Abstract
In plants, the ability to produce hydrophobic substances that would provide protection from dehydration was required for the transition to land. This genome-wide investigation outlines the evolution of GDSL-type esterase/lipase (GELP) proteins in the moss Physcomitrium patens and suggests possible functions of some genes. GELP proteins play roles in the formation of hydrophobic polymers such as cutin and suberin that protect against dehydration and pathogen attack. GELP proteins are also implicated in processes such as pollen development and seed metabolism and germination. The P. patens GELP gene family comprises 48 genes and 14 pseudogenes. Phylogenetic analysis of all P. patens GELP sequences along with vascular plant GELP proteins with reported functions revealed that the P. patens genes clustered within previously identified A, B and C clades. A duplication model predicting the expansion of the GELP gene family within the P. patens lineage was constructed. Expression analysis combined with phylogenetic analysis suggested candidate genes for functions such as defence against pathogens, cutin metabolism, spore development and spore germination. The presence of relatively fewer GELP genes in P. patens may reduce the occurrence of functional redundancy that complicates the characterization of vascular plant GELP genes. Knockout lines of GELP31, which is highly expressed in sporophytes, were constructed. Gelp31 spores contained amorphous oil bodies and germinated late, suggesting (a) role(s) of GELP31 in lipid metabolism in spore development or germination. Future knockout studies of other candidate GELP genes will further elucidate the relationship between expansion of the family and the ability to withstand the harsh land environment.
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References
Abascal F, Zardoy R, Telford MJ (2010) TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38:W7–W13. https://doi.org/10.1093/nar/gkq291
Agee AE, Surpin M, Sohn EJ et al (2010) Modified vacuole phenotype1 is an Arabidopsis myrosinase-associated protein involved in endomembrane protein trafficking. Plant Physiol 152:120–132. https://doi.org/10.1104/pp.109.145078
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723. https://doi.org/10.1109/TAC.1974.1100705
Almagro Armenteros JJ, Salvatore M, Winther O, Emanuelsson O, von Heijne G, Elofsson A, Nielsen H (2019) Detecting sequence signals in targeting peptides using deep learning. Life Sci All. 2:201900429. https://doi.org/10.26508/lsa.201900429
Ashton NW, Cove DJ (1977) The isolation and preliminary characterization of auxotrophic and analogue resistant mutants in the moss Physcomitrella patens. Mol Genet Genom 154:87–95. https://doi.org/10.1007/BF00265581
Brick DJ, Brumlik MJ, Buckley JT, Cao J-X, Davies PC, Misra S, Tranbarger TJ, Upton C (1995) A new family of lipolytic plant enzymes with members in rice, Arabidopsis and maize. FEBS Lett 277:475–480. https://doi.org/10.1016/0014-5793(95)01405-5
Budke JM, Goffinet B (2016) Comparative cuticle development reveals taller sporophytes are covered by thicker calyptra cuticles in mosses. Front Plant Sci 7:832
Chen M, Du X, Zhu Y, Wang Z, Hua S, Li Z, Guo W, Zhang G, Peng J, Jiang L (2012) Seed fatty acid reducer acts downstream of gibberellin signalling pathway to lower seed fatty acid storage in arabidopsis. Plant Cell Environ 35:2155–2169. https://doi.org/10.1111/j.1365-3040.2012.02546.x
Daku RM, Rabbi F, Buttigieg J, Coulson IM, Horne D, Martens G, Ashton NW, Suh D-Y (2016) PpASCL, the Physcomitrella patens anther-specific chalcone synthase-like enzyme implicated in sporopollenin biosynthesis, is needed for integrity of the moss spore wall and spore viability. PLoS ONE 11:0146817. https://doi.org/10.1371/journal.pone.0146817
Ding L-M, Guo X-J, Li M, Fu Z-L, Yan S-Z, Zhu K-M, Wang Z, Tan X-L (2019a) Improving seed germination and oil contents by regulating the GDSL transcriptional level in Brassica napus. Plant Cell Rep 38:243–253. https://doi.org/10.1007/s00299-018-2365-7
Ding L-N, Li M, Wang W-J, Cao J, Wang Z, Zhu K-M, Yang Y-H, Li Y-L, Tan X-L (2019b) Advances in plant GDSL lipases: from sequences to functional mechanisms. Acta Physiol Plant 41:151. https://doi.org/10.1007/s11738-019-2944-4
Eastmond PJ (2006) Sugar-Dependent1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell 18:665–675. https://doi.org/10.1105/tpc.105.040543
Fernandez-Pozo N, Haas FB, Meyberg R et al (2020) PEATmoss (Physcomitrella Expression Atlas Tool): a unified gene expression atlas for the model plant Physcomitrella patens. Plant J 102:165–177. https://doi.org/10.1111/tpj.14607
