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Comprehensive analysis of the INDETERMINATE DOMAIN (IDD) gene family in Marchantia polymorpha brings new insight into evolutionary developmental biology

BMC Genomics volume 26, Article number: 415 (2025) Cite this article

Abstract

Background

SHORTROOT (SHR) and SCARECROW (SCR) are key regulators of plant cell fate. An increasing number of studies have illustrated that the SHR-SCR pathway depends on some INDETERMINATE DOMAIN (IDD) family transcription factors in regulating genes involved in tissue and organ morphogenesis, nutrients transport and metabolism, photoperiodic flowering and stress response. Recent genome sequencing and analysis revealed that only seven IDDs exist in the liverwort Marchantia polymorpha, one of the early diverging extant land plant lineages. However, little is known concerning how the IDDs and the SHR/SCR-IDD pathway work in the ancestral land plants.

Results

In this study, IDD gene family members of this liverwort and other classic model plants were classified into seven branches on the basis of phylogenetic analysis. Gene structure and protein motif analyses suggested that most of the MpIDDs are comparatively evolutionary conserved. Protein structure prediction showed that MpIDDs display similar core domain organization with the IDD proteins from the same branches. Cis-regulatory element prediction demonstrated that MpIDDs might be hormone and stress responsive. The expression levels of most MpIDDs display tissue specificities and could be changed by hormone treatment. All the MpIDDs are located in the nucleus, and most of them have autoactivation activity. Yeast two-hybrid assays confirmed the interactions between MpGRAS8/MpSHR and MpIDD3, MpIDD4 or MpIDD5, as well as MpGRAS3/MpSCR and MpIDD1 or MpIDD2. Taken together, our results provide comprehensive information on IDD gene family in M. polymorpha for further exploring their function in depth, and highlight the importance of the SHR/SCR-IDD pathway in plant development and evolution.

Conclusions

Through bioinformatics analysis and experimental determination of expression patterns, subcellular localization, autoactivation, and protein interaction, this study provided crucial information for a deeper understanding of the functions of MpIDDs in evolutionary developmental studies.

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Introduction

Plant development process is controlled elaborately by transcription factors (TFs). TFs are expressed in specific stages and tissues, and bind to the promoters of downstream genes for transcriptional regulation independently or cooperatively by recruiting other TFs, to determine the destiny of plant tissues and cells thereby. The classic SHORTROOT (SHR)-SCARECROW (SCR) pathway plays pivotal roles in plant development [1,2,3,4,5]. An increasing body of evidence has demonstrated that the INDETERMINATE DOMAIN (IDD) family genes are expressed in a tissue and cell type-specific manner, and regulate plant development through forming complex with SHR-SCR [6,7,8,9,10,11].

SHR and SCR, members of the plant specific GRAS (GIBBERELLIC ACID INSENSITIVE, REPRESSOR OF GA1, and SCARECROW) transcription factor family, are critical for the cell fate determination and cell division/differentiation processes during plant development [1,2,3,4,5]. The expression pattern of SHR and SCR has an intimate relevance to their functions. In Arabidopsis root apical meristem, SCR is expressed in the quiescent center (QC), cortex-endodermis initial/daughter (CEI/CEID) and endodermis; The SHR transcript is made in the stele, but the SHR protein moves outwards to the cell layer where SCR is expressed. After entering the CEI/CEID, SHR activates the transcription of SCR and, along with SCR and other TFs, promote the transcription of cell cycle genes that are required for the periclinal division of CEID to form the endodermis and cortex [6, 9, 10, 12, 13]. The SHR-SCR complex hinders the further movement of SHR from the endodermis by increasing the transcription of SCR, ensuring the formation of a single layer of endodermis in plants. Therefore, SHR and SCR are both critical factors for the determination of the endodermal cell fate [6, 7, 9, 14, 15]. In QC cells, SCR functions upstream of the RETINOBLASTOMA-RELATED gene to control the expression of some cell cycle TFs for QC maintenance [16]. In Arabidopsis leaves, SCR is expressed in the bundle sheath cells, whereas SHR is expressed in the central xylem but the SHR protein moves to the outer bundle sheath cells [4, 17]. Mutations in SHR and SCR result in the loss or enlargement of the bundle sheath cells respectively [4]. Similarly, the transcription of SCR is also restricted in the starch sheath of hypocotyls or inflorescence stems [5, 18], and SHR is mainly transcribed in the vasculature of hypocotyls but the SHR protein moves to the adjacent starch sheath layer [5]. Both genes contribute to the gravitropic response and amyloplast sedimentation in hypocotyls [5, 19].

The IDD family belongs to a plant-specific transcription factor family characterized by the presence of multiple zinc finger motifs [20]. The diverse functions of the IDD family genes in the regulation of growth and development, hormone signaling and metabolic processes in angiosperms have been reviewed by Coelho et al. [21]. A series of researchers have associated the SHR-SCR pathway with IDD family members. Through transcriptional data mining and ChIP-PCR confirmation, two members of IDD family, MAGPIE (MGP) and NUTCRACKER (NUC) have been shown to be the direct targets of SHR and SCR in vivo [6, 7]. JACKDAW (JKD), another member of the IDD family, expresses mainly in the QC, the CEI/CEID and the ground tissue. MGP has similar expression pattern as JKD, but is excluded from the QC. SHR and SCR are both indispensable for the expression of JKD and MGP. Mutation in JKD causes slight reduction in root length and meristem cell number, disorganization of the QC, ectopic periclinal divisions in the cortex, and an increase in cortex and endodermis cell numbers. JKD acts mainly through SHR but not SCR in these processes. However, MGP has an opposite effect on the ground tissue patterning. Yeast two-hybrid and BiFC assays showed that JKD and MGP can interact with the SHR-SCR complex, and that SCR and JKD retain SHR in the nuclei of the QC and endodermis [8]. BALDIBIS (BIB), the closest homolog of JKD, shows a similar expression pattern to that of JKD. After the expression of BIB was knocked down in jkd background, an increase in both cell layers and cell number per layer was seen in the root meristem of the resulting plants. Although there are more cell layers, only one layer in the vicinity of the epidermis possesses endodermal identity. The additional ground tissue layers carry cortex identity. The epidermal cell fate also changes. These reprogrammed cell fates correlate with the ectopic activation of CYCD6 expression in jkd and jkd bib. JKD, BIB and SCR on their own can individually bind SHR, but all together, they exhibit the strongest effect on SHR nuclear retention. The decreased BIB and JKD binding in jkd bib leads to expansion of the SHR protein expression domain [9]. More members of IDD family, NUC, BLUEJAY (BLJ) and IMPERIALEAGLE (IME), have been shown to be expressed in the ground tissue. Together with SCR, most of these ground tissue-specific IDD genes collaboratively maintain the ground tissue identity [10]. In rice, a monocot model plant, OsSHR1, OsSHR2, OsIDD12 and OsIDD13, are all expressed in the vascular tissue of developing leaves [11]. The OsIDD12 and OsIDD13 dimer targets a cis-element in intron 3 of OsPIN-FORMED (PIN) 5c. The interaction of OsSHR1/2 with the OsIDD12/13 dimer mediates OsPIN5c repression. This SHR-IDD-PIN regulatory circuit modulates minor vein formation and ground cell differentiation [11]. In addition to the above evidence from molecular genetics, a crystal structure of SHR-SCR-IDD10 (JKD) ternary complex has been resolved, which provides details concerning this canonical interaction [22].

