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Article

Genome-Wide Identification and Characterization of YABBY Gene Family in Juglans regia and Juglans mandshurica

by
Hengzhao Liu
1,†,
Hang Ye
1,†,
Jiangtao Wang
1,
Shenqun Chen
2,†,
Mengdi Li
1,
Gang Wang
2,
Na Hou
2,* and
Peng Zhao
1,*
1
Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life Sciences, Northwest University, Xi’an 710069, China
2
Guizhou Academy of Forestry, Guiyang 550005, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2022, 12(8), 1914; https://doi.org/10.3390/agronomy12081914
Submission received: 15 July 2022 / Revised: 6 August 2022 / Accepted: 11 August 2022 / Published: 14 August 2022
(This article belongs to the Topic Plant Functional Genomics and Crop Genetic Improvement)
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Abstract

:
The YABBY gene family is a plant transcription factor that exists in all seed plants. YABBY family members have been studied extensively in various plants and were to play significant roles in plant growth and development. Juglans, especially walnuts, are important economic tree species that are widely distributed worldwide. However, the identification and related research of YABBY in Juglans have not been reported to date. In this study, we identified 19 YABBY genes from two Juglans species, namely, J. regia and J. mandshurica. Ten JrYABBY genes and nine JmYABBY genes were divided into five subfamilies (YAB1/3, YAB2, INO, CRC, and YAB5). Sequence analysis revealed that all encoded YABBY protein sequences had a highly conserved YABBY and C2C2 zinc-finger domains. An analysis of the assumed cis-acting elements revealed that JrYABBY and JmYABBY genes were deeply involved in phytohormone and light responses. Further, gene expression pattern analysis suggested that most walnut YABBY genes were likely involved in peel and flower development and responses to biotic stress. This study not only suppled novel insights into the evolutionary basis of YABBY gene families in Juglans, but also provided clues for the further functional verification and investigation of YABBY genes in other tree species.

1. Introduction

The YABBY transcription factor has a prominent role in regulating plant growth and developmental activities, such as the plant developmental, flowering, abiotic, and biotic responses [1,2,3,4,5]. YABBY proteins are comprised of two highly conserved DNA-binding domains, namely the zinc finger-like domain (C2C2) and helix–loop–helix domain (YABBY), respectively [2]. In important crops, YABBY genes have been examined in their related genomes, including 21 in Wheat [3], 17 in soybean [4], 8 in rice [5] and 30 in Cucumber [6]. In woody plants, YABBY genes have been examined in their related genomes, namely, 55 genes in seven species of Magnoliids [7].
The development of plants depends on the function of the shoot apical meristem (SAM), which is established during embryogenesis [8,9]. Following the determination of the fates of apiece cells in differentiated organs, the development of lateral organ primordia is still regulated by the meristem through undetermined signals [10]. Recent impalement studies in Arabidopsis thaliana indicated that the activities of YABBY genes were involved in this signal transduction [11].
As specific types of transcription factor family members related to plant morphogenesis, YABBY genes play critical roles in the regulation of various developmental processes in eudicots such as the establishment of ad axial–abaxial polarity, lamina expansion, and floral development [9,12,13]. This is due to their significant functionalities, genomic characteristics, and expression patterns, which have been extensively studied in various plants [14,15]. Although the YABBY gene family is deeply involved in plant life processes, its expressions are not conserved and its functions have not been well investigated to date [16]. According to previous studies, the YABBY gene family is divided into five distinct groups in angiosperms, which present different expression patterns in leaves and flowers [4,17].
In Arabidopsis, YABBY genes play significant roles in the establishment of dorsal ventral polarity, leaf expansion, and flower development [18,19]. The Arabidopsis YABBY gene family contains six members, namely, FIL (FILAMEN-TOUS FLOWER), CRC (CRABSCLAW), INO (INNER NO OUTER; YABBY4), YAB2 (YABBY2), YAB3 (YABBY3), and YAB5 (YABBY5) [20,21,22]. Phylogenetic analysis has shown that FIL and YAB3 are closely related, which may be due to gene replication. The expression of these two genes was observed in the abaxial cells of the initial primordium of the developing organ, which determined the fate of abaxial cells [23]. FIL genes participated in the development of flowers and leaves [24], whereas CRC genes were transcribed in tissues such as the abaxial carpel, placentas, and nectarium. Furthermore, INO and its role in ovule development were mainly characterized in the model plant species Arabidopsis. Arabidopsis INO was restrictively expressed in the furthermost cell layer of the outer integument in ovules to promote its growth [7,25,26]. YAB3, YAB2, and YAB5 are referred to as the “vegetative YABBY genes” of Arabidopsis, with YAB2 and YAB3 expressed in the abaxial domains of all leaf-derived organs, including cotyledons, leaves, and floral organs [9,27,28].
YABBY genes have also been identified in numerous other species. In Nelumbo nucifera, NnYABBY genes were highly expressed during plant growth, but not in mature tissues, which indicated that YABBY was a considerable regulatory factor in Nelumbo growth [29]. A total of 17 YABBY genes were identified in the soybean genome [4], and it was found that the survival rate of wild-type seeds was higher than that of GM seeds (YABBY10). The results revealed that this gene might have negative regulatory effects on environmental stress resistance [29]. Moreover, there were eight YABBY members found in Oryza sativa, and expression analysis showed that they might play significant roles in floral development and hormone responses [5,30].
The genus Juglans belongs to the Juglandaceae family, which is an important economic tree species worldwide with important material uses, in addition to having food, medicinal and artistic values [2]. However, YABBY genes, as important regulatory factors that affect plant growth and development, have rarely been studied in Juglans. Thus, the identification and characterization of this gene family in Juglans species is warranted, in addition to extensive directly corresponding studies. In recent years, the publication of the reference genomes of J. regia [31] and J. mandshurica [32] provided valuable opportunities to investigate important functional genes involved in plant development and environmental adaption. The WAK, WRKY, and NAC gene families have been identified in walnut; thus, these studies have provided an effective molecular basis for the genetic improvement and breeding of walnut. In this study, for the first time, we identified and analyzed the YABBY gene family in J. regia and its wild related species J. mandshurica. Specifically, the conserved domain characteristics, gene structure analysis, chromosome localization, gene duplication identification, phylogenetic relationships, and transcriptome expression profiles of YABBY members were elucidated for these two Juglans species [33]. Our study initially revealed the genetic and evolutionary origins of the YABBY gene family in the Juglans species, and laid the foundation for the further in-depth verification of YABBY gene functionality in other agronomic tree species.

