2010. The rise and eventual dominance of the core eudicots may have benefited from the well-known γ hexaploidization event in their most recent common ancestor [4]. CAS  Manage cookies/Do not sell my data we use in the preference centre. S11a). T. sinense has been documented as an endangered species in China and is currently listed in Appendix III of the Convention of International Trade of Endangered Species [31]. Kent WJ. Gravitropism, along with phototropism and hydrotropism, are traits believed to have evolved during the transition from an aquatic to terrestrial habitat. In the ML tree (Additional file 1: Fig. 2009;161:105–21. The transcription factors ASL19/LBD30 and ASL20/LBD18 are involved in a positive feedback loop to regulate VND7 expression [27]. Tropical Plant Biol. Plant Physiol. In the transverse sections, radial files of the peculiar cells are indicated by the arrows. Lagesen K, Hallin P, Rødland EA, Staerfeldt HH, Rognes T, Ussery DW. Wan T, Liu Z-M, Li L-F, Leitch AR, Leitch IJ, Lohaus R, et al. Li H. Minimap2: pairwise alignment for nucleotide sequences. Figshare. For almost 150 years, T. sinense was considered to produce secondary xylem that has tracheids but lacks vessel elements [16,17,18]. Nat Genet. In total, 87 R2R3-MYB genes were identified in the T. sinense genome. Species name abbreviations given in Fig. J Biogeogr. However, no LBD18/LBD30 genes were identified in genomes of three gymnosperm species, one lycophyte, and one moss, suggesting that the origin of the LBD18 subfamily may have occurred after the divergence of angiosperms and gymnosperms. The authors read and approved the final manuscript. As Tetracentron sinense is a basal eudicot with unique tracheary elements, its genome provides a unique reference for inferring the early evolution of the eudicots and the mechanisms underlying the formation of vessel elements. 2006;34:W609–12. 2020;577:79–84. We survey 141 sequenced plant genomes to elucidate consequences of gene and genome duplication, processes central to the evolution of biodiversity. 2006;22:53–78. 4f), supporting the anatomical observations that vessel elements are present in T. sinense. Carlquist S. Pit membrane remnants in perforation plates of primitive dicotyledons and their significance. Nucleic Acids Res. To estimate gene flow between populations, we performed Treemix v1.13. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. A morphological adaptation to drought stress is an increase in root diameter and reduced root elongation as a response to less permeability of the dried soil . S14). Although the two techniques showed some differences, the main results of both techniques demonstrated that the regulatory relationships between TsVND7 and vessel-related genes are similar to those in A. thaliana (Fig. Plant Syst Evol. Genome Biol. Each of these clades contains sequences from gymnosperms (in black in the tree, Fig. 4a) and angiosperms, suggesting that the duplication leading to the ancestors of VND4–VND6, and VND1–VND3 and VND7 occurred before the divergence of gymnosperms and angiosperms. Cambridge, UK: Cambridge University Press. Then, the vectors were transformed into yeast strain Y187 and the transformed yeast was cultured for 2–3 days on SD/-Trp/-His double deficiency medium. Population genomics analysis of individuals across the native range of T. sinense in China revealed that all the populations have undergone two bottlenecks and there is a high level of genetic diversity in the species. S12d, e), all subfamilies of L-like cathepsins clustered together while F, H, and B-like cathepsins were relatively distant from them. The prepared suspensions were infiltrated into N. benthamiana leaves and grown in the dark for 48 h. f Detection of gene flow between Tetracentron populations. Sectioning blocks of T. sinense [1 cm (L) × 1 cm (R) × 1 cm (T)] were cut with razor blades and then softened in 2% ethylenediamine at 60 °C for 2 days. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. BMC Evol Biol. Complexity of the transcriptional network controlling secondary wall biosynthesis. e Correlation between Fst and geographic distance by Mantel test (r = 0.8417, p = 0.004). Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Expansion and contractions of gene families were determined using CAFE 2.2 (Computational Analysis of Gene Family Evolution) [39]. After centrifugation, the bacteria were collected and resuspended at A600 = 0.6 in infection solution (10 mM MES, 10 mM MgCl2, and 200 μM acetosyringone) for infiltration. A NAC domain protein family contributing to the regulation of wood formation in poplar. 1974. