A, Irihimovitch V. et al. Juvenility and vegetative phase transition in tropical/subtropical tree crops. Front Plant Sci. 2019; 10:729

[55] Lee YS, Lee DY, Cho LH. et al. Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice (N Y). 2014; 7:31

[56] Li XY, Guo F, Ma SY. et al. Regulation of flowering time via miR172-mediated APETALA2-like expression in ornamental gloxinia (Sinningia speciosa). J Zhejiang Univ Sci B. 2019; 20:322-31

[57] Yang T, Sun Y, Wang Y. et al. AtHSPR is involved in GA- and light intensity-mediated control of flowering time and seed set in Arabidopsis. J Exp Bot. 2020; 71:3543-59

[58] Sheng J, Li X, Zhang D. Gibberellins, brassinolide, and ethylene signaling were involved in flower differentiation and development in Nelumbo nucifera. Hortic Plant J. 2022; 8:243-50

[59] He J, Xin P, Ma X. et al. Gibberellin metabolism in flowering plants: an update and perspectives. Front Plant Sci. 2020; 11:532

[60] Bao S, Hua C, Shen L. et al. New insights into gibberellin signaling in regulating flowering in Arabidopsis. J Integr Plant Biol. 2020; 62:118-31

[61] Yan J, Li X, Zeng B. et al. FKF1 F-box protein promotes flowering in part by negatively regulating DELLA protein stability under long-day photoperiod in Arabidopsis. J Integr Plant Biol. 2020; 62:1717-40

[62] Li M, An F, Li W. et al. DELLA proteins interact with FLC to repress flowering transition. J Integr Plant Biol. 2016; 58:642-55

[63] Bonhomme F, Kurz B, Melzer S. et al. Cytokinin and gibberellin activate SaMADS a, a gene apparently involved in regulation of the floral transition in Sinapis alba. Plant J. 2000; 24:103-11

[64] Cucinotta M, Cavalleri A, Chandler JW. et al. Auxin and flower development: a blossoming field. Cold Spring Harb Perspect Biol. 2021; 13:a039974

[65] Oka M, Miyamoto K, Okada K. et al. Auxin polar transport and flower formation in Arabidopsis thaliana transformed with indoleacetamide hydrolase (iaaH) gene. Plant Cell Physiol. 1999; 40:231-7

[66] Liu X, Dinh TT, Li D. et al. AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA2 in floral meristem determinacy. Plant J. 2014; 80:629-41

[67] Wahl V, Ponnu J, Schlereth A. et al. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science. 2013; 339:704-7

[68] Zhang ZW, Fu YF, Zhou YH. et al. Nitrogen and nitric oxide regulate Arabidopsis flowering differently. Plant Sci. 2019; 284:177-84

[69] Kataya ARA, Elshobaky A, Heidari B. et al. Multi-targeted trehalose-6-phosphate phosphatase I harbors a novel peroxisomal targeting signal 1 and is essential for flowering and development. Planta. 2020; 251:98

[70] Fichtner F, Olas JJ, Feil R. et al. Functional features of TREHALOSE-6-PHOSPHATE SYNTHASE1, an essential enzyme in Arabidopsis. Plant Cell. 2020; 32:1949-72

[71] Yoon J, Cho L-H, Tun W. et al. Sucrose signaling in higher plants. Plant Sci. 2021; 302:110703

[72] Coito JL, Silva H, Ramos MJN. et al. Vitis flower sex specification acts downstream and independently of the ABCDE model genes. Front Plant Sci. 2018; 9:1029

[73] Collinsworth AW, Priest EL, Masica AL. Evaluating the cost-effectiveness of the ABCDE bundle: impact of bundle adherence on inpatient and 1-year mortality and costs of care. Crit Care Med. 2020; 48:1752-9

[74] Ghaemizadeh F, Dashti F, Shafeinia A. Expression pattern of ABCDE model genes in floral organs of bolting garlic clone. Gene Expr Patterns. 2019; 34:119059

[75] Palumbo F, Vannozzi A, Magon G. et al. Genomics of flower identity in grapevine (Vitis vinifera L.). Front Plant Sci. 2019; 10:316