2. Materials and Methods

2.1. Identification of YABBY Transcription Factors in J. regia and J. mandshurica

To identify the potential YABBY gene candidates for the two walnut species, AtYABBY reference protein sequences (https://www.arabidopsis.org/ (accessed on 10 February 2022)) were employed as query sequences, and the genomic sequences of J. regia (https://www.ncbi.nlm.nih.gov/genome/ (accessed on 10 February 2022)) and J. mandshurica were used as databases for blastp with an E-value < 1 × 10−5. Subsequently, the protein domains of all candidates were analyzed to determine the final YABBY members. Specifically, the candidate members that did not contain “C2C2” domains and “YABBY” or “YABBY_super” family domains were removed by searching the Conserved Domain Database (CDD) in NCBI [33]. Furthermore, hmmersearch analysis was also performed via the Pfam online tools (http://pfam.xfam.org/ (accessed on 10 February 2022))) to remove the candidate sequences without the YABBY domain (pf04690).

2.2. Characteristics and Phylogenetic Relationships of Identified YABBYs

The physicochemical properties of all identified YABBY properties were predicted from the EXPASY online tools (http://www.expasy.org/tools/protparam.html (accessed on 10 February 2022))). Subsequently, the subcellular locations of all identified members were predicted using the Wolf PSORT website (https://wolfpsort.hgc.jp/ (accessed on 10 February 2022))).
The chromosomal locations of YABBY genes were found using TBtools software [34]. The collinearity analysis of gene replication patterns was conducted using MCScanX software [35]. KaKs_Calculator 2.0 software [36] was employed to calculate the Ka/Ks ratio.
The maximum likelihood (ML) tree was reconstructed for the YABBY members in J. regia and J. mandshurica, where the YABBY genes of Arabidopsis Thaliana and Oryza sativa were adopted as the outgroups. IQTREE software was used to construct the ML tree, whereas JTT+G4 was selected as the best-fit substitution model according to the BIC scores with 1000 ultra-fast bootstraps.