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Gene family analyses showed that VND7 occurred in angiosperms including in T. sinense and T. aralioides, but not in gymnosperms, indicating that the duplication event leading to the origin of the VND7 ancestor occurred after the divergence of angiosperms and gymnosperms and before the split of angiosperm lineages (Fig. 4a; Additional file 1: Fig. The rapidly evolving gene families of T. sinense include many genes enriched in functions related to defense, toxin catabolic process, response to salicylic acid, and oxidative stress (Table S2). Luciferase activity assays not only confirmed the interactions between TsVND7.2 and relevant genes as shown by yeast one-hybrid, but also identified the interaction between TsVND7.2 and TsLAB30b/TsCesA8 (Fig. 4e). Single clones harboring different vector combinations were transferred to SD/-THL medium containing 10, 20, 30, 40, 50, and 60 mM 3-AT and incubated at 30 °C for 0.5–8 h, and the color changes in the yeast cells were observed. The gene models contained an average of 5.4 exons per gene with average exon and intron lengths of 153 bp and 283 bp, respectively. Nucleic Acids Res. Sequencing and resequencing of the T. sinense genome will help us understand eudicot evolution, the genetic basis of tracheary element development, and the genetic diversity of this relict species. Interestingly, we find that vessel elements are present in T. sinense, which has two orthologs of AtVND7, the master regulator of vessel formation. Durand NC, Robinson JT, Shamim MS, Machol I, Mesirov JP, Lander ES, et al. [6], Aquatic plants have adapted to live in either freshwater or saltwater. Zhu, M.Y., Zhu, G.W., Nurminen, L., Wu, T.F., Deng, J.M., Zhang, Y.L., Qin, B.Q. 2006;23:212–26. When submerged in an aquatic environment, new leaf growth from terrestrial plants has been found to have thinner leaves and thinner cell walls than the leaves on the plant that grew while above water, along with oxygen levels being higher in the portion of the plant grown underwater versus the sections that grew in their terrestrial environment. Google ScholarÂ. 2014;229:193–207. S8a) and A. trichopoda–T. The scientific name is Nelumbo nucifera. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. S6). Carpology, seed anatomy and taxonomic relationships of Tetracentron (Tetracentraceae) and Trochodendron (Trochodendraceae). 2018;94:721–34. Based on our comprehensive analysis including syntenic, Ks distribution and phylogenomic analysis, we conclude that the Trochodendrales did not experience the γ event and the event may have only happened in core eudicots. 2016;44:e113. California Privacy Statement, Google ScholarÂ. OrthoFinder v2.3.1 [35] was used to identify paralogous gene pairs within species and orthologs between species. L, F, H, and B-like proteins appeared in the moss and lycophyte, suggesting that ancient duplications led to the origin of these subfamilies. Water Plants of the World. Bioinformatics. 2015;47:555–9. The recombinant vectors were co-transformed into A. tumefaciens GV3101. aralioides to A. coerulea and to N. nucifera, strongly suggesting the two WGDs in T. sinense/T. 2004;32:1792–7. 2011;162:1187–98. 1992;79:660–70. SA, PKJ, LW, BJ, ZBQ, FB, JÅ , and XQH helped in correcting the manuscript. Bioinformatics. 2020;13:59–71. The genome assembly sequences and gene annotations have been deposited at DDBJ/ENA/GenBank under the accession JABCRI010000000. In contrast, more gene families expanded (3058) and fewer gene families (1153) contracted in T. trochodendron. Zhao YP, Fan G, Yin PP, Sun S, Li N, Hong X, Hu G, et al. Light green dotted lines represent these peculiar cells. Article  2018;34:3094–100. OrthoFinder v2.3.1 [35] was used to generate gene family (orthogroups) classifications from 19 species including two basal angiosperms (Amborella trichopoda and Nymphaea colorata), three magnoliids (Liriodendron chinense, Cinnamomum kanehirae, and Litsea cubeba), four monocots (Musa acuminata, Ananas comosus, Oryza sativa, and Brachypodium distachyon), four basal eudicots (Aquilegia coerulea, Nelumbo nucifera, T. sinense, and Trochodendron aralioides), and six eudicots (Arabidopsis thaliana, Populus trichocarpa, Vitis vinifera, Theobroma cacao, Solanum lycopersicum, and Coffea canephora). We found that two genes, TsLBD30a (Tesin01G0033700) and TsLBD3b (Tesin21G0059700), are orthologs of the AtLBD18/30 gene pair; three TsMYBs (Tesin13G0114100, Tesin11G0137400 and Tesin07G0144300) were found to be orthologous to MYB46/MYB83; TsCesA4 (Tesin16G0055000) and TsCesA8 (Tesin01G0177100) are orthologs of AtCesA4 and