Reticulon Proteins Modulate Autophagy of the Endoplasmic Reticulum in Maize Endosperm

Overview

Journal Elife

Specialty Biology

Date 2020 Feb 4

PMID 32011236

Citations 45

Authors

Xiaoguo Zhang

Xinxin Ding

Richard Scott Marshall

Julio Paez-Valencia

Patrick Lacey

Richard David Vierstra

Marisa S Otegui

Affiliations

Soon will be listed here.

Abstract

Reticulon (Rtn) proteins shape tubular domains of the endoplasmic reticulum (ER), and in some cases are autophagy receptors for selective ER turnover. We have found that maize Rtn1 and Rtn2 control ER homeostasis and autophagic flux in endosperm aleurone cells, where the ER accumulates lipid droplets and synthesizes storage protein accretions metabolized during germination. Maize Rtn1 and Rtn2 are expressed in the endosperm, localize to the ER, and re-model ER architecture in a dose-dependent manner. Rtn1 and Rtn2 interact with Atg8a using four Atg8-interacting motifs (AIMs) located at the C-terminus, cytoplasmic loop, and within the transmembrane segments. Binding between Rtn2 and Atg8 is elevated upon ER stress. Maize mutants display increased autophagy and up-regulation of an ER stress-responsive chaperone. We propose that maize Rtn1 and Rtn2 act as receptors for autophagy-mediated ER turnover, and thus are critical for ER homeostasis and suppression of ER stress.

Citing Articles

The landscape in telomere related gene prognostic signature for survival and medication treatment effectiveness prediction in hepatocellular carcinoma.

Zhou K, Liu X, Wang M, Duan J, Zhao X, Yin H Discov Oncol. 2024; 15(1):765.

PMID: 39692822 PMC: 11655892. DOI: 10.1007/s12672-024-01659-w.

Visualizing ER-phagy and ER architecture in vivo.

Sang Y, Li B, Su T, Zhan H, Xiong Y, Huang Z J Cell Biol. 2024; 223(12).

PMID: 39556340 PMC: 11575016. DOI: 10.1083/jcb.202408061.

The MON1-CCZ1 complex plays dual roles in autophagic degradation and vacuolar protein transport in rice.

Zhang B, Wang Y, Zhu Y, Pan T, Yan H, Wang X J Integr Plant Biol. 2024; 67(1):35-54.

PMID: 39474758 PMC: 11734111. DOI: 10.1111/jipb.13792.

Genome-wide transcriptome and gene family analysis reveal candidate genes associated with potassium uptake of maize colonized by arbuscular mycorrhizal fungi.

Xu Y, Yan Y, Zhou T, Chun J, Tu Y, Yang X BMC Plant Biol. 2024; 24(1):838.

PMID: 39242995 PMC: 11378567. DOI: 10.1186/s12870-024-05398-6.

Protein disulfide isomerase-9 interacts with the lumenal region of the transmembrane endoplasmic reticulum stress sensor kinase, IRE1, to modulate the unfolded protein response in .

Carrillo R, Iwai K, Albertson A, Dang G, Christopher D Front Plant Sci. 2024; 15:1389658.

PMID: 38817940 PMC: 11137178. DOI: 10.3389/fpls.2024.1389658.

References

Schafer J, Schessner J, Bircham P, Tsuji T, Funaya C, Pajonk O . ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast. EMBO J. 2019; 39(2):e102586. PMC: 6960443. DOI: 10.15252/embj.2019102586. View

Pagny S, Gillikin J, Leborgne-Castel N, Lerouge P, Boston R, Faye L . Protein recycling from the Golgi apparatus to the endoplasmic reticulum in plants and its minor contribution to calreticulin retention. Plant Cell. 2000; 12(5):739-56. PMC: 139924. DOI: 10.1105/tpc.12.5.739. View

Chino H, Hatta T, Natsume T, Mizushima N . Intrinsically Disordered Protein TEX264 Mediates ER-phagy. Mol Cell. 2019; 74(5):909-921.e6. DOI: 10.1016/j.molcel.2019.03.033. View

Fumagalli F, Noack J, Bergmann T, Cebollero E, Pisoni G, Fasana E . Translocon component Sec62 acts in endoplasmic reticulum turnover during stress recovery. Nat Cell Biol. 2016; 18(11):1173-1184. DOI: 10.1038/ncb3423. View

