High-Quality de novo Genome Assembly of Huajingxian 74, a Receptor Parent of Single Segment Substitution Lines

Li Fangping, Gao Yanhao, Wu Bingqi, Cai Qingpei, Zhan Pengling, Yang Weifeng, Shi Wanxuan, Li Xiaohua, Yang Zifeng, Tan Quanya, Luan Xin, Zhang Guiquan,Wang Shaokui

Letter

High-QualityGenome Assembly of Huajingxian 74, a Receptor Parent of Single Segment Substitution Lines

Li Fangping, Gao Yanhao, Wu Bingqi, Cai Qingpei, Zhan Pengling, Yang Weifeng, Shi Wanxuan, Li Xiaohua, Yang Zifeng, Tan Quanya, Luan Xin, Zhang Guiquan,Wang Shaokui

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Rice (L.) is grown nearly worldwide and provides the staple food for more than half of the global population (Luo et al, 2017). The genomes of several cultivated rice varieties including Nipponbare (NPB)(Kawahara et al, 2013; Sakai et al, 2013), IR64 (Tanaka et al, 2020), 93-11 (Zhang et al, 2018) and R498 (Du et al, 2017) at chromosome level, and Minghui 63 and Zhenshan 97 (Zhang et al, 2016) at scaffold level have been assembled,annotated and released, among which the R498 and NPB genomes are widely used as reference genomes in rice research. However, there are thousands of rice cultivars, landraces and wild rice varieties in the world with dramatically different genetic backgrounds, and the genomes of native rice varieties in South China, which is one of the major rice production areas in China, have not beenassembled. Huajingxian 74 (HJX74) is anrice variety bred in South China Agricultural University, Guangdong Province with widely environmental adaptability and high yield (www.ricedata.cn/ variety/varis/602548.htm). HJX74 exhibits significant phenotypic and genetic differences from those varieties whose whole genomes have been properly sequenced and assembled (Fig. 1).

In the past 30 years, a large library of single segment substitution lines (SSSLs) has been constructed using HJX74 as the receptor plant and 43 accessions that belong to 7 species of rice AA genome as donors. Hence, all these SSSLs are in the same genetic background (Zhang, 2019). The SSSL library has made a great contribution to the identification of QTLs/genes involved in disease resistance, fertility, panicle length, stress resistance, grain shape determination and so on (Wang S K et al, 2015; Fang et al, 2019; Wang et al, 2019). In addition, the SSSL library has provided a powerful platform for rice breeding by design (Luan et al, 2019; Zhao et al, 2019). The construction of a high-quality genome of the receptor parent (HJX74) of the SSSL library is therefore essential for improving the efficiency of rice genetic and mechanism studies for desirable agronomic traits, as well as accelerating the processof rice breeding by design. We produced a high-precision HJX74chromosomal genome by performingwhole-genome sequencing in the PacBio platform (Rhoads and Au, 2015), followed by the Hi-C-assisted assembly mount technology(van Berkum et al, 2010). The corresponding online platform has been constructed as well (https://RiceGenomicHJX.xiaomy.net). The sequence andassembly of the HJX74 genome will significantly enrich the understanding of rice genome and provide a powerful tool for rice studies.

A total of 7 380 677 reads (137.31 Gb) of the HJX74 genome sequences were produced by PacBio SeqⅡ (Fig. 2-A and -B), and 51.23 Gb and 40.93 Gb of the sequence data were generated by common and Hi-C library preparation illumina sequencing, respectively. The overlapped group files (contig) consisting of 155 fasta format sequences with the size of 399.00 Mb (N50 = 14.41 Mb) (Table S1) were produced after being assembled and polished.

Visualization of the Hi-C signals indicated that 12 square matrix areas in the Hi-C heat map displayed significant differences from the background signal corresponding to the chromosome number of the rice nuclear genome (Fig. S1). The final polished scaffold genome was constructed by the Hi-C data and the consensus sequence file spanned 398.87 Mb, and there were 108 contigs for HJX74 including 12 chromosome lengthscontigs (Fig. 2-D and Table S1). The genome assemblies recovered more than 98% of the 1 440 Benchmarking Universal single- copy orthologs (BUSCO) embryophyte genes and completely assembled more than 92.5% of the 248 embryophyte core genes from the Core Eukaryotic Genes Mapping Approach (CEGMA) database (Li et al, 2020) (Table S2). Long terminal repeat-retotransposons (LTR-RTs) assembly index (LAI) of the HJX74 genome was calculated to be 23.42, which is close to the high-quality rice genome of NPB (22.59) and R498 (23.94) (Table S3).