IDD gene members have been identified in the genomes of Arabidopsis (16), rice (15) and maize (23) [20, 23, 24]. Functional characterization of IDD genes in these angiosperms are laborious and challenging, as some of the idd single mutants displayed no obvious or faint phenotype, and the phenotype was enhanced only when more related IDD members were mutated [9, 25,26,27,28]. With an important phylogenetic position, a low redundancy in regulatory genes and the feasibility of genetic transformation, the liverwort Marchantia polymorpha L. has become a new model plant for evolutionary developmental (evo-devo) studies [29, 30]. The M. polymorpha genome possesses only seven IDD family members, nearly one third of the numbers in model angiosperms [29]. The simple genomic context of M. polymorpha should facilitate the elucidation of the functions of MpIDD genes. Furthermore, in order to adapt to the land, M. polymorpha has acquired a considerable number of new traits and regulatory strategies, which has been gradually refined during the evolution of modern plants. Thus, learning from M. polymorpha could shed light on numerous mechanisms that plants have adopted in the evolutionary courses.

However, to date, the functions of most MpIDD genes have not been well-studied. The basic information concerning MpIDD family genes is still uncharacterized. The interactions between MpIDDs and MpSHR or MpSCR have not been resolved. In the present study, we first undertook a phylogenetic analysis of IDD genes in representative plants from charophyte, liverwort, moss, lycophyte, gymnosperm and angiosperm. The MpIDD gene structures, conserved protein motifs, protein structures and promoter elements were analyzed by bioinformatic tools. Tissue-specific expression and responses to phytohormones of MpIDDs were then investigated by quantitative real-time PCR. The subcellular localization and autoactivation activity of MpIDDs were identified. Using yeast two-hybrid assay, the interactions between MpIDDs and SHR or SCR counterparts in the liverwort were determined. Together, these results provide the foundation for further functional dissection of MpIDDs and help us understand the significance of the SHR/SCR-IDD pathway during the terrestrialization of plants.

Materials and methods

Datasets and sequence retrieval

All the protein amino acid sequences of Klebsormidium nitens, Chara braunii, Anthoceros agrestis, M. polymorpha, M. polymorpha montivagans, Takakia lepidozioides, Physcomitrium patens, Selaginella moellendorffii, Picea abies, Arabidopsis thaliana, Oryza sativa and Zea mays were obtained from http://www.plantmorphogenesis.bio.titech.ac.jp/~algae_genome_project/klebsormidium/kf_download.htm, https://plants.ensembl.org/Chara_braunii/Info/Index, https://www.hornworts.uzh.ch/en/hornwort-genomes.html, https://marchantia.info/, https://www.takakia.com/, Phytozome (https://phytozome-next.jgi.doe.gov/—genomic database versions: Marchantia polymorpha v6.1, Physcomitrium patens v6.1, Selaginella moellendorffii v1.0, Pabies 01, Arabidopsis thaliana TAIR10, Oryza sativa v7.0, and Zea mays RefGen_V4) [31] and PlantTFDB v.4.0 [32], and their previous identifiers were listed in Table S1. The MpIDD 3.0 kb upstream promoter sequences and gene information were acquired from Phytozome. The protein sequences and MpIDDs DNA sequences files in FASTA format were in supplementary materials.

Plant materials and treatments

The plant used in this study was M. polymorpha accession Takaragaike-1 (Tak-1) donated by professor Chizuko Yamamuro from Fujian Agriculture and Forestry University Haixia Institute of Science and Technology. Thalli were cultivated on half-strength Gamborg’s B5 (1/2B5) medium plus 1% sucrose and 1% Agar under 16-h light/8-h dark cycle at 22℃.

For tissue-specific expression analysis, the samples were collected from meristem, gemma cup, gemma, rhizoid and whole sample of the three-week-old Tak-1 plants. For hormone treatments, 10-day-old gemmae grown on 1/2B5 medium were transferred to media containing 5 μM gibberellin (GA3), 100 μM abscisic acid (ABA), 150 μM jasmonic acid methyl ester (MeJA), 1 μM indole-3-acetic acid (IAA), 0.1 mM salicylic acid (SA) or 50 μM 6-benzylaminopurine (6-BA) for 24 h, respectively. After hormone treatment, the whole samples were harvested. All the samples prepared with three biological replicates were frozen in liquid nitrogen immediately and stored in -80 ℃ for RNA isolation.

The IDDs phylogenetic analysis

To determine the evolutionary relationship between IDD proteins from representative plants of different species, two KnIDDs, two CbIDDs, four AaIDDs, seven MpIDDs, 9 MpmIDDs, six TlIDDs, 17 PpIDDs, 11 SmIDDs, 17 PaIDDs, 22 AtIDDs, 28 OsIDDs and 37 ZmIDDs were identified. The ClustalW v2.1 software [33] was used to conduct the multiple sequence alignments with default gap penalties. These sequence alignments were then manually adjusted to minimize insertion/deletion events to improve the reliability of the phylogenetic tree. Then MEGA version 11 [34] was used to construct a neighbor joining tree with the following parameters: No. of differences method, 10% site coverage cutoff, uniform rates among sites and 1000 interior-branch tests. The phylogenetic tree file in Newick format has been provided in the supplementary materials.

