棉纤维起始发育过程中microRNA的鉴定及功能分析
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摘要
棉花是世界上最重要的天然纤维来源之一,在纺织业中具有重要作用,同时还是纤维素合成以及细胞伸长研究的模式植物。棉纤维是从胚珠表皮上分化和突起的单细胞,与拟南芥表皮毛具有很大的相似性,后者可以作为棉纤维研究的模式。棉纤维包括长绒(lint)和短绒(fuzz),前者在开花当天从棉花胚珠外珠被表皮层分化突起,后者在开花后4-5天时从外珠被表皮上突起。microRNA (miRNA)是真核生物中发现的一类内源性的具有调控功能的非编码小分子RNA,通过碱基互补配对的方式识别靶标mRNA,通过靶基因切割或翻译抑制的方式调控靶基因表达。miRNA在植物生长发育各个方面和生物非生物胁迫抗性调节中发挥重要的作用。
本研究利用高通量测序方法测序3个纤维起始发育突变体(XZ142FLM, MD17FLM和SL1-7-1FLM),2个短绒起始发育突变体(N1NSM和n2NSM)和正常纤维TM-1六个材料棉纤维起始发育期的小RNA,利用雷蒙德氏棉和陆地棉基因组序列鉴定棉花MIRNA前体,用Northern blotting验证新miRNA在棉花中的表达；根据miRNA在野生型和突变体中的表达差异鉴定棉纤维起始调控的关键miRNA;用转录组数字表达谱验证miRNA靶基因的表达；利用5'RACE验证miRNA对靶基因mRNA的剪切。研究结果如下：
1.陆地棉胚珠早期发育过程中miRNA的鉴定
以陆地棉遗传标准系TM-1为研究材料,建立了棉花纤维起始发育时期和短绒起始发育时期的小RNA混库,TM-LA(-3,-1,0,1DPA)和TM-LB (-1,0,1,3,5DPA)。利用HiSeq测序技术共检测到了三千万条小RNA序列,共检测到33个已知miRNA家族表达。利用雷蒙德氏棉基因组序列,成功鉴定出了93个新的MIRNAs前体,包括28个已知miRNA家族的新成员,它们属于10个家族；另外65为全新的miRNA,它们可以产生43个不同成熟体,将其编号为miR7234-miR7276。Northern blotting验证发现miR7235,miR7244和miR7251在-3DPA和3DPA的胚珠中的表达量相同,与测序结果一致。miR7235可以靶向肌动蛋白ATP酶超家族蛋白基因,它可以介导该家族基因Gra#S24823914和Ghi#S42313172mRNA的切割,切点位于miRNA与mRNA的互补区域miR7235第10和第11个碱基之间。
2.陆地棉基因组序列在microRNA鉴定中的应用
以三个纤维起始发育突变体为材料,建立了棉花纤维起始发育时期(-3,-1,0,1DPA)的小RNA混库；以短绒起始发育突变体为材料,构建短绒起始发育时期(-1,0,1,3,5DPA)的小RNA混库；结合野生型小RNA混库(TM-LA和TM-LB),共七个库,每个库的小RNAs序列超过了16M。利用陆地棉基因组组装序列鉴定出322个新的棉花MIRNAs前体。这些前体的长度变化很大,从79nt到544nt不等,主要集中在80-200nt,平均长度是149.8nt。它们所形成的miRNA成熟体中,74.2%第一个碱基是“尿嘧啶”。这322条MIRNAs中,197个前体属于38个已知家族；剩余125条不与miRBase库(Release20)中任何miRNA同源,为新的miRNA.这125个新miRNA前体可以产生102条不同的miRNA成熟体,归类于86个新的miRNA家族,将其命名为ghr-miRn01-86。
58条新MIRNAs前体获得的成熟体序列存在一定变异,包括长度的变异和位置变异。同一家族中不同成熟体序列的差异主要是成熟体5’端和3’端起止位置存在差异和碱基的变异,它们的表达差异非常大。以miR156/535家族成员为例证明了成熟体序列差异对于靶基因的选择和靶基因mRNA的切割位点造成影响。
3.棉花miRNA在纤维起始发育过程中功能分析
利用七个棉纤维起始时期小RNA库鉴定这148个miRNA家族在野生型和突变体中的表达。在野生型TM-1中下调而在突变体中共同上调表达的miRNA,包括miRl56,miR160, miR160*, miR166, miR167, miR171,miR535, miR827等保守家族,miR2948*, miR3476, miR7495, miR7504, miR7505, miR7508等非保守家族,以及miRn13, miRn21, miRn51, miRn60, miRn77, miRn80等七个新家族。在野生型TM-1中上调表达而在突变体中共同下调表达的miRNA,包括miR162, miR164, miR166*, miR172, miR396*, miR403, miR482*等保守家族,miR2949, miR7122, miR7502, miR7511四个非保守家族,以及新家族的miRn08和miRn81。野生型TM-1与突变体比较,在三个纤维起始突变体中共同上调表达而在两个短绒起始突变体中共同下调表达的miRNA,包括miR169, miR172*, miR390, miR390*, miR394, miR396, miR482等保守家族,非保守家族的miR2948,以及新鉴定家族的miRn07, miRn76, miRn85, miRn85*。用六种实验材料-3,-1,1,3和5DPA胚珠的转录组表达谱验证miRNA靶基因的表达,发现差异表达的39个miRNA家族的靶基因有237个。经过对靶基因的表达模式分析,鉴定出73个基因可能受对应的miRNA调控。用5'RACE验证了8个miRNA对11个靶基因的剪切。结果显示miR164, miR171, miR394和miR396介导7个基因mRNA剪切的切点位于miRNA的第10和第11个碱基之间；miR397, miR530和miRn20介导的靶基因切割位点位于mRNA和miRNA结合区域上游6-10nt的位置；miRn80的靶基因Chi#S28642014的切割位点位于结合区域的下游80nt处。切点位置偏离miRNA的第10和第11个碱基之间的mRNA切割事件是由其他小RNA切割导致。
