Genome-wide identification and expression profiling of SET DOMAIN GROUP family in Dendrobium catenatum

doi:10.21203/rs.2.16026/v1

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Genome-wide identification and expression profiling of SET DOMAIN GROUP family in Dendrobium catenatum

https://doi.org/10.21203/rs.2.16026/v1

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published 28 Jan, 2020

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Background: Dendrobium catenatum used as a precious Chinese herbal medicine is a kind of epiphytic orchid plant which grows on the trunks and cliffs and often faces up to diverse environmental stresses. SET DOMAIN GROUP (SDG) proteins act as histone lysine methyltransferases which are involved in pleiotropic developmental events and stress responses through modifying chromatin structure and regulating gene transcription, but their roles in D. catenatum are unknown.

Results: In this study, we identified 44 SDG proteins from D. catenatum genome. Subsequently, comprehensive analyses related to gene structure, protein domain organization, and phylogenetic relationship were performed to evaluate these D. catenatum SDG (DcSDG) proteins, along with the well-investigated homologs from the model plants Arabidopsis thaliana and Oryza sativa as well as the newly characterized 42 SDG proteins from a closely related orchid plant Phalaenopsis equestris . We showed DcSDG proteins can be grouped into eight distinct classes (I~VII and M), mostly consistent with the previous description. Based on the catalytic substrates of the reported SDG members mainly in Arabidopsis, Class I (E(z)-Like) is predicted to account for the deposition of H3K27me2/3, Class II (Ash-like) for H3K36me, Class III (Trx/ATX-like) for H3K4me2/3, Class M (ATXR3/7) for H3K4me, Class IV (Su(var)-like) for H3K27me1, Class V (Suv-like) for H3K9me, as well as class VI (S-ET) and class VII (RBCMT) for methylation of both histone and non-histone proteins. RNA-seq derived expression profiling showed that DcSDG proteins usually have wide but distinguished expression in different tissues and organs. Finally, environmental stresses examination showed the expression of DcASHR3, DcSUVR3, DcATXR4, DcATXR5b, and DcSDG49 is closely associated with drought-recovery treatment, the expression of DcSUVH5a , DcATXR5a and DcSUVR14a is significantly influenced by low temperature, and even 61% DcSDG genes are in response to heat shock.

Conclusions: This study systematically identifies and classifies SDG genes in orchid plant D. catenatum , indicates their functional divergence during the evolution, and discovers their broad roles in the developmental programs and stress responses. These results provide constructive clues for further functional investigation and epigenetic mechanism dissection of SET-containing proteins in orchid.

Plant Molecular Biology and Genetics

SDG

SET domain

histone lysine methylation

expression profiling

environmental stress

Spatiotemporal expression patterns of a set of genes associated with developmental and environmental stimuli are largely regulated by epigenetic modifications, which mainly consist of DNA methylation, non-coding RNAs, chromatin remodeling and histone modifications [1]. Histone modifications may occur post-translationally on many residues in histone tails and core regions. These modifications mainly include methylation, acylation, phosphorylation, ubiquitination, citrullination, hydroxylation, O-GlcNAcylation and ADP-ribosylation [2, 3], which constitute different combinations, that is, “histone code”, and act in chromatin-templated processes [4, 5]. Among these covalent modifications, histone methylation displays complicated features as it not only occurs on distinct residues (lysine and arginine) and positions, but also involves different numbers (1~3) of methyl groups [6]. Histone lysine modification is catalyzed by histone lysine methyltransferases / SET DOMAIN GROUP (SDG) proteins which commonly possess an evolutionarily conserved SET domain as catalytic module [7], except for H3K79 methyltransferase DOT1, which lacks a SET domain [8]. SDG-catalyzed histone methylation at specific lysine residues can cause similar or opposite effects on gene expression, such as those of H3K4 and H3K36 associated with gene activation, whereas those of H3K9, H3K27, H4K20 associated with gene repression [9].

Based on the sequence homology and phylogenetic reconstruction, plant SDG proteins can be categorized into seven distinct classes: class I, E(z) homologs (H3K27me writer); class II, ASH1 homologs (H3K36me writer); class III, Trx homologs and related proteins (H3K4me writer); class IV, proteins with a SET domain and a PHD domain; class V, Su(var) homologs and relatives (H3K9me writer); class VI, proteins with an interrupted SET domain (S-ET); class VII, RBCMT and other SET related proteins for targeting non-histone proteins [10, 11]. SDG genes have been discovered in bacteria, viruses, and eukaryotes [12, 13]. The presence of SDG genes in bacteria was initially considered a consequence of horizontal gene transfer from eukaryotic hosts [14, 15]. However, investigation on more released genomes of prokaryotic organisms including not only pathogens and symbionts, but also free-living bacteria and archaea suggests that SDG genes have undergone independent evolution in prokaryotes, which is unrelated to the evolution of eukaryotic SDGs, on the other hand, an ancient horizontal gene transfer occurred between bacteria and archaea [13, 16].

SDG family has currently been systematically identified and classified in the genomes of Arabidopsis (49 members) [10, 17], Brassica rapa (49) [11], grapevine (33) [18], populus (59) [19], maize (43) [20], rice (43) [21], tomato (52) [22], sweet orange (47) [23], cotton (52) [24], C4 panicoid model foxtail millet (53) [25], and litchi (48) [26]. However, the SDG family in orchid species, which constitutes an extremely evolutionary branch, remains elusive.

SDG proteins and related histone methylation marks are widely involved in diverse growth and developmental processes, such as seed dormancy, repression of vegetative-to-embryonic reversion, shoot branching, root system architecture, chloroplast development, flowering time, vernalization, floral organ development, ovule and anther development, embryo and endosperm development, plant senescence, carotenoid biosynthesis, and thigmomorphogenesis [27–32]. They are also implicated in the response to biotic and abiotic stresses. SDG8 is required for plant defense against necrotrophic fungal pathogens by regulating a subset of genes within jasmonic acid (JA) and/or ethylene signaling pathway [27] and for basal and R protein-mediated resistance to bacterial pathogens in Arabidopsis [33]. Loss-of-function mutant sdg8 results in enhanced susceptibility to the fungal and bacterial pathogens. ARABIDOPSIS TRITHORAX-LIKE PROTEIN1 (ATX1) as H3K4me3 writer orchestrates expression of defense response genes in antagonistic salicylic acid (SA)/JA signaling pathways by directly activating the expression of the SA/JA signaling mediator WRKY70 gene through establishing H3K4me3 marks on its nucleosomes [34]. In addition, ATX1 is involved in drought stress response, and itsdisruption results in decreased tolerance to dehydration stress in atx1 plants [35]. ATX1 modulates dehydration stress signaling in both abscisic acid (ABA)-dependent and -independent pathways. During ABA-dependent pathway, dehydration stress induces ATX1 binding to NCED3 locus, which encodes the rate-limiting enzyme in ABA biosynthesis. Subsequently the deposition of H3K4me3 mark and recruitment of RNA polymerase II are increased, leading to enhanced NCED3 expression and ABA production [36]. Dehydration stress causes dynamic and specific changes in global histone H3K4me1/2/3 patterns in Arabidopsis,especially H3K4me3 marks with broad distribution profiles on the nucleosomes of stress-induced genes [37]. Similarly, drought stress triggers massive changes in H3K4me3 enrichments on numerous loci (respectively including 3927/910 genes with increased/decreased depositions) in rice seedlings, showing positive correlation with their transcript changes in response to drought stress [38]. However, when Arabidopsis exposed to cold temperatures, H3K27me3 deposition gradually decreases in the chromatins of two cold-responsive genes, COR15A and ATGOLS3 [39].