Girard A-L, Mounet F, Lemaire-Chamley M et al (2012) Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24:3119–3134. https://doi.org/10.1105/tpc.112.101055
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. https://doi.org/10.1093/nar/gkr944
Hilton S, Buckley JT (1991) Studies on the reaction mechanism of a microbial lipase/acyltransferase using chemical modification and site-directed mutagenesis. J Biol Chem 266:997–1000
Hiss M, Laule O, Meskauskiene RM et al (2014) Large-scale gene expression profiling data for the model moss Physcomitrella patens aid understanding of developmental progression, culture and stress conditions. Plant J 79:530–539. https://doi.org/10.1111/tpj.12572
Hiss M, Meyberg R, Westermann J, Haas FB, Schneider L, Schallenberg-Rüdinger M, Ullrich KK, Rensing SA (2017) Sexual reproduction, sporophyte development and molecular variation in the model moss Physcomitrella patens: introducing the ecotype Reute. Plant J 90:606–620. https://doi.org/10.1111/tpj.13501
Hong L, Brown J, Segerson NA, Rose JKC, Roeder AHK (2017) CUTIN SYNTHASE 2 maintains progressively developing cuticular ridges in Arabidopsis sepals. Mol Plant 10:560–574. https://doi.org/10.1016/j.molp.2017.01.002
Huang C-Y, Chung C-I, Lin Y-C, Hsing Y-IC, Huang AHC (2009) Oil bodies and oleosins in Physcomitrella possess characteristics representative of early trends in evolution. Plant Physiol 150:1192–1203. https://doi.org/10.1104/pp.109.138123
Huang L-M, Lai C-P, Chen L-FO, Chan M-T, Shaw J-F (2015) Arabidopsis SFAR4 is a novel GDSL-type esterase involved in fatty acid degradation and glucose tolerance. Bot Stud 56:33. https://doi.org/10.1186/s40529-015-0114-6
Jeffery CJ (2020) Enzymes, pseudoenzymes, and moonlighting proteins: diversity of function in protein superfamilies. FEBS J 287:4141–4149. https://doi.org/10.1111/febs.15446
Knight CD, Cove DJ, Boyd PJ, Ashton NW (1988) The isolation of biochemical and developmental mutants in Physcomitrella patens. In: Glime JM (ed) Methods in bryology, Hattori Botanical Laboratory. Nichinan, Japan
Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338. https://doi.org/10.1146/annurev.genet.39.073003.114725
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lai C-P, Huang L-M, Chen L-FO, Chan M-T, Shaw J-F (2017) Genome-wide analysis of GDSL-type esterases/lipases in Arabidopsis. Plant Mol Biol 95:181–197. https://doi.org/10.1007/s11103-017-0648-y
Lang D, Ullrich KK, Murat F et al (2018) The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant J 93:515–533. https://doi.org/10.1111/tpj.13801
Larsson A (2014) AliView: a fast and lightweight alignment viewer and editor for large data sets. Bioinformatics 30:3276–3278. https://doi.org/10.1093/bioinformatics/btu531
Li L, Aslam M, Rabbi F, Vanderwel MC, Ashton NW, Suh D-Y (2018) PpORS, an ancient type III polyketide synthase, is required for integrity of leaf cuticle and resistance to dehydration in the moss, Physcomitrella patens. Planta 247:527–541. https://doi.org/10.1007/s00425-017-2806-5
Ling H (2008) Sequence analysis of GDSL lipase gene family in Arabidopsis thaliana. Pak J Biol Sci 11:763–767. https://doi.org/10.3923/pjbs.2008.763.767
Lu M, Zhou J, Jiang S, Zeng Y, Li C, Tan X (2023) The fasciclin-like arabinogalactan proteins of Camellia oil tree are involved in pollen tube growth. Plant Sci 326:111518. https://doi.org/10.1016/j.plantsci.2022.111518
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Basutkar P, Tivey ARN, Potter SC, Finn RD, Lopez R (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47:W636–W641. https://doi.org/10.1093/nar/gkz268
Nakano RT, Matsushima R, Nagano AJ, Fukao Y, Fujiwara M, Kondo M, Nishimura M, Hara-Nishimura I (2012) ERMO3/MVP1/GOLD36 is involved in a cell type-specific mechanism for maintaining ER morphology in Arabidopsis thaliana. PLoS ONE 7:49103. https://doi.org/10.1371/journal.pone.0049103
Nie Y, Foster CSP, Zhu T, Yao R, Duchène DA, Ho SYW, Zhong B (2020) Accounting for uncertainty in the evolutionary timescale of green plants through clock-partitioning and fossil calibration strategies. Syst Biol 69:1–16. https://doi.org/10.1093/sysbio/syz032
Ortiz-Ramírez C, Hernandez-Coronado M, Thamm A, Catarino B, Wang M, Dolan L, Feijó JA, Becker JD (2016) A transcriptome atlas of Physcomitrella patens provides insights into the evolution and development of land plants. Mol Plant 9:205–220. https://doi.org/10.1016/j.molp.2015.12.002
Perroud P-F, Haas FB, Hiss M et al (2018) The Physcomitrella patens gene atlas project: large-scale RNA-seq based expression data. Plant J 95:168–182. https://doi.org/10.1111/tpj.13940
