Homologous Proteins of the Manganese Transporter PAM71 Are Localized in the Golgi Apparatus and Endoplasmic Reticulum

Overview

Journal Plants (Basel)

Date 2020 Feb 20

PMID 32069796

Citations 8

Authors

Natalie Hoecker

Anna Honke

Katharina Frey

Dario Leister

Anja Schneider

Affiliations

Soon will be listed here.

Abstract

Chloroplast manganese transporter 1 (CMT1) and photosynthesis-affected mutant 71 (PAM71) are two membrane proteins that function sequentially to mediate the passage of manganese across the chloroplast envelope and the thylakoid membrane. CMT1 and PAM71 belong to a small five-member protein family in . The other three, photosynthesis-affected mutant 71 like 3 (PML3), PML4 and PML5 are not predicted to reside in chloroplast membranes. In this study, the subcellular localization of PML3:GFP, PML4:GFP and PML5:GFP was determined using transient and stable expression assays. PML3:GFP localizes to the Golgi apparatus, whereas PML4:GFP and PML5:GFP are found in the endoplasmic reticulum. We also examined patterns of , and promoter activity. Although the precise expression pattern of each promoter was unique, all three genes were expressed in the leaf vasculature and in roots. Greenhouse grown single mutants , , and the double mutant did not exhibit growth defects, however an inspection of the root growth revealed a difference between and the other genotypes, including wild-type, in 500 µM manganese growth conditions. Strikingly, overexpression of PML3 resulted in a stunted growth phenotype. Putative functions of PML3, PML4 and PML5 are discussed in light of what is known about PAM71 and CMT1.

Citing Articles

New insights into the pathogenicity of TMEM165 variants using structural modeling based on AlphaFold 2 predictions.

Legrand D, Herbaut M, Durin Z, Brysbaert G, Bardor M, Lensink M Comput Struct Biotechnol J. 2023; 21:3424-3436.

PMID: 37416081 PMC: 10319644. DOI: 10.1016/j.csbj.2023.06.015.

Dissecting the relative contribution of ECA3 and group 8/9 cation diffusion facilitators to manganese homeostasis in .

Farthing E, Henbest K, Garcia-Becerra T, Peaston K, Williams L Plant Direct. 2023; 7(5):e495.

PMID: 37228331 PMC: 10202827. DOI: 10.1002/pld3.495.

Insights into the regulation of cellular Mn homeostasis via TMEM165.

Vicogne D, Beauval N, Durin Z, Allorge D, Kondratska K, Haustrate A Biochim Biophys Acta Mol Basis Dis. 2023; 1869(6):166717.

PMID: 37062452 PMC: 10639120. DOI: 10.1016/j.bbadis.2023.166717.

Manganese management in plants: Golgi transporter determines manganese allocation and cell wall composition.

Wege S Plant Physiol. 2022; 190(4):2077-2079.

PMID: 36124988 PMC: 9706420. DOI: 10.1093/plphys/kiac429.

Towards understanding the extensive diversity of protein N-glycan structures in eukaryotes.

Toustou C, Walet-Balieu M, Kiefer-Meyer M, Houdou M, Lerouge P, Foulquier F Biol Rev Camb Philos Soc. 2021; 97(2):732-748.

PMID: 34873817 PMC: 9300197. DOI: 10.1111/brv.12820.

References

Zhang B, Zhang C, Liu C, Jing Y, Wang Y, Jin L . Inner Envelope CHLOROPLAST MANGANESE TRANSPORTER 1 Supports Manganese Homeostasis and Phototrophic Growth in Arabidopsis. Mol Plant. 2018; 11(7):943-954. DOI: 10.1016/j.molp.2018.04.007. View

Demaegd D, Foulquier F, Colinet A, Gremillon L, Legrand D, Mariot P . Newly characterized Golgi-localized family of proteins is involved in calcium and pH homeostasis in yeast and human cells. Proc Natl Acad Sci U S A. 2013; 110(17):6859-64. PMC: 3637739. DOI: 10.1073/pnas.1219871110. View

