Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion

Fitzek E, Orton L, Entwistle S, Grayburn W, Ausland C, Duvall MR, Yin Y (2019)

Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Fitzek, ElisabethUniBi; Orton, Lauren; Entwistle, Sarah; Grayburn, W; Ausland, Catherine; Duvall, Melvin R.; Yin, Yanbin
Abstract / Bemerkung
Previous analysis of charophyte green algal (CGA) genomes and transcriptomes for specific protein families revealed that numerous land plant characteristics had already evolved in CGA. In this study, we have sequenced and assembled the transcriptome of Zygnema circumcarinatum UTEX 1559, and combined its predicted protein sequences with those of 13 additional species [five embryophytes (Emb), eight charophytes (Cha), and two chlorophytes (Chl) as the outgroup] for a comprehensive comparative genomics analysis. In total 25,485 orthologous gene clusters (OGCs, equivalent to protein families) of the 14 species were classified into nine OGC groups. For example, the Cha+Emb group contains 4,174 OGCs found in both Cha and Emb but not Chl species, representing protein families that have evolved in the common ancestor of Cha and Emb. Different OGC groups were subjected to a Gene Ontology (GO) enrichment analysis with the Chl+Cha+Emb group (including 5,031 OGCs found in Chl and Cha and Emb) as the control. Interestingly, nine of the 20 top enriched GO terms in the Cha+Emb group are cell wall-related, such as biological processes involving celluloses, pectins, lignins, and xyloglucans. Furthermore, three glycosyltransferase families (GT2, 8, 43) were selected for in-depth phylogenetic analyses, which confirmed their presence in UTEX 1559. More importantly, of different CGA groups, only Zygnematophyceae has land plant cellulose synthase (CesA) orthologs, while other charophyte CesAs form a CGA-specific CesA-like (Csl) subfamily (likely also carries cellulose synthesis activity). Quantitative real-time-PCR experiments were performed on selected GT family genes in UTEX 1559. After osmotic stress treatment, significantly elevated expression was found for GT2 family genes ZcCesA, ZcCslC and ZcCslA-like (possibly mannan and xyloglucan synthases, respectively), as well as for GT8 family genes (possibly pectin synthases). All these suggest that the UTEX 1559 cell wall polysaccharide synthesis-related genes respond to osmotic stress in a manner that is similar to land plants.
charophyte green algae; RNA-seq; Zygnema circumcarinatum; glycosyltransferases; osmotic stress; gene expression
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Fitzek E, Orton L, Entwistle S, et al. Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion. FRONTIERS IN PLANT SCIENCE. 2019;10: 732.
Fitzek, E., Orton, L., Entwistle, S., Grayburn, W., Ausland, C., Duvall, M. R., & Yin, Y. (2019). Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion. FRONTIERS IN PLANT SCIENCE, 10, 732. doi:10.3389/fpls.2019.00732
Fitzek, Elisabeth, Orton, Lauren, Entwistle, Sarah, Grayburn, W, Ausland, Catherine, Duvall, Melvin R., and Yin, Yanbin. 2019. “Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion”. FRONTIERS IN PLANT SCIENCE 10: 732.
Fitzek, E., Orton, L., Entwistle, S., Grayburn, W., Ausland, C., Duvall, M. R., and Yin, Y. (2019). Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion. FRONTIERS IN PLANT SCIENCE 10:732.
Fitzek, E., et al., 2019. Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion. FRONTIERS IN PLANT SCIENCE, 10: 732.
E. Fitzek, et al., “Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion”, FRONTIERS IN PLANT SCIENCE, vol. 10, 2019, : 732.
Fitzek, E., Orton, L., Entwistle, S., Grayburn, W., Ausland, C., Duvall, M.R., Yin, Y.: Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion. FRONTIERS IN PLANT SCIENCE. 10, : 732 (2019).
Fitzek, Elisabeth, Orton, Lauren, Entwistle, Sarah, Grayburn, W, Ausland, Catherine, Duvall, Melvin R., and Yin, Yanbin. “Cell Wall Enzymes in Zygnema circumcarinatum UTEX 1559 Respond to Osmotic Stress in a Plant-Like Fashion”. FRONTIERS IN PLANT SCIENCE 10 (2019): 732.

60 References

Daten bereitgestellt von Europe PubMed Central.

Plant evolution: landmarks on the path to terrestrial life.
de Vries J, Archibald JM., New Phytol. 217(4), 2018
PMID: 29318635
Embryophyte stress signaling evolved in the algal progenitors of land plants.
de Vries J, Curtis BA, Gould SB, Archibald JM., Proc. Natl. Acad. Sci. U.S.A. 115(15), 2018
PMID: 29581286
How Embryophytic is the Biosynthesis of Phenylpropanoids and their Derivatives in Streptophyte Algae?
de Vries J, de Vries S, Slamovits CH, Rose LE, Archibald JM., Plant Cell Physiol. 58(5), 2017
PMID: 28340089
Streptophyte Terrestrialization in Light of Plastid Evolution.
de Vries J, Stanton A, Archibald JM, Gould SB., Trends Plant Sci. 21(6), 2016
PMID: 26895731
Algal ancestor of land plants was preadapted for symbiosis.
