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2022 , Vol. 43 >Issue 8: 1545 - 1553

DOI: https://doi.org/10.3969/j.issn.1000-2561.2022.08.003

Omics & Biotechnology

Assembly and Sequence Analysis of Chloroplast Genome of Amygdalus persica

  • GONG Yihui ,
  • ZHOU Guihua ,
  • LI Limei ,
  • ZENG Yongxian ,
  • CHEN Zhiyin , *
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  • School of Agriculture & Biotechnology, Hunan University of Humanities, Science and Technology, Loudi, Hunan 417000, China
*CHEN Zhiyin,E-mail： 。

Received date: 2022-01-18

  Revised date: 2022-02-23

  Online published: 2022-09-09

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Abstract

In this study, the complete chloroplast genome of Amygdalus persica L. ‘Jinxiu' was assembled and sequenced. Illumina NovaSeq 6000 platform was used to sequence DNA of A. persica L. ‘Jinxiu', and the chloroplast genome was assembled and annotated by SPAdes v3.10.1. We used the chloroplast genome of Prunus persica as the reference, the feature analysis and phylogenetic analysis study were investigated, laying a foundation for the further development of the genetics and identification of A. persica. The total length of the complete A. persica L. ‘Jinxiu' chloroplast genome was 157 786 bp, including typical quadripartite structure, with a GC content of 36.77% and a AT content of 63.23%. The chloroplast genome had a large single copy region (LSC), a pair of inverted repeats (IR), and a small single copy region (SSC), and the sequence length was 85 924 bp, 26 381 bp, and 19 100 bp, with GC contents of 34.61%, 42.58%, 30.41%, respectively. A total of 130 genes were annotated, consisting of 85 protein-coding genes, 37 tRNA genes and eight rRNA genes. The genes were divided into four categories according to the functions, including photosynthesis, self-replication, other genes and genes of unknown function. The genes included 18 double-copy genes, which were the subunit of NADH dehydrogenase gene (ndhB), four self-replication genes (rpl2, rpl23, rps12 and rps7), four rRNA genes (rrn16, rrn23, rrn4.5 and rrn5), seven tRNA genes (trnA-UGC, trnI-CAU, trnI-GAU, trnL-CAA, trnN-GUU, trnR-ACG and trnV-GAC), two unknown function protein genes (ycf1and ycf2). A total of 248 microsatellites were founded in the chloroplast genome of A. persica L. ‘Jinxiu'. The simple sequence repeats (SSRs) were spaced disproportionately through the chloroplast genome, with the largest number of SSRs distributed in the LSC region, followed by the SSC and IR regions. LSC, SSC and IR regions had 165, 44 and 39 SSRs, respectively. The number of SSRs in LSC, SSC and IR regions was 66.53%, 17.74%, and 15.73%, respectively. The SSRs were mononucleotides, especially for A/T. The second most abundant motif type was the trinucleotide type, especially ATA, TAT and TTA. Phylogenetic analysis showed that ‘Jinxiu' was closely related to the plant of Prunus persica (MW042696.1) This study would provide a method suitable for the assembly of the complete chloroplast genome and the analysis of feature of the whole chloroplast genome of the ‘Jinxiu', which also could provide evidence for its identification and phylogeny of ‘Jinxiu'.

Key words： Amygdalus persica L. ‘Jinxiu'; chloroplast genome; assembly; sequence analysis; phylogenetic analysis

Cite this article

GONG Yihui , ZHOU Guihua , LI Limei , ZENG Yongxian , CHEN Zhiyin . Assembly and Sequence Analysis of Chloroplast Genome of Amygdalus persica[J]. Chinese Journal of Tropical Crops, 2022 , 43(8) : 1545 -1553 . DOI: 10.3969/j.issn.1000-2561.2022.08.003