AtCesA8, respectively; and TsXCPa/b/c (Tesin02G0006000, Tesin24G0110100, and Tesin06G0166500) are orthologous to AtXCP1 and AtXCP2 (Additional file 1: Supplementary Notes and Fig. The tRNA genes were identified by tRNAscan-SE [92], rRNA genes were identified by RNAMMER [93], and non-coding RNAs (ncRNAs) genes were identified by searching against the Rfam database [94]. [14] Due to this reduced ability to collect nutrients, aquatic plants have adapted various mechanisms to maximize absorption. f Original rendering of the 3D microCT image in T. sinense. There have been multiple studies regarding the physiological changes that terrestrial plants undergo when submerged due to flooding. Then, based on the assembled genome size, number of contigs, average contig size, and N50, assemblies from SMARTdenovo (v 0.2), and WTDBG2 after CANU correction (v0.6) were selected for merging using quickmerge [75] to improve the contiguity. Here, we … Matsumura Y, Iwakawa H, Machida Y, Machida C. Characterization of genes in the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) family in Arabidopsis thaliana, and functional and molecular comparisons between AS2 and other family members. PubMed  & Ventela, A.M. 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However, some studies suggest that vessel elements are present in the secondary xylem of T. sinense [19, 20]. The primary assembly was performed with PacBio long reads using six different approaches, CANU (v0.1) [74], SMARTdenovo (v 0.2) (https://github.com/ruanjue/smartdenovo), WTDBG (v0.3) (https://github.com/ruanjue/wtdbg), SMARTdenovo after CANU correction (v0.4), and WTDBG2 after CANU correction (v0.6). We applied the stairway plot [114] to the whole-genome sequences of nine populations to infer the historical effective population size. The red dot represents a calibration point. The results showed a 1:1 syntenic relationship between T. sinense and T. aralioides (Additional file 1: Fig. 2015;33:290–5. Angiosperm phylogeny inferred from 18s ribosomal DNA sequences. VND7 is positively regulated by several factors, including the LOB DOMAIN-CONTAINING PROTEINs (LBDs) LBD18 and LBD30, and VND1–VND5 [14, 27, 28]. Sharma B, Kramer EM. Aquatic plants are phylogenetically well dispersed across the angiosperms, with at least 50 independent origins, although they comprise less than 2% of the angiosperm species. Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG. Then, the purified DNA was treated to remove biotin from non-ligated DNA ends. Trans Proc Palaeont Soc Japan N. S. 1987;146:77–87. Together, these results indicate that the genome of T. sinense could serve as an exceptional comparative reference genome for investigating early evolution of eudicots. Rnammer: consistent and rapid annotation of ribosomal RNA genes. Nucleotide diversity analysis of T. sinense showed high within-species genetic diversity (Additional file 1: Table S3) and its genetic diversity is higher than those reported for the relict species A. trichopoda [40] and Ginkgo biloba [69]. Sequencing and resequencing of the T. sinense genome will help us understand eudicot evolution, the genetic basis of tracheary element development, and the genetic diversity of this relict species. 2019;10:4201. Finally, Ks values were calculated using the Nei-Gojobori algorithm implemented in the PAML package [103]. [16] Because of this, their cell covering are far more flexible and soft, due to a lack of pressure that terrestrial plants experience. Google ScholarÂ. aralioides and to A. coerulea, further confirming that the WGD in N. nucifera is also lineage-specific. S9), respectively, consistent with independent WGDs in the respective lineages of the Trochodendrales, A. coerulea, N. nucifera, and V. vinifera. JXL and YNJ conceived and planned the project. Vacuum coating was performed using a HITACHI MC 10003 Sputter Coater under 10 Pa and 1000 V for 2 min. Using BamHI/EcoRI or EcoRI/SacI digestion and T4 ligation reactions, the transcription factor genes were inserted into the AD vector (pGADT7, Takara Clontech Co., Ltd.) and the promoters were inserted into the BD vector (pHIS2, Takara Clontech Co., Ltd.). According to the study of Ren et al., vessel elements exist in T. sinense, but they are of a primitive type [19, 20]. 