AtCAP2 is Crucial for Lytic Vacuole Biogenesis During Germination by Positively Regulating Vacuolar Protein Trafficking

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2018 Jan 31

PMID 29378957

Citations 7

Authors

Yun Kwon

Jinbo Shen

Myoung Hui Lee

Kyoung Rok Geem

Liwen Jiang

Inhwan Hwang

Affiliations

Soon will be listed here.

Abstract

Protein trafficking is a fundamental mechanism of subcellular organization and contributes to organellar biogenesis. AtCAP2 is an homolog of the calcium-dependent protein kinase 1 adaptor protein 2 (McCAP2), a member of the syntaxin superfamily. Here, we show that AtCAP2 plays an important role in the conversion to the lytic vacuole (LV) during early plant development. The loss-of-function mutant displayed delays in protein storage vacuole (PSV) protein degradation, PSV fusion, LV acidification, and biosynthesis of several vacuolar proteins during germination. At the mature stage, plants accumulated vacuolar proteins in the prevacuolar compartment (PVC) instead of the LV. In wild-type plants, AtCAP2 localizes to the PVC as a peripheral membrane protein and in the PVC compartment recruits glyceraldehyde-3-phosphate dehydrogenase C2 (GAPC2) to the PVC. We propose that AtCAP2 contributes to LV biogenesis during early plant development by supporting the trafficking of specific proteins involved in the PSV-to-LV transition and LV acidification during early stages of plant development.

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References

Tisdale E, Kelly C, Artalejo C . Glyceraldehyde-3-phosphate dehydrogenase interacts with Rab2 and plays an essential role in endoplasmic reticulum to Golgi transport exclusive of its glycolytic activity. J Biol Chem. 2004; 279(52):54046-52. DOI: 10.1074/jbc.M409472200. View

Jiang Y, Sverdlov M, Toth P, Huang L, Du G, Liu Y . Phosphatidic Acid Produced by RalA-activated PLD2 Stimulates Caveolae-mediated Endocytosis and Trafficking in Endothelial Cells. J Biol Chem. 2016; 291(39):20729-38. PMC: 5034062. DOI: 10.1074/jbc.M116.752485. View

Gao C, Yu C, Qu S, San M, Li K, Lo S . The Golgi-localized Arabidopsis endomembrane protein12 contains both endoplasmic reticulum export and Golgi retention signals at its C terminus. Plant Cell. 2012; 24(5):2086-104. PMC: 3442589. DOI: 10.1105/tpc.112.096057. View

Krebs M, Beyhl D, Gorlich E, Al-Rasheid K, Marten I, Stierhof Y . Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci U S A. 2010; 107(7):3251-6. PMC: 2840351. DOI: 10.1073/pnas.0913035107. View

Konig S, Ischebeck T, Lerche J, Stenzel I, Heilmann I . Salt-stress-induced association of phosphatidylinositol 4,5-bisphosphate with clathrin-coated vesicles in plants. Biochem J. 2008; 415(3):387-99. DOI: 10.1042/BJ20081306. View

Zheng H, Staehelin L . Protein storage vacuoles are transformed into lytic vacuoles in root meristematic cells of germinating seedlings by multiple, cell type-specific mechanisms. Plant Physiol. 2011; 155(4):2023-35. PMC: 3091105. DOI: 10.1104/pp.110.170159. View

Kaneda M, Takeuchi K, Inoue K, Umeda M . Localization of the phosphatidylserine-binding site of glyceraldehyde-3-phosphate dehydrogenase responsible for membrane fusion. J Biochem. 1998; 122(6):1233-40. DOI: 10.1093/oxfordjournals.jbchem.a021886. View

Wu X, Ebine K, Ueda T, Qiu Q . AtNHX5 and AtNHX6 Are Required for the Subcellular Localization of the SNARE Complex That Mediates the Trafficking of Seed Storage Proteins in Arabidopsis. PLoS One. 2016; 11(3):e0151658. PMC: 4795774. DOI: 10.1371/journal.pone.0151658. View

Jaillais Y, Fobis-Loisy I, Miege C, Rollin C, Gaude T . AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature. 2006; 443(7107):106-9. DOI: 10.1038/nature05046. View

10.

Kim H, Park M, Kim S, Hwang I . Actin filaments play a critical role in vacuolar trafficking at the Golgi complex in plant cells. Plant Cell. 2005; 17(3):888-902. PMC: 1069706. DOI: 10.1105/tpc.104.028829. View

11.

Isono E, Katsiarimpa A, Muller I, Anzenberger F, Stierhof Y, Geldner N . The deubiquitinating enzyme AMSH3 is required for intracellular trafficking and vacuole biogenesis in Arabidopsis thaliana. Plant Cell. 2010; 22(6):1826-37. PMC: 2910964. DOI: 10.1105/tpc.110.075952. View

12.

McLoughlin F, Arisz S, Dekker H, Kramer G, de Koster C, Haring M . Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem J. 2013; 450(3):573-81. DOI: 10.1042/BJ20121639. View

13.

He F, Huang F, Wilson K, Tan-Wilson A . Protein storage vacuole acidification as a control of storage protein mobilization in soybeans. J Exp Bot. 2007; 58(5):1059-70. DOI: 10.1093/jxb/erl267. View

14.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

15.

Frigerio L, Hinz G, Robinson D . Multiple vacuoles in plant cells: rule or exception?. Traffic. 2008; 9(10):1564-70. DOI: 10.1111/j.1600-0854.2008.00776.x. View

16.

ROBBINS A, Ward R, Oliver C . A mutation in glyceraldehyde 3-phosphate dehydrogenase alters endocytosis in CHO cells. J Cell Biol. 1995; 130(5):1093-104. PMC: 2120546. DOI: 10.1083/jcb.130.5.1093. View

17.

Sanderfoot A, Kovaleva V, Bassham D, Raikhel N . Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol Biol Cell. 2001; 12(12):3733-43. PMC: 60751. DOI: 10.1091/mbc.12.12.3733. View

18.

Henry E, Fung N, Liu J, Drakakaki G, Coaker G . Beyond glycolysis: GAPDHs are multi-functional enzymes involved in regulation of ROS, autophagy, and plant immune responses. PLoS Genet. 2015; 11(4):e1005199. PMC: 4412566. DOI: 10.1371/journal.pgen.1005199. View

19.

Rojo E, Gillmor C, Kovaleva V, Somerville C, Raikhel N . VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev Cell. 2001; 1(2):303-10. DOI: 10.1016/s1534-5807(01)00024-7. View

20.

Shen J, Suen P, Wang X, Lin Y, Lo S, Rojo E . An in vivo expression system for the identification of cargo proteins of vacuolar sorting receptors in Arabidopsis culture cells. Plant J. 2013; 75(6):1003-17. DOI: 10.1111/tpj.12257. View