title: Subfunctionalization of sigma factors during the evolution of land plants based on mutant analysis of liverwort (Marchantia polymorpha L.) MpSIG1.
abstract: Sigma factor is a subunit of plastid-encoded RNA polymerase that regulates the transcription of plastid-encoded genes by recognizing a set of promoters. Sigma factors have increased in copy number and have diversified during the evolution of land plants, but details of this process remain unknown. Liverworts represent the basal group of embryophytes and are expected to retain the ancestral features of land plants. In liverwort (Marchantia polymorpha L.), we isolated and characterized a T-DNA-tagged mutant (Mpsig1) of sigma factor 1 (MpSIG1). The mutant did not show any visible phenotypes, implying that MpSIG1 function is redundant with that of other sigma factors. However, quantitative reverse-transcription polymerase chain reaction and RNA gel blot analysis revealed that genes related to photosynthesis were downregulated, resulting in the minor reduction of some protein complexes. The transcript levels of genes clustered in the petL, psaA, psbB, psbK, and psbE operons of liverwort were lower than those in the wild type, a result similar to that in the SIG1 defective mutant in rice (Oryza sativa). Overexpression analysis revealed primitive functional divergence between the SIG1 and SIG2 proteins in bryophytes, whereas these proteins still retain functional redundancy. We also discovered that the predominant sigma factor for ndhF mRNA expression has been diversified in liverwort, Arabidopsis (Arabidopsis thaliana), and rice. Our study shows the ancestral function of SIG1 and the process of functional partitioning (subfunctionalization) of sigma factors during the evolution of land plants.
authors.affiliation: Department of Botany, Graduate School of Science, Kyoto University, Japan.
authors.forename: Minoru
authors.initials: M
authors.lastname: Ueda
authors.forename: Tsuneaki
authors.initials: T
authors.lastname: Takami
authors.forename: Lianwei
authors.initials: L
authors.lastname: Peng
authors.forename: Kimitsune
authors.initials: K
authors.lastname: Ishizaki
authors.forename: Takayuki
authors.initials: T
authors.lastname: Kohchi
authors.forename: Toshiharu
authors.initials: T
authors.lastname: Shikanai
authors.forename: Yoshiki
authors.initials: Y
authors.lastname: Nishimura
mesh_terms: D017360:Arabidopsis / Q000235:genetics; D012321:DNA-Directed RNA Polymerases / Q000235:genetics; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant; D047008:Marchantia / Q000235:genetics*; D008969:Molecular Sequence Data; D009154:Mutation; D012275:Oryza / Q000235:genetics; D010944:Plants; D018087:Plastids / Q000235:genetics; D011401:Promoter Regions, Genetic; D012808:Sigma Factor / Q000235:genetics*
chemical_list: C413368:Sig2 sigma factor; D012808:Sigma Factor; D012321:DNA-Directed RNA Polymerases
keywords: Marchantia; chloroplast transcription; gene duplication; plastid-encoded RNA polymerase
references.citation: Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12246-51
references.pmid: 12218172
references.citation: Philos Trans R Soc Lond B Biol Sci. 2013 Jun 10;368(1622):20120260
references.pmid: 23754813
references.citation: Nature. 2002 Jun 13;417(6890):712-9
references.pmid: 12000971
references.citation: FEBS Lett. 1997 Aug 18;413(2):309-13
references.pmid: 9280303
references.citation: FEBS Lett. 2001 Jun 15;499(1-2):87-91
references.pmid: 11418118
references.citation: Mol Biol Evol. 2007 Aug;24(8):1596-9
references.pmid: 17488738
references.citation: Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14948-53
references.pmid: 9405719
references.citation: Nucleic Acids Res. 2007;35(11):3676-92
references.pmid: 17488843
references.citation: Nucleic Acids Res. 2002 Jan 15;30(2):439-46
references.pmid: 11788705
references.citation: Nucleic Acids Res. 2005 Oct 20;33(18):5991-9
references.pmid: 16243785
references.citation: Biochimie. 2000 Jun-Jul;82(6-7):559-72
references.pmid: 10946107
references.citation: J Exp Bot. 2012 Feb;63(4):1713-23
references.pmid: 22282538
