A molecular atlas of plastid and mitochondrial proteins reveals organellar remodeling during plant evolutionary transitions from algae to angiosperms.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Source:
      Publisher: Public Library of Science Country of Publication: United States NLM ID: 101183755 Publication Model: eCollection Cited Medium: Internet ISSN: 1545-7885 (Electronic) Linking ISSN: 15449173 NLM ISO Abbreviation: PLoS Biol Subsets: MEDLINE
    • Publication Information:
      Original Publication: San Francisco, CA : Public Library of Science, [2003]-
    • Subject Terms:
    • Abstract:
      Algae and plants carry 2 organelles of endosymbiotic origin that have been co-evolving in their host cells for more than a billion years. The biology of plastids and mitochondria can differ significantly across major lineages and organelle changes likely accompanied the adaptation to new ecological niches such as the terrestrial habitat. Based on organelle proteome data and the genomes of 168 phototrophic (Archaeplastida) versus a broad range of 518 non-phototrophic eukaryotes, we screened for changes in plastid and mitochondrial biology across 1 billion years of evolution. Taking into account 331,571 protein families (or orthogroups), we identify 31,625 protein families that are unique to primary plastid-bearing eukaryotes. The 1,906 and 825 protein families are predicted to operate in plastids and mitochondria, respectively. Tracing the evolutionary history of these protein families through evolutionary time uncovers the significant remodeling the organelles experienced from algae to land plants. The analyses of gained orthogroups identifies molecular changes of organelle biology that connect to the diversification of major lineages and facilitated major transitions from chlorophytes en route to the global greening and origin of angiosperms.
      Competing Interests: The authors have declared that no competing interests exist.
      (Copyright: © 2024 K. Raval et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)
    • References:
      Planta. 2006 Aug;224(3):556-68. (PMID: 16514542)
      Trends Plant Sci. 2016 Jun;21(6):467-476. (PMID: 26895731)
      Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7308-13. (PMID: 9207087)
      Plant Physiol. 2016 Jan;170(1):263-72. (PMID: 26518344)
      Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):12040-5. (PMID: 20551224)
      Proc Natl Acad Sci U S A. 2018 Jun 19;115(25):6506-6511. (PMID: 29784790)
      Plant Physiol. 2011 Feb;155(2):851-65. (PMID: 21173024)
      Genome Biol Evol. 2021 Jul 6;13(7):. (PMID: 33950183)
      Nature. 2019 Oct;574(7780):679-685. (PMID: 31645766)
      Annu Rev Plant Biol. 2014;65:443-72. (PMID: 24471836)
      Nat Commun. 2013;4:1941. (PMID: 23770768)
      Front Plant Sci. 2020 Feb 04;11:7. (PMID: 32117358)
      Plant Physiol. 2014 Oct;166(2):808-28. (PMID: 25165398)
      Plant Cell Physiol. 2021 Feb 4;61(12):2004-2017. (PMID: 33067620)
      Plant Physiol. 2022 Aug 29;190(1):72-84. (PMID: 35642902)
      Philos Trans R Soc Lond B Biol Sci. 2014 Mar 03;369(1640):20130226. (PMID: 24591713)
      Nat Protoc. 2017 Jun;12(6):1110-1135. (PMID: 28471460)