Cotton is the source of the most important renewable, natural textile fiber in the world and is of significant importance in the textile industry. Meanwhile, Cotton provides a novel system in which to better understand the genetic and biochemical control of cell elongation as well as cellulose biosynthesis. Cotton'fibers'are trichomes derived from epidermal cells of the developing seed. These trichomes share many similarities with those found on Arabidopsis thaliana leaves and which could serve as a model for elucidating the genetic mechanisms that control cotton fiber and seed development. MicroRNAs (miRNAs) are endogenous20-24nucleotides in length, non-coding RNAs, serving as a class of post-transcriptional regulators in eukaryotic organism. MiRNAs negatively regulate their target genes by mRNA cleavage or translation expression via extensive complementarity between miRNAs and their targets. Increasing evidence has demonstrated that plant miRNAs have functions in a wide range of developmental processes and biotic and abiotic stress.
In this study, we sequenced seven small RNA libraries constructed from young ovules during fiber initial period using three fibreless mutants (XZ142FLM, MD17FLM, SL1-7-1FLM), two fuzzless mutants (N1NSM, n2NSM) and wild type TM-1. New MIRNAs precursors were predicted in cotton using genome sequence of Gossypium raimondii and Gossypium hirsutum. Some of the novel miRNAs and candidate target genes were validated by the Northern blot and5'RACE. MiRNAs associated with fiber initiation were identified according to different expression between WT and the five mutants. Targets genes expression were validated using transcriptome profiling and the cleavage sites were validated using5' RACE. The main results were as follows:
1. Genome-wide identification of miRNAs during fiber and ovule initial development
The Upland cotton Texas Marker-1(TM-1) was used to construct small RNA libraries from young ovules during lint and fuzz initial period. TM-LA was pooled from-3,-1,0and1DPA, and TM-LB was pooled from-1,0,1,3and5DPA. A total of33million small RNA sequences were obtained, and33known miRNA families were expressed in TM-1ovules. Overall,93new miRNA precursors were identified, of which28belonged to10known families and the other65were considered to be novel miRNAs.65precursors containing43small RNAs which were numbered in consecutive order from miR7234to miR7276. Northern blotting validated that miR7235, miR7244and miR7251expressed equally between-1DPA and3DPA as the same as the deep sequencing results. It was predicted miR7235could target a series of Actin-like ATPase superfamily protein, two of which were validated using5'RACE with cleavage sites between the10th and11th nucleotide of miR7235.
