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Molecular Evidence for Origin, Diversification and Ancient www.nature.com/scientificreports OPEN Molecular evidence for origin, diversifcation and ancient gene duplication of plant subtilases Received: 22 January 2019 Accepted: 9 August 2019 (SBTs) Published: xx xx xxxx Yan Xu1,2,3, Sibo Wang2,4,5, Linzhou Li2,6, Sunil Kumar Sahu 2,4, Morten Petersen5, Xin Liu 2,4, Michael Melkonian7, Gengyun Zhang2,4 & Huan Liu 2,4,5 Plant subtilases (SBTs) are a widely distributed family of serine proteases which participates in plant developmental processes and immune responses. Although SBTs are divided into seven subgroups in plants, their origin and evolution, particularly in green algae remain elusive. Here, we present a comprehensive large-scale evolutionary analysis of all subtilases. The plant subtilases SBT1-5 were found to be monophyletic, nested within a larger radiation of bacteria suggesting that they originated from bacteria by a single horizontal gene transfer (HGT) event. A group of bacterial subtilases comprising representatives from four phyla was identifed as a sister group to SBT1-5. The phylogenetic analyses, based on evaluation of novel streptophyte algal genomes, suggested that the recipient of the HGT of bacterial subtilases was the common ancestor of Coleochaetophyceae, Zygnematophyceae and embryophytes. Following the HGT, the subtilase gene duplicated in the common ancestor and the two genes diversifed into SBT2 and SBT1, 3–5 respectively. Comparative structural analysis of homology-modeled SBT2 proteins also showed their conservation from bacteria to embryophytes. Our study provides the frst molecular evidence about the evolution of plant subtilases via HGT followed by a frst gene duplication in the common ancestor of Coleochaetophyceae, Zygnematophyceae, and embryophytes, and subsequent expansion in embryophytes. Serine proteases are a highly abundant and functionally diverse class of proteins which occupy a notable place in plants1,2. According to the MEROPS peptidase database, the clan SB is one of 13 clans of serine proteases that are widely distributed in Archaea, Bacteria, and eukaryotes2–4. Clan SB contains two families, family S8 (ofen called the subtilase family) and family S53 (the sedolisin family)4. Te catalytic mechanisms of the two families of clan SB are diferent. In family S8 the active site residues form a catalytic triad in the order Asp, His, Ser, whereas fam- ily S53 contains a catalytic tetrad in the order Glu, Asp, Asp, Ser. Family S8 is the second largest family of serine proteases and is divided into two subfamilies, S8A (type example subtilisin) and S8B (type example kexin)5. Plant subtilisin-like proteases (also known as plant subtilases, SBTs) belong to subfamiliy S8A. Te frst subtilase cloned from plants was cucumisin from melon fruit6. In the past 20 years, several SBT gene families have been revealed throughout the plant kingdom, in Vitis vinifera7,8, Arabidopsis thaliana9, Oryza sativa10, Solanum lycopersicum11,12, Solanum tuberosum13, and others. Te Arabidopsis proteome alone comprises 56 subtilases. Based on these fndings SBTs have been divided into six subgroups9, and recently one of the sub- groups (SBT6.1) was described as a seventh subgroup (SBT7)14. Schaller et al. have summarized most of the functions of plant subtilases, such as in embryogenesis, seed devel- opment and germination, cuticle formation and epidermal patterning, vascular development, programmed cell 1BGI Education Center, University of Chinese Academy of Sciences, Shenzhen, 518083, China. 2BGI-Shenzhen, Beishan Industrial Zone, Yantian District, Shenzhen, 518083, China. 3China National GeneBank, Institute of New Agricultural Resources, BGI-Shenzhen, Jinsha Road, Shenzhen, 518120, China. 4State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen, 518083, China. 5Department of Biology, University of Copenhagen, Copenhagen, Denmark. 6School of Biology and Biological Engineering, South China University of Technology, Guangzhou, 510006, China. 7Botanical Institute, Cologne Biocenter, University of Cologne, Cologne, D-50674, Germany. Yan Xu, Sibo Wang and Linzhou Li contributed equally. Correspondence and requests for materials should be addressed to H.L. (email: [email protected]) SCIENTIFIC REPORTS | (2019) 9:12485 | https://doi.org/10.1038/s41598-019-48664-6 1 www.nature.com/scientificreports/ www.nature.com/scientificreports a. b. Embryophyta Alveolata Streptophyte algae Euglenozoa Chlorophyta Stramenopiles Glaucophyta Amoebozoa Rhodophyta Fungi Bacteria Archaea Chloroflexi Chloroflexi Firmicutes 100 Bacterial S8A genes 100 Caldiserica (S8 cluster 1) SBT1-5 97 Caldiserica 98 Coprothermobacterota 84 Actinobacteria Chloroflexi Chloroflexi 98 Gamma-proteobacteria 83 75 S8 cluster 1 86 100 Delta-proteobacteria Delta-proteobacteria