      J Mol Biol. 2000 Feb 4;295(5):1103-12. (PMID: 10653689)
      Commun Biol. 2021 Mar 25;4(1):412. (PMID: 33767367)
      PLoS Biol. 2024 May 7;22(5):e3002608. (PMID: 38713727)
      iScience. 2020 Mar 27;23(3):100896. (PMID: 32088393)
      Mol Plant. 2017 May 1;10(5):749-763. (PMID: 28412544)
      Plant Physiol. 2010 Nov;154(3):1172-82. (PMID: 20841453)
      Proc Natl Acad Sci U S A. 2013 Mar 26;110(13):5247-52. (PMID: 23503846)
      Sci Adv. 2023 Aug 9;9(32):eadj4493. (PMID: 37556561)
      Front Plant Sci. 2020 Aug 11;11:1198. (PMID: 32849743)
      Plant Cell. 2010 Aug;22(8):2630-41. (PMID: 20682837)
      Mol Plant. 2011 Mar;4(2):229-40. (PMID: 21220584)
      Elife. 2022 Nov 10;11:. (PMID: 36355038)
      Genes Dev. 2012 May 15;26(10):1022-7. (PMID: 22549728)
      Plant Cell. 2018 Aug;30(8):1807-1823. (PMID: 29967285)
      Front Plant Sci. 2014 Oct 13;5:535. (PMID: 25352854)
      J Biol Chem. 2013 Jul 12;288(28):20267-79. (PMID: 23720747)
      Plant J. 2016 Mar;85(5):607-21. (PMID: 26800847)
      PLoS One. 2018 Aug 31;13(8):e0203442. (PMID: 30169501)
      Plant J. 2021 Nov;108(4):912-959. (PMID: 34528296)
      Physiol Plant. 2014 Mar;150(3):477-92. (PMID: 24111559)
      Proc Natl Acad Sci U S A. 2017 Aug 1;114(31):E6361-E6370. (PMID: 28716924)
      J Plant Res. 2013 May;126(3):403-14. (PMID: 23076438)
      Philos Trans R Soc Lond B Biol Sci. 2020 Jun 22;375(1801):20190410. (PMID: 32362265)
      Curr Biol. 2015 Oct 5;25(19):2527-34. (PMID: 26387714)
      Planta. 2010 Jul;232(2):471-81. (PMID: 20473685)
      Nat Microbiol. 2016 Sep 12;1(11):16160. (PMID: 27617693)
      Elife. 2023 Mar 02;12:. (PMID: 36862572)
      Nat Plants. 2020 Feb;6(2):107-118. (PMID: 32042158)
      New Phytol. 2018 Mar;217(4):1428-1434. (PMID: 29318635)
      Mol Biol Evol. 2015 Dec;32(12):3186-93. (PMID: 26341299)
      Plant Cell Physiol. 2020 Jun 1;61(6):1144-1157. (PMID: 32219438)
      Front Plant Sci. 2014 Apr 16;5:135. (PMID: 24795732)
      Proc Natl Acad Sci U S A. 2016 Nov 15;113(46):E7307-E7316. (PMID: 27799549)
      Nat Ecol Evol. 2022 Nov;6(11):1634-1643. (PMID: 36175544)
      Cell. 2020 May 28;181(5):1097-1111.e12. (PMID: 32442406)
      Int J Mol Sci. 2022 Mar 04;23(5):. (PMID: 35269961)
      Cell. 2019 Nov 14;179(5):1057-1067.e14. (PMID: 31730849)
      Protoplasma. 2014 Nov;251(6):1491-509. (PMID: 24802109)
      Plant J. 2004 May;38(3):448-59. (PMID: 15086805)
      Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14693-8. (PMID: 19666500)
      Plant Physiol. 2012 Oct;160(2):638-52. (PMID: 22864585)
      Plant Cell. 2022 Jan 20;34(1):228-246. (PMID: 34459922)
      Plant Sci. 2018 Jan;266:117-129. (PMID: 29241561)
      Plant Physiol. 2015 Jul;168(3):1140-51. (PMID: 25944826)
      Curr Opin Plant Biol. 2017 Jun;37:63-69. (PMID: 28433946)
      Plant J. 2018 Feb;93(3):515-533. (PMID: 29237241)
      J Exp Bot. 2015 Apr;66(7):2067-77. (PMID: 25740923)
      Nat Ecol Evol. 2017 Jun 19;1:193. (PMID: 29388565)
      Proc Natl Acad Sci U S A. 2015 Oct 13;112(41):12876-81. (PMID: 26424450)
      Plant Physiol. 2011 Apr;155(4):1520-32. (PMID: 21346173)
      Front Genet. 2021 Sep 29;12:757109. (PMID: 34659369)
