Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination

Wen-Yu Liu, Yao-Ming Chang, Chun-Chang Chen, Chen-Hua Lu, Yeh-Hwa Wu, Mei-Yeh Lu, Di-Rong Chen, Chun-Chieh Shih, Chiou-Rong Sheue, Hsuan-Cheng Huang, Chun-Ping Yu, Hsin-Hung Lin, Shin-Han Shiu, Mauricesb Ku, Wen-Hsiung Li

Research output: Contribution to journalArticle

41 Citations (Scopus)

Abstract

Our anatomical analysis revealed that a dry maize seed contains four to five embryonic leaves at different developmental stages. Rudimentary kranz structure (KS) is apparent in the first leaf with a substantial density, but its density decreases toward younger leaves. Upon imbibition, leaf expansion occurs rapidly with new KSs initiated from the palisade-like ground meristem cells in the middle of the leaf. In parallel to the anatomical analysis, we obtained the time course transcriptomes for the embryonic leaves in dry and imbibed seeds every 6 h up to hour 72. Over this time course, the embryonic leaves exhibit transcripts of 30,255 genes at a level that can be regarded as "expressed." In dry seeds, ∼25,500 genes are expressed, showing functional enrichment in transcription, RNA processing, protein synthesis, primary metabolic pathways, and calcium transport. During the 72-h time course, ∼13,900 genes, including 590 transcription factor genes, are differentially expressed. Indeed, by 30 h postimbibition, ∼2,200 genes expressed in dry seeds are already down-regulated, and ∼2,000 are upregulated. Moreover, the top 1% expressed genes at 54 h or later are very different from those before 30 h, reflecting important developmental and physiological transitions. Interestingly, clusters of genes involved in hormone metabolism, signaling, and responses are differentially expressed at various time points and TF gene expression is also modular and stage specific. Our dataset provides an opportunity for hypothesizing the timing of regulatory actions, particularly in the context of KS development.
Original languageEnglish
Pages (from-to)3979-3984
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number10
DOIs
Publication statusPublished - 2013
Externally publishedYes

Fingerprint

seed germination
corn
leaves
genes
seeds
hormone metabolism
imbibition
leaf development
multigene family
meristems
transcriptome
biochemical pathways
transcription factors
transcription (genetics)
protein synthesis
developmental stages
RNA
calcium
gene expression
cells

Keywords

  • Gene expression profiling
  • Plant hormones
  • Plant leaf development
  • deetiolated 2 protein
  • gibberellin a1
  • senescence related gene 1 protein
  • transcription factor
  • ubiquitin protein ligase E3
  • unclassified drug
  • article
  • calcium transport
  • down regulation
  • gene expression profiling
  • genetic transcription
  • germination
  • maize
  • meristem
  • plant growth
  • plant leaf
  • priority journal
  • protein synthesis
  • RNA processing
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Germination
  • Plant Growth Regulators
  • Plant Leaves
  • Plant Proteins
  • RNA, Plant
  • Seeds
  • Transcription Factors
  • Zea mays

Cite this

Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination. / Liu, Wen-Yu; Chang, Yao-Ming; Chen, Chun-Chang; Lu, Chen-Hua; Wu, Yeh-Hwa; Lu, Mei-Yeh; Chen, Di-Rong; Shih, Chun-Chieh; Sheue, Chiou-Rong; Huang, Hsuan-Cheng; Yu, Chun-Ping; Lin, Hsin-Hung; Shiu, Shin-Han; Ku, Mauricesb; Li, Wen-Hsiung.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, No. 10, 2013, p. 3979-3984.