Bacterial Subtilases 79 100 Actinobacteria 69 100 Chloroflexi Actinobacteria Actinobacteria 40 83 100 Bacterial Subtilases S8 cluster 2 100 100 Gamma-proteobacteria 98 59 Proteinase K 97 Chloroflexi 99 Beta-proteobacteria/Gamma-proteobacteria Beta-proteobacteria/Gamma-proteobacteria KP43 proteinase 93 100 Gamma-proteobacteria 70 Beta-proteobacteria 88 100 Firmicutes 83 Actinobacteria 56 57 SBT7 97 Chloroflexi 95 68 Actinobacteria Mesotaenium endlicherianum S8 cluster 4 99 Streptophyte algae Coleochaete scutata HGT 100 92 Streptophyte algae 100 “Spirotaenia sp.” Plant Subtilases 100 Streptophyte algae (SBT2) 73 Tree scale: 1 Embryophyta SBT6 100 S8 cluster 3 Figure 1. Phylogenetic relationship of the S8A protease gene subfamily. (a) Maximum likelihood unrooted phylogenetic tree of the S8A subfamily from representative Archaea, Bacteria and eukaryote species was constructed with IQ-TREE (model: LG + R10, predicted by Modelfnder) using an ultrafast bootstrap approximation (100,000 bootstrap replicates). Colored domains display eight diferent clusters in the S8A subfamily. Te domains with a continuous line indicate resolved clusters, while domains with dotted lines represent undefned clusters. Te colored circles at the top lef represent the species composition of individual clusters. Te plant subtilases (SBT1-5) apparently originated from bacterial subtilases (red branches in in paraphyletic divergences) through a single HGT. (b) Phylogenetic analysis of plant subtilases using an extended taxon sampling of bacterial subtilases to search for a bacterial sister group to the plant subtilases was constructed by Maximum Likelihood using 500 bootstrap replicates (model: WAG + F + R7, predicted by Modelfnder). Plant subtilases are monophyletic with a clade of bacterial sequences derived from four phyla (Proteobacteria (only Gammaproteobacteria and Betaproteobacteria), Chlorofexi, Actinobacteria and Firmicutes). Te streptophyte algal sequences from Mesotaenium endlicherianum, Coleochaete scutata and “Spirotaenia sp.” diverge paraphyletically from the common ancestor of the plant subtilases with “Spirotaenia sp.” in sister position to embryophytes (the detailed tree with all taxon and species names is shown as Supplementary Fig. S1). Some bacterial S8 genes from the phylogenetic tree of the S8 cluster 1 (a) were selected as an outgroup. death, organ abscission, and plant responses to their biotic and abiotic environments15–17. However, many specifc functions and physiological substrates of SBTs still need to be explored. Previous studies have found that land plant subtilases were derived from a single HGT (horizontal gene transfer) event18. Horizontal gene transfer is proposed relative to vertical gene transfer, which breaks down the boundaries of kinship and complicates the pos- sibility of gene fow. Many genes found in algae doesn’t have any homologs in higher plants were suggesting their possible bacterial origin. For instance, two alginate-specifc enzymes, MC5E and GDP-mannose dehydrogenase show high similarity with the bacterial genes, indicating that these genes might have undergone a non-canonical evolutionary history. Taylor and Qiu (2017) investigated the evolutionary history of plant subtilases through a phylogenetic analysis using 2,460 subtilase amino acid sequences of 341 species, and identifed 11 new gene lin- eages14. Meanwhile, the presence of plant subtilases in streptophyte algae, the grade of green algae most closely related to land plants (embryophytes), was also frst reported in their study, based on analysis of transcriptomes14. Plant subtilases seem to have experienced several gene duplications, which were accompanied by functional diversifcation7. Due to their multiple duplications and complex evolutionary history, it is important to explore the origin and diversifcation of SBTs among Viridiplantae including the streptophyte algae. We have recently sequenced the genomes of several streptophyte algal species (unpublished data) enabling us to explore the evo- lution of subtilases including all major lineages of streptophyte algae. We reconstructed the phylogeny of all S8A subtilases existing in archaea, bacteria, and eukaryotes. Ten we focused on the origin and evolution of plant subtilases (SBTs). Here we show that plant subtilases originated from bacteria by HGT into streptophyte algae followed by a gene duplication event in the common ancestor of Coleochaetophyceae, Zygnematophyceae and embryophytes. Our study provides new information about the origin and early diversifcation of plant subtilases and thus contributes to a better understanding of the phylogeny of the S8A protease family. Results Classifcation of the S8A gene family and putative origins of plant-type subtilases. To explore the phylogenetic relationship
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