基于叶球转录组数据比较的甘蓝杂种优势分析
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摘要
对甘蓝两个杂交组合F_1的杂种优势进行了田间性状统计分析以及叶球转录组测序分析。所调查的9个园艺学性状中,单球质量和球主叶柄质量在F_1代及其亲本之间差异显著,其中单球质量的中亲优势和超亲优势在两个组合F_1中表现突出,即产量杂种优势较为明显。通过叶球转录组分析,分别筛选获得了4组差异表达基因,在相同标准下,两个杂交组合中父本与F_1代的差异表达基因明显多于母本与F_1代的差异表达基因,表明母本的表达谱与F_1更相似,即母本在F_1叶球杂种优势形成中的贡献较大,而且上调差异表达基因的差异倍数明显高于下调差异表达基因,表明上调基因在F_1代甘蓝叶球杂种优势建成中有重要作用。进一步将差异表达基因进行GO(Gene ontology)分类、COG(Cluster of orthologous groups of proteins)分类、KEGG(Kyoto encyclopedia of genes and genomes)通路富集分析以及可变剪接分析,发现差异表达基因显著富集到生长发育、碳水化合物转运和代谢、信号转导以及氨基酸的合成、转运和代谢等途径。随机选取7个差异表达基因进行实时荧光定量PCR验证,结果与RNA-seq数据基本一致,证明转录组数据的可靠性。本研究中获得的与甘蓝叶球杂种优势形成相关的差异表达基因,为后续甘蓝杂种优势分子机制研究提供数据支持。
In two F_1 hybrids,we performed heterosis analysis through field traits survey and transcriptome sequencing of cabbage heads leaves. The result found that among the nine horticultural traits,head weight and main petiole weight showed significant differences between F_1 hybrids and their parents,among which the head weight exhibited a high value of MPH(mid-parent heterosis)and HPH(high-parent heterosis)in the two F_1 hybrids,which means the yield heterosis is obvious. Four groups of differentially expressed genes(DEGs)were compared through transcriptome analysis of cabbage heads leaves. We found that the number of DEGs between F_1 hybrids and paternal lines were significantly higher than that between F_1 hybrids and their maternal lines in the same criteria. It means similar gene expression profile between maternal lines and their F_1 hybrids or a bigger contribution of maternal lines than paternal lines in the formation process of cabbage heads leaves of F_1 hybrids. Besides,the fold change of up-regulated genes were higher than that of down-regulated genes,which implied an important role of up-regulated genes in the formation process of cabbage heads leaves of F_1 hybrids. The DEGs were further conducted GO(Gene Ontology),COG(Cluster of Orthologous Groups of proteins),KEGG(Kyoto Encyclopedia of Genes and Genomes)pathway enrichment and alternative splicing analysis. The result found that DEGs are highly involved in growth and development,carbohydrate transport and metabolism,signal transduction and amino acid biosynthesis,transport and metabolism pathways. Seven DEGs were randomly selected to perform qRT-PCR and the result was basically consistent with RNA-seq,demonstrating the reliability of transcriptome data. The DEGs that we screened associated with the formation process of heterosis of cabbage heads leaves,able to provide data support for the subsequent research on the molecular mechanism of cabbage heterosis.
In two F_1 hybrids,we performed heterosis analysis through field traits survey and transcriptome sequencing of cabbage heads leaves. The result found that among the nine horticultural traits,head weight and main petiole weight showed significant differences between F_1 hybrids and their parents,among which the head weight exhibited a high value of MPH(mid-parent heterosis)and HPH(high-parent heterosis)in the two F_1 hybrids,which means the yield heterosis is obvious. Four groups of differentially expressed genes(DEGs)were compared through transcriptome analysis of cabbage heads leaves. We found that the number of DEGs between F_1 hybrids and paternal lines were significantly higher than that between F_1 hybrids and their maternal lines in the same criteria. It means similar gene expression profile between maternal lines and their F_1 hybrids or a bigger contribution of maternal lines than paternal lines in the formation process of cabbage heads leaves of F_1 hybrids. Besides,the fold change of up-regulated genes were higher than that of down-regulated genes,which implied an important role of up-regulated genes in the formation process of cabbage heads leaves of F_1 hybrids. The DEGs were further conducted GO(Gene Ontology),COG(Cluster of Orthologous Groups of proteins),KEGG(Kyoto Encyclopedia of Genes and Genomes)pathway enrichment and alternative splicing analysis. The result found that DEGs are highly involved in growth and development,carbohydrate transport and metabolism,signal transduction and amino acid biosynthesis,transport and metabolism pathways. Seven DEGs were randomly selected to perform qRT-PCR and the result was basically consistent with RNA-seq,demonstrating the reliability of transcriptome data. The DEGs that we screened associated with the formation process of heterosis of cabbage heads leaves,able to provide data support for the subsequent research on the molecular mechanism of cabbage heterosis.
