Callose is a plant-specific polysaccharide (β-1,3-glucan) playing an important role in angiosperms in many developmental processes and responses to biotic and abiotic stresses. Callose is synthesised at the plasma membrane of plant cells by callose synthase (CalS) and, among others, represents the main polysaccharide in the callose wall surrounding the tetrads of developing microspores and in the growing pollen tube wall. CalS proteins involvement in spore development is a plesiomorphic feature of terrestrial plants, but very little is known about their evolutionary origin and relationships amongst the members of this protein family. We performed thorough comparative analyses of callose synthase family proteins from major plant lineages to determine their evolutionary history across the plant kingdom. A total of 1211 candidate CalS sequences were identified and compared amongst diverse taxonomic groups of plants, from bryophytes to angiosperms. Phylogenetic analyses identified six main clades of CalS proteins and suggested duplications during the evolution of specialised functions. Twelve family members had previously been identified in Arabidopsis thaliana. We focused on five CalS subfamilies directly linked to pollen function and found that proteins expressed in pollen evolved twice. CalS9/10 and CalS11/12 formed well-defined clades, whereas pollen-specific CalS5 was found within subfamilies that mostly did not express in mature pollen vegetative cell, although were found in sperm cells. Expression of five out of seven mature pollen-expressed CalS genes was affected by mutations in bzip transcription factors. Only three subfamilies, CalS5, CalS10, and CalS11, however, formed monophyletic, mostly conserved clades. The pairs CalS9/CalS10, CalS11/CalS12 and CalS3 may have diverged after angiosperms diversified from lycophytes and bryophytes. Our analysis of fully sequenced plant proteins identified new evolutionary lineages of callose synthase subfamilies and has established a basis for understanding their functional evolution in terrestrial plants.

Laboratory of Pollen Biology Institute of Experimental Botany Academy of Sciences of the Czech Republic Rozvojová 263 Praha 6 Czech Republic

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Wellman CH. 2004. Origin, function and development of the spore wall in early land plants In: Hemsley AR, Poole I, eds. Evolution of plant physiology. Kew: Royal Botanic Gardens, 43–63. doi: 10.1104/pp.103.033068 DOI

Wallace S, Fleming A, Wellman CH, Beerling DJ. 2011. Evolutionary development of the plant spore and pollen wall. AoB Plants 2011 plr027 doi: 10.1093/aobpla/plr027 PubMed DOI PMC

Firon N, Nepi M, Pacini E. 2012. Water status associated processes mark critical stages in pollen development and functioning. Annals of Botany 109/7: 1201–1213. doi: 10.1093/aob/mcs070 PubMed DOI PMC

Quilichini TD, Grienenberger E, Douglas CJ (2015) The biosynthesis, composition and assembly of the outer pollen wall: A tough case to crack. Phytochemistry 113:170–182. doi: 10.1016/j.phytochem.2014.05.002 PubMed DOI

Williams JS (2008) Novelties of the flowering plant pollen tube underlie diversification of a key life history stage. Proc Natl Acad Sci U S A 105 (32):11259–11263 doi: 10.1073/pnas.0800036105 PubMed DOI PMC

Dong XY, Hong ZL, Sivaramakrishnan M, Mahfouz M, Verma DPS. 2005. Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant Journal 42: 315–328. doi: 10.1111/j.1365-313X.2005.02379.x PubMed DOI

Nishikawa SI, Zinkl GM, Swanson RJ, Maruyama D, Preuss D. 2005. Callose (beta-1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biology 5: 9 doi: 10.1186/1471-2229-5-9 PubMed DOI PMC

Paxson-Sowders DM, Dodrill CH, Owen HA, Makaroff CA (2001) DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol 127: 1739–1749 PubMed PMC

Ariizumi T, Hatakeyama K, Hinata K, Inatsugi R, Nishida I, Sato S, Kato T, Tabata S, Toriyama K (2004) Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J 39: 170–181 doi: 10.1111/j.1365-313X.2004.02118.x PubMed DOI

Guan YF, Huang XY, Zhu J, Gao JF, Zhang HX, Yang ZN (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol 147: 852–863 doi: 10.1104/pp.108.118026 PubMed DOI PMC