[76] Liu X, Gu J, Wang J. et al. Lily breeding by using molecular tools and transformation systems. Mol Biol Rep. 2014; 41:6899-908

[77] Heiduk A, Pramanik D, Spaans M. et al. Pitfall flower development and organ identity of Ceropegia sandersonii (Apocynaceae-Asclepiadoideae). Plants (Basel). 2020; 9:1767

[78] Di Marzo M, Herrera-Ubaldo H, Caporali E. et al. SEEDSTICK controls Arabidopsis fruit size by regulating cytokinin levels and FRUITFULL. Cell Rep. 2020; 30:2846-2857.e3

[79] Luo C, Liu H, Ren J. et al. Cold-inducible expression of an Arabidopsis thaliana AP 2 transcription factor gene, AtCRAP2, promotes flowering under unsuitable low-temperatures in chrysanthemum. Plant Physiol Biochem. 2020; 146:220-30

[80] Pi M, Hu S, Cheng L. et al. The MADS-box gene FveSEP3 plays essential roles in flower organogenesis and fruit development in woodland strawberry. Hortic Res. 2021; 8:247

[81] Fei X, Shi Q, Qi Y. et al. ZbAGL11, a class D MADS-box transcription factor of Zanthoxylum bungeanum, is involved in sporophytic apomixis. Hortic Res. 2021; 8:23

[82] Chen H, Ji H, Zhu S. et al. Carotenoid and transcriptome profiles of a novel citrus cultivar ‘Jinlegan’ reveal mechanisms of yellowish fruit formation. Hortic Adv. 2023; 1:5

[83] Hori K, Matsubara K, Yano M. Genetic control of flowering time in rice: integration of Mendelian genetics and genomics. Theor Appl Genet. 2016; 129:2241-52

[84] Huang R, Liu D, Huang M. et al. CpWRKY71, a WRKY transcription factor gene of Wintersweet (Chimonanthus praecox), promotes flowering and leaf senescence in Arabidopsis. Int J Mol Sci. 2019; 20:5325

[85] Li W, Wang H, Yu D. Arabidopsis WRKY transcription factors WRKY12 and WRKY13 oppositely regulate flowering under short-day conditions. Mol Plant. 2016; 9:1492-503

[86] Newton RJ, Hay FR, Ellis RH. Temporal patterns of seed germination in early spring-flowering temperate woodland geophytes are modified by warming. Ann Bot. 2020; 125:1013-23

[87] Blair L, Auge G, Donohue K. Effect of FLOWERING LOCUS C on seed germination depends on dormancy. Funct Plant Biol. 2017; 44:493-506

[88] Zhang L, Chen F, Zhang X. et al. The water lily genome and the early evolution of flowering plants. Nature. 2020; 577:79-84

[89] Waheed S, Zeng L. The critical role of miRNAs in regulation of flowering time and flower development. Genes (Basel). 2020; 11:319

[90] Xu M, Hu T, Zhao J. et al. Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes in Arabidopsis thaliana. PLoS Genet. 2016; 12:e1006263

[91] Aguilar-Jaramillo AE, Marín-González E, Matías-Hernández L. et al. TEMPRANILLO is a direct repressor of the microRNA miR172. Plant J. 2019; 100:522-35

[92] Millar AA, Lohe A, Wong G. Biology and function of miR159 in plants. Plants (Basel). 2019; 8:255

[93] Xu MY, Zhang L, Li WW. et al. Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J Exp Bot. 2014; 65:89-101

[94] Pei Q, Yu T, Wu T. et al. Comprehensive identification and analyses of the Hsf gene family in the whole-genome of three Apiaceae species. Hortic Plant J. 2021; 7:457-68

[95] Tong W, Feng S, Yang Q. et al. Integration of the metabolome and transcriptome reveals the metabolites and genes related to nutritional and medicinal value in Coriandrum sativum. J Integr Agric. 2021; 20:1807-18

[96] Li YC, Lu YC. BLASTP-ACC: parallel architecture and hardware accelerator design for BLAST-based protein sequence alignment. IEEE Trans Biomed Circuits Syst. 2019; 13:1771-82

