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PMID: 30208757 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Autophagy regulates glucose-mediated root meristem activity by modulating ROS production in Arabidopsis.

Autophagy ·Vol. 15 ·No. 3 ·2019-00-00 ·Pages 407-422

Huang L, Yu LJ, Zhang X, Fan B, Wang FZ, Dai YS, Qi H, Zhou Y, Xie LJ, Xiao S

Abstract

Glucose produced from photosynthesis is a key nutrient signal regulating root meristem activity in plants; however, the underlying mechanisms remain poorly understood. Here, we show that, by modulating reactive oxygen species (ROS) levels, the conserved macroautophagy/autophagy degradation pathway contributes to glucose-regulated root meristem maintenance. In Arabidopsis thaliana roots, a short exposure to elevated glucose temporarily suppresses constitutive autophagosome formation. The autophagy-defective autophagy-related gene (atg) mutants have enhanced tolerance to glucose, established downstream of the glucose sensors, and accumulate less glucose-induced ROS in the root tips. Moreover, the enhanced root meristem activities in the atg mutants are associated with improved auxin gradients and auxin responses. By acting with AT4G39850/ABCD1 (ATP-binding cassette D1; Formerly PXA1/peroxisomal ABC transporter 1), autophagy plays an indispensable role in the glucose-promoted degradation of root peroxisomes, and the atg mutant phenotype is partially rescued by the overexpression of ABCD1. Together, our findings suggest that autophagy is an essential mechanism for glucose-mediated maintenance of the root meristem. Abbreviation: ABA: abscisic acid; ABCD1: ATP-binding cassette D1; ABO: ABA overly sensitive; AsA: ascorbic acid; ATG: autophagy related; CFP: cyan fluorescent protein; Co-IP: co-immunoprecipitation; DAB: 3',3'-diaininobenzidine; DCFH-DA: 2',7'-dichlorodihydrofluorescin diacetate; DR5: a synthetic auxin response element consists of tandem direct repeats of 11 bp that included the auxin-responsive TGTCTC element; DZ: differentiation zone; EZ, elongation zone; GFP, green fluorescent protein; GSH, glutathione; GUS: β-glucuronidase; HXK1: hexokinase 1; H2O2: hydrogen peroxide; IAA: indole-3-acetic acid; IBA: indole-3-butyric acid; KIN10/11: SNF1 kinase homolog 10/11; MDC: monodansylcadaverine; MS: Murashige and Skoog; MZ: meristem zone; NBT: nitroblue tetrazolium; NPA: 1-N-naphtylphthalamic acid; OxIAA: 2-oxindole-3-acetic acid; PIN: PIN-FORMED; PLT: PLETHORA; QC: quiescent center; RGS1: Regulator of G-protein signaling 1; ROS: reactive oxygen species; SCR: SCARECROW; SHR, SHORT-ROOT; SKL: Ser-Lys-Leu; SnRK1: SNF1-related kinase 1; TOR: target of rapamycin; UPB1: UPBEAT1; WOX5: WUSCHEL related homeobox 5; Y2H: yeast two-hybrid; YFP: yellow fluorescent protein.

Keywords
Autophagy glucose peroxisome reactive oxygen species root meristem
MeSH Terms
ATP Binding Cassette Transporter, Subfamily D, Member 1/metabolism Arabidopsis/genetics,metabolism Arabidopsis Proteins/metabolism Autophagosomes/metabolism Autophagy/drug effects,genetics Autophagy-Related Proteins/genetics,metabolism Gene Expression Regulation, Plant Glucose/pharmacology Indoleacetic Acids/metabolism Meristem/metabolism Peroxisomes/metabolism Plant Roots/genetics,metabolism Reactive Oxygen Species/metabolism Signal Transduction/drug effects,genetics
Chemicals
ATP Binding Cassette Transporter, Subfamily D, Member 1 Arabidopsis Proteins Autophagy-Related Proteins Indoleacetic Acids Reactive Oxygen Species Glucose
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Huang Li
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Yu Lu-Jun
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Zhang Xue
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Fan Biao
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Wang Feng-Zhu
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Dai Yang-Shuo
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Qi Hua
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Zhou Ying
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Xie Li-Juan
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
Xiao Shi
a State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences , Sun Yat-sen University , Guangzhou , China.