Delaux PM, Radhakrishnan GV, Jayaraman D, Cheema J, Malbreil M, Volkening JD, Sekimoto H, Nishiyama T, Melkonian M, Pokorny L, Rothfels CJ, Sederoff HW, Stevenson DW, Surek B, Zhang Y, Sussman MR, Dunand C, Morris RJ, Roux C, Wong GK, Oldroyd GE, Ane JM., Proc. Natl. Acad. Sci. U.S.A. 112(43), 2015
PMID: 26438870
The Evolutionary Origin of a Terrestrial Flora.
Delwiche CF, Cooper ED., Curr. Biol. 25(19), 2015
PMID: 26439353
Lignin-like compounds and sporopollenin coleochaete, an algal model for land plant ancestry.
Delwiche CF, Graham LE, Thomson N., Science 245(4916), 1989
PMID: 17744148
Editorial: Charophytes: Evolutionary Ancestors of Plants and Emerging Models for Plant Research.
Domozych D, Sorensen I, Popper ZA., Front Plant Sci 8(), 2017
PMID: 28352277
HMMER web server: 2015 update.
Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR., Nucleic Acids Res. 43(W1), 2015
PMID: 25943547
UniProt: the universal protein knowledgebase.
The UniProt Consortium., Nucleic Acids Res. 45(D1), 2016
PMID: 27899622
Phytozome: a comparative platform for green plant genomics.
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS., Nucleic Acids Res. 40(Database issue), 2011
PMID: 22110026
Full-length transcriptome assembly from RNA-Seq data without a reference genome.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A., Nat. Biotechnol. 29(7), 2011
PMID: 21572440
Origin of land plants: do conjugating green algae hold the key?
Wodniok S, Brinkmann H, Glockner G, Heidel AJ, Philippe H, Melkonian M, Becker B., BMC Evol. Biol. 11(), 2011
PMID: 21501468
Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense reaction.
Holzinger A, Kaplan F, Blaas K, Zechmann B, Komsic-Buchmann K, Becker B., PLoS ONE 9(10), 2014
PMID: 25340847
Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation.
Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, Sato S, Yamada T, Mori H, Tajima N, Moriyama T, Ikeuchi M, Watanabe M, Wada H, Kobayashi K, Saito M, Masuda T, Sasaki-Sekimoto Y, Mashiguchi K, Awai K, Shimojima M, Masuda S, Iwai M, Nobusawa T, Narise T, Kondo S, Saito H, Sato R, Murakawa M, Ihara Y, Oshima-Yamada Y, Ohtaka K, Satoh M, Sonobe K, Ishii M, Ohtani R, Kanamori-Sato M, Honoki R, Miyazaki D, Mochizuki H, Umetsu J, Higashi K, Shibata D, Kamiya Y, Sato N, Nakamura Y, Tabata S, Ida S, Kurokawa K, Ohta H., Nat Commun 5(), 2014
PMID: 24865297
Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis.
Jensen JK, Busse-Wicher M, Poulsen CP, Fangel JU, Smith PJ, Yang JY, Pena MJ, Dinesen MH, Martens HJ, Melkonian M, Wong GK, Moremen KW, Wilkerson CG, Scheller HV, Dupree P, Ulvskov P, Urbanowicz BR, Harholt J., New Phytol. 218(3), 2018
PMID: 29460505
Conservation of ethylene as a plant hormone over 450 million years of evolution.
Ju C, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR, Delwiche CF, Chang C., Nat Plants 1(), 2015
PMID: 27246051
Streptophyte algae and the origin of embryophytes.
Becker B, Marin B., Ann. Bot. 103(7), 2009
PMID: 19273476
OrthoMCL: identification of ortholog groups for eukaryotic genomes.
Li L, Stoeckert CJ Jr, Roos DS., Genome Res. 13(9), 2003
PMID: 12952885
Evolution, gene expression profiling and 3D modeling of CSLD proteins in cotton.
Li Y, Yang T, Dai D, Hu Y, Guo X, Guo H., BMC Plant Biol. 17(1), 2017
PMID: 28693426
Novel cell wall architecture of isoxaben-habituated Arabidopsis suspension-cultured cells: global transcript profiling and cellular analysis.
Manfield IW, Orfila C, McCartney L, Harholt J, Bernal AJ, Scheller HV, Gilmartin PM, Mikkelsen JD, Paul Knox J, Willats WG., Plant J. 40(2), 2004
PMID: 15447652
Charophyte algae and land plant origins.