黄桃（Amygdalus persica L.）隶属于蔷薇科（Rosaceae）桃属,典型的呼吸跃变型果实,因果肉呈黄色而得名。其中‘锦绣'黄桃是一个典型的优良黄桃品种,主要分布在湖南、上海、江苏和福建等地,成熟于盛夏高温季节7—9月。‘锦绣'黄桃具有色泽金黄、果汁丰富、果形优美、风味诱人等特点[1],深受国内外广大消费者的欢迎。‘锦绣'黄桃含有丰富的胡萝卜素、番茄黄素、维生素C、锌、硒等多种人体所需的营养元素,在市场中具有较高的经济价值[2]。‘锦绣'黄桃具有生津止渴、润肠通便、滋阴补肾及提高免疫力等功效[3-4]。目前,有关‘锦绣'黄桃的研究工作主要集中于优质丰产栽培技术[5-6]、果实生理性病害机制[7]及果实软化[8]等方面研究,然而有关‘锦绣'黄桃叶绿体全基因组组装、基因特征和序列分析等尚未见报道。
叶绿体是绿色植物中一个重要的细胞器,通过进行光合作用为植物生长发育提供所需要的营养物质和能量,具有一套完整的遗传信息表达系统[9]。叶绿体基因组一般为双链环状分子,具有一个典型的四分体结构,包括一个大单拷贝区（large single copy region,LSC）、小单拷贝区（small single copy region,SSC）、反向重复区A（inverted repeat region A,IRA）和反向重复区B（inverted repeat region B,IRB）[10⇓-12]。与核基因组相比,叶绿体基因组表现出单亲遗传;并且叶绿体基因组在基因类型、基因结构等方面比线粒体基因组和核基因组更为保守,已成为研究植物物种系统发育地位的重要手段。近年来,在蔷薇科植物叶绿体基因组测序方面取得了良好的成果。多种蔷薇科植物的叶绿体基因组测序结果已在NCBI公布,如桃树（Prunus persica L.）、梨（Pyrus communis L.）、苹果（Malus domestica Borkh.）、草莓（Fragaria × ananassa D.）、杏（Prunus armeniaca L.）、枇杷（Rhaphiolepis bibas L.）、山楂（Crataegus pinnatifida Bunge）和柑橘（Citrus sinensis L.）等[13⇓⇓⇓⇓⇓⇓-20]。本研究利用Illumina NovaSeq 6000技术测定‘锦绣'黄桃叶绿体基因组序列,分析组装后‘锦绣'黄桃叶绿体基因组结构和特点,分析简单重复序列（simple sequence repeat,SSR）位点和反向重复序列的特征,并基于40种蔷薇科植物进行系统发育关系的比较分析,为今后开展黄桃品种鉴定、遗传育种和物种多样性分析提供参考依据。

1 材料与方法

1.1 材料

‘锦绣'黄桃树叶采自娄底市福缘高科生态农业有限公司,采摘嫩绿色黄桃叶片,立即用液氮速冻后放置于-80℃的超低温冰箱中,用于后续叶绿体全基因组的测序分析。

1.2 方法

1.2.1 DNA的提取

将采集的‘锦绣'黄桃树嫩绿色叶片置于研钵中加入液氮研磨至粉末,用天根生化科技（北京）有限公司的植物基因组DNA提取试剂盒（DP305）提取高质量的总DNA,并对‘锦绣'黄桃总DNA的质量进行检测。

1.2.2 测序分析

将质量合格的‘锦绣'黄桃总DNA样品送南京集思慧远生物科技有限公司进行测序,采用Illumina NovaSeq 6000平台对黄桃叶绿体DNA进行双端（pair ends,PE）测序,读长为PE150,共获得6.57 Gb原始数据。利用fastp（version 0.20.0, https://github.com/OpenGene/fastp)对reads进行质量控制,共得到21 926 286条clean reads,Q20为97.44%,Q30为92.71%,可用于后续‘锦绣'黄桃叶绿体全基因组的组装和注释。