引文
Abe M. 2005. FD,a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science,309(5737):1052–1056.
Adnan M,Morton G,Hadi S. 2011. Analysis of rpoS and bolA gene expression under various stress-induced environments in planktonic and biofilm phase using 2-??CT method. Mol Cell Biochem,357(1–2):275–282.
Bell G D M,Kane N C,Rieseberg L H,Adams K L. 2013. RNA-Seq analysis of allele-specific expression,hybrid effects,and regulatory divergence in hybrids compared with their parents from natural populations. Genome Biology and Evolution,5(7):1309–1323.
Berger F,Chaudhury A. 2009. Parental memories shape seeds. Trends Plant Sci,14(10):550–556.
Bolle C. 2004. The role of GRAS proteins in plant signal transduction and development. Planta,218(5):683–692.
Bonhomme S,Budar F,Férault M,Pelletier G. 1991. A 2.5 kb Nco I fragment of Ogura radish mitochondrial DNA is correlated with cytoplasmic male-sterility in Brassica cybrids. Curr Genet,19:121–127.
Bruce A B. 1910. The mandelian theory of heredity and augmentation of vigor. Science,32:627–628.
Chamala S,Feng G Q,Chavarro C,Barbazuk W B. 2015. Genome-wide identification of evolutionarily conserved alternative splicing events in flowering plants. Front Bioeng Biotechnol,3:33.
Chen L,Bian J M,Shi S L,Yu J F,Khanzada H,Mustafa Wassan G,Zhu C L,Luo X,Tong S,Yang X R,Peng X S,Yong S,Yu Q Y,He X P,Fu J R,Chen X R,Hu L F,Ouyang L J,He H H. 2018. Genetic analysis for the grain number heterosis of a super-hybrid rice WFYT025combination using RNA-Seq. Rice,11(1):37.
Cheverud J M,Routman E J. 1995. Epistasis and its contribution to genetic variance components. Genetics,139(3):1455–1461.
Costa V,Angelini C,DeFeis I,Ciccodicola A. 2010. Uncovering the complexity of transcriptomes with RNA-Seq. J Biomed Biotechnol,2010(5757):853916.
Dubos C,Stracke R,Grotewold E,Weisshaar B,Martin C,Lepiniec L. 2010. MYB transcription factors in Arabidopsis. Trends Plant Sci,15(10):573–581.East E M. 1936. Heterosis. Genetics,21(4):375.
Ge X M,Chen W H,Song S H,Wang W W,Hu S N,Yu J. 2008. Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9and its parental lines. BMC Plant Biol,8(1):114.
Grelon M,Budar F,Bonhomme S,Pelletier G. 1994. Ogura cytoplasmic male-sterility(CMS)-associated orf138 is translated into a mitochondrial membrane polypeptide in male-sterile Brassica hybrids. Mol Gen Genet,243:540–547.
Groszmann M,Greaves I K,Fujimoto R,James Peacock W,Dennis E S. 2013. The role of epigenetics in hybrid vigour. Trends in Genetics,29(12):684–690.
Hu X,Wang H,Diao X,Liu Z,Li K,Wu Y,Liang Q J,Wang H,Huang C L. 2016. Transcriptome profiling and comparison of maize ear heterosis during the spikelet and floret differentiation stages. BMC Genomics,17:959.
James A B,Syed N H,Bordage S,Marshall J,Gillian A,Nimmo G A,Jenkins G I,Herzyk P,Brown J W S,Nimmo H G. 2012. Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell,24:961–981.
