Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis

Yao-Ming Chang, Wen-Yu Liu, Chun-Chieh Shih, Meng-Ni Shen, Chen-Hua Lu, Mei-Yeh Lu, Hui-Wen Yang, Tzi-Yuan Wang, Chun-Chang Chen, Stella Maris Chen, Wen-Hsiung Li, Mauricesb Ku

研究成果: 雜誌貢獻文章

77 引文 (Scopus)

摘要

To study the regulatory and functional differentiation between the mesophyll (M) and bundle sheath (BS) cells of maize (Zea mays), we isolated large quantities of highly homogeneous M and BS cells from newly matured second leaves for transcriptome profiling by RNA sequencing. A total of 52,421 annotated genes with at least one read were found in the two transcriptomes. Defining a gene with more than one read per kilobase per million mapped reads as expressed, we identified 18,482 expressed genes; 14,972 were expressed in M cells, including 53 M-enriched transcription factor (TF) genes, whereas 17,269 were expressed in BS cells, including 214 BS-enriched TF genes. Interestingly, many TF gene families show a conspicuous BS preference in expression. Pathway analyses reveal differentiation between the two cell types in various functional categories, with the M cells playing more important roles in light reaction, protein synthesis and folding, tetrapyrrole synthesis, and RNA binding, while the BS cells specialize in transport, signaling, protein degradation and posttranslational modification, major carbon, hydrogen, and oxygen metabolism, cell division and organization, and development. Genes coding for several transporters involved in the shuttle of C4 metabolites and BS cell wall development have been identified, to our knowledge, for the first time. This comprehensive data set will be useful for studying M/BS differentiation in regulation and function. © 2012 American Society of Plant Biologists.
原文英語
頁(從 - 到)165-177
頁數13
期刊Plant Physiology
160
發行號1
DOIs
出版狀態已發佈 - 2012
對外發佈Yes

指紋

bundle sheath cells
transcriptomics
mesophyll
Zea mays
corn
Genes
genes
Transcription Factors
transcription factors
Tetrapyrroles
RNA Sequence Analysis
protein folding
Protein Folding
post-translational modification
Gene Expression Profiling
cells
Post Translational Protein Processing
protein degradation
Transcriptome
transcriptome

引用此文

Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. / Chang, Yao-Ming; Liu, Wen-Yu; Shih, Chun-Chieh; Shen, Meng-Ni; Lu, Chen-Hua; Lu, Mei-Yeh ; Yang, Hui-Wen; Wang, Tzi-Yuan; Chen, Chun-Chang; Chen, Stella Maris; Li, Wen-Hsiung; Ku, Mauricesb.

於: Plant Physiology, 卷 160, 編號 1, 2012, p. 165-177.