1.2.3 叶绿体基因组组装

采用SPAdes v3.10.1[21](http://cab.spbu.ru/software/spades/)组装软件对‘锦绣'黄桃叶绿体基因组进行组装分析,选用黄桃同属蔷薇科的桃树（Prunus persica,MW698812.1）为参考序列。然后用Gapfiller v2.1.1[22]软件(https://sourceforge.net/projects/gapfiller/)和pseudo genome进行基因组序列修补和校正,最后组装出完整的‘锦绣'黄桃叶绿体环状基因组序列。

1.2.4 叶绿体基因组特征分析

先用prodigal v2.6.3(https://www.github.com/hyattpd/Prodigal)对‘锦绣'黄桃叶绿体基因组进行编码基因（CDS）预测,然后利用hmmer v3.1b2(http://www.hmmer.org/)、aragorn v1.2.38(http://130.235.244.92/ARAGORN/)软件分别对rRNA和tRNA基因进行预测,再利用OGDRAW(https://chlorobox.mpimp-golm.mpg.de/OGDraw.html)制作‘锦绣'黄桃叶绿体基因组图谱,利用MISA v1.0（MIcroSAtellite identification tool, http://pgrc.ipk-gatersleben.de/misa/misa.html)软件分析‘锦绣'黄桃叶绿体全基因组SSR位点,Find repeats工具获得‘锦绣'黄桃、梨、苹果等7种蔷薇科植物的LSC序列、SSC序列和IR序列,利用MAFFT[23]软件进行多重序列比对,最后使用RAxML v8.2.10(https://cme.h-its.org/exelixis/software.html)软件进行系统发育分析。

2 结果与分析

2.1 叶绿体基因组结构

基于Illumina NovaSeq 6000测序表明,‘锦绣'黄桃叶绿体基因组（OK545754.1）总长度为157 786 bp,碱基为6 577 885 800个,是一个典型的4分区域结构,包括LSC、SSC、IRA和IRB共4个区段,其序列长度分别为85 924、19 100、26 381、26 381 bp（图1）。整个基因组中GC和AT的含量分别为36.77%和63.23%,GC含量在SSC、LSC和IR区域的占比存在较大的差异,GC含量最高的区域是IR,为42.58%;LSC次之,34.61%;SSC中GC含量最低,为30.41%（表1）。值得关注的是,部分ycf1基因在IRA和SSC的交界处重复（图1）。
表1 黄桃叶绿体基因组碱基组成

Tab. 1 Base composition of chloroplast genome in A. persica

区域Area A/% T/% C/% G/% 长度Length/bp GC/%
LSC 31.79 33.59 17.87 16.74 85 924 34.61
SSC 34.71 34.88 15.91 14.50 19 100 30.41
IRA/IRB 28.76 28.67 20.53 22.05 26 381 42.58
总体 31.12 32.12 18.78 17.99 157 786 36.77
图1 黄桃叶绿体基因组

Fig. 1 Map of A. persica chloroplast genome

2.2 叶绿体基因组特征

首先分别利用prodigal v2.6.3、hmmer v3.1b2和aragorn v1.2.38软件对叶绿体的CDS、rRNA和tRNA进行预测,得到第1种注释结果,然后根据NCBI上已报道的近缘物种,提取其基因序列,并使用blast v2.6(https://blast.ncbi.nlm.nih.gov/Blast.cgi)比对组装的序列,得到第2种注释结果。最后比较这2种注释结果中有差别的基因,去除错误注释及冗余的注释,确定多外显子边界,从而获得最终的注释。在‘锦绣'黄桃叶绿体基因组上共注释130个基因,其中编码蛋白基因（CDS）、tRNA基因、rRNA基因分别为 85、37、8个（表2）。按照功能分类将其分成4大类：光合作用相关基因（photosynthesis genes）、自我复制基因（self-replication genes）、其他基因（other genes）、未知功能基因（genes of unknown function）。
表2 黄桃叶绿体基因组编码的基因