Research output: Contribution to journalArticle

Liu, W-Y, Chang, Y-M, Chen, C-C, Lu, C-H, Wu, Y-H, Lu, M-Y, Chen, D-R, Shih, C-C, Sheue, C-R, Huang, H-C, Yu, C-P, Lin, H-H, Shiu, S-H, Ku, M & Li, W-H 2013, 'Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination', Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 10, pp. 3979-3984. https://doi.org/10.1073/pnas.1301009110
Liu, Wen-Yu ; Chang, Yao-Ming ; Chen, Chun-Chang ; Lu, Chen-Hua ; Wu, Yeh-Hwa ; Lu, Mei-Yeh ; Chen, Di-Rong ; Shih, Chun-Chieh ; Sheue, Chiou-Rong ; Huang, Hsuan-Cheng ; Yu, Chun-Ping ; Lin, Hsin-Hung ; Shiu, Shin-Han ; Ku, Mauricesb ; Li, Wen-Hsiung. / Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination. In: Proceedings of the National Academy of Sciences of the United States of America. 2013 ; Vol. 110, No. 10. pp. 3979-3984.
@article{b4ad659467df457cab031e33fe57f1e3,
title = "Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination",
abstract = "Our anatomical analysis revealed that a dry maize seed contains four to five embryonic leaves at different developmental stages. Rudimentary kranz structure (KS) is apparent in the first leaf with a substantial density, but its density decreases toward younger leaves. Upon imbibition, leaf expansion occurs rapidly with new KSs initiated from the palisade-like ground meristem cells in the middle of the leaf. In parallel to the anatomical analysis, we obtained the time course transcriptomes for the embryonic leaves in dry and imbibed seeds every 6 h up to hour 72. Over this time course, the embryonic leaves exhibit transcripts of 30,255 genes at a level that can be regarded as {"}expressed.{"} In dry seeds, ∼25,500 genes are expressed, showing functional enrichment in transcription, RNA processing, protein synthesis, primary metabolic pathways, and calcium transport. During the 72-h time course, ∼13,900 genes, including 590 transcription factor genes, are differentially expressed. Indeed, by 30 h postimbibition, ∼2,200 genes expressed in dry seeds are already down-regulated, and ∼2,000 are upregulated. Moreover, the top 1{\%} expressed genes at 54 h or later are very different from those before 30 h, reflecting important developmental and physiological transitions. Interestingly, clusters of genes involved in hormone metabolism, signaling, and responses are differentially expressed at various time points and TF gene expression is also modular and stage specific. Our dataset provides an opportunity for hypothesizing the timing of regulatory actions, particularly in the context of KS development.",
keywords = "Gene expression profiling, Plant hormones, Plant leaf development, deetiolated 2 protein, gibberellin a1, senescence related gene 1 protein, transcription factor, ubiquitin protein ligase E3, unclassified drug, article, calcium transport, down regulation, gene expression profiling, genetic transcription, germination, maize, meristem, plant growth, plant leaf, priority journal, protein synthesis, RNA processing, Gene Expression Profiling, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Genes, Plant, Germination, Plant Growth Regulators, Plant Leaves, Plant Proteins, RNA, Plant, Seeds, Transcription Factors, Zea mays",
author = "Wen-Yu Liu and Yao-Ming Chang and Chun-Chang Chen and Chen-Hua Lu and Yeh-Hwa Wu and Mei-Yeh Lu and Di-Rong Chen and Chun-Chieh Shih and Chiou-Rong Sheue and Hsuan-Cheng Huang and Chun-Ping Yu and Hsin-Hung Lin and Shin-Han Shiu and Mauricesb Ku and Wen-Hsiung Li",