MpIDD gene structures analysis and conserved motifs prediction

For MpIDD gene structures and conserved motifs analysis, the IBS version 1.0.3 software [35] was used to visualize genes exon–intron structures including exons, introns, UTRs and gene length. The online MEME suite 5.5.5 program (http://meme-suite.org) [36] was used to identify protein sequences for conserved motifs prediction with the following parameters: the maximum number of motifs, 4; the minimum motif width, 6; the maximum motif width, 50; the minimum sites per motif, 2; the maximum sites per motif, 6; and default parameters. Finally, motifs with low e-value were shown and used for analysis.

Protein 3D structure analysis

The IDD amino acid sequences were used to predict 3D structures for all MpIDDs and related AtIDDs or other IDDs from the same branch. 3D modeling was performed using the AlphaFold Server AlphaFold 3 (https://golgi.sandbox.google.com/) [37]. The result of the 3D structure prediction was visualized by PyMOL 3.1.3.1 [38].

MpIDDs cis-regulatory elements prediction

To predict MpIDDs cis-regulatory elements, putative cis-acting elements in 3.0 kb upstream promoter sequences of MpIDDs were determined using the PlantCARE transcription factor 5.0 database (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) [39]. Finally, the types and numbers of predicted cis-acting elements of the MpIDD genes were visualized by TBtools v2.034 [40].

RNA isolation and quantitative real-time PCR (qRT-PCR)

Total RNA was extracted using the RNAIso plus kit (TaKaRa Bio, Dalian, China). Genomic DNA was removed from total RNA using RNase-free DNaseI (Fermentas, USA). cDNA was obtained by PrimeScriptTM II 1st Strand cDNA Synthesis Kit (TaKaRa, Dalian, China). The expression level of each MpIDDs was monitored on a Biorad CFX Connect Real-Time PCR Detection System (BioRad, SG) using the ChamQ™ Universal SYBR qPCR Master Mix (Vazyme, Nanjing, China). Melting curve analysis showed that all the products generated single peaks. PCR primers were designed using Primer Premier 5.0 software and primer sequences were listed in Table S2. Internal control gene for qRT-PCR was MpEF1α and its primer sequences was listed in Table S2. Each cDNA sample was quantified in technical triplicate and biological triplicate. The relative RNA level of each gene was calculated according to the 2–ΔΔCT method. Finally, the relative expression levels of MpIDDs were visualized by GraphPad Prism version 8.0.2.263 for Windows.

Subcellular localization of MpIDD proteins

The coding sequences of MpIDDs were amplified by PCR and cloned in-frame with the reporter gene GFP driven by 35S promoter. All the PCR primers for cloning were listed in Table S2. After verified by sequencing, the recombinants were transformed into Agrobacterium tumefaciens strain GV3101. The agrobacteria colonies were inoculated into the liquid Luria Broth (LB) and cultured at 28 ℃, 180 rpm for 36 h. The cells were pelleted by centrifugation and then dispersed in AS buffer (10 mM MES, 10 mM MgCl2, 200 μM acetosyringone, pH5.7) to reach OD 0.6–0.8 at 600 nm. The resuspension was injected into the leaves of 4-week-old tobacco. After growing for 48 h at room temperature, the leaf epidermis cells were observed under light or fluorescence using Olympus BX53 compound microscope.

Autoactivation activity analysis of MpIDDs

The coding sequences of MpIDDs were amplified from Tak-1 cDNA by PCR. The products were digested by relevant restriction enzymes and inserted into the pGBKT7 vector. All the PCR primers for cloning were listed in Table S2. The correct recombinants confirmed by sequencing were transformed into yeast strain AH109 and selected on SD:/-Trp medium (Solid medium without tryptophan). The successfully transformed yeast cells were grown on SD:/-Trp,-His medium (Solid medium without tryptophan and histidine) or SD-Trp-His plus X-α-gal media to test the autoactivation activities of MpIDDs.

The GRAS family phylogenetic analysis

To verify the evolutionary relationship of the GRAS family proteins in Arabidopsis and M. polymorpha, the ClustalW v2.1 program [33] was used to initially align GRAS family protein sequences with default gap penalties. These alignments were then adjusted to minimize insertion/deletion events manually. Finally, the MEGA version 11 program [34] was used to conduct the phylogenetic tree using the neighbor-joining method based on the No. of differences model with the following option settings: partial deletion for gaps, uniform rates among sites, 20% site coverage cutoff, 1000 interior-branch test and branches bootstrap values more than 50% were shown.

Yeast two-hybrid assay

Yeast two-hybrid was performed to determine the interactions between MpIDDs and MpGRAS8/MpSHR or MpGRAS3/MpSCR. The coding sequences of MpIDDs were obtained by PCR and purified. The products were cut by restriction enzymes and inserted into the prey vector pGADT7 with the matching ends. The coding sequences of MpGRAS8/MpSHR and MpGRAS3/MpSCR were amplified and cloned into the bait vector pGBKT7 by ligation and In-Fusion Cloning, respectively. All the recombined vectors were verified to be correctly constructed by sequencing. The yeast cells co-transformed by the bait and prey vectors were grown on SD:/-Leu,-Trp medium (Solid medium without leucine and tryptophan) to select the successfully transformed clones containing both vectors. The protein interactions were confirmed by growing cells on SD:/-Leu,-Trp,-His,-Ade (Solid medium without leucine, tryptophan, histidine and adenine) or SD:/-Leu,-Trp,-His,-Ade, plus X-α-gal media. 40 mM of 3-aminotriazole (3-AT) was supplemented to the medium to suppress the autoactivation activities of MpGRAS8/MpSHR and MpGRAS3/MpSCR. All the PCR primers for cloning were listed in Table S2.