本组患者采取手术治疗。根据诊疗结果,选择适当的手术治疗方式,本组患者所采用的手术方法有:肠粘连松解术、乙状结肠切除术、结肠切除术、降结肠造口、小肠部分切除术、嵌顿性疝复位+修补术等。

Combining ab initio, protein and expressed sequence tag (EST) evidences with consensus gene prediction (Zhang et al, 2015), we annotated the HJX74 genome with 46 993 non-redundant genes. Among them, 39 002 genes (83.0%) form 27 202 clusters with genes from 11 otherspecies, whereas 7 991 genes present singletons in the OrthoVenn2 (Wang Y et al, 2015). The clustering analysis based on Markov Clustering (MCL) algorithm indicates high annotation reliability. Totally2 850 single-copy gene clusters were generated by the orthologous cluster analysis of direct homology in 9varieties,,andon the platform OthoVenn2 (Table S4). The phylogenetic tree constructed by using the coding region nucleic acid sequence of 2 850 single- copy lineal homologous gene clusters indicated that HJX74 was clustered in the clade ofsubspand hadthe closest genetic relationship with IR64 (Fig. 1-B and Table S5). HJX74 was genetically far from NPB and R498, even HJX74 and R498 were clustered within therice clade, which is consistent with the SNPs, InDels and persence and absence variations (PAVs) across the 12 chromosomes in HJX74 compared to NPB and R498 (Fig. 2-A and -B; Fig. S2 and Tables S6 and S7). In addition, more genes were presented in HJX74/ R498 at a peak of 0.4–0.5 than HJX74/NPB from the density curve of(Kryazhimskiy and Plotkin, 2008), which suggested more genes in HJX74 were positively selected when compared with R498 than the comparation with NPB (Fig. 2-C). The reason for this phenomenon is possiblydue to the crossbreeding between rice subspecies (and) during the HJX74 breeding process and preference toas germplasm resources for rice breeding in South China.

Fig. 1. Phenotype (A) and phylogeney (B) of HJX74 (Huajingxian 74).

Phylogenetic tree constructed by the maximum- likelihood method using coding sequences of single copy lineal homologous genes (the genes were showed in Table S4). Totally 12 species or varieties were used for alignment, 9 of them are cultivated rice (Nipponbare, 93-11, R498, Zhenshan 97, IR64, Minghui 63, Basmati, DomSuid and HJX74) and the other 3 are wild rice (,and).

Fig. 2. Characteristics of Huajingxian 74 (HJX74) genome and synteny examining, SNPs (single nucleotidepolymorphisms) and InDels (Inserts/Deletes) mining,/comparison with Nipponbare (NPB) and R498.

A, Distribution of SNPs and InDels between HJX74 and NPB (the data refer to Table S5).

B, Distribution of SNPs and InDels between HJX74 and R498 (the data refer to Table S6).

C,/distribution of different combinations. The verticallines represent average values of/.

D, Chromosomal synteny among HJX74 and two reference genomes of rice.

E, Interactive dot plot between HJX74 and NPB.

F, Interactive dot plot between HJX74 and R498.

G, Characteristics of the HJX74 genome. Tracks from outside to inside are the 12 chromosomes of HJX74, GC content, long terminal repeat density, and simple sequence repeat density (the data refer to Table S11).

The relative lengths of HJX74 chromosomes are consistent with NPB and R498 (Table S3). According to the whole- genome comparison, the genome of HJX74, at the position of about 12–17 Mb on chromosome 6, showed a sequence inversion with a length of about 5 Mb compared with the NPB genome, while the HJX74 sequence was in the same order as R498 (Fig. S3). Besides, the HJX74 genome was nearly 8.1 Mb and 25.2 Mb larger than R498 (390.9 Mb) and NPB (373.8 Mb), respectively. We performed a whole-genome comparison to examine the synteny between the HJX74 and R498/NPB genomes using the python version program MCScanX (Wang et al, 2012). HJX74 showed a high degree of synteny and the same large inversion in the middle of chromosome 6 with/genomes, which was consistent with the whole-genome alignment between the HJX74 and R498/NPB genomes(Fig. 2-D to -F and Fig. S3). This phenomenon or the disorderedalignment to NPB in the same locus was also respectively detected in the genomes of, Basmati 334 and DomSufid (Choi et al, 2020; Xie et al, 2020). This long fragment staining inversion phenomenon existed in this site indeed, which suggested that the inversion might have been occurred during the process of rice subspecies differentiation. There is a about 3 Mb large-scale syntenic block between the short arms of chromosomes 11 and 12 according to the synteny plot, which was estimated to result from a duplication event 7.7 million years ago and was consistent with previous research (The Rice Chromosomes 11 and 12 Sequencing Consortia, 2005).