Gibalová A, Reňák D, Matczuk K, Dupl'áková N, Cháb D, Twell D, Honys D (2009) AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen. Plant Molecular Biology 70 (5):581–601. doi: 10.1007/s11103-009-9493-y PubMed DOI

Backues SK, Korasick DA, Heese A, Bednarek SY (2010) The Arabidopsis Dynamin-Related Protein2 Family Is Essential for Gametophyte Development. Plant Cell 22 (10):3218–3231. doi: 10.1105/tpc.110.077727 PubMed DOI PMC

Reyes F, Leon G, Donoso M, Brandizzi F, Weber APM, Orellana A (2010) The nucleotide sugar transporters AtUTr1 and AtUTr3 are required for the incorporation of UDP-glucose into the endoplasmic reticulum, are essential for pollen development and are needed for embryo sac progress in Arabidopsis thaliana. Plant Journal 61 (3):423–435. doi: 10.1111/j.1365-313X.2009.04066.x PubMed DOI

Park J-I, Ishimizu T, Suwabe K, Sudo K, Masuko H, Hakozaki H, Nou I-S, Suzuki G, Watanabe M (2010) UDP-Glucose Pyrophosphorylase is Rate Limiting in Vegetative and Reproductive Phases in Arabidopsis thaliana. Plant and Cell Physiology 51 (6):981–996. doi: 10.1093/pcp/pcq057 PubMed DOI

Quilichini TD, Friedmann MC, Samuels AL, Douglas CJ (2010) ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiol 154: 678–690 doi: 10.1104/pp.110.161968 PubMed DOI PMC

Dobritsa AA, Lei Z, Nishikawa S, Urbanczyk-Wochniak E, Huhman DV, Preuss D, Sumner LW (2010) LAP5 and LAP6 encode anther-specific proteins with similarity to chalcone synthase essential for pollen exine development in Arabidopsis. Plant Physiol 153 (3):937–955. doi: 10.1104/pp.110.157446 PubMed DOI PMC

Yang J, Tian L, Sun M-X, Huang X-Y, Zhu J, Guan Y-F, Jia Q-S, Yang Z-N (2013) AUXIN RESPONSE FACTOR17 Is Essential for Pollen Wall Pattern Formation in Arabidopsis. Plant Physiology 162 (2):720–731. doi: 10.1104/pp.113.214940 PubMed DOI PMC

Gibalová A, Steinbachová L, Hafidh S, Bláhová V, Gadiou Z, Michailidis C, Müller K, Pleskot R, Dupláková N, Honys D (2017) Characterization of pollen-expressed bZIP protein interactions and the role of ATbZIP18 in the male gametophyte. Plant Reprod 30 (1):1–17. doi: 10.1007/s00497-016-0295-5 PubMed DOI

Pacini E, Dolferus R. 2016. The trials and tribulations of the plant male gametophyte. Understanding reproductive stage stress tolerance. In Abiotic and Biotic Stress in Plants. Recent Advances and Future Perspectives; Shanker AK, Shanker C, Eds.; InTech: Rijeka, Croatia, 2016; pp. 703–754.

Ellinger D, Voigt CA. 2014. Callose biosynthesis in Arabidopsis with a focus on pathogen response: what we have learned within the last decade. Annals of Botany 114: 1349–1358. doi: 10.1093/aob/mcu120 PubMed DOI PMC

Chen X-Y, Kim J-Y. 2009. Callose synthesis in higher plants. Plant Signaling & Behavior 4: 489–492. PubMed PMC

Waterkeyn L. and Beinfait A. 1970. On a possible function of the callosic special wall in Ipomoea purpurea (L.) Roth. Grana 10: 13–20.

