{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T11:57:10Z","timestamp":1791460630053,"version":"4.3.4"},"reference-count":45,"publisher":"Oxford University Press (OUP)","issue":"7","license":[{"start":{"date-parts":[[2021,1,22]],"date-time":"2021-01-22T00:00:00Z","timestamp":1611273600000},"content-version":"vor","delay-in-days":1677,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science (JSPS)","doi-asserted-by":"publisher","award":["25440158"],"award-info":[{"award-number":["25440158"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science (JSPS)","doi-asserted-by":"publisher","award":["26117720"],"award-info":[{"award-number":["26117720"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science (JSPS)","doi-asserted-by":"publisher","award":["15K07130"],"award-info":[{"award-number":["15K07130"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2016,8,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>It is believed that the plastids in green plants lost peptidoglycan (i.e., a bacterial cell wall-containing d-amino acids) during their evolution from an endosymbiotic cyanobacterium. Although wall-like structures could not be detected in the plastids of green plants, the moss Physcomitrella patens has the genes required to generate peptidoglycan (Mur genes), and knocking out these genes causes defects in chloroplast division. Here, we generated P. patens knockout lines (\u2206Pp-ddl) for a homolog of the bacterial peptidoglycan-synthetic gene encoding d-Ala:d-Ala ligase. \u2206Pp-ddl had a macrochloroplast phenotype, similar to other Mur knockout lines. The addition of d-Ala-d-Ala (DA-DA) to the medium suppressed the appearance of giant chloroplasts in \u2206Pp-ddl, but the addition of l-Ala-l-Ala (LA-LA), DA-LA, LA-DA, or d-Ala did not. Recently, a metabolic method for labeling bacterial peptidoglycan was established using ethynyl-DA-DA (EDA-DA) and click chemistry to attach an azide-modified fluorophore to the ethynyl group. The \u2206Pp-ddl line complemented with EDA-DA showed that moss chloroplasts are completely surrounded by peptidoglycan. Our findings strongly suggest that the moss plastids have a peptidoglycan wall containing d-amino acids. By contrast, no plastid phenotypes were observed in the T-DNA tagged ddl mutant lines of Arabidopsis thaliana.<\/jats:p>","DOI":"10.1105\/tpc.16.00104","type":"journal-article","created":{"date-parts":[[2016,6,21]],"date-time":"2016-06-21T03:34:22Z","timestamp":1466480062000},"page":"1521-1532","source":"Crossref","is-referenced-by-count":87,"title":["Moss Chloroplasts Are Surrounded by a Peptidoglycan Wall Containing D-Amino Acids"],"prefix":"10.1093","volume":"28","author":[{"given":"Takayuki","family":"Hirano","sequence":"first","affiliation":[{"name":"Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Koji","family":"Tanidokoro","sequence":"additional","affiliation":[{"name":"Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasuhiro","family":"Shimizu","sequence":"additional","affiliation":[{"name":"Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yutaka","family":"Kawarabayasi","sequence":"additional","affiliation":[{"name":"Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan"},{"name":"National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki 305-8566, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Toshihisa","family":"Ohshima","sequence":"additional","affiliation":[{"name":"Faculty of Engineering, Osaka Institute of Technology, Asahi-ku, Osaka 535-8585, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Momo","family":"Sato","sequence":"additional","affiliation":[{"name":"Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shinji","family":"Tadano","sequence":"additional","affiliation":[{"name":"Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hayato","family":"Ishikawa","sequence":"additional","affiliation":[{"name":"Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Susumu","family":"Takio","sequence":"additional","affiliation":[{"name":"Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan"},{"name":"Center for Marine Environment Studies, Kumamoto University, Kumamoto 860-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katsuaki","family":"Takechi","sequence":"additional","affiliation":[{"name":"Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hiroyoshi","family":"Takano","sequence":"additional","affiliation":[{"name":"Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan"},{"name":"Institute of Pulsed Power Science, Kumamoto University, Kumamoto 