Tab. 2 Genes present in chloroplast genome of A. persica

基因分类 Category of genes 基因分组
Group of genes		 基因名称
Name of genes
光合作用相关基因 Subunits of photosystem I psaA、psaB、psaC、psaI、psaJ
Subunits of photosystem II psbA、psbB、psbC、psbD、psbE、psbF、psbH、psbI、psbJ、psbK、psbL、psbM、psbN、psbT、psbZ
Subunits of NADH dehydrogenase ndhA*、ndhB*(2)、ndhC、ndhD、ndhE、ndhF、ndhG、ndhH、ndhI、ndhJ、ndhK
Subunits of cytochrome b/f complex petA、petB*、petD*、petG、petL、petN
Subunits of ATP synthase atpA、atpB、atpE、atpF*、atpH、atpI
Large subunit of rubisco rbcL
Subunits photochlorophyllide reductase
自我复制相关基因 Proteins of large ribosomal subunit rpl14、rpl16*、rpl2*(2)、rpl20、rpl22、rpl23(2)、rpl32、rpl33、rpl36
Proteins of small ribosomal subunit rps11、rps12**(2)、rps14、rps15、rps16*、rps18、rps19、rps2、rps3、rps4、rps7(2)、rps8
Subunits of RNA polymerase rpoA、rpoB、rpoC1*、rpoC2
Ribosomal RNAs rrn16(2)、rrn23(2)、rrn4.5(2)、rrn5(2)
Transfer RNAs trnA-UGC*(2)、trnC-GCA、trnD-GUC、trnE-UUC、trnF-GAA、trnG-GCC、trnG-GCC*、trnH-GUG、trnI-CAU(2)、trnI-GAU*(2)、trnK-UUU*、trnL-CAA(2)、trnL-UAA*、trnL-UAG、trnM-CAU、trnN-GUU(2)、trnP-UGG、trnQ-UUG、trnR-ACG(2)、trnR-UCU、trnS-GCU、trnS-GGA、trnS-UGA、trnT-GGU、trnT-UGU、trnV-GAC(2)、trnV-UAC*、trnW-CCA、trnY-GUA、trnfM-CAU
其他基因 Maturase matK
Protease clpP**
Envelope membrane protein cemA
Acetyl-CoA carboxylase accD
c-type cytochrome synthesis gene ccsA
Translation initiation factor
other
未知功能
基因		 Conserved hypothetical chloroplast ORF ycf1(2)、ycf2(2)、ycf3**、ycf4

注：*表示含有一个内含子;**表示含有2个内含子;Gene(2)表示拷贝数大于1的基因,括号中为其拷贝数。

Note: * indicates one intron in the gene; ** indicates two introns in the gene; Gene(2) indicate the gene with copy number greater than one, and the copy number in brackets.

由表2可知,双拷贝基因有18个,占13.85%,分别是1个NADH 脱氢酶亚基基因（ndhB）、4个自我复制基因（rpl2、rpl23、rps12、rps7）、4 个 rRNA 基因（rrn16、rrn23、rrn4.5、rrn5）、7个tRNA基因（trnA-UGC、trnI-CAU、trnI-GAU、trnL-CAA、trnN-GUU、trnR-ACG、trnV-GAC）、2个未知功能蛋白基因（ycf1、ycf2）。值得研究者关注的是,有4个基因（ycf1、ycf2、ycf3、ycf4）在‘锦绣'黄桃叶绿体基因组中未能鉴定出蛋白功能,仍需通过更先进的分子手段对它们进行功能分析。
在‘锦绣'黄桃叶绿体基因组大部分基因不含内含子,只有少数基因含有1个或2个内含子,其中ndhA、ndhB、petB、petD、atpF、rpl16、rpl2、rps16、rpoC1、trnA-UGC、trnG-GCC、trnI-GAU、trnK-UUU、trnL-UAA各含有1个内含子。而rps12、clpP、ycf3基因分别含有2个内含子,未能在‘锦绣'黄桃叶绿体基因组中鉴定出假基因（表2）。

