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).

本組患者采取手術(shù)治療。根據(jù)診療結(jié)果,選擇適當(dāng)?shù)氖中g(shù)治療方式,本組患者所采用的手術(shù)方法有:腸粘連松解術(shù)、乙狀結(jié)腸切除術(shù)、結(jié)腸切除術(shù)、降結(jié)腸造口、小腸部分切除術(shù)、嵌頓性疝復(fù)位+修補(bǔ)術(shù)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，試驗(yàn)組小鼠十二指腸絨毛長(zhǎng)度與對(duì)照組相比分別提高11.31%和8.84%(P＜0.05)，試驗(yàn)組小鼠十二指腸絨毛長(zhǎng)度/隱窩深度與對(duì)照組相比分別提高18.32%和14.66%(P＜0.05)，試驗(yàn)組隱窩深度與對(duì)照組相比差異不顯著(P＞0.05)，但有降低趨勢(shì)。試驗(yàn)組之間的小鼠十二指腸絨毛長(zhǎng)度、隱窩深度及V/C均差異不顯著(P＞0.05)。綜上所述，預(yù)消化蛋白可以顯著提高小鼠十二指腸絨毛長(zhǎng)度和絨毛長(zhǎng)度/隱窩深度比值(P＜0.05)，有降低隱窩深度的趨勢(shì)(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

這種“以寫促讀”策略中的“寫作”，是為了幫助學(xué)生有效提取、梳理、概括文本信息，厘清文章脈絡(luò)，并掌握相應(yīng)的閱讀策略。閱讀和寫作的結(jié)合點(diǎn)在于對(duì)文本信息的歸類整理和思路脈絡(luò)的梳理。在教學(xué)中，可以采用畫結(jié)構(gòu)圖、畫線索圖、列提綱、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，在深圳境內(nèi)，選擇留仙洞以南的所有車站及上屋北站、光明城站和公明廣場(chǎng)站作為快車?？奎c(diǎn)；在東莞境內(nèi)，選擇華為站、大朗西站(與東莞1號(hào)線和贛深鐵路換乘)及松山湖北站(終點(diǎn)站)作為快車停靠點(diǎn)。13號(hào)線快慢車的停站方案如圖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，云南稅務(wù)部門深化稅務(wù)、銀行信息互通，將“銀稅互動(dòng)”從“線下”拓展了“線上”，推出“云稅貸”“稅易貸”等產(chǎn)品，基于小企業(yè)納稅信息，運(yùn)用大數(shù)據(jù)分析，采取線上自助操作的純信用短期流動(dòng)資金貸款產(chǎn)品，從申請(qǐng)到貸款到賬只需要幾分鐘的時(shí)間，高效、快速解決企業(yè)融資難題。

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

Table S8. Presence and absence variations length distribution.

（三）運(yùn)用多媒體多維的展現(xiàn)文章內(nèi)容。傳統(tǒng)的教學(xué)，不能夠?qū)⒙曇?、文章、圖片、影像、動(dòng)畫等各類信息有機(jī)的結(jié)合在一起，而多媒體新式教育的方式就打破了純銅教學(xué)并能夠彌補(bǔ)傳統(tǒng)教學(xué)的不足，更加形象，直觀的展現(xiàn)信息，多維展現(xiàn)課文內(nèi)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為可溶性膳食纖維得率；X 1，X2，X3，X4 分別為料液比、堿液濃度、提取溫度、提取時(shí)間4個(gè)自變量的編碼值。

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

故意殺人罪在主觀方面必須存在剝奪他人生命的故意。因?yàn)榘滩〉膰?yán)重性，在認(rèn)定故意傳播艾滋病的行為人的主觀故意方面時(shí)，很難排除剝奪他人生命的故意，即行為人明知自己的行為會(huì)發(fā)生致人死亡的危害結(jié)果，并希望或放任這種結(jié)果的發(fā)生。因此如果將故意傳播艾滋病認(rèn)定為故意殺人罪，那么傳播者在主觀上應(yīng)該具備殺人的故意，因此將沒(méi)有殺人故意的情況排除在外。

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尤其是在提倡和諧社會(huì)的今天，供電企業(yè)的營(yíng)銷服務(wù)質(zhì)量顯得尤為重要。好的營(yíng)銷服務(wù)不僅能保證客戶的安全可靠用電，還能提升企業(yè)形象，提高企業(yè)經(jīng)濟(jì)效益，有利于企業(yè)的未來(lái)發(fā)展?，F(xiàn)代供電企業(yè)必須轉(zhuǎn)變思想，放棄傳統(tǒng)的墨守成規(guī)，不斷學(xué)習(xí)新時(shí)期的先進(jìn)理念，開(kāi)拓思路，勇于創(chuàng)新，以優(yōu)質(zhì)服務(wù)為企業(yè)發(fā)展之根本。在以人為本的基礎(chǔ)上，加強(qiáng)企業(yè)員工營(yíng)銷服務(wù)理論知識(shí)學(xué)習(xí)，完善各項(xiàng)風(fēng)險(xiǎn)管控措施，爭(zhēng)取把供電營(yíng)銷服務(wù)提升至一個(gè)新水平，增強(qiáng)供電企業(yè)在市場(chǎng)中的競(jìng)爭(zhēng)力。

File S1. Methods.

(1)滿載緊急制動(dòng)減速：輸送機(jī)在緊急制動(dòng)過(guò)程中各處的膠帶張力均應(yīng)大于零，嚴(yán)防膠帶松弛、撒煤或疊帶事故。F1= 484.15 kN，F(xiàn)2= 285.2 kN ，F(xiàn)3=156 kN；

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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)