Transcriptome landscape of the early Brassica napus seed
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摘要
Brassica napus L.(canola) is one of the world's most economically important oilseeds. Despite our growing knowledge of Brassica genetics, we still know little about the genes and gene regulatory networks underlying early seed development. In this work, we use laser microdissection coupled with RNA sequencing to profile gene activity of both the maternal and filial subregions of the globular seed. We find subregions of the chalazal end including the chalazal endosperm, chalazal proliferating tissue, and chalazal seed coat, have unique transcriptome profiles associated with hormone biosynthesis and polysaccharide metabolism. We confirm that the chalazal seed coat is uniquely enriched for sucrose biosynthesis and transport, and that the chalazal endosperm may function as an important regulator of the maternal region through brassinosteroid synthesis. The chalazal proliferating tissue,a poorly understood subregion, was specifically enriched in transcripts associated with megasporogenesis and trehalose biosynthesis, suggesting this ephemeral structure plays an important role in both sporophytic development and carbon nutrient balance, respectively. Finally, compartmentalization of transcription factors and their regulatory circuits has uncovered previously unknown roles for the chalazal pole in early seed development.
Brassica napus L.(canola) is one of the world's most economically important oilseeds. Despite our growing knowledge of Brassica genetics, we still know little about the genes and gene regulatory networks underlying early seed development. In this work, we use laser microdissection coupled with RNA sequencing to profile gene activity of both the maternal and filial subregions of the globular seed. We find subregions of the chalazal end including the chalazal endosperm, chalazal proliferating tissue, and chalazal seed coat, have unique transcriptome profiles associated with hormone biosynthesis and polysaccharide metabolism. We confirm that the chalazal seed coat is uniquely enriched for sucrose biosynthesis and transport, and that the chalazal endosperm may function as an important regulator of the maternal region through brassinosteroid synthesis. The chalazal proliferating tissue,a poorly understood subregion, was specifically enriched in transcripts associated with megasporogenesis and trehalose biosynthesis, suggesting this ephemeral structure plays an important role in both sporophytic development and carbon nutrient balance, respectively. Finally, compartmentalization of transcription factors and their regulatory circuits has uncovered previously unknown roles for the chalazal pole in early seed development.
Brassica napus L.(canola) is one of the world's most economically important oilseeds. Despite our growing knowledge of Brassica genetics, we still know little about the genes and gene regulatory networks underlying early seed development. In this work, we use laser microdissection coupled with RNA sequencing to profile gene activity of both the maternal and filial subregions of the globular seed. We find subregions of the chalazal end including the chalazal endosperm, chalazal proliferating tissue, and chalazal seed coat, have unique transcriptome profiles associated with hormone biosynthesis and polysaccharide metabolism. We confirm that the chalazal seed coat is uniquely enriched for sucrose biosynthesis and transport, and that the chalazal endosperm may function as an important regulator of the maternal region through brassinosteroid synthesis. The chalazal proliferating tissue,a poorly understood subregion, was specifically enriched in transcripts associated with megasporogenesis and trehalose biosynthesis, suggesting this ephemeral structure plays an important role in both sporophytic development and carbon nutrient balance, respectively. Finally, compartmentalization of transcription factors and their regulatory circuits has uncovered previously unknown roles for the chalazal pole in early seed development.