note = "被引用次數:11 Export Date: 21 March 2016 CODEN: PNASA 通訊地址: Shiu, S.-H.; Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan; 電子郵件: shius@msu.edu 化學物質/CAS: gibberellin a1, 545-97-1; Plant Growth Regulators; Plant Proteins; RNA, Plant; Transcription Factors 參考文獻: Li, P., The developmental dynamics of the maize leaf transcriptome (2010) Nat Genet, 42 (12), pp. 1060-1067; Bosabalidis, A.M., Evert, R.F., Russin, W.A., Ontogeny of the vascular bundles and contiguous tissues in the maize leaf blade (1994) Am J Bot, 81 (6), pp. 745-752; Zhang, H., PlantTFDB 2.0: Update and improvement of the comprehensive plant transcription factor database (2011) Nucleic Acids Res, 39, pp. D1114-D1117. , Database issue; Pandey, G.K., The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis (2004) Plant Cell, 16 (7), pp. 1912-1924; Stiefel, V., Expression of a maize cell wall hydroxyproline-rich glycoprotein gene in early leaf and root vascular differentiation (1990) Plant Cell, 2 (8), pp. 785-793; Baier, M., Dietz, K.J., The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: Its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants (1997) Plant J, 12 (1), pp. 179-190; Clouse, S.D., Sasse, J.M., BRASSINOSTEROIDS: Essential regulators of plant growth and development (1998) Annu Rev Plant Physiol Plant Mol Biol, 49, pp. 427-451; Ca{\~n}o-Delgado, A., BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis (2004) Development, 131 (21), pp. 5341-5351; Bowman, J.L., Eshed, Y., Formation and maintenance of the shoot apical meristem (2000) Trends Plant Sci, 5 (3), pp. 110-115; Bewley, J.D., Seed germination and dormancy (1997) Plant Cell, 9 (7), pp. 1055-1066; Bentsink, L., Koornneef, M., Seed dormancy and germination (2008) Arabidopsis Book, 6, pp. e0119; Hua, Z., Vierstra, R.D., The cullin-RING ubiquitin-protein ligases (2011) Annu Rev Plant Biol, 62, pp. 299-334; Finkelstein, R., Reeves, W., Ariizumi, T., Steber, C., Molecular aspects of seed dormancy (2008) Annu Rev Plant Biol, 59, pp. 387-415; Yoshida, T., AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation (2010) Plant J, 61 (4), pp. 672-685; Greenboim-Wainberg, Y., Cross talk between gibberellin and cytokinin: The Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling (2005) Plant Cell, 17 (1), pp. 92-102; Hej{\'a}tko, J., The histidine kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots (2009) Plant Cell, 21 (7), pp. 2008-2021; Sauer, M., Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity (2006) Genes Dev, 20 (20), pp. 2902-2911; Manfre, A.J., Lanni, L.M., Marcotte Jr., W.R., The Arabidopsis group 1 LATE EMBRYOGENESIS ABUNDANT protein ATEM6 is required for normal seed development (2006) Plant Physiol, 140 (1), pp. 140-149; Mccarty, D.R., The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator (1991) Cell, 66 (5), pp. 895-905; Pysh, L.D., Aukerman, M.J., Schmidt, R.J., OHP1: A maize basic domain/leucine zipper protein that interacts with opaque2 (1993) Plant Cell, 5 (2), pp. 227-236; Candela, H., Johnston, R., Gerhold, A., Foster, T., Hake, S., The milkweed pod1 gene encodes a KANADI protein that is required for abaxial/adaxial patterning in maize leaves (2008) Plant Cell, 20 (8), pp. 2073-2087; Hall, L.N., Rossini, L., Cribb, L., Langdale, J.A., GOLDEN 2: A novel transcriptional regulator of cellular differentiation in the maize leaf (1998) Plant Cell, 10 (6), pp. 925-936; Rossini, L., Cribb, L., Martin, D.J., Langdale, J.A., The maize golden2 gene defines a novel class of transcriptional regulators in plants (2001) Plant Cell, 13 (5), pp. 1231-1244; Bomblies, K., Doebley, J.F., Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication (2006) Genetics, 172 (1), pp. 519-531; Zhou, J., Sebastian, J., Lee, J.Y., Signaling and gene regulatory programs in plant vascular stem cells (2011) Genesis, 49 (12), pp. 885-904; Lau, S., De Smet, I., Kolb, M., Meinhardt, H., J{\"u}rgens, G., Auxin triggers a genetic switch (2011) Nat Cell Biol, 13 (5), pp. 611-615; Weijers, D., Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis (2006) Dev Cell, 10 (2), pp. 265-270; Trapnell, C., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks (2012) Nat Protoc, 7 (3), pp. 562-578; Tarazona, S., Garc{\'i}a-Alcalde, F., Dopazo, J., Ferrer, A., Conesa, A., Differential expression in RNA-seq: A matter of depth (2011) Genome Res, 21 (12), pp. 2213-2223; Thimm, O., MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes (2004) Plant J, 37 (6), pp. 914-939",
year = "2013",
doi = "10.1073/pnas.1301009110",
language = "English",
volume = "110",
pages = "3979--3984",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "National Academy of Sciences",
number = "10",

