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Research Paper

Selective autophagy regulates heat stress memory in Arabidopsis by NBR1-mediated targeting of HSP90.1 and ROF1

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Pages 2184-2199 | Received 31 Oct 2019, Accepted 28 Aug 2020, Published online: 24 Sep 2020

References

  • McClung CR, Davis SJ. Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr Biol. 2010;20:1086–1092.
  • Mittler R, Finka A, Goloubinoff P. How do plants feel the heat? Trends Biochem Sci. 2012;37:118–125.
  • Bokszczanin KL. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front Plant Sci. 2013;4:315.
  • Niu Y, Xiang Y. An overview of biomembrane functions in plant responses to high-temperature stress. Front Plant Sci. 2018;9:915.
  • Chen B, Retzlaff M, Roos T, et al. Cellular strategies of protein quality control. Cold Spring Harbor Perspect Biol. 2011;3:a004374.
  • Bita C, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci. 2013;4:273.
  • Liu J, Feng L, Li J, et al. Genetic and epigenetic control of plant heat responses. Front Plant Sci. 2015;6:267.
  • Song C, Chung WS, Lim CO. Overexpression of heat shock factor gene HsfA3 increases galactinol levels and oxidative stress tolerance in Arabidopsis. Mol Cells. 2016;39:477.
  • Charng YY, Liu HC, Liu NY, et al. Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol. 2006;140:1297–1305.
  • Stief A, Altmann S, Hoffmann K, et al. Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell. 2014;26:1792–1807.
  • Sedaghatmehr M, Mueller-Roeber B, Balazadeh S. The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermorecovery in Arabidopsis. Nat Commun. 2016;7:12439.
  • Huot B, Yao J, Montgomery BL, et al. Growth-defense tradeoffs in plants: A balancing act to optimize fitness. Mol Plant. 2014;7:1267–1287.
  • Kumar SV, Wigge PA. H2A. Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell. 2010;140:136–147.
  • Crisp PA, Ganguly D, Eichten SR, et al. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv. 2016;2:e1501340.
  • Brzezinka K, Altmann S, Czesnick H, et al. Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling. eLife. 2016;5:e17061.
  • Lämke J, Bäurle I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 2017;18:124.
  • Ling Y, Serrano N, Gao G, et al. Thermopriming triggers splicing memory in Arabidopsis. J Exp Bot. 2018;69:2659–2675.
  • Serrano N, Ling Y, Bahieldin A, et al. Thermopriming reprograms metabolic homeostasis to confer heat tolerance. Sci Rep. 2019;9:181.
  • Nishizawa A, Yabuta Y, Yoshida E, et al. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 2006;48:535–547.
  • Charng YY, Liu HC, Liu NY, et al. A heat-inducible transcription factor, HSFA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 2007;143:251–262.
  • Duncan RF. Inhibition of Hsp90 function delays and impairs recovery from heat shock. Febs J. 2005;272:5244–5256.
  • Meiri D, Breiman A. Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90. 1 and affecting the accumulation of HSFA2‐regulated sHSPs. Plant J. 2009;59:387–399.
  • Riggs DL, Roberts PJ, Chirillo SC, et al. The Hsp90‐binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. EMBO J. 2003;22:1158–1167.
  • Standaert RF, Galat A, Verdine GL, et al. Molecular cloning and overexpression of the human FK506-binding protein FKBP. Nature. 1990;346:671–674.
  • Sedaghlatmehr M, Thirumalaikumar VP, Kamranfar I, et al. A regulatory role of autophagy for resetting the memory of heat stress in plants. Plant Cell Environ. 2019;42:1054–1064.
  • Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosomal formation. Annu Rev Cell Dev Biol. 2011;27:107–132.
  • Xie Y, Kang R, Sun X, et al. Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy. 2015;11:28–45.
  • Michaeli S, Honig A, Levanony H, et al. Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole. Plant Cell. 2014;26:4084–4101.