引文
Becker MG,Walker PL,Pulgar-Vidal NC,Belmonte MF(2017)SeqEnrich:A tool to predict transcription factor networks from co-expressed Arabidopsis and Brassica napus gene sets.PLoS ONE 12:e0178256
Belmonte MF,Kirkbride RC,Stone SL,Pelletier JM,Bui AQ,Yeung EC,Hashimoto M,Fei J,Harada CM,Munoz MD,Le BH,Drews GN,Brady SM,Goldberg RB,Harada JJ(2013)Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed.Proc Natl Acad Sci USA 110:E435-44
Besnard J,Zhao C,Avice J,Vitha S,Hyodo A,Pilot G,Okumoto S(2018)Arabidopsis UMAMIT24 and 25 are amino acid exporters involved in seed loading.J Exp Bot 69:5221-5232
Bolger AM,Lohse M,Usadel B(2014)Trimmomatic:A flexible trimmer for Illumina sequence data.Bioinformatics 30:2114-20
Brown RC,Lemmon BE,Nguyen H(2004)Comparative anatomy of the chalazal endosperm cyst in seeds of the Brassicaceae.Bot J Linn Soc 144:375-394
Chalhoub B,Denoeud F,Liu S,Parkin IAP,Tang H,Wang X,Chiquet J,Belcram H,Tong C,Samans B,Correa M,Silva D,Just J,Falentin C,Koh CS,Le Clainche I,Bernard M,Bento P,Noel B,Labadie K,Alberti A,Charles M,Arnaud D,Guo H,Daviaud C,Alamery S,Jabbari K,Zhao M,Edger PP,Chelaifa H,Tack D,Lassalle G,Mestiri I,Schnel N,Le Paslier MC,Fan G,Renault V,Bayer PE,Golicz AA,Manoli S,Lee TH,Thi VH,Chalabi S,Hu Q,Tollenaere R,Lu Y,Battail C,Shen J,Sidebottom CH,Wang X,Canaguier A,Chauveau A,Berard A,Deniot G,Guan M,Liu Z,Sun F,Lim YP,Lyons E,Town CD,Bancroft I,Wang X,Meng J,Ma J,Pires JC,King GJ,Brunel D,Delourme R,Renard M,Aury JM,Adams KL,Batley J,Snowdon RJ,Tost J,Edwards D,Zhou Y,Hua W,Sharpe AG,Paterson AH,Guan C,Wincker P(2014)Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome.Science 345:950-953
Chan A,Belmonte M(2013)Histological and ultrastructural changes in canola(Brassica napus)funicular anatomy during the seed lifecycle.Botany 91:671-679
Chan AC,Khan D,Girard IJ,Becker MG,Millar JL,Sytnik D,Belmonte MF(2016)Tissue-specific laser microdissection of the Brassica napus funiculus improves gene discovery and spatial identification of biological processes.J Exp Bot67:3561-71
Chen LQ,Lin IW,Qu XQ,Sosso D,McFarlane HE,Londo?o A,Samuels AL,Frommer WB(2015)A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo.Plant Cell 27:607-619
Debeaujon I,Nesi N,Perez P,Devic M,Grandjean O,Caboche M,Lepiniec L(2003)Proanthocyanidin-accumulating cells in Arabidopsis testa:Regulation of differentiation and role in seed development.Plant Cell 15:2514-2531
Eastmond PJ,van Dijken AJH,Spielman M,Kerr A,Tissier AF,Dickinson HG,Jones JDG,Smeekens SC,Graham IA(2002)Trehalose-6-phosphate synthase 1,which catalyses the first step in trehalose synthesis,is essential for Arabidopsis embryo maturation.Plant J 29:225-235
Ehlers K,Bhide AS,Tekleyohans DG,Wittkop B,Snowdon RJ,Becker A(2016)The MADS box genes ABS,SHP1,and SHP2are essential for the coordination of cell divisions in ovule and seed coat development and for endosperm formation in Arabidopsis thaliana.PLoS ONE 11:e0165075
FAOSTAT(2014)Available from:http://www.fao.org/faostat/en/#compare
Figueroa CM,Lunn JE(2016)A tale of two sugars:Trehalose6-phosphate and sucrose.Plant Physiol 172:7-27
Fore SR,Porter P,Lazarus W(2011)Net energy balance of small-scale on-farm biodiesel production from canola and soybean.Biomass Bioenerg 35:2234-2244