Voeltz G, Prinz W, Shibata Y, Rist J, Rapoport T . A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell. 2006; 124(3):573-86. DOI: 10.1016/j.cell.2005.11.047. View

Hanada T, Noda N, Satomi Y, Ichimura Y, Fujioka Y, Takao T . The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem. 2007; 282(52):37298-302. DOI: 10.1074/jbc.C700195200. View

Kriechbaumer V, Maneta-Peyret L, Fouillen L, Botchway S, Upson J, Hughes L . The odd one out: Arabidopsis reticulon 20 does not bend ER membranes but has a role in lipid regulation. Sci Rep. 2018; 8(1):2310. PMC: 5797236. DOI: 10.1038/s41598-018-20840-0. View

Stefano G, Brandizzi F . Advances in Plant ER Architecture and Dynamics. Plant Physiol. 2017; 176(1):178-186. PMC: 5761816. DOI: 10.1104/pp.17.01261. View

Doelling J, Walker J, Friedman E, Thompson A, Vierstra R . The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem. 2002; 277(36):33105-14. DOI: 10.1074/jbc.M204630200. View

10.

Muller O, Sattler T, Flotenmeyer M, Schwarz H, Plattner H, Mayer A . Autophagic tubes: vacuolar invaginations involved in lateral membrane sorting and inverse vesicle budding. J Cell Biol. 2000; 151(3):519-28. PMC: 2185586. DOI: 10.1083/jcb.151.3.519. View

11.

Wilkinson S . Emerging Principles of Selective ER Autophagy. J Mol Biol. 2019; 432(1):185-205. PMC: 6971691. DOI: 10.1016/j.jmb.2019.05.012. View

12.

Liang J, Lingeman E, Ahmed S, Corn J . Atlastins remodel the endoplasmic reticulum for selective autophagy. J Cell Biol. 2018; 217(10):3354-3367. PMC: 6168278. DOI: 10.1083/jcb.201804185. View

13.

Breeze E, Dzimitrowicz N, Kriechbaumer V, Brooks R, Botchway S, Brady J . A C-terminal amphipathic helix is necessary for the in vivo tubule-shaping function of a plant reticulon. Proc Natl Acad Sci U S A. 2016; 113(39):10902-7. PMC: 5047209. DOI: 10.1073/pnas.1605434113. View

14.

Zhan J, Thakare D, Ma C, Lloyd A, Nixon N, Arakaki A . RNA sequencing of laser-capture microdissected compartments of the maize kernel identifies regulatory modules associated with endosperm cell differentiation. Plant Cell. 2015; 27(3):513-31. PMC: 4558669. DOI: 10.1105/tpc.114.135657. View

15.

di Scala F, Dupuis L, Gaiddon C, de Tapia M, Jokic N, Gonzalez De Aguilar J . Tissue specificity and regulation of the N-terminal diversity of reticulon 3. Biochem J. 2004; 385(Pt 1):125-34. PMC: 1134680. DOI: 10.1042/BJ20040458. View

16.

Howell S . Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol. 2013; 64:477-99. DOI: 10.1146/annurev-arplant-050312-120053. View

17.

Romanov J, Walczak M, Ibiricu I, Schuchner S, Ogris E, Kraft C . Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J. 2012; 31(22):4304-17. PMC: 3501226. DOI: 10.1038/emboj.2012.278. View

18.

Srivastava R, Li Z, Russo G, Tang J, Bi R, Muppirala U . Response to Persistent ER Stress in Plants: A Multiphasic Process That Transitions Cells from Prosurvival Activities to Cell Death. Plant Cell. 2018; 30(6):1220-1242. PMC: 6048783. DOI: 10.1105/tpc.18.00153. View

19.

Wang G, Qi W, Wu Q, Yao D, Zhang J, Zhu J . Identification and Characterization of Maize floury4 as a Novel Semidominant Opaque Mutant That Disrupts Protein Body Assembly. Plant Physiol. 2014; 165(2):582-594. PMC: 4044854. DOI: 10.1104/pp.114.238030. View

20.

Schuck S, Gallagher C, Walter P . ER-phagy mediates selective degradation of endoplasmic reticulum independently of the core autophagy machinery. J Cell Sci. 2014; 127(Pt 18):4078-88. PMC: 4163648. DOI: 10.1242/jcs.154716. View