Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in C4-related metabolite fluxes and development

Manandhar-Shrestha K, Tamot B, Pratt EPS, Saitie S, Bräutigam A, Weber APM, Hoffmann-Benning S (2013)
Frontiers in Plant Science 4: 65.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Manandhar-Shrestha, K.; Tamot, B.; Pratt, E. P. S.; Saitie, S.; Bräutigam, AndreaUniBi ; Weber, Andreas P. M.; Hoffmann-Benning, Susanne
Abstract / Bemerkung
As the world population grows, our need for food increases drastically. Limited amounts of arable land lead to a competition between food and fuel crops, while changes in the global climate may impact future crop yields. Thus, a second "green revolution will need a better understanding of the processes essential for plant growth and development. One approach toward the solution of this problem is to better understand regulatory and transport processes in C4 plants. C4 plants display an up to 10-fold higher apparent CO2 assimilation and higher yields while maintaining high water use efficiency. This requires differential regulation of mesophyll (M) and bundle sheath (BS) chloroplast development as well as higher metabolic fluxes of photosynthetic intermediates between cells and particularly across chloroplast envelopes. While previous analyses of overall chloroplast membranes have yielded significant insight, our comparative proteomics approach using enriched BS and M chloroplast envelopes of Zea mays allowed us to identify 37 proteins of unknown function that have not been seen in these earlier studies. We identified 280 proteins, 84% of which are known/predicted to be present in chloroplasts. Seventy-four percent have a known or predicted membrane association. Twenty-one membrane proteins were 2-15 times more abundant in BS cells, while 36 of the proteins were more abundant in M chloroplast envelopes. These proteins could represent additional candidates of proteins essential for development or metabolite transport processes in C4 plants. RT-PCR confirmed differential expression of 13 candidate genes. Chloroplast association for seven proteins was confirmed using YFP/GFP labeling. Gene expression of four putative transporters was examined throughout the leaf and during the greening of leaves. Genes for a PIC-like protein and an ER-AP-like protein show an early transient increase in gene expression during the transition to light. In addition, PIC gene expression is increased in the immature part of the leaf and was lower in the fully developed parts of the leaf, suggesting a need for/incorporation of the protein during chloroplast development.
Stichworte
C4plant; chloroplast envelope proteins; photosynthesis; mesophyll cells; bundle sheath cells
Erscheinungsjahr
2013
Zeitschriftentitel
Frontiers in Plant Science
Band
4
Art.-Nr.
65
ISSN
1664-462X
Page URI
https://pub.uni-bielefeld.de/record/2915145

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Manandhar-Shrestha K, Tamot B, Pratt EPS, et al. Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in C4-related metabolite fluxes and development. Frontiers in Plant Science. 2013;4: 65.
Manandhar-Shrestha, K., Tamot, B., Pratt, E. P. S., Saitie, S., Bräutigam, A., Weber, A. P. M., & Hoffmann-Benning, S. (2013). Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in C4-related metabolite fluxes and development. Frontiers in Plant Science, 4, 65. doi:10.3389/fpls.2013.00065
Manandhar-Shrestha, K., Tamot, B., Pratt, E. P. S., Saitie, S., Bräutigam, A., Weber, A. P. M., and Hoffmann-Benning, S. (2013). Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in C4-related metabolite fluxes and development. Frontiers in Plant Science 4:65.
Manandhar-Shrestha, K., et al., 2013. Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in C4-related metabolite fluxes and development. Frontiers in Plant Science, 4: 65.
K. Manandhar-Shrestha, et al., “Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in C4-related metabolite fluxes and development”, Frontiers in Plant Science, vol. 4, 2013, : 65.
Manandhar-Shrestha, K., Tamot, B., Pratt, E.P.S., Saitie, S., Bräutigam, A., Weber, A.P.M., Hoffmann-Benning, S.: Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in C4-related metabolite fluxes and development. Frontiers in Plant Science. 4, : 65 (2013).
Manandhar-Shrestha, K., Tamot, B., Pratt, E. P. S., Saitie, S., Bräutigam, Andrea, Weber, Andreas P. M., and Hoffmann-Benning, Susanne. “Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in C4-related metabolite fluxes and development”. Frontiers in Plant Science 4 (2013): 65.
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7 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