Galili T,O’Callaghan A,Sidi J,Sievert C(2018)Heatmaply:An Rpackage for creating interactive cluster heatmaps for online publishing.Bioinformatics 34:1600-1602
Goff LA,Trapnell C,Kelley D(2012)CummeRbund:Visualization and exploration of Cufflinks high-throughput sequencing data.R Packag.Version 2.2
Ikeda M,Fujiwara S,Mitsuda N,Ohme-Takagi M(2012)A triagnostic basic helix-loop-helix system regulates cell elongation in Arabidopsis.Plant Cell 24:4483-4497
Jiang WB,Huang HY,Hu YW,Zhu SW,Wang ZY,Lin WH(2013)Brassinosteroid regulates seed size and shape in Arabidopsis.Plant Physiol 162:1965-77
Khan D,Millar JL,Girard IJ,Belmonte MF(2014)Transcriptional circuitry underlying seed coat development in Arabidopsis.Plant Sci 219-220:51-60
Khan D,Millar JL,Girard IJ,Chan A,Kirkbride RC,Pelletier JM,Kost S,Becker MG,Yeung EC,Stasolla C,Goldberg RB,Harada JJ,Belmonte MF(2015)Transcriptome atlas of the Arabidopsis funiculus:A study of maternal seed subregions.Plant J 82:41-53
Kim D,Langmead B,Salzberg SL(2015)HISAT:A fast spliced aligner with low memory requirements.Nat Methods 12:357-360
Kirik V,Simon M,Huelskamp M,Schiefelbein J(2003)The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis.Dev Biol 268:506-513
Klepikova AV,Kasianov AS,Gerasimov ES,Logacheva MD,Penin AA(2016)A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling.Plant J 88:1058-1070
Kumar R,Ichihashi Y,Kimura S,Chitwood DH,Headland LR,Peng J,Maloof JN,Sinha NR(2012)A high-throughput method for Illumina RNA-seq library preparation.Front Plant Sci 3:1-10
Luo M,Dennis E(2005)MINISEED3(MIN3),a WRKY family gene,and HAIKU2(IKU2),a Leucine-Rich Repeat(LRR)KINASEgene,are regulators of seed size in Arabidopsis.Proc Natl Acad Sci USA 102:17531-17536
Millar JL,Khan D,Becker MG,Chan A,Dufresne A,Sumner M,Belmonte MF(2015)Chalazal seed coat development in Brassica napus.Plant Sci 241:45-54
Mizzotti C,Mendes MA,Caporali E,Schnittger A,Kater MM,Battaglia R,Colombo L(2012)The MADS box genes SEEDSTICK and ARABIDOPSIS Bsisterplay a maternal role in fertilization and seed development.Plant J 70:409-420
Nguyen H,Brown RC,Lemmon BE(2000)The specialized chalazal endosperm in Arabidopsis thaliana and Lepidium virginicum(Brassicaceae).Protoplasma 212:99-110
Park JS,Kim JB,Cho KJ,Cheon CI,Sung MK,Choung MG,Roh KH(2008)Arabidopsis R2R3-MYB transcription factor AtMYB60 functions as a transcriptional repressor of anthocyanin biosynthesis in lettuce(Lactuca sativa).Plant Cell Rep 27:985-994
Pesch M,Dartan B,Birkenbihl R,Somssich IE,Hülskamp M(2014)Arabidopsis TTG2 regulates TRY expression through enhancement of activator complex-triggered activation.Plant Cell 26:4067-4083
Pesch M,Hülskamp M(2011)Role of TRIPTYCHON in trichome patterning in Arabidopsis.BMC Plant Biol 11:130
Rahman H(2013)Review:Breeding spring canola(Brassica napus L.)by the use of exotic germplasm.Can J Plant Sci93:363-373
Schon MA,Nodine MD(2017)Widespread contamination of Arabidopsis embryo and endosperm transcriptome data sets.Plant Cell 29:608-617
Schulz P,Jensen WA(1971)Capsella embryogenesis:The chalazal proliferating tissue.J Cell Sci 8:201-27
Schulz P,Jensen WA,Jensen WA(1974)Capsella embryogenesis:The development of free nuclear endosperm.Protoplasma 80:183-205