2.3. Cis-Acting Element Prediction and Gene Expression Analysis

The prediction of cis-acting elements was performed using 2000 bp sequences upstream of the YABBY genes in PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/ (accessed on 10 February 2022)). The walnut transcriptome sequencing data under pathogen stress were downloaded from NCBI (accession number GSE147083: https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE147083 (accessed on 10 February 2022)) [37]. The original data were filtered using FASTP [38], followed by sequence alignments using HISAT2 [39]. Next, gene expressions were calculated using FeatureCounts software. Finally, TBtools [34] was employed to visualize the heatmaps of these candidate genes.

3. Results

3.1. Genome-Wide Identification and Phylogenetic Analysis of YABBY Gene Family in J. regia and J. mandshurica

YABBY gene members were identified in J. regia and its wild relative species J. mandshurica. By screening candidate protein domains, 10 genes in J. regia and nine genes in J. mandshurica, encoding for YABBY proteins, were identified. Akin to YABBY proteins found in other plants, all JrYABBY and JmYABBY contained two conserved domains corresponding to zinc C2C2 FNGER and YABBY. To facilitate analysis, we renamed all the members according to the order in which they were located in the chromosomes. The gene names and protein sequences of all identified YABBY members are shown in Table S1.
A maximum likelihood phylogenetic tree was constructed using the protein sequences of Arabidopsis thaliana, Oryza sativa, J. regia, and J. mandshurica (Figure 1). Members of the YABBY family were divided into five major clades. The largest group was YABBY1/YABBY3, which contained four J. regia YABBYs (JrYABBY2, JrYABBY3, JrYABBY5, and JrYABBY9), three J. mandshurica YABBYs (JmYABBY5, JmYABBY6, and JmYABBY7), and three Oryza sativa YABBYs (OsYABBY3, OsYABBY4, and OsYABBY5), which were clustered together with two YABBY proteins in Arabidopsis (AtYABBY1 and AtYABBY3). The group I (INO) contained one YABBY member each in J. regia, J. mandshurica, Oryza sativa, and Arabidopsis thaliana. Group III (YABBY5) consisted of two YABBYs from J. regia (JrYABBY1 and JrYABBY6), two YABBYs (JmYABBY1 and JmYABBY2) from J. mandshurica, and one YABBY (AtYABBY5) from Arabidopsis. The IV (CRC) group contained YABBY members (JrYABBY7 and JmYABBY4) of the four species. Group V (YABBY2) was the second largest group with two J. regia YABBYs (JrYABBY4 and JrYABBY10), two J. mandshurica YABBYs (JmYABBY8 and JmYABBY9), three O. sativa YABBYs (OsYABBY1, OsYABBY2, and OsYABBY6), and one A. thaliana YABBY (AtYABBY2).

3.2. Physicochemical Properties and Subcellular Localization Analysis of YABBY Proteins in J. regia and J. mandshurica

The lengths of the YABBY proteins in J. regia ranged from 168 amino acids (aa) (JrYABBY7) to 215 aa (JrYABBY5), with an average length of 194 aa (Table 1). In contrast, the YABBY proteins in J. mandshurica were shorter, ranging from 122 aa (JmYABBY4) to 215 aa (JmYABBY6), with an average length of 180 aa. The molecular weights (MWs) of the JrYABBY proteins ranged from 19.75 kDa (JrYABBY4) to 23.91 kDa (JrYABBY5), with an average of 21.50 kDa. The MWs of JmYABBY proteins were lower than those of JrYABBY, ranging from 13.40 kDa (JmYABBY4) to 23.88 kDa (JmYABBY6), with an average of 19.90 kDa. Furthermore, four YABBY proteins were acidic (isoelectric point < 7) in J. regia (JrYABBY8) and J. mandshurica (JmYABBY3, JmYABBY4, and JmYABBY6), respectively. There were a total of four YABBY proteins with instability index values of >50 in J. regia and J. mandshurica. Almost all the identified YABBY proteins had negative grand average of hydropathicity (GRAVY) values (with only one exception (JmYABBY3)) for these two species, indicating that they were hydrophilic. As expected, all identified YABBY genes resided in the nucleus (Table 1).