研究成果: 雜誌貢獻文章

Chang, Y-M, Liu, W-Y, Shih, C-C, Shen, M-N, Lu, C-H, Lu, M-Y, Yang, H-W, Wang, T-Y, Chen, C-C, Chen, SM, Li, W-H & Ku, M 2012, 'Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis', Plant Physiology, 卷 160, 編號 1, 頁 165-177. https://doi.org/10.1104/pp.112.203810
Chang, Yao-Ming ; Liu, Wen-Yu ; Shih, Chun-Chieh ; Shen, Meng-Ni ; Lu, Chen-Hua ; Lu, Mei-Yeh ; Yang, Hui-Wen ; Wang, Tzi-Yuan ; Chen, Chun-Chang ; Chen, Stella Maris ; Li, Wen-Hsiung ; Ku, Mauricesb. / Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. 於: Plant Physiology. 2012 ; 卷 160, 編號 1. 頁 165-177.
@article{3b341a20e32f47daaffb086589797603,
title = "Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis",
abstract = "To study the regulatory and functional differentiation between the mesophyll (M) and bundle sheath (BS) cells of maize (Zea mays), we isolated large quantities of highly homogeneous M and BS cells from newly matured second leaves for transcriptome profiling by RNA sequencing. A total of 52,421 annotated genes with at least one read were found in the two transcriptomes. Defining a gene with more than one read per kilobase per million mapped reads as expressed, we identified 18,482 expressed genes; 14,972 were expressed in M cells, including 53 M-enriched transcription factor (TF) genes, whereas 17,269 were expressed in BS cells, including 214 BS-enriched TF genes. Interestingly, many TF gene families show a conspicuous BS preference in expression. Pathway analyses reveal differentiation between the two cell types in various functional categories, with the M cells playing more important roles in light reaction, protein synthesis and folding, tetrapyrrole synthesis, and RNA binding, while the BS cells specialize in transport, signaling, protein degradation and posttranslational modification, major carbon, hydrogen, and oxygen metabolism, cell division and organization, and development. Genes coding for several transporters involved in the shuttle of C4 metabolites and BS cell wall development have been identified, to our knowledge, for the first time. This comprehensive data set will be useful for studying M/BS differentiation in regulation and function. {\circledC} 2012 American Society of Plant Biologists.",
keywords = "plant RNA, transcription factor, transcriptome, vegetable protein, article, cell differentiation, cell wall, chromosome map, cytology, gene expression profiling, gene expression regulation, genetics, maize, mesophyll cell, metabolism, photosynthesis, plant cell, plant epidermis, plant gene, plant leaf, plasmodesma, protein synthesis, protein transport, protoplast, signal transduction, vascular bundle (plant), Cell Differentiation, Cell Wall, Chromosome Mapping, Gene Expression Profiling, Gene Expression Regulation, Plant, Genes, Plant, Mesophyll Cells, Photosynthesis, Plant Cells, Plant Epidermis, Plant Leaves, Plant Proteins, Plant Vascular Bundle, Plasmodesmata, Protein Biosynthesis, Protein Transport, Protoplasts, RNA, Plant, Signal Transduction, Transcription Factors, Transcriptome, Zea mays",
author = "Yao-Ming Chang and Wen-Yu Liu and Chun-Chieh Shih and Meng-Ni Shen and Chen-Hua Lu and Mei-Yeh Lu and Hui-Wen Yang and Tzi-Yuan Wang and Chun-Chang Chen and Chen, {Stella Maris} and Wen-Hsiung Li and Mauricesb Ku",