References (80)
80 references, click to expand
  1. The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis.
    Plant Cell. 2011 Oct;23(10):3761-79 PMID: 21984698
  2. Control of root meristem size by DA1-RELATED PROTEIN2 in Arabidopsis.
    Plant Physiol. 2013 Mar;161(3):1542-56 PMID: 23296689
  3. Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth.
    Plant Cell. 2013 Dec;25(12):4956-66 PMID: 24368791
  4. Autophagy: pathways for self-eating in plant cells.
    Annu Rev Plant Biol. 2012;63:215-37 PMID: 22242963
  5. Environmental Control of Root System Biology.
    Annu Rev Plant Biol. 2016 Apr 29;67:619-42 PMID: 26905656
  6. Function and regulation of transcription factors involved in root apical meristem and stem cell maintenance.
    Front Plant Sci. 2015 Jul 06;6:505 PMID: 26217359
  7. Arabidopsis Hexokinase-Like1 and Hexokinase1 form a critical node in mediating plant glucose and ethylene responses.
    Plant Physiol. 2012 Apr;158(4):1965-75 PMID: 22366209
  8. Interaction between glucose and brassinosteroid during the regulation of lateral root development in Arabidopsis.
    Plant Physiol. 2015 May;168(1):307-20 PMID: 25810094
  9. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants.
    Plant J. 2007 Sep;51(6):1126-36 PMID: 17666025
  10. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development.
    Nature. 2007 Oct 25;449(7165):1053-7 PMID: 17960244
  11. The plant-specific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis.
    Plant Physiol. 2010 Oct;154(2):772-83 PMID: 20699397
  12. A central integrator of transcription networks in plant stress and energy signalling.
    Nature. 2007 Aug 23;448(7156):938-42 PMID: 17671505
  13. Glucose inhibits root meristem growth via ABA INSENSITIVE 5, which represses PIN1 accumulation and auxin activity in Arabidopsis.
    Plant Cell Environ. 2014 Jun;37(6):1338-50 PMID: 24237322
  14. TRAF Family Proteins Regulate Autophagy Dynamics by Modulating AUTOPHAGY PROTEIN6 Stability in Arabidopsis.
    Plant Cell. 2017 Apr;29(4):890-911 PMID: 28351989
  15. Autophagy and the integrated stress response.
    Mol Cell. 2010 Oct 22;40(2):280-93 PMID: 20965422
  16. Hormonal regulation of stem cell maintenance in roots.
    J Exp Bot. 2013 Mar;64(5):1153-65 PMID: 23183258
  17. Sugar and hormone connections.
    Trends Plant Sci. 2003 Mar;8(3):110-6 PMID: 12663220
  18. AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells.
    Plant Cell Physiol. 2006 Dec;47(12):1641-52 PMID: 17085765
  19. Redox regulation of plant stem cell fate.
    EMBO J. 2017 Oct 2;36(19):2844-2855 PMID: 28838936
  20. Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis.
    Development. 1993 Sep;119(1):57-70 PMID: 8275864
  21. Plant autophagy--more than a starvation response.
    Curr Opin Plant Biol. 2007 Dec;10(6):587-93 PMID: 17702643
  22. Auxin metabolism in the root apical meristem.
    Plant Physiol. 2000 Mar;122(3):925-32 PMID: 10712557
  23. The gene encoding Arabidopsis acyl-CoA-binding protein 3 is pathogen inducible and subject to circadian regulation.
    J Exp Bot. 2012 May;63(8):2985-3000 PMID: 22345636
  24. Control of Arabidopsis root development.
    Annu Rev Plant Biol. 2012;63:563-90 PMID: 22404466
  25. Glucose-TOR signalling reprograms the transcriptome and activates meristems.
    Nature. 2013 Apr 11;496(7444):181-6 PMID: 23542588
  26. Hexokinase as a sugar sensor in higher plants.
    Plant Cell. 1997 Jan;9(1):5-19 PMID: 9014361
  27. Production of reactive oxygen intermediates (O(2)(.-), H(2)O(2), and (.)OH) by maize roots and their role in wall loosening and elongation growth.