860-8555, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2016,6,20]]},"reference":[{"key":"2021040918541330300_b1","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1126\/science.1086391","article-title":"Genome-wide insertional mutagenesis of Arabidopsis thaliana.","volume":"301","author":"Alonso","year":"2003","journal-title":"Science"},{"key":"2021040918541330300_b2","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1038\/35048692","article-title":"Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.","volume":"408","author":"Arabidopsis Genome Initiative","year":"2000","journal-title":"Nature"},{"key":"2021040918541330300_b3","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/BF00265581","article-title":"The isolation and preliminary characterisation of auxotrophic and analogue resistant mutants of the moss, Physcomitrella patens.","volume":"154","author":"Ashton","year":"1977","journal-title":"Mol. Gen. Genet."},{"key":"2021040918541330300_b4","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/0003-2697(84)90106-4","article-title":"Determination of d- and l-aspartate in amino acid mixtures by high-performance liquid chromatography after derivatization with a chiral adduct of o-phthaldialdehyde","volume":"137","author":"Aswad","year":"1984","journal-title":"Anal. Biochem."},{"key":"2021040918541330300_b5","doi-asserted-by":"crossref","first-page":"960","DOI":"10.1126\/science.1203810","article-title":"The Selaginella genome identifies genetic changes associated with the evolution of vascular plants","volume":"332","author":"Banks","year":"2011","journal-title":"Science"},{"key":"2021040918541330300_b6","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1128\/AAC.00558-10","article-title":"Structure of the Mycobacterium tuberculosis \u00a0d-alanine:d-alanine ligase, a target of the antituberculosis drug d-cycloserine","volume":"55","author":"Bruning","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"2021040918541330300_b7","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/S0960-9822(02)00483-9","article-title":"Engineered GFP as a vital reporter in plants","volume":"6","author":"Chiu","year":"1996","journal-title":"Curr. Biol."},{"key":"2021040918541330300_b8","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1006\/jmbi.2000.3903","article-title":"Predicting subcellular localization of proteins based on their N-terminal amino acid sequence","volume":"300","author":"Emanuelsson","year":"2000","journal-title":"J. Mol. Biol."},{"key":"2021040918541330300_b9","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1038\/nbt946","article-title":"A conditional marker gene allowing both positive and negative selection in plants","volume":"22","author":"Erikson","year":"2004","journal-title":"Nat. Biotechnol."},{"key":"2021040918541330300_b10","doi-asserted-by":"crossref","first-page":"1464","DOI":"10.1016\/S0031-9422(00)98674-6","article-title":"The occurrence of d-alanine and d-alanyl-d-alanine in Phalaris tuberosa.","volume":"14","author":"Frahn","year":"1975","journal-title":"Phytochemistry"},{"key":"2021040918541330300_b11","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1111\/j.1365-313X.2007.03379.x","article-title":"An Arabidopsis homolog of the bacterial peptidoglycan synthesis enzyme MurE has an essential role in chloroplast development","volume":"53","author":"Garcia","year":"2008","journal-title":"Plant J."},{"key":"2021040918541330300_b12","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1016\/j.biocel.2012.01.005","article-title":"d-Serine: a key to synaptic plasticity?","volume":"44","author":"Henneberger","year":"2012","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"2021040918541330300_b13","doi-asserted-by":"crossref","first-page":"2047","DOI":"10.1093\/pcp\/pcp158","article-title":"The peptidoglycan biosynthesis genes MurA and MraY are related to chloroplast division in the moss Physcomitrella patens.","volume":"50","author":"Homi","year":"2009","journal-title":"Plant Cell Physiol."},{"key":"2021040918541330300_b14","doi-asserted-by":"crossref","first-page":"3978","DOI":"10.1038\/ncomms4978","article-title":"Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation","volume":"5","author":"Hori","year":"2014","journal-title":"Nat. Commun."},{"key":"2021040918541330300_b15","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/S0176-1617(97)80193-9","article-title":"\u03b2-Lactam antibiotics inhibit chloroplast division in a moss (Physcomitrella patens) but not in tomato (Lycopersicon esculentum)","volume":"150","author":"Kasten","year":"1997","journal-title":"Plant Physiol."