Dendrobium catenatum (also known as Dendrobium officinale) belongs to the Orchidaceae family, is a rare and precious Chinese medicinal herb. The stem of D. catenatum is the major medicinal part used for relieving upset stomach, promoting body fluid production, and nourishing Yin and antipyresis in traditional remedy and health care [40]. Furthermore, the plant stem contains bioactive extracts with anticancer, hepatoprotective, hypolipidemic, antifatigue, antioxidant, anticonstipation, hypoglycemic, gastric ulcer-protective, and antihypertensive eﬀects, and immunoenhancement, as confirmed by modern pharmacology [41]. However, given its long-time extensive demand and over-exploitation, D. catenatum suffers from near extinction, and was once defined as an endangered medicinal plant in China [42]. In the past 20 years, D. catenatum has been successfully cultivated and became an important economic crop for health care. However, environmental stresses, such as drought, cold, and high temperature, extremely restrict its growth, resulting in heavy yield loss [43]. Hence, it is necessary to screen and identify the candidate genes conferring resistance to differential environmental stresses in D. catenatum molecular breeding.

To obtain a detailed understanding on the SDG family in medicinal orchid plants, we identified SDG members throughout the genome of D. catenatum, and subsequently performed comprehensive assessments on the phylogenetic relationship, gene structure, domain organization, gene expression profiling, and response to environmental stresses. Our results provide insights into the evolution and function of SDG genes in medicinal orchid plants.

Identification of SDG Proteins in the D. catenatum Genome

To obtain all of the members of SDG proteins in D. catenatum, we performed BLASTP search using known Arabidopsisand riceSDG proteins as queries against D. catenatum genome (NCBI accession NO. NW_018281164.1). First, we checked the SDG genes of Arabidopsis and rice in the Superfamily 1.75 database (http://supfam.org/SUPERFAMILY/), we discovered 49 genes in Arabidopsis thaliana, corresponding to those reported in literature [10, 17]. On the other hand, 46 genes were identified in Oryza sativa, three (Os01g65730/OsSET44, Os01g74500/OsSET45, Os06g03676/OsSET46) more than the 43 reported genes [21]. Reciprocal BLAST was carried out to confirm that the hits from D. catenatum and its close relative Phalaenopsis equestris belong to the SDG family. Finally, we obtained 44 SDG genes in D. catenatum (Table 1 and Fig. 1) and 42 in P. equestris (Additional file 1), and they were named after their Arabidopsis homologs.

To characterize and classify the SDG family in D. catenatum, we used SDG proteins in the dicot model plant A. thaliana, the monocot model plant O. sativa, and its close relative P. equestris as references for phylogenetic analysis. The results showed that the 181 SDG proteins from the above four species could be clustered into eight classes (I~VII and M), mostly corresponding to the classification criteria in Arabidopsis [10]. By contrast, ARABIDOPSIS TRITHORAX RELATED 3 (ATXR3) branch was previously classified into Class III [10], but it was separated from the other branches and near ATXR7-like proteins in Class IV in this study (Fig. 1).. Considering their similar substrate specificities, we combined ATXR3 branch and the neighboring ATXR7-like proteins and categorized them under class M, as supported by the further phylogenetic analysis among Classes III, IV, and M (Fig. 4).. Given the high limited reports on Class VI and VII, which feature potential functions for non-histone and histone methylation, we mainly focused on the roles of Classes I~V and M with well-investigated histone methylation specificity in this study.

Class I: E(z)-Like (H3K27me2/3)

Class I contains two E(z) homologs in each of monocot plants D. catenatum, P. equestris and rice, and three well-characterized homologs, namely, CURLY LEAF (CLF), SWINGER (SWN), and MEAEA (MEA), that represent three distinct clades in the dicot plant Arabidopsis (Fig. 2). The genes in this class contain 15~16 introns, which are extremely longer in the two orchid species compared with those of Arabidopsis and rice. This result suggests that overall intron length positively correlated with the corresponding genome size. A similar phenomenon related to intron/exon proportion was also observed in the members of the other classes as will be mentioned later. The three Arabidopsis E(z) proteins act as the catalytic subunits of the evolutionarily conserved Polycomb Repressive Complex 2 (PRC2), which is involved in the deposition of H3K27me3 repressive mark on the target gene locus [44]. CLF (dominant H3K27me3 writer) and SWN act redundantly in vegetative and reproductive development, whereas MEA functions exclusively in suppression of central cell proliferation and endosperm development [45–47]. Rice E(z) homologs SDG711 and SDG718 participate in long-day and short-day signals to mediate the accurate photoperiod control of flowering time, respectively [48]. In addition, SDG711 is involved in the control of inflorescence/panicle meristem activity. Its overexpression enhances inflorescence meristem activity and panicle size, whereas its downregulation shows the opposite effect [49]. Clades I–1 (CLF-like) and I–2 (SWN-like) each contain one ortholog in the examined species, but Clade I–3 (MEA-like) is confined to Arabidopsis. Plant E(z)-like proteins generally harbor highly conserved domain organization at the C-terminal region, which includes a SANT domain, the cysteine rich CXC domain, and the signature SET domain, except for DcCLF and PeSWN, which lack the SANT domain, and DcSWN, which possesses an additional SANT domain at the N-terminus.

Class II: Ash-Like (H3K36me)

Class II can be further divided into five clades, each of which consists of a single member per plant species, except for two members of Clade II–1 in Arabidopsis and D. catenatum (Fig. 3).. Clades II–1 to II–4 exist in all the examined species, but Clade II–5 is only found in rice and contains a single member, SDG707, with unknown function. Class II proteins generally share three conserved domains: an Associated with SET (AWS), SET, and PostSET domains [10, 50].

Clade II–1 (ASHH3-like) members are relatively shorter than their homologs in the four other clades. Arabidopsis ASHH3/SDG7 is required for proper timing in response to vernalization as the sdg7 mutant displays vernalization-hypersensitive phenotype and rapid induction of cold-specific PRC2 component VERNALIZATION INSENSITIVE 3 (VIN3) upon exposure to cold [51]. SDG7 lacks detectable HKMTase activity, although it displays lysine methylation activity in vitro against the plasma membrane aquaporin AtPIP2;1 [52]. By contrast, rice ortholog SDG724/LVP possesses H3K36 methylation activity, and SDG724 depletion results in a global decrease in H3K36me1/2/3 levels. SDG724 contains a predicted nuclear localization signal at the C terminus, whereas SDG7-GFP fusion protein localizes to the cytosol [52, 53]. SDG724 promotes heading date through mediating H3K36me2/3 deposition at the MADS50 and RFT1 loci. The loss of SDG724 leads to a late flowering phenotype [53]. Notably, DcASHH3a/3b in D. catenatum lack AWS domain, different from PeASHH3 from its close relative P. equestris and ASHH3 orthologs in Arabidopsis and rice, and their functional divergence during speciation is interesting to investigate.

