title: 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.
abstract: 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.
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University East Lansing, MI, USA.
authors.forename: K
authors.initials: K
authors.lastname: Manandhar-Shrestha
authors.forename: B
authors.initials: B
authors.lastname: Tamot
authors.forename: E P S
authors.initials: EP
authors.lastname: Pratt
authors.forename: S
authors.initials: S
authors.lastname: Saitie
authors.forename: A
authors.initials: A
authors.lastname: Bräutigam
authors.forename: A P M
authors.initials: AP
authors.lastname: Weber
authors.forename: Susanne
authors.initials: S
authors.lastname: Hoffmann-Benning
keywords: C4 plant; bundle sheath cells; chloroplast envelope proteins; mesophyll cells; photosynthesis
references.citation: Biochim Biophys Acta. 2002 Jun 12;1590(1-3):177-89
references.pmid: 12180471
references.citation: Proc Natl Acad Sci U S A. 1981 Jun;78(6):3595-9
references.pmid: 16593034
references.citation: J Biol Chem. 2006 Jun 30;281(26):17989-98
references.pmid: 16624824
references.citation: Plant Cell. 2004 Feb;16(2):478-99
references.pmid: 14729914
references.citation: Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9504-9
references.pmid: 9256512
references.citation: J Biol Chem. 2004 Feb 6;279(6):4768-81
references.pmid: 14593120
references.citation: Plant Physiol. 2009 Dec;151(4):1790-801
references.pmid: 19767385
references.citation: Plant Physiol. 2012 Mar;158(3):1172-92
references.pmid: 22274653
references.citation: Front Plant Sci. 2011 Dec 14;2:97
references.pmid: 22629266
references.citation: Plant Physiol. 2001 Jan;125(1):46-9
references.pmid: 11154293
references.citation: J Mol Biol. 2004 Oct 22;343(3):589-99
references.pmid: 15465047
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:627-654
references.pmid: 15012303
references.citation: Plant Cell Physiol. 2006 Dec;47(12):1663-73
references.pmid: 17098784
references.citation: Mol Cell Proteomics. 2003 May;2(5):325-45
references.pmid: 12766230
references.citation: Plant Physiol. 1973 Jun;51(6):1133-7
references.pmid: 16658479
references.citation: J Mol Biol. 2000 Jul 21;300(4):1005-16
references.pmid: 10891285
references.citation: Biochem J. 1969 Sep;114(3):489-98
references.pmid: 4309527
references.citation: Anal Chem. 2002 Oct 15;74(20):5383-92
references.pmid: 12403597
references.citation: Curr Opin Plant Biol. 2004 Jun;7(3):247-53
references.pmid: 15134744
references.citation: Plant Physiol. 2011 Apr;155(4):1511-9
references.pmid: 21263040
references.citation: Annu Rev Plant Biol. 2007;58:199-217
references.pmid: 17201689
references.citation: Protein Sci. 1999 May;8(5):978-84
references.pmid: 10338008
references.citation: Plant Cell Physiol. 2006 Mar;47(3):432-6
references.pmid: 16418230
references.citation: EMBO J. 1999 Oct 15;18(20):5505-16
references.pmid: 10523295
references.citation: Nucleic Acids Res. 2011 Jan;39(Database issue):D225-9
references.pmid: 21109532
references.citation: Plant Physiol. 2008 Sep;148(1):568-79
references.pmid: 18599648
references.citation: Plant Mol Biol. 2000 Nov;44(4):451-61
references.pmid: 11197321
references.citation: Plant Physiol. 2010 Mar;152(3):1219-50
references.pmid: 20089766
references.citation: PLoS One. 2012;7(3):e34455
references.pmid: 22479632
references.citation: Plant Cell. 2002 Jan;14(1):211-36
references.pmid: 11826309
references.citation: Trends Plant Sci. 2009 Feb;14(2):100-9
references.pmid: 19162526
references.citation: Nature. 2001 Mar 1;410(6824):84-8
references.pmid: 11242046
references.citation: Mol Cell Proteomics. 2010 Jun;9(6):1063-84
references.pmid: 20061580
references.citation: Mol Cell Proteomics. 2008 Sep;7(9):1609-38
references.pmid: 18453340
references.citation: Biochem J. 2007 Sep 15;406(3):415-25
references.pmid: 17576201
references.citation: FEBS Lett. 2007 Jul 24;581(18):3356-62
references.pmid: 17604024
references.citation: Front Plant Sci. 2012 Jan 23;3:7
references.pmid: 22645566
references.citation: Plant Cell. 2005 Nov;17(11):3111-40
references.pmid: 16243905
references.citation: Protein Sci. 2003 Apr;12(4):748-59
references.pmid: 12649433
references.citation: Plant J. 2011 Jan;65(1):15-26
references.pmid: 21175886
references.citation: PLoS One. 2007 Aug 08;2(8):e718
references.pmid: 17684564
references.citation: Plant J. 2006 Feb;45(4):616-29
references.pmid: 16441352
references.citation: Genome Biol. 2007;8(10):R212
references.pmid: 17919328
references.citation: Plant Cell. 1998 Jul;10(7):1207-16
references.pmid: 9668138
references.citation: Plant Cell Physiol. 2004 Feb;45(2):187-200
references.pmid: 14988489
references.citation: Mol Plant. 2010 Jan;3(1):21-53
references.pmid: 20038549
references.citation: Plant Physiol. 1992 Dec;100(4):1621-6
references.pmid: 16653176
references.citation: Curr Biol. 2004 Mar 9;14(5):354-62
references.pmid: 15028209
references.citation: J Biol Chem. 2007 Jan 12;282(2):1170-4
references.pmid: 17077082
references.citation: FEBS Lett. 2007 May 25;581(12):2215-22
references.pmid: 17316618
references.citation: Anal Chem. 1996 Mar 1;68(5):850-8
references.pmid: 8779443
references.citation: Anal Chem. 2004 Jul 15;76(14):4193-201
references.pmid: 15253663
references.citation: Annu Rev Plant Biol. 2005;56:133-64
references.pmid: 15862092
references.citation: Biochim Biophys Acta. 2011 Aug;1807(8):878-86
references.pmid: 21605544
references.citation: Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
references.pmid: 9254694
references.citation: J Biol Chem. 1950 Aug;185(2):781-7
references.pmid: 14774424
references.citation: Plant Physiol. 2012 Jan;158(1):156-89
references.pmid: 22065420
references.citation: Mol Cell Proteomics. 2005 Aug;4(8):1072-84
references.pmid: 15901827
references.citation: Nat Genet. 2010 Dec;42(12):1060-7
references.pmid: 21037569
references.citation: New Phytol. 2004 Feb;161(2):341-370
references.pmid: 33873498
references.citation: Plant J. 2011 Jun;66(5):759-69
references.pmid: 21309871
references.citation: J Proteome Res. 2003 Jul-Aug;2(4):413-25
references.pmid: 12938931
references.citation: Bioinformatics. 2008 Aug 1;24(15):1662-8
references.pmid: 18474507
references.citation: Nat Biotechnol. 2007 Jan;25(1):117-24
references.pmid: 17187058
references.citation: Plant Cell. 2011 Dec;23(12):4208-20
references.pmid: 22186372
references.citation: Anal Chem. 2005 Oct 1;77(19):6218-24
references.pmid: 16194081