}

TY - JOUR

T1 - Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination

AU - Liu, Wen-Yu

AU - Chang, Yao-Ming

AU - Chen, Chun-Chang

AU - Lu, Chen-Hua

AU - Wu, Yeh-Hwa

AU - Lu, Mei-Yeh

AU - Chen, Di-Rong

AU - Shih, Chun-Chieh

AU - Sheue, Chiou-Rong

AU - Huang, Hsuan-Cheng

AU - Yu, Chun-Ping

AU - Lin, Hsin-Hung

AU - Shiu, Shin-Han

AU - Ku, Mauricesb

AU - Li, Wen-Hsiung

N1 - 被引用次數:11 Export Date: 21 March 2016 CODEN: PNASA 通訊地址: Shiu, S.-H.; Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan; 電子郵件: shius@msu.edu 化學物質/CAS: gibberellin a1, 545-97-1; Plant Growth Regulators; Plant Proteins; RNA, Plant; Transcription Factors 參考文獻: Li, P., The developmental dynamics of the maize leaf transcriptome (2010) Nat Genet, 42 (12), pp. 1060-1067; Bosabalidis, A.M., Evert, R.F., Russin, W.A., Ontogeny of the vascular bundles and contiguous tissues in the maize leaf blade (1994) Am J Bot, 81 (6), pp. 745-752; Zhang, H., PlantTFDB 2.0: Update and improvement of the comprehensive plant transcription factor database (2011) Nucleic Acids Res, 39, pp. D1114-D1117. , Database issue; Pandey, G.K., The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis (2004) Plant Cell, 16 (7), pp. 1912-1924; Stiefel, V., Expression of a maize cell wall hydroxyproline-rich glycoprotein gene in early leaf and root vascular differentiation (1990) Plant Cell, 2 (8), pp. 785-793; Baier, M., Dietz, K.J., The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: Its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants (1997) Plant J, 12 (1), pp. 179-190; Clouse, S.D., Sasse, J.M., BRASSINOSTEROIDS: Essential regulators of plant growth and development (1998) Annu Rev Plant Physiol Plant Mol Biol, 49, pp. 427-451; Caño-Delgado, A., BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis (2004) Development, 131 (21), pp. 5341-5351; Bowman, J.L., Eshed, Y., Formation and maintenance of the shoot apical meristem (2000) Trends Plant Sci, 5 (3), pp. 110-115; Bewley, J.D., Seed germination and dormancy (1997) Plant Cell, 9 (7), pp. 1055-1066; Bentsink, L., Koornneef, M., Seed dormancy and germination (2008) Arabidopsis Book, 6, pp. e0119; Hua, Z., Vierstra, R.D., The cullin-RING ubiquitin-protein ligases (2011) Annu Rev Plant Biol, 62, pp. 299-334; Finkelstein, R., Reeves, W., Ariizumi, T., Steber, C., Molecular aspects of seed dormancy (2008) Annu Rev Plant Biol, 59, pp. 387-415; Yoshida, T., AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation (2010) Plant J, 61 (4), pp. 672-685; Greenboim-Wainberg, Y., Cross talk between gibberellin and cytokinin: The Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling (2005) Plant Cell, 17 (1), pp. 92-102; Hejátko, J., The histidine kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots (2009) Plant Cell, 21 (7), pp. 2008-2021; Sauer, M., Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity (2006) Genes Dev, 20 (20), pp. 2902-2911; Manfre, A.J., Lanni, L.M., Marcotte Jr., W.R., The Arabidopsis group 1 LATE EMBRYOGENESIS ABUNDANT protein ATEM6 is required for normal seed development (2006) Plant Physiol, 140 (1), pp. 140-149; Mccarty, D.R., The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator (1991) Cell, 66 (5), pp. 895-905; Pysh, L.D., Aukerman, M.J., Schmidt, R.J., OHP1: A maize basic domain/leucine zipper protein that interacts with opaque2 (1993) Plant Cell, 5 (2), pp. 227-236; Candela, H., Johnston, R., Gerhold, A., Foster, T., Hake, S., The milkweed pod1 gene encodes a KANADI protein that is required for abaxial/adaxial patterning in maize leaves (2008) Plant Cell, 20 (8), pp. 2073-2087; Hall, L.N., Rossini, L., Cribb, L., Langdale, J.A., GOLDEN 2: A novel transcriptional regulator of cellular differentiation in the maize leaf (1998) Plant Cell, 10 (6), pp. 925-936; Rossini, L., Cribb, L., Martin, D.J., Langdale, J.A., The maize golden2 gene defines a novel class of transcriptional regulators in plants (2001) Plant Cell, 13 (5), pp. 1231-1244; Bomblies, K., Doebley, J.F., Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication (2006) Genetics, 172 (1), pp. 519-531; Zhou, J., Sebastian, J., Lee, J.Y., Signaling and gene regulatory programs in plant vascular stem cells (2011) Genesis, 49 (12), pp. 885-904; Lau, S., De Smet, I., Kolb, M., Meinhardt, H., Jürgens, G., Auxin triggers a genetic switch (2011) Nat Cell Biol, 13 (5), pp. 611-615; Weijers, D., Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis (2006) Dev Cell, 10 (2), pp. 265-270; Trapnell, C., Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks (2012) Nat Protoc, 7 (3), pp. 562-578; Tarazona, S., García-Alcalde, F., Dopazo, J., Ferrer, A., Conesa, A., Differential expression in RNA-seq: A matter of depth (2011) Genome Res, 21 (12), pp. 2213-2223; Thimm, O., MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes (2004) Plant J, 37 (6), pp. 914-939