2. Genome sequence of upland cotton was used in miRNAs identification.
Three fibreless mutants (XZ142FLM, MD17FLM, SL1-7-1FLM) were used to construct small RNA libraries during fiber initial period (-3,-1,0and1DPA), and two fuzzless mutants (N1NSM, n2NSM) were used to construct small RNA libraries during fuzz initial period (-1,0,1,3and5DPA). Taken TM-LA and TM-LB together, seven libraries were constructed, each with more than16M reads. Using the genome sequence of upland cotton, a total of322new MIRNAs were identified in upland cotton. The precursors varied in length, from79to544nt, and had an average length of149.8nt. The majority of the miRNAs (74.2%) have a uridine at5'terminal. Among the322miRNAs,197belong to38known families, the other125have no homolog in miRBase (Release20), and we labeled them as novel miRNAs. Those novel MIRNA precursors produce102distinct miRNA mature sequence belonging to86families, and number them as ghr-miRn01-86.
58of the new MIRNAs precursors produce mature sequences with variances in size or position. Distinct members of the same family have variances in start site or nucleotides. The expression of the members differs a lot. The members of miR156/535could target the same target genes with score and the cleavage products differ by two nucleotides depending on which miRNA guides the processing event.
3. Function analysis of miRNA associated with fiber initiation
Taken cotton known miRNA and the new miRNAs identified in this study together,62known families and86novel miRNA families were identified in upland cotton. MiRNA downregulated in wild type TM-1and upregulated in the five mutants include seven conserved families (miR156, miR160, miR160*, miR166, miR167, miR171, miR535, miR827), six less conserved miRNA families (miR2948*, miR3476, miR7495, miR7504, miR7505, miR7508) and six novel families (miRn13, miRn21, miRn51, miRn60, miRn77, miRn80). MiRNA upregulated in wild type TM-1and downregulated in the five mutants included seven conserved families (miR162, miR164, miR166*, miR172, miR396*, miR403, miR482*), four less conserved miRNA families (miR2949, miR7122, miR7502, miR7511) and two novel miRNAs (miRn08and miRn81). Compared with TM-1, miRNAs upregulated in fiberless mutants and downregulated in fuzzless mutants included miR169, miR172*, miR390, miR390*, miR394, miR396, miR482, miR2948, miRn07, miRn76, miRn85, miRn85*. Targets genes expression of the39differentially expressed miRNAs were validated using transcriptome profiling. Cluster analysis of227target genes showed that expression pattern of73genes were complementary with miRNA. Eleven target genes of eight miRNA were validated using5'RACE. Seven target genes of miR164, miR171, miR394and miR396were cleaved in the exact site between nucleotides10and11from the5'end of the miRNA. Target genes of miR397, miR530and miRn20were cleaved at6-1Ont upstream of complementary region. Target gene of miRn80was cleaved at80nt downstream of complementary region. We found cleavage sites away from the10th and11th nucleotide of miRNA were actually cleavage by other small RNA.
