YABBY family is a plant specific transcription factor family, which is involved in the establishment of plant tissue dorsoventral polarity (Siegfried et al., 1999; Bonaccorso et al., 2012; Yang et al., 2019), differentiation of late lateral organ (Siegfried et al., 1999; Toriba et al., 2007; Bonaccorso et al., 2012), development of leaf and leaf derived organ (Hirano 2004; Bonaccorso et al., 2012; Shamimuzzaman and Vodkin 2013; Yang et al., 2019), plant morphogenesis (Strable et al., 2017), flower formation (Strable and Vollbrecht, 2019; Yang et al., 2019), male sterility and fertility restoration (Zhang and Zhang, 2014), fruit development (Cong et al., 2008; Han et al., 2015; Filyushin et al., 2017; Zhang et al., 2019), biosynthesis of secondary metabolites (Bonaccorso et al., 2012; Boter et al., 2015; Wang et al., 2016; Kayani et al., 2019), plant biotic and abiotic stress (Zhao et al., 2017; Yang et al., 2018; Li et al., 2019). So far, the research on YABBY family has been thoroughly studied in Arabidopsis thaliana (Sawa et al., 1999; Siegfried et al., 1999), Oryza sativa (Liu et al., 2007; Toriba et al., 2007), Vitis vinifera (Zhang et al., 2019), Gossypium spp (Yang et al., 2018), etc. Six members of YABBY gene family were identified in Arabidopsis genome and were divided into five subfamilies: CRC, INO, FIL/YAB3, YAB2 and YAB5. Among them, CRC and INO subfamily genes are expressed in reproductive organs such as pericardium cells and ovules, which are called flower-specific YABBY genes. FIL/YAB3, YAB2 and YAB5 subfamily genes are expressed in cotyledons, leaves and floral organs, so they are called vegetative growth YABBY genes (Sawa et al., 1999; Siegfried et al., 1999). A total of 17 YABBY genes were identified in soybean genome. Overexpression of GmYABBY10 in Arabidopsis thaliana showed that stress treatment could inhibit seed germination, root length and root surface area of transgenic plants, suggesting that GmYABBY10 may be a negatively regulator in plant resistances to drought and salt stresses (Zhao et al., 2017). Yang et al. (2019) identified a GmFILa transcription factor from soybean, which belongs to the FIL subfamily. mRNA hybridization analysis showed that the transcription factor was specifically expressed in leaf and flower bud primordium. Overexpression of this gene in Arabidopsis thaliana resulted in changes in dorsoventral polarity of epidermal leaves, prolonged flowering and inhibited apical meristem development (Yang et al., 2019). 12, 12 and 23 YABBY genes were identified in Gossypium arboreum, Gossypium raimondii and Gossypium hirsutum, respectively. Sequence analysis showed that all cotton YABBY genes contained N-terminal C2C2 type zinc finger domain and a C-terminal YABBY domain. Gene expression analysis showed that YABBY gene plays an important role in ovule development and biotic stress (Yang et al., 2018). Seven YABBY genes were identified in grape and divided into five subfamilies. Tissue structure analysis showed that the YABBY gene family was involved in multiple physiological processes in plants. Analysis of expression during ovule development in 4 cultivars showed that one gene, VvYABBY4, was preferentially expressed during the period of ovule abortion in seedless cultivars. Transgenic expression of VvYABBY4 in tomato conferred reduced plant stature, dark green leaves, elongated pistil, and reduced size of fruit and seeds (Zhang et al., 2019). Nine YABBY genes were identified in tomato. This gene family plays an important role in regulating the shape and size of fruit (Han et al., 2015). In addition, studies have shown that YABBYs are involved in plant secondary metabolism biosynthesis (Boter et al., 2015; Kayani et al., 2019). For example, Arabidopsis FIL regulates anthocyanin biosynthesis (Boter et al., 2015). AaYABBY5 in Artemisia annua regulates gene expression by enhancing the promoter activity of CYP71AV1 and DBR2, and then positively regulates artemisinin biosynthesis (Kayani et al., 2019). YABBY5 from spearmint (Mentha spicata) negatively regulates the synthesis of monoterpenes and terpenes (Wang et al., 2016). YABBYs have dual functions in regulating the synthesis of secondary metabolites. It can be used as an activator of secondary metabolites and an inhibitor of secondary metabolites. Their specific functions depend on their interacting target complexes (Bonaccorso et al., 2012).