Falter C, Zwikiwics C, Eggert D, Blümke A, Naumann M, Wolff K et al. 2015. Glucanocellulosic ethanol: the undiscovered biofuel potential in energy crops and marine biomass. Scientific Reports 5: 13722, doi: 10.1038/srep13722 PubMed DOI PMC

Richmond TA, and Somerville CR. 2000. The cellulose synthase superfamily. Plant Physiology 124, 495–498. PubMed PMC

Verma DPS, Hong ZL. 2001. Plant callose synthase complexes. Plant Molecular Biology 47: 693–701. PubMed

Hong Z, Delauney AJ, Verma DPS. 2001. A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell 13: 755–768. PubMed PMC

Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU. 2005. A gene expression map of Arabidopsis thaliana development. Nat Genet 37 (5):501–506. doi: 10.1038/ng1543 PubMed DOI

Voigt CA, Schafer W, Salomon S. 2006. A comprehensive view on organ-specific callose synthesis in wheat (Triticum aestivum L.): glucan synthase-like gene expression, callose synthase activity, callose quantification and deposition. Plant Physiology and Biochemistry 44: 242–247. doi: 10.1016/j.plaphy.2006.05.001 PubMed DOI

Piršelová B, Matušíková I. 2013. Callose: The plant cell wall polysaccharide with multiple biological functions. Acta Physiologiae Plantarum 35: 635–644.·: doi: 10.1007/s11738-012-1103-y DOI

Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ. 2007. An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets. PLoS ONE 2(8): e718 doi: 10.1371/journal.pone.0000718 PubMed DOI PMC

Xie B, Deng YF, Kanaoka MM, Okada K, Hong ZL. 2012. Expression of Arabidopsis callose synthase 5 results in callose accumulation and cell wall permeability alteration. Plant Science 183: 1–8. doi: 10.1016/j.plantsci.2011.10.015 PubMed DOI

Stone BA, Clarke AE. 1992. Chemistry and physiology of higher plant1,3-b-glucans(Callose) In: Stone BA, Clarke AE (Eds). Chemistry and biology of (1,3)-b-glucans. Bundoora, Australia: La Trobe University Press, p. 365–429.

McCormick S. 2004. Control of male gametophyte development. PlantCell 16 (Suppl): S142–53. PubMed PMC

Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE. 2005. Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Molecular Biology 58: 333–349. doi: 10.1007/s11103-005-4526-7 PubMed DOI

Zhang C, Guinel FC and Moffatt BA. 2002. A comparative ultrastructural study of pollen development in Arabidopsis thaliana ecotype Columbia and male-sterile mutant Apt1-3. Protoplasma, 219, 59–71. PubMed

Lu P, Chai M, Yang J, Ning G, Wang G, Ma H. 2014. The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 Gene Is Required for Male Fertility through Regulating Callose Metabolism during Microsporogenesis. Plant Physiology 164/4: 1893–1904. doi: 10.1104/pp.113.233387 PubMed DOI PMC

Cui W, Lee J-Y. 2016. Arabidopsis callose synthses CalS1/8 regulate plasmodesmatal permeability during stress. Nature Plants 16034. doi: 10.1038/NPLANTS.2016.34 PubMed DOI

Vatén A, Dettmer J, Wu S, Stierhof YD, Miyashima S, Yadav SR, et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell. 2011;21: 1144–1155. doi: 10.1016/j.devcel.2011.10.006 . PubMed DOI

Abercrombie JM, O'Meara BC, Moffatt AR, Williams JH. 2011. Developmental evolution of flowering plant pollen tube cell walls: callose synthase (CalS) gene expression patterns. Evolution and Development 2: 13. PubMed PMC

Töller A, Brownfield L, Neu C, Twell D, Schulze-Lefert P. 2008. Dual function of Arabidopsis glucan synthase-like genes GSL8 and GSL10 in male gametophyte development and plant growth. Plant Journal 54: 911–923. doi: 10.1111/j.1365-313X.2008.03462.x PubMed DOI

Maeda H, Song W, Sage T, DellaPenna D. 2014. Role of callose synthases in transfer cell wall development in tocopherol deficient Arabidopsis mutants. Frontiers in Plant Science 5. PubMed PMC

Huang LJ, Chen XY, Rim Y, Han X, Cho WK, Kim SW, Kim JY. 2009. Arabidopsis glucan synthase-like 10 functions in male gametogenesis. Journal of Plant Physiology 166: 344–352. doi: 10.1016/j.jplph.2008.06.010 PubMed DOI

Thiele K, Wanner G, Kindzierski V, et al. 2009. The timely deposition of callose is essential for cytokinesis in Arabidopsis. Plant Journal 58: 13–26. doi: 10.1111/j.1365-313X.2008.03760.x PubMed DOI

Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE, Xie B, et al. 2010. Dysregulation of cell-to-cell connectivity and stomatal pattering by loss-of-fuction mutation in Arabidopsis chorus (glucan synthase-like8). Development 137: 1731–1741. doi: 10.1242/dev.049197 PubMed DOI

Xu T, Zhang C, Zhou Q, Yang ZN. 2016. Pollen wall pattern in Arabidopsis. Science Bulletin 61: 832–837.