Results

The IDD family protein phylogenetic analysis

To explore the evolutionary relationship of IDDs, a phylogenetic tree was constructed with 162 IDD proteins from K. nitens, C. braunii, A. agrestis, M. polymorpha, M. polymorpha montivagans, T. lepidozioides, P. patens, S. moellendorffii, P. abies, A. thaliana, O. sativa and Z. mays, using neighbor-joining method followed by alignments of their full-length protein sequences (Fig. 1). These proteins were separated into seven branches (I, II, III, IV, V, VI and VII). Except for branch II, seven MpIDDs were grouped to the remaining six branches. In charophyte alga K. nitens and C. braunii, the common ancestors of the land plants [41, 42], only two IDD proteins were found respectively, which may be sister to all IDDs in land plants. IDDs in bryophyte groups, one hornwort (A. agrestis), two liverworts (M. polymorpha and M. polymorpha montivagans) and two mosses (T. lepidozioides and P. patens), were in close proximity to each other in most cases. It was as expected that most MpIDDs and MpmIDDs had the closest homology. Branch I had representatives from ten out of twelve chosen species. Thirteen P. patens IDDs with high homology were grouped together in branch I, as a consequence of whole genome duplication in moss [43]. MpIDD3 showed a close relationship with AtIDD3 and AtIDD8 in this branch. Branch II included a large number of IDD members from angiosperms, accounting for 17.3% of the total. We speculate that sequences clustered in branch II might function exclusively in angiosperms. Branch III owned MpIDD7, which showed homology to ZmID1 and OsID1. Branch IV contained nine species. MpIDD2 and the AtIDD14-16 subclade were grouped close to each other in branch IV. MpIDD3, MpIDD7 and MpIDD2 might perform conserved functions as AtIDDs, OsIDDs and ZmIDDs, as they were in the same branch. MpIDD4, MpIDD5 and 33 IDD proteins from other species were grouped in branch V, the functions of these proteins were largely unknown. MpIDD6 and most AtWIPs were the main members in branch VI. WIP domain containing proteins, named after their initial three amino acids, have a highly conserved C-terminal region consisting of four zinc fingers [44]. The WIP lineage could be considered as sister to the IDD lineage concerning the origin of IDD before flowering plants [45]. In branch VII, there were only three PaIDDs and three bryophyte IDDs, indicating that these IDDs might have functions different from those previously characterized in Arabidopsis, rice and maize.

Fig. 1
figure 1

Circular phylogenetic tree showing evolutionary relationships between KnIDD, CbIDD, AaIDD, MpIDD, MpmIDD, TlIDD, PpIDD, SmIDD, PaIDD, AtIDD, OsIDD and ZmIDD proteins. The evolutionary history was inferred by using the neighbor-joining method based on the No. of differences method with the following option settings: 10% site coverage cutoff, uniform rates among sites and 1000 interior-branch tests. The analysis involved 162 amino acid sequences. The IDD family protein sequences were obtained from http://www.plantmorphogenesis.bio.titech.ac.jp/~algae_genome_project/klebsormidium/kf_download.htm, https://plants.ensembl.org/Chara_braunii/Info/Index, https://www.hornworts.uzh.ch/en/hornwort-genomes.html, https://marchantia.info/, https://www.takakia.com/, Phytozome (genomic database versions: Marchantia polymorpha v6.1, Physcomitrium patens v6.1, Selaginella moellendorffii v1.0, Pabies 01, Arabidopsis thaliana TAIR10, Oryza sativa v7.0, and Zea mays RefGen_V4) [31] and PlantTFDB v.4.0 [32], and the ClustalW v2.1 software [33] was used to conduct the multiple IDD protein sequences alignments. The MEGA version 11 [34] was used to perform the evolutionary analyses. The accession numbers for these genes were listed in Supplementary Table S1. Black, incarnadine, grey orange, red, grey blue, light purple, blue, purple, indigo, orange, yellow and green represented IDD genes from K. nitens, C. braunii, A. agrestis, M. polymorpha, M. polymorpha montivagans, T. lepidozioides, P. patens, S. moellendorffii, P. abies, A. thaliana, O. sativa and Z. mays, respectively

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Gene structure and motif composition of MpIDDs

The MpIDDs gene sequences and structures were analyzed. The results showed that MpIDD1, MpIDD4 and MpIDD5 are all single-exon genes of similar length, suggesting that they might have the same evolutionary origin and perform similar functions in M. polymorpha. MpIDD6 has two short exons that might be originated from an insertion event in a long exon. MpIDD7 is constituted by four short exons and its coding sequence is the shortest one. While MpIDD2 and MpIDD3 possess four and three exons, respectively, the total length of their exons is nearly the same, and both encode long proteins in M. polymorpha (Fig. 2A).

Fig. 2
figure 2

Gene structures and conserved motifs in MpIDD gene family. A Gene structures of MpIDD family members were generated by IBS version 1.0.3 software [35]. The black boxes and arrows represented exons, and lines represented introns, while the white boxes and arrows indicated 5’-UTR and 3’-UTR, respectively. B Conserved motifs of MpIDD proteins. The online MEME suite 5.5.5 program (http://meme-suite.org) was used to identify conserved motif sequences. Different colored boxes represented different motifs. Motifs consensus sequences were displayed in Fig. S1

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The IDD family proteins in angiosperms are characterized by the presence of a conserved ID domain, which consists of two C2H2 and two C2HC zinc-finger motifs with DNA-binding ability [20, 46, 47]. We found four types of conserved motifs in MpIDDs, among which only motif 1 is the standard C2H2 zinc finger, while motif 2 and 3 possess Cys/His-rich regions (CH3 in motif 2 and HC2 in motif 3) (Fig. 2B, Fig. S1). It has been reported that the CH3 motif could fold into a zinc finger and bind DNA properly [48]. Motif 4 seems to be an imperfect zinc finger motif with only a single residue of histidine and cysteine (Fig. S1). MpIDD1 to 7 have all four types of motifs (Fig. 2B).

SHR binding motif (RR/KDxxITHxAFCD), which is believed to constitute the interface between SHR and AtIDD10/JKD, is conserved in most Arabidopsis IDD protein members (AtIDD1-13) [22]. In M. polymorpha IDD proteins, only MpIDD3 possesses this motif (RRDSFITHRAFCD, residues 306–318), implying that MpIDD3 has the potential to form a heterodimer with MpSHR.