Pomegranate fruit as a very important functional food, is rich in flavonoids, ellagitannins and other phenolic compounds, with effects of anti-inflammatory, anti-atherosclerosis, anti-diabetic, anti-breast cancer, anti-prostate cancer, anti-colon cancer and so on (Johanningsmeier and Harris, 2011; Qin et al., 2017). Pomegranate fruit development, biosynthesis of secondary metabolites and pomegranate grain development have been the focus of current research (Luo et al., 2018; Xia et al., 2019). However, there are few reports on the regulation of pomegranate YABBY gene family on growth and development, fruit development and biosynthesis of secondary metabolites in pomegranate. In this study, bioinformatics analysis of pomegranate YABBY is to be carried out based on the genome data of pomegranate, and to provide a theoretical basis for further clarifying the function of YABBY.

1 Results and Analysis

1.1 Identification of YABBY gene family and analysis of physicochemical properties in Punica granatum L.

In this study, Perl script was used to extract YABBY family sequences from pomegranate genome database. The Pfam database, Batch Web CD-Search Tool and SMART online software were used for sequence analysis, and 6 sequences with YABBY conserved domains were obtained by synthesizing the three database structures. The YABBY gene family of Punica granatum L. was named according to its homology with YABBY gene of A. thaliana (Table 1), and the ExPASy online tool was used to analyze its physicochemical properties. The results showed that the amino acid length of pomegranate YABBY gene family ranged from 123 aa (PgCRC) to 224 aa (PgFILa), the molecular weight of the protein was 13.38 kD (PgCRC)~24.74 KD (PgFILa). Its isoelectric point (pI) ranged from 8.58 to 9.06. All pI of PgYABBYs gene family is greater than 8, indicating that PgYABBYs protein is alkaline. The instability coefficient of PgYABBYs protein ranged from 40.04 to 62.61, the aliphatic amino acid index ranged from 60.98 to 76.65, the GRAVY value ranged from-0.313 to-0.678, which was less than 0, indicating that PgYABBY proteins were hydrophilic proteins.

Figure 1 New ICT based fertility management model in private dairy farm India as well as abroad

1.2 Phylogenetic analysis of pomegranate YABBY gene family

Based on the phylogenetic tree analysis, we could know the phylogenetic relationship between YABBY gene family in Punica granatum L. and dicotyledonous plants (Arabidopsis thaliana, Glycine max, Solanum lycopersicum and Vitis vinifera), monocotyledonous plants (Oryza sativa, Ananas comosus and Zea mays). A phylogenetic tree was constructed for 74 YABBY protein sequences from Arabidopsis thaliana, Glycine max, Solanum lycopersicum, Vitis vinifera, Oryza sativa, Ananas comosus and Zea mays (Figure 1). The results showed that the 6 pomegranate YABBYs were divided into five subfamilies of YAB2, CRC, YAB5, FIL/YAB3 and INO together with YABBY of other species. The six PgYABBYs were divided into five subfamilies. Except FIL/YAB3 subfamily contained PgFILa and PgFILb, the other subfamilies only contained one PgYABBY. Among these five subfamilies, FIL/YAB3 is the largest family, which has a total of 25 members. There are more YABBY genes in maize, rice and soybean, with the number of 6, 5 and 4, respectively, and two genes in other species. The second largest subfamily is YAB2, which is composed of 20 genes. There are four genes of the subfamily in maize, soybean and pineapple, two genes in rice, tomato and grape, and one gene in Arabidopsis and pomegranate. YAB5 subfamily is the smallest, which is unique to dicotyledon plants. Except for two YABBY genes in soybean and tomato, there is one YABBY gene in other dicotyledon plants. To further understand the phylogenetic relationship of PgYABBY, the phylogenetic tree (Figure 2A) was constructed with 6 YABBY protein sequences. It was found that pomegranate YABBY protein was divided into five subfamilies, and PgFILa and PgFILb were divided into the same subfamily.