note = "被引用次數:41 Export Date: 21 March 2016 CODEN: PLPHA 通訊地址: Li, W.-H.; Biodiversity Research Center, Academia Sinica, Taipei, 115, Taiwan; 電子郵件: whli@sinica.edu.tw 化學物質/CAS: Plant Proteins; RNA, Plant; Transcription Factors 參考文獻: Aggarwal, P., Padmanabhan, B., Bhat, A., Sarvepalli, K., Sadhale, P.P., Nath, U., The TCP4 transcription factor of Arabidopsis blocks cell division in yeast at G1→S transition (2011) Biochem Biophys Res Commun, 410, pp. 276-281; Aoki, N., Ohnishi, J.-I., Kanai, R., Two different mechanisms for transport of pyruvate into mesophyll chloroplasts of C4 plants: A comparative study (1992) Plant Cell Physiol, 33, pp. 805-809; Aoyagi, K., Nakamoto, H., Pyruvate, Pi dikinase in bundle sheath strands as well as in mesophyll cells in maize leaves (1985) Plant Physiol, 78, pp. 661-664; Botha, C., Cross, R., van Bel, A., Peter, C., Phloem loading in the sucrose-export-defective (SXD-1) mutant maize is limited by callose deposition at plasmodesmata in bundle sheath-vascular parenchyma interface (2000) Protoplasma, 214, pp. 65-72; Collinge, M., Boller, T., Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding (2001) Plant Mol Biol, 46, pp. 521-529; Cribb, L., Hall, L.N., Langdale, J.A., Four mutant alleles elucidate the role of the G2 protein in the development of C(4) and C(3) photosynthesizing maize tissues (2001) Genetics, 159, pp. 787-797; Cubas, P., Lauter, N., Doebley, J., Coen, E., The TCP domain: A motif found in proteins regulating plant growth and development (1999) Plant J, 18, pp. 215-222; Dai, Z., Ku, M., Edwards, G.E., C4 photosynthesis (the CO2-concentrating mechanism and photorespiration) (1993) Plant Physiol, 103, pp. 83-90; Dai, Z., Ku, M., Edwards, G.E., C4 photosynthesis (the effects of leaf development on the CO2-concentrating mechanism and photorespiration in maize) (1995) Plant Physiol, 107, pp. 815-825; de Veau, E.J., Burris, J.E., Photorespiratory rates in wheat and maize as determined by o-labeling (1989) Plant Physiol, 90, pp. 500-511; Evans, J.R., von Caemmerer, S., Carbon dioxide diffusion inside leaves (1996) Plant Physiol, 110, pp. 339-346; Evert, R.F., Eschrich, W., Heyser, W., Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L (1977) Planta, 136, pp. 77-89; Finet, C., Fourquin, C., Vinauger, M., Berne-Dedieu, A., Chambrier, P., Paindavoine, S., Scutt, C.P., Parallel structural evolution of auxin response factors in the angiosperms (2010) Plant J, 63, pp. 952-959; Flugge, U.I., Phosphate translocators in plastids (1999) Annu Rev Plant Physiol Plant Mol Biol, 50, pp. 27-45; Friso, G., Majeran, W., Huang, M., Sun, Q., van Wijk, K.J., Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: Large-scale quantitative proteomics using the first maize genome assembly (2010) Plant Physiol, 152, pp. 1219-1250; Furbank, R.T., Evolution of the C(4) photosynthetic mechanism: Are there really three C(4) acid decarboxylation types? (2011) J Exp Bot, 62, pp. 3103-3108; Furumoto, T., Hata, S., Izui K (1999) cDNA cloning and characterization of maize phosphoenolpyruvate carboxykinase, a bundle sheath cell-specific enzyme Plant Mol Biol, 41, pp. 301-311; Furumoto, T., Hata, S., Izui, K., Isolation and characterization of cDNAs for differentially accumulated transcripts between mesophyll cells and bundle sheath strands of maize leaves (2000) Plant Cell Physiol, 41, pp. 1200-1209; Furumoto, T., Yamaguchi, T., Ohshima-Ichie, Y., Nakamura, M., Tsuchida-Iwata, Y., Shimamura, M., Ohnishi, J., Westhoff, P., A plastidial sodium-dependent pyruvate transporter (2011) Nature, 476, pp. 472-475; Gamas, P., Niebel, F., Lescure, N., Cullimore, J., Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development (1996) Mol Plant Microbe Interact, 9, pp. 233-242; Gowik, U., Br{\"a}utigam, A., Weber, K.L., Weber, A.P., Westhoff, P., Evolution of C4 photosynthesis in the genus Flaveria: How many and which genes does it take to make C4? 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year = "2012",
doi = "10.1104/pp.112.203810",
language = "English",
volume = "160",
pages = "165--177",
journal = "Plant Physiology",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "1",