Laloum T,Martín G,Duque P. 2017. Alternative splicing control of abiotic stress responses. Trends Plant Sci,23(2):140.
Liscum E,Reed J W. 2002. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol,49(3–4):387–400.
Lisec J,Meyer R C,Steinfath M,Redestig H,Becher M,Witucka-Wall H,Fiehn O,T?rjék O,Selbig J,Altmann T,Willmitzer L. 2008. Identification of metabolic and biomass QTL in Arabidopsis thaliana in a parallel analysis of RIL and IL populations. Plant J,53:960–972.
Liu Z S,Qin J X,Tian X J,Xu S B,Wang Y,Li H X,Wang X M,Peng H R,Yao Y Y,Hu Z R,Ni Z F,Xin M M,Sun Q X. 2018. Global profiling of alternative splicing landscape responsive to drought,heat and their combination in wheat(Triticum aestivum L.). Plant Biotechnol J,16(3):714–726.
Mao X Z,Cai T,Olyarchuk J G,Wei L P. 2005. Automated genome annotation and pathway identification using the KEGG Orthology(KO)as a controlled vocabulary. Bioinformatics,21(19):3787–3793.
Mastrangelo A M,Marone D,LaidòG,Leonardis A M E,Vita P D. 2012. Alternative splicing:enhancing ability to cope with stress via transcriptome plasticity. Plant Sci,185(4):40–49.
Minvielle F. 1987. Dominance is not necessary for heterosis:a two-locus model. Genet Res,49:245–247.
Ng M,Yanofsky M F. 2001. Function and evolution of the plant MADS-box gene family. Nature Rev Genet,2:186–195.
Olsen A N,Ernst H A,Leggio L L,Skriver K. 2005. NAC transcription factors:structurally distinct,functionally diverse. Trends Plant Sci,10(2):79–87.
Romagnoli S,Maddaloni M,Livini C,Motto M. 1990. Relationship between gene expression and hybrid vigor in primary root tips of young maize(Zea mays L.)plantlets. Theor Appl Genet,80(6):769–775.
Scascitelli M,Cognet M,Adams K L. 2010. An interspecific plant hybrid shows novel changes in parental splice forms of genes for splicing factors.Genetics,184(4):975–983.
Song G S,Zhai H L,Peng Y G,Zhang L,Wei G,Chen X Y,Xiao Y G,Wang L,Chen Y J,Wu B,Chen B,Zhang Y,Chen H,Feng X J,Gong W K,Liu Y,Yin Z J,Wang F,Liu G Z,Xu H L,Wei X L,Zhao X L,Ouwerkerk P B F,Hankemeier T,Reijmers T,Heijden R V D,Lu C M,Wang M,Greef J V D,Zhu Z. 2010. Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Mol Plant,3(6):1012–1025.
Song S H,Qu H Z,Chen C,Hu S N,Yu J. 2007. Differential gene expression in an elite hybrid rice cultivar(Oryza sativa L.)and its parental lines based on SAGE data. BMC Plant Biol,7(1):49.
Springer N M,Stupar R M. 2007. Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize. Plant Cell,19(8):2391–2402.
Stupar R M,Hermanson P J,Springer N M. 2007. Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol,145(2):411–425.
Tang W,Zheng Y,Dong J,Yu J,Yue J Y,Liu F F,Guo X H,Huang S X,Wisniewski M,Sun J Q,Niu X L,Ding J,Liu J,Fei Z J,Liu YS.2016.ComprehensivetranscriptomeprofilingrevealslongnoncodingRNAexpressionandalternativesplicingregulationduringfruit development and ripening in kiwifruit(Actinidia chinensis). Front Plant Sci,7:335.
Wang L,Greaves I K,Groszmann M,Wu L M,Dennis E S,Peacock W J. 2015. Hybrid mimics and hybrid vigor in Arabidopsis. Proc Natl Acad Sci USA,112:4959–4967.