Shannon P,Markiel A,Ozier O,Baliga NS,Wang JT,Ramage D,Amin N,Schwikowski B,Ideker T(2003)Cytoscape:A software environment for integrated models of biomolecular interaction networks.Genome Res 13:2498-2504
Tapia-Lopez R,Garc?a-Ponce B,Dubrovsky JG,Garay-Arroyo A,Perez-Ru?z R V,Kim S-H,Acevedo F,Pelaz S,Alvarez-Buylla ER(2008)An AGAMOUS-related MADS-box gene,XAL1(AGL12),regulates root meristem cell proliferation and flowering transition in Arabidopsis.Plant Physiol 146:1182-1192
Tominaga R,Iwata M,Sano R,Inoue K,Okada K,Wada T(2008)Arabidopsis CAPRICE-LIKE MYB 3(CPL3)controls endoreduplication and flowering development in addition to trichome and root hair formation.Development 135:1335-1345
Trapnell C,Williams BA,Pertea G,Mortazavi A,Kwan G,van Baren MJ,Salzberg SL,Wold BJ,Pachter L(2010)Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.Nat Biotechnol 28:511-515
Vandesteene L,Ramon M,Le Roy K,Van Dijck P,Rolland F(2010)A single active trehalose-6-P synthase(TPS)and a family of putative regulatory TPS-like proteins in Arabidopsis.Mol Plant 3:406-419
Vogiatzaki E,Baroux C,Jung JY,Poirier Y(2017)PHO1 exports phosphate from the chalazal seed coat to the embryo in developing Arabidopsis seeds.Curr Biol 27:2893-2900.e3
Wang Z,Chen M,Chen T,Xuan L,Li Z,Du X,Zhou L,Zhang G,Jiang L(2014)TRANSPARENT TESTA2 regulates embryonic fatty acid biosynthesis by targeting FUSCA3 during the early developmental stage of Arabidopsis seeds.Plant J 77:757-769
Wilkinson L(2011)ggplot2:Elegant graphics for data analysis by WICKHAM,H.Biometrics 67:678-679
Zheng Q,Perry SE(2014)Alterations in the transcriptome of soybean in response to enhanced somatic embryogenesis promoted by orthologs of AGAMOUS-Like15 and AGAMOUS-Like18.Plant Physiol 164:1365-77
Belmonte MF,Kirkbride RC,Stone SL,Pelletier JM,Bui AQ,Yeung EC,Hashimoto M,Fei J,Harada CM,Munoz MD,Le BH,Drews GN,Brady SM,Goldberg RB,Harada JJ(2013)Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed.Proc Natl Acad Sci USA 110:E435-44
Besnard J,Zhao C,Avice J,Vitha S,Hyodo A,Pilot G,Okumoto S(2018)Arabidopsis UMAMIT24 and 25 are amino acid exporters involved in seed loading.J Exp Bot 69:5221-5232
Bolger AM,Lohse M,Usadel B(2014)Trimmomatic:A flexible trimmer for Illumina sequence data.Bioinformatics 30:2114-20
Brown RC,Lemmon BE,Nguyen H(2004)Comparative anatomy of the chalazal endosperm cyst in seeds of the Brassicaceae.Bot J Linn Soc 144:375-394
Chalhoub B,Denoeud F,Liu S,Parkin IAP,Tang H,Wang X,Chiquet J,Belcram H,Tong C,Samans B,Correa M,Silva D,Just J,Falentin C,Koh CS,Le Clainche I,Bernard M,Bento P,Noel B,Labadie K,Alberti A,Charles M,Arnaud D,Guo H,Daviaud C,Alamery S,Jabbari K,Zhao M,Edger PP,Chelaifa H,Tack D,Lassalle G,Mestiri I,Schnel N,Le Paslier MC,Fan G,Renault V,Bayer PE,Golicz AA,Manoli S,Lee TH,Thi VH,Chalabi S,Hu Q,Tollenaere R,Lu Y,Battail C,Shen J,Sidebottom CH,Wang X,Canaguier A,Chauveau A,Berard A,Deniot G,Guan M,Liu Z,Sun F,Lim YP,Lyons E,Town CD,Bancroft I,Wang X,Meng J,Ma J,Pires JC,King GJ,Brunel D,Delourme R,Renard M,Aury JM,Adams KL,Batley J,Snowdon RJ,Tost J,Edwards D,Zhou Y,Hua W,Sharpe AG,Paterson AH,Guan C,Wincker P(2014)Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome.Science 345:950-953
Chan A,Belmonte M(2013)Histological and ultrastructural changes in canola(Brassica napus)funicular anatomy during the seed lifecycle.Botany 91:671-679