}

TY - JOUR

T1 - Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis

AU - Chang, Yao-Ming

AU - Liu, Wen-Yu

AU - Shih, Chun-Chieh

AU - Shen, Meng-Ni

AU - Lu, Chen-Hua

AU - Lu, Mei-Yeh

AU - Yang, Hui-Wen

AU - Wang, Tzi-Yuan

AU - Chen, Chun-Chang

AU - Chen, Stella Maris

AU - Li, Wen-Hsiung

AU - Ku, Mauricesb

N1 - 被引用次數:41 Export Date: 21 March 2016 CODEN: PLPHA 通訊地址: Li, W.-H.; Biodiversity Research Center, Academia Sinica, Taipei, 115, Taiwan; 電子郵件: whli@sinica.edu.tw 化學物質/CAS: Plant Proteins; RNA, Plant; Transcription Factors 參考文獻: Aggarwal, P., Padmanabhan, B., Bhat, A., Sarvepalli, K., Sadhale, P.P., Nath, U., The TCP4 transcription factor of Arabidopsis blocks cell division in yeast at G1→S transition (2011) Biochem Biophys Res Commun, 410, pp. 276-281; Aoki, N., Ohnishi, J.-I., Kanai, R., Two different mechanisms for transport of pyruvate into mesophyll chloroplasts of C4 plants: A comparative study (1992) Plant Cell Physiol, 33, pp. 805-809; Aoyagi, K., Nakamoto, H., Pyruvate, Pi dikinase in bundle sheath strands as well as in mesophyll cells in maize leaves (1985) Plant Physiol, 78, pp. 661-664; Botha, C., Cross, R., van Bel, A., Peter, C., Phloem loading in the sucrose-export-defective (SXD-1) mutant maize is limited by callose deposition at plasmodesmata in bundle sheath-vascular parenchyma interface (2000) Protoplasma, 214, pp. 65-72; Collinge, M., Boller, T., Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding (2001) Plant Mol Biol, 46, pp. 521-529; Cribb, L., Hall, L.N., Langdale, J.A., Four mutant alleles elucidate the role of the G2 protein in the development of C(4) and C(3) photosynthesizing maize tissues (2001) Genetics, 159, pp. 787-797; Cubas, P., Lauter, N., Doebley, J., Coen, E., The TCP domain: A motif found in proteins regulating plant growth and development (1999) Plant J, 18, pp. 215-222; Dai, Z., Ku, M., Edwards, G.E., C4 photosynthesis (the CO2-concentrating mechanism and photorespiration) (1993) Plant Physiol, 103, pp. 83-90; Dai, Z., Ku, M., Edwards, G.E., C4 photosynthesis (the effects of leaf development on the CO2-concentrating mechanism and photorespiration in maize) (1995) Plant Physiol, 107, pp. 815-825; de Veau, E.J., Burris, J.E., Photorespiratory rates in wheat and maize as determined by o-labeling (1989) Plant Physiol, 90, pp. 500-511; Evans, J.R., von Caemmerer, S., Carbon dioxide diffusion inside leaves (1996) Plant Physiol, 110, pp. 339-346; Evert, R.F., Eschrich, W., Heyser, W., Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L (1977) Planta, 136, pp. 77-89; Finet, C., Fourquin, C., Vinauger, M., Berne-Dedieu, A., Chambrier, P., Paindavoine, S., Scutt, C.P., Parallel structural evolution of auxin response factors in the angiosperms (2010) Plant J, 63, pp. 952-959; Flugge, U.I., Phosphate translocators in plastids (1999) Annu Rev Plant Physiol Plant Mol Biol, 50, pp. 27-45; Friso, G., Majeran, W., Huang, M., Sun, Q., van Wijk, K.J., Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: Large-scale quantitative proteomics using the first maize genome assembly (2010) Plant Physiol, 152, pp. 1219-1250; Furbank, R.T., Evolution of the C(4) photosynthetic mechanism: Are there really three C(4) acid decarboxylation types? (2011) J Exp Bot, 62, pp. 3103-3108; Furumoto, T., Hata, S., Izui K (1999) cDNA cloning and characterization of maize phosphoenolpyruvate carboxykinase, a bundle sheath cell-specific enzyme Plant Mol Biol, 41, pp. 301-311; Furumoto, T., Hata, S., Izui, K., Isolation and characterization of cDNAs for differentially accumulated transcripts between mesophyll cells and bundle sheath strands of maize leaves (2000) Plant Cell Physiol, 41, pp. 1200-1209; Furumoto, T., Yamaguchi, T., Ohshima-Ichie, Y., Nakamura, M., Tsuchida-Iwata, Y., Shimamura, M., Ohnishi, J., Westhoff, P., A plastidial sodium-dependent pyruvate transporter (2011) Nature, 476, pp. 472-475; Gamas, P., Niebel, F., Lescure, N., Cullimore, J., Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development (1996) Mol Plant Microbe Interact, 9, pp. 233-242; Gowik, U., Bräutigam, A., Weber, K.L., Weber, A.P., Westhoff, P., Evolution of C4 photosynthesis in the genus Flaveria: How many and which genes does it take to make C4? (2011) Plant Cell, 23, pp. 2087-2105; Gowik, U., Westhoff, P., The path from C3 to C4 photosynthesis (2011) Plant Physiol, 155, pp. 56-63; Gray, J.E., Plant development: Three steps for stomata (2007) Curr Biol, 17, pp. R213-R215; Guan, Y.F., Huang, X.Y., Zhu, J., Gao, J.F., Zhang, H.X., Yang, Z.N., RUP-TURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis (2008) Plant Physiol, 147, pp. 852-863; Gutierrez, M., Huber, S.C., Ku, S.B., Kanai, R., Edwards, G.E., Intracellular localization of carbon metabolism in mesophyll cells of C4 plants (1974) III International Congress On Photosynthesis Research, pp. 1219-1230. , In M Avron, Elsevier Science Publishers, Amsterdam, The Netherlands; Haake, V., Cook, D., Riechmann, J.L., Pineda, O., Thomashow, M.F., Zhang, J.Z., Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis (2002) Plant Physiol, 130, pp. 639-648; 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, pp. 925-936; 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PY - 2012