Ellinger D, Voigt CA. 2014Callose biosynthesis in Arabidopsis with a focus on pathogen response: what we have learned within the last decade. Annals of Botany 114/6: 1349–1358. doi: 10.1093/aob/mcu120 PubMed DOI PMC

Yang J, Tian L, Sun M-X, Huang X-Y, Zhu J, Guan Y-Y et al. 2013. Auxin Response Factor17 is essential for pollen wall pattern formation in Arabidopsis. Plant Physiology 162/2: 720–731. doi: 10.1104/pp.113.214940 PubMed DOI PMC

Schuette S, Wood AJ, Geisler M, Geisler-Lee J, Ligrone R, Renzaglia KS. 2009. Novel localization of callose in the spores of Physcomitrella patens and phylogenomics of the callose synthase gene family. Annals of Botany 103: 749–756. doi: 10.1093/aob/mcn268 PubMed DOI PMC

Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biology 5 (11). doi:R85 PubMed PMC

Majerská J, Schrumpfová Prochazková P, Dokládal L, Schořová S, Stejskal K, Obořil M, Honys D, Kozaková L, Polanská PS, Sýkorová E (2016) Tandem affinity purification of AtTERT reveals putative interaction partners of plant telomerase in vivo. Protoplasma. doi: 10.1007/s00709-016-1042-3 PubMed DOI

Fíla J, Záveská Drábková L, Gibalová A and Honys D. 2017. When simple meets complex; pollen and the -omics—Obermeyer G. and Feijó J.(ed.) Pollen Tip Growth—From Biophysical Aspects to System Biology. Springer International Publishing AG, pp. 247–292.

Craigon DJ, James N, Okyere J, Higgins J, Jotham J, May S (2004) NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res 32 (Database issue):D575–577 doi: 10.1093/nar/gkh133 PubMed DOI PMC

Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98 (1):31–36 doi: 10.1073/pnas.98.1.31 PubMed DOI PMC

Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: Model validation, design issues and standard error application. Genome Biol 2:R32 PubMed PMC

Hafidh S, Breznenová K, Honys D (2012) De novo post-pollen mitosis II tobacco pollen tube transcriptome. Plant Signal Behav 7 (8):918–921. doi: 10.4161/psb.20745 PubMed DOI PMC

Hafidh S, Breznenová K, Ružička P, Fecikova J, Čapková V, Honys D (2012) Comprehensive analysis of tobacco pollen transcriptome unveils common pathways in polar cell expansion and underlying heterochronic shift during spermatogenesis. BMC Plant Biol 12:24 doi: 10.1186/1471-2229-12-24 PubMed DOI PMC

Bokvaj P, Hafidh S, Honys D 2015. Transcriptome profiling of male gametophyte development in Nicotiana tabacum. Genomics Data 3: 106–111. doi: 10.1016/j.gdata.2014.12.002 PubMed DOI PMC

Honys D, Reňák D, Feciková J, Jedelský PL, Nebesářová J, Dobrev P, Čapková V (2009) Cytoskeleton-associated large RNP complexes in tobacco male gametopyte (EPPs) are associated with ribosomes and are involved in protein synthesis, processing and localisation. Journal of Proteome Research, 8(4): 2015–2031. doi: 10.1021/pr8009897 PubMed DOI

Jurečková JF, Sýkorová E, Hafidh S, Honys D, Fajkus J, Fojtová M (2017) Tissue-specific expression of telomerase reverse transcriptase gene variants in Nicotiana tabacum. Planta 245 (3):549–561. doi: 10.1007/s00425-016-2624-1 PubMed DOI