PY - 2013

Y1 - 2013

N2 - Our anatomical analysis revealed that a dry maize seed contains four to five embryonic leaves at different developmental stages. Rudimentary kranz structure (KS) is apparent in the first leaf with a substantial density, but its density decreases toward younger leaves. Upon imbibition, leaf expansion occurs rapidly with new KSs initiated from the palisade-like ground meristem cells in the middle of the leaf. In parallel to the anatomical analysis, we obtained the time course transcriptomes for the embryonic leaves in dry and imbibed seeds every 6 h up to hour 72. Over this time course, the embryonic leaves exhibit transcripts of 30,255 genes at a level that can be regarded as "expressed." In dry seeds, ∼25,500 genes are expressed, showing functional enrichment in transcription, RNA processing, protein synthesis, primary metabolic pathways, and calcium transport. During the 72-h time course, ∼13,900 genes, including 590 transcription factor genes, are differentially expressed. Indeed, by 30 h postimbibition, ∼2,200 genes expressed in dry seeds are already down-regulated, and ∼2,000 are upregulated. Moreover, the top 1% expressed genes at 54 h or later are very different from those before 30 h, reflecting important developmental and physiological transitions. Interestingly, clusters of genes involved in hormone metabolism, signaling, and responses are differentially expressed at various time points and TF gene expression is also modular and stage specific. Our dataset provides an opportunity for hypothesizing the timing of regulatory actions, particularly in the context of KS development.

AB - Our anatomical analysis revealed that a dry maize seed contains four to five embryonic leaves at different developmental stages. Rudimentary kranz structure (KS) is apparent in the first leaf with a substantial density, but its density decreases toward younger leaves. Upon imbibition, leaf expansion occurs rapidly with new KSs initiated from the palisade-like ground meristem cells in the middle of the leaf. In parallel to the anatomical analysis, we obtained the time course transcriptomes for the embryonic leaves in dry and imbibed seeds every 6 h up to hour 72. Over this time course, the embryonic leaves exhibit transcripts of 30,255 genes at a level that can be regarded as "expressed." In dry seeds, ∼25,500 genes are expressed, showing functional enrichment in transcription, RNA processing, protein synthesis, primary metabolic pathways, and calcium transport. During the 72-h time course, ∼13,900 genes, including 590 transcription factor genes, are differentially expressed. Indeed, by 30 h postimbibition, ∼2,200 genes expressed in dry seeds are already down-regulated, and ∼2,000 are upregulated. Moreover, the top 1% expressed genes at 54 h or later are very different from those before 30 h, reflecting important developmental and physiological transitions. Interestingly, clusters of genes involved in hormone metabolism, signaling, and responses are differentially expressed at various time points and TF gene expression is also modular and stage specific. Our dataset provides an opportunity for hypothesizing the timing of regulatory actions, particularly in the context of KS development.

KW - Gene expression profiling

KW - Plant hormones

KW - Plant leaf development

KW - deetiolated 2 protein

KW - gibberellin a1

KW - senescence related gene 1 protein

KW - transcription factor

KW - ubiquitin protein ligase E3

KW - unclassified drug

KW - article

KW - calcium transport

KW - down regulation

KW - gene expression profiling

KW - genetic transcription

KW - germination

KW - maize

KW - meristem

KW - plant growth

KW - plant leaf

KW - priority journal

KW - protein synthesis

KW - RNA processing

KW - Gene Expression Profiling

KW - Gene Expression Regulation, Developmental

KW - Gene Expression Regulation, Plant

KW - Genes, Plant

KW - Germination

KW - Plant Growth Regulators

KW - Plant Leaves

KW - Plant Proteins

KW - RNA, Plant

KW - Seeds

KW - Transcription Factors

KW - Zea mays

UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-84874642661&origin=inward&txGid=7bfd684ea92a5a856b0356959e4a3a6c

UR - https://www.scopus.com/results/citedbyresults.uri?sort=plf-f&cite=2-s2.0-84874642661&src=s&imp=t&sid=1ec4d3e2944d1aa134b83d33eee0c9e2&sot=cite&sdt=a&sl=0&origin=recordpage&editSaveSearch=&txGid=123925371499b32d6f0c355a74c3c349

U2 - 10.1073/pnas.1301009110

DO - 10.1073/pnas.1301009110

M3 - Article

VL - 110

SP - 3979

EP - 3984

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 10

ER -