Y1 - 2012

N2 - To study the regulatory and functional differentiation between the mesophyll (M) and bundle sheath (BS) cells of maize (Zea mays), we isolated large quantities of highly homogeneous M and BS cells from newly matured second leaves for transcriptome profiling by RNA sequencing. A total of 52,421 annotated genes with at least one read were found in the two transcriptomes. Defining a gene with more than one read per kilobase per million mapped reads as expressed, we identified 18,482 expressed genes; 14,972 were expressed in M cells, including 53 M-enriched transcription factor (TF) genes, whereas 17,269 were expressed in BS cells, including 214 BS-enriched TF genes. Interestingly, many TF gene families show a conspicuous BS preference in expression. Pathway analyses reveal differentiation between the two cell types in various functional categories, with the M cells playing more important roles in light reaction, protein synthesis and folding, tetrapyrrole synthesis, and RNA binding, while the BS cells specialize in transport, signaling, protein degradation and posttranslational modification, major carbon, hydrogen, and oxygen metabolism, cell division and organization, and development. Genes coding for several transporters involved in the shuttle of C4 metabolites and BS cell wall development have been identified, to our knowledge, for the first time. This comprehensive data set will be useful for studying M/BS differentiation in regulation and function. © 2012 American Society of Plant Biologists.

AB - To study the regulatory and functional differentiation between the mesophyll (M) and bundle sheath (BS) cells of maize (Zea mays), we isolated large quantities of highly homogeneous M and BS cells from newly matured second leaves for transcriptome profiling by RNA sequencing. A total of 52,421 annotated genes with at least one read were found in the two transcriptomes. Defining a gene with more than one read per kilobase per million mapped reads as expressed, we identified 18,482 expressed genes; 14,972 were expressed in M cells, including 53 M-enriched transcription factor (TF) genes, whereas 17,269 were expressed in BS cells, including 214 BS-enriched TF genes. Interestingly, many TF gene families show a conspicuous BS preference in expression. Pathway analyses reveal differentiation between the two cell types in various functional categories, with the M cells playing more important roles in light reaction, protein synthesis and folding, tetrapyrrole synthesis, and RNA binding, while the BS cells specialize in transport, signaling, protein degradation and posttranslational modification, major carbon, hydrogen, and oxygen metabolism, cell division and organization, and development. Genes coding for several transporters involved in the shuttle of C4 metabolites and BS cell wall development have been identified, to our knowledge, for the first time. This comprehensive data set will be useful for studying M/BS differentiation in regulation and function. © 2012 American Society of Plant Biologists.

KW - plant RNA

KW - transcription factor

KW - transcriptome

KW - vegetable protein

KW - article

KW - cell differentiation

KW - cell wall

KW - chromosome map

KW - cytology

KW - gene expression profiling

KW - gene expression regulation

KW - genetics

KW - maize

KW - mesophyll cell

KW - metabolism

KW - photosynthesis

KW - plant cell

KW - plant epidermis

KW - plant gene

KW - plant leaf

KW - plasmodesma

KW - protein synthesis

KW - protein transport

KW - protoplast

KW - signal transduction

KW - vascular bundle (plant)

KW - Cell Differentiation

KW - Cell Wall

KW - Chromosome Mapping

KW - Gene Expression Profiling

KW - Gene Expression Regulation, Plant

KW - Genes, Plant

KW - Mesophyll Cells

KW - Photosynthesis

KW - Plant Cells

KW - Plant Epidermis

KW - Plant Leaves

KW - Plant Proteins

KW - Plant Vascular Bundle

KW - Plasmodesmata

KW - Protein Biosynthesis

KW - Protein Transport

KW - Protoplasts

KW - RNA, Plant

KW - Signal Transduction

KW - Transcription Factors

KW - Transcriptome

KW - Zea mays

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UR - https://www.scopus.com/results/citedbyresults.uri?sort=plf-f&cite=2-s2.0-84865839724&src=s&imp=t&sid=778b9da366eec9860ca33a13c9b6416e&sot=cite&sdt=a&sl=0&origin=recordpage&editSaveSearch=&txGid=633fda7a57616f39a67dd1aa0732c272

U2 - 10.1104/pp.112.203810

DO - 10.1104/pp.112.203810

M3 - Article

VL - 160

SP - 165

EP - 177

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 1

ER -