Rabbi F, Renzaglia KS, Ashton NW, Suh D-Y (2020) Reactive oxygen species are required for spore-wall formation in Physcomitrella patens. Botany 98:575–587. https://doi.org/10.1139/cjb-2020-0012
Reina JJ, Guerrero C, Heredia A (2007) Isolation, characterization, and localization of AgaSGNH cDNA: a new SGNH-motif plant hydrolase specific to Agave americana L. leaf epidermis. J Exp Bot 58:2717–2731. https://doi.org/10.1093/jxb/erm136
Rensing SA, Lang D, Zimmer AD et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69. https://doi.org/10.1126/science.1150646
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA Sequence Polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
RStudio Team (2020) R Studio: integrated development for R. RStudio, PBC, Boston, MA. http://www.rstudio.com/
Sakakibara K, Nishiyama T, Deguchi H, Hasebe M (2008) Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evol Dev 10:555–566. https://doi.org/10.1111/j.1525-142X.2008.00271.x
Schmidt MA, Herman EM (2008) Suppression of soybean oleosin produces micro-oil bodies that aggregate into oil body/ER complexes. Mol Plant 1:910–924. https://doi.org/10.1093/mp/ssn049
Seifert GJ (2018) Fascinating fasciclins: A surprisingly widespread family of proteins that mediate interactions between the cell exterior and the cell surface. Int J Mol Sci 19:1628. https://doi.org/10.3390/ijms19061628
Su H-G, Zhang X-H, Wang T-T, Wei W-L, Wang Y-X, Chen J, Zhou Y-B, Chen M, Ma Y-Z, Xu Z-S, Min D-H (2020) Genome-wide identification, evolution, and expression of GDSL-type esterase/lipase gene family in soybean. Front Plant Sci 11:726. https://doi.org/10.3389/fpls.2020.0
Teufel F, Almagro Armenteros JJ, Johansen AR, Gislason MH, Pihl SI, Tsirigos KD, Winther O, Brunak S, von Heijne G, Nielsen H (2022) SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol 40:1023–1025. https://doi.org/10.1038/s41587-021-01156-3
Thumuluri V, Almagro Armenteros JJ, Johansen AR, Nielsen H, Winther O (2022) DeepLoc 2.0: multi-label subcellular localization prediction using protein language models. Nucleic Acids Res 50:W228–W234. https://doi.org/10.1093/nar/gkac278
Upton C, Buckley JT (1995) A new family of lipolytic enzymes? Trends Biochem Sci 20:178–179. https://doi.org/10.1016/s0968-0004(00)89002-7
Volokita M, Rosilio T, Rivkin N, Zik M (2011) Combining comparative sequence and genomic data to ascertain phylogenetic relationships and explore the evolution of the large GDSL-lipase family in land plants. Mol Biol Evol 28:551–565. https://doi.org/10.1093/molbev/msq226
Vujaklija I, Bielen A, Paradžik T, Biđin S, Goldstein P, Vujaklija D (2016) An effective approach for annotation of protein families with low sequence similarity and conserved motifs: identifying GDSL hydrolases across the plant kingdom. BMC Bioinformat 17:91. https://doi.org/10.1186/s12859-016-0919-7
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699. https://doi.org/10.1093/oxfordjournals.molbev.a003851
Yeats TH, Huang W, Chatterjee S, Viart HM-F, Clausen MH, Stark RE, Rose JKC (2014) Tomato CUTIN DEFICIENT 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants. Plant J 77:667–675. https://doi.org/10.1111/tpj.12422
Zhang P, Zhang H, Du J, Qiao Y (2022) Genome-wide identification and co-expression analysis of GDSL genes related to suberin formation during fruit russeting in pear. Hortic Plant J 8:153–170. https://doi.org/10.1016/j.hpj.2021.11.010
Acknowledgements
We thank David Le for help with sequence analysis.
Funding
This work was supported by a Natural Sciences and Engineering Research Council of Canada Discovery grant (RGPIN-2018–04286). VA and FR were supported in part by University of Regina Graduate Scholarships. FR was a Saskatchewan Innovation Opportunity Graduate Scholarship recipient. WB and VEV were NSERC Undergraduate Summer Research Award recipients.
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EB performed the genome-wide study and FR performed the gene knockout study. WB, VEV and VA contributed to data collection and presentation. KR obtained microscopic images. EB and D-YS wrote the manuscript. D-YS designed the study. All authors read and approved the final manuscript.
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Barker, E.I., Rabbi, F., Brisbourne, W.A. et al. Genome-wide analysis of the GDSL esterase/lipase family genes in Physcomitrium patens and the involvement of GELP31 in spore germination. Mol Genet Genomics 298, 1155–1172 (2023). https://doi.org/10.1007/s00438-023-02041-1
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DOI: https://doi.org/10.1007/s00438-023-02041-1