The 3D protein structure prediction of MpIDDs and related IDDs from other plant species

To gain further insights into the evolutionary relationship and potential functions of IDD proteins, the predicted 3D structures of the MpIDDs and related IDDs from the same branch were compared. The result revealed that these IDD proteins mainly consist of α-helices, β-sheets and random coils (Table 1). The MpIDDs exhibit main domains comprising Zinc Fingers (Fig. 3), in line with the preliminary secondary structure predictions (Table 1). The reliability scores of the core domain predictions were all above 50 (Fig. S2). In branch VII, MpIDD1 and an adjacent MpmIDD protein (MpmSA2 0073s0010.1) shared similar configuration (Fig. 3A). MpIDD2 and AtIDD14-16 were grouped in branch IV (Fig. 1), with the Zinc finger domains of MpIDD2 and AtIDD15 being nearly the same, and all owned a long α-helix at their C-termini (Table 1, Fig. 3B). In branch I, MpIDD3 showed homology to AtIDD3 and AtIDD8 (Fig. 1), and the arrangement of Zinc Finger domains of MpIDD3 and AtIDD3 was quite comparable to each other (Fig. 3C). In branch V, the Zinc Finger domains of MpIDD4 and MpIDD5 and their neighboring MpmIDD protein MpmSA2 0263s0160.1 and MpmSA2 0020s0300.1 had analogous structures (Fig. 3D and E). In branch VI, the Zinc Finger domains of MpIDD6 and AtWIP2 from the same clade almost overlapped (Fig. 3F). The organization of MpIDD7 and ZmID1 in branch III matched each other (Fig. 3G). The similarity residing in these IDD proteins implies that they might have shared functions and common evolutionary origins.

Table 1 The predicted secondary structures of IDD proteins in Fig. 3
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Fig. 3
figure 3

The predicted 3D protein structure models of MpIDD proteins and structure alignment of MpIDDs and other IDDs from the same groups. The first column showed the 3D structures of MpIDDs, the second column showed the 3D structures of related IDD proteins from the same branches, the third column showed the structure alignments of MpIDD and related IDD proteins. In the first and second columns, α-helices, β-sheets and random coils were represented by dark green, yellow and gray respectively, and the gray balls denoted zinc atoms. In the third column, the 3D structures of MpIDDs and related IDDs were denoted as green and red respectively

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Cis-regulatory elements in MpIDDs

To gain insight into the functions of MpIDDs, cis-regulatory elements in their promoter sequences, which were taken as 3.0-kb fragments upstream of the coding regions, were analyzed. The result showed that 29 types of cis-regulatory elements were present (Fig. 4, Table S3), which could be divided into three types: hormone response related elements, development-related elements, and abiotic stress related elements.

Fig. 4
figure 4

Types and locations of predicted cis-regulatory elements of the MpIDD genes. Elements were visualized using TBtools software. 3.0 kb upstream promoter sequences of MpIDD genes were analyzed. Anoxic specific inducibility related element represented by GC-motif. Low-temperature responsive element, Meristem expression related element and Anaerobic induction related element were represented by LTR, CAT-box and ARE, respectively. Gibberellin responsive elements included TATC-box, P-box and GARE-motif. Light responsive element included GT1-motif, TCT-motif, Box 4, AE-box, Sp1, G-Box, I-box, ACE, ATCT-motif, GATA-motif, GATT-motif, TCCC-motif, GTGGC-motif, chs-CMA2a and AAAC-motif. ABA responsive element, Defense and stress responsive element and Salicylic acid responsive element were represented by ABRE, TC-rich repeats and TCA-element, respectively. MeJA responsive element included CGTCA-motif and TGACG-motif. Auxin responsive element included TGA-element and AuxRR-core. The information for all the cis-regulatory elements of the MpIDD genes were listed in Table S3

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GA responsive element, ABA responsive element, MeJA responsive element, auxin responsive element and SA responsive element were classified into hormone response related elements. Four out of seven MpIDD genes own SA responsive element. ABA responsive element, auxin responsive element and MeJA responsive element were distributed in the promoters of all seven MpIDDs, indicating that MpIDDs might be involved in diverse hormone signaling pathways (Fig. 4, Table S3).

Meristem expression related element and light responsive element were grouped into development-related elements. In particular, six out of seven MpIDD genes had meristem expression related elements and each MpIDD possessed at least 11 light responsive elements, implying that MpIDDs in M. polymorpha might participate in photosynthetic processes and mediate meristem morphogenesis (Fig. 4, Table S3).

Anoxic specific inducibility related element, anaerobic induction related element, low-temperature responsive element (LTR), defense and stress responsive element were grouped as abiotic stress related elements. Anoxic specific inducibility related element was distributed in all seven MpIDDs. Four MpIDDs harbored anaerobic induction related element, six MpIDDs had LTR, and four MpIDDs had defense and stress responsive element. These results suggested that MpIDDs might be involved in stress-related biological processes in M. polymorpha (Fig. 4, Table S3).

Tissue-specific expression patterns of MpIDDs

To determine if MpIDDs are involved in vegetative growth in a tissue-specific manner, we examined their expression patterns in different tissues of three-week-old M. polymorpha plants (Fig. 5, Fig. S3). The qRT-PCR results showed that, among the seven MpIDD genes, MpIDD1 had the highest level of expression in the meristem, which suggests that MpIDD1 might influence plant growth processes. MpIDD2 expression was specific to gemma cups, indicating that this gene may play an important role in gemma cup development. MpIDD3 did not show an obvious expression preference in the meristem, gemma cups, gemmae or rhizoids, but displayed a slightly higher level of expression in the whole plant, suggesting the existence of more MpIDD3 transcript in the remaining parts of the thallus. The expression levels of MpIDD5 in rhizoids was extremely high, nearly four times that of the whole sample, revealing that MpIDD5 might be involved in rhizoid development. Contrary to MpIDD5, MpIDD6 had a very low expression in rhizoids; instead, it was highly expressed in gemmae and meristem, showing that MpIDD6 might play a part in gemmae and meristem development. The transcript of MpIDD7 largely accumulated in gemma cups and meristem, implying a possible role of MpIDD7 in gemma cups and meristem development. Compared to other MpIDDs, MpIDD4 had the least degree of tissue-specificity.