3.3. Protein Domain and Gene Structure Distribution Analysis of YABBY Genes in J. regia and J. mandshurica

The reconstructed ML tree based on the two species under study (Figure 2a) presented similar topologies to those using four species (Figure 1). Gene structural analysis revealed that the YABBY proteins were relatively conservative, and all YABBY genes contained at least one conserved domain (Figure 2b). Moreover, each JrYABBY and JmYABBY gene contained the C2C2 zinc finger and YABBY domains (Figure 2d).
Among the 10 YABBY genes in J. regia, eight contained six introns and two contained five introns. Among the nine YABBY genes in J. midthoracic, five contained six introns, three contained four introns, and one contained three introns. The numbers of exons were different between J. regia and J. mandshurica (Table S2, Figure 2c), where JmYABBY8 had only four exons, whereas JmYABBY3, JmYABBY4, JmYABBY9, and JrYABBY4 had five. The other YABBY genes in J. regia and J. mandshurica contained seven exons. These results indicated that the main structural characteristics in YABBY genes included six introns and seven exons. Interestingly, it was worthy of note that several YABBY members possessed relatively long introns, particularly JrYABBY4, JrYABBY10, JmYABBY8, and JmYABBY9, which belonged to the YABBY II subgroup (Figure 1).

3.4. Chromosomal Distribution and Duplication Mode Analysis of YABBY Gene Family in J. regia and J. mandshurica

To investigate chromosomal localizations, JrYABBY and JmYABBY genes were obtained and mapped to seven different corresponding chromosomes. For J. regia, except for two JrYABBY members on chr5, chr13, and chr14 chromosomes, there was only one JrYABBY member on the other chromosomes. For J. mandshurica, there were two JmYABBY members on chr5 and chr13 chromosomes, with only one JmYABBY member on other chromosomes.
The numbers of YABBY members identified in J. regia (ten) and J. mandshurica (nine) were nearly doubled in contrast to Arabidopsis. Notably, the results of gene duplication analysis showed that there were no tandem repeats between these identified YABBY genes. Similar results were also obtained from other species such as maize, cotton, and Oryza sativa. In contrast, whole-genome duplication (WGD) and dispersed duplication (DSD) may be the driving forces behind YABBY gene duplication, with 10 YABBY genes subject to WGD followed by DSD (nine genes) (Table 2, Figure 3).

3.5. Collinearity and Selective Pressure Analysis of YABBY Members in J. regia and J. mandshurica

Collinearity analysis revealed that there were 12 and eight YABBY paralogous gene pairs in J. regia and J. mandshurica, respectively, and 18 YABBY orthologous gene pairs between the two Juglans species (Figure 4). It was clear that the number of orthologous gene pairs identified between the two species was greater than that of paralogous gene pairs within the given species (Table S3). To investigate the selective pressure of these homologous gene pairs, their Ka/Ks values were calculated. The Ka/Ks ratio of most homologous YABBY pairs was lower than one, suggesting that they underwent purifying selection and may have evolved at a relatively low rate.

3.6. Analysis of Cis-Acting Elements in J. regia and J. mandshurica

To investigate the potential functions of YABBY genes in J. regia and J. mandshurica, we analyzed the cis-acting elements in their upstream promoter regions. The results revealed that the upstream promoter regions of the YABBY genes contained the greatest number of cis-acting elements in the two species. Further, the identified cis-acting elements were associated with four types of life activities: plant development and growth, phytohormone responses, abiotic stress responses, and light responses (Figure 5). Moreover, stress response elements such as MBS under drought stress and LTR under low temperature stress were also found. It is worth noting that development-related elements were also found, including CAT-box (meristem), circadian (circadian control), and the GCN4_motif. These results suggested that YABBYs may play a role in plant development, in addition to stress and phytohormone responses in J. regia and its wild related species J. mandshurica.