},{"key":"2021040918541330300_b16","doi-asserted-by":"crossref","first-page":"776","DOI":"10.1093\/pcp\/pcg096","article-title":"Effects of antibiotics that inhibit the bacterial peptidoglycan synthesis pathway on moss chloroplast division","volume":"44","author":"Katayama","year":"2003","journal-title":"Plant Cell Physiol."},{"key":"2021040918541330300_b17","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1098\/rstb.2009.0103","article-title":"The endosymbiotic origin, diversification and fate of plastids","volume":"365","author":"Keeling","year":"2010","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"2021040918541330300_b18","doi-asserted-by":"crossref","first-page":"2305","DOI":"10.1002\/jssc.200900101","article-title":"Separation and sensitive detection of d-amino acids in biological matrices","volume":"32","author":"Kirschner","year":"2009","journal-title":"J. Sep. Sci."},{"key":"2021040918541330300_b19","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1007\/s00203-005-0046-8","article-title":"Wide variation in the cyanobacterial complement of presumptive penicillin-binding proteins","volume":"184","author":"Legan\u00e9s","year":"2005","journal-title":"Arch. Microbiol."},{"key":"2021040918541330300_b20","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1038\/nature12892","article-title":"A new metabolic cell-wall labelling method reveals peptidoglycan in Chlamydia trachomatis.","volume":"506","author":"Liechti","year":"2014","journal-title":"Nature"},{"key":"2021040918541330300_b21","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1007\/s002030100280","article-title":"Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell","volume":"175","author":"Lindsay","year":"2001","journal-title":"Arch. Microbiol."},{"key":"2021040918541330300_b22","doi-asserted-by":"crossref","first-page":"6753","DOI":"10.1073\/pnas.0510693103","article-title":"Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss","volume":"103","author":"Machida","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021040918541330300_b23","doi-asserted-by":"crossref","first-page":"e40734","DOI":"10.1371\/journal.pone.0040734","article-title":"Treatment with antibiotics that interfere with peptidoglycan biosynthesis inhibits chloroplast division in the desmid Closterium.","volume":"7","author":"Matsumoto","year":"2012","journal-title":"PLoS One"},{"key":"2021040918541330300_b24","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.tim.2005.12.004","article-title":"Building the invisible wall: updating the chlamydial peptidoglycan anomaly","volume":"14","author":"McCoy","year":"2006","journal-title":"Trends Microbiol."},{"key":"2021040918541330300_b25","doi-asserted-by":"crossref","first-page":"1751","DOI":"10.1093\/genetics\/159.4.1751","article-title":"Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana.","volume":"159","author":"McElver","year":"2001","journal-title":"Genetics"},{"key":"2021040918541330300_b26","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1126\/science.1143609","article-title":"The Chlamydomonas genome reveals the evolution of key animal and plant functions","volume":"318","author":"Merchant","year":"2007","journal-title":"Science"},{"key":"2021040918541330300_b27","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1126\/science.1201101","article-title":"Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil d-serine","volume":"332","author":"Michard","year":"2011","journal-title":"Science"},{"key":"2021040918541330300_b28","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1093\/dnares\/7.1.9","article-title":"Tagged mutagenesis and gene-trap in the moss, Physcomitrella patens by shuttle mutagenesis","volume":"7","author":"Nishiyama","year":"2000","journal-title":"DNA Res."},{"key":"2021040918541330300_b29","doi-asserted-by":"crossref","first-page":"2439","DOI":"10.1080\/00021369.1973.10861017","article-title":"Isolation and characterization of d-alanyl- d-alanine from tobacco leaves","volume":"37","author":"Noma","year":"1973","journal-title":"Agric. Biol. Chem."},{"key":"2021040918541330300_b30","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1105\/tpc.105.036392","article-title":"pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression","volume":"18","author":"Pfalz","year":"2006","journal-title":"Plant Cell"},{"key":"2021040918541330300_b31","doi-asserted-by":"crossref","first-page":"2856","DOI":"10.1038\/ncomms3856","article-title":"Discovery of chlamydial peptidoglycan reveals bacteria with murein sacculi but without FtsZ","volume":"4","author":"Pilhofer","year":"2013","journal-title":"Nat. Commun."