Figure 1 New ICT based fertility management model in private dairy farm India as well as abroad

Figure 1 New ICT based fertility management model in private dairy farm India as well as abroad

1.3 Analysis of conserved motifs of YABBY gene family in Punica granatum L.

To know the conserved motifs of YABBY gene family in Punica granatum L., MEME was used for motifs analysis, after that, TBtools was used for the results visualization of base sequence analysis. A total of 10 motifs were obtained (Table 2), and analysis results showed (Figure 2B) the number and composition of motifs from different PgYABBYs were different. PgCRC contains 3 motifs, PgINO contains 2 motifs. The motif composition of PgFILa and PgFILb genes are same, with the number of 7, and the motifs are arranged in the same order. All six PgYABBYs contain motif2, so it is speculated that motif2 is the core motif of YABBY gene family, which is particularly important for the function of YABBY gene. PgYAB5 contains 4 motifs, PgYAB2 contains 5 motifs. PgYAB2 has the same 4 motifs as PgYAB5 (motif2, motif8, motif1 and motif3), but also has motif9, which is the common motif of PgCRC and PgYAB2. In addition to core motif2, PgCRC also contains a family-specific motif10 and motif9, suggesting that motif10 is particularly important for PgCRC to perform its function. Except PgCRC, other PgYABBYs contain motif1.

Figure 1 New ICT based fertility management model in private dairy farm India as well as abroad

1.4 Intron/exon structure analysis of YABBY gene family in Punica granatum L.

To study the structure of the genes, TBtools software was used to draw the gene structure (Figure 2C). The results showed that the PgYABBY gene structure was different, and the number of introns varied greatly. PgCRC structure is the simplest, which contains three introns and four exons. PgYAB5, PgFILa and PgFILb genes contain six introns and seven exons.

1.5 Sequence alignment of YABBY gene family in Punica granatum L.

The encoded protein of YABBY gene contains N-terminal C2C2 type zinc finger domain and a C-terminal YABBY domain. To study whether the pomegranate YABBY family contains conserved domains, Clustal and Gendoc were used for sequence analysis of YABBY family genes from Arabidopsis and Punica granatum. The results showed (Figure 3) that the members of pomegranate YABBY family all contained two conserved domains: C2C2 type zinc finger domain and YABBY domain (helix-loop-helix).

Figure 1 New ICT based fertility management model in private dairy farm India as well as abroad

1.6 Expression analysis of YABBY gene family in Punica granatum L.

To study the function of YABBY gene family, expression analysis of YABBY gene family was performed based on the transcriptome data in NCBI. Results showed (Figure 4A) that the expression levels of YABBY gene family members in different tissues and organs were different. Most PgYABBY genes are highly expressed in leaves and flowers, while the expression levels are low or not expressed in different tissues of roots and fruits at different developmental stages. For example, other PgYABBY genes were not expressed in roots except for the low expression of PgYAB2. PgCRC was not expressed in leaves. Other PgYABBY genes were highly expressed in leaves, and PgFILb was the highest, followed by PgYAB2. All PgYABBY genes were expressed in flowers, but the expression abundance was different, and PgFILb was the highest, followed by PgCRC. PgCRC was expressed only in flowers. PgINO was not expressed at 50 d of root, peel development and 140 d of peel development, but was low expressed at 95 d of leaf, flower and peel development. At different stages of inner seed coat development, the expression of PgINO increased first and then decreased. With the development of inner seed coat, the expression of PgINO gene gradually decreased. PgFILa was highly expressed in leaves, and it was not expressed at 95 d of root and peel development, at 140 d of peel development and at different stages of outer seed coat development. With the development of inner seed coat, the expression level gradually decreased. PgYAB2 was expressed in other tissues except for the outer seed coat, and the expression level in leaves was the highest, followed by that in flowers. With the development of peel and inner seed coat, the expression level of PgYAB2 gradually decreased. PgYAB5 was not expressed in root, inner seed coat and outer seed coat, and was highest expressed in leaves. PgFILb was highly expressed in leaves and flowers, and gradually decreased with the development of inner seed coat.

Figure 1 New ICT based fertility management model in private dairy farm India as well as abroad

To study the role of PgYABBY gene family in the development of pomegranate seed firmness, the expression analysis of YABBY gene family was carried out with the inner seed coat of three different cultivars Dabenzi, Baiyushizi and Tunisi at 50 d after flowering as materials (Figure 4B). It was found that the expression trend of PgYABBY gene family in three varieties was quite different. PgCRC was not expressed in all three varieties. PgYAB5 gene was expressed in all three varieties. The expression trends of PgFILa, PgFILb, PgINO and PgYAB2 genes in three pomegranate cultivars were consistent, that is, the highest expression in hard-seed pomegranate, the medium expression in semi-soft-seed pomegranate and the lowest expression in soft-seed pomegranate. PgFILa, PgFILb, PgINO and PgYAB2 genes were positively correlated with the pomegranate seed firmness.