The Plastoglobule-Localized Metallopeptidase PGM48 Is a Positive Regulator of Senescence in Arabidopsis thaliana.
Bhuiyan NH, Friso G, Rowland E, Majsec K, van Wijk KJ., Plant Cell 28(12), 2016
PMID: 27895226
Physiological and transcriptional analyses of developmental stages along sugarcane leaf.
Mattiello L, Riaño-Pachón DM, Martins MC, da Cruz LP, Bassi D, Marchiori PE, Ribeiro RV, Labate MT, Labate CA, Menossi M., BMC Plant Biol 15(), 2015
PMID: 26714767
Unknown components of the plastidial permeome.
Pick TR, Weber AP., Front Plant Sci 5(), 2014
PMID: 25191333
Application of proteomics for improving crop protection/artificial regulation.
Komatsu S, Mock HP, Yang P, Svensson B., Front Plant Sci 4(), 2013
PMID: 24391656

74 References

Daten bereitgestellt von Europe PubMed Central.

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ., Nucleic Acids Res. 25(17), 1997
PMID: 9254694
The path of carbon in photosynthesis.
BASSHAM JA, BENSON AA, CALVIN M., J. Biol. Chem. 185(2), 1950
PMID: 14774424
A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea.
Bolter B, Soll J, Hill K, Hemmler R, Wagner R., EMBO J. 18(20), 1999
PMID: 10523295
Dynamic Remodeling of the Plastid Envelope Membranes - A Tool for Chloroplast Envelope in vivo Localizations.
Breuers FK, Brautigam A, Geimer S, Welzel UY, Stefano G, Renna L, Brandizzi F, Weber AP., Front Plant Sci 3(), 2012
PMID: 22645566
The Plastid Outer Envelope - A Highly Dynamic Interface between Plastid and Cytoplasm.
Breuers FK, Brautigam A, Weber AP., Front Plant Sci 2(), 2011
PMID: 22629266
Separation and characterization of inner and outer envelope membranes of pea chloroplasts.
Cline K, Andrews J, Mersey B, Newcomb EH, Keegstra K., Proc. Natl. Acad. Sci. U.S.A. 78(6), 1981
PMID: 16593034
Gateway-compatible vectors for plant functional genomics and proteomics.
Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS., Plant J. 45(4), 2006
PMID: 16441352
What does it take to be C4? Lessons from the evolution of C4 photosynthesis.
Edwards GE, Furbank RT, Hatch MD, Osmond CB., Plant Physiol. 125(1), 2001
PMID: 11154293
Predicting subcellular localization of proteins based on their N-terminal amino acid sequence.
Emanuelsson O, Nielsen H, Brunak S, von Heijne G., J. Mol. Biol. 300(4), 2000
PMID: 10891285
AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins.
Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S, Bruley C, Garin J, Joyard J, Masselon C, Rolland N., Mol. Cell Proteomics 9(6), 2010
PMID: 20061580
Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana.
Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N., Mol. Cell Proteomics 2(5), 2003
PMID: 12766230
In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database.
Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, Sun Q, Wijk KJ., Plant Cell 16(2), 2004
PMID: 14729914
Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis.
Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, Gage DA, Phinney BS., J. Proteome Res. 2(4), 2003
PMID: 12938931
OEP37 is a new member of the chloroplast outer membrane ion channels.
Goetze TA, Philippar K, Ilkavets I, Soll J, Wagner R., J. Biol. Chem. 281(26), 2006
PMID: 16624824
C-4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure
Hatch M.., 1987
Concerning a dual function of coupled cyclic electron transport in leaves.
Heber U, Walker D., Plant Physiol. 100(4), 1992
PMID: 16653176
“Protein subcellular localization prediction with WoLF PSORT,”
Horton P., Park K.-J., Obayashi T., Nakai K.., 2006
Toc, tic, and chloroplast protein import.
Jarvis P, Soll J., Biochim. Biophys. Acta 1590(1-3), 2002
PMID: 12180471
LIPID-TRANSFER PROTEINS IN PLANTS.
Kader JC., Annu. Rev. Plant Physiol. Plant Mol. Biol. 47(), 1996
PMID: 15012303
Lipid transfer proteins: a puzzling family of plant proteins
Kader J.-C.., 1997
Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search.
Keller A, Nesvizhskii AI, Kolker E, Aebersold R., Anal. Chem. 74(20), 2002
PMID: 12403597
The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism.
Kinoshita H, Nagasaki J, Yoshikawa N, Yamamoto A, Takito S, Kawasaki M, Sugiyama T, Miyake H, Weber APM, Taniguchi M., Plant J. 65(1), 2010
PMID: 21175886
plprot: a comprehensive proteome database for different plastid types.
Kleffmann T, Hirsch-Hoffmann M, Gruissem W, Baginsky S., Plant Cell Physiol. 47(3), 2006
PMID: 16418230
The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions.
Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, Gruissem W, Baginsky S., Curr. Biol. 14(5), 2004
PMID: 15028209
Analysis of protein interactions at native chloroplast membranes by ellipsometry.
Kriechbaumer V, Nabok A, Mustafa MK, Al-Ammar R, Tsargorodskaya A, Smith DP, Abell BM., PLoS ONE 7(3), 2012
PMID: 22479632