Wei G,Tao Y,Liu G Z,Chen C,Luo R Y,Xia H A,Gan Q,Zeng H P,Lu Z K,Han Y N,Li X B,Song G S,Zhai H L,Peng Y G,Li D Y,Xu H G,Wei X L,Cao M L,Deng H F,Xin Y Y,Fu X Q,Yuan L P,Yu J,Zhu Z,Zhu L H. 2009. A transcriptomic analysis of super hybrid rice LYP9 and its parents. Proc Natl Acad Sci USA,106(19):7695–7701.
Yang H,Wang X,Wei Y,Deng Z,Liu H,Chen J S,Dai L J,Xia Z H,He G M,Li D J. 2018. Transcriptomic analyses reveal molecular mechanisms underlying growth heterosis and weakness of rubber tree seedlings. BMC Plant Biol,18(1):10.
Young M D,Wakefield M J,Smyth G K,Oshlack A. 2010. Gene ontology analysis for RNA-seq:accounting for selection bias. Genome Biol,11 (2):R14.
Yu J,Miao J,Zhang Z,Xiong H,Zhu X,Sun X,Pan Y,Liang Y,Zhang Q,Abdul R R M,Li J,Zhang H,Li Z. 2018. Alternative splicing of OsLG3b controls grain length and yield in Japonica rice. Plant Biotechnol J,16:1667–1678.
Zhai R R,Feng Y,Wang H M,Zhan X D,Shen X H,Wu W M,Zhang Y X,Chen D B,Dai G X,Yang Z L,Cao L Y,Cheng S H. 2013.Transcriptome analysis of rice root heterosis by RNA-Seq. BMC Genomics,14(1):19.
Zhang C B,Lin C J,Fu F Y,Zhong X F,Peng B,Yan H,Zhang J Y,Zhang W L,Wang P N,Ding X Y,Zhang W,Zhao L M. 2017. Comparative transcriptome analysis of flower heterosis in two soybean F1 hybrids by RNA-seq. PLoS ONE,12(7):e0181061.
Zhang H Y,He H,Chen L B,Li L,Liang M Z,Wang X F,Liu X G,He G M,Chen R S,Ma L G,Deng X W. 2008. A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol Plant,1(5):720–731.
Zhang Q S,Zhang X Q,Wang S B,Tan C,Zhou G F,Li C D. 2016. Involvement of alternative splicing in barley seed germination. PLoS ONE,11 (3):e0152824.
Zhang T F,Li B,Zhang D F,Jia G Q,Li Z Y,Wang S C. 2012. Genome-wide transcriptional analysis of yield and heterosis-associated genes in maize(Zea mays L.). J Integr Agri,11(8):1245–1256.
Adnan M,Morton G,Hadi S. 2011. Analysis of rpoS and bolA gene expression under various stress-induced environments in planktonic and biofilm phase using 2-??CT method. Mol Cell Biochem,357(1–2):275–282.
Bell G D M,Kane N C,Rieseberg L H,Adams K L. 2013. RNA-Seq analysis of allele-specific expression,hybrid effects,and regulatory divergence in hybrids compared with their parents from natural populations. Genome Biology and Evolution,5(7):1309–1323.
Berger F,Chaudhury A. 2009. Parental memories shape seeds. Trends Plant Sci,14(10):550–556.
Bolle C. 2004. The role of GRAS proteins in plant signal transduction and development. Planta,218(5):683–692.
Bonhomme S,Budar F,Férault M,Pelletier G. 1991. A 2.5 kb Nco I fragment of Ogura radish mitochondrial DNA is correlated with cytoplasmic male-sterility in Brassica cybrids. Curr Genet,19:121–127.
Bruce A B. 1910. The mandelian theory of heredity and augmentation of vigor. Science,32:627–628.
Chamala S,Feng G Q,Chavarro C,Barbazuk W B. 2015. Genome-wide identification of evolutionarily conserved alternative splicing events in flowering plants. Front Bioeng Biotechnol,3:33.
Chen L,Bian J M,Shi S L,Yu J F,Khanzada H,Mustafa Wassan G,Zhu C L,Luo X,Tong S,Yang X R,Peng X S,Yong S,Yu Q Y,He X P,Fu J R,Chen X R,Hu L F,Ouyang L J,He H H. 2018. Genetic analysis for the grain number heterosis of a super-hybrid rice WFYT025combination using RNA-Seq. Rice,11(1):37.