Clade II–2 (ASHR3-like) members are characterized by an additional PHD domain near the N-terminus, except for rice SDG736. ASHR3/SDG4 participates in regulating pollen tube growth and stamen development, and its overexpression leads to growth arrest, anther degeneration and male sterility [54, 55]. ASHR3 harbors catalytic activities on H3K36me1 and possible H3K36me2, which is involved in regulating cell division competence in the root meristem and quiescent center [56].

Clade II–3 (ASHH1-like) members display uniform protein length and highly conserved AWS-SET-PostSET domain combination at the N-terminus. Arabidopsis ASHH1/SDG26 localized in the nucleus can methylate oligonucleosomes in vitro, and ASHH1/SDG26 knockout leads to a late-flowering phenotype through decreased H3K4me3 and H3K36me3 level at the SOC1 locus [57, 58]. Similarly, the knockdown of riceortholog SDG708 causes a late-flowering phenotype under both long-day and short-day conditions due to the down-regulation of the key flowering genes Hd3a, RFT1, and Ehd1 and a genome-wide decrease in H3K36me1/2/3 levels during early growth stages [59]. Predictably, D. catenatum DcASHH1 harbors a similar function.

Clade II–4 (ASHH2-like) proteins are considerably longer than the others, and characterized by an additional CW domain near to the N-terminal triple domain combination. In Arabidopsis, ASHH2/SDG8, as the major H3K36 methyltransferase, specifically accounts for the di- and tri-methylation of H3K36 [58, 60]. SDG8 targets are enriched in a set of light- and/or carbon-responsive genes involved in specific biological processes, such as defense response, nutrient metabolism, photosynthesis, and energy production [61]. SDG8 deletion leads to pleiotropic phenotypes, including small organ size [62], increased shoot branching [31], early flowering [62, 63], defective ovule and anther development [64], altered carotenoid composition [29, 65], reduced pathogen resistance [27, 33], and perturbed touch response [30]. Consistently, the knockdown of rice ortholog SDG725 causes wide-ranging defects, including dwarfism, shortened internodes, erect leaves and small seeds [32]. In the aspect of protein architecture, ASHH2 ortholog in D. catenatum or P. equestris is more similar to Arabidopsis SDG8 than rice SDG725.

Class III: Trx/ATX-Like (H3K4me2/3)

Class III consists of five members, which can be further divided into three clades in each examined plant species (Fig. 4). Class III proteins characterized tandem PHD domains in the middle region and SET–PostSET domain combination at the N-terminus. Moreover, several clades contain additional distinct domains, such as PWWP domain specific to Clade III–1/2, and FYRN–FYRC domain combination specific to Clade III–1.

Clade III–1 (ATX1-like) contains two members in Arabidopsis, and one in each of the three other species. In Arabidopsis, ATX1 and ATX2 paralogs exhibit similar domain architectures and occasionally share partially redundant function [66]. However, in most cases, both exhibit distinct expression patterns and influence the expressions of largely nonoverlapping gene sets [67]. For the shared targets, ATX1 and ATX2 account for the deposition of H3K4me3 and H3K4me2 marks, respectively [67]. Notably, atx1 mutant displays a pleiotropic phenotype, whereas atx2 mutant is wildtype-like [67, 68]. Different from Arabidopsis atx1 with early-flowering phenotype [67], rice ortholog mutant ostrx1/sdg723 exhibits late-flowering through decreased H3K4me3 levels at the central flowering time integrator Ehd1. OsTRX1 can rescue Arabidopsis atx1 phenotype [69–71], suggesting that ATX1-like proteins demonstrate conserved biochemical and molecular functions during evolution. However, ATX1-like proteins produce specific phenotypes in distinct species due to the differences in developmental context. Thus, DcATX1 and PeATX1 in orchid may play important roles in flowering time control.

Clade III–2 (ATX3-like) includes three members in each tested species. Arabidopsis ATX3/4/5 are clustered together and separated from the monocot orthologs. The orthologs from D. catenatum, and P. equestris are consistently clustered together, concordant with their close relationship. In Arabidopsis, ATX3/4/5 exhibit a common evolutionary origin, identical domain structure, and similar expression patterns. They also function redundantly in genome-wide H3K4me2 and H3K4me3 profiles. Furthermore, atx3 atx4 atx5 triple mutant with dwarfism and reduced fertility displays exaggerated phenotypes when combined with the atx2 mutant but not with atx1 [72]. In rice, ATX3-like proteins SDG721 and SDG705 function redundantly in modulating H3K4 methylation levels. The loss of both genes results in semi-dwarfism, shortened panicle branching and, reduced cell length due to decreased transcription levels and H3K4me3 deposition associated with gibberellin biosynthetic and signaling genes [73]. Considering the dwarf phenotype of ATX3-like mutants in Arabidopsis and rice, the homologs in D. catenatum and P. equestris might be involved in regulating plant architecture.

Clade III–3 shows specificity toward the examined monocots and contains one copy per species. D. catenatum DcATX3d and P. equestris PeATX3d are characterized by an additional Jas domain at the C-terminus, in contrast with the rice ortholog OsSET37/SDG732. Further survey of this clade will be helpful for understanding the evolution of SDG family in monocots.

Class M: ATXR3/7 (H3K4me)

Class M comprises of two clades, namely, Clade M–1 (ATXR7-like) and M–2 (ATXR3-like). Each clade contains one copy per plant species (Fig. 4). ATXR7-like proteins usually lack extra domains, except for PeATXR7 with a C-terminal GYF domain. Arabidopsis ATXR7/SDG25 acts as the writer of H3K4 monomethylation (H3K4me1), and the sdg25 null mutant displays significantly reduced global levels of H3K4me1 and early flowering phenotype due to the deactivation of FLOWERING LOCUS C (FLC) expression [60, 74]. ATXR3-like proteins also contain only one copy in each species, are characterized by the presence of DUF4339 domain in the middle region, except for OsSET27/SDG701. Arabidopsis ATXR3/SDG2 is the major H3K4me3 writer, whose depletion leads to reduced H3K4me3 deposition at a global level and pleiotropic defects in both sporophyte and gametophyte development [28, 75, 76]. D. catenatum DcATXR3 and P. equestris PeATXR3 feature a more similar protein architecture to Arabidopsis ATXR3/SDG2 than rice SDG701. This finding suggests that ATXR3-like proteins in orchid may retain their ancestral role, whereas rice ortholog may functionally diverge, as attributed to the loss of specific domain and partial sequence.