3.7. Gene Expression Profile Analysis of YABBY Genes in J. regia and J. mandshurica

To determine the expression profiles of tissue-specific YABBY in J. regia and its wild related species J. mandshurica, we analyzed the transcriptome data of female flowers, male flowers, leaves, and green fruit peels of these two species (Figure 6; Table S4). For J. regia, the JrYABBY3 gene exhibited relatively low expression levels in all studied tissues. Most JrYABBY genes were highly expressed in green pericarp, except for JrYABBY1, 6, and 8. JrYABBY 1 and 6 were primarily expressed in leaves, whereas JrYABBY 7 and 8 were found to be significantly expressed in female and male flowers, respectively. For J. mandshurica, most JmYABBY genes exhibited high expression levels in the tissues under study, except for JmYABBY 4 and 6 in J. regia and JmYABBY4 and JmYABBY6 in J. mandshurica. The above results revealed that YABBY genes in J. regia and J. mandshurica were related to the growth and development of flowers, leaves, and fruits.
To further investigate the roles of JrYABBY in J. regia stress responses, we analyzed gene expression patterns in different varieties of walnuts under biotic stress. In summary, the expression levels of JrYABBY genes in anthracnose-resistant cultivars (F26) were higher than those in anthracnose-susceptible cultivars (F423), which suggested that JrYABBY may play a role in anthracnose resistance in walnut. The YABBY genes typically presented low expression levels in the early-stage cultivars (F423); however, JrYABBY2 4 and 10 were highly expressed in the early-stage anthracnose-resistant cultivars (F26). This signified the important roles of the YABBY genes in defending against early-stage biotic stress.

4. Discussion

As economic forest species, the common walnut (J. regia) and its wild relative (J. mandshurica), have significant economic, nutritional, and medicinal value [40]. However, knowledge regarding the characteristics and functions of YABBY genes across J. regia and its wild related species J. mandshurica is negligible. With the recent completion of whole-genome sequencing, comparative studies of the key gene families for these two species have become possible [33,40].The YABBY gene family is a class of unique transcription factor in seed plants that contain the C2C2 zinc finger and YABBY domains [4,12], and plays critical roles in a variety of biological processes, such as the development of abaxial-paraxial polarity in plant leaves, reproductive organ formation and development, plant hormone signal responses, plant biotic and abiotic stresses, leaf extension, and agricultural production [41,42].
In this study, the YABBY genes in J. regia and J. mandshurica were identified and analyzed, and it was found that walnut had more YABBY members than Arabidopsis. Further, genetic structural analysis indicated that the YABBY genes in walnut exhibited more diversity and variations. This may have been related to the participation of YABBY gene family members in additional evolutionary biological regulation processes. For this study, there were ten YABBY genes identified in J. regia and nine in J. mandshurica. To elucidate the evolutionary relationships between JrYABBY and JmYABBY, we constructed a phylogenetic tree that included YABBY proteins in four species (Figure 1). According to the phylogenetic relationships, JrYABBY and JmYABBY genes were divided into five different clades, which was consistent with the classification of YABBY genes in Arabidopsis and tomato [23,43]. The expression of CRC and INO subfamilies in Arabidopsis was related to the reproductive organs of plants, whereas the FIL, YAB2, YAB3, and YAB5 subfamilies were expressed in both leaves and flowers. FIL regulates Arabidopsis flower development, positively regulates genes involved in plant development, and participates in anthocyanin accumulation through two-way activation and repression [21].
We renamed the YABBY genes according to their locations on various chromosomes. All identified JrYABBY and JmYABBY genes contained C2C2 zinc finger and YABBY domains (Figure 1, Figure 2 and Figure 3). Genes of the same subfamilies (e.g., JrYABBY2 and JrYABBY5, JmYABBY5 and JmYABBY6) exhibited similar motif and exon–intron structures. This apparently recent evolution meant that these pairs of genes may have similar functions (Figure 2, Table S2). Conversely, the evolutionary differentiation of genetic structures implied variations in gene function [44]. To investigate the selective pressures of these homologous gene pairs, their Ka/Ks values were calculated. The Ka/Ks ratios of most YABBY homologous gene pairs were lower than 1, suggesting that they had undergone purifying selection and may have evolved at a relatively low rate (Table S3).
Gene replication and differentiation events are considered to be major contributors to the momentum of evolution. The number of YABBY genes in J. regia and J. mandshurica was greater than in Arabidopsis; thus, we conjectured that the differences in the number of YABBY genes between species may be due to gene duplication or loss during evolutionary processes. Fragmentation and tandem duplications contribute to the expansion of gene families [45]. Therefore, we explored the main extended YABBY gene family replication types in walnut and J. mandshurica. However, in this study, no tandem repeat gene events were discovered in the YABBY gene family. In contrast, the WGD may be the major force leading to YABBY duplication and expansion in walnut species (Table 2).
The expressions of genes are primarily the result of the interactions between cis-acting elements and trans-acting factors. By analyzing the cis-acting elements of promoters and their upstream sequences, the functions of genes can be predicted. Various cis-acting elements in gene promoters may be correlated with different gene functions [19]. This study found that YABBY genes contained significant quantities of cis-regulatory elements associated with phytohormones (e.g., gibberellin, abscisic acid, and jasmonic acid) and light responses, along with endosperm expression-related active elements; thus, JrYABBY and JmYABBY genes were likely closely related to these aspects (Figure 5).
It was speculated that JrYABBY and JmYABBY genes may be related to leaf and fruit development in J. regia and J. mandshurica. To probe the expression patterns of YABBY in J. regia and J. mandshurica, we performed an analysis based on the transcriptome data of female flowers, male flowers, leaves, and green pericarps between these two species (Figure 6, Table S4). The results indicated that JrYABBY and JmYABBY genes were significantly upregulated in lateral organs such as fruits and leaves. This further verified that JrYABBY and JmYABBY genes were similar to the Arabidopsis YABBY gene, which had specific effects on the development of lateral organs and leaves. Further detailed elucidation of how JrYABBY and JmYABBY genes induce fruit development in J. regia and J. mandshurica will require comprehensive and systematic molecular biological experiments and analysis [46]. The transcriptome profile revealed that JrYABBY2, JrYABBY3, JrYABBY5, and JrYABBY10 were significantly expressed in fruit peel, which may play similar roles as the FIL gene in Arabidopsis (Figure 6); it was speculated that they may be related to the accumulation of anthocyanin. It was clear in mature flowers that the expression of JrYABBY2, belonging to the YAB1/YAB3 subfamily, regulated the development of flowers and fruits, which was consistent with previous research [10,17].
In this study, the YABBY gene family members in J. regia and J. mandshurica were systematically identified using bioinformatics methods. Simultaneously, the physicochemical properties, conserved domains, chromosomal localization, evolutionary relationships, cis-acting elements, and expression patterns of the YABBY gene family members, which were relatively conserved in J. regia and J. mandshurica, were analyzed. Many WGD events occurred during the expansion of the YABBY gene family. Furthermore, transcriptome profiles showed distinct expression patterns in different tissues, which suggested the specific functions of these identified YABBY genes. This study provides theoretical support and references for the functional characterization of the YABBY gene family in Juglans.