    Plant Physiol. 2004 Oct;136(2):3114-23; discussion 3001 PMID: 15466236
  28. The AMP-Activated Protein Kinase KIN10 Is Involved in the Regulation of Autophagy in Arabidopsis.
    Front Plant Sci. 2017 Jul 10;8:1201 PMID: 28740502
  29. A P-Loop NTPase Regulates Quiescent Center Cell Division and Distal Stem Cell Identity through the Regulation of ROS Homeostasis in Arabidopsis Root.
    PLoS Genet. 2016 Sep 01;12(9):e1006175 PMID: 27583367
  30. Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10294-9 PMID: 9707641
  31. Sugars as signaling molecules.
    Curr Opin Plant Biol. 1999 Oct;2(5):410-8 PMID: 10508760
  32. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root.
    Cell. 1999 Nov 24;99(5):463-72 PMID: 10589675
  33. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis.
    Nat Protoc. 2007;2(7):1565-72 PMID: 17585298
  34. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants.
    J Exp Bot. 2006;57(3):449-59 PMID: 16397003
  35. Mutations in the Arabidopsis peroxisomal ABC transporter COMATOSE allow differentiation between multiple functions in planta: insights from an allelic series.
    Mol Biol Cell. 2009 Jan;20(1):530-43 PMID: 19019987
  36. Regulation of macroautophagy by mTOR and Beclin 1 complexes.
    Biochimie. 2008 Feb;90(2):313-23 PMID: 17928127
  37. Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases.
    New Phytol. 2007;174(2):332-41 PMID: 17388896
  38. Autophagy in plants and phytopathogens.
    FEBS Lett. 2010 Apr 2;584(7):1350-8 PMID: 20079356
  39. Role of plant autophagy in stress response.
    Protein Cell. 2011 Oct;2(10):784-91 PMID: 22058033
  40. ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci.
    Plant J. 2010 May;62(3):483-93 PMID: 20136727
  41. Cytokinin interplay with ethylene, auxin, and glucose signaling controls Arabidopsis seedling root directional growth.
    Plant Physiol. 2011 Aug;156(4):1851-66 PMID: 21666052
  42. Auxin control of root development.
    Cold Spring Harb Perspect Biol. 2010 Jun;2(6):a001537 PMID: 20516130
  43. ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis.
    PLoS Genet. 2014 Dec 18;10(12):e1004791 PMID: 25522358
  44. ABNORMAL INFLORESCENCE MERISTEM1 Functions in Salicylic Acid Biosynthesis to Maintain Proper Reactive Oxygen Species Levels for Root Meristem Activity in Rice.
    Plant Cell. 2017 Mar;29(3):560-574 PMID: 28298519
  45. Evidence of oxidative attenuation of auxin signalling.
    J Exp Bot. 2013 Jun;64(9):2629-39 PMID: 23709674
  46. Dissecting regulatory pathways of G1/S control in Arabidopsis: common and distinct targets of CYCD3;1, E2Fa and E2Fc.
    Plant Mol Biol. 2009 Nov;71(4-5):345-65 PMID: 19662336
  47. Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence.
    Plant Cell. 2010 May;22(5):1463-82 PMID: 20442372
  48. TOR is a negative regulator of autophagy in Arabidopsis thaliana.
    PLoS One. 2010 Jul 29;5(7):e11883 PMID: 20686696
  49. An overview of autophagy: morphology, mechanism, and regulation.
    Antioxid Redox Signal. 2014 Jan 20;20(3):460-73 PMID: 23725295
  50. SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana.
    PLoS One. 2017 Aug 4;12(8):e0182591 PMID: 28783755
  51. Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana.