2 Discussion

YABBY family is a plant specific transcription factor, which plays important roles in leaf and fruit development, floral organogenesis, and secondary metabolism as well. The number of YABBY genes in different species varies greatly due to genome size, chromosome number and chromosome ploidy (Yamaguchi et al., 2004). A total of 6, 9, 8, 17, 7, and 13 YABBY genes were identified in Arabidopsis thaliana (Sawa et al., 1999; Siegfried et al., 1999), Solanum lycopersicum (Han et al., 2015), Oryza sativa (Toriba et al., 2007), Glycine max (Zhao et al., 2017), Vitis vinifera (Zhang et al., 2019), and Zea mays (Cao et al., 2005), respectively. In this study, 6 YABBY genes were identified in Punica granatum, which may be due to the lack of gene expansion of the YABBY gene family in evolution. And a total of 7 YABBY genes were identified in Vitis vinifera, which may be due to the same reason (Zhang et al., 2019).

To study the evolutionary relationship of YABBY gene in pomegranate, a phylogenetic tree was constructed using YABBY gene from 8 species, including dicotyledons and monocotyledons. The results showed that the YABBY gene of all plants could be divided into 5 subfamilies. Consistent with the expectation, the YABBY gene of pomegranate has close genetic relationship with dicotyledons (Vitis vinifera, Solanum lycopersicum, Arabidopsis thaliana, Glycine max), but far genetic relationship with monocotyledons. In addition, YAB5 subfamily is not existed in monocotyledons, this subfamily is unique to dicotyledons. It is speculated that YAB5 subfamily may be produced by the differentiation of YAB2 subfamily during the evolution of species (Yang et al., 2018; Zhang et al., 2019).

Gene structure and conserved domain analysis were carried out with the phylogenetic tree to study the structural characteristics of the gene. The results showed that the genes of the same subfamily with the same gene structure and conserved domain. For example, PgFILa and PgFILb have the same motif and intron/exon structure, they are closely related in evolution, indicating that they may have the same function. In addition, genes far from PgFILa and PgFILb in phylogenetic evolution may have different functions from them. Among the five subfamilies, PgYAB5 and PgYAB2 contained 4 same motifs, indicating that the two genes may be generated by the latest gene duplication in species evolution, and their functions may be similar.

Sequence alignment analysis showed that YABBY proteins in Arabidopsis and pomegranate had high homology in zinc finger structure and YABBY domain, indicating that the YABBY domain is quite conserved even though the YABBY gene produces different subfamilies during evolution. The YABBY conserved domain is particularly important for the unique functions of YABBY family genes.

The completion of pomegranate genome provides the possibility for studying the relationship between genes and traits. Studies in Arabidopsis thaliana have shown that FIL/YAB3, YAB2 and YAB5 genes are expressed in cotyledons, leaves and floral organs, so these genes are called vegetative growth genes. CRC and INO are expressed in reproductive organs such as outer coat cells of carpels and ovules, so these genes are called reproductive YABBY genes (Sawa et al., 1999; Siegfried et al., 1999). PgFILagFILa, PgFILb, PgYAB2 and PgYAB5 genes were expressed highest in leaves, followed by flowers, and were not expressed or low expressed at different developmental stages of peel, outer seed coat and inner seed. The expression levels of PgYAB2 and PgYAB5 were the highest in leaves, and they were not or almost not expressed at different stages of outer seed coat development. The expression levels gradually decreased during inner seed coat development. It indicated that PgYAB2 and PgYAB5 might have the same function, which was consistent with the motif composition results of the two. PgCRC was only expressed in flowers and not expressed in other tissues and organs, indicating that this gene was a flower-specific gene. The expression of PgINO was higher at different developmental stages of inner and outer seed coat, but the lowest in leaves. Studies of Arabidopsis thaliana and plants of Chenopodium showed that the expression of CRC and INO are specific in floral organ (Sawa et al., 1999; Siegfried et al., 1999; Soundararajan et al., 2019). VvYABBY4, was preferentially expressed during the period of ovule abortion in seedless cultivars. Transgenic expression of VvYABBY4 in tomato conferred reduced plant stature, dark green leaves, elongated pistil, and reduced size of fruit and seeds (Zhang et al., 2019). PgYAB2 and VvYABBY4 belong to YAB2 subfamily, and the same subfamily genes may have the same function. The expression of PgYAB2 gene was the highest in leaves, followed by flowers. With the development of peel and inner seed coat, the expression level decreased gradually, indicating that the gene may negatively regulate the development of pomegranate peel and seed. Studies on YABBY gene family in tomato showed that tomato YABBY gene family had dual functions in the formation of fruit shape and fruit size, in which YAB1, INO, YAB3 and YAB5 negatively regulated fruit shape and size (Han et al., 2015). The expression of PgINO decreased gradually during the development of pomegranate outer seed coat, indicating that PgINO may negatively regulate the development of pomegranate outer seed coat. Seed firmness is an important factor affecting the quality of pomegranate fruit, which is closely related to lignin metabolism (Luo et al., 2018). Lignin is an important secondary metabolite during plant development, which has many biological functions such as enhancing mechanical strength, cell wall firmness and ensuring nutrient transport (Qin et al., 2017). PgFILa, PgFILb, PgINO and PgYAB2 were differentially expressed in 3 pomegranate cultivars, and the gene expression was positively correlated with the firmness of pomegranate seeds, and the expression of PgFILb was significantly different in 3 pomegranate cultivars. Arabidopsis thaliana FIL negatively regulates anthocyanin biosynthesis, suggesting that PgFILb gene may regulate the firmness of pomegranate seeds by regulating secondary metabolites such as lignin or hemicellulose.