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

Matheson L, Suri S, Hanton S, Chatre L, Brandizzi F . Correct targeting of plant ARF GTPases relies on distinct protein domains. Traffic. 2007; 9(1):103-20. DOI: 10.1111/j.1600-0854.2007.00671.x. View

Amos R, Mohnen D . Critical Review of Plant Cell Wall Matrix Polysaccharide Glycosyltransferase Activities Verified by Heterologous Protein Expression. Front Plant Sci. 2019; 10:915. PMC: 6646851. DOI: 10.3389/fpls.2019.00915. View

Foulquier F, Amyere M, Jaeken J, Zeevaert R, Schollen E, Race V . TMEM165 deficiency causes a congenital disorder of glycosylation. Am J Hum Genet. 2012; 91(1):15-26. PMC: 3397274. DOI: 10.1016/j.ajhg.2012.05.002. View

Schmittgen T, Livak K . Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3(6):1101-8. DOI: 10.1038/nprot.2008.73. View

Hoecker N, Leister D, Schneider A . Plants contain small families of UPF0016 proteins including the PHOTOSYNTHESIS AFFECTED MUTANT71 transporter. Plant Signal Behav. 2017; 12(2):e1278101. PMC: 5351731. DOI: 10.1080/15592324.2016.1278101. View

Mills R, Doherty M, Lopez-Marques R, Weimar T, Dupree P, Palmgren M . ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol. 2007; 146(1):116-28. PMC: 2230566. DOI: 10.1104/pp.107.110817. View

10.

Peiter E, Montanini B, Gobert A, Pedas P, Husted S, Maathuis F . A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proc Natl Acad Sci U S A. 2007; 104(20):8532-7. PMC: 1895984. DOI: 10.1073/pnas.0609507104. View

11.

Karimi M, Inze D, Depicker A . GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002; 7(5):193-5. DOI: 10.1016/s1360-1385(02)02251-3. View

12.

Demaegd D, Colinet A, Deschamps A, Morsomme P . Molecular evolution of a novel family of putative calcium transporters. PLoS One. 2014; 9(6):e100851. PMC: 4067407. DOI: 10.1371/journal.pone.0100851. View

13.

Wei X, Su X, Cao P, Liu X, Chang W, Li M . Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution. Nature. 2016; 534(7605):69-74. DOI: 10.1038/nature18020. View

14.

Nunan K, Scheller H . Solubilization of an arabinan arabinosyltransferase activity from mung bean hypocotyls. Plant Physiol. 2003; 132(1):331-42. PMC: 166978. DOI: 10.1104/pp.102.019406. View

15.

Driouich A, Follet-Gueye M, Bernard S, Kousar S, Chevalier L, Vicre-Gibouin M . Golgi-mediated synthesis and secretion of matrix polysaccharides of the primary cell wall of higher plants. Front Plant Sci. 2012; 3:79. PMC: 3355623. DOI: 10.3389/fpls.2012.00079. View

16.

Eroglu S, Meier B, von Wiren N, Peiter E . The Vacuolar Manganese Transporter MTP8 Determines Tolerance to Iron Deficiency-Induced Chlorosis in Arabidopsis. Plant Physiol. 2015; 170(2):1030-45. PMC: 4734556. DOI: 10.1104/pp.15.01194. View

17.

Nelson B, Cai X, Nebenfuhr A . A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 2007; 51(6):1126-36. DOI: 10.1111/j.1365-313X.2007.03212.x. View

18.

Potelle S, Morelle W, Dulary E, Duvet S, Vicogne D, Spriet C . Glycosylation abnormalities in Gdt1p/TMEM165 deficient cells result from a defect in Golgi manganese homeostasis. Hum Mol Genet. 2016; 25(8):1489-500. DOI: 10.1093/hmg/ddw026. View

19.

Umena Y, Kawakami K, Shen J, Kamiya N . Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature. 2011; 473(7345):55-60. DOI: 10.1038/nature09913. View

20.

Schweiger R, Muller N, Schmitt M, Soll J, Schwenkert S . AtTPR7 is a chaperone-docking protein of the Sec translocon in Arabidopsis. J Cell Sci. 2012; 125(Pt 21):5196-207. DOI: 10.1242/jcs.111054. View