2.3 SSR分析

采用MISA v1.0软件对‘锦绣'黄桃叶绿体基因组进行了SSR分析（图2）。共在‘锦绣'黄桃叶绿体基因组中查找248个符合条件的SSR位点,分布在LSC、SSC、IR区域的SSR位点分别为165、44、39个,占比分别为66.53%、17.74%、15.73%。在所有SSR中,单核苷酸重复单元有158个,双核苷酸重复单元有17个,三核苷酸重复单元有69个,四核苷酸重复单元有5个,五核苷酸重复单元有2个,其中最多重复基元是A/T,然后依次是AT/TA、ATA、TAT、TTA。结果表明,A/T碱基占优势,具有碱基偏好性。这与‘锦绣'黄桃叶绿体基因组63.23%的AT含量相一致,可能是AT碱基比GC碱基更容易解链有关。
图2 黄桃叶绿体基因组中SSR位点类型及数量

Fig. 2 Type and number of SSR loci of A. persica chloroplast genome

2.4 蔷薇科IR区边界比较分析

‘锦绣'黄桃与蔷薇科桃树、苹果、梨、杏、枇杷、山楂6个不同物种叶绿体基因组进行IR区边界比较（图3）,结果发现,这7种果树叶绿体基因组总长度为157 786~159 926 bp,从小到大依次为‘锦绣'黄桃、桃、杏、枇杷、山楂、梨、苹果。其中桃树与‘锦绣'黄桃基因结构和种类很相似,rpl2基因全部位于IRa区域内,长度为1502 bp,ycf1 基因分别位于IRb/SSC和SSC/IRa边界,或许与IR/SSC边界的扩张有很大的关系。位于SSC/IRa边界的ycf1基因长度为5616 bp,但ycf1位于IRb/SSC边界的ycf1基因全长仅为1056 bp。然而梨、苹果和枇杷物种都没有rpl22基因。
图3 蔷薇科7个物种叶绿体全基因组IR边界的比较示意图

Fig. 3 Comparison schematic diagram of chloroplast genome IR boundaries of seven species of Rosaceae

2.5 进化树分析

为了解‘锦绣'黄桃在蔷薇科中的进化位置,将测得的‘锦绣'黄桃叶绿体基因组序列与已在NCBI网站公布的39种蔷薇科的叶绿体全基因组进行多重序列比对,并利用RAxML v8.2.10软件构建进化树。由图4可知,同科不同属的物种与‘锦绣'黄桃相距较远,说明这些物种与‘锦绣'黄桃亲缘关系较远,18种不同的果树与‘锦绣'黄桃聚类为一组,其中桃属（Prunus persica,MH169125.1）与‘锦绣'黄桃的距离最近,说明‘锦绣'黄桃与该桃树品种的亲缘关系最近。
图4 基于叶绿体全基因组的40个物种的最大似然法聚类结果

Fig. 4 Cluster analysis of 40 species using complete chloroplast genome sequence by Maximum Likelihood Method