Fig. 5
figure 5

The expression level of MpIDD1 to 7 in different tissues of three-week-old M. polymorpha. The bars are means ± standard deviation (SD) from three technical replicates. Three biological replicates and three technical replicates were conducted. All the experiments showed the same expression trend. Only one biological replicate was presented here, the other two replicates were included in Fig. S3. MpEF1α was used as an internal control and the lowest expression level was set to 1. t- tests, * P < 0.05; ** P < 0.01; *** P < 0.001; **** P < 0.0001

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Responses of MpIDDs to phytohormone treatments

Based on the former cis-regulatory elements analysis results, we examined the responsiveness of MpIDDs to hormone treatments through qRT-PCR. Six plant hormones (GA3, ABA, MeJA, IAA, SA and 6-BA) were used (Fig. 6, Fig. S4). The results showed that none of the seven MpIDDs respond to GA3 at a concentration of 5 μM. ABA treatment obviously down-regulated the expression level of MpIDD1, MpIDD2 and MpIDD5. MeJA treatment caused an increase in the transcription level of MpIDD6 and MpIDD7. IAA treatment suppressed the expression of MpIDD1, but enhanced the expression of MpIDD2, MpIDD3, MpIDD6 and MpIDD7. With SA treatment, the transcription level of MpIDD2, MpIDD3 and MpIDD7 was elevated. MpIDD1 and MpIDD7 behaved oppositely in response to 6-BA treatment.

Fig. 6
figure 6

MpIDDs relative expression level under different plant hormone treatments. Transcript levels were determined in whole sample by qRT-PCR under hormones stresses. The bars are means ± standard deviation (SD) from three biological replicates and three technical replicates; Three biological replicates were presented in Fig. S4. t- tests, ** P < 0.01; *** P < 0.001; **** P < 0.0001. MpEF1α was used as an internal control and the expression levels of MpIDDs on 1/2 B5 medium were set to 1

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The subcellular localization and autoactivation activity of MpIDDs

After being translated in cytoplasm, TFs are transported into nucleus to regulate the expression of downstream genes. In order to determine if MpIDDs are TFs, we expressed their fusion proteins with Green Fluorescent Protein (GFP) in tobacco leaves using the CaMV35S promoter and examined their subcellular localization. The transient expressed fluorescence signals reflected the localization of MpIDDs. The signals of all seven MpIDD-GFP fusion proteins were observed mainly in the nucleus (Fig. 7), whereas the signal from the control, CaMV35S-driven GFP, was detected in both the nucleus and cytoplasm (Fig. 7). The nuclear localization of MpIDDs indicates that they might serve as TFs.

Fig. 7
figure 7

Subcellular localization assay of MpIDDs. The transient expression of the 35S:MpIDDs:Green fluorescent protein (GFP) fusing constructs and 35S:GFP construct in Nicotiana tabacum were performed. GFP signals were observed using an Olympus BX53F compound microscope. Scale bar = 100 μm

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TFs bind to the promoters of downstream targets, activating or suppressing transcription. To investigate the transcriptional activity of MpIDDs, the coding sequences of MpIDDs were fused with the GAL4 DNA binding domain in the pGBKT7 vector. The recombinants were then transformed into yeast strain AH109. The growth conditions and the blue color of the colonies on the histidine-deficient plates were monitored to assess the transcriptional activation activity of MpIDDs (Fig. 8). The result showed that all the yeast cells grew normally on the SD:/-Trp plate, suggesting the successful transformation of the recombinants (Fig. 8, the left three columns). The cells carrying pGBKT7-MpIDD1, pGBKT7-MpIDD4 and pGBKT7-MpIDD5 grew well on the SD:/-Trp,-His plate, and displayed dark blue on SD:/-Trp,-His + X-α-gal plate (Fig. 8, the 1st, 4th and 5th rows), but the negative control (pGBKT7) failed to grow on the histidine-deficient plates (Fig. 8, the last row). suggesting the strong autoactivation activity of these three proteins. The cells carrying pGBKT7-MpIDD2 and pGBKT7-MpIDD3 grew moderately on the SD:/-Trp,-His plate, and displayed light blue on SD:/-Trp,-His + X-α-gal plates (Fig. 8, the 2nd and 3rd rows), indicating that these two proteins had weak autoactivation activity. The cells carrying pGBKT7-MpIDD6 and pGBKT7-MpIDD7 did not grow on the histidine-deficient plates (Fig. 8, the 6th and 7th rows), suggesting lack of autoactivation activity in MpIDD6 and MpIDD7.

Fig. 8
figure 8

Autoactivation assay of MpIDDs. The transformed yeast cells were first cultured on SD:/-Trp medium and then selected both on SD:/-Trp,-His and SD:/-Trp,-His + X-α-gal medium. The pGBKT7 vector was used as a negative control

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The interactions between MpIDDs and MpGRAS8/MpSHR or MpGRAS3/MpSCR

To search for the orthologs of AtSHR and AtSCR in M. polymorpha genome, a phylogenetic tree was constructed using the full-length deduced amino acid sequences of GRAS family proteins from Arabidopsis and M. polymorpha (Fig. S5). MpGRAS8 and AtSHR (support value 79) were obviously homologous based on interior-branch test analysis. Although the support value was low, MpGRAS3 was the closest GRAS protein in M. polymorpha to AtSCR (Fig. S5). A phylogenomic analysis from 19 taxa representing the major green lineages also provided evidence that MpGRAS3 with AtSCR, and MpGRAS8 with AtSHR share more homology [49]. The possible reason for the low support value of MpGRAS3 and AtSCR may be due to the distant relationship between the first land plant M. polymorpha and the angiosperm Arabidopsis.

We determined protein–protein interactions between the seven MpIDDs and MpGRAS8/MpSHR or MpGRAS3/MpSCR using yeast two-hybrid assay (Fig. 9). Five MpIDD members could interact with MpGRAS8/MpSHR or MpGRAS3/MpSCR. For MpGRAS8/MpSHR, MpIDD3 appeared to be the strongest interactor, while MpIDD4 and MpIDD5 interacted only weakly. Despite a strong autoactivation activity in the MpGRAS3/MpSCR-BD fusion protein, MpIDD1 and MpIDD2 clearly displayed stronger signals than the negative control. In summary, our results showed that most MpIDDs function together with MpGRAS8/MpSHR or MpGRAS3/MpSCR.