      Arabidopsis Book. 2013;11:e0161. (PMID: 23505340)
      Plant Cell. 2018 Sep;30(9):2082-2098. (PMID: 30099384)
      J Exp Bot. 2022 Nov 19;73(21):7182-7197. (PMID: 36055768)
      Front Plant Sci. 2022 Mar 14;13:863076. (PMID: 35360315)
      Plant Physiol. 2020 Dec;184(4):1998-2010. (PMID: 32934149)
      Cell. 2017 Oct 5;171(2):287-304.e15. (PMID: 28985561)
      Curr Biol. 2009 Jan 27;19(2):151-6. (PMID: 19135368)
      Plant Physiol. 2002 Jan;128(1):223-35. (PMID: 11788768)
      Annu Rev Plant Biol. 2013;64:583-607. (PMID: 23451781)
      J Plant Physiol. 2012 Aug 15;169(12):1212-5. (PMID: 22572242)
      Mol Biol Evol. 2018 Aug 1;35(8):1869-1886. (PMID: 29688518)
      DNA Res. 2019 Aug 1;26(4):287-299. (PMID: 31098614)
      Photosynth Res. 2013 Oct;116(2-3):427-36. (PMID: 23873414)
      Curr Genet. 2011 Jun;57(3):151-68. (PMID: 21533645)
      Plant Cell. 2008 Aug;20(8):2190-204. (PMID: 18689504)
      J Cell Biol. 2004 May 10;165(3):323-34. (PMID: 15138290)
      Science. 2012 Nov 2;338(6107):655-9. (PMID: 23118188)
      Plant Cell. 2008 Mar;20(3):502-7. (PMID: 18359853)
      Trends Microbiol. 2016 Jul;24(7):525-534. (PMID: 27040918)
      Nat Rev Mol Cell Biol. 2013 Dec;14(12):787-802. (PMID: 24263360)
      J Phycol. 2015 Aug;51(4):624-36. (PMID: 26986787)
      Nucleic Acids Res. 2017 Jan 4;45(D1):D353-D361. (PMID: 27899662)
      Plant Physiol Biochem. 2015 Feb;87:61-72. (PMID: 25557464)
      Plant Physiol. 2016 Feb;170(2):947-55. (PMID: 26620523)
      J Exp Bot. 2020 Feb 19;71(4):1226-1238. (PMID: 31730153)
      Annu Rev Plant Biol. 2014;65:415-42. (PMID: 24471833)
      Proc Natl Acad Sci U S A. 2016 Feb 23;113(8):E1116-25. (PMID: 26862170)
      Food Energy Secur. 2022 Mar 17;12(2):e379. (PMID: 38440693)
      Nat Plants. 2020 Mar;6(3):259-272. (PMID: 32170292)
      J Biol Chem. 2013 Nov 1;288(44):31540-8. (PMID: 24047899)
      Plant Physiol. 2018 Jun;177(2):684-697. (PMID: 29686056)
      Front Plant Sci. 2017 Jun 08;8:987. (PMID: 28642782)
      Proc Natl Acad Sci U S A. 2019 Dec 3;116(49):24900-24906. (PMID: 31732672)
      Plant Mol Biol. 2020 Sep;104(1-2):39-53. (PMID: 32564178)
      Plant Cell Physiol. 2009 May;50(5):956-69. (PMID: 19318374)
      Nat Commun. 2021 Mar 25;12(1):1879. (PMID: 33767194)
      Plant Cell Rep. 2011 Jan;30(1):37-48. (PMID: 20972793)
      Curr Biol. 2011 Jul 26;21(14):R540-1. (PMID: 21783030)
      J Integr Plant Biol. 2012 Feb;54(2):87-98. (PMID: 22353560)
      Nat Struct Mol Biol. 2010 Jun;17(6):740-4. (PMID: 20473316)
      J Plant Physiol. 2016 Dec 1;207:78-83. (PMID: 27835768)
      Nat Commun. 2014 May 28;5:3978. (PMID: 24865297)
      J Biol Chem. 2009 Sep 11;284(37):25343-52. (PMID: 19617353)
      Plant J. 2020 Mar;101(5):1040-1056. (PMID: 31630458)
      Genome Biol. 2022 Mar 28;23(1):85. (PMID: 35346327)
      Plant J. 2008 Oct;56(1):157-68. (PMID: 18557832)
      Genome Biol. 2019 Nov 14;20(1):238. (PMID: 31727128)
      Plant Physiol. 2010 Jul;153(3):1016-30. (PMID: 20457805)
      Plant Cell. 2017 Jul;29(7):1657-1677. (PMID: 28684429)
      Cells. 2021 Jan 21;10(2):. (PMID: 33494215)
      Plant Physiol. 2013 Oct;163(2):867-81. (PMID: 23969600)