5. Conclusions

For this study, we identified ten JrYABBY and nine JmYABBY genes in J. regia and J. mandshurica. Phylogenetic analysis revealed that the YABBY genes could be divided into five groups and, akin to other angiosperms/basic angiosperms, they possess unique sequence characteristics beyond the conserved amino acid domains. Phylogenetic and synchronic analyses revealed that the YABBY gene family was evolutionarily conservative. Although YABBY genes were not evenly distributed across chromosomes, they were consistent across homologous chromosomes, which suggested that they were relatively conserved across sub-genomes. Expression Profile Analysis indicated that the YABBY gene family determined significant functions in the development and growth of green pericarps, flowers, and fruits. Further exploration is required to determine whether JrYABBY and JmYABBY genes may play various roles at different stages of development of other lateral organs such as flowers and leaves.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy12081914/s1, Table S1. Protein sequences of all YABBY genes of two Juglans species; Table S2. Number of exons and introns of YABBY genes in Juglans regia and J. mandshurica; Table S3. Estimated Ka/Ks ratios of duplicated YABBY gene pairs in Juglans regia and J. mandshurica; Table S4. FPKM values of all YABBY genes of two Juglans species.

Author Contributions

H.L. and H.Y. analyzed and interpreted the raw data. H.L. H.Y. S.C. and J.W. wrote the first draft. M.L., N.H., G.W. and J.W. collected the samples. N.H. and P.Z. finished the work of language editing. P.Z. conceived the main concepts for this study. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the National Natural Science Foundation of China (32070372 and 31860215), by the Bridging Project for the Enterprises and the Local walnut R&D Groups in Guizhou Province (grant number [2015] 4010 and [2019] 5643), by innovation and application of Guizhou walnut germplasm (Qianlin ke [2022] 17) and Study on the Vitality and Stigma of Guizhou Wuren Walnut Pollen (Qianlin J [2022] No. 05).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw data were downloaded from the SRA database under accession number (GSE147083).