references.citation: Plant Cell. 2011 Oct;23(10):3824-41
references.pmid: 21990940
references.citation: J Biol Chem. 2000 Mar 31;275(13):9215-21
references.pmid: 10734058
references.citation: Plant Cell Rep. 2007 Jul;26(7):845-59
references.pmid: 17356883
references.citation: Curr Genet. 2006 May;49(5):333-40
references.pmid: 16453112
references.citation: Plant Mol Biol. 1992 May;19(1):149-68
references.pmid: 1600166
references.citation: Science. 2013 Mar 15;339(6125):1316-9
references.pmid: 23493713
references.citation: Biochim Biophys Acta. 2001 Jan 26;1517(2):302-6
references.pmid: 11342113
references.citation: Plant Cell. 2009 Nov;21(11):3623-40
references.pmid: 19903870
references.citation: Plant J. 2013 Jan;73(1):1-13
references.pmid: 22950756
references.citation: Proc Natl Acad Sci U S A. 2010 Jun 8;107(23):10760-4
references.pmid: 20498041
references.citation: Int J Mol Sci. 2012 Sep 25;13(10):12182-94
references.pmid: 23202891
references.citation: Nucleic Acids Res. 1998 Jan 15;26(2):415-9
references.pmid: 9421493
references.citation: Plant Mol Biol. 2003 Feb;51(3):385-99
references.pmid: 12602869
references.citation: Plant J. 2012 Nov;72(4):683-93
references.pmid: 22862786
references.citation: Biosci Biotechnol Biochem. 2004 Apr;68(4):973-7
references.pmid: 15118338
references.citation: Plant J. 2005 Apr;42(2):133-44
references.pmid: 15807777
references.citation: Plant Cell Rep. 2008 Sep;27(9):1467-73
references.pmid: 18553085
references.citation: Plant Cell Physiol. 2004 Apr;45(4):357-68
references.pmid: 15111710
references.citation: Plant Cell Physiol. 2008 Jul;49(7):1084-91
references.pmid: 18535011
references.citation: Nat Rev Genet. 2008 May;9(5):383-95
references.pmid: 18368053
references.citation: Plant Physiol. 2011 Apr;155(4):1520-32
references.pmid: 21346173
references.citation: Trends Plant Sci. 2012 Oct;17(10):575-83
references.pmid: 22784827
references.citation: Nat Rev Genet. 2004 Feb;5(2):123-35
references.pmid: 14735123
references.citation: Genome Biol Evol. 2010;2:888-96
references.pmid: 21071627
references.citation: Mol Biol Evol. 1987 Jul;4(4):406-25
references.pmid: 3447015
references.citation: Int Rev Cytol. 1992;141:233-357
references.pmid: 1452433
references.citation: FEBS Lett. 2000 Sep 8;481(1):47-52
references.pmid: 10984613
references.citation: Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3304-9
references.pmid: 14976253
references.citation: Annu Rev Plant Biol. 2010;61:125-55
references.pmid: 20192740
references.citation: Trends Plant Sci. 2008 Dec;13(12):663-70
references.pmid: 19004664
references.citation: Genetics. 1999 Apr;151(4):1531-45
references.pmid: 10101175
references.citation: Photosynth Res. 2004;82(3):339-49
references.pmid: 16143845
references.citation: Science. 2009 Apr 17;324(5925):353
references.pmid: 19372423
references.citation: Nucleic Acids Res. 2003 Dec 15;31(24):7090-8
references.pmid: 14654684
references.citation: Plant Cell Physiol. 2011 Sep;52(9):1560-8
references.pmid: 21785130
references.citation: Nucleic Acids Res. 2003 Sep 15;31(18):5324-31
references.pmid: 12954768
references.citation: Curr Genet. 2007 Nov;52(5-6):267-74
references.pmid: 17957369
references.citation: Plant Physiol. 2004 Dec;136(4):4285-98
references.pmid: 15563615
references.citation: New Phytol. 2010 Oct;188(2):365-9
references.pmid: 20731783
references.citation: Plant Mol Biol. 2011 Jul;76(3-5):235-49
references.pmid: 21107995
references.citation: Plant Cell Physiol. 2007 Jan;48(1):186-92
references.pmid: 17148693
references.citation: Nucleic Acids Res. 2007;35(2):455-64
references.pmid: 17175536
references.citation: J Plant Physiol. 2011 Aug 15;168(12):1345-60
references.pmid: 21316793
references.citation: Evolution. 1985 Jul;39(4):783-791
references.pmid: 28561359
references.citation: Plant J. 2007 Oct;52(1):124-32
references.pmid: 17651366
references.citation: Biochim Biophys Acta. 2011 Aug;1807(8):945-53
references.pmid: 21029720
references.citation: Plant Cell Physiol. 2001 Oct;42(10):1034-43
references.pmid: 11673617
references.citation: Plant J. 1995 Sep;8(3):457-63
references.pmid: 7550382