      Nucleic Acids Res. 2009 Jan;37(Database issue):D969-74. (PMID: 18832363)
      Plant Physiol Biochem. 2021 Feb;159:148-159. (PMID: 33360238)
      Plant Physiol. 2015 May;168(1):132-43. (PMID: 25792253)
      Plant J. 2024 Jan;117(2):385-403. (PMID: 37733835)
      Nucleic Acids Res. 2021 Jan 8;49(D1):D412-D419. (PMID: 33125078)
      Proc Natl Acad Sci U S A. 2007 Jun 12;104(24):10270-5. (PMID: 17540731)
      Nat Methods. 2015 Jan;12(1):59-60. (PMID: 25402007)
      Trends Cell Biol. 2016 Dec;26(12):894-905. (PMID: 27524662)
      Trends Plant Sci. 2022 Sep;27(9):847-857. (PMID: 35739050)
      Proc Natl Acad Sci U S A. 2008 Jul 1;105(26):9123-8. (PMID: 18567673)
      Nat Plants. 2015 Mar 30;1(4):15035. (PMID: 27247035)
      Trends Plant Sci. 2023 Mar;28(3):312-329. (PMID: 36328872)
      Cell. 2018 Jul 12;174(2):448-464.e24. (PMID: 30007417)
      Nat Ecol Evol. 2020 Sep;4(9):1220-1231. (PMID: 32572216)
      Proc Biol Sci. 2001 Jul 7;268(1474):1417-22. (PMID: 11429143)
      Trends Plant Sci. 2005 Nov;10(11):521-5. (PMID: 16169274)
      Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86. (PMID: 22110026)
      New Phytol. 2014 Dec;204(4):765-81. (PMID: 25263843)
      Trends Cell Biol. 2021 Jan;31(1):9-16. (PMID: 33121860)
      J Biol Chem. 2005 Mar 4;280(9):8143-9. (PMID: 15598655)
      Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):20248-53. (PMID: 22128333)
      Front Plant Sci. 2022 Apr 21;13:880423. (PMID: 35528945)
      PLoS Biol. 2018 Sep 13;16(9):e2005895. (PMID: 30212465)
      J Exp Bot. 2011 Mar;62(6):1775-801. (PMID: 21220783)
      Plant Mol Biol. 2022 Mar;108(4-5):307-323. (PMID: 35006475)
      Elife. 2020 Apr 16;9:. (PMID: 32297859)
      Annu Rev Plant Biol. 2023 May 22;74:285-312. (PMID: 36854476)
      Plant Cell. 2012 Jul;24(7):3026-39. (PMID: 22797473)
      Nucleic Acids Res. 2016 Jan 4;44(D1):D733-45. (PMID: 26553804)
      J Cell Sci. 2018 Jan 29;131(2):. (PMID: 28893840)
      Phytochemistry. 2021 Apr;184:112652. (PMID: 33535085)
      Nat Plants. 2020 Feb;6(2):95-106. (PMID: 31844283)
      Plant J. 2021 Aug;107(4):975-1002. (PMID: 34165823)
      Genome Biol. 2015 Aug 06;16:157. (PMID: 26243257)
      PLoS One. 2015 Mar 24;10(3):e0121943. (PMID: 25803274)
      Nature. 2015 Aug 27;524(7566):427-32. (PMID: 26287458)
      Dev Cell. 2004 Feb;6(2):229-40. (PMID: 14960277)
      PLoS One. 2013;8(3):e59001. (PMID: 23536846)
      Physiol Plant. 2013 Jul;148(3):408-21. (PMID: 23082802)
      BMC Plant Biol. 2015 Apr 09;15:98. (PMID: 25886741)
      Plant Physiol. 2014 Apr;164(4):2081-95. (PMID: 24515833)
      Plant Cell Environ. 2014 Sep;37(9):2201-10. (PMID: 24506786)
      Evolution. 1997 Dec;51(6):1699-1711. (PMID: 28565128)
      Biochem Biophys Res Commun. 2019 Aug 6;515(4):699-705. (PMID: 31186142)
    • Accession Number:
      0 (Mitochondrial Proteins)
      0 (Plant Proteins)
      0 (Proteome)
    • Publication Date:
      Date Created: 20240507 Date Completed: 20240529 Latest Revision: 20240531
    • Publication Date:
      20240531
    • Accession Number:
      PMC11135702
    • Accession Number:
      10.1371/journal.pbio.3002608
    • Accession Number:
      38713727