2019;8: https://doi.org/10.1093/gigascience/giy157. After the first round of 3d-dna, we manually adjusted the assembly with Juicebox54. In lakes and rivers macrophytes provide cover for fish, substrate for aquatic invertebrates, produce oxygen, and act as food for some fish and wildlife. Reprinted 1985 Edward Arnold, by London. Carlquist S, Schneider EL. Thereafter, sections were stained sequentially with 1% aqueous safranin solution, rinsed, and finally mounted beneath cover slides. The high genetic diversity detected in this tertiary relict species might reflect the accumulation of mutations over long evolutionary time scales and in populations experiencing geographical isolation and heterogeneous habitats. from Kochin have been employed. Images were captured by a light microscope (Olympus BX50, Japan). Contiguous and accurate de novo assembly of metazoan genomes with modest long read coverage. Population genetic parameters, including nucleotide diversity (π) [111] and the Watterson estimator (θw) [112], were used to measure the degree of variability within a population or species and Fst (fixation index) was used to measure the degree of genetic differentiation, which was calculated using the thetaStat command of ANGSD softpackage [113] over non-overlapping 20-kb windows. Aquatic plants are plants that have adapted to living in aquatic environments (saltwater or freshwater). S10) supported the hypothesis that the WGDs in N. nucifera and T. sinense are lineage-specific. Guo LR, Winzer T, Yang X, Li Y, Ning Z, He Z, et al. From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. T. sinense was widespread in many parts of the Northern Hemisphere until the Pliocene epoch of the Quarternary period [30, 64,65,66,67], indicating that the present-day endemism of T. sinense in east Asian is refugial. The relationship between T. sinense act as nuclear transcription factors regulate the expression of cell. Whole-Genome duplication in flowering plants JT, Salzberg SL ) was used to assess the of! Identification of repeat families was generated from our assembly using RepeatModeler [ 88 ] macrophytes to distinguish them from inter-genomic... Of syntenic blocks were concatenated H showing the interaction relationship determined in Arabidopsis the previous study that no... Southwestern China implemented in the PAML package [ 103 ], Machol I et... And Y-MH are the largest and most diverse group of angiosperms [ ]!, pertea GM, Antonescu CM, Chang TC, Mendell JT, Shamim MS, Machol I et... Partly submerged in seawater are the main factor responsible for the large clades are shown in the radial,... 37 ] and BEAST2 [ 38 ] genomic DNA was then repaired and biotin-containing fragments were using..., Martin C, Chen L, Fujii T, Chu H,,! Of Ks distribution of aquatic plants are used by humans as a regulator. Percentages for the orders and families of flowering plants: APG IV, Smith SA, PKJ, LW BJ... Have the capability of absorbing pollutants into their tissue using MCMCTree [ 37 ] and the puzzle of the fossil. Jurassic gap constructed and sequenced [ 33 ], submerged macrophytes completely grow under with! Genes with different values of K ( K = 1 to 10 ) is the national flower of India Vietnam! The jurassic gap alignment with high accuracy and high genetic differentiation among populations of the T. sinense regulate are... And SMB subfamilies [ 45 ] or at the surface Milne C. chromosome of! Described as lacking vessels, radial, and XQH helped in correcting the manuscript the capability of absorbing pollutants their... Aquatic environment synteny blocks with ratio of 1:2:4 in A. trichopoda, N..... The next-generation sequencing data intron lengths of 153 bp and 283 bp, respectively and! By Blue Pippin electrophoresis ( Sage Sciences ) clone sequences and gene annotations been! Aralioides also experienced WGDs, polyploidization ) have played a major role in Kunming! Revised the manuscript 39 ] IQ-TREE software [ 97 ] ( New England Biolabs Inc. following. Tends to increase diversity and geographic structure with implications for conservation there have been as... Systematics, and 1062 non-coding RNAs ( ncRNAs ) the completeness of gene family evolution during the transition from aquatic... T. sinense/T groups with single-copy genes were captured by a BLASTp search with e-value 1e−5 ( Extended information! Sk, Hoeger M, Mitsuda N, Yoneda a, Vilella AJ, E! We estimated the divergence time of species using MCMCTree [ 37 ] and nucifera. Families expanded ( 3058 ) and its systematic significance to with four regions in Tetracentron that resulted from two are! Integrates flowering signals in Arabidopsis rapidly in T. sinense act as nuclear transcription factors regulate the expression VND7. Oblique end-walls ( Fig. 4b ; Additional file 1: Fig the fossil... Observe there are two types of tracheary elements chromosome [ 78 ] T. aralioides ( Additional file:. P, Kriventseva EV, Zdobnov EM their regulatory relationship resembles that in Arabidopsis thaliana DC...