Fig. 9
figure 9

Interactions of MpIDDs with MpGRAS8/MpSHR or MpGRAS3/MpSCR. Yeast cells transformed with different combinations of prey and bait plasmids were grown on the SD:/-Leu,-Trp, SD:/-Leu,-Trp,-His,-Ade as well as SD:/-Leu,-Trp,-His,-Ade + X-α-gal medium

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Discussion

IDD gene family encodes plant-specific TFs that regulate various aspects of plant growth and development. Seven IDD genes are found in the genome of the liverwort M. polymorpha (Fig. 1) [29]. Thus far, only MpIDD6/MpWIP has been reported to have a role in controlling air pore complex formation [50]. The functions of most MpIDDs await being revealed.

According to our phylogenetic tree, all the IDDs from 12 plant species can be divided into seven branches (I-VII, Fig. 1). In branch I, MpIDD3 shows relatively high homology to AtIDD3/MGP and AtIDD8/NUC, which participate in the SHR-SCR regulatory network to regulate ground tissue patterning in Arabidopsis root (Fig. 1) [6,7,8, 10]. We found the SHR binding motif in MpIDD3, and our yeast two-hybrid results suggest that MpGRAS8/MpSHR strongly interacts with MpIDD3 (Fig. 9). However, MpIDD3 does not show tissue specificity in the meristem, gemma cup, gemma or rhizoid, but displays a slightly higher expression level in the thallus (Fig. 5). Therefore, we infer that the MpSHR-MpIDD3 complex might play a part in the development of thallus. Additionally, AtIDD8 links the sugar signaling with photoperiodic flowering [51], and AtIDD3 was previously shown to bind to DELLA and respond to GA, a key determinant of floral transition in angiosperms [52, 53]. Nevertheless, our promoter element analysis failed to identify any GA responsive element in the 3.0 kb promoter of MpIDD3 (Fig. 4, Table S3), and only IAA and SA can elevate the expression level of MpIDD3 (Fig. 6). In our hormone treatment assay, none of the MpIDDs responded to GA3 (Fig. 6). GAs are a variety of tetracyclic diterpenoid compounds produced and sensed by many plants, especially by angiosperms. Sun et al. reported that only ent-kaurenoic acid (KA) and GA12, two intermediates in GA biosynthesis pathway, could be synthesized by M. polymorpha, and many common forms of GAs, GA1, GA3 and GA4, for instance, showed no bioactivity in the liverwort M. polymorpha [54]. For this reason, we could not rule out that the expression level of MpIDD3 might be changed by KA or GA12. Further examination of the MpIDD3 expression pattern and function in sexual organs is required to define the role of MpIDD3 in sexual reproduction.

In branch III, MpIDD7, ZmID1 and OsID1 share high sequence similarities (Fig. 1). ZmID1 and OsID1, mainly expressed in leaves, regulate the expression of flowering-time genes in the transition from vegetative growth to flowering [55,56,57,58,59,60]. Our tissue expression data concerning the vegetative growth phase identified a high expression level of MpIDD7 in gemma-cup and meristem (Fig. 5). From Marpolbase Expression Database (https://mbex.marchantia.info/), we found that the transcription level of MpIDD7 is high in the sexual organs in M. polymorpha. It can be deduced that MpIDD7 has broader expression than its counterparts in rice and maize and may also promote flowering in early land plant through a similar pathway. Besides, the expression of MpIDD7 can be elevated remarkably by MeJA and cytokinin treatments (Fig. 6). Exogenous MeJA treatments can induce genes involved in flower developments in oilseed rape and promote the opening of sorghum florets [61, 62]. Cytokinin promotes flowering in Arabidopsis but suppresses flowering in rice and maize [63, 64]. By mediating crosstalk between MeJA and cytokinin pathways, MpIDD7 might regulate flowering through an ancestral mechanism co-opted by angiosperms.

MpIDD2 belongs to branch IV, which consists of many regulators of auxin signaling in angiosperms. AtIDD14, AtIDD15 and AtIDD16 influence lateral organ morphogenesis and gravitropic responses by directly targeting genes in auxin biosynthesis and transport [25]. OsIDD14/Loose Plant Architecture1 (LPA1) is highly expressed in the lamina joint, internodes, older tiller base and leaf sheath pulvinus, and affects the tiller angle, shoot gravitropism, lamina inclination and resistance to sheath blight disease via manipulating auxin flux [65,66,67]. The repression of the auxin transporter gene OsPIN5c by OsIDD12 and OsIDD13 is responsible for the SHR-mediated minor vein differentiation in rice [11]. In agreement with these, our results showed that MpIDD2 is greatly induced by IAA treatment (Fig. 6). Additionally, MpIDD2 has a gemma-cup specific expression pattern (Fig. 5). Gemma cup is an organ that is periodically produced on the dorsal midrib of the thallus in M. polymorpha, and gives birth to hundreds of gemmae as a means of vegetative reproduction [68]. Most IDDs from Arabidopsis and rice in this branch are concerned with lateral organ morphogenesis, such as branch orientation, tiller angle and lamina inclination [25, 65, 66]. A recent study supported the notion that the mechanisms for gemma cup generation in M. polymorpha and lateral organ formation in angiosperms are conserved [69]. Therefore, there is a high probability that MpIDD2 controls the gemma cup development via an auxin-dependent pathway. Remarkably, the scr mutant lacks endodermis in the inflorescence stem and shows horizontal lateral branches that is agravitropic [19, 70]. We discovered that MpGRAS3/MpSCR has an intense affinity to MpIDD2 (Fig. 9), implying that MpSCR-MpIDD2 complex is likely to be a key element in gemma cup establishment during early land plant evolution. Moreover, the expression level of MpIDD2 is significantly changed by ABA and SA treatment (Fig. 6), suggesting that MpIDD2 might respond to stresses.