There are a considerable number of PAVs between the genomes of HJX74 and NPB (Table S8 and Fig. S2-B). Comparedwith NPB, the HJX74 genome has more long-fragment insertion sequences and repeated fragment expansions (Fig. S2-B). Three NPB chromosomes (NPB-Chr.02, NPB-Chr.03 and NPB-Chr.10) with the greatest difference from HJX74 were compared. The long-term insertions (> 10 kb) and tandem/repeats contributed significantly to the longer chromosome length of HJX74 compared to NPB (Fig. S4-A to -C). This result tallies with the previous report that the chromosome length difference was most probably due to the changes in tandem/repeat regions (Kim et al, 2017). In contrast, the length of each chromosome of HJX74 was close to that of R498 with an average length difference about 0.075 Mb (Table S9).

Then, we found that the LTR-RT length and type ratio (Gypsy/ Copia/unknown) of the HJX74 genome were similar to those of R498, but significantly different from those of NPB (Table S10). Previous research reported that the two subspecies of rice,and, have experienced independent amplification or loss of LTR-RTs after the divergence (Du et al, 2017). In this study, the chromosome structure comparison showed fewer differences in PAVs and LTR-RTs between twovarieties HJX74 and R498, but their PAVs and LTR-RTs were very different from those of NPB. Meanwhile, a total of 26 647 simple sequence repeat loci, with the number of repeating units ≥ 3 bp, were detected in 12 chromosomes of HJX74 (Fig. 2-G and Table S11), which demonstrated the promising application of the HJX74 genome in the development of molecular breeding markers.

To encourage the use of the genome of HJX74 and other rice varieties, a platform (https://RiceGenomicHJX.xiaomy.net) supporting sequence search (Blast), gene browse, download and extraction were built with the support from the Guangdong Provincial Key Laboratory of Plant Molecular Breeding, China. The platform also collects information about the mutation sites in HJX74 and other rice genomes, and multiple rice research platforms and websites. Further improvement and development of the platform is underway to optimize its application (Fig. S5).

由表2可知，试验组小鼠十二指肠绒毛长度与对照组相比分别提高11.31%和8.84%(P＜0.05)，试验组小鼠十二指肠绒毛长度/隐窝深度与对照组相比分别提高18.32%和14.66%(P＜0.05)，试验组隐窝深度与对照组相比差异不显著(P＞0.05)，但有降低趋势。试验组之间的小鼠十二指肠绒毛长度、隐窝深度及V/C均差异不显著(P＞0.05)。综上所述，预消化蛋白可以显著提高小鼠十二指肠绒毛长度和绒毛长度/隐窝深度比值(P＜0.05)，有降低隐窝深度的趋势(P＞0.05)。

In previous studies, considerable progress has been made by combining bioinformatics and whole genome sequencing methods (such as RNA-seq and genome-wide association study) with traditional molecular biology methods for germplasm resource mining and molecular breeding in rice (Shao et al, 2019; Groen et al, 2020). However, these technologies require a reliable reference genome. Here, we presented a highly contiguous and near-complete genome assembly for HJX74, a high-yieldingrice variety widely-grown in South China. As a platform variety, HJX74 has been implemented to construct a large SSSL library with 2 360 independent lines (Zhang, 2019). The SSSL library has an excellent application prospect in rice breeding by design and QTL/gene identifications (Zhou et al, 2017). Compared with NPB, the utilization of the HJX74 reference genome is able to detect more SNP loci or insertion/deletion sites in many PAVs while combining with whole genome sequencing technologies (Fig. S6). Our work provides a precise reference genome and an accessible utilization platform for further research based on the SSSL library. There is no doubt that this reference genome of the receptor parent of the SSSL library will contribute to simplifying the mining and identification processes of rice functional genes controlling agronomic traits of interest, thereby promoting the research and application of rice breeding by design.

AcknowledgEments

This study was supported by the National Key Research and Development Program of China (Grant No. 2016YFD0100406), National College Students Innovation and Entrepreneurship Foundation of China (Grant No. 201910564054), National Natural Science Foundation of China (Grant Nos. 91735304 and 31622041) and Special Project for Leading Talents in Innovation of Science and Technology of Guangdong Province, China (Grant No. 2016TX03N224). We thank Ji Zhe (Department of Plant Sciences, University of Oxford) for suggestions.

Supplemental DatA

这种“以写促读”策略中的“写作”，是为了帮助学生有效提取、梳理、概括文本信息，厘清文章脉络，并掌握相应的阅读策略。阅读和写作的结合点在于对文本信息的归类整理和思路脉络的梳理。在教学中，可以采用画结构图、画线索图、列提纲、做表格等形式。

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Fig. S1. Hi-C interactive heat map.