Class IV: Su(var)-like (H3K27me1)

Class IV can be divided into two clades, Clade IV-I (ATXR5-like) and IV-II (ATXR6-like), which encode shorter proteins characteristic of an N-terminal PHD domain in addition to the defined SET domain, except for PeATXR5 (Fig. 4). In Arabidopsis, ATXR5 and ATXR6 manifesting H3K27 monomethyltransferase activity show largely overlapping functions. The depletion of both results in global H3K27me1 reduction, heterochromatin decondensation, and over-replication of heterochromatin [77, 78]. ATXR5/6 are proposed to be recruited to the replication fork during S phase through interaction with PROLIFERATING CELL NUCLEAR ANTIGEN (PCNA), in which they specifically add H3K27me1 to the newly incorporated histone variant H3.1 required for mitotic inheritance of this heterochromatic mark and the protection of H3.3-enriched genes against heterochromatization during DNA replication [79]. In addition, a key RNA metabolism component Serrate (SE) promotes ATXR5/6-mediated H3K27me1 mark to repress the expression of transposable element [80]. The overexpression of either ATXR5 or ATXR6 causes male sterility [81]. ATXR5 and ATXR6 probably perform separate roles because of ATXR5 with a dual localization in plastids and nucleus but ATXR6 solely in nucleus [81].

Class V: Suv-Like (H3K9me)

Class V contains 15 members in Arabidopsis, 14 in rice and D. catenatum, and 13 in P. equestris; These members can be further divided into two subclasses, SUVH and SUVR, which include Clades V–1 to V–3 and V–4 to V–6, respectively (Fig. 5). Class V proteins are usually characterized by PreSET–SET–PostSET or PreSET–SET domain combinations. SUVH proteins often contain another symbolic SET- and RING-ASSOCIATED (SRA) domain, whereas SUVR proteins in Clades V–4 and V–5 often include another WIYLD domain and tandem ZnF_C2H2 domains, respectively. SUVH genes usually lack introns, except for the members of SUVH4 branch and two members (PeSUVH45 and SDG727) of SUVH5 branch, whereas SUVR genes contain variable number of introns. In general, Class V members are responsible for methylation of histone H3 lysine 9 (H3K9me), in which H3K9 dimethylation (H3K9me2) is the critical mark for gene silencing and DNA methylation, and are involved in heterochromatin formation and reprogramming of gene expression [82].

SUVH subclass

In Clade V–1, the five members SUVH1/3/7/8/10 in Arabidopsis cluster together, and are distinct from the five homologs in rice and each of the two homologs in D. catenatum or P. equestris. This result indicates that duplication of these clade members occurred after divergence between dicots and monocots. However, the two orthologs in either D. catenatum or P. equestris respectively pair together, indicating that their gene duplication occurred before the split of Dendrobium and Phalaenopsis. Arabidopsis SUVH1/SDG32 performs a distinct anti-silencing function to promote the expression of genes targeted by DNA methylation but fails to alter DNA methylation levels. The knockout of SUVH1/SDG32 causes no effect on H3K9me2 levels but reduces H3K4me3 levels [83]. Furthermore, chromatin immunoprecipitation-based sequencing (ChIP-Seq) showed that SUVH1 binds to highly methylated genomic loci targeted by RNA-directed DNA methylation (RdDM) at the whole-genome level. SUVH1 and its paralog SUVH3 function partially redundantly and interact with three DNAJ domain-containing homologs (SDJ1/2/3) to form the SUVH–SDJ complex, which is required for the transcriptional activation of promoter methylated genes and plant viability [84]. However, SDG728, asone of SUVH1 homologs in rice, retains its classical function to mediate H3K9 methylation and participate in retrotransposon repression. Its knockdown leads to decreased H3K9 methylation and altered seed morphology, whereas its overexpression leads to increased H3K9 methylation [85]. D. catenatum and P. equestris include two SUVH1-like proteins, far less than the five members in Arabidopsis and rice. Thus, the function of SUVH1 homologs and the evolutionary mechanisms in orchids require further investigation.

Clade V–2 comprises two members for each examined species, and these members lack PostSET domains, in contrast with those in clade V–1. In Arabidopsis, SUVH2 and SUVH9 as sister paralogs show overlapping functions in RdDM and heterochromatic gene silencing in spite of some developmental specialization [86, 87]. SUVH2 displays a central role in heterochromatic gene silencing with strong dosage effects [88]. Its knockout results in a significant reduction in heterochromatin-specific histone methylation marks (H3K9me1/2, H3K27me3, and H4K20me1) and DNA hypomethylation at the chromocenter heterochromatin. SUVH2 overexpression leads to ectopic heterochromatization accompanied with significant developmental defects, such as extreme dwarfism and curly cotyledon [86, 88]. SUVH2 and SUVH9 may feature inactive histone methyltransferase activity [89, 90]. However, the simultaneous absences of SUVH2 and SUVH9 lead to a marked decrease in H3K9me2 levels in the RdDM loci [87, 91]. SUVH2 and SUVH9 can bind to methylated DNA through their SRA domains and facilitate the recruitment of Pol V to RdDM loci via association with the chromatin-remodeling DDR complex and MORC complex [89, 91]. Considering the highly similar domain organization among SUVH2-like proteins in these examined species, their function should be evolutionarily conserved.

Clade V–3 proteins could be further divided into two branches (SUVH4 and SUVH5). SUVH4 branch possesses one member in each species, whereas SUVH5 branch contains two members in Arabidopsis and rice, and three members in D. catenatum or P. equestris. In Arabidopsis, SUVH4/KRYPTONITE (KYP), SUVH5, and SUVH6 as H3K9 methyltransferases are required to maintain DNA methylation, and act genetically downstream of H3K9 methylation. Furthermore, together with H3K9 methylation, these genes constitute a self-reinforcing feedback loop [92–97]. SUVH4/KYP as the predominant H3K9 methyltransferase can mono-, and di- but not tri-methylate H3K9, and its mutation leads to a nearly complete loss of H3K9me2, slight reduction in H3K9me1, loss of DNA methylation and reduced gene silencing [82]. The suvh4 suvh5 suvh6 triple mutant displays strong phenotype and loses both H3K9me1 and H3K9me2 at target loci [94]. SUVH4/KYP controls seed dormancy, and its knockout and overexpression cause increased and decreased dormancy, respectively [98]. SUVH5 and SUVH6 as sister paralogs in SUVH5 branch also exhibit HKMTase activities with locus-specific features. SUVH4, together with SUVH5 or SUVH6, controls Ta3 and Mu1 transposons and PAI1–PAI4 transcribed inverted repeat locus, respectively [82, 93, 94]. SUVH4, SUVH5 and SUVH6 can bind 5-methyl-cytosine (5mC) in CG, CHH, and CHG sequence contexts via their SRA domains, where SUVH4 shows a preference for CHG methylation over the other two sequences, SUVH6 prefers both CHG and CHH methylation, whereas SUVH5 shows similar binding activity in all contexts [97, 99]. In rice, SUVH4-like protein SDG714 mediates H3K9 methylation, participating in DNA methylation, transposition of transposable elements, and genome stability [100]. SDG714 Knockdown causes reduced CG and CNG methylation as well as H3K9 methylation at the copia-like retrotransposon Tos17 locus, resulting in a mostly glabrous phenotype lacking macro trichomes in glumes, leaves, and culms [100]. In addition, SDG714 and SUVH5-like proteins SDG727 and SDG710 exhibit antagonistic functions with the histone H3K9 demethylase JMJ706. The knockdown of these genes could partially complement the jmj706 phenotype and reduced H3K9 methylation [85]. Notably, PeSUVH4 protein in P. equestris is evidently short and lack SRA and PostSET domains, compared with SUVH4-like proteinsin the three other species. The divergence of SUVH4 between orchid genus Dendrobium and phalaenopsis is worthy of investigation.