MpIDD6/MpWIP is a member of branch VI. The promoter of MpIDD6/MpWIP is active in developing air pores, and its reduced expression causes air pore complex defect [50]. Our result showed that MpIDD6/MpWIP is highly expressed in gemmae and meristem by means of tissue quantitative RT-PCR (Fig. 5), which does not have the resolution to tell if it is expressed in air pores. Further information we have provided is that MpIDD6/MpWIP is up-regulated by IAA or MeJA treatment (Fig. 6). In angiosperms, auxin level is negatively correlated with the number of stomata [71, 72]. JA signaling can trigger stomatal closure through activating K+ channel by a Ca2+ sensor-kinase complex [73], and yet the air pore in the liverwort M. polymorpha cannot open and close as stomata [68]. Hence, it will be interesting to investigate whether auxin and JA signaling have a role in air pore development in the early land plants. Besides, it is noteworthy that, in rice and green millet, the orthologs of AtSHR or AtSCR all mediate stomatal patterning [11, 74,75,76]. Further mechanism study revealed a connection of OsSHRs with OsIDD12/OsIDD13 (the branch IV members) as well as auxin transport [11], which points to the possibility that MpIDD6/MpWIP mediated air pore development maybe auxin-related. Moreover, genetic analysis showed that MpIDD6/MpWIP might act as a transcriptional repressor [50], coinciding with our biochemical results that MpIDD6/MpWIP had no autoactivation activity (Fig. 8).

Although the remaining three MpIDDs are grouped with IDD proteins of unknown functions in the phylogenetic tree (Fig. 1), which gives us no further information, we attempted to interpret the functions of these three genes from other data. The transcript of MpIDD1 is abundant in meristem and downregulated by ABA, IAA or 6BA treatment, and MpIDD1 binds to MpGRAS3/MpSCR (Fig. 5, Fig. 6 and Fig. 9). Auxin and cytokinin act synergistically or antagonistically in shoot apical meristem formation and maintenance in angiosperms [77]. ABA can modulate the cell proliferation in the root meristem in Arabidopsis [78]. To be sure, further experiments are needed to verify the function of the MpSCR-MpIDD1 complex in meristem development in M. polymorpha. Once confirmed, it is proposed to investigate whether auxin, cytokinin or ABA signaling are involved in this process. MpIDD4 and MpIDD5 are also detected as MpGRAS8/MpSHR bound co-regulators, although the interactions are weak (Fig. 9). Unfortunately, no tissue-specificity or hormone treatment responsiveness concerning MpIDD4 could be deduced from our results. MpIDD5 displays an extremely high expression level in rhizoids (Fig. 5), and is repressed by ABA treatment (Fig. 6). It is believed that the rhizoids of bryophytes and root hairs of angiosperms are evolutionary conserved [79]. ROOTHAIR DEFECTIVE SIX-LIKE (RSL) transcription factor positively regulates rhizoids development in the angiosperm Arabidopsis and the bryophytes P. patens and M. polymorpha [80, 81]. ABA negatively controls root hair growth in Arabidopsis through OBF BINDING PROTEIN4 (OBP4)-mediated inhibition of RSL2 [82]. In line with this view, it is worth exploring the function of the MpGRAS8/MpSHR-MpIDD5 complex in rhizoid formation in M. polymorpha and determining whether this process is regulated via a conserved ABA-dependent way.

Conclusions

In conclusion, we have identified the phylogenetic relationship between MpIDDs and IDDs in representative plants from different taxa. The MpIDDs gene structures were analyzed to confirm the conserved gene organization of this family. Protein motif search showed the existence of classic C2H2 and noncanonical zinc fingers in MpIDDs, and protein structure prediction presented the core domain similarity between MpIDDs and related IDDs from the same phylogenetic groups. Tissue-specific expression pattern analysis revealed the MpIDDs enriched in meristem, gemma cup, gemma and rhizoid respectively. Most MpIDDs respond transcriptionally to at least one kind of hormone, in accordance with the presence of multiple cis-regulatory elements in their promoter sequences. All MpIDDs are nuclear localized and most have autoactivity. Results from yeast two-hybrid assays raised the possibility that the MpIDDs also act as co-transcription factors of MpGRAS8/MpSHR or MpGRAS3/MpSCR, resembling the situation in angiosperms. Our results thus provide valuable information for further elucidating MpIDDs gene functions.

Data availability

Data is provided within the manuscript or supplementary information files.

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Acknowledgements

We thank Dr. Chizuko Yamamuro (Fujian Agriculture and Forestry University, China) for providing the Tak-1 material.

Funding

This work was supported by a grant from the Northwest A&F University (K5020223594).

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Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F University, Yangling, Shaanxi, 712100, China

    Congye Zhou, Ting Yang, Manlei Cai, Fei Yu, Huawei Liu & Jing Fu

  2. Department of Biological Science, Florida State University, Tallahassee, FL, 32306, USA

    Hongchang Cui

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Contributions

C.Y.Z., J.F. and M.L.C. conducted the experiments; T.Y. provided technical assistance; H.C.C. edited the manuscript and provided advice; F.Y. supervised C.Y.Z.; H.W.L.supervised M.L.C.; J.F. wrote the manuscript. All authors read and approved the manuscript.

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12864_2025_11609_MOESM7_ESM.pptx

Supplementary Material 7: Fig. S1 The consensus sequences of conserved motifs in MpIDD gene family. Fig. S2 The reliability of the predicted IDD structures. Blue, cyan, yellow and orange represented confidence > 90%, 70-90%, 50-70% and < 50%, respectively. Fig. S3 The expression level of MpIDD1 to 7 in different tissues of three-week-old M. polymorpha. A. The second biological replicate. B. The third biological replicate. Fig. S4 MpIDDs relative expression level under phytohormone treatments. A. The first biological replicate. B. The second biological replicate. C. The third biological replicate. Fig. S5 Phylogenetic tree showing evolutionary relationships of GRAS family proteins in Arabidopsis and M. polymorpha. The evolutionary history was inferred by using the Maximum Likelihood method based on the Poisson correction model [83]. The tree with the highest log likelihood (-29597.43) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying Neighbor-Join and BioNJ algorithms to a matrix of pairwise distances estimated using a JTT model, and then selecting the topology with superior log likelihood value. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 46 amino acid sequences obtained from Phytozome (Marchantia polymorpha v6.1, Arabidopsis thaliana TAIR10) and the accession numbers of GRAS genes were listed in Table S1. All positions with less than 80% site coverage were eliminated. That is, fewer than 20% alignment gaps, missing data, and ambiguous bases were allowed at any position. There was a total of 358 positions in the final dataset. Evolutionary analyses were conducted in MEGA7 [84].

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Zhou, C., Yang, T., Cai, M. et al. Comprehensive analysis of the INDETERMINATE DOMAIN (IDD) gene family in Marchantia polymorpha brings new insight into evolutionary developmental biology. BMC Genomics 26, 415 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12864-025-11609-7

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BMC Genomics

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