Sievers F. et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7, 539 doi: 10.1038/msb.2011.75 PubMed DOI PMC

Néron B, Ménager H, Maufrais C, Joly N, Maupetit J, Letort S et al. 2009. Mobyle: a new full web bioinformatics framework. Bioinformatics 25 (22): 3005–3011. doi: 10.1093/bioinformatics/btp493 PubMed DOI PMC

Söding J (2005) Protein homology detection by HMM–HMM comparison. Bioinformatics 21: 951–960. doi: 10.1093/bioinformatics/bti125 PubMed DOI

Chen Y, Zou M, Cao Y. 2014. Transcriptome analysis of the Arabidopsis semi-in vivo pollen tube guidance system uncovers a distinct gene expression profile. J Plant Biol 57 (2):93–105.

Kumar S, Stecher G, and Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–1874. doi: 10.1093/molbev/msw054 PubMed DOI PMC

Letunic I and Bork P. 2016. Interactive Tree Of Life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. doi: 10.1093/nar/gkw290 PubMed DOI PMC

Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014 May 1; 30(9): 1312–1313. PubMed PMC

Tamura K, Battistuzzi FU, Billing-Ross P, Murillo O, Filipski A, Kumar S 2012. Estimating divergence time in large molecular phylogenies. PNAS 109/47: 19333–19338. PubMed PMC

Bateman A., Birney E., Cerruti L., Durbin R., Etwiller L., Eddy SR. et al. 2002. The Pfam Protein Families Database Nucl. Acids Res. 30(1):276–280. PubMed PMC

Geer LY, Domarchev M, Lipman DJ, Bryant SH. 2002. CDART: protein homology by domain architecture. Genome Research 12/10: 1619–1623. doi: 10.1101/gr.278202 PubMed DOI PMC

Bailey TL, Bodén M, Buske FA, Frith M, Grant CE, Clementi L et al. 2009. MEME SUITE: tools for motif discovery and searching", Nucleic Acids Research, 37: W202–W208. doi: 10.1093/nar/gkp335 PubMed DOI PMC

Hu B, Jin J, Guo A-Y, Zhang H, Luo J. and Gao G. 2015. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics, 31(8):1296–1297. doi: 10.1093/bioinformatics/btu817 PubMed DOI PMC

Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiology 148 (2):1168–1181. doi: 10.1104/pp.108.125229 PubMed DOI PMC

Honys D, Combe JP, Twell D, Čapková V (2000) The translationally repressed pollen-specific ntp303 mRNA is stored in non-polysomal mRNPs during pollen maturation. Sex Plant Reprod 13: 135–144.

Edwards, KD, Fernandez-Pozo N, Drake-Stowe K., M. Humphry M, Evans AD, Bombarely AD et al. 2017. A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency. BMC genomics 18: 448–462. doi: 10.1186/s12864-017-3791-6 PubMed DOI PMC

Ward DM, Vaughn MB, Shiflett SL, White PL, Pollock AL, Hill J et al. 2005. The role of LIP5 and CHMP5 in multivesicular body formation and HIV-1 budding in mammalian cells. Biological Chemistry 280: 10548–10555. PubMed

Douglas CM, Foor F, Marrinan JA, Morin N, Nielsen JB, Dahl AM et al. 1994. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-beta-D-glucan synthase. PNAS 91/26: 12907–11. PubMed PMC

Williams JH, Taylor ML, O'Meara BC. 2014. Repeated evolution of tricellular (and bicellular) pollen. American Journal of Botany 101 (4):559–571. doi: 10.3732/ajb.1300423 PubMed DOI

Wickett N. J., Mirarab S., Nguyen N., Warnow T., Carpenter E., Matasci N., et al. 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. PNAS 111: E4859–E4868. doi: 10.1073/pnas.1323926111 PubMed DOI PMC

Gaudiner JC, Taylor NG, Turner SR 2003. Control of cellulose synthase complex localization in developing xylem. Plant Cell 15/8:1740–1748. doi: 10.1105/tpc.012815 PubMed DOI PMC

Evolutionary diversification of cytokinin-specific glucosyltransferases in angiosperms and enigma of missing cis-zeatin O-glucosyltransferase gene in Brassicaceae