    Autophagy. 2015;11(12):2233-46 PMID: 26566261
  52. DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling.
    Plant Cell. 2012 May;24(5):1815-33 PMID: 22652060
  53. The α/β hydrolase CGI-58 and peroxisomal transport protein PXA1 coregulate lipid homeostasis and signaling in Arabidopsis.
    Plant Cell. 2013 May;25(5):1726-39 PMID: 23667126
  54. Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance.
    Curr Biol. 2003 Aug 19;13(16):1435-41 PMID: 12932329
  55. The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness.
    Plant Cell. 2009 Sep;21(9):2733-49 PMID: 19794119
  56. The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development.
    Plant Cell. 2000 Jan;12(1):97-110 PMID: 10634910
  57. Gas chromatography mass spectrometry-based metabolite profiling in plants.
    Nat Protoc. 2006;1(1):387-96 PMID: 17406261
  58. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana.
    Development. 2004 Feb;131(3):657-68 PMID: 14711878
  59. Autophagy in Plants--What's New on the Menu?
    Trends Plant Sci. 2016 Feb;21(2):134-144 PMID: 26598298
  60. Plant hormone cross-talk: the pivot of root growth.
    J Exp Bot. 2015 Feb;66(4):1113-21 PMID: 25628331
  61. Autophagy as a mediator of life and death in plants.
    Curr Opin Plant Biol. 2017 Dec;40:122-130 PMID: 28946008
  62. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root.
    Cell. 2010 Nov 12;143(4):606-16 PMID: 21074051
  63. Master Regulators in Plant Glucose Signaling Networks.
    J Plant Biol. 2014 Apr;57(2):67-79 PMID: 25530701
  64. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling.
    Science. 2003 Apr 11;300(5617):332-6 PMID: 12690200
  65. AtRGS1 function in Arabidopsis thaliana.
    Methods Enzymol. 2004;389:338-50 PMID: 15313575
  66. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem.
    Genes Dev. 2003 Feb 1;17(3):354-8 PMID: 12569126
  67. Sugar and phytohormone response pathways: navigating a signalling network.
    J Exp Bot. 2004 Jan;55(395):253-64 PMID: 14673024
  68. Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid.
    Plant Cell. 2013 Oct;25(10):3858-70 PMID: 24163311
  69. Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development.
    PLoS One. 2009;4(2):e4502 PMID: 19223973
  70. Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot.
    Development. 2000 Feb;127(3):595-603 PMID: 10631180
  71. Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis.
    Plant Cell. 2013 Dec;25(12):4967-83 PMID: 24368788
  72. Reactive oxygen species and autophagy in plants and algae.
    Plant Physiol. 2012 Sep;160(1):156-64 PMID: 22744983
  73. One-step transformation of yeast in stationary phase.
    Curr Genet. 1992 Jan;21(1):83-4 PMID: 1735128
  74. Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase.
    J Exp Bot. 2003 Jan;54(382):467-75 PMID: 12508057
  75. TOR-Dependent and -Independent Pathways Regulate Autophagy in Arabidopsis thaliana.
    Front Plant Sci. 2017 Jul 11;8:1204 PMID: 28744293
  76. Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes.
    Genetics. 2000 Nov;156(3):1323-37 PMID: 11063705
  77. Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis.
    Nat Cell Biol. 2012 Oct;14(10):1079-88 PMID: 22940907
  78. Reactive Oxygen Species: From Harmful Molecules to Fine-Tuning Regulators of Stem Cell Niche Maintenance.
    PLoS Genet. 2016 Sep 01;12(9):e1006251 PMID: 27583383
  79. AtMMS21, an SMC5/6 complex subunit, is involved in stem cell niche maintenance and DNA damage responses in Arabidopsis roots.
    Plant Physiol. 2013 Apr;161(4):1755-68 PMID: 23426194
  80. Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control.
    Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2745-50 PMID: 11038608
Article Info
Journal
Autophagy
Abbr.
Autophagy
ISSN
1554-8635
Published
2019-00-00
Epub
2018-00-22
Pages
407-422
Language
English
Region
United States
NLM ID
101265188
PMCID
PMC6351127
Subset
IM
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