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Maximum likelihood phylogenetic (ML) tree of YABBY proteins of Arabidopsis thaliana, Oryza sativa, Juglans regia, and Juglans mandshurica.
Figure 1. Maximum likelihood phylogenetic (ML) tree of YABBY proteins of Arabidopsis thaliana, Oryza sativa, Juglans regia, and Juglans mandshurica.
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Figure 2. Gene structures and protein domains of YABBY gene members. (a) Maximum likelihood phylogenetic tree of YABBY in two Juglans species. (b) Protein domains of YABBYS in two Juglans species. Various domains are represented by different colored boxes. (c) Gene structures of YABBYS in two Juglans species. Green boxes indicate exons, and gray lines indicate introns. (d) Multiple sequence alignment of the YABBY family genes from two Juglans species.
Figure 2. Gene structures and protein domains of YABBY gene members. (a) Maximum likelihood phylogenetic tree of YABBY in two Juglans species. (b) Protein domains of YABBYS in two Juglans species. Various domains are represented by different colored boxes. (c) Gene structures of YABBYS in two Juglans species. Green boxes indicate exons, and gray lines indicate introns. (d) Multiple sequence alignment of the YABBY family genes from two Juglans species.
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Figure 3. Chromosomal distribution of YABBY genes. (a) Chromosomal distribution of YABBY genes in J. regia. (b) Chromosomal distribution of YABBY genes in J. mandshurica. Chromosome numbers are shown below each chromosome. Black, JrYABBY genes, JmYABBY genes. Green, J. regia chromosomes; Yellow, J. mandshurica chromosomes.
Figure 3. Chromosomal distribution of YABBY genes. (a) Chromosomal distribution of YABBY genes in J. regia. (b) Chromosomal distribution of YABBY genes in J. mandshurica. Chromosome numbers are shown below each chromosome. Black, JrYABBY genes, JmYABBY genes. Green, J. regia chromosomes; Yellow, J. mandshurica chromosomes.
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Figure 4. Genome-wide synteny analysis of YABBY genes for J. regia and J. mandshurica. Orthologous and paralogous YABBY genes were mapped onto the chromosomes and linked by each other. Red lines indicate orthologous gene pairs, blue lines indicate paralogous gene pairs.
Figure 4. Genome-wide synteny analysis of YABBY genes for J. regia and J. mandshurica. Orthologous and paralogous YABBY genes were mapped onto the chromosomes and linked by each other. Red lines indicate orthologous gene pairs, blue lines indicate paralogous gene pairs.
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Figure 5. Cis-acting elements in promoter regions of YABBY genes in two Juglans species. Based on functional annotations, the cis-acting elements were categorized into four major classes: plant development and growth, phytohormone responses, abiotic stress responses, and light responsive cis-acting elements. Numbers in the colored boxes represent the number of cis-acting elements.
Figure 5. Cis-acting elements in promoter regions of YABBY genes in two Juglans species. Based on functional annotations, the cis-acting elements were categorized into four major classes: plant development and growth, phytohormone responses, abiotic stress responses, and light responsive cis-acting elements. Numbers in the colored boxes represent the number of cis-acting elements.
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Figure 6. Expression patterns of YABBY genes in J. regia and J. mandshurica. (a) Expression patterns of identified YABBYs in female flowers, male flowers, leaves, and green pericarps of J. regia.; RF, female flowers of J. regia; RM, male flowers of J. regia; RL, leaves of J. regia; RG, green pericarp of J. regia. (b) Expression patterns of identified YABBYs in female flowers, male flowers, leaves, and green pericarps of J. mandshurica. MF, female flowers of J. mandshurica; MM, male flowers of J. mandshurica; ML, leaves of J. mandshurica; MG, green pericarps of J. mandshurica. (c) Expression patterns of identified YABBY genes in J. regia under biotic stress. F26 indicates anthracnose-resistant varieties, F423 indicates anthracnose-susceptible varieties. Numbers after ‘-’ represent time after infection (unit: hour). Colored scale reflects gene expression levels.