本研究利用高通量测序方法测序3个纤维起始发育突变体(XZ142FLM, MD17FLM和SL1-7-1FLM),2个短绒起始发育突变体(N1NSM和n2NSM)和正常纤维TM-1六个材料棉纤维起始发育期的小RNA,利用雷蒙德氏棉和陆地棉基因组序列鉴定棉花MIRNA前体,用Northern blotting验证新miRNA在棉花中的表达；根据miRNA在野生型和突变体中的表达差异鉴定棉纤维起始调控的关键miRNA;用转录组数字表达谱验证miRNA靶基因的表达；利用5'RACE验证miRNA对靶基因mRNA的剪切。研究结果如下：
1.陆地棉胚珠早期发育过程中miRNA的鉴定
以陆地棉遗传标准系TM-1为研究材料,建立了棉花纤维起始发育时期和短绒起始发育时期的小RNA混库,TM-LA(-3,-1,0,1DPA)和TM-LB (-1,0,1,3,5DPA)。利用HiSeq测序技术共检测到了三千万条小RNA序列,共检测到33个已知miRNA家族表达。利用雷蒙德氏棉基因组序列,成功鉴定出了93个新的MIRNAs前体,包括28个已知miRNA家族的新成员,它们属于10个家族；另外65为全新的miRNA,它们可以产生43个不同成熟体,将其编号为miR7234-miR7276。Northern blotting验证发现miR7235,miR7244和miR7251在-3DPA和3DPA的胚珠中的表达量相同,与测序结果一致。miR7235可以靶向肌动蛋白ATP酶超家族蛋白基因,它可以介导该家族基因Gra#S24823914和Ghi#S42313172mRNA的切割,切点位于miRNA与mRNA的互补区域miR7235第10和第11个碱基之间。
2.陆地棉基因组序列在microRNA鉴定中的应用
以三个纤维起始发育突变体为材料,建立了棉花纤维起始发育时期(-3,-1,0,1DPA)的小RNA混库；以短绒起始发育突变体为材料,构建短绒起始发育时期(-1,0,1,3,5DPA)的小RNA混库；结合野生型小RNA混库(TM-LA和TM-LB),共七个库,每个库的小RNAs序列超过了16M。利用陆地棉基因组组装序列鉴定出322个新的棉花MIRNAs前体。这些前体的长度变化很大,从79nt到544nt不等,主要集中在80-200nt,平均长度是149.8nt。它们所形成的miRNA成熟体中,74.2%第一个碱基是“尿嘧啶”。这322条MIRNAs中,197个前体属于38个已知家族；剩余125条不与miRBase库(Release20)中任何miRNA同源,为新的miRNA.这125个新miRNA前体可以产生102条不同的miRNA成熟体,归类于86个新的miRNA家族,将其命名为ghr-miRn01-86。
58条新MIRNAs前体获得的成熟体序列存在一定变异,包括长度的变异和位置变异。同一家族中不同成熟体序列的差异主要是成熟体5’端和3’端起止位置存在差异和碱基的变异,它们的表达差异非常大。以miR156/535家族成员为例证明了成熟体序列差异对于靶基因的选择和靶基因mRNA的切割位点造成影响。
3.棉花miRNA在纤维起始发育过程中功能分析
利用七个棉纤维起始时期小RNA库鉴定这148个miRNA家族在野生型和突变体中的表达。在野生型TM-1中下调而在突变体中共同上调表达的miRNA,包括miRl56,miR160, miR160*, miR166, miR167, miR171,miR535, miR827等保守家族,miR2948*, miR3476, miR7495, miR7504, miR7505, miR7508等非保守家族,以及miRn13, miRn21, miRn51, miRn60, miRn77, miRn80等七个新家族。在野生型TM-1中上调表达而在突变体中共同下调表达的miRNA,包括miR162, miR164, miR166*, miR172, miR396*, miR403, miR482*等保守家族,miR2949, miR7122, miR7502, miR7511四个非保守家族,以及新家族的miRn08和miRn81。野生型TM-1与突变体比较,在三个纤维起始突变体中共同上调表达而在两个短绒起始突变体中共同下调表达的miRNA,包括miR169, miR172*, miR390, miR390*, miR394, miR396, miR482等保守家族,非保守家族的miR2948,以及新鉴定家族的miRn07, miRn76, miRn85, miRn85*。用六种实验材料-3,-1,1,3和5DPA胚珠的转录组表达谱验证miRNA靶基因的表达,发现差异表达的39个miRNA家族的靶基因有237个。经过对靶基因的表达模式分析,鉴定出73个基因可能受对应的miRNA调控。用5'RACE验证了8个miRNA对11个靶基因的剪切。结果显示miR164, miR171, miR394和miR396介导7个基因mRNA剪切的切点位于miRNA的第10和第11个碱基之间；miR397, miR530和miRn20介导的靶基因切割位点位于mRNA和miRNA结合区域上游6-10nt的位置；miRn80的靶基因Chi#S28642014的切割位点位于结合区域的下游80nt处。切点位置偏离miRNA的第10和第11个碱基之间的mRNA切割事件是由其他小RNA切割导致。
Cotton is the source of the most important renewable, natural textile fiber in the world and is of significant importance in the textile industry. Meanwhile, Cotton provides a novel system in which to better understand the genetic and biochemical control of cell elongation as well as cellulose biosynthesis. Cotton'fibers'are trichomes derived from epidermal cells of the developing seed. These trichomes share many similarities with those found on Arabidopsis thaliana leaves and which could serve as a model for elucidating the genetic mechanisms that control cotton fiber and seed development. MicroRNAs (miRNAs) are endogenous20-24nucleotides in length, non-coding RNAs, serving as a class of post-transcriptional regulators in eukaryotic organism. MiRNAs negatively regulate their target genes by mRNA cleavage or translation expression via extensive complementarity between miRNAs and their targets. Increasing evidence has demonstrated that plant miRNAs have functions in a wide range of developmental processes and biotic and abiotic stress.