Fig. S2. Cumulative sequence length and presence and absence variation distribution.

Fig. S3. Interactive dot plot of Huajingxian 74 and two reference rice genomes (R498 and Nipponbare).

因此，在深圳境内，选择留仙洞以南的所有车站及上屋北站、光明城站和公明广场站作为快车停靠点；在东莞境内，选择华为站、大朗西站(与东莞1号线和赣深铁路换乘)及松山湖北站(终点站)作为快车停靠点。13号线快慢车的停站方案如图2所示。

Fig. S4. Presence and absence variations types and distribution of some chromosomes with significantly different lengths between Huajingxian 74 and Nipponbare.

Fig. S5. Online platform of Huajingxian 74 genome data.

Fig. S6. Sequence difference in presence and absence variation locus.

Table S1. Comparison of contigs and scaffolds among Huajingxian 74 and two reference rice genomes.

Table S2. Evaluation of Huajingxian 74 genome assembly by Benchmarking Universal single-copy ortholog and Core Eukaryotic Genes Mapping Approach.

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Table S4. Clustering of homologous genes of 12 species of rice.

Table S5. Single copy homologous genes of 12species.

Table S6. Mutation site of Huajingxian 74 compared with Nipponbare.

今年4月，云南税务部门深化税务、银行信息互通，将“银税互动”从“线下”拓展了“线上”，推出“云税贷”“税易贷”等产品，基于小企业纳税信息，运用大数据分析，采取线上自助操作的纯信用短期流动资金贷款产品，从申请到贷款到账只需要几分钟的时间，高效、快速解决企业融资难题。

Table S7. Mutation site of Huajingxian 74 compared with R498.

Table S8. Presence and absence variations length distribution.

（三）运用多媒体多维的展现文章内容。传统的教学，不能够将声音、文章、图片、影像、动画等各类信息有机的结合在一起，而多媒体新式教育的方式就打破了纯铜教学并能够弥补传统教学的不足，更加形象，直观的展现信息，多维展现课文内容。

Table S9. Chromosome lengths of Huajingxian 74, Nipponbare and R498.

Table S10. Long terminal repeat-retotransposons in Huajingxian 74, R498 and Nipponbare.

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Table S11. Detection of simple sequence repeat locus on Huajingxian 74 genome.

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式中：Y为可溶性膳食纤维得率；X 1，X2，X3，X4 分别为料液比、碱液浓度、提取温度、提取时间4个自变量的编码值。

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Table S3. Long terminal repeat-retotransposons assembly index of R498, Nipponbare, 93-11 and Huajingxian 74.

故意杀人罪在主观方面必须存在剥夺他人生命的故意。因为艾滋病的严重性，在认定故意传播艾滋病的行为人的主观故意方面时，很难排除剥夺他人生命的故意，即行为人明知自己的行为会发生致人死亡的危害结果，并希望或放任这种结果的发生。因此如果将故意传播艾滋病认定为故意杀人罪，那么传播者在主观上应该具备杀人的故意，因此将没有杀人故意的情况排除在外。

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File S1. Methods.

(1)满载紧急制动减速：输送机在紧急制动过程中各处的胶带张力均应大于零，严防胶带松弛、撒煤或叠带事故。F1= 484.15 kN，F2= 285.2 kN ，F3=156 kN；

加氢进料泵联锁逻辑如图2所示，主要联锁内容包括：停液力透平联锁，用于防止液力透平转速超高或热高分液位抽空引起高压串低压；分别停主/备泵联锁，用于保护泵不发生喘振或其他泵体自身异常对泵造成的损坏；切断泵出口总管联锁，用于保护装置进料量不低于装置最小处理负荷量和避免泵出口总管发生流量倒流造成的高压反串低压。

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北京奇步自动化控制设备有限公司是一家自动化工程公司，以工业现场自动化总线工程为发展方向，以“客户创造价值”为宗旨，立志做自动化领域一流企业。公司专业从事自动化生产线系统集成、液压（或气动）工装夹具、物流线、自动化精密元件、专业设备的技术研发、生产制造和销售服务。公司严格执行国际行业标准，认真践行ISO9001质量体系标准和要求，以高质量、标准化的产品以及完善的售后服务，赢得口碑，树立品牌。

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11 August 2020;

18 September 2020

Copyright © 2021, China National Rice Research Institute. Hosting by Elsevier B V

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Peer review under responsibility of China National Rice Research Institute

http://dx.doi.org/10.1016/j.rsci.2020.09.010

Wang Shaokui (shaokuiwang@scau.edu.cn)