Figure 6. Expression patterns of YABBY genes in J. regia and J. mandshurica. (a) Expression patterns of identified YABBYs in female flowers, male flowers, leaves, and green pericarps of J. regia.; RF, female flowers of J. regia; RM, male flowers of J. regia; RL, leaves of J. regia; RG, green pericarp of J. regia. (b) Expression patterns of identified YABBYs in female flowers, male flowers, leaves, and green pericarps of J. mandshurica. MF, female flowers of J. mandshurica; MM, male flowers of J. mandshurica; ML, leaves of J. mandshurica; MG, green pericarps of J. mandshurica. (c) Expression patterns of identified YABBY genes in J. regia under biotic stress. F26 indicates anthracnose-resistant varieties, F423 indicates anthracnose-susceptible varieties. Numbers after ‘-’ represent time after infection (unit: hour). Colored scale reflects gene expression levels.
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Table
Table 1. Predicted protein data of YABBY in J. regia and J. mandshurica.
Table 1. Predicted protein data of YABBY in J. regia and J. mandshurica.
Gene NameNo. of Amino AcidsMol. Wt (Da)Isoelectric Point (pI)Instability Index (II)Aliphatic IndexGrand Average of Hydropathicity (GRAVY)Subcellular Localization a
JrYABBY119221,332.248.83 37.17 72.71 −0.354 nucl
JrYABBY2 211 23,466.72 7.71 49.57 77.58 −0.315nucl
JrYABBY3 213 23,467.82 8.58 50.22 77.37 −0.299 nucl
JrYABBY4 177 19,751.41 8.48 48.15 68.93 −0.494 nucl
JrYABBY5 215 23,918.36 7.71 47.33 79.81 −0.304 nucl
JrYABBY6 187 20,819.69 8.76 37.96 76.26 −0.306 nucl
JrYABBY7 168 18,543.27 9.26 41.79 72.56 −0.39 nucl
JrYABBY8 186 20,892.41 5.68 71.33 71.83 −0.492 nucl
JrYABBY9 207 22,630.76 8.25 48.02 75.89 −0.293 nucl
JrYABBY10 181 20,172.9 7.64 52.41 65.25 −0.532 nucl
JmYABBY1 202 22,227.28 8.6535.7876.83−0.240nucl
JmYABBY218220,381.328.3440.9279.34−0.196nucl
JmYABBY318620,887.85 5.86 59.77 93.28 0.022nucl
JmYABBY4 122 13,404.34 6.8042.39 82.30 −0.191nucl
JmYABBY5 211 23,466.72 7.71 49.57 77.58−0.315nucl
JmYABBY621523,887.33 8.25 45.8282.98−0.262nucl
JmYABBY7 207 22,700.9 8.25 48.81 78.21−0.259nucl
JmYABBY813815,184.456.9844.6774.13−0.204nucl
JmYABBY915517,011.658.9945.4680.52−0.168nucl
a Note:plas: chlo: chloroplast; nucl: nucleus.
Table
Table 2. Four duplicated types of YABBY genes in J. regia and J. mandshurica.
Table 2. Four duplicated types of YABBY genes in J. regia and J. mandshurica.
Gene NameWhole Genome Duplication
(WGD)		Tandem Duplication
(TD)		Dispersed Duplication
(DSD)		Proximal Duplication
(PD)
JrYABBY1√
JrYABBY2√
JrYABBY3√
JrYABBY4 √
JrYABBY5√
JrYABBY6√
JrYABBY7 √
JrYABBY8 √
JrYABBY9 √
JrYABBY10√
JmYABBY1√
JmYABBY2√
JmYABBY3 √
JmYABBY4 √
JmYABBY5√
JmYABBY6√
JmYABBY7 √
JmYABBY8 √
JmYABBY9 √
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Liu, H.; Ye, H.; Wang, J.; Chen, S.; Li, M.; Wang, G.; Hou, N.; Zhao, P. Genome-Wide Identification and Characterization of YABBY Gene Family in Juglans regia and Juglans mandshurica. Agronomy 2022, 12, 1914. https://doi.org/10.3390/agronomy12081914

AMA Style

Liu H, Ye H, Wang J, Chen S, Li M, Wang G, Hou N, Zhao P. Genome-Wide Identification and Characterization of YABBY Gene Family in Juglans regia and Juglans mandshurica. Agronomy. 2022; 12(8):1914. https://doi.org/10.3390/agronomy12081914

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Liu, Hengzhao, Hang Ye, Jiangtao Wang, Shenqun Chen, Mengdi Li, Gang Wang, Na Hou, and Peng Zhao. 2022. "Genome-Wide Identification and Characterization of YABBY Gene Family in Juglans regia and Juglans mandshurica" Agronomy 12, no. 8: 1914. https://doi.org/10.3390/agronomy12081914

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