SUVR subclass

In Clade V–4, there are 3 members in Arabidopsis and P. equestris, 1 in rice, and 4 inD. catenatum, respectively. In Arabidopsis, SUVR2 mediates transcriptional silencing in both RdDM-dependent and -independent manners. SUVR2–SUVR1 tight complex in association with SNF2-related chromatin-remodeling factors CHR19, CHR27, and CHR28 contributes to the silencing function of SUVR2 [101]. SUVR4 participates in the epigenetic defense mechanism by introducing H3K9me3 marks to repress potentially harmful transposon activity [102]. SUVR4 specifically converts H3K9me1 into H3K9me3 at transposons and pseudogenes within the euchromatin; SUVR4 binds to ubiquitin by its N-terminal WIYLD domain, facilitating its conversion from a strict di-methylase into a di-/tri-methylase in vitro [102, 103]. SUVR1 and SUVR2 can also interact with ubiquitin via their WIYLD domains [103], but show no detected histone methyltransferase activity in vitro [101, 104]. This finding indicates that SUVR1/2 function in transcriptional silencing is independent of ubiquitin binding and histone methyltransferase activity. In this study, D. catenatum DcSUVR4, P. equestris PeSUVR4, and rice SDG712 were grouped together with Arabidopsis SUVR4 but not with SUVR1/2, implying that they possess ubiquitin binding and HKMTase activity, except for PeSUVR4, which includes an obviously short sequence and lacks WIYLD and PreSET domains.

Clade V–5 contains one member in each tested species, and characterized by an additional tandem ZnF_C2H2 domain, except for SDG706. In Arabidopsis, SUVR5 lacks the SRA domain but recognizes specific DNA sequences through its zinc finger motifs and establishes the heterochromatic state through H3K9me2 deposition in a DNA methylation-independent manner [105]. The knockout of SUVR5 leads to delayed flowering, and no further enhanced phenotype occurs in the quintuple suvr1 suvr2 suvr3 suvr4 suvr5 mutants [105, 106]. This finding suggests that SUVR5 is a dominant developmental regulator in SUVR subclass.

Clade V–6members exist in one copy in each species, and their encoding proteins are notably shorter than those of the other clades in this class. Arabidopsis SUVR3 contains an additional AWS domain close to the SET–PostSET domain combination, and DcSUVR3 contains an intact PreSET–SET–PostSET domain combination. However, SUVR3 orthologs in rice and in P. equestris only contain a PreSET domain, suggesting that the genes in Clade V–6 may undergo less selective pressures and become increasingly divergent during evolution. The functions of the genes in this clade remain uncharacterized thus far.

Tissue and organ expression profiles of DcSDG genes

To investigate the potential roles of DcSDGs during growth and development in D. catenatum, we detected the expression profiles of DcSDGs by reanalyzing the RNA-seq data from different plant tissues and organs, including leaf, root, green root tip, white part of root, stem, flower bud, sepal, labellum (lip), pollinia, and gynostemium (column) [107].

On the basis of hierarchical clustering (Fig. 6 and Additional file 2), the expression patterns of DcSDGs could be divided into two groups, G1 and G2. G1 genes usually feature low expressions in most tissues and organs. However, several genes are highly expressed in specific tissues and organs, such as DcATX3d in flower bud, DcASHR3 in root and flower bud, and DcATXR5a, DcSUVH5a, and DcATX3a in pollinia. G2 genes display diverse expression profiles in diﬀerent tissues and organs. The majority of G2 group genes are highly expressed in most of the detected tissues and organs, whereas several show intermediate expression in most tissues and organs, such as DcASHH3a, DcASHH1, DcSUVH5b, and DcSDG47. Furthermore, ~86% of genes (38/44) present intermediate and high expressions in flower buds, compared with ~77% (34) in root and gynostemium, ~57% (25) in leaf, ~45% (20) in stem, ~43% (19) in pollinia, ~55% (24) in sepal, and ~64% (28) in labellum. These findings suggest that DcSDG family plays essential roles in flower bud formation. Notably, DcSDG51 in leaf, DcSUVH2b in pollinia, and DcSUVH1a in root and stem display the most distinguished expressions, indicating their prominent functions in specific tissues.

The expression profiles of six duplicated DcSDG gene pairs were further compared (Additional file 3). In general, one copy showed higher expression levels than the others in all tissues, except for DcSUVH5a/5b pairs, suggesting that one paralog might performed a dominant function during plant growth and development. DcASHH3a/3b, DcATX3b/3c, DcATXR5a/5b and DcSUVR14b/14c exhibited similar expression patterns, whereas DcSUVH5a/5b pairs displayed differential expression profiles in the detected tissues and organs. These results indicate that distinct duplicated gene pairs might undergo different evolutionary pressures and diverge at varying periods.

Expression levels of DcSDGs in response to environmental stresses

D. catenatum is an epiphytic orchid plant that grows on trunks and cliffs and often experiences diverse environmental stresses, such as drought, cold, and high temperature. To detect the responses of DcSDG genes to drought stress, the expression profiles of DcSDGs were assessed by analyzing the RNA-seq data from the leaves under different drought treatments [108] (Fig. 7a and Additional file 4). In brief, the seedlings were irrigated on the 1st day, and no water was provided from the 2nd day to the 7th day, and recovered on the 8th day. Leaves were sampled at both 06:30 and 18:30 on the 2nd (DR5 and DR8), 7th (DR6 and DR10), and 9th (DR7 and DR15) days, respectively, and at 18:30 on the 8th day (DR11). The results showed that one-week of drought stress notably repressed the expressions of DcCLF, DcASHR3, DcSUVR3, and DcSUVR14c, but obviously induced the expression of DcATXR5b, DcATXR4, and DcSDG49 when sampling at both dawn and dusk. Subsequently, rewatering restored the expression levels of DcASHR3, DcSUVR3, DcATXR5b, DcATXR4, and DcSDG49.

To explore the possible roles of SDG proteins inresponse to cold stress, we evaluated the expression levels of DcSDGs through analyzing the raw RNA-seq reads from the leaves of D. catenatum seedlings treated at 20 ℃ (control) and 0 ℃ for 20 h, respectively [43] (Fig. 8a and Additional file 5). Data showed that 32% of DcSDG genes (14) showed transcription change in response to cold stress. For example, genes with upregulated expression consisted of DcASHH1 (II), DcATX3b (III), DcSUVH4 (V), DcSUVH5a (V), DcSUVH5b (V), DcSDG45 (VII), and DcSDG51 (VII), whereas genes with deregulated expressions included DcATXR5a (IV), DcATXR5b (IV), DcSUVR14a (V), DcASHR1 (VI), DcASHR2 (VI), DcATXR2 (VI), and DcSDG50 (VII). The expression levels of DcSUVH5a, DcATXR5a, DcASHR2 and DcSUVR14a (fold change >2 or <0.5) are significantly influenced by cold.