In this study, we sequenced seven small RNA libraries constructed from young ovules during fiber initial period using three fibreless mutants (XZ142FLM, MD17FLM, SL1-7-1FLM), two fuzzless mutants (N1NSM, n2NSM) and wild type TM-1. New MIRNAs precursors were predicted in cotton using genome sequence of Gossypium raimondii and Gossypium hirsutum. Some of the novel miRNAs and candidate target genes were validated by the Northern blot and5'RACE. MiRNAs associated with fiber initiation were identified according to different expression between WT and the five mutants. Targets genes expression were validated using transcriptome profiling and the cleavage sites were validated using5' RACE. The main results were as follows:
1. Genome-wide identification of miRNAs during fiber and ovule initial development
The Upland cotton Texas Marker-1(TM-1) was used to construct small RNA libraries from young ovules during lint and fuzz initial period. TM-LA was pooled from-3,-1,0and1DPA, and TM-LB was pooled from-1,0,1,3and5DPA. A total of33million small RNA sequences were obtained, and33known miRNA families were expressed in TM-1ovules. Overall,93new miRNA precursors were identified, of which28belonged to10known families and the other65were considered to be novel miRNAs.65precursors containing43small RNAs which were numbered in consecutive order from miR7234to miR7276. Northern blotting validated that miR7235, miR7244and miR7251expressed equally between-1DPA and3DPA as the same as the deep sequencing results. It was predicted miR7235could target a series of Actin-like ATPase superfamily protein, two of which were validated using5'RACE with cleavage sites between the10th and11th nucleotide of miR7235.
2. Genome sequence of upland cotton was used in miRNAs identification.
Three fibreless mutants (XZ142FLM, MD17FLM, SL1-7-1FLM) were used to construct small RNA libraries during fiber initial period (-3,-1,0and1DPA), and two fuzzless mutants (N1NSM, n2NSM) were used to construct small RNA libraries during fuzz initial period (-1,0,1,3and5DPA). Taken TM-LA and TM-LB together, seven libraries were constructed, each with more than16M reads. Using the genome sequence of upland cotton, a total of322new MIRNAs were identified in upland cotton. The precursors varied in length, from79to544nt, and had an average length of149.8nt. The majority of the miRNAs (74.2%) have a uridine at5'terminal. Among the322miRNAs,197belong to38known families, the other125have no homolog in miRBase (Release20), and we labeled them as novel miRNAs. Those novel MIRNA precursors produce102distinct miRNA mature sequence belonging to86families, and number them as ghr-miRn01-86.
58of the new MIRNAs precursors produce mature sequences with variances in size or position. Distinct members of the same family have variances in start site or nucleotides. The expression of the members differs a lot. The members of miR156/535could target the same target genes with score and the cleavage products differ by two nucleotides depending on which miRNA guides the processing event.
3. Function analysis of miRNA associated with fiber initiation
Taken cotton known miRNA and the new miRNAs identified in this study together,62known families and86novel miRNA families were identified in upland cotton. MiRNA downregulated in wild type TM-1and upregulated in the five mutants include seven conserved families (miR156, miR160, miR160*, miR166, miR167, miR171, miR535, miR827), six less conserved miRNA families (miR2948*, miR3476, miR7495, miR7504, miR7505, miR7508) and six novel families (miRn13, miRn21, miRn51, miRn60, miRn77, miRn80). MiRNA upregulated in wild type TM-1and downregulated in the five mutants included seven conserved families (miR162, miR164, miR166*, miR172, miR396*, miR403, miR482*), four less conserved miRNA families (miR2949, miR7122, miR7502, miR7511) and two novel miRNAs (miRn08and miRn81). Compared with TM-1, miRNAs upregulated in fiberless mutants and downregulated in fuzzless mutants included miR169, miR172*, miR390, miR390*, miR394, miR396, miR482, miR2948, miRn07, miRn76, miRn85, miRn85*. Targets genes expression of the39differentially expressed miRNAs were validated using transcriptome profiling. Cluster analysis of227target genes showed that expression pattern of73genes were complementary with miRNA. Eleven target genes of eight miRNA were validated using5'RACE. Seven target genes of miR164, miR171, miR394and miR396were cleaved in the exact site between nucleotides10and11from the5'end of the miRNA. Target genes of miR397, miR530and miRn20were cleaved at6-1Ont upstream of complementary region. Target gene of miRn80was cleaved at80nt downstream of complementary region. We found cleavage sites away from the10th and11th nucleotide of miRNA were actually cleavage by other small RNA.
引文
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