Chan AC,Khan D,Girard IJ,Becker MG,Millar JL,Sytnik D,Belmonte MF(2016)Tissue-specific laser microdissection of the Brassica napus funiculus improves gene discovery and spatial identification of biological processes.J Exp Bot67:3561-71
Chen LQ,Lin IW,Qu XQ,Sosso D,McFarlane HE,Londo?o A,Samuels AL,Frommer WB(2015)A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo.Plant Cell 27:607-619
Debeaujon I,Nesi N,Perez P,Devic M,Grandjean O,Caboche M,Lepiniec L(2003)Proanthocyanidin-accumulating cells in Arabidopsis testa:Regulation of differentiation and role in seed development.Plant Cell 15:2514-2531
Eastmond PJ,van Dijken AJH,Spielman M,Kerr A,Tissier AF,Dickinson HG,Jones JDG,Smeekens SC,Graham IA(2002)Trehalose-6-phosphate synthase 1,which catalyses the first step in trehalose synthesis,is essential for Arabidopsis embryo maturation.Plant J 29:225-235
Ehlers K,Bhide AS,Tekleyohans DG,Wittkop B,Snowdon RJ,Becker A(2016)The MADS box genes ABS,SHP1,and SHP2are essential for the coordination of cell divisions in ovule and seed coat development and for endosperm formation in Arabidopsis thaliana.PLoS ONE 11:e0165075
FAOSTAT(2014)Available from:http://www.fao.org/faostat/en/#compare
Figueroa CM,Lunn JE(2016)A tale of two sugars:Trehalose6-phosphate and sucrose.Plant Physiol 172:7-27
Fore SR,Porter P,Lazarus W(2011)Net energy balance of small-scale on-farm biodiesel production from canola and soybean.Biomass Bioenerg 35:2234-2244
Galili T,O’Callaghan A,Sidi J,Sievert C(2018)Heatmaply:An Rpackage for creating interactive cluster heatmaps for online publishing.Bioinformatics 34:1600-1602
Goff LA,Trapnell C,Kelley D(2012)CummeRbund:Visualization and exploration of Cufflinks high-throughput sequencing data.R Packag.Version 2.2
Ikeda M,Fujiwara S,Mitsuda N,Ohme-Takagi M(2012)A triagnostic basic helix-loop-helix system regulates cell elongation in Arabidopsis.Plant Cell 24:4483-4497
Jiang WB,Huang HY,Hu YW,Zhu SW,Wang ZY,Lin WH(2013)Brassinosteroid regulates seed size and shape in Arabidopsis.Plant Physiol 162:1965-77
Khan D,Millar JL,Girard IJ,Belmonte MF(2014)Transcriptional circuitry underlying seed coat development in Arabidopsis.Plant Sci 219-220:51-60
Khan D,Millar JL,Girard IJ,Chan A,Kirkbride RC,Pelletier JM,Kost S,Becker MG,Yeung EC,Stasolla C,Goldberg RB,Harada JJ,Belmonte MF(2015)Transcriptome atlas of the Arabidopsis funiculus:A study of maternal seed subregions.Plant J 82:41-53
Kim D,Langmead B,Salzberg SL(2015)HISAT:A fast spliced aligner with low memory requirements.Nat Methods 12:357-360
Kirik V,Simon M,Huelskamp M,Schiefelbein J(2003)The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis.Dev Biol 268:506-513
Klepikova AV,Kasianov AS,Gerasimov ES,Logacheva MD,Penin AA(2016)A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling.Plant J 88:1058-1070
Kumar R,Ichihashi Y,Kimura S,Chitwood DH,Headland LR,Peng J,Maloof JN,Sinha NR(2012)A high-throughput method for Illumina RNA-seq library preparation.Front Plant Sci 3:1-10
Luo M,Dennis E(2005)MINISEED3(MIN3),a WRKY family gene,and HAIKU2(IKU2),a Leucine-Rich Repeat(LRR)KINASEgene,are regulators of seed size in Arabidopsis.Proc Natl Acad Sci USA 102:17531-17536