To further understand the roles of the DcSDG proteins in response to high temperature (35℃) stress, the expression profiles of SDG genes in the leaves of D. catenatum seedlings were examined by quantitative reverse-transcription–polymerase chain reaction (RT-qPCR) (Fig. 8). The results show the diverse expression patterns of DcSDG genes during heat shock treatment. At 3 h after treatment (HAT), the number of upregulated genes (10) was slightly higher than that of downregulated genes (7). At 6 HAT, more DcSDG genes were induced (15 upregulated genes versus 10 downregulated genes). At 12 HAT, the number of upregulated genes (27) was evidently higher than that of downregulated genes (3). Of the genes examined upon exposure to heat shock, three Class II genes (DcASHH3a/3b, DcATX3a), five Class V genes (DcSUVH2a/2b, DcSUR14b/14c, DcSUVR3), two Class VI genes (DcATXR1 and DcASHR1), two Class VII genes (DcSDG45/48), and one Class M gene DcATXR3 were distinguished from the corresponding control in at least at one time point (P<0.05, Fig. 8).

Characterization and classification of SDG proteins in D. catenatum

Over the last 20 years, SDG proteins in diverse plants, especially in the model plant Arabidopsis have been fully characterized [10]. A considerable amount of SDG proteins has been functionally investigated, providing the valuable reference information for precise protein classification at the genome-wide level. D. catenatum shows extensive application value in China and can be used in the food service industry, pharmaceutical, cosmetics, health products, and ornamental horticulture. The recent successful genome sequencing of D. catenatum associated with its unique developmental and living features promoted its use as a model orchid plant with great theoretical relevance [109]. In this study, 44 SDG proteins in D. catenatum was screened and identified from its genome sequence. Through the comprehensive evaluation of the sequence features, phylogenetic relationships, and substrate specificities based on previous classification criteria and published experimental data, this study divided the SDG proteins into eight classes: Class-I (H3K27me2/3), Class-II (H3K36), Class-III (H3K4me2/3), Class-M (H3K4me), Class-IV (H3K27me1), Class-V (H3K9me), Class-VI/S-ET (undefined), Class-VII/ RBCMT (non-histone Rubisco).

To date, the understanding of Class VI and VII is highly limited. Class VI includes six clades (Additional file 6), whose members feature a long S-ET domain interrupted by a Zf-MYND domain and have not been functionally characterized in plants. In mammalian ASHR1 homologs, SET And MYND Domain Containing 3 (SMYD3) may methylate histones H3K4 and H4K5, whereas SMYD2 can dimethylate H3K36 and repress gene transcription [110–112]. SMYD proteins also possess non-histone substrates, such as SMYD2 for p53 and estrogen receptor α and SMYD3 for VEGFR1 and MAP3K2, in the nucleus and cytoplasm [113–116]. Class VII consists of nine clades (Additional file 7), whose members are characterized by an additional Rubisco substrate-binding (Rubis-subs-bind) domain and conserved in plants and animals. In flowering plants, chloroplast-localized Rubisco large subunit N-methyltransferase (LSMT) performs the conserved and ancient functions to methylate the Rubisco small subunit and fructose–1,6-bisphosphate aldolase (FBA). Moreover, this enzyme evolved an extra novel role to catalyze the K14 trimethylation of Rubisco large subunit in Fabaceae, Cucurbitaceae, and Rosaceae [117, 118]. Based on the strict correlation between the presence of the His-Ala/Pro-Trp triad motif and the Rubisco methylation status [117], LSMTs in D. catenatum and the other three examined species only retained the ancestral function due to absence of this triad motif. In addition, pTAC14 associated with thylakoid is required for proper chloroplast development [119]. In animal, Class VII homolog SETD3 with additional Rubis-subs-bind domain exhibits a H3K36 methyltransferase activity [120]. Therefore, the members of Class VI and VII in plants may be involved in the methylation of both histone and non-histone proteins; such assumption is beyond the previous expectation.

Evolution and function divergence of SDG proteins

Gene duplication, as a critical driving force, provides extra copy of genetic material to tolerate random mutations to survive the natural selection and create new species during evolution. Gene duplication, including tandem duplication and polyploidy (whole genome duplication, WGD), considerably contributes to the formation of gene families [24], such as the SDG family containing 44 members in D. catenatum. D. catenatum has undergone at least four rounds of WGD events, including two ancient WGDs before (ζ) and after (ε) the angiosperm split from gymnosperm, a τ WGD shared by most monocots and a recent WGD specific to the Orchidaceae lineage [107, 121]. Duplicate genes usually undergo three evolutionary fates, nonfunctionalization with silencing function, neofunctionalization with novel function, and subfunctionalization with partial function [122]. D. catenatum contains six pairs of duplicated DcSDG genes. In DcSUVH2a/2b pairs, DcSUVH2a was unexpressed in all examined tissues, implying that neofunctionalization might have occurred. DcASHH3a/3b, DcATX3b/3c, DcATXR5a/5b and DcSUVR14b/14c pairs displayed similar expression patterns, indicating that they might have experienced subfunctionalization. DcSUVH5a/5b pairs exhibited differential expression profiles in the different tissues and organs, indicating that novel expression specificity and function have developed.

Involvement of SDG proteins in plant development programs and environmental stress responses

SDG proteins associated with the corresponding histone methylations can output precise developmental instructions through diverse mechanisms. (1) Different SDG proteins show similar catalytic specificity, but act on distinct sets of genes. As the writers of H3K4 methylation, ATX3/4/5 have different targets from ATXR3/SDG2 [72]. (2) Several SDG members act as the core subunits in specific conserved complexes. Class I E(z) homologs (CLF, SWN and MEA), together with p55-like protein MSI1; ESC-like protein FIE; and Su(z)12-like proteins FIS2, EMF2 and VRN2 constitute different PRC2 complexes, functioning in distinct developmental phases [123]. (3) Specific SDG proteins can interplay with other types of epigenetic regulators. SUVH4/5/6 interacts with the histone deacetylase HDA6 to silence a subset of transposons through histone H3K9 methylation and H3 deacetylation [124]. (4) Some SDG proteins can crosstalk with phytohormone signaling. Arabidopsis SDG8 and rice ortholog SDG725 mediate the deposition of H3K36me2/3 marks, and are involved in brassinosteroid (BR)-regulated gene expression through interacting with BR signal component BES1 and binding to BR biosynthesis or signaling genes D11, BRI1, and BU1 [32, 125]. Further in-depth molecular dissection of SDG members in D. catenatum with specific developmental and living modes will enrich the action mechanisms of the SDG gene family.