3 Materials and Methods

3.1 Genome and transcriptome data acquisition

Downloaded pomegranate genome database and transcriptome database from NCBI database (Qin et al., 2017). Perl script was used to extract the protein and nucleotide sequences of YABBY gene. Downloaded YABBY protein sequence from PlantTFDB database such as dicotyledoneae Arabidopsis thaliana (Sawa et al., 1999; Siegfried et al., 1999), Solanum lycopersicum (Han et al., 2015), Glycine max (Zhao et al., 2017), Vitis vinifera (Zhang et al., 2019), and monocotyledoneae Oryza sativa (Toriba et al., 2007), Zea mays (Cao et al., 2015), Ananas comosus (Li et al., 2019), and named according to the relevant references.

3.2 Identification and physicochemical properties analysis of YABBY gene family members in Punica granatum L.

Pfam database, SMART and Batch Web CD-Search Tool were used for prediction of the PgYABBY conserved domain. Based on the results, the pgYABBY gene was named according to the genetic relationship between YABBY gene family of pomegranate and Arabidopsis. ExPASy was used to analyze the physicochemical properties such as isoelectric point and protein molecular weight of YABBY family members.

3.3 Construction of phylogenetic tree

Clustal was used for multiple sequence alignment of candidate proteins with the YABBY protein sequences of dicotyledonous plants (Arabidopsis thaliana, Solanum lycopersicum, Glycine max and Vitis vinifera) and monocotyledonous plants (Oryza sativa, Zea mays and Ananas comosus). MEGAX software was used to construct the phylogenetic tree by Neighbor-joining (Bootstrap=1000).

3.4 Analysis of protein structure, conserved motif, gene structure and multiple sequence alignment of pomegranate YABBY

MEME (http://meme.sdsc.edu/meme/ meme-in.tro.html) was used for motifs analysis of pomegranate YABBY. TBtools (http://dx.doi.org/10.1101/289660) was used for the results visualization of base sequence analysis, and gene structure analysis of pomegranate YABBY gene family based on the obtained pomegranate YABBY gene protein sequence and pomegranate genome GFF3 data. Multiple sequence alignment of pomegranate and Arabidopsis YABBY protein was performed by Clustal software, and the results were displayed by Gendoc software.

3.5 RNA-Seq analysis of pomegranate YABBY gene family

Downloaded transcriptome data of peel, outer seed coat and inner seed coat in different tissues (Roots, leaves and flowers) and developmental stages (50 d, 95 d and 140 d after pollination) from “Dabenzi” and three pomegranate varieties (pomegranate with firmness seed "Dabenzi", semi-soft seed "Baiyushizi" and soft seed pomegranate "Tunisi") 50 d after pollination from NCBI (Qin et al., 2017). TBtools was used to draw gene expression heatmap after that, visualization was carried out.

Authors’ contributions

LSL completed most of the data analysis work. LXJ was the experimental designers and executor of this study and was the project designer and the person in charge of the experimental design, data analysis, thesis writing and revision. Both authors read and approved the final manuscript.

Acknowledgments

This study was supported by the Basic Research Program for Youth of Yunnan Provincial Science and Technology Department (2016FD091), the Master and Doctor Program of Honghe University (XJ16B06) and the Biology Key Construction Discipline Project of Honghe University.

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