},{"key":"2021040918541330300_b32","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1126\/science.1188800","article-title":"Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri.","volume":"329","author":"Prochnik","year":"2010","journal-title":"Science"},{"key":"2021040918541330300_b33","doi-asserted-by":"crossref","first-page":"1704","DOI":"10.1093\/pcp\/pch194","article-title":"A mechanosensitive anion channel in Arabidopsis thaliana mesophyll cells","volume":"45","author":"Qi","year":"2004","journal-title":"Plant Cell Physiol."},{"key":"2021040918541330300_b34","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1126\/science.1150646","article-title":"The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants","volume":"319","author":"Rensing","year":"2008","journal-title":"Science"},{"key":"2021040918541330300_b35","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1016\/0024-3205(76)90244-7","article-title":"d-amino acids in higher plants","volume":"19","author":"Robinson","year":"1976","journal-title":"Life Sci."},{"key":"2021040918541330300_b36","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1111\/j.1525-142X.2008.00271.x","article-title":"Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development","volume":"10","author":"Sakakibara","year":"2008","journal-title":"Evol. Dev."},{"key":"2021040918541330300_b37","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/S1360-1385(01)02179-3","article-title":"Protein import into cyanelles","volume":"7","author":"Steiner","year":"2002","journal-title":"Trends Plant Sci."},{"key":"2021040918541330300_b38","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1111\/j.1365-313X.2004.02195.x","article-title":"Affinity purification of the tobacco plastid RNA polymerase and in vitro reconstitution of the holoenzyme","volume":"40","author":"Suzuki","year":"2004","journal-title":"Plant J."},{"key":"2021040918541330300_b39","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.bbagen.2009.07.020","article-title":"Plastid peptidoglycan","volume":"1800","author":"Takano","year":"2010","journal-title":"Biochim. Biophys. Acta"},{"key":"2021040918541330300_b40","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1261\/rna.7114505","article-title":"Bicistronic and fused monocistronic transcripts are derived from adjacent loci in the Arabidopsis genome","volume":"11","author":"Thimmapuram","year":"2005","journal-title":"RNA"},{"key":"2021040918541330300_b41","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1038\/nrmicro2677","article-title":"From the regulation of peptidoglycan synthesis to bacterial growth and morphology","volume":"10","author":"Typas","year":"2011","journal-title":"Nat. Rev. Microbiol."},{"key":"2021040918541330300_b42","doi-asserted-by":"crossref","first-page":"6878","DOI":"10.1038\/ncomms7878","article-title":"Anammox Planctomycetes have a peptidoglycan cell wall","volume":"6","author":"van Teeseling","year":"2015","journal-title":"Nat. Commun."},{"key":"2021040918541330300_b43","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.tim.2009.12.004","article-title":"Architecture of peptidoglycan: more data and more models","volume":"18","author":"Vollmer","year":"2010","journal-title":"Trends Microbiol."},{"key":"2021040918541330300_b44","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1128\/JB.103.3.778-788.1970","article-title":"Mechanism of d-cycloserine action: transport systems for d-alanine, d-cycloserine, l-alanine, and glycine","volume":"103","author":"Wargel","year":"1970","journal-title":"J. Bacteriol."},{"key":"2021040918541330300_b45","doi-asserted-by":"crossref","first-page":"e1994","DOI":"10.1371\/journal.pone.0001994","article-title":"Sorting signals, N-terminal modifications and abundance of the chloroplast proteome","volume":"3","author":"Zybailov","year":"2008","journal-title":"PLoS One"}],"container-title":["The Plant Cell"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/plcell\/article-pdf\/28\/7\/1521\/37009659\/plcell_v28_7_1521.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/plcell\/article-pdf\/28\/7\/1521\/37009659\/plcell_v28_7_1521.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,2]],"date-time":"2022-07-02T00:34:49Z","timestamp":1656722089000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/plcell\/article\/28\/7\/1521\/6098325"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,6,20]]},"references-count":45,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2016,6,20]]},"published-print":{"date-parts":[[2016,8,4]]}},"URL":"https:\/\/doi.org\/10.1105\/tpc.16.00104","relation":{},"ISSN":["1532-298X","1040-4651"],"issn-type":[{"value":"1532-298X","type":"electronic"},{"value":"1040-4651","type":"print"}],"subject":[],"published-other":{"date-parts":[[2016,7,1]]},"published":{"date-parts":[[2016,6,20]]}}}