Histone methylation established by SDG proteins are widely involved in responses to environmental stresses and pathogen challenges [27, 33, 35–38]. Studies have reported that drought stress can cause global changes of histone H3K4 methylation patterns in Arabidopsis and rice [37, 38]. Class III member ATX1 is implicated in drought stress response via both ABA-dependent and -independent pathways in Arabidopsis [35, 36]. Here we observed that the dynamic expression changes of DcASHR3 (Class II), DcSUVR3 (V), DcATXR5b (V), DcATXR4 (VI), and DcSDG49 (VII) were closely associated with water-drought-rewater treatment, indicating that methylations of H3K36 and H3K9 are also involved in drought response. H3K36me3 and H3K27me3 have been proven to play antagonistic roles in the cold-induced epigenetic switch at the Arabidopsis FLC locus [126]. In D. catenatum, we identified six significant cold-responsive DcSDG genes, including DcASHH1 with putative H3K36 activity (Class II), DcATX3b/3d with putative H3K4 activity (Class III), DcATXR5a/5b with putative H3K27 activity (Class M), DcSUVH5a/5b and DcSUVR14a/3 with putative H3K9 activity (Class V) (Fig. 8). The results indicate diverse histone methylation marks with specific DcSDG proteins that perform certain roles during cold treatment. It will be intriguing to further investigate their direct targets by high throughput ChIP-seq method combined with excellent commercial antibodies against various histone methylation marks. Recently, Huang et al. [24] thoroughly identified cotton SDG genes and noted that the expressions of most of these genes decreased under high-temperature conditions. In this study, we observed 61% of DcSDG genes are in response to heat shock, but the number of upregulated genes was considerably higher than that of downregulated ones. This finding may be related to the particularly epiphytic lifestyle and crassulacean acid metabolism pathway in D. catenatum.

In this study, we identified 44 SDG proteins in D. catenatum and 42 in its close relative P. equestris, and replenished three other SDG members (Os01g65730/OsSET44, Os01g74500/OsSET45, and Os06g03676/OsSET46) into the previous rice SDG gene family (43 members). On the basis of the phylogenetic relationship and substrate specificity, these genes were divided into eight classes by using well-characterized Arabidopsis SDG members as references. In addition, we analyzed the expression profiles of D. catenatum SDG genes in different tissues and organs and their responses to diverse environmental stresses. Our findings provide comprehensive information on the classification and expression profiles on D. catenatum SDG genes, and will lay the foundation for the functional characterization of the SDG gene family in orchids.

Identification of SDG gene family in D. catenatum and P. equestris

All the SDG sequences including genomic DNAs, CDS and proteins in Oryza sativa and Arabidopsis thaliana were retrieved from Phytozome database (http://phytozome.jgi.doe.gov/pz/portal.html). Of these, the protein sequences were used as queries to search homologs of D. catenatum and P. equestris against NCBI database using BLASTp tool. All the hits were further confirmed by the existence of the signature SET domain detected using on-line biosofts PROSITE (http://prosite.expasy.org/), SMART (http:// smart.embl-heidelberg.de/) and PFam (http://pfam.xfam.org/search).

Analysis of gene structure, domain architecture and phylogenetic relationship

The gene structure including the intron-exon distribution pattern was reconstructed by Gene Structure Display Server GSDS 2.0 (http://gsds.cbi.pku.edu.cn/) [127]. The domain organization was analyzed using SMART and Pfam databases. Phylogenetic analysis was performed using MEGA7 [128]. The full-length amino acid sequences of J-proteins were used for constructing neighbor-joining (NJ) trees with the following settings: pairwise deletion option for gaps/missing data treatment; p-distance method for Substitution model; and bootstrap test of 1000 replicates for evaluation of internal branch reliability.

In silico expression profiling of DcSDG genes

For the tissue and organ expression profiling of DcSDG genes, The raw RNA-seq data of leaf (SRR4431601), root (SRX2938667), Green root tip (SRR4431599), white part of root (SRR4431598), stem (SRR4431600), flower bud (SRR4431603), sepal (SRR4431597), labellum (SRR4431602), pollinia (SRR5722145) and gynostemium (SRR4431596) in an individual of wild D. catenatum were downloaded from the NCBI Sequence Read Archive (SRA) provided by Zhang et al [107]. For drought stress and stress removal experiment in 8-month-old D. catenatum plants [108], irrigation was performed on the 1^st day, omitted from the 2^nd to the 7^th day, and resumed on the 8^th day, watering every two days at 15:30. Consequently, the raw RNA-seq reads were obtained from the leaves that were harvested at both 06:30 and 18:30 on the 2^nd [DR5 (NCBI: SRR7223299) and DR8 (SRR7223300)], 7^th [DR6 (SRR7223298) and DR10 (SRR7223296)], and 9^th [DR7 (SRR7223301) and DR15 (SRR7223297)] days, respectively, and at 18:30 on the 8^th day [DR11 (SRR7223295)]. For the expression analysis of DcSDG genes in response to cold stress, the raw RNA-seq reads of leaves under 20 °C control condition (SRR3210630, SRR3210635 and SRR3210636) and 0°C cold treatment for 20 h (SRR3210613, SRR3210621 and SRR3210626) were obtained from NCBI provided by Wu et al [43]. Reads of all the samples were aligned to the NCBI Dendrobium reference genome using HISAT package [129] The mapped reads of each sample were assembled using StringTie [130]. Then, all transcriptomes from Samples were merged to reconstruct a comprehensive transcriptome using perl scripts. After the ﬁnal transcriptome was generated, StringTie and edgeR was used to estimate the expression levels of all transcripts. StringTie was used to perform expression level for mRNAs by calculating FPKM. DcSDG genes were selected and differentially expressed genes were defined with log2 (fold change) >1 or <–1 and with statistical significance (p value < 0.05) by R package. Heatmap was generated using TIGR MultiExperiment Viewer (MeV4.9) software [131].

Plant material and heat shock treatment

D. catenatum cultivar “Jingpin 1” (Breed NO. Zhe R-SV-DO–015–2014, Zhejiang Province, China) constructed by professor Jin-Ping Si as our lab PI was used in this study. D. catenatum was grown in greenhouse at 20 °C under a 12h light/12h dark regime. 1-year-old seedlings were treated at 35 ℃ heat shock for indicated time (3h, 6h and 12h) in a temperature-controlled incubator, compared with the mock plants at 20 ℃. Then the leaves were harvested, snap frozen in liquid nitrogen and stored at –70 ℃ for further expression analysis.

Real-Time quantitative RT-PCR (RT-qPCR)

Total RNA was extracted from the leaves using TRIzol reagent (Invitrogen, USA) followed by RNase-free DNase I treatment. First strand cDNA synthesis was performed via PrimerScript RT Enzyme Mix I kit (TaKaRa, Japan), according to the manufacturer’s instructions. RT-qPCR reaction mixture (10 μl) was prepared according to the manual of SYBR^®Premix Ex Taq^TM II (Tli RNaseH Plus) kit (TaKaRa, Japan). Then the reaction was carried out on CFX96 Touch™ Real-Time PCR Detection System (BIO-RAD, USA) in three technical replicates for each biological triplicate using the primers listed in Additional file 8. The reaction condition was set as the following temperature profile: 94 ℃ for 3 m, 40 cycles of 94 °C for 20s, 60 ℃ for 20s, 72℃ for 20s. The constitutive DcACTIN was used as the reference gene. The expression value of each gene tested was normalized with the internal reference gene, and the relative expression level was calculated with 2^-ΔΔCT method [132].