Millar JL,Khan D,Becker MG,Chan A,Dufresne A,Sumner M,Belmonte MF(2015)Chalazal seed coat development in Brassica napus.Plant Sci 241:45-54
Mizzotti C,Mendes MA,Caporali E,Schnittger A,Kater MM,Battaglia R,Colombo L(2012)The MADS box genes SEEDSTICK and ARABIDOPSIS Bsisterplay a maternal role in fertilization and seed development.Plant J 70:409-420
Nguyen H,Brown RC,Lemmon BE(2000)The specialized chalazal endosperm in Arabidopsis thaliana and Lepidium virginicum(Brassicaceae).Protoplasma 212:99-110
Park JS,Kim JB,Cho KJ,Cheon CI,Sung MK,Choung MG,Roh KH(2008)Arabidopsis R2R3-MYB transcription factor AtMYB60 functions as a transcriptional repressor of anthocyanin biosynthesis in lettuce(Lactuca sativa).Plant Cell Rep 27:985-994
Pesch M,Dartan B,Birkenbihl R,Somssich IE,Hülskamp M(2014)Arabidopsis TTG2 regulates TRY expression through enhancement of activator complex-triggered activation.Plant Cell 26:4067-4083
Pesch M,Hülskamp M(2011)Role of TRIPTYCHON in trichome patterning in Arabidopsis.BMC Plant Biol 11:130
Rahman H(2013)Review:Breeding spring canola(Brassica napus L.)by the use of exotic germplasm.Can J Plant Sci93:363-373
Schon MA,Nodine MD(2017)Widespread contamination of Arabidopsis embryo and endosperm transcriptome data sets.Plant Cell 29:608-617
Schulz P,Jensen WA(1971)Capsella embryogenesis:The chalazal proliferating tissue.J Cell Sci 8:201-27
Schulz P,Jensen WA,Jensen WA(1974)Capsella embryogenesis:The development of free nuclear endosperm.Protoplasma 80:183-205
Shannon P,Markiel A,Ozier O,Baliga NS,Wang JT,Ramage D,Amin N,Schwikowski B,Ideker T(2003)Cytoscape:A software environment for integrated models of biomolecular interaction networks.Genome Res 13:2498-2504
Tapia-Lopez R,Garc?a-Ponce B,Dubrovsky JG,Garay-Arroyo A,Perez-Ru?z R V,Kim S-H,Acevedo F,Pelaz S,Alvarez-Buylla ER(2008)An AGAMOUS-related MADS-box gene,XAL1(AGL12),regulates root meristem cell proliferation and flowering transition in Arabidopsis.Plant Physiol 146:1182-1192
Tominaga R,Iwata M,Sano R,Inoue K,Okada K,Wada T(2008)Arabidopsis CAPRICE-LIKE MYB 3(CPL3)controls endoreduplication and flowering development in addition to trichome and root hair formation.Development 135:1335-1345
Trapnell C,Williams BA,Pertea G,Mortazavi A,Kwan G,van Baren MJ,Salzberg SL,Wold BJ,Pachter L(2010)Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.Nat Biotechnol 28:511-515
Vandesteene L,Ramon M,Le Roy K,Van Dijck P,Rolland F(2010)A single active trehalose-6-P synthase(TPS)and a family of putative regulatory TPS-like proteins in Arabidopsis.Mol Plant 3:406-419
Vogiatzaki E,Baroux C,Jung JY,Poirier Y(2017)PHO1 exports phosphate from the chalazal seed coat to the embryo in developing Arabidopsis seeds.Curr Biol 27:2893-2900.e3
Wang Z,Chen M,Chen T,Xuan L,Li Z,Du X,Zhou L,Zhang G,Jiang L(2014)TRANSPARENT TESTA2 regulates embryonic fatty acid biosynthesis by targeting FUSCA3 during the early developmental stage of Arabidopsis seeds.Plant J 77:757-769
Wilkinson L(2011)ggplot2:Elegant graphics for data analysis by WICKHAM,H.Biometrics 67:678-679
Zheng Q,Perry SE(2014)Alterations in the transcriptome of soybean in response to enhanced somatic embryogenesis promoted by orthologs of AGAMOUS-Like15 and AGAMOUS-Like18.Plant Physiol 164:1365-77
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