Exaptive Evolution of Target of Rapamycin Signaling in Multicellular Eukaryotes

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2020 Jul 11

PMID 32649861

Citations 36

Authors

Jacob O Brunkard

Affiliations

Soon will be listed here.

Abstract

Target of rapamycin (TOR) is a protein kinase that coordinates metabolism with nutrient and energy availability in eukaryotes. TOR and its primary interactors, RAPTOR and LST8, have been remarkably evolutionarily static since they arose in the unicellular last common ancestor of plants, fungi, and animals, but the upstream regulatory mechanisms and downstream effectors of TOR signaling have evolved considerable diversity in these separate lineages. Here, I focus on the roles of exaptation and adaptation in the evolution of novel signaling axes in the TOR network in multicellular eukaryotes, concentrating especially on amino acid sensing, cell-cell signaling, and cell differentiation.

Citing Articles

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DRMY1 promotes robust morphogenesis in Arabidopsis by sustaining the translation of cytokinin-signaling inhibitor proteins.

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References

Han J, Jeong S, Park M, Kim G, Kwon N, Kim H . Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell. 2012; 149(2):410-24. DOI: 10.1016/j.cell.2012.02.044. View

Bonfils G, Jaquenoud M, Bontron S, Ostrowicz C, Ungermann C, De Virgilio C . Leucyl-tRNA synthetase controls TORC1 via the EGO complex. Mol Cell. 2012; 46(1):105-10. DOI: 10.1016/j.molcel.2012.02.009. View

Kindrachuk J, Ork B, Hart B, Mazur S, Holbrook M, Frieman M . Antiviral potential of ERK/MAPK and PI3K/AKT/mTOR signaling modulation for Middle East respiratory syndrome coronavirus infection as identified by temporal kinome analysis. Antimicrob Agents Chemother. 2014; 59(2):1088-99. PMC: 4335870. DOI: 10.1128/AAC.03659-14. View

Lee J, Wang X, Cui W, Sager R, Modla S, Czymmek K . A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell. 2011; 23(9):3353-73. PMC: 3203451. DOI: 10.1105/tpc.111.087742. View

Zhang N, Meng Y, Li X, Zhou Y, Ma L, Fu L . Metabolite-mediated TOR signaling regulates the circadian clock in . Proc Natl Acad Sci U S A. 2019; 116(51):25395-25397. PMC: 6926049. DOI: 10.1073/pnas.1913095116. View

Henriques R, Bogre L, Horvath B, Magyar Z . Balancing act: matching growth with environment by the TOR signalling pathway. J Exp Bot. 2014; 65(10):2691-701. DOI: 10.1093/jxb/eru049. View

Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolai M . The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep. 2007; 8(9):864-70. PMC: 1973950. DOI: 10.1038/sj.embor.7401043. View

Li X, Cai W, Liu Y, Li H, Fu L, Liu Z . Differential TOR activation and cell proliferation in root and shoot apexes. Proc Natl Acad Sci U S A. 2017; 114(10):2765-2770. PMC: 5347562. DOI: 10.1073/pnas.1618782114. View

Lee J, Cho U, Karin M . Sestrin regulation of TORC1: Is Sestrin a leucine sensor?. Sci Signal. 2016; 9(431):re5. PMC: 4902175. DOI: 10.1126/scisignal.aaf2885. View

10.

Wolfson R, Sabatini D . The Dawn of the Age of Amino Acid Sensors for the mTORC1 Pathway. Cell Metab. 2017; 26(2):301-309. PMC: 5560103. DOI: 10.1016/j.cmet.2017.07.001. View

11.

Fu L, Wang P, Xiong Y . Target of Rapamycin Signaling in Plant Stress Responses. Plant Physiol. 2020; 182(4):1613-1623. PMC: 7140942. DOI: 10.1104/pp.19.01214. View

12.

Levy A, Erlanger M, Rosenthal M, Epel B . A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis. Plant J. 2007; 49(4):669-82. DOI: 10.1111/j.1365-313X.2006.02986.x. View

13.

Bar-Peled L, Chantranupong L, Cherniack A, Chen W, Ottina K, Grabiner B . A Tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1. Science. 2013; 340(6136):1100-6. PMC: 3728654. DOI: 10.1126/science.1232044. View

14.

Turgeon R . The role of phloem loading reconsidered. Plant Physiol. 2010; 152(4):1817-23. PMC: 2850027. DOI: 10.1104/pp.110.153023. View

15.

Saxton R, Knockenhauer K, Wolfson R, Chantranupong L, Pacold M, Wang T . Structural basis for leucine sensing by the Sestrin2-mTORC1 pathway. Science. 2015; 351(6268):53-8. PMC: 4698039. DOI: 10.1126/science.aad2087. View

16.

Schaufelberger M, Galbier F, Herger A, de Brito Francisco R, Roffler S, Clement G . Mutations in the Arabidopsis ROL17/isopropylmalate synthase 1 locus alter amino acid content, modify the TOR network, and suppress the root hair cell development mutant lrx1. J Exp Bot. 2019; 70(8):2313-2323. PMC: 6463047. DOI: 10.1093/jxb/ery463. View

17.

Montane M, Menand B . ATP-competitive mTOR kinase inhibitors delay plant growth by triggering early differentiation of meristematic cells but no developmental patterning change. J Exp Bot. 2013; 64(14):4361-74. PMC: 3808319. DOI: 10.1093/jxb/ert242. View

18.

Chuluunbaatar U, Roller R, Feldman M, Brown S, Shokat K, Mohr I . Constitutive mTORC1 activation by a herpesvirus Akt surrogate stimulates mRNA translation and viral replication. Genes Dev. 2010; 24(23):2627-39. PMC: 2994037. DOI: 10.1101/gad.1978310. View

19.

Schepetilnikov M, Kobayashi K, Geldreich A, Caranta C, Robaglia C, Keller M . Viral factor TAV recruits TOR/S6K1 signalling to activate reinitiation after long ORF translation. EMBO J. 2011; 30(7):1343-56. PMC: 3094109. DOI: 10.1038/emboj.2011.39. View

20.

Meade N, Furey C, Li H, Verma R, Chai Q, Rollins M . Poxviruses Evade Cytosolic Sensing through Disruption of an mTORC1-mTORC2 Regulatory Circuit. Cell. 2018; 174(5):1143-1157.e17. PMC: 6172959. DOI: 10.1016/j.cell.2018.06.053. View