[97] Sobieraj DM, Weeda ER, Nguyen E. et al. Association of inhaled corticosteroids and long-acting β-agonists as controller and quick relief therapy with exacerbations and symptom control in persistent asthma: a systematic review and meta-analysis. JAMA. 2018; 319:1485-96

[98] Lu S, Wang J, Chitsaz F. et al. CDD/SPARCLE:the conserved domain database in 2020. Nucleic Acids Res. 2020; 48:D265-d268

[99] Bailey TL, Johnson J, Grant CE. et al. The MEME suite. Nucleic Acids Res. 2015; 43:W39-49

[100] Chow CN, Lee TY, Hung YC. et al. PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants. Nucleic Acids Res. 2019; 47:D1155-d1163

[101] Amith MT, Fujimoto K, Tao C. NET-EXPO: a Gephi plugin towards social network analysis of network exposure for unipartite and bipartite graphs. HCI Int. 2019; 1034:3-12

[102] Jia A, Xu L, Wang Y. Venn diagrams in bioinformatics. Brief Bioinform. 2021; 22:bbab108

[103] El-Gebali S, Mistry J, Bateman A. et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019; 47:D427-32

[104] Vesztrocy AW, Dessimoz C. A gene ontology tutorial in python. Methods Mol Biol. 2017; 1446:221-9

[105] Virtanen P, Gommers R, Oliphant TE. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat Methods. 2020; 17:261-72

[106] Zhang Y, Zhang Y, Li B. et al. Polyploidy events shaped the expansion of transcription factors in Cucurbitaceae and exploitation of genes for tendril development. Hortic Plant J. 2022; 8:562-74

[107] Liang Z, Zhang Q, Ji C. et al. Reorganization of the 3D chromatin architecture of rice genomes during heat stress. BMC Biol. 2021; 19:53

[108] Liu C, Cheng YJ, Wang JW. et al. Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat Plants. 2017; 3:742-8

[109] Sullivan A, Purohit PK, Freese NH. et al. An ’eFP-Seq Browser’ for visualizing and exploring RNA sequencing data. Plant J. 2019; 100:641-54

[110] Yano R, Nonaka S, Ezura H. Melonet-DB, a grand RNA-Seq gene expression atlas in melon (Cucumis melo L.). Plant Cell Physiol. 2018; 59:e4

[111] Fu CH, Chen YW, Hsiao YY. et al. OrchidBase: a collection of sequences of the transcriptome derived from orchids. Plant Cell Physiol. 2011; 52:238-43

[112] Flores-Tornero M, Proost S, Mutwil M. et al. Transcriptomics of manually isolated Amborella trichopoda egg apparatus cells. Plant Reprod. 2019; 32:15-27

[113] Kielbasa SM, Bluthgen N, Fahling M. et al. Targetfinder.org: a resource for systematic discovery of transcription factor target genes. Nucleic Acids Res. 2010; 38:W233-8

[114] Song X, Yang Q, Bai Y. et al. Comprehensive analysis of SSRs and database construction using all complete gene-coding sequences in major horticultural and representative plants. Hortic Res. 2021; 8:122

[115] Song X, Nie F, Chen W. et al. Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander. Hortic Res. 2020; 7:55

[116] Yu T, Bai Y, Liu Z. et al. Large-scale analyses of heat shock transcription factors and database construction based on whole-genome genes in horticultural and representative plants. Hortic Res. 2022; 9:uhac035

[117] Meng F, Tang Q, Chu T. et al. TCMPG: an integrative database for traditional Chinese medicine plant genomes. Hortic Res. 2022; 9:uhac060

[118] Liu Z, Li N, Yu T. et al. The Brassicaceae Genome Resource (TBGR): a comprehensive genome platform for Brassicaceae plants. Plant Physiol. 2022; 190:226-37

[119] Yu T, Ma X, Liu Z. et al. TVIR: a comprehensive vegetable information resource database for comparative and functional genomic studies. Hortic Res. 2022; 9:uhac213