Leegood R., Edwards G.., 1996
Resequencing of 200 human exomes identifies an excess of low-frequency non-synonymous coding variants.
Li Y, Vinckenbosch N, Tian G, Huerta-Sanchez E, Jiang T, Jiang H, Albrechtsen A, Andersen G, Cao H, Korneliussen T, Grarup N, Guo Y, Hellman I, Jin X, Li Q, Liu J, Liu X, Sparso T, Tang M, Wu H, Wu R, Yu C, Zheng H, Astrup A, Bolund L, Holmkvist J, Jorgensen T, Kristiansen K, Schmitz O, Schwartz TW, Zhang X, Li R, Yang H, Wang J, Hansen T, Pedersen O, Nielsen R, Wang J., Nat. Genet. 42(11), 2010
PMID: 20890277
Modulation of the neuronal glutamate transporter EAAC1 by the interacting protein GTRAP3-18.
Lin CI, Orlov I, Ruggiero AM, Dykes-Hoberg M, Lee A, Jackson M, Rothstein JD., Nature 410(6824), 2001
PMID: 11242046
Intracellular metabolite transporters in plants.
Linka N, Weber AP., Mol Plant 3(1), 2009
PMID: 20038549
Patentability issues surrounding antivirals.
Lu DL, Collison AM, Kowalski TJ., Nat. Biotechnol. 25(12), 2007
PMID: 18066035
The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis.
Lundquist PK, Poliakov A, Bhuiyan NH, Zybailov B, Sun Q, van Wijk KJ., Plant Physiol. 158(3), 2012
PMID: 22274653
Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions.
Majeran W, Friso G, Asakura Y, Qu X, Huang M, Ponnala L, Watkins KP, Barkan A, van Wijk KJ., Plant Physiol. 158(1), 2011
PMID: 22065420
Cell-type-specific differentiation of chloroplasts in C4 plants.
Majeran W, van Wijk KJ., Trends Plant Sci. 14(2), 2009
PMID: 19162526
Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells.
Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q, van Wijk KJ., Mol. Cell Proteomics 7(9), 2008
PMID: 18453340
CDD: a Conserved Domain Database for the functional annotation of proteins.
Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH., Nucleic Acids Res. 39(Database issue), 2010
PMID: 21109532
Evolution of C4 photosynthetic genes and overexpression of maize C4 genes in rice
Matsuoka M., Nomura M., Agarie S., Miyao-Tokutomi M., Ku M.., 1998
Differential biogenesis of photosystem II in mesophyll and bundle-sheath cells of monocotyledonous NADP-malic enzyme-type C4 plants: the non-stoichiometric abundance of the subunits of photosystem II in the bundle-sheath chloroplasts and the translational activity of the plastome-encoded genes
Meierhoff K., Westhoff P.., 1993
Reticulon-like proteins in Arabidopsis thaliana: structural organization and ER localization.
Nziengui H, Bouhidel K, Pillon D, Der C, Marty F, Schoefs B., FEBS Lett. 581(18), 2007
PMID: 17604024
Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction.
Peltier JB, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Soderberg L, Roepstorff P, von Heijne G, van Wijk KJ., Plant Cell 14(1), 2002
PMID: 11826309
Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation.
Pick TR, Brautigam A, Schluter U, Denton AK, Colmsee C, Scholz U, Fahnenstich H, Pieruschka R, Rascher U, Sonnewald U, Weber AP., Plant Cell 23(12), 2011
PMID: 22186372
A high-conductance solute channel in the chloroplastic outer envelope from Pea.
Pohlmeyer K, Soll J, Grimm R, Hill K, Wagner R., Plant Cell 10(7), 1998
PMID: 9668138
Isolation and characterization of an amino acid-selective channel protein present in the chloroplastic outer envelope membrane.
Pohlmeyer K, Soll J, Steinkamp T, Hinnah S, Wagner R., Proc. Natl. Acad. Sci. U.S.A. 94(17), 1997
PMID: 9256512
Reprint of: Regulation of photosynthetic electron transport.
Rochaix JD., Biochim. Biophys. Acta 1807(8), 2011
PMID: 21605544
The evolution of C4 photosynthesis.
Sage RF., New Phytol. 161(2), 2004
PMID: IND43668189
Prediction of the plant beta-barrel proteome: a case study of the chloroplast outer envelope.
Schleiff E, Eichacker LA, Eckart K, Becker T, Mirus O, Stahl T, Soll J., Protein Sci. 12(4), 2003
PMID: 12649433
Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
Shevchenko A, Wilm M, Vorm O, Mann M., Anal. Chem. 68(5), 1996
PMID: 8779443
Cyclic electron transport around photosystem I: genetic approaches.
Shikanai T., Annu Rev Plant Biol 58(), 2007
PMID: 17201689
Proteome analysis of bell pepper (Capsicum annuum L.) chromoplasts.
Siddique MA, Grossmann J, Gruissem W, Baginsky S., Plant Cell Physiol. 47(12), 2006
PMID: 17098784
Conservation and developmental control of alternative splicing in maebl among malaria parasites.
Singh N, Preiser P, Renia L, Balu B, Barnwell J, Blair P, Jarra W, Voza T, Landau I, Adams JH., J. Mol. Biol. 343(3), 2004
PMID: 15465047
TLP18.3, a novel thylakoid lumen protein regulating photosystem II repair cycle.
Sirpio S, Allahverdiyeva Y, Suorsa M, Paakkarinen V, Vainonen J, Battchikova N, Aro EM., Biochem. J. 406(3), 2007
PMID: 17576201