Cheverud J M,Routman E J. 1995. Epistasis and its contribution to genetic variance components. Genetics,139(3):1455–1461.
Costa V,Angelini C,DeFeis I,Ciccodicola A. 2010. Uncovering the complexity of transcriptomes with RNA-Seq. J Biomed Biotechnol,2010(5757):853916.
Dubos C,Stracke R,Grotewold E,Weisshaar B,Martin C,Lepiniec L. 2010. MYB transcription factors in Arabidopsis. Trends Plant Sci,15(10):573–581.East E M. 1936. Heterosis. Genetics,21(4):375.
Ge X M,Chen W H,Song S H,Wang W W,Hu S N,Yu J. 2008. Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9and its parental lines. BMC Plant Biol,8(1):114.
Grelon M,Budar F,Bonhomme S,Pelletier G. 1994. Ogura cytoplasmic male-sterility(CMS)-associated orf138 is translated into a mitochondrial membrane polypeptide in male-sterile Brassica hybrids. Mol Gen Genet,243:540–547.
Groszmann M,Greaves I K,Fujimoto R,James Peacock W,Dennis E S. 2013. The role of epigenetics in hybrid vigour. Trends in Genetics,29(12):684–690.
Hu X,Wang H,Diao X,Liu Z,Li K,Wu Y,Liang Q J,Wang H,Huang C L. 2016. Transcriptome profiling and comparison of maize ear heterosis during the spikelet and floret differentiation stages. BMC Genomics,17:959.
James A B,Syed N H,Bordage S,Marshall J,Gillian A,Nimmo G A,Jenkins G I,Herzyk P,Brown J W S,Nimmo H G. 2012. Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell,24:961–981.
Laloum T,Martín G,Duque P. 2017. Alternative splicing control of abiotic stress responses. Trends Plant Sci,23(2):140.
Liscum E,Reed J W. 2002. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol,49(3–4):387–400.
Lisec J,Meyer R C,Steinfath M,Redestig H,Becher M,Witucka-Wall H,Fiehn O,T?rjék O,Selbig J,Altmann T,Willmitzer L. 2008. Identification of metabolic and biomass QTL in Arabidopsis thaliana in a parallel analysis of RIL and IL populations. Plant J,53:960–972.
Liu Z S,Qin J X,Tian X J,Xu S B,Wang Y,Li H X,Wang X M,Peng H R,Yao Y Y,Hu Z R,Ni Z F,Xin M M,Sun Q X. 2018. Global profiling of alternative splicing landscape responsive to drought,heat and their combination in wheat(Triticum aestivum L.). Plant Biotechnol J,16(3):714–726.
Mao X Z,Cai T,Olyarchuk J G,Wei L P. 2005. Automated genome annotation and pathway identification using the KEGG Orthology(KO)as a controlled vocabulary. Bioinformatics,21(19):3787–3793.
Mastrangelo A M,Marone D,LaidòG,Leonardis A M E,Vita P D. 2012. Alternative splicing:enhancing ability to cope with stress via transcriptome plasticity. Plant Sci,185(4):40–49.
Minvielle F. 1987. Dominance is not necessary for heterosis:a two-locus model. Genet Res,49:245–247.
Ng M,Yanofsky M F. 2001. Function and evolution of the plant MADS-box gene family. Nature Rev Genet,2:186–195.
Olsen A N,Ernst H A,Leggio L L,Skriver K. 2005. NAC transcription factors:structurally distinct,functionally diverse. Trends Plant Sci,10(2):79–87.
Romagnoli S,Maddaloni M,Livini C,Motto M. 1990. Relationship between gene expression and hybrid vigor in primary root tips of young maize(Zea mays L.)plantlets. Theor Appl Genet,80(6):769–775.
Scascitelli M,Cognet M,Adams K L. 2010. An interspecific plant hybrid shows novel changes in parental splice forms of genes for splicing factors.Genetics,184(4):975–983.