ABA: abscisic acid; ATX1: ARABIDOPSIS TRITHORAX-LIKE PROTEIN1; ATXR3: ARABIDOPSIS TRITHORAX RELATED 3; BR: Brassinosteroid; ChIP-Seq: Chromatin immunoprecipitation-based sequencing; CLF: CURLY LEAF; E(Z): zeste; FBA: Fructose–1,6-bisphosphate aldolase; FLC: FLOWERING LOCUS C; HKMTase: Histone lysine methyltransferase; JA: Jasmonic acid; KYP: KRYPTONITE; MEA: MEAEA; NJ: Neighbor-joining; PRC2: Polycomb Repressive Complex 2; RBCMT: Ribulose–1,5-bisphosphate carboxylase/oxygenase (Rubisco) methyltransferase; RdDM: RNA-directed DNA methylation; RT-qPCR: Real-time quantitative polymerase chain reaction; Rubis-subs-bind: Rubisco substrate-binding; SA: salicylic acid; SDG: SET DOMAIN GROUP; SET: Su(var), E(z), and Trithorax; SRA: SET- and RING-ASSOCIATED; SMYD3: SET And MYND Domain Containing 3; Su(var): Suppressor of variegation; SWN: SWINGER; Trx: Trithorax; VIN3: VERNALIZATION INSENSITIVE 3; WGD: Whole genome duplication

Ethics approval and consent to participate

The D. catenatum used in this study is a commercial cultivar “Jingpin 1”, which was cultivated by Prof Jinping Si (Zhejiang A&F University), was authorized by Zhejiang Province with Breed NO. Zhe R-SV-DO–015–2014. It does not require ethical approval.

Consent to publish

Not applicable.

Availability of data and materials

All data generated or analyzed during this study are included in this published article and its Additional files. The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

This work was funded by National Key R&D Program of China (2017YFC1702201) focusing on wild imitation cultivation and stress response mechanisms of Dendrobium, National Natural Science Foundation of China (31870310) focusing on epigenetic mechanism of Dendrobium epiphytic lifestyle, Scientific R&D Foundation for Talent Start-up Project of Zhejiang A&F University (2017FR035) focusing on the functional dissection of histone methylation in Dendrobium, and the State Key Laboratory of Subtropical Silviculture (ZY20180206) focusing on metabolic mechanism of environmental fitness in Dendrobium.

Authors’ contributions

DHC and JPS planned and designed the research. HLQ performed the experiments. DHC, HLQ, YH and LZ analyzed the data. DHC and JPS wrote the article. All of the authors approved the manuscript.

Acknowledgements

We thank the manuscript editing provided by the professional editing company EnPapers (http://www.enpapers.com/).

Authors’ Information

¹State Key Laboratory of Subtropical Silviculture, SFGA Engineering Research Center for Dendrobium catenatum (D. officinale),, Zhejiang A&F University, Lin’an, Hangzhou, Zhejiang 311300, China, ²Key Laboratory of Education Department of Hunan Province on Plant Genetics and Molecular Biology, Hunan Agricultural University, Changsha 410128, China

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Table 1 Classification of SDG genes in D. catenatum.
No.	Name	Gene ID	Clade	exon number	Protein (aa)	Isoform
1	DcCLF	LOC110113338	I	16	918	2
2	DcSWN	LOC110098601	I	17	895	0
3	DcASHH1	LOC110107485	II	10	498	0
4	DcASHH2	LOC110097541	II	18	1,992	0
5	DcASHH3a	LOC110095009	II	9	377	0
6	DcASHH3b	LOC110105604	II	9	235	0
7	DcASHR3	LOC110103080	II	11	487	1
8	DcATX1	LOC110096723	III	25	1,081	0
9	DcATX3a	LOC110094707	III	22	980	0
10	DcATX3b	LOC110093543	III	24	1,060	0
11	DcATX3c	LOC110116505	III	26	942	4
12	DcATX3d	LOC110100284	III	19	2,038	0
13	DcATXR3	LOC110093028	M	21	2,360	0
14	DcATXR7	LOC110110427	M	24	1,304	6
15	DcATXR5a	LOC110100023	IV	7	413	3
16	DcATXR5b	LOC110102586	IV	8	373	3
17	DcATXR6	LOC110107042	IV	4	268	0
18	DcSUVH1a	LOC110091884	V	3	682	0
19	DcSUVH1b	LOC110100064	V	3	680	1
20	DcSUVH2a	LOC110104355	V	3	664	1
21	DcSUVH2b	LOC110111597	V	2	640	0
22	DcSUVH4	LOC110103468	V	20	752	4
23	DcSUVH45	LOC110096224	V	2	765	1
24	DcSUVH5a	LOC110109813	V	2	1,048	1
25	DcSUVH5b	LOC110101480	V	2	1,099	0
26	DcSUVR14a	LOC110104063	V	13	783	8
27	DcSUVR14b	LOC110097487	V	9	668	0
28	DcSUVR14c	LOC110097357	V	8	785	0
29	DcSUVR3	LOC110096832	V	2	337	0
30	DcSUVR4	LOC110109382	V	13	723	8
31	DcSUVR5	LOC110092659	V	14	1,658	2
32	DcASHR1	LOC110098638	VI	14	496	0
33	DcASHR2	LOC110112079	VI	3	385	2
34	DcATXR1	LOC110097453	VI	1	521	0
35	DcATXR2	LOC110107001	VI	15	494	0
36	DcATXR4	LOC110103199	VI	8	339	0
37	DcSDG42	LOC110104315	VI	14	765	4
38	DcSDG45	LOC110107875	VII	6	490	0
39	DcSDG46	LOC110111739	VII	6	494	1
40	DcSDG47	LOC110091896	VII	11	556	2
41	DcSDG48	LOC110099042	VII	12	499	0
42	DcSDG49	LOC110092290	VII	16	476	5
43	DcSDG50	LOC110113229	VII	8	482	2
44	DcSDG51	LOC110094849	VII	13	503	0

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Genome-wide identification and expression profiling of SET DOMAIN GROUP family in Dendrobium catenatum

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Journal Publication

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Abstract

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Background

Results

Identification of SDG Proteins in the D. catenatum Genome

Class I: E(z)-Like (H3K27me2/3)

Class II: Ash-Like (H3K36me)

Class III: Trx/ATX-Like (H3K4me2/3)

Class M: ATXR3/7 (H3K4me)

Class IV: Su(var)-like (H3K27me1)

Class V: Suv-Like (H3K9me)

SUVH subclass

SUVR subclass

Tissue and organ expression profiles of DcSDG genes

Expression levels of DcSDGs in response to environmental stresses

Discussion

Characterization and classification of SDG proteins in D. catenatum

Evolution and function divergence of SDG proteins

Involvement of SDG proteins in plant development programs and environmental stress responses

Conclusion

Methods

Identification of SDG gene family in D. catenatum and P. equestris

Analysis of gene structure, domain architecture and phylogenetic relationship

In silico expression profiling of DcSDG genes

Plant material and heat shock treatment

Real-Time quantitative RT-PCR (RT-qPCR)

Abbreviations

Declarations

Ethics approval and consent to participate

Consent to publish

Availability of data and materials

Competing interests

Funding

Authors’ contributions

Acknowledgements

Authors’ Information

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