3 讨论

黄桃是我国最重要的特色水果之一,具有较高的营养价值和商业价值,在水果市场上具有极高的竞争力,在我国农业产业发展中占有重要的地位。近年来,随着高通量测序技术和组装软件的不断完善,虽然有一些桃树品种（如油桃Prunus persica var. nectarina）的叶绿体基因组被报道出来[13,24],但是‘锦绣'黄桃品种的叶绿体基因组研究却一直尚未被报道。本研究发现与苹果、桃、梨等其他6个蔷薇科物种相比,‘锦绣'黄桃叶绿体基因组是高度保守的,‘锦绣'黄桃叶绿体基因组长度为157 786 bp,共注释到130个基因,蛋白编码基因、tRNA、rRNA基因数分别为85、37、8个。LIU等[13]研究发现,‘瑞光18号'油桃品种的叶绿体基因组全长为157 494 bp,共注释到116个基因,其中76个为蛋白编码基因,35个tRNA,6个rRNA。SHARKO等[24]研究发现,‘Sovetskiy' 桃品种的叶绿体基因组全长为157 756  bp,共注释到126个基因,其中81个为蛋白编码基因,37个为tRNA,8个rRNA。‘锦绣'黄桃的叶绿体基因组长度均大于‘瑞光18号'和‘Sovetskiy'品种,注释到的编码基因、tRNA和rRNA数量均大于‘瑞光18号'和‘Sovetskiy'品种,可能是由于不同桃树品种具有不同的遗传特性造成这种差异。上述研究表明,不同的桃品种其叶绿体基因组长度和注释到基因数量存在一定的差异,为今后开展桃品种分类和遗传多样性奠定了良好基础。
SSR广泛分布于真核生物和原核生物基因中,具有共显性。本研究在‘锦绣'黄桃叶绿体中共鉴定出248个SSR,其中SSR数量分布最多的区域是LSC区域,为165个,主要由A和T碱基组成,这与菜头肾叶绿体基因SSR分析结果相似[25]。SSR分布存在单核苷酸、双核苷酸、三核苷酸、四核苷酸、五核苷酸重复单元等类型,在‘锦绣'黄桃叶绿体组中以单核苷酸重复占绝对优势,主要是A/T,其次是三核苷酸类型,其优势重复单元类型是ATA、TAT和TTA。WANG等[26]在长裂苦苣菜（Sonchus brachyotus）叶绿体基因组查找出175个SSR位点,以单核苷酸重复占绝对优势,主要是A/T。本研究对‘锦绣'黄桃的SSR分析与WANG等[26]研究结果相似。但是,不同物种叶绿体基因组中SSR位点的重复单元存在很大差异。赵祺等[25]发现菜头肾叶绿体基因组以TTG/TTA和ATA/ATA三核苷酸单位重复为主。板蓝（Strobilanthes cusia）和穿心莲（Andrographis paniculata）以二核苷酸重复为主,重复基元占比最大的类型是AG/CT和AT/AT[27-28]。本研究发现‘锦绣'黄桃叶绿体基因组中存在丰富的SSR变异位点,为后续开发SSR标记及进一步揭示‘锦绣'黄桃的系统发育地位提供了可靠的分子手段。
叶绿体基因组提供了丰富的植物分类和系统发育信息。本研究将‘锦绣'黄桃与其他39种蔷薇科的叶绿体基因组进行多重序列比对并进行系统发育分析。结果发现‘锦绣'黄桃与桃属（Prunus persica,MH169125.1）的亲缘关系最近,其结果与《中国植物志》记载的分类相一致[29]。SHARKO等[24]研究发现,‘Sovetskiy'桃品种与‘Nemared'桃品种（Prunus persica,NC014697.1）的亲缘关系最近。LIU等[13]分析了‘瑞光18号'油桃品种与10种蔷薇科物种的系统发育位置,结果发现‘瑞光18号'与桃属（Prunus persica,NC014697）的亲缘关系最近。本研究将‘锦绣'黄桃的系统发育分析结果与SHARKO等[24]和LIU等[13]研究结果相似,说明‘锦绣'黄桃、‘瑞光18号'、‘Nemared'和‘Sovetskiy'均属于蔷薇科桃属,获得了更多相似的亲本遗传信息,其亲缘关系也就最近。本研究明确了‘锦绣'黄桃的系统发育地位及与其他蔷薇科不同属的系统发育关系,为进一步开展品种鉴定和驯化分析奠定基础;本研究通过对‘锦绣'黄桃叶绿体基因组组装和序列分析,为今后开展蔷薇科的遗传进化分析提供了有用的遗传信息。

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