  • Farré JC, Subramani S. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat Rev Mol Cell Bio. 2016;17:537.
  • Hafrén A, Macia JL, Love AJ, et al. Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. Proc Natl Acad Sci USA. 2017;114:E2026–E2035.
  • Nolan TM, Brennan B, Yang M, et al. Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev Cell. 2017;41:33–46.
  • Gatica D, Lahiri V, Klionsky DJ. Cargo recognition and degradation by selective autophagy. Nat Cell Biol. 2018;20:233.
  • Marshall RS, Li F, Gemperline DC, et al. Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol Cell. 2015;58:1053–1066.
  • Broda M, Millar AH, Van Aken O. Mitophagy: a mechanism for plant growth and survival. Trends Plant Sci. 2018;23:434–450.
  • Yang F, Kimberlin AN, Elowsky CG, et al. A plant immune receptor degraded by selective autophagy. Mol Plant. 2019;12:113–123.
  • Marshall RS, Hua Z, Mali S, et al. ATG8-binding UIM proteins define a new class of autophagy adaptors and receptors. Cell. 2019;177:766–781.
  • Birgisdottir ÅB, Lamark T, Johansen T. The LIR motif–crucial for selective autophagy. J Cell Sci. 2013;126:3237–3247.
  • Zhou J, Wang J, Yu JQ, et al. Role and regulation of autophagy in heat stress responses of tomato plants. Front Plant Sci. 2014a;5:174.
  • Li WW, Chen M, Zhong L, et al. Overexpression of the autophagy-related gene SiATG8a from foxtail millet (Setaria italica L.) confers tolerance to both nitrogen starvation and drought stress in Arabidopsis. Biochem Biophys Res Commun. 2015;468:800–806.
  • Zhai Y, Wang H, Minmin L, et al. Both silencing-and over-expression of pepper CaATG8c gene compromise plant tolerance to heat and salt stress. Environ Exp Bot. 2017;141:10–18.
  • Üstün S, Hafrén A, Liu Q, et al. Bacteria exploit autophagy for proteasome degradation and enhanced virulence in plants. Plant Cell. 2018;30:668–685.
  • Zhou J, Wang J, Cheng Y, et al. NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet. 2013;9:e1003196.
  • Jung H, Lee HN, Marshall RS, et al. Arabidopsis cargo receptor NBR1 mediates selective autophagy of defective proteins. J Exp Bot. 2020;71(1):73–89. .
  • Thompson AR, Doelling JH, Suttangkakul A, et al. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 2005;138:2097–2110.
  • Wang R, Zhang Y, Kieffer M, et al. HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat Commun. 2016;7:10269.
  • Svenning S, Lamark T, Krause K, et al. Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy. 2011;7:993–1010.
  • Schramm F, Ganguli A, Kiehlmann E, et al. The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol Biol. 2006;60:759–772.
  • Lämke J, Brzezinka K, Altmann S, et al. A hit‐and‐run heat shock factor governs sustained histone methylation and transcriptional stress memory. Embo J. 2016;35:162–175.
  • Sung DY, Vierling E, Guy CL. Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 2001;126:789–800.
  • Perez DE, Hoyer JS, Johnson A, et al. BOBBER1 is a non-canonical Arabidopsis small heat shock protein required for both development and thermotolerance. Plant Physiol. 2009;151:241–252.
  • Jacob P, Hirt H, Bendahmane A. The heat‐shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J. 2017;15:405–414.
  • McLoughlin F, Kim M, Marshall RS, et al. Hsp101 interacts with the proteasome and promotes the clearance of ubiquitylated protein aggregates. Plant Physiol. 2019;180:1829–1847.
  • Dagdas YF, Belhaj K, Maqbool A, et al. An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. eLife. 2016;5:e10856.
  • Zhou J, Zhang Y, Qi J, et al. E3 ubiquitin ligase CHIP and NBR1-mediated selective autophagy protect additively against proteotoxicity in plant stress responses. PLoS Genet. 2014b;10:e1004116.