Taiz L., Zeiger E.., 2006
Differentiation of dicarboxylate transporters in mesophyll and bundle sheath chloroplasts of maize.
Taniguchi Y, Nagasaki J, Kawasaki M, Miyake H, Sugiyama T, Taniguchi M., Plant Cell Physiol. 45(2), 2004
PMID: 14988489
Mouse maps of gene expression in the brain.
Koester SE, Insel TR., Genome Biol. 8(5), 2007
PMID: 17521453
SPOCTOPUS: a combined predictor of signal peptides and membrane protein topology.
Viklund H, Bernsel A, Skwark M, Elofsson A., Bioinformatics 24(24), 2008
PMID: 18945683
Proteome analysis of the rice etioplast: metabolic and regulatory networks and novel protein functions.
von Zychlinski A, Kleffmann T, Krishnamurthy N, Sjolander K, Baginsky S, Gruissem W., Mol. Cell Proteomics 4(8), 2005
PMID: 15901827
Plant metabolism. Editorial.
Dudareva N, Pichersky E, Werck-Reichhart D, Lewinsohn E., Mol Plant 3(1), 2010
PMID: 20085892
Solute transporters of the plastid envelope membrane.
Weber AP, Schwacke R, Flugge UI., Annu Rev Plant Biol 56(), 2005
PMID: 15862092
An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets.
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ., PLoS ONE 2(8), 2007
PMID: 17684564
The role of hexokinase in plant sugar signal transduction and growth and development.
Xiao W, Sheen J, Jang JC., Plant Mol. Biol. 44(4), 2000
PMID: 11197321

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