McCourt RM, Delwiche CF, Karol KG., Trends Ecol. Evol. (Amst.) 19(12), 2004
PMID: 16701329
Phospholipid-based signaling in plants.
Meijer HJ, Munnik T., Annu Rev Plant Biol 54(), 2003
PMID: 14502992
Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae.
Mikkelsen MD, Harholt J, Ulvskov P, Johansen IE, Fangel JU, Doblin MS, Bacic A, Willats WG., Ann. Bot. 114(6), 2014
PMID: 25204387
Corrigendum: Identification and evolution of a plant cell wall specific glycoprotein glycosyl transferase, ExAD.
Moller SR, Yi X, Velasquez SM, Gille S, Hansen PLM, Poulsen CP, Olsen CE, Rejzek M, Parsons H, Yang Z, Wandall HH, Clausen H, Field RA, Pauly M, Estevez JM, Harholt J, Ulvskov P, Petersen BL., Sci Rep 7(), 2017
PMID: 28535152
Phospholipases Dζ1 and Dζ2 have distinct roles in growth and antioxidant systems in Arabidopsis thaliana responding to salt stress.
Ben Othman A, Ellouzi H, Planchais S, De Vos D, Faiyue B, Carol P, Abdelly C, Savoure A., Planta 246(4), 2017
PMID: 28667438
Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate.
Munnik T, Meijer HJ, Ter Riet B, Hirt H, Frank W, Bartels D, Musgrave A., Plant J. 22(2), 2000
PMID: 10792830
Cold stress affects H+-ATPase and phospholipase D activity in Arabidopsis.
Muzi C, Camoni L, Visconti S, Aducci P., Plant Physiol. Biochem. 108(), 2016
PMID: 27497302
The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization.
Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D, Ullrich KK, Haas FB, Vanderstraeten L, Becker D, Lang D, Vosolsobe S, Rombauts S, Wilhelmsson PKI, Janitza P, Kern R, Heyl A, Rumpler F, Villalobos LIAC, Clay JM, Skokan R, Toyoda A, Suzuki Y, Kagoshima H, Schijlen E, Tajeshwar N, Catarino B, Hetherington AJ, Saltykova A, Bonnot C, Breuninger H, Symeonidi A, Radhakrishnan GV, Van Nieuwerburgh F, Deforce D, Chang C, Karol KG, Hedrich R, Ulvskov P, Glockner G, Delwiche CF, Petrasek J, Van de Peer Y, Friml J, Beilby M, Dolan L, Kohara Y, Sugano S, Fujiyama A, Delaux PM, Quint M, Theißen G, Hagemann M, Harholt J, Dunand C, Zachgo S, Langdale J, Maumus F, Van Der Straeten D, Gould SB, Rensing SA., Cell 174(2), 2018
PMID: 30007417
Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex.
Nixon BT, Mansouri K, Singh A, Du J, Davis JK, Lee JG, Slabaugh E, Vandavasi VG, O'Neill H, Roberts EM, Roberts AW, Yingling YG, Haigler CH., Sci Rep 6(), 2016
PMID: 27345599
Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants.
Norris JH, Li X, Huang S, Van de Meene AML, Tran ML, Killeavy E, Chaves AM, Mallon B, Mercure D, Tan HT, Burton RA, Doblin MS, Kim SH, Roberts AW., Plant Physiol. 175(1), 2017
PMID: 28768816
FastTree 2--approximately maximum-likelihood trees for large alignments.
Price MN, Dehal PS, Arkin AP., PLoS ONE 5(3), 2010
PMID: 20224823
Plants under Stress: Involvement of Auxin and Cytokinin.
Bielach A, Hrtyan M, Tognetti VB., Int J Mol Sci 18(7), 2017
PMID: 28677656
Quality control and preprocessing of metagenomic datasets.
Schmieder R, Edwards R., Bioinformatics 27(6), 2011
PMID: 21278185
Automated generation of heuristics for biological sequence comparison.
Slater GS, Birney E., BMC Bioinformatics 6(), 2005
PMID: 15713233
The charophycean green algae provide insights into the early origins of plant cell walls.
Sorensen I, Pettolino FA, Bacic A, Ralph J, Lu F, O'Neill MA, Fei Z, Rose JK, Domozych DS, Willats WG., Plant J. 68(2), 2011
PMID: 21707800
Mannan synthase activity in the CSLD family.
Verhertbruggen Y, Yin L, Oikawa A, Scheller HV., Plant Signal Behav 6(10), 2011
PMID: 21904114
Plant hormone-mediated regulation of stress responses.
Verma V, Ravindran P, Kumar PP., BMC Plant Biol. 16(), 2016
PMID: 27079791
Expression profiling and integrative analysis of the CESA/CSL superfamily in rice.
Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, Cui X, Peng L., BMC Plant Biol. 10(), 2010
PMID: 21167079
Phylotranscriptomic analysis of the origin and early diversification of land plants.
Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, Ayyampalayam S, Barker MS, Burleigh JG, Gitzendanner MA, Ruhfel BR, Wafula E, Der JP, Graham SW, Mathews S, Melkonian M, Soltis DE, Soltis PS, Miles NW, Rothfels CJ, Pokorny L, Shaw AJ, DeGironimo L, Stevenson DW, Surek B, Villarreal JC, Roure B, Philippe H, dePamphilis CW, Chen T, Deyholos MK, Baucom RS, Kutchan TM, Augustin MM, Wang J, Zhang Y, Tian Z, Yan Z, Wu X, Sun X, Wong GK, Leebens-Mack J., Proc. Natl. Acad. Sci. U.S.A. 111(45), 2014
PMID: 25355905
Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome.
Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K, Yamaoka S, Nishihama R, Nakamura Y, Berger F, Adam C, Aki SS, Althoff F, Araki T, Arteaga-Vazquez MA, Balasubrmanian S, Barry K, Bauer D, Boehm CR, Briginshaw L, Caballero-Perez J, Catarino B, Chen F, Chiyoda S, Chovatia M, Davies KM, Delmans M, Demura T, Dierschke T, Dolan L, Dorantes-Acosta AE, Eklund DM, Florent SN, Flores-Sandoval E, Fujiyama A, Fukuzawa H, Galik B, Grimanelli D, Grimwood J, Grossniklaus U, Hamada T, Haseloff J, Hetherington AJ, Higo A, Hirakawa Y, Hundley HN, Ikeda Y, Inoue K, Inoue SI, Ishida S, Jia Q, Kakita M, Kanazawa T, Kawai Y, Kawashima T, Kennedy M, Kinose K, Kinoshita T, Kohara Y, Koide E, Komatsu K, Kopischke S, Kubo M, Kyozuka J, Lagercrantz U, Lin SS, Lindquist E, Lipzen AM, Lu CW, De Luna E, Martienssen RA, Minamino N, Mizutani M, Mizutani M, Mochizuki N, Monte I, Mosher R, Nagasaki H, Nakagami H, Naramoto S, Nishitani K, Ohtani M, Okamoto T, Okumura M, Phillips J, Pollak B, Reinders A, Rovekamp M, Sano R, Sawa S, Schmid MW, Shirakawa M, Solano R, Spunde A, Suetsugu N, Sugano S, Sugiyama A, Sun R, Suzuki Y, Takenaka M, Takezawa D, Tomogane H, Tsuzuki M, Ueda T, Umeda M, Ward JM, Watanabe Y, Yazaki K, Yokoyama R, Yoshitake Y, Yotsui I, Zachgo S, Schmutz J., Cell 171(2), 2017
PMID: 28985561
Identification of novel proteins in isolated polyphosphate vacuoles in the primitive red alga Cyanidioschyzon merolae.
Yagisawa F, Nishida K, Yoshida M, Ohnuma M, Shimada T, Fujiwara T, Yoshida Y, Misumi O, Kuroiwa H, Kuroiwa T., Plant J. 60(5), 2009
PMID: 19709388
The cooperative activities of CSLD2, CSLD3, and CSLD5 are required for normal Arabidopsis development.
Yin L, Verhertbruggen Y, Oikawa A, Manisseri C, Knierim B, Prak L, Jensen JK, Knox JP, Auer M, Willats WG, Scheller HV., Mol Plant 4(6), 2011
PMID: 21471331
Evolution and function of the plant cell wall synthesis-related glycosyltransferase family 8.
Yin Y, Chen H, Hahn MG, Mohnen D, Xu Y., Plant Physiol. 153(4), 2010
PMID: 20522722
The cellulose synthase superfamily in fully sequenced plants and algae.
Yin Y, Huang J, Xu Y., BMC Plant Biol. 9(), 2009
PMID: 19646250
dbCAN: a web resource for automated carbohydrate-active enzyme annotation.
Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y., Nucleic Acids Res. 40(Web Server issue), 2012
PMID: 22645317
Fast and sensitive protein alignment using DIAMOND.
Buchfink B, Xie C, Huson DH., Nat. Methods 12(1), 2014
PMID: 25402007
The Evolution of Cell Division: From Streptophyte Algae to Land Plants.
Buschmann H, Zachgo S., Trends Plant Sci. 21(10), 2016
PMID: 27477927
XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan.
Chiniquy D, Sharma V, Schultink A, Baidoo EE, Rautengarten C, Cheng K, Carroll A, Ulvskov P, Harholt J, Keasling JD, Pauly M, Scheller HV, Ronald PC., Proc. Natl. Acad. Sci. U.S.A. 109(42), 2012
PMID: 23027943

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