  • Tarnowski L, Collados Rodriguez M, Brzywczy J, et al. Overexpression of the selective autophagy cargo receptor NBR1 modifies plant response to sulfur deficit. Cells. 2020;9(3):669.
  • Driedonks N, Xu J, Peters JL, et al. Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat. Front Plant Sci. 2015;6:999.
  • Krishna P, Gloor G. The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones. 2001;6:238.
  • Pratt WB, Galigniana MD, Harrel JM, et al. Role of Hsp90 and the Hsp90-binding immunophilins in signalling protein movement. Cell Signal. 2004;16:857–872.
  • Yamada K, Nishimura M. Cytosolic heat shock protein 90 regulates heat shock transcription factor in Arabidopsis thaliana. Plant Signal Behav. 2008;3:660–662.
  • Ohama N, Sato H, Shinozaki K, et al. Transcriptional regulatory network of plant heat stress response. Trends Plant Sci. 2017;22:53–65.
  • Scharf KD, Berberich T, Ebersberger I, et al. The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta. 2012;1819:104–119.
  • Liu J, Feng L, Gu X, et al. An H3K27me3 demethylase-HSFA2 regulatory loop orchestrates transgenerational thermorecovery in Arabidopsis. Cell Res. 2019;29:379–390.
  • Meiri D, Tazat K, Cohen-Peer R, et al. Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. Plant Mol Biol. 2010;72:191.
  • Kraft C, Deplazes A, Sohrmann M, et al. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol. 2008;10:602.
  • Wyant GA, Abu-Remaileh M, Frenkel EM, et al. NUFIP1 is a ribosome receptor for starvation-induced ribophagy. Science. 2018;360:751–758.
  • Floyd BE, Morriss SC, MacIntosh GC, et al. Evidence for autophagy-dependent pathways of rRNA turnover in Arabidopsis. Autophagy. 2015;11(12):2199–2212. .
  • McLoughlin F, Augustine RC, Marshall RS, et al. Maize multi-omics reveal roles for autophagic recycling in proteome remodelling and lipid turnover. Nat Plants. 2018;4(12):1056–1070. .
  • Kragler F, Curin M, Trutnyeva K, et al. MPB2C, a microtubule-associated plant protein binds to and interferes with cell-to-cell transport of tobacco mosaic virus movement protein. Plant Physiol. 2003;132:1870–1883.
  • Grefen C, Donald N, Hashimoto K, et al. A ubiquitin‐10 promoter‐based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 2010;64:355–365.
  • Hafrén A, Üstün S, Hochmuth A, et al. Turnip mosaic virus counteracts selective autophagy of the viral silencing suppressor HCpro. Plant Physiol. 2018;176:649–662.
  • Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743.
  • Salem MA, Jüppner J, Bajdzienko K, et al. Protocol: a fast, comprehensive and reproducible one-step extraction method for the rapid preparation of polar and semi-polar metabolites, lipids, proteins, starch and cell wall polymers from a single sample. Plant Methods. 2016;12:45.
  • Rappsilber J, Mann M, Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc. 2007;2:1896.
  • Cox J, Matthias M. MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26:1367.
  • Cox J, Neuhauser N, Michalski A, et al. Andromeda: A peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10:1794–1805.
  • Martin K, Kopperud K, Chakrabarty R, et al. Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J. 2009;59:150–162.
  • Gallo-Oller G, Ordonez R, Dotor J. A new background subtraction method for Western blot densitometry band quantification through image analysis software. J Immunol Methods. 2018;457:1–5.
  • Balazadeh S, Riano-Pachón DM, Mueller-Roeber B. Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol. 2008;10:63–75.
  • Arvidsson S, Kwasniewski M, Riano-Pachón DM, et al. QuantPrime–a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinf. 2008;9:465.
  • Perez-Riverol Y, Csordas A, Bai J, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47:442–450.