Song G S,Zhai H L,Peng Y G,Zhang L,Wei G,Chen X Y,Xiao Y G,Wang L,Chen Y J,Wu B,Chen B,Zhang Y,Chen H,Feng X J,Gong W K,Liu Y,Yin Z J,Wang F,Liu G Z,Xu H L,Wei X L,Zhao X L,Ouwerkerk P B F,Hankemeier T,Reijmers T,Heijden R V D,Lu C M,Wang M,Greef J V D,Zhu Z. 2010. Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Mol Plant,3(6):1012–1025.
Song S H,Qu H Z,Chen C,Hu S N,Yu J. 2007. Differential gene expression in an elite hybrid rice cultivar(Oryza sativa L.)and its parental lines based on SAGE data. BMC Plant Biol,7(1):49.
Springer N M,Stupar R M. 2007. Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize. Plant Cell,19(8):2391–2402.
Stupar R M,Hermanson P J,Springer N M. 2007. Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol,145(2):411–425.
Tang W,Zheng Y,Dong J,Yu J,Yue J Y,Liu F F,Guo X H,Huang S X,Wisniewski M,Sun J Q,Niu X L,Ding J,Liu J,Fei Z J,Liu YS.2016.ComprehensivetranscriptomeprofilingrevealslongnoncodingRNAexpressionandalternativesplicingregulationduringfruit development and ripening in kiwifruit(Actinidia chinensis). Front Plant Sci,7:335.
Wang L,Greaves I K,Groszmann M,Wu L M,Dennis E S,Peacock W J. 2015. Hybrid mimics and hybrid vigor in Arabidopsis. Proc Natl Acad Sci USA,112:4959–4967.
Wei G,Tao Y,Liu G Z,Chen C,Luo R Y,Xia H A,Gan Q,Zeng H P,Lu Z K,Han Y N,Li X B,Song G S,Zhai H L,Peng Y G,Li D Y,Xu H G,Wei X L,Cao M L,Deng H F,Xin Y Y,Fu X Q,Yuan L P,Yu J,Zhu Z,Zhu L H. 2009. A transcriptomic analysis of super hybrid rice LYP9 and its parents. Proc Natl Acad Sci USA,106(19):7695–7701.
Yang H,Wang X,Wei Y,Deng Z,Liu H,Chen J S,Dai L J,Xia Z H,He G M,Li D J. 2018. Transcriptomic analyses reveal molecular mechanisms underlying growth heterosis and weakness of rubber tree seedlings. BMC Plant Biol,18(1):10.
Young M D,Wakefield M J,Smyth G K,Oshlack A. 2010. Gene ontology analysis for RNA-seq:accounting for selection bias. Genome Biol,11 (2):R14.
Yu J,Miao J,Zhang Z,Xiong H,Zhu X,Sun X,Pan Y,Liang Y,Zhang Q,Abdul R R M,Li J,Zhang H,Li Z. 2018. Alternative splicing of OsLG3b controls grain length and yield in Japonica rice. Plant Biotechnol J,16:1667–1678.
Zhai R R,Feng Y,Wang H M,Zhan X D,Shen X H,Wu W M,Zhang Y X,Chen D B,Dai G X,Yang Z L,Cao L Y,Cheng S H. 2013.Transcriptome analysis of rice root heterosis by RNA-Seq. BMC Genomics,14(1):19.
Zhang C B,Lin C J,Fu F Y,Zhong X F,Peng B,Yan H,Zhang J Y,Zhang W L,Wang P N,Ding X Y,Zhang W,Zhao L M. 2017. Comparative transcriptome analysis of flower heterosis in two soybean F1 hybrids by RNA-seq. PLoS ONE,12(7):e0181061.
Zhang H Y,He H,Chen L B,Li L,Liang M Z,Wang X F,Liu X G,He G M,Chen R S,Ma L G,Deng X W. 2008. A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol Plant,1(5):720–731.
Zhang Q S,Zhang X Q,Wang S B,Tan C,Zhou G F,Li C D. 2016. Involvement of alternative splicing in barley seed germination. PLoS ONE,11 (3):e0152824.
Zhang T F,Li B,Zhang D F,Jia G Q,Li Z Y,Wang S C. 2012. Genome-wide transcriptional analysis of yield and heterosis-associated genes in maize